Multiple forms of tubulin: Different gene products and covalent modifications

International Review of Cytology

Volumn 178, Issue , 1997, Pages 207-275

  Ludueña, Richard F ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Microtubules; Posttranslational modifications; Tubulin isotypes; Tubulins

Indexed keywords

GENE PRODUCT; ISOPROTEIN; TUBULIN;

ACETYLATION; CELL ORGANELLE; HUMAN; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; STRUCTURE ACTIVITY RELATION;

EID: 0030709242     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0074-7696(08)62138-5     Document Type: Article

References (401)

1. Ahmad, S., Singh, B., and Gupta, R. S. (1991). Nucleotide sequences of three different isoforms of β-tubulin cDNA from Chinese hamster ovary cells. Biochim. Biophys. Acta 1090, 252-254.
2. Aletta, J. M. (1996). Phosphorylation of type III β-tubulin in PC12 cell neuntes during NGF-induced process outgrowth. J. Neurobiol. 31, 461-475.
3. Alexander, J. E., Hunt, D. F., Lee, M. K., Shabanowitz, J., Michel, H., Berlin, S. C., Macdonald, T. L., Sundberg, R. J., Rebhun, L. I., and Frankfurter, A. (1991). Characterization of posttranslational modifications in neuron-specific class III β-tubulin by mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 88, 4685-4689.
4. Alexandraki, D., and Ruderman, J. V. (1983). Evolution of αq- and β-tubulin genes as inferred by the nucleotide sequences of sea urchin cDNA clones. J. Mol. Evol. 19, 397-410.
5. Alonso, A. del C., Arce, C. A., and Barra, H. S. (1993). Tyrosinatable and non-tyrosinatable tubulin subpopulations in rat muscle in comparison with those in brain. Biochim. Biophys. Acta 1163, 26-30.
6. Aniello, F., Couchie, D., Gripois, D., and Nunez, J. (1991). Regulation of five tubulin isotypes by thyroid hormone during brain development. J. Neurochem. 57, 1781-1786.
7. Arai, T., and Matsumoto, G. (1988). Subcellular localization of functionally differentiated microtubules in squid neurons: Regional distribution of microtubule-associated proteins and β-tubulin isotypes. J. Neurochem. 51, 1825-1838.
8. Arce, C. A., and Barra, H. S. (1983). Association of tubulinyl-tyrosine carboxypeptidase with microtubules. FEBS Lett. 157, 75-78.
9. Arce, C. A., Rodriguez, J. A., Barra, H. S., and Caputto, R. (1975). Incorporation of L-tyrosine, L-phenylalanine and L-3,4-dihydroxyphenylalanine as single units into rat brain tubulin. Eur. J. Biochem. 59, 145-149.
10. Argaraña, C. E., Barra, H. S., and Caputto, R. (1980). Tubulinyl-tyrosine carboxypeptidase from chicken brain: properties and partial purification. J. Neurochem. 34, 114-118.
11. Arregui, C. O., and Barra, H. S. (1995). Segmented pattern of tyrosinated microtubules assembly in neurites of chick retinal neurons. BioCell 19, 49-55.
12. Asai, D. J., and Remolona, N. M. (1989). Tubulin isotype usage in vivo: A unique spatial distribution of the minor neuronal-specific β-tubulin isotype in pheochromocytoma cells. Dev. Biol. 132, 398-409.
13. Atashi, J. R., Klinz, S. G., Ingraham, C. A., Matten, W. T., Schachner, M., and Maness, P. F. (1992). Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron 8, 831-842.
14. Audebert, S., Desbruyéres, E., Gruszczynski, C., Koulakoff, A., Gros, F., Denoulet, P., and Eddé, B. (1993). Reversible polyglutamylation of α- and β-tubulin and microtubule dynamics in mouse brain neurons. Mol. Biol. Cell 4, 615-626.
15. Audebert, S., Koulakoff, A., Berwald-Netter, Y., Gros, F., Denoulet, P., and Eddé, B. (1994). Developmental regulation of polyglutamylated α- and β-tubulin in mouse brain neurons. J. Cell Sci. 107, 2313-2322.
16. Bai, R. L., Lin, C., Nguyen, N. Y., Liu, T. Y., and Hamel, E. (1989). Identification of the cysteine residue of beta-tubulin affected by the antimitotic agent 2,4-dichlorobenzyl thiocyanate, facilitated by separation of the protein subunits of tubulin by hydrophobic column chromatography. Biochemistry 28, 5606-5612.
17. Banerjee, A. (1997). Differential effects of colchicine and its B-ring modified analog MTPT on the assembly-independent GTPase activity of purified β-tubulin isoforms from bovine brain. Biochem. Biophys. Res. Commun. 231, 698-700.
18. Banerjee, A., and Ludueña, R. F. (1987). Kinetics of association and dissociation of colchicinetubulin complex from brain and renal tubulin. Evidence for the existence of multiple isotypes of tubulin in brain with differential affinity to colchicine. FEBS Lett. 219, 103-107.
19. Banerjee, A., and Ludueña, R. F. (1991). Distinct colchicine binding kinetics of bovine brain tubulin lacking the type III isotype of β-tubulin. J. Biol. Cliem. 266, 1689-1691.
20. Banerjee, A., and Ludueña, R. F. (1992). Kinetics of colchicine binding to purified β-tubulin isotypes from bovine brain. J. Biol. Chem. 267, 13335-13339.
21. Banerjee, A., Roach, M. C., Wall, K. A., Lopata, M. A., Cleveland, D. W., and Ludueña, R. F. (1988). A monoclonal antibody against the type II isotype of β-tubulin. Preparation of isotypically altered tubulin. J. Biol. Chem. 263, 3029-3034.
22. Banerjee, A., Roach, M. C, Trcka, P., and Luduena, R. F. (1990). Increased microtubule assembly in bovine brain tubulin lacking the type III isotype of β-tubulin. J. Biol. Chem. 265, 1794-1799.
23. IV tubulin dimers from bovine brain. J. Biol. Chem. 267, 5625-5630.
24. Iv. J. Biol. Chem. 269, 10324-10329.
25. IV. Eur. J. Biochem. 246, 420-424.
26. Barahona, I., Soares, H., Cyme, L., Penque, D., Denoulet, P., and Rodrigues-Pousada, C. (1988). Sequence of one α- and two β-tubulin genes of Tetrahymena pyriformis. J. Mol. Biol 202, 365-382.
27. Barra, H. S., Arce, C. A., Rodríguez, J. A., and Caputto, R. (1974). Some common properties of the protein that incorporates tyrosine as a single unit and the microtubule proteins. Biochem. Biophys. Res. Commun. 60, 1384-1390.
28. Behnke, O., and Forer, A. (1967). Evidence for four classes of microtubules in individual cells. J. Cell Sci. 2, 169-192.
29. Bernier-Valentin, F., Aunis, D., and Roussel, B. (1983). Evidence for tubulin-binding sites on cellular membranes: Plasma membranes, mitochondrial membranes, and secretory granule membranes. J. Cell Biol. 97, 209-216.
30. Best, A., Ahmed, S., Kozma, R., and Lim, L. (1996). The ras-related GTPase Racl binds tubulin. J. Biol. Chem. 271, 3756-3762.
31. Bhattacharyya, B., and Wolff, J. (1975). Membrane-bound tubulin in brain and thyroid tissue. J. Biol. Chem. 250, 7639-7646.
32. Bicker, J. J., and Yazdani-Buicky, M. (1992). The multiple β-tubulin genes of Xenopus: Isolation and developmental expression of a germ-cell isotype β-tubulin gene. Differentiation (Berlin) 50, 15-23.
33. Bo, J., and Wensink, P. C. (1989). The promoter region of the Drosophila α2-tubulin gene directs testicular and neural specific expression. Development (Cambridge, UK) 106, 581-587.
34. Bond, J. F., Fridovich-Keil, J. L., Pillus, L., Mulligan, R. C., and Solomon, F. (1986). A chicken-yeast chimeric β-tubulin protein is incorporated into mouse microtubules in vivo. Cell (Cambridge, Mass.) 44, 461-468.
35. Boucher, D., Larcher, J.-C., Gros, F., and Denoulet, P. (1994). Polyglutamylation of tubulin as a progressive regulator of in vitro interactions between the microtubule-associated protein tau and tubulin. Biochemistry 33, 12471-12477.
36. Bré, M.-H., Redeker, V., Quibell, M., Darmanaden-Delorme, J., Bressac, C., Cosson, J., Huitorel, P., Schmitter, J.-M., Rossier, J., Johnson, T., Adoutte, A., and Levilliers, N. (1996). Axonemal tubulin polyglycylation probes with two monoclonal antibodies: Widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J. Cell Sci. 109, 727-738.
37. Bressac, C., Bré, M.-H., Darmanaden-Delorme, J., Laurent, M., Levilliers, N., and Fleury, A. (1995). A massive new posttranslational modification occurs on axonemal tubulin at the final step of spermatogenesis in Drosophila. Eur. J. Cell Biol. 67, 346-355.
38. Breviario, D., Giam, S., and Meoni, C. (1995). Three rice cDNA clones encoding different β-tubulin isotypes. Plant Physiol. 108, 823-824.
39. Bryan, J., and Wilson, L. (1971). Are cytoplasraic microtubules heteropolymers? Proc. Natl. Acad. Sci. U.S.A. 68, 1762-1766.
40. Bughio, N. I., Faubert, G. M., and Prichard, R. K. (1991). Identification of tubulin isoforms in different tissues of Ascaris suiim using anti-tubulin monoclonal antibodies. Int. J. Parasitol. 21, 913-918.
41. Buhr, T. L., and Dickman, M. B. (1994). Isolation, characterization, and expression of a second β-tubulin-encoding gene from Collectotriclmm gloeosporiodes f. Sp. aeschynomene, Appl. Environ. Microbiol. 60, 4155-4159.
42. Burgoyne, R. D., Cambray-Deakin, M. A., Lewis, S. A., Sarkar, S., and Cowan, N. J. (1988). Differential distribution of β-tubulin isotypes in cerebellum. EMBO J. 7, 2311-2319.
43. Burland, T. G., Paul, E. C. A., Oetliker, M., and Dove, W. F. (1988). A gene encoding the major beta tubulin of the mitotic spindle in Physarum polycephalum plasmodia. Mol. Cell. Biol. 8, 1275-1281.
44. Burns, R. G., and Surridge, C. (1990). Analysis of β-tubulin sequences reveals highly conserved, coordinated amino acid substitutions. Evidence that these 'hot spots' are directly involved in the conformational change required for dynamic instability. FEBS Lett. 271, 1-8.
45. Buttgereit, D., Paululat, A., and Renkawitz-Pohl, R. (1996). Muscle development and attachment to the epidermis is accompanied by expression of β3 and β1 tubulin isotypes, respectively. Int. J. Dev. Biol. 40, 189-196.
46. Byrd, A. D., Schardl, C. L., Songlin, P. J., Mogen, K. L., and Siegel, M. R. (1990). The β-tubulin gene of Epichloë typhina from perennial ryegrass (Lolium perenne). Curr. Genet. 18, 347-354.
47. Caccamo, D., Katsetos, C. D., Herman, M. M., Frankfurter, A., Collins, V. P., and Rubinstein, L. J. (1989). Immunohistochemistry of a spontaneous murine ovarian teratoma with neuroepithelial differentiation. Lab. Invest. 60, 390-398.
