Structurally similar Drosophila α-tubulins are functionally distinct in vivo

Molecular Biology of the Cell

Volumn 8, Issue 3, 1997, Pages 481-500

  Hutchens, Jeffrey A ^a   Hoyle, Henry D ^a   Turner, F Rudolf ^a   Raff, Elizabeth C ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN;

ARTICLE; AXONEME; CYTOSKELETON; DROSOPHILA; GENE EXPRESSION; GERM CELL; MALE STERILITY; MICROTUBULE; MICROTUBULE ASSEMBLY; MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN STRUCTURE; SPERMATID; SPERMATOGENESIS;

EID: 0030893287     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.3.481     Document Type: Article

References (45)

1. Audebert, S., Desbruyeres, E., Gruszczynski, C., Koulakoff, A., Gros, F., Denoulet, P., and Edde, B. (1993). Reversible polyglutamylation of alpha-and beta-tubulin and microtubule dynamics in mouse brain neurons. Mol. Biol. Cell. 4, 615-626.
2. Bré, M.H., de Nechaud, B., Wolff, A., and Fleury, A. (1994). Glutamylated tubulin probed in ciliates with the monoclonal antibody GT335. Cell Motil. Cytoskeleton 27, 337-349.
3. 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. Devel. Biol. 177, 117-135.
4. Eddé, B., Rossier, J., Le Caer, J.-P., Desbruyeres, E., Gros, F., and Denoulet, P. (1990). Posttranslational glutamylation of α-tubulin. Science 247, 83-85.
5. Eddé, B., Rossier, J., Le, C.J., Berwald, N.Y., Koulakoff, A., Gros, F., and Denoulet, P. (1991). A combination of posttranslational modifications is responsible for the production of neuronal alpha-tubulin heterogeneity. J. Cell. Biochem. 46, 134-142.
6. Fackenthal, J.D., Hutchens, J.A., Turner, F.R., and Raff, E.C. (1995). Structural analysis of mutations in the Drosophila β2-tubulin isoform reveal regions in the β-tubulin molecule required for general and for tissue-specific functions. Genetics 139, 267-286.
7. Fackenthal, J.D., Turner, F.R., and Raff, E.C. (1993). Tissue-specific microtubule functions in Drosophila spermatogenesis require the β2-tubulin isotype-specific carboxy terminus. Dev. Biol. 158, 213-227.
8. Fouquet, J.P., Edde, B., Kann, M.L., Wolff, A., Desbruyeres, E., and Denoulet, P. (1994). Differential distribution of glutamylated tubulin during spermatogenesis in mammalian testis. Cell Motil. Cytoskeleton 27, 49-58.
9. 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.
10. Fuller, M.T., Caulton, J.H., Hutchens, J.A., Kaufman, T.C., and Raff, E.C. (1988). Mutations that encode partially functional β2-tubulin subunits have different effects on structurally different microtubule arrays. J. Cell Biol. 107, 141-152.
11. Hays, T.S., Deuring, R., Robertson, B., Prout, M., and Fuller, M.T. (1989). Interacting proteins identified by genetic interactions: a missense mutation in alpha-tubulin fails to complement alleles of the testis-specific beta-tubulin gene of Drosophila melanogaster. Mol. Cell. Biol. 9, 875-884.
12. Hazelrigg, T., and Kaufman, T.C. (1983). Revertants of dominant mutations associated with the Antennapedia gene complex of Drosophila melanogaster. Genetics 105, 581-600.
13. Hoyle, H.D., Hutchens, J.A., Turner, F.R., and Raff, E.C. (1995). Regulation of beta-tubulin function and expression in Drosophila spermatogenesis. Dev. Genet. 16, 148-170.
14. Hoyle, H.D., and Raff, E.C. (1990). Two Drosophila beta-tubulin isoforms are not functionally equivalent. J. Cell Biol. 111, 1009-1026.
15. 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 31, 655-670.
16. Kimble, M., Dettman, R.W., and Raff, E.C. (1990). The β3-tubulin gene of Drosophila melanogaster is essential for viability and fertility. Genetics 126, 991-1005.
17. 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.
18. Kirk, K.E., and Morris, N.R. (1993). Either alpha-tubulin isogene product is sufficient for microtubule function during all stages of growth and differentiation in Aspergillus nidulans. Mol. Cell. Biol. 13, 4465-4476.
19. L'Hernault, S.W., and Rosenbaum, J.L. (1985). Chlamydomonas alpha-tubulin is posttranslationally modified by acetylation on the epsilon-amino group of lysine. Biochemistry 24, 473-478.
20. le Dizet, M., and Piperno, G. (1987). Identification of an acetylation site of Chlamydomonas alpha-tubulin. Proc. Natl. Acad. Sci. USA 84, 5720-5724.
21. Lindsley, D.L., and Tokuyasu, K.T. (1980). Spermatogenesis. In: The Genetics and Biology of Drosophila, ed. M. Ashburner and T.R.F. Wright, New York: Academic Press, 225-294.
