Post-translational modifications regulate microtubule function

Nature Reviews Molecular Cell Biology

Volumn 4, Issue 12, 2003, Pages 938-947

  Westermann, Stefan ^a   Weber, Klaus ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; DIMER; HISTONE;

MICROTUBULE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW;

ACETYLATION; ANIMALS; GLUTAMIC ACID; GLYCINE; MICROTUBULES; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, QUATERNARY; TUBULIN; TYROSINE;

EID: 0345169048     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1260     Document Type: Review

References (102)

1. Luduena, R. F. Multiple forms of tubulin: different gene products and covalent modifications. Int. Rev. Cytol. 178, 207-275 (1998).
2. MacRae, T. H. Tubulin post-translational modifications - enzymes and their mechanisms of action. Eur. J. Biochem. 244, 265-278 (1997).
3. Nogales, E., Whittaker, M., Milligan, R. A. & Downing, K. H. High-resolution model of the microtubule. Cell 96, 79-88 (1999).
4. Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199-203 (1996).
5. Jimenez, M. A. et al. Helicity of α(404-451) and β(394-445) tubulin C-terminal recombinant peptides. Protein Sci. 8, 788-799 (1999).
6. Sullivan, K. F. & Cleveland, D. W. Identification of conserved isotype-defining variable region sequences for four vertebrate β tubulin polypeptide classes. Proc. Natl Acad. Sci. USA 83, 4327-4331 (1986).
7. Mejiliano, M. R. & Himes, R. H. Assembly properties of tubulin after carboxyl group modification. J. Biol. Chem. 266, 657-664 (1991).
8. Mejillano, M. R., Tolo, E. T., Williams, R. C. Jr. & Himes, R. H. The conversion of tubulin carboxyl groups to amides has a stabilizing effect on microtubules. Biochemistry 31, 3478-3483 (1992).
9. Fackenthal, J. D., Turner, F. R. & Raff, E. C. Tissue-specific microtubule functions in Drosophila spermatogenesis require the β2-tubulin isotype-specific carboxy terminus. Dev. Biol. 158, 213-227 (1993).
10. Duan, J. & Gorovsky, M. A. Both carboxy-terminal tails of α- and β-tubulin are essential, but either one will suffice. Curr. Biol. 12, 313-316 (2002). Elegant genetic experiments identify essential functions for the tubulin carboxy-terminal tails in Tetrahymena.
11. Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41-45 (2000).
12. L'Hernault, S. W. & Rosenbaum, J. L. Chlamydomonas α-tubulin is posttranslationally modified by acetylation on the ε-amino group of a lysine. Biochemistry 24, 473-478 (1985).
13. LeDizet, M. & Piperno, G. Identification of an acetylation site of Chlamydomonas α-tubulin. Proc. Natl Acad. Sci. USA 84, 5720-5724 (1987).
14. Sasse, R. & Gull, K. Tubulin post-translational modifications and the construction of microtubular organelles in Trypanosoma brucei. J. Cell Sci. 90, 577-589 (1988).
15. Weber, K., Schneider, A., Westermann, S., Muller, N. & Plessmann, U. Posttranslational modifications of α- and β-tubulin in Giardia lamblia, an ancient eukaryote. FEBS Lett. 419, 87-91 (1997).
16. Schneider, A., Plessmann, U., Felleisen, R. & Weber, K. Posttranslational modifications of trichomonad tubulins; identification of multiple glutamylation sites. FEBS Lett. 429, 399-402 (1998).
17. Schneider, A., Plessmann, U. & Weber, K. Subpellicular and flagellar microtubules of Trypanosoma brucei are extensively glutamylated. J. Cell Sci. 110, 431-437 (1997).
18. Maruta, H., Greer, K. & Rosenbaum, J. L. The acetylation of α-tubulin and its relationship to the assembly and disassembly of microtubules. J. Cell Biol. 103, 571-579 (1986).
19. Hubbert, C. et al. HDAC6 is a microtubule-associated deacetylase. Nature 417, 455-458 (2002).