48. Cameron, L. E., Hutsul, J.-A., Thorlacius, L., and LéJohn, H. B. (1990). Cloning and analysis of β-tubulin gene from a protoctist. J. Biol. Chern. 265, 15245-15252.
49. Canals, J. M., Ruiz-Avila, L., Aguado, F., Majó, G., and Marsal, J. (1995). Cloning, characterization and expression of the cDNA encoding a neuron-specific α-tubulin isoform highly represented in the electric lobe of Torpedo marmorata. Gene 158, 219-223.
50. Carpenter, J. L., Ploense, S. E., Snustad, D. P., and Silflow, C. D. (1992). Preferential expression of an α-tubulin gene of Arabidopsis in pollen. Plant Cell 4, 557-571.
51. Casano, C., Ragusa, M., Cutrera, M., Costa, S., and Gianguzza, F. (1996). Spatial expression of a and β tubulin genes in the late embryogenesis of the sea urchin Paracentrolus lividus. Int. J. Dev. Biol. 40, 1033-1041.
52. Casu, R. E. (1993). Sequence of a cDNA encoding β-tubulin from Babesia bovis. Mol. Biochein. Parasitol. 59, 339-340.
53. Chu, B., Snustad, D. P., and Carter, J. V. (1993). Alteration of β-tubulin gene expression during low-temperature exposure in leaves of Arabidopsis thaliana. Plant Physiol. 103, 371-377.
54. Cleveland, D. W. (1987). The multitubulin hypothesis revisited: What have we learned? J. Cell Biol. 104, 381-383.
55. Cleveland, D. W., and Sullivan, K. F. (1985). Molecular biology and genetics of tubulin. Annu. Rev. Biochem. 54, 331-365.
56. Coe, I. R., Munro, R., and Sherwood, N. M. (1992). Isolation of different brain-specific isotypes of α-tubulins from chum salmon (Oncorhynchus keta). DNA Seq. - J. DNA Seq. Map. 3, 257-262.
57. Conner, T. W., Thompson, M. D., and Silflow, C. D. (1989). Structure of the three β-tubulin-encoding genes of the unicellular alga, Polytomella agilis. Gene 84, 345-358.
58. Conzelmann, K. K., and Helftenbein, E. (1987). Nucleotide sequence and expression of two β-tubulin genes in Stylonichia lemnae. J. Mol. Biol. 198, 643-653.
59. Cooley, R. N., and Caten, C. E. (1993). Molecular analysis of the Septoria nodorum β-tubulin gene and characterization of a benomyl-resistance mutation. Mol. Gen. Genet. 237, 58-64.
60. Correia, J. J., Lipscomb, L. D., and Lobert, S. (1993). Nondisulfide crosslinking and chemical cleavage of tubulin subunits: pH and temperature dependence. Arch. Biochem. Biophys. 300, 105-114.
61. Coulson, R. M. R., Connor, V., Chen, J. C., and Ajioka, J. W. (1996). Differential expression of Leishmania major β-tubulin genes during the acquisition of promastigote infectivity. Mol. Biochem. Parasitol. 82, 227-236.
62. Cowan, N. J., and Dudley, L. (1983). Tubulin isotypes and the multigene tubulin families. Int. Rev. Cytol. 85, 147-173.
63. Cowan, N. J., Lewis, S. A., Gu, W., and Burgoyne, R. D. (1988). Tubulin isotypes and their interaction with microtubule associated proteins. Protoplasma 145, 106-111.
64. v-src in PC12 cells. J. Mol. Neurosci. 4, 63-71.
65. Crute, B. E., and Van Buskirk, R. G. (1992). A casein kinase-like kinase phosphorylates β-tubulin and may be a microtubule-associated protein. J. Neurochem. 59, 2017-2023.
66. Cunningham, D. B., Buchschacher, G. L., Burland, T. G., Dove, W. F., Kassier, D., and Paul, E. C. A. (1993). Cloning and characterization of the altA α-tubulin gene of Physarum. J. Gen. MicrobioL 139, 137-151.
67. Damen, W. G. M., van Grunsven, L. A., and van Loon, A. E. (1994). Transcriptional regulation of tubulin gene expression in differentiating trochoblasts during early development of Patella vulgata. Development (Cambridge, UK) 120, 2835-2845.
68. Davis, M.-T. B., and Miller, S. G. (1988). Expression of a testis β-tubulin gene in Heliothis virescens during spermatogenesis. Insect Biochem. 18, 389-394.
69. Delgado-Viscogliosi, P., Brugerolle, G., and Viscogliosi, E. (1996). Tubulin post-translational modifications in the primitive protist Trichomonas vaginalis. Cell Motil. Cytoskel. 33, 288-297.
70. Delves, C. J., Ridley, R. G., Goman, M., Holloway, S. P., Hyde, J. E., and Scaife, J. G. (1989). Cloning of a β-tubulin gene from Plasmodium falciparum. Mol. Microbiol. 3, 1511-1519.
71. Demers, D. M., Metcalf, A. E., Talbot, P., and Hyman, B. C. (1996). Multiple lobster tubulin isoforms are encoded by a simple gene family. Gene 171, 185-191.
72. de Pereda, J. M., and Andreu, J. M. (1996). Mapping surface sequences of the tubulin dimer and taxol-induced microtubules with limited proteolysis. Biochemistry 35, 14184-14202.
73. de Pereda, J. M., Leynadier, D., Evangelio, J. A., Chacón, P., and Andreu, J. M. (1996). Tubulin secondary structure analysis, limited proteolysis sites, and homology to FtsZ. Biochemistry 35, 14203-14215.
74. Deny, W. B., Wilson, L., Khan, I. A., Luduena, R. F., and Jordan, M. A. (1997). Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified β-tubulin isotypes. Biochemistry 36, 3554-3562.
75. Detrich, H. W., and Parker, S. K. (1993). Divergent neural β tubulin from the Antarctic fish Notothenia coriiceps neglecta: Potential sequence contributions to cold adaptation of microtubule assembly. Cell Motil. Cytoskel. 24, 156-166.
76. Detrich, H. W., Prasad, V., and Luduena, R. F. (1987). Cold-stable microtubules from Antarctic fishes contain unique a tubulins. J. Biol. Chem. 262, 8360-8366.
77. Detrich, H. W., Fitzgerald, T. J., Dinsmore, J. H., and Marchese-Ragona, S. P. (1992). Brain and egg tubulins from Antarctic fishes are functionally and structurally distinct. J. Biol. Chem. 267, 18766-18775.
78. Dettman, R. W., Turner, F. R., and Raff, E. C. (1996). Genetic analysis of the Drosophila β3-tubulin gene demonstrates that the microtubule cytoskeleton in the cells of the visceral mesoderm is required for morphogenesis of the midgut endoderm. Dev. Biol. 177,117-135.
79. Diaz, E. C., Martin, F., and Tagu, D. (1996). Eucalypt α-tubulin: cDNA cloning and increased level of transcripts in ectomycorrhizal root system. Plant Mol. Biol. 31, 905-910.
80. Diaz-Nido, J., Serrano, L., López-Otin, C., Vandekerckhove, J., and Avila, J. (1990). Phosphorylation of a neuronal-specific β-tubulin isotype. J. Biol. Chem. 265, 13949-13954.
81. Dibbayawan, T. P., Harper, J. D. I., Elliott, J. E., Gunning, B. E. S., and Marc, J. (1995). A γ-tubulin that associates specifically with centrioles in HeLa cells and the basal body complex in Chlamydomonas. Cell Biol. Int. 19, 559-567.
82. Di Bernardo, M. G., Gianguzza, F., Ciaccio, M., Palla, F., Colombo, P., Di Blasi, F., Fais, M., and Spinelli, G. (1989). Nucleotide sequence of a full length cDNA clone encoding for β-tubuIin of the sea urchin Paracentrotus lividus. Nucleic Acids Res. 17, 5851.
83. Diggins, M. A., and Dove, W. F. (1987). Distribution of acetylated alpha-tubulin in Physarum polycephalum. J. Cell Dial. 104, 303-309.
84. Dobrzyhski, J. K., Sternlicht, M. L., Fair, G. W., and Sternlicht, H. (1996). Newly-synthesized β-tubulin demonstrates domain-specific interactions with the cytosolic chaperonin. Biochemistry 35, 15870-15882.
85. Doshi, P., Bossie, C. A., Doonan, J. H., May, G. S., and Morris, N. R. (1991). Two α-tubulin genes of Aspergillus nidulans encode divergent proteins. Mol. Gen. Genet. 225,1129-141.
86. Driscoll, M., Dean, E., Reilly, E., Bergholz, E., and Chalfie, M. (1989). Genetic and molecular analysis of a Caenorhabdilis elegans β-tubulin that conveys benzimidazole sensitivity. J. Cell Biol. 109, 2993-3003.
87. Dudek, S. M., and Johnson, G. V. W. (1995). Postnatal changes in serine/threonine protein phosphatases and their association with the microtubules. Dev. Brain Res. 90, 54-61.
88. Dumontet, C., Duran, G. E., Steger, K. A., Beketic-Oreskovic, L., and Sikic, B. I. (1996). Resistance mechanisms in human sarcoma mutants derived by single-step exposure to paclitaxel (taxol). Cancer Res. 56, 1091-1097.
89. Dupuis, P. (1992). The β-tubulin genes of Parameciiim are interrupted by two 27 bp introns. MBO J. 11, 3713-3719.
90. Dupuis-Williams, P., Klotz, C., Mazarguil, H., and Beisson, J. (1996). The tubulin gene family of Parameciiim: Characterization and expression of the αPT1 and αPT2 genes which code for α-tubulins with unusual C-terminal amino acids, GLY and ALA. Biol. Cell. 87, 83-93.
91. Duvaux-Miret, O., Baratte, B., Dissous, C., and Capron, A. (1991). Molecular cloning and sequencing of the α-tubulin gene from Schistosoma mansoni. Mol. Biochem. Parasitol. 49, 337-340.
92. Dyer, M., Volpe, F., Delves, C. J., Somia, N., Burns, S., and Scaife, J. G. (1992). Cloning and sequence of a β-tubulin cDNA from Pnemnocystis carinii: Possible implications for drug therapy. Mol. Microbiol. 6, 991-1001.
93. Eddé, B., Rossier, J., Le Caer, J.-P., Desbruyères, E., Gros, F., and Denoulet, P. (1990). Posttranslational glutamylation of α-tubulin. Science 247, 83-85.
94. Eddé, B., Rossier, J., Le Caer, J.-P., Promé, J.-C., Desbruyères, E., Gros, F., and Denoulet, P. (1992). Polyglutamylated α-tubulin can enter the tyrosination/detyrosination cycle. Biochemistry 31, 403-410.
95. Edlind, T. D., Li, J., Visvesvara, G. S., Vodkin, M. H., McLaughlin, G. L., and Katiyar, S. K. (1996). Phylogenetic analysis of β-tubulin sequences from amitochondrial protozoa. Mol. Phylogenet. Evol. 5, 359-367.
96. Eipper, B. A. (1972). Rat brain microtubule protein: Purification and determination of covalently bound phosphate and carbohydrate. Proc. Natl. Acad. Sci. U.S.A. 69, 2283-2287.