22. Lindsley, D.L., and Zimm, G.G. (1992). The Genome of Drosophila melanogaster. San Diego, CA: Academic Press.
23. Matthews, K.A., and Kaufman, T.C. (1987). Developmental consequences of mutations in the 84B alpha-tubulin gene of Drosophila melanogaster. Dev. Biol. 119, 100-114.
24. Matthews, K.A., Miller, D.F., and Kaufman, T.C. (1989). Developmental distribution of RNA and protein products of the Drosophila alpha-tubulin gene family. Dev. Biol. 132, 45-61.
25. Matthews, K.A., Miller, D.F., and Kaufman, T.C. (1990). Functional implications of the unusual spatial distribution of a minor alpha-tubulin isotype in Drosophila: a common thread among chordotonal ligaments, developing muscle, and testis cyst cells. Dev. Biol. 137, 171-183.
26. Matthews, K.A., Rees, D., and Kaufman, T.C. (1993). A functionally specialized alpha-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila. Development 117, 977-991.
27. May, G.S. (1989). The highly divergent β-tubulins of Aspergillus nidulans are functionally interchangeable. J. Cell Biol. 109, 2267-2274.
28. Michiels, F., Gasch, A., Kaltschmidt, B., and Renkawitz-Pohl, R. (1989). A 14-bp promoter element directs the testis specificity of the Drosophila β2-tubulin gene. EMBO J. 8, 1559-1565.
29. Michiels, F., Wolk, A., and Renkawitz-Pohl, R. (1991). Further sequence requirements for male germ cell-specific expression under the control of the 14-bp promoter element (beta-2UE1) of the Drosophila beta-2 tubulin gene. Nucleic Acids Res. 19, 4515-4522.
30. 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.
31. Pirrotta, V. (1988). Vectors for P-mediated transformation of Drosophila. In: Vectors: A Survey of Molecular Cloning Vectors and Their Uses, ed. R.L. Rodriguez and D.T. Denhardt, Stoneham, MA: Butterworth Publishers, 437-456.
32. Raff, E.C. (1994). The role of multiple tubulin isoforms in cellular microtubule function. In: Microtubules, ed. J.S. Hyams and C.W. Lloyd, New York: John Wiley & Sons, 85-110.
33. 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.
34. Raff, E.C., and Fuller, M.T. (1984). Genetic analysis of microtubule function in Drosophila. In: Molecular Biology of the Cytoskeleton, ed. G.G. Borisy, D.W. Cleveland, and D.B. Murphy, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 293-304.
35. Raff, E.C., Fuller, M.T., Kaufman, T.C., Kemphues, K.J., Rudolph, J.E., and Raff, R.A. (1982). Regulation of tubulin gene expression during embryogenesis in Drosophila melanogaster. Cell 28, 33-40.
36. Robertson, H.M., Preston, C.R., Phillis, R.W., Johnson-Schlitz, D.M., Benz, W.K., and Engels, W.R. (1988). A stable source of P-element transposase in Drosophila melanogaster. Genetics 118, 461-470.
37. Rüdiger, M., Plessman, U., Kloppel, K.D., Wehland, J., and Weber, K. (1992). Class II tubulin, the major brain beta-tubulin isotype, is polyglutamylated on glutamic acid residue 435. FEBS Lett. 308, 101-105.
38. Rüdiger, M., Plessman, U., Rüdiger, A.H., and Weber, K. (1995). β-Tubulin of bull sperm is polyglycylated. FEBS Lett. 354, 147-151.
39. 8) reveal both an ancient divergence in metazoan isotypes and structural constraints for beta-tubulin function. Mol. Cell. Biol. 7, 2231-2242.
40. Sanchez, F., Natzle, J.E., Cleveland, D.W., Kirschner, M.W., and McCarthy, B.J. (1980). A dispersed multigene family encoding tubulin in Drosophila melanogaster. Cell 22, 845-854.
41. Schatz, P.J., Solomon, F., and Botstein, D. (1986). Genetically essential and nonessential α-tubulin genes specify functionally interchangeable proteins. Mol. Cell. Biol. 6, 3722-3733.
42. Silflow, C.D. (1991). Why do tubulin gene families lack diversity in flagellate/ciliate protists? Protoplasma 164, 9-11.
43. Tates, A.D. (1971). Cytodifferentiation during Spermatogenesis in Drosophila melanogaster: An Electron Microscope Study. The Hague, the Netherlands: J.H. Pasmans.
44. Theurkauf, W.E. (1992). Behavior of structurally divergent alpha-tubulin isotypes during Drosophila embryogenesis: evidence for post-translational regulation of isotype abundance. Dev. Biol. 154, 205-217.
45. Theurkauf, W.E., Baum, H., Bo, J., and Wensink, P.C. (1986). Tissue-specific and constitutive alpha-tubulin genes of Drosophila melanogaster code for structurally distinct proteins. Proc. Natl. Acad. Sci. USA. 83, 8477-8481.