97. Eipper, B. A. (1974a). Rat brain tubulin and protein kinase activity. J. Biol. Client. 249, 1398-1406.
98. Eipper, B. A. (1974b). Properties of rat brain tubulin. J. Biol. Chem. 249, 1407-1416.
99. Elard, L., Comes, A. M., and Humbert, J. F. (1996). Sequences of β-tubulin cDNA from benzimidazole-susceptible and -resistant strains of Teladorsagia circumcinta, a nematode parasite of small ruminants. Mol. Biochem. Parasitol. 79, 249-253.
100. Erickson, H. P. (1995). FtsZ, a prokaryotic homolog of tubulin? Cell (Cambridge, Mass.) 80, 367-370.
101. Erickson, H. P., Taylor, D. W., Taylor, K. A., and Bramhill, D. (1996). Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc. Nat!. Acad. Sci. U.S.A. 93, 519-523.
102. Ersfeld, K., Wehland, J., Plessmann, Dodermont, H., Gerke, V., and Weber, K. (1993). Characterization of the tubulin-tyrosine ligase. J. Cell Biol. 120, 725-732.
103. Fackenthal, J. D., Turner, F. R., and Raff, E. C. (1993). Tissue-specific microtubule functions in Drosophila spermatogenesis require the β-tubulin isotype-specific carboxy terminus. Dev. Biol. 158, 213-227.
104. Fackenthal, J. D., Hutchens, J. A., Turner, F. R., and Raff, E. C. (1995). Structural analysis of mutations in the Drosophila β2-tubulin isoform reveals regions in the β-tubulin molecule required for general and for tissue-specific microtubule functions. Genetics 139, 267-286.
105. Falconer, M. M., Echeverri, C. J., and Brown, D. L. (1992). Differential sorting of beta tubulin isotypes into colchicine-stable microtubules during neuronal and muscle differentiation of embryonal carcinoma cells. Cell Motil. Cyloskel. 21, 313-325.
106. Falconer, M. M., Vaillant, A., Reuhl, K. R., Laferrière, N., and Brown, D. L. (1994). The molecular basis of microtubule stability in neurons. NeuroToxicology 15, 109-122.
107. Ferreira, A., and Caceres, A. (1992). Expression of the class III β-tubulin isotype in developing neurons in culture. J. Neurosd. Res. 32, 516-529.
108. Fong, D., Wallach, M., Keithly, J., Melera, P. W., and Chang, K.-P. (1994). Differential expression of mRNAs for α- and β-tubulin during differentiation of the parasitic protozoan Leishmania mexicana. Proc. Natl. Acad. Sci. U.S.A. 81, 5782-5786.
109. Fontalba, A., Avila, J., and Zabala, J. C. (1995). β-Tubulin folding is modulated by the isotypespecific carboxy-terminal domain. J. Mol. Biol. 246, 628-636.
110. Fosket, D. E., Tonoike, H., Han, I.-S., and Colon, A. (1993). What is the significance of the relatively large tubulin multigene families for plant morphogenesis? In "Morphogenesis in Plants" (K. A. Roubelakis-Angelakis and K. Tran Thanh Van, eds.), pp. 55-87. Plenum, New York.
111. Fouquet, J.-P., Eddé, B., Kann, M.-L., Wolff, A., Desbruyères, E., and Denoulet, P. (1994). Differential distribution of glutamylated tubulin during spermatogenesis in mammalian testis. Cell Motil. Cyloskel. 27, 49-58.
112. Fouquet, J.-P., Prigent, Y., and Kann, M.-L. (1996). Comparative immunogold analysis of tubulin isoforms in the mouse sperm flagellum: Unique distribution of glutamylated tubulin. Mol. Reprod. Dev. 43, 358-365.
113. Fuchs, U., Moepps, B., Maucher, H. P., and Schraudolf, H. (1993). Isolation, characterization and sequence of a cDNA encoding γ-tubulin protein from the fern Anemia phyllitidis L. Sw. Plant Mol. Biol. 23, 595-603.
114. Fukushige, T., Yasuda, H., and Siddiqui, S. S. (1993). Molecular cloning and developmental expression of the alpha-2 tubulin gene of Caenorhabditis elegans. J. Mol. Biol. 234, 1290-1300.
115. Fukushige, T., Yasuda, H., and Siddiqui, S. S. (1995). Selective expression of the tba-1 α tubulin gene in a set of mechanosensory and motor neurons during the development of Caenorhabditis elegans. Biochim. Biophys. Acta 1261, 401-416.
116. Fuller, M. T., Caulton, J. H., Hutchens, J. A., Kaufman, T. C., and Raff, E. C. (1987). Genetic analysis of microtubule structure: A β-tubulin mutation causes the formation of aberrant microtubules in vivo and in vitro. J. Cell Biol. 104, 385-394.
117. Fuller, S. D., Gowen, B. E., Reinsch, S., Sawyer, A., Buendia, B., Wepf, R., and Karsenti, E. 1995). The core of the mammalian centriole contains γ-tubulin. Curr. Biol. 5, 1384-1393.
118. Fulton, C., and Simpson, P. A. (1976). Selective synthesis and utilization of flagellar tubulin. The multi-tubulin hypothesis. In "Cell Motility" (R. Goldman, T. Pollard, and J. Rosenbaum, eds.), Vol. 3, pp. 987-1005. Cold Spring Harbor Lab. Press, Cold Spring Harbor, NY.
119. Furuhata, S., Kameya, T., Toya, S., and Frankfurter, A. (1993). Immunohistochemical analysis of 61 pituitary adenomas with a monoclonal antibody to the neuron-specific β-tubulin isotype. Acta Neuropalhol. 86, 518-520.
120. Gaertig, J., Thatcher, T. H., McGrath, K. E., Callahan, R. C., and Gorovsky, M. A. (1993). Perspectives on tubulin isotype function and evolution based on the observation that Tetra-hymena thermophila microtubules contain a single α- and β-tubulin. Cell Molil. Cytoskel. 25, 243-253.
121. Gagnon, C., White, D., Cosson, J., Huitorel, P., Eddé, B., Desbruyères, E., Paturle-Lafanechère, L., Multigner, L., Job, D., and Cibert, C. (1996). The polyglutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility. J. Cell Sci. 109, 1545-1553.
122. Gallo, J.-M., and Precigout, E. (1988). Tubulin expression in trypanosomes. Biol. Cell. 64, 137-143.
123. Garber, A. T., Hawkins, N., and Dixon, G. H. (1991). The predicted protein sequence of a fish testis-specific α-tubulin cDNA shows conservation of isotype-specific amino acid substitutions. DNA Seq. 2, 47-51.
124. Garcia-Rocha, M., Avila, J., and Lozano, J. (1997). The ζ isozyme of protein kinase C binds to tubulin through the pseudosubstrate domain. Exp. Cell Res. 230, 1-8.
125. Gard, D. L., and Kirschner, M. W. (1985). A polymer-dependent increase in phosphorylation of β-tubulin accompanies differentiation of a mouse neuroblastoma cell line. J. Cell Biol. 100, 764-774.
126. Geary, T. G., Nulf, S. C., Favreau, M. A., Tang, L., Prichard, R. K., Hatzenbuhler, N. T., Shea, M. H., Alexander, S. J., and Klein, R. D. (1992). Three β-tubulin cDNAs from the parasitic nematode Haemonchus contonus. Mol. Biochem. Parasitol. 50, 295-306.
127. Geyp, M., Ireland, C. M., and Pittman, S. M. (1996). Increased tubulin acetylation accompanies reversion to stable ploidy in vincristine-resistant CCRF-CEM cells. Cancer Genet. Cytogenet. 87, 117-122.
128. Gianguzza, F., Di Bernardo, M. G., Sollazzo, M., Palla, F., Ciaccio, M., Carra, E., and Spinelli, G. (1989). DNA sequence and pattern of expression of the sea urchin (Paracentrotus lividus) α-tubulin genes. Mol. Reprod. Dev. 1, 170-181.
129. Gianguzza, F., Di Bernardo, M. G., Fais, M., Palla, F., Casano, C., Russo, R., and Spinelli, G. (1990). Sequence and expression of Paracentrotus lividus a tubulin gene. Nucleic Acids Res. 18, 4915.
130. Gianguzza, F., Casano, C., and Ragusa, M. (1995). α-Tubulin marker gene of neural territory of sea urchin embryos detected by whole-mount in situ hybridization. Int. J. Dev. Biol. 39, 477-483.
131. Giani, S., and Breviario, D. (1996). Rice β-tubulins mRNA levels are modulated during flower development and in response to external stimuli, plant Sci. 116, 147-157.
132. Goddard, R. H., Wick, S. M., Silflow, C. D., and Snustad, D. P. (1994). Microtubule components of the plant cell cytoskeleton. Plant Physiol. 104, 1-6.
133. Gold, S. E., Casale, W. L., and Keen, N. T. (1991). Characterization of two β-tubulin genes from Geotrichiim candidiim. Mot. Gen. Genet. 230, 104-112.
134. Goldman, G. H., Temmerman, W., Jacobs, D., Contreras, R., Van Montagu, M., Herrera-Estrella, A. (1993). A nucleotide substitution in one of the β-tubulin genes of Trichoderma viride confers resistance to the antimitotic drug methyl benzimidazole-2-yl-carbamate. Mol. Gen. Genet. 240, 73-80.
135. Goldsmith, M., Connolly, J., Kumar, N., Wu, J., Yarbrough, L., and van der Kooy, D. (1991). Conserved β-tubulin binding domain for the microtubule-associated motors underlying sperm motility and fast axonal transport. Cell Molil. Cytoskel. 20, 249-262.
136. Good, P. J., Richter, K., and Dawid, I. B. (1989). The sequence of a nervous system-specific, class II β-tubulin gene from Xenopiis laevis. Nucleic Acids Res. 17, 8000.
137. Grant, W. N., and Mascord, L. J. (1996). Beta-tubulin gene polymorphism and benzimidazole resistance in Trichostrongylus colubriformis. Int. J. Parasitol. 26, 71-77.
138. Greer, K., Maruta, H., I'Hernault, S. W., and Rosenbaum, J. L. (1985). α-Tubulin acetylase activity in isolated Chlamydomonas flagella. J. Cell Biol. 101,2081-2084.
139. Gu, W., Lewis, S.A., and Cowan, N. J. (1988). Generation of antisera that discriminate among mammalian α-tubulins: Introduction of specialized isotypes into cultured cells results in their coassembly without disruption of normal microtubule function. J. Cell Biol. 106,2011-2022.
140. Guénette, S., Prichard, R. G., Klein, R. D., and Matlashewski, G. (1991). Characterization ofaβ-tubuIin gène and β-tubulin gene products of Brugia pahangi. Mol. Biochein. Parasitol. 44, 153-164.
141. Guénette, S., "Prichard, R. K., and Matlashewski, G. (1992). Identification of a novel Brugia pahangi β-tubulin gene (β2) and a 22-nucleotide spliced leader séquence on β1-tubulin mRNA. Mol. Biochem. Parasitol. 50, 275-284.
142. Guiltinan, M. J., Ma, D.-P., Barker, R. F., Bustos, M. M., Cyr, R. J., Yadegari, R., and Fosket, D. E. (1987). The isolation, characterization and sequence of two divergent β-tubulin gènes from soybean (Glycine max L.). Plant Mol. Biol. 10, 171-184.
143. Gundersen, G. G., Kalmoski, M. H., and Bulinski, J. C. (1984). Distinct populations of microtubules: Tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell (Cambridge, Mass.) 38, 779-789.
144. Gurland, G., and Gundersen, G. G. (1995). Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J. Cell Biol. 131, 1275-1290.
145. Haber, M., Burkhart, C. A., Regl, D. L., Madafiglio, J., Norris, M. D., and Horwitz, S. B. (1995). Altered expression of Mβ2, the class II β-tubulin isotype, in a murine J774.2 cell line with a high level of taxol resistance. J. Biol. Chem. 270, 31269-31275.
146. Hamelin, M., Scott, I. M., Way, J. C., and Culotti, J. G. (1992). The mec-7 β-tubulin gene of Caenorhabditis elegans is expressed primarily in the touch receptor neurons. EMBO J. 11, 2885-2893.
147. Harlow, P., and Nemer, M. (1987a). Developmental and tissue-specific regulation ofβ-tubulin gene expression in the embryo of the sea urchin Slrongylocentroliis purpiiratiis. Genes Dev. 1, 147-160.
148. Harlow, P., and Nemer, M. (19875). Coordinate and selective β-tubulin gene expression associated with cilium formation in sea urchin embryos. Genes Dev. 1, 1293-1304.
149. Harlow, P., Litwin, S., and Nemer, M. (1988). Synonymous nucleotide substitution rates of β-tubulin and histone genes conform to high overall genomic rates in rodents but not in sea urchins. J. Mol. Evol. 27, 56-64.
150. Harper, D. S., and Jahn, C. L. (1989). Differential use of termination codons in ciliated protozoa. Proc. Natl. Acad. Sci. U.S.A. 86, 3252-3256.
151. Harper, J. F., and Mages, W. (1988). Organization and structure of Volvox β-tubulin genes. Mol Gen. Genet. 213, 315-325.
152. Harris, G. S., Keath, E. J., and Medoff, J. (1989). Characterization of alpha and beta tubulin genes in the dimorphic fungus Histoplasma capsiilatum. J. Gen. Microbiol. 135,1817-1832.
153. Havercroft, J. C., and Cleveland, D. W. (1984). Programmed expression of β-tubulin genes during development and differentiation of the chicken. J. Cell Biol. 99,1927-1935.
154. Hawksworth, D. L., Sutton, B. C., and Ainsworth, G. C. (1983). "Dictionary of the Fungi," 7th ed. Commonwealth Mycological Institute, Kew, Surrey, UK.
155. Hecht, N. B., Distel, R. J., Yelick, P. C., Tanhauser, S. M., Driscoll, C. E., Goldberg, E., and Tung, K. S. K. (1988). Localization of a highly divergent mammalian testicular a tubulin that is not detectable in brain. Mol. Cell. Biol. 8, 996-1000.
156. Helm, R., Selkirk, M. E., Bradley, J. E., Burns, R. G., Hamilton, A. J., Crofts, S., and Maizels, R. M. (1989). Localization and immunogenicity of tubulin in the filarial nematodes Brugia malayi and B. pahangi. Parasite Imnmnol. 11, 479-502.
157. Hiraoka, Y., Toda, T., and Yanagida, M. (1984). The NDA3 gene of fission yeast encodes β-tubulin: a cold sensitive nda3 mutation reversibly blocks spindle formation and chromosome movement in mitosis. Cell (Cambridge, Mass.) 39, 349-358.
158. Huffman, P. N., and Cleveland, D. W. (1988). Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: Induction of a specific β-tubulin isotype. Proc. Natl. Acad. Sci. U.S.A. 85, 4530-4533.
159. Huffman, P. N., and Luduena, R. F. (1996). Changes in the isotype composition of β-tubulin delivered to regenerating sensory axons by slow axonal transport. Brain Res. 742, 329-333.
160. Huffman, P. N., Lopata, M. A., Watson, D. F., and Luduena, R. F. (1992). Axonal transport of class II and III β-tubulin: Evidence that the slow
161. Holloway, S. P., Gerousis, M., Delves, C. J., Sims, P. F. G., Scaife, J. G., and Hyde, J. E. (1990). The tubulin genes of the human malaria parasite Plasmodiiim falcipantm, their chromosomal location and sequence analysis of the α-tubulin II gene. Mol. Biochem. Parasitol. 43, 257-270.
162. Hoyle, H. D., and Raff, E. C. (1990). Two Drosophila beta tubulin isoforms are not functionally equivalent. J. Cell Biol. 11, 1009-1026.
163. Hoyle, H. D., Hutchens, J. A., Turner, F. R., and Raff, E. C. (1995). Regulation of β-tubulin βm function and expression in Drosophila spermatogenesis. Dev. Genet. 16,148-170.
164. Hussey, P. J., Naas, N., Hunsperger, J., Larkin, J., Snustad, D. P., and Silfiow, C. D. (1990). The β-tubulin gene family in Zea mays: Two differentially expressed β-tubulin genes. Plant Mol. Biol. 15, 957-972.
165. Hyams, J. S., and Lloyd, C. \V., eds. (1994). "Microtubules." Wiley-Liss, New York.
166. Ikeda, Y., and Steiner, M. (1978). Sulfhydryls of platelet tubulin: Their role in polymerization and colchicine binding. Biochemistry 17, 3454-3459.
167. Ilschner, S., and Brandt, R. (1996). The transition of microglia to a ramified phenotype is associated with the formation of stable acetylated and detyrosinated microtubules. Glia 18, 129-140.
168. Janiak, A., Villar, R., Cassoly, R., and Rendu, F. (1995). Tubulin is not phosphorylated in resting and thrombin-activated platelets. J. Biochem. (Tokyo) 117, 296-302.
169. III and other tubulin genes during peripheral and central neuron development. J. Cell Sci. 103, 643-651.
170. Jongewaard, I., Colon, A., and Fosket, D. E. (1994). Distribution of transcripts of the tubBl β-tubulin gene in developing soybean (Glycine max [L.] Merr.) seedling organs. Protoplasma 183, 77-85.
171. Joseph, M. K., Fernström, M. A., and Soloff, M. S. (1982). Switching of β- to α-tubulin phosphorylation in uterine smooth muscle of parturient rats. J. Biol. Chem. 257, 11728-11733.
172. Joshi, H. C., and Cleveland, D. W. (1989). Differential utilization of β-tubulin isotypes in differentiating neuntes. J. Cell Biol. 109, 663-673.
173. Joshi, H. C., and Cleveland, D. W. (1990). Diversity among tubulin subunits: Toward what functional end? Cell Motil. Cytoskel. 16, 159-163.
174. Joshi, H. C., Yen, T. J., and Cleveland, D. W. (1987). In vivo coassembly of a divergent β-tubulin subunit (cβ6) into microtubules of different function./. Cell Biol. 105,2179-2190.
175. Joyce, C. M., Villemur, R., Snustad, D. P., and Silfiow, C. D. (1992). Tubulin gene expression in maize (Zea mays L.). Change in isotype expression along the developmental axis of seedling root. J. Mol. Biol. 227, 97-107.
176. Kang, M. S., Choi, Y., J., Kirn, M. C., Lim, C. O., Hwang, I., and Cho, M. J. (1994). Isolation and characterization of twoβ-tubulin cDNA clones from rice. Plant Mol. Biol. 26,1975-1979.
177. Kapeller, R., Toker, T., Cantley, L. C., and Carpenter, C. L. 1995). Phosphoinositide 3-kinase binds constitutively to o/β-tubulin and binds to -y-tubulin in response to insulin. J. Biol. Chem. 270, 25985-25991.
178. Katiyar, S. K., and Edlind, T. D. (1994). β-tubulin genes of Trichomonas vaginalis. Mol. Biochem. Parasitol. 64, 33-42.
179. Katsetos, C. D., Herman, M. M., Frankfurter, A., offer, S., Perentes, E., and Rubinstein, L. J. (1991). Neuron-associated class III β-tubulin isotype, microtubule-associated protein 2, and synaptophysin in human retinoblastomas in situ. Lab. Invest. 64, 45-54.
180. Kemphues, K. J., Kaufman, T. C., Raff, R. A., and Raff, E. C. (1982). The testis-specific β-tubulin subunit in Drosophila melanogaster has multiple functions in spermatogenesis. Cell (Cambridge, Mass.) 31, 655-670.
181. Khan, I. A., and Luduena, R. F. (1995). Effect of vinblastine on the assembly of isotypically pure tubulins from bovine brain, Mol. Biol. Cell 6, 30a.
182. III-tubulin. Biochemistry 35, 3704-3711.
183. Khawaja, S., Gundersen, G. G., and Bulinski, J. C. (1988). Enhanced stability of microtubules enriched in detyrosinated tubulin is not a direct function of detyrosination level. J. Cell Biol. 106, 141-149.
184. Kimble, M., Incardona, J. P., and Raff, E. C. (1989). A variant β-tubulin isoform of Drosophila melanogaster (β3) is expressed primarily in tissues of mesodermal origin in embryos and pupae, and is utilized in populations of transient microtubules. Dev. Biol. 131, 415-429.
185. Kimble, M., Dettman, R. W., and Raff, E. C. (1990). The β3-tubuIin gene of Drosophila melanogaster is essential for viability and fertility. Genetics 126, 991-1005.
186. Kimmel, J. E., Samson, S., Wu, J., Hirschberg, R., and Yarbrough, L. R. (1985). Tubulin genes of the African trypanosome Trypanosoma brucei rhodesiense: Nucleotide sequence of a 3.7 kb fragment containing genes for alpha and beta tubulins. Gene 35, 237-248.
187. Kirk, K. E., and Morris, N. R. (1993). Either β-tubulin isogene product is sufficient for microtubule function during all stages of growth and differentiation in Aspergillus nidulans. Mol. Cell. Biol. 13, 4465-4476.
188. Kirk-Mason, K. E., Turner, M. J., and Chakraborty, P. R. (1988). Cloning and sequence of tubulin cDNA from Giardia lamblia. Nucleic Acids Res. 16, 2733.
189. Klein, R. D., Nulf, S. C., Alexander-Bowman, S. J., Mainone, C. B., Winterrowd, C. A., and Geary, T. G. (1992). Cloning of a cDNA encoding α-tubulin from Haemonclms contortus. Mol. Biochem. Parasitol. 56, 345-348.
190. Koga-Ban, Y., Niki, T., Nagamura, Y., Sasaki, T., and Minobe, Y. (1995). cDNA sequences of three kinds of β-tubulins from rice. DNA Res. 2, 21-26.
191. Komma, D. J., and Endow, S. A. (1997). Enhancement of the ncd microtubule motor mutant by mutants of αTub67C. J. Cell Sci. 110, 229-237.
192. Koontz, D. A., and Choi, J. H. (1993). Evidence for phosphorylation of tubulin in carrot suspension cells. Physiol. Plant. 87, 576-583.
193. Kopczak, S. D., Haas, N. A., Hussey, P. J., Silflow, C. D., and Snustad, D. P. (1992). The small genome of Arabidopsis contains at least six expressed α-tubulin genes. Plant Cell 4, 539-547.
194. Kost, S. A., and Oblinger, M. M. (1993). Immature corticospinal neurons respond to axotomy with changes in tubulin gene expression. Brain Res. Bull. 30, 469-475.
195. Kozminski, K. G., Diener, D. R., and Rosenbaum, J. L. (1993). High level expression of nonacetylatable α-tubulin in Chlamydomonas reinhardtii. CellMotil. Cytoskel. 25,158-170.
196. Krauhs, E., Little, M., Kempf, T., Hofer-Warbinek, R., Ade, W., and Ponstingl, H. (1981). Complete amino acid sequence of β-tubulin from porcine brain. Proc. Natl. Acad. Sci. U.S.A. 78, 4156-4160.
197. Kreis, T. E. (1987). Microtubules containing detyrosinated tubulin are less dynamic. EMBO J. 6, 2597-2606.
198. Kreis, T., and Vale, R., eds. (1993). "Guidebook to the Cytoskeletal and Motor Proteins." Oxford University Press, Oxford.
199. Kumar, N., and Flavin, M. (1981). Preferential action of a brain detyrosinolating carboxypeptidase on polymerized tubulin. J. Biol. Chem. 256, 7678-7686.
200. Kwa, M. S. G., Veenstra, J. G., and Roos, M. H. (1993). Molecular characterisation of β-tubulin genes present in benzimidazole-resistant populations of Haemonchus contortus. Mol. Biochem. Parasitol. 60, 133-144.
201. Lai, E. Y., Remillard, S. P., and Fulton, C. (1994). A β-tubulin gene of Naegleria encodes a carboxy-terminal tyrosine. Aromatic amino acids are conserved at carboxy termini. J. Mol. Biol. 235, 377-388.
202. Laing, N., Dahllöf, B., Hartley-Asp, B., Ranganathan, S., and Tew, K. D. (1997). Interaction of estramustine with tubulin isotypes. Biochemistry 36, 871-878.
203. Lajoie-Mazenc, I., Détraves, C., Rotaru, V., Garés, M., Tollon, Y., Jean, C., Julian, M., Wright, M., and Raynaud-Messina, B. (1996). A single gamma-tubulin gene and mRNA, but two gamma-tubulin polypeptides differing by their binding to the spindle pole organizing centres. J. Cell Sci. 109, 2483-2492.
204. Laporte, K., Rossignol, M., and Traas, J. A. (1993). Interaction of tubulin with the plasma membrane: Tubulin is present in purified plasmalemma and behaves as an integral membrane protein. Planta 191, 413-416.
205. Larcher, J.-C., Boucher, D., Lazereg, S., Gros, F., and Denoulet, P. (1996). Interaction of kinesin motor domains with α- and β-tubulin subunits at a tau-independent binding site. Regulation of polyglutamylation. J. Biol. Chem. 271, 22117-22124.
206. LeDizet, M., and Piperno, G. (1986). Cytoplasmic microtubules containing acetylated α-tubulin in Chlamydomonas reinhardtii: Spatial arrangement and properties. J. Cell Biol. 103, 13-22.
207. LeDizet, M., and Piperno, G. (1991). Detection of acetylated α-tubulin by specific antibodies. In "Methods in Enzymology" (R. B. Vallée, éd.), Vol. 196, pp. 264-275. Academic Press, San Diego, CA.
208. Lee, M. K., Tuttle, J. B., Rebhun, L. I., Cleveland, D. W., and Frankfurter, A. (1990). The expression and posttranslational modification of a neuron-specific β-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskel. 17, 118-132.
209. Leiss, D., Hinz, U., Gasch, A., Mertz, R., and Renkawitz-Pohl, R. (1988). β3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development (Cambridge, UK) 104, 525-531.
210. Levilliers, N., Fleury, A., and Hill, A.-M. (1995). Monoclonal and polyclonal antibodies detect a new type of post-translational modification of axonemal tubulin. J. Cell Sci. 108,3013-3028.
211. Levine, N. D., Corliss, J. O., Cox, F. E. G., Deroux, G., Grain, J., Honigberg, B. M., Leedale, G. F., Loeblich, A. R., Lom, J., Lynn, D., Merinfeld, E. G., Page, F. C., Poljansky, G., Sprague, V., Vavra, J., and Wallace, F. G. (1980). A newly revised classification of the protozoa. J. Protozool. 27, 37-58.
212. Lewis, S. A., and Cowan, N. J. (1988). Complex regulation and functional versatility of mammalian α- and β-tubulin isotypes during the differentiation of testis and muscle cells. J. Cell Biol. 106, 2023-2033.
213. Lewis, S. A., and Cowan, N. J. (1990). Tubulin genes: Structure, expression, and regulation. In "Microtubule Proteins" (J. Avila, éd.), pp. 37-66. CRC Press, Boca Raton, FL.
214. Lewis, S. A., Gilmartin, M. E., Hall, J. L., and Cowan, N. J. (1985a). Three expressed sequences within the human β-tubulin multigene family each define a distinct isotype. J. Mol. Biol. 182, 11-20.
215. Lewis, S. A., Lee, M. G. S., and Cowan, N. J. (1985b). Five mouse tubulin isotypes and their regulated expression during development. J. Cell Biol. 101, 852-861.
216. Lewis, S. A., Gu, W., and Cowan, N. J. (1987). Free intermingling of mammalian β-tubulin isotypes among functionally distinct microtubules. Cell (Cambridge, Mass.) 49, 539-548.
217. L'Hernault, S. W., and Rosenbaum, J. L. (1985). Chlamydomonas α-tubulin is posttranslationally modified by acetylation on the e-amino group of a lysine. Biochemistry 24, 473-478.
218. Li, J., Katiyar, S. K., Hamelin, A., Visvesvara, G., and Edlind, T. D. (1996). Tubulin genes from AIDS-associated microsporidia and implications for phytogeny and benzimidazole sensitivity. Mol. Biochem. Parasitol. 78, 289-295.
219. Li, Q., and Joshi, H. C. (1995). γ-Tubulin is a minus end-specific microtubule binding protein. J. Cell Biol. 131, 207-214.
220. Liang, A., and Heckmann, K. (1993). The macronuclear γ-tubulin-encoding gene of Euplotes octocarinatiis contains two introns and an in-frame TGA. Gene 136, 319-322.
221. Liang, A., Schmidt, H. J., and Heckmann, K. (1994). The α- and β-tubulin genes of Euplotes octocarinalus. J, Eukaryotic Microbiol. 41, 163-169.
222. Liang, A., Ruiz, F., Heckmann, K., Klotz, C., Tollon, Y., Beisson, J., and Wright, M. (1996). Gamma-tubulin is permanently associated with basal bodies in ciliates,. EUT. J. Cell.Biol. 70, 331-338.
223. Liaud, M.-R, Brinkmann, H., and Cerff, R. (1992). The 0-tubulin gene family of pea: Primary structures, genomic organization and intron-dependent evolution of genes. Plant Mol. Biol. 18, 639-651.
224. Liaud, M.-R, Brandt, U., and Cerff, R. (1995). The marine red alga Chondrus crispus has a highly divergent β-tubulin gene with a characteristic 5' intron: Functional and evolutionary implications. Plant Mol. Biol. 28, 313-325.
225. Linder, S., Schliwa, M., and Kube-Granderath, E. (1997). Sequence analysis and immunofiuorescence study of α- and β-tubulins in Reticulomyxa filosa: Implications of the high degree of β2-tubulin divergence. Cell Motil. Cytoskel. 36, 164-178.
226. Little, M. (1979). Identification of a second β chain in pig brain tubulin. FEES Lett. 108, 283-286.
227. Little, M., and Luduefia, R. F. (1985). Structural differences between brain β1- and β2-tubulins: Implications for microtubule assembly and colchicine binding. EMBO J. 4, 51-56.
228. Little, M., and Luduena, R. F. (1987). Location of two cysteines in brain β1-tubulin that can be cross-linked after removal of exchangeable GTP. Biochim. Biophys. Acta 912, 28-33.
229. Little, M., and Seehaus.T. (1988). Comparative analysis of tubulin sequences. Camp. Biochem. Physiol. B 90B, 655-670.
230. Little, M., Luduena, R. F., Langford, G. M., Asnes, C. F., and Farrell, K. (1981). Comparison of proteolytic cleavage patterns of α-tubulins and β-tubulins from taxonomically distant species. J. Mol. Biol. 149, 95-107.
231. Liu, B., Joshi, H. C., Wilson, T. J., Silfiow, C. D., Palevitz, B. A., and Snustad, D. P. (1994). γ-Tubulin in Arabidopsis: Gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6, 303-314.
232. Lobert, S., Frankfurter, A., and Correia, J. J. (1995). Binding of vinblastine to phosphocellulose-purified and aβ-class III tubulin: The role of nucleotides and β-tubulin isotypes. Biochemistry 34, 8050-8060.
233. Lopata, M. A., and Cleveland, D. W. (1987). In vivo microtubules are copolymers of available β-tubuIin isotypes: Localization of each of six vertebrate β-tubulin isotypes using polyclonal antibodies elicited by synthetic peptide antigens. J. Cell Biol. 105, 1707-1720.
234. Lopez, I., Khan, S., Sevik, M., Cande, W. Z., and Hussey, P. J. (1995). Isolation of a full length cDNA encoding Zea mays γ-tubulin. Plant Physiol. 107, 309-310.
235. Lu, Q., and Luduena, R. F. (1993a). Removal ofβm isotype enhances taxol induced microtubule assembly. Cell Struct. Funct. 18, 173-182.
236. Lu, Q., and Luduena, R. F. (1993b). Analysis of GTPase activities of isotypically purified bovine β tubulin dimers. Mol. Biol. Cell 4, 264a.
237. IV tubulin dimers in the absence of microtubule-associated proteins. J. Biol. Chem. 269, 2041-2047.
238. Ludueña, R. F. (1993). Are tubulin isotypes functionally significant. Mol. Biol. Cell 4, 445-457.
239. Luduena, R. R, Shooter, E. M., and Wilson, L. (1977). Structure of the tubulin dimer. J. Biol. Chem. 252, 7006-7014.
240. 2-Tubulin, a frm f chordate brain tubulin with lesser reactivity toward an assembly-inhibiting sulhydryl-directed cross-linking reagent. Biochemistry 21, 4787-4794.
241. Luduena, R. F., Roach, M. C., Jordan, M. A., and Murphy, D. B. (1985). Different reactivities of brain and erythrocyte tubulins toward a sulhydryl group-directed reagent that inhibits microtubule assembly. J. Biol. Chem. 260, 1257-1264.
242. Luduena, R. F., Anderson, W. H., Prasad, V., Jordan, M. A., Ferrigni, K. C., Roach, M. C., Horowitz, P. M., Murphy, D. B., and Fellous, A. (1986). Interactions of vinblastine and maytansine with tubulin. Ann. N. Y. Acad. Sci. 466, 718-732.
243. Luduena, R. F., Zimmermann, H.-P., and Little, M. (1988). Identification of the phosphorylated β-tubulin isotype in differentiated neuroblastoma cells. FEES Lett. 230,142-146.
244. Luduena,-R. F., Roach, M. C., Prasad, V., Chaudhuri, A. R., Tomita, L, Mizuhashi, F., and Murata, K. (1996). Interaction of bovine brain tubulin with the 4(l//)-pyrizinone derivative IKP104, an antimitotic drug with a complex set of effects on the conformational stability of the tubulin molecule. Biochemistry 34, 15751-15759.
245. Luo, H., and Perlin, M. H. (1993). The γ-tubulin-encoding gene from the basidiomycete fungus, Ustilago violacea, has a long 5'-untranslated region. Gene 137, 187-194.
246. MacKay, R. M., and Gallant, J. W. (1991). Beta-tubulins are encoded by at least four genes in the brown alga Ectocarpits variabilis. Plant Mol Biol. 17, 487-492.
247. Maraziotis, T., Perentes, E., Karamitopoulou, E., Nakagawa, Y., Gessaga, E. C., Probst, A., and Frankfurter, A. (1992). Neuron-associated class III β-tubulin isotype, retinal S-antigen, synaptophysin, and glial fibrillary acidic protein in human medulloblastomas: A clinicopathological analysis of 36 cases. Acta Neuropathol. 84, 355-363.
248. Margolin, W., Wang, R., and Kumar, M. (1996). Isolation of an ftsZ homolog from the Archaebacterium Halobacterium salinarium: Implications for the evolution of ftsZ and tubulin. J. Bacterial. 178, 1320-1327.
249. Margulis, L., and Schwartz, K. V. (1988). "Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth." Freeman, New York.
250. Margutti-Pinto, M. E. B., Khan, A., Scaife, J. A., and Fothergill-Gilmore, L. A. (1995). Organization and structure of an Onchocerca β-tubulin gene. Braz. J. Med. Biol. Res. 28,1043-1053.
251. Marschall, L. G., Jeng, R. L., Mulholland, J., and Stearns, T. (1996). Analysis of Tub4p, a yeast γ-tubulin-like protein: Implications for microtubule-organizing center function. J. Cell Biol. 134, 443-454.
252. Maruta, H., Greer, K., and Rosenbaum, J. L. (1986). The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules.J. Cell Biol. 103,571-579.
253. Mary, J., Redeker, V., Le Caer, J.-P., Promé, J.-C., and Rossier, J. (1994). Class I and IVa β-tubulin isotypes expressed in adult mouse brain are glutamylated. FEBS Lett. 353, 89-94.
254. Mary, J., Redeker, V., Le Caer, J.-P., Rossier, J., and Schmitter, J.-M. (1996). Posttranslational modifications in the C-terminal tail of axonemal tubulin from sea urchin sperm. J. Biol. Chem. 271, 9928-9933.
255. Matesic, D. F., Philp, N. J., Murray, J. M., and Liebman, P. A. (1992). Tubulin in bovine rod outer segments. J. Cell Sci. 103,157-166.
256. Matsuzaki, F., Harada, F., Nabeshima, Y., Fujii-Kuriyama, Y., and Yahara, I. (1987). Cloning of cDNAs for two β-tubulin isotypes expressed in murine T cell lymphoma, L5178Y and analysis of their translation products. Cell Struct. Funct. 12, 317-325.
257. c-src in nerve growth cone membranes. J. Cell Biol. Ill, 1959-1970.
258. Matthews, K. A., Miller, D. F. B., and Kaufman, T. C. (1989). Developmental distribution of RNA and protein products of Drosophila α-tubulin gene family. Dev. Biol. 132, 45-61.
259. Matthews, K. A., Rees, D., and Kaufman, T. C. (1993). A functionally specialized α-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila. Development (Cambridge, UK) 117, 977-991.
260. May, G. S. (1989). The highly divergent β-tubulins of Aspergillus nidtilans are functionally interchangeable.J. Cell Biol. 109, 2267-2274.
261. May, G. S., Tsang, M. L.-S., Smith, H., Fidel, S., and Morris, N. R. (1987). Aspergillus nidulans β-tubulin genes are unusually divergent. Gene 55, 231-243.
262. Mejillano, M. R., Shivanna, B. D., and Hirnes, R. H. (1996). Studies on the nocodazoleinduced GTPase activity of tubulin. Arch. Diochem. Biophys. 336, 130-138.
263. Memberg, S. P., and Hall, A. K. (1995). Dividing neuron precursors express neuron-specific tubulin. J. Neurobiol. 27, 26-43.
264. Miceli, C., Ballarini, P., de Giuseppe, G., Valbonesi, A., and Luporini, P. (1994). Identification of the tubulin gene family and sequence determination of one β-tubulin gene in a coldpoikilotherm protozoan, the Antarctic ciliate Euplotes focardii. J. Eitkaryotic Microbiol. 41, 420-427.
265. 2 tubulins are identical in Drosophila melanogaster and D. hydei but differ from the ubiquitous β1 tubulin. Chromosoma 95, 387-395.
266. Middleton, K. M., and Morgan, G. T. (1989). An oocyte-expressed α-tubulin gene in Xenopus laevis: Sequence required for the initiation of transcription. Nucleic Acids Res. 17, 5041-5055.
267. Miller, F. D., Naus, C. C., Durand, M., Bloom, F. E., and Milner, R. J. (1987). Isotypes of α-tubulin are differentially regulated during neuronal maturation. J. Cell Biol. 105, 3065-3073.
268. Miller, R. H., Lasek, R. J., and Katz, M. J. (1987). Preferred microtubules for vesicle transport in lobster axons. Science 235, 220-222.
269. Monteiro, M. J., and Cleveland, D. W. (1988). Sequence of chicken αβ1 tubulin. Analysis of a complete set of vertebrate β-tubulin isotypes. J. Mol. Biol. 199, 439-446.
270. Moody, S. A., Miller, V., Spanos, A., and Frankfurter, A. (1996). Developmental expression of a neuron-specific β-tubulin in frog (Xenopus laevis): A marker for growing axons during the embryonic period. J. Comp. Neural. 364, 219-230.
271. Moritz, M., Braunfeld, M. B., Sedat, J. W., Alberts, B., and Agard, D. A. (1995). Microtubule elongation by-γ-tubulin-containing rings in the centrosome. Nature (London) 378, 638-640.
272. Moskowitz, P. F., and Oblinger, M. M. (1995). Sensory neurons selectively upregulate synthesis and transport of the ftn-tubulin protein during axonal regeneration. j. Neurosci. 15, 1545-1555.
273. Mukherjee, A., and Lutkenhaus, J. (1994). Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacterial. 176, 2754-2758.
274. Multigner, L., Gagnon, J., Van Dorsselaer, A., and Job, D. (1992). Stabilization of sea urchin flagellar microtubules by histone HI. Nature (London) 360, 33-39.
275. Multigner, L., Pignot-Paintrand, I., Saoudi, Y., Job, D., Plessmann, U., Rüdiger, M., and Weber, K. (1996). The A and B tubules of the outer doublets of sea urchin sperm axonemes are composed of different tubulin variants. Biochemistry 35, 10862-10871.
276. Murphy, D. B., and Wallis, K. T. (1983). Isolation of microtubule protein from chicken erythrocytes and determination of the critical concentration for tubulin polymerization in vitro and in vivo. J. Biol. Chem. 258, 8357-8364.
277. Murphy, D. B., Wallis, K. T., Machlin, P. S., Ratrie, H., and Cleveland, D. W. (1987). The sequence and expression of the divergent β-tubulin in chicken erythrocytes.J. Biol. Chem. 262, 14305-14312.
278. Nagel, S. D., and Boothroyd, J. C. (1988). The α- and β-tubulins of Toxoplasma gondii are encoded by single copy genes containing multiple introns. Mol. Biochem. Parasitol. 29, 261-273.
279. Najbauer, J., Orpiszewski, J., and Aswad, D. W. (1996). Molecular aging of tubulin: Accumulation of isoaspartyl sites in vitro and in vivo. Biochemistry 35, 5183-5190.
280. Neff, N. F., Thomas, J. H., Grisafi, P., and Botstein, D. (1983). Isolation of the β-tubulin gene from yeast and demonstration of its essential function in vivo. Cell (Cambridge, Mass.) 33,211-219.
281. Nelson, R. G., Kim, K., Gooze, L., Petersen, C., and Gut, J. (1991). Identification and isolation of Cryptosporidiiim parvum genes encoding microtubule and microfilament proteins.J. Protoiool. 38, 52S-55S.
282. Niggli, V., and Burger, M. M. (1987). Interaction of the cytoskeleton with the plasma membrane. J. Membr. Biol. 100, 97-121.
283. Nogales, E., Wolf, S. G., Khan, I. A., Luduena, R. F., and Downing, K. H. (1995). Structure of tubulin at 6.5 A and location of the taxol-binding site. Nature (London) 375, 424-427.
284. Nowak, C., and Kuck, U. (1994). Development of an homologous transformation system for Acremdniiim chrysogenum based on the β-tubulin gene. Curr. Genet. 25, 34-40.
285. Oakley, B. R. (1994). γ-Tubulin. In "Microtubules" (J. S. Hyams and C. W. Lloyd, eds.), pp. 33-45. Wiley-Liss, New York.
286. Oakley, C. E., and Oakley, B. R. (1989). Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillits nidalans. Nature (London) 338, 662-664.
287. Okamura, S., and Azumano, I. (1988). Primary structure of the carboxy-terminal region of a higher plant beta-tubulin. Biochem. Int. 16,1103-1109.
288. Orbach, M. J., Porro, E. B., and Yanofsky, C. (1986). Cloning and characterization of the gene for β-tubulin from a benomyl-resistant mutant of Neurospora crassa and its use as a dominant selectable marker. Mol. Cell. Biol. 6, 2452-2461.
289. Panaccione, D. G., and Hanau, R. M. (1990). Characterization of two divergent β-tubulin genes from Collectrichum graminicola. Gene 86, 163-170.
290. Panda, D., Miller, H. P., Banerjee, A., Luduena, R. F., and Wilson, L. (1994). Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc. Natl. Acad. Sci. U.S.A. 91,11358-11362.
291. Paturle-Lafanechère, L., Eddé, B., Denoulet, P., Van Dorsselaer, A., Mazarguil, H., Le Caer, J. P., Wehland, J., and Job, D. (1991). Characterization of a major brain tubulin variant which cannot be tyrosinated. Biochemistry 30, 10523-10528.
292. Paturle-Lafanechère, L., Manier, M., Trigault, M., Pirollet F., Mazarguil, H., and Job, D. (1994). Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies.J. Cell Sci. 107, 1529-1543.
293. Paul, E. C. A., Buchschacher, G. L., Cunningham, D. B., Dove, W. F., and Burland, T. G. (1992). Preferential expression of one β-tubulin gene during flagellate development in Physarwn. J. Gen. Microbiol. 138, 229-238.
294. Peters, J. D., Furlong, M. T., Asai, D. J., Harrison, M. L., and Geahlen, R. L. (1996). Syk, activated by cross-linking the B-cell antigen receptor, localizes to the cytosol where it interacts with and phosphorylates α-tubulin on tyrosine. J. Biol Chem. 271, 4755-4762.
295. Picquot, P., and Lambert, A.-M. (1988). Tubulin from monocotyledon endosperm cells: Partic-ular biochemical and immunological properties. J. Plant Physiol. 132, 561-568.
296. Piperno, G., and Fuller, M. T. (1985). Monoclonal antibodies specific for an acetylated form of α-tubulin recognize the antigen in cilia and flagella from a variety of organisms.J. Cell Biol. 101, 2085-2094.
297. Piperno, G., and Luck, D. J. (1976). Phosphorylation of axonemal proteins in Clilamydomonas reinhardtii. J. Biol. Chem. 251, 2161-2167.
298. Piperno, G., LeDizet, M., and Chang, X.-J. (1987). Microtubules containing acetylated α-tubulin in mammalian cells in culture.J. Cell Biol. 104, 289-302.
299. Ponstingl, H., Krauhs, E., Little, M., and Kempf, T. (1981). Complete amino acid sequence of α-tubulin from porcine brain. Proc. Natl. Acad. Sci. U.S.A. 78, 2757-2761.
300. Prasad, A. R. S., Luduena, R. F., and Horowitz, P. M. (1986). Bis(8-anilinonaphthalene-1-sulfonate) as a probe for tubulin decay. Biochemistry 25, 739-742.
301. Prasad, A. R. S., and Luduena, R. F. (1987). Chemical modification of bovine brain tubulin with the guanine nucleotide affinity analogue 5'-fluorosuIfonyIbenzoylguanosine. Biochem. Int. 14, 85-93.
302. Pratt, L. F., and Cleveland, D. W. (1988). A survey of the α-tubulin gene family in chicken: Unexpected sequence heterogeneity in the polypeptides encoded by five expressed genes. EMBO J. 7, 931-940.
303. Pratt, L. F., Okamura, S., and Cleveland, D. W. (1987). A divergent testis-specific α-tubulin isotype that does not contain a coded C-terminal tyrosine. Mol. Cell. Biol. 7, 552-555.
304. Przyborski, S. A., and Cambray-Deakin, M. A. (1996). Developmental regulation of α-tubulin mRNAs during the differentiation of cultured cerebellar granule cells. Mol. Brain Res. 36, 179-183.
305. Raff, E. C. (1994). The role of multiple tubulin isoforms in cellular microtubule function. In "Microtubules" (J. S. Hyams and C. W. Lloyd, eds.), pp. 85-109. Wiley-Liss, New York.
306. Raff, E. C., Fackenthal, J. D., Hutchens, J. A., Hoyle, H. D., and Turner, F. R. (1997). Microtubule architecture specified by a β-tubulin isoform. Science 275, 70-73.
307. IVa-tubulin isotypes in human prostate carcinoma cells as a result of estramustine resistance. Cancer Res. 56, 2584-2589.
308. Rawlings, D. J., Fujioka, H., Fried, M., Keister, D. B., Aikawa, M., and Kaslow, D. C. (1992). β-Tubulin II is a male-specific protein in Plasmodium falciparum. Mot. Biochem. Parasitol. 56, 239-250.
309. Raybin, D., and Flavin, M. (1977). Enzyme which specifically adds tyrosine to the a chain of tubulin. Biochemistry 16, 2189-2194.
310. Redeker, V., LeCaer, J.-P., Rossier, J., and Promé, J.-C. (1991). Structure of the polyglutamyl side chain posttranslationally added to the α-tubulin. J. Biol. Chem. 266, 23461-23466.
311. Redeker, V., Melki, R., Promé, D., Le Caer, J.-P., and Rossier, J. (1992). Structure of tubulin C-terminal domain obtained by subtilisin treatment. The major a and β tubulin isotypes from pig brain are glutamylated. FEES Lett. 313, 185-192.
312. Redeker, V., Levilliers, N., Schmitter, J.-M., Le Caer, J.-P., Rossier, J., Adoutte, A., and Bre, M.-H. (1994). Polyglycylation of tubulin: A posttranslational modification in axonemal microtubules. Science 266, 1688-1691.
313. Redeker, V., Rusconi, F., Mary J., Promé, J.-C., and Rossier, J. (1996). Structure of the C-terminal tail of α-tubulin: Increase of heterogeneity from newborn to adult.J. Neurochem. 67, 2104-2114.
314. IV is the major β-tubulin isotype in bovine cilia. Cell Motil. Cytoskel. 25, 19-29.
315. 1-tubulin. J- Biol. Chem. 259, 12063-12071.
316. Rogers, H. J., Greenland, A. J., and Hussey, P. J. (1993). Four members of the maize β-tubulin gene family are expressed in the male gametophyte. Plant J. 4, 875-882.
317. Roos, M. H., Boersema, J. H., Borgsteede, F. H. M., Cornelissen, J. Taylor, M., and Ruitenberg, E. J. (1990). Molecular analysis of selection for benzimidazole resistance in the sheep parasite Haemonclius contortus. Mol. Biochem. Parasitol. 43, 77-88.
318. Rüdiger, A., Rüdiger, M., Weber, K., and Schomburg, D. (1995). haracterization of post-
319. translational modifications of brain tubulin by matrix-assisted laser desorption/ionization mass spectrometry: Direct one-step analysis of a limited subtilisin digest. Anal. Biochem. 224, 532-537.
320. Rüdiger, M., and Weber, K. (1993). Characterization of the post-translational modifications in tubulin from the marginal band of avian erythrocytes. Eitr. J. Biochem. 218, 107-116.
321. Rüdiger, M., Plessman, U., Klöppel, K.-D., Wehland, J., and Weber, K. (1992). Class II tubulin, the major brain β tubulin isotype is polyglutamylated on glutamic acid residue 435. FEES Lett. 308, 101-105.
322. Rüdiger, M., Plessman, U., Rüdiger, A.-H., and Weber, K. (1995). β tubulin of bull sperm is polyglycylated. FEES Lett. 264, 147-151.
323. 8) reveal both an ancient divergence in metazoan isotypes and structural constraints for beta-tubulin function. Mol. Cell. Biol. 7, 2231-2242.
324. Russo, P., Juuti, J. T., and Raudaskoski, M. (1992). Cloning, sequence and expression of a β-tubulin-encoding gene in the homobasidiomycete Schizophyllttm commune. Gene 119, 175-182.
325. Rutberg, M., Modig, C., and Wallin, W. (1996). Detyrosination of tubulin is not correlated to cold-adaptation of microtubules in cultured cells from the Atlantic cod (Cadus morluia). Histochem. J. 28, 511-521.
326. Sagan, L. (1967). On the origin of mitosing cells.J. Tlieor. Biol. 14, 225-274.
327. Sale, W. S., Besharse, J. C., and Piperno, G. (1988). Distribution of acetylated α-tubulin in retina and in in vitro-assembled microtubules. Cell Motil. Cytoskel. 9, 243-253.
328. Sasse, R., Glyn, M. C. P., Birkett, C. R., and Gull, K. (1987). Acetylated α-tubulin in Physamm: Immunological characterization of the isotype and its usage in particular microtubular organelles. J. Cell Biol. 104, 41-49.
329. Savage, C., Hamelin, M., Culotti, J. G., Coulson, A., Albertson, D. G., and Chaine, M. (1989). inec-7 is a β-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev. 3, 870-881.
330. Schantz, M.-L., and Schantz, R. (1989). Sequence of a cDNA clone encoding β tubulin from Euglena gracilis. Nucleic Acids Res. 17, 6727.
331. Schatz, P. J., Pillus, L., Grisafi, P., Solomon, F., and Botstein, D. (1986a). Two functional α-tubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins. Mol. Cell. Biol. 6, 3711-3721.
332. Schatz, P. J., Solomon, F., and Botstein, D. (1986b). Genetically essential and nonessential α-tubulin genes specify functionally interchangeable proteins. Mol. Cell. Biol. 6, 3722-3733.
333. Schwarz, P. M., and Ludueña, R. F. (1996). Different patterns of decay among tubulin isotypes. Mol. Biol. Cell 7, 43a.
334. Scott, C. A., Walker, C. C., Neal, D. A., Harper, C. E., Bloodgood, R. A., Somers, K. D., Mills, S. E., Rebhun, L. I., and Levine, P. A. (1990). β-Tubulin epitope expression in normal and malignant epithelial cells.
335. Scott, V., Sherwin, T., and Gull, K. (1997). -y-Tubulin in trypanosomes: Molecular characterization and localization to multiple and diverse microtubule organizing centres.J. Cell Sci. 110, 157-168.
336. Serrano, L., Díaz-Nido, J., Wandosell, F., and Avila, J. (1987). Tubulin phosphorylation by casein kinase II is similar to that found in vivo. J. Cell Biol. 105, 1731-1739.
337. Serrano, L., Dfez, J. C., Wandosell, F., Avila, J., and Little, M. (1989). Calcium binding properties of the beta tubulin subunit from chicken erythrocytes. Biochem. Int. 19, 235-246.
338. Sharma, J., and Luduena, R. F. (1994). Use of N,N'-polymethylenebis(iodoacetamide) derivatives as probes for the detection of conformational differences in tubulin isotypes./. Protein Chem. 13, 165-176.
339. Sherwood, J. E., and Somerville, S. C. (1990). Sequence of the Erysiphe graminis f. Sp. hordei gene encoding β-tubulin. Nucleic Acids Res. 18, 1052.
340. Shivanna, B. D., Mejillano, M. R., Williams, T. D., and Himes, R. H. (1993). The GTP-binding site of β-tubulin: Identification of cysteine-12 as the major site of cross-linking by direct photoaffinity labeling. J. Biol. Chem. 268, 127-132.
341. Siddiqui, S. S., Aamodt, E., Rastinejad, F., and Culotti, J. (1989). Anti-tubulin monoclonal antibodies that bind to specific neurons in Caenorl:abdilis elegans. J. Neurosci. 9, 2963-2972.
342. Silflow, C. D., Chisholm, R. L., Conner, T. W., and Ranum, L. P. W. (1985). The two alpha-
343. tubulin genes of Chlamydonwnas reinhardi code for slightly different proteins. Mol. Cell. Biol. 5, 2389-2398.
344. Slepecky, N. B., Henderson, C. G., and Saha, S. (1995). Post-translational modifications of tubulin suggest that dynamic microtubules are not present in sensory cells and stable microtubules are present in supporting cells of the mammalian cochlea. Hear. Res. 91, 136-147.
345. Smith, H. A., Allaudeen, H. S., Whitman, M. H., Koltin, Y., and German, J. A. (1988). Isolation and characterization of a β-tubulin gene from Candida albicans. Gene 63, 53-63.
346. Snustad, D. P., Haas, N. A., Kopczak, S. D., and Silflow, C. D. (1992). The small genome of Arabidopsis contains at least nine expressed β-tubulin genes. Plant Cell 4, 549-556.
347. Sobel, S. G., and Snyder, M. (1995). A highly divergent γ-tubulin gene is essential for cell growth and proper microtubule organization in Saccharomyces cerevisiae. J. Cell Biol. 131, 1775-1788.
348. Song, Q., Combest, W. L., and Gilbert, L. I. (1994). Spermine and polylysine enhanced phosphorylation of calmodulin and tubulin in an insect endocrine gland. Mol. Cell. Endocrinol. 99, 1-10.
349. Sorri, O., Åström, H., and Raudaskoski, M. (1996). Actin and tubulin expression and isotype pattern during tobacco pollen tube growth. Sex. Plant Reprod. 9, 255-263.
350. Souto-Padron, T., Cunha e Suva, N. L., and de Souza, W. (1993). Acetylated alpha-tubulin in Trypanosoma cruzi: Immunocytochemical localization. Mem. Inst. Oswaldo Cruz 88, 517-528.
351. Spang, A., Geissler, S., Grein, K., and Schiebel, E. (1996). y-Tubulin-like tub4p of Saccharomyces cerevisiae is associated with the spindle pole body substructures that organize microtubules and is required for mitotic spindle formation.J. Cell Biol. 134, 429-441.
352. Steiner, M. (1984). Affinity labeling of the exchangeable nucleotide binding site in platelet tubulin. Biochem. Biophys. Res. Commun. 123, 92-99.
353. Stephens, R. E. (1975). Structural chemistry of the axoneme: Evidence for chemically and functionally unique tubulin dimers in outer fibers. Soc. Gen. Physiol. Ser. 30, 181-204.
354. Stephens, R. E. (1981). Chemical differences distinguish ciliary membrane and axonemal tubulin. Biochemistry 20, 4716-4723.
355. Stephens, R. E. (1986). Membrane tubulin. Biol. Cell. 57, 95-110.
356. Stephens, R. E. (1995). Ciliary membrane tubulin: Isolation and fractionation. Methods Cell Biol. 47, 431-436.
357. Stephens, R. E., Oleszko-Szuts, S., and Good, M. J. (1987). Evidence that tubulin forms an integral membrane skeleton in molluscan gill cilia.J. Cell Sci. 88, 527-535.
358. Stöcker, M., Garcia-Mas, J., Arús, P., Messeguer, R., and Puigdomènech, P. (1993). A highly conserved α-tubulin sequence from Prunus amygdalus. Plant Mol. Biol. 22, 913-916.
359. Sullivan, K. F. (1988). Structure and utilization of tubulin isotypes. Annu. Rev. Cell Biol. 4, 687-716.
360. Sullivan, K. F., and Cleveland, D. W. (1986). Identification of conserved and isotype-defming variable region sequences for four vertebrate β tubulin polypeptide classes. Proc. Natl. Acad. Sci. U.S.A. 83, 4327-4331.
361. Sullivan, K. F., Lau, J. T. Y., and Cleveland, D. W. (1985). Apparent gene conversion between β-tubulin genes yields multiple regulatory pathways for a single β-tubulin polypeptide isotype. Mol. Cell. Biol. 5, 2454-2465.
362. Sullivan, K. F., Machlin, P. S., Ratrie, H., and Cleveland, D. W. (1986a). Sequence and expression of the chicken β3 tubulin gene. A vertebrate testis β-tubulin isotype. J. Biol. Chem. 261, 13317-13322.
363. Sullivan, K. F., Havercroft, J. C., Machlin, P. S., and Cleveland, D. W. (1986b). Sequence and expression of the chicken β5- and β4-tubulin genes define a pair of divergent β-tubulins with complementary patterns of expression. Mol. Cell. Biol. 6, 4409-4418.
364. Takahashi, M., Tomizawa, K., Sato, K., Ohtake, A., and Omori, A. (1995). A novel tautubulin kinase from bovine brain. FEBS Lett. 372, 59-94.
365. Taylor, M. A., Wright, F., and Davies, H. V. (1994). Characterization of the cDNA clones of two β-tubulin genes and their expression in the potato plant (Solanum tuberosum L.). Plant Mol. Biol. 26, 1013-1018.
366. Theurkauf, W. E. (1992). Behavior of structurally divergent α-tubulin isotypes during Drosopliila embryogenesis: Evidence for post-translational regulation of isotype abundance. Dev. Biol. 154, 205-217.
367. Theurkauf, W. E., Baum, H., Bo, J., and Wensink, P. C. (1986). Tissue-specific and constitutive α-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. Proc. Natl. Acad. Sci. U.S.A. 83, 8477-8481.
368. Tian, G., Huang, Y., Rommelaere, H., Vandekerckhove, J., Ampe, C., and Cowan, N. J. (1996). Pathway leading to correctly folded β-tubulin. Cell (Cambridge, Mass.) 86, 287-296.
369. Toda, T., Adachi, Y., Hiraoka, Y., and Yanagida, M. (1984). Identification of the pleiotropic cell division cycle gene NDA2 as one of two different α-tubulin genes in Schizosaccharomyces pombe. Cell (Cambridge, Mass.) 37, 233-242.
370. Tomarev, S. L, Zinovieva, R. D., and Piatigorsky, J. (1993). Primary structure and lens-specific expression of genes for an intermediate filament protein and a β-tubulin in cephalopods. Biochim. Biophys. Acta 1216, 245-254.
371. Trinczek, B., Marx, A., Mandelkow, E.-M., Murphy, D. B., and Mandelkow, E. (1993). Dynamics of microtubules from erythrocyte marginal bands. Mol. Biol. Cell 4, 323-335.
372. Trivinos-Lagos, L., Ohmachi, T., Albrightson, C., Burns, R. G., Ennis, H. L., and Chisholm, R. L. (1993). The highly divergent α- and β-tubulins from Dictyostelium discoideum are encoded by single genes.J. Cell Sci. 105, 903-911.
373. Vassilevskaia, T. D., Bekman, E., Jackson, P., Ricardo, C. P., and Rodrigues-Pousada, C. (1996). Developmental expression and regulation by light of two closely related β-tubulin genes in Lupimis albus. Plant Mol. Biol. 32, 1185-1189.
374. Villasante, A., Wang, D., Dobner, P., Dolph, P., Lewis, S. A., and Cowan, N. J. (1986). Six mouse α-tubulin mRNAs encode five distinct isotypes: Testis-specific expression of two sister genes. Mol. Cell. Biol. 6, 2409-2419.
375. Villemur, R., Joyce, C. M., Haas, N. A., Goddard, R. H., Kopczak, S. D., Hussey, P. J., Snustad, D. P., and Silfiow, C. D. (1992). β-Tubulin gene family of maize (Zea mays L.). Evidence for two ancient α-tubulin genes in plants. J. Mol. Biol. 227, 81-96.
376. Villemur, R., Haas, N. A., Joyce, C. M., Snustad, D. P., and Silfiow, C. D. (1994). Characterization of four new β-tubulin genes and their expression during male flower development in maize (Zea mays L.) Plant Mol Biol. 24, 295-315.
377. Vinores, S. A., Derevjanik, N. L., Mahlow, J., Hacke, S. F., Haller, J. A., deJuan, E., Frankfurter, A., and Campochiaro, P. A. (1995). Class III β-tubulin in human retinal pigment epithelial cells in culture and in epiretinal membranes. Exp. Eye Res. 60, 385-400.
378. Volker, K. W., and Knüll, H. R. (1993). Glycolytic enzyme-tubulin interactions: Role of tubulin carboxy terminal. J. Mol. Recognition 6, 167-177.
379. Volker, K. W., Reinitz, C. A., and Knüll, H. R. (1995). Glycolytic enzymes and assembly of microtubule networks. Comp. Biochem. Physiol. B 112B, 503-514.
380. Waiden, P. D., Monteiro, M. J., Gull, K., and Cox, R. A. (1989a). Structure and expression of an α-tubulin gene of Physanim polycephaliim. Eur. J. Biochem. 181, 583-592.
381. Waiden, P. D., Blindt, A. B., Birke, C. R., Cox, R. A., and Gull, K. (1989b). Recognition of specific Physanim alpha-tubulin isotypes by a monoclonal antibody. Sequence heterogeneity around the acetylation site at lysine 40. Eur. J. Biochem. 185, 383-389.
382. Wang, D., Villasante, A., Lewis, S. A., and Cowan, N. J. (1986). The mammalian β-tubulin repertoire: Hematopoietic expression of a novel, heterologous β-tubulin isotype.J. Cell Biol. 103, 1903-1910.
383. Wang, N., and Rasenick, M. M. (1991). TubuIin-G protein interactions involve microtubule polymerization domains. Biochemistry 30, 10957-10965.
384. Weatherbee, J. A., May, G. S., Gambino, J., and Morris, N. R. (1985). Involvement of a particular species of beta-tubulin (beta3) in conidial development in Aspergillus nidulans. J. Cell Biol. 101, 706-711.
385. Weber, K., Schneider, A., Müller, N., and Plessman, U. (1996). Polyglycylation of tubulin in the diplomonad Giardia lamblia, one of the oldest eukaryotes. FEBS Lett. 393, 27-30.
386. Webster, P. J., Seta, K. A., Chung, S. C., and Mansour, T. E. (1992). A cDNA encoding an α-tubulin from Schistosoma tiiansoni. Mol. Biochem. Parasitol. 51, 169-170.
387. Wehland, J., and Weber, K. (1987). Tubulin-tyrosine ligase has a binding site on β-tubulin: A two domain structure of the enzyme.J. Cell Biol. 104, 1059-1067.
388. Wesseling, J. G., Dirks, R., Smits, M. A., and Schoenmakers, J. G. G. (1989). Nucleotide sequence and expression of a β-tubulin gene from Plasmodium falciparum, a malarial parasite of man. Gene 83, 301-309.
389. Wilson, L. (1970). Properties of colchicine binding protein from chick embryo brain. Interactions with vinca alkaloids and podophyllotoxin. Biochemistry 9, 4999-5007.
390. Wilson, P. J., and Forer, A. (1989). Acetylated α-tubulin in spermatogenic cells of the crane fly Neplirotoina siituralis: Kinetochore microtubules are selectively acetylated. Cell Motil. Cytoskel. 14, 237-250.
391. Wolf, K. W. (1996a). Cytology of Lepidoptera VIII. Acetylation of α-tubulin in mitotic and meiotic spindles of two Lepidoptera species, Ephestia kiteliniella (Pyralidae) and Pieris brassicae (Pieridae). Protoplasma 190, 88-98.
392. Wolf, K. W. (1996b). Acetylation of α-tubulin in male meiotic spindles of Pyrrlwcoris apterus, an insect with holokinetic chromosomes. Protoplasma 191, 148-157.
393. Wolf, K. W., Regan, C. L., and Fuller, M. T. (1988). Temporal and spatial pattern of differences in microtubule behaviour during Drosophila embryogenesis revealed by distribution of a tubulin isoform. Development (Cambridge, UK) 102, 311-324.
394. Wolff, A., de Néchaud, B., Chillet, D., Mazarguil, H., Desbruyères, E., Audebert, S., Eddé, B., Gros, F., and Denoulet, P. (1992). Distribution of glutamylated a and β-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Enr. J. Cell Biol. 59, 425-432.
395. Wu, W.-L., and Morgan, G. T. (1994). Ovary-specific expression of a gene encoding a divergent α-tubulin isotype in Xenopus. Differentiation (Berlin) 58, 9-18.
396. Xiang, H., and MacRae, T. H. (1995). Production and utilization of detyrosinated tubulin in developing Anemia larvae: Evidence for a tubulin-reactive carboxypeptidase. Biochem. Cell Biol. 73, 673-685.
397. Yan, K., and Dickman, M. B. (1996). Isolation of a β-tubulin gene from Fusarium moniliforme that confers cold-sensitive benomyl resistance. Appl. Environ. Microbiol. 62, 3053-3056.
398. Yoshimura, T., Demura, T., Igarashi, M., and Fukuda, H. (1996). Differential expression of three genes for different β-tubulin isotypes during the initial culture of Zinnia mesophyll cells that divide and differentiate into tracheary elements. Plant Cell Physiol. 37, 1167-1176.
399. Youngblom, J., Schloss, J. A., and Silflow, C. D. (1984). The two β-tubulin genes of Chlamydomonas reinhardtii code for identical proteins. Mol. Cell. Biol. 4, 2686-2696.
400. Zheng, Y., Wong, M. L., Alberts, B., and Mitchison, T. (1995). Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature (London) 378, 578-583.
401. Zhu, G., and Keithly, J. S. (1996). The beta tubulin gene of Eimeria tenella. Mol. Biochem. Parasitol. 76, 315-319.