20. Matsuyama, A. et al. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820-6831 (2002).
21. Zhang, Y. et al. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J. 22, 1168-1179 (2003).
22. +-dependent tubulin deacetylase. Mol. Cell 11, 437-444 (2003). References 19-22 identify HDAC6 and SIRT2 as tubulin deacetylases and propose a role for tubulin acetylation in cell motility.
23. Kozminski, K. G., Diener, D. R. & Rosenbaum, J. L. High level expression of nonacetylatable α-tubulin in Chlamydomonas reinhardtii. Cell Motil. Cytoskeleton 25, 158-170 (1993).
24. Gaertig, J. et al. Acetylation of lysine 40 in α-tubulin is not essential in Tetrahymena thermophila. J. Cell Biol. 129, 1301-1310 (1995).
25. Haggarty, S. J., Koeller, K. M., Wong, J. C., Grozinger, C. M. & Schreiber, S. L. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl Acad. Sci. USA 100, 4389-4394 (2003).
26. Palazzo, A., Ackerman, B. & Gundersen, G. G. Cell biology: tubulin acetylation and cell motility. Nature 421, 230 (2003).
27. Redeker, V. et al. Polyglycylation of tubulin: a posttranslational modification in axonemal microtubules. Science 266, 1688-1691 (1994).
28. Rudiger, M., Plessmann, U., Rudiger, A. H. & Weber, K. β tubulin of bull sperm is poyglycylated. FEBS Lett. 364, 147-151 (1995).
29. Plessmann, U. & Weber, K. Mammalian sperm tubulin: an exceptionally large number of variants based on several posttranslational modifications. J. Protein Chem. 16, 385-390 (1997).
30. Mary, J., Redeker, V., Le Caer, J. P., Rossier, J. & Schmitter, J. M. Posttranslational modifications of axonemal tubulin. J. Protein Chem. 16, 403-407 (1997).
31. Bre, M. H., Redeker, V., Vinh, J., Rossier, J. & Levilliers, N. Tubulin polyglycylation: differential posttranslational modification of dynamic cytoplasmic and stable axonemal microtubules in paramecium. Mol. Biol. Cell 9, 2655-2665 (1998).
32. Weber, K., Schneider, A., Muller, N. & Plessmann, U. Polyglycylation of tubulin in the diplomonad Giardia lamblia, one of the oldest eukaryotes. FEBS Lett. 393, 27-30 (1996).
33. Xia, L. et al. Polyglycylation of tubulin is essential and affects cell motility and division in Tetrahymena thermophila. J. Cell Biol. 149, 1097-1106 (2000).
34. Thazhath, R., Liu, C. & Gaertig, J. Polyglycylation domain of β-tubulin maintains axonemal architecture and affects cytokinesis in Tetrahymena. Nature Cell Biol. 4, 256-259 (2002). References 33 and 34 provide a careful analysis of tubulin polyglycylation in Tetrahymena and identify its essential functions in cell motility and cytokinesis.
35. Edde, B. et al. Posttranslational glutamylation of α-tubulin. Science 247, 83-85 (1990).
36. Mary, J., Redeker, V., Le Caer, J. P., Prome, J. C. & Rossier, J. Class I and IVa β-tubulin isotypes expressed in adult mouse brain are glutamylated. FEBS Lett. 353, 89-94 (1994).
37. Rudiger, M., Plessman, U., Kloppel, K. D., Wehland, J. & Weber, K. Class II tubulin, the major brain β tubulin isotype is polyglutamylated on glutamic acid residue 435. FEBS Lett. 308, 101-105 (1992).
38. Alexander, J. et al. Characterization of posttranslational modifications in neuron-specific class III β-tubulin by mass spectrometry. Proc. Natl Acad. Sci. USA 88, 4685-4689 (1991).
39. Redeker, V., Rossier, J. & Frankfurter, A. Posttranslational modifications of the C-terminus of α-tubulin in adult rat brain: α4 is glutamylated at two residues. Biochemistry 37, 14838-14844 (1998).
40. Bre, M. H., de Nechaud, B., Wolff, A. & Fleury, A. Glutamylated tubulin probed in ciliates with the monoclonal antibody GT335. Cell Motil. Cytoskeleton 27, 337-349 (1994).
41. Lechtreck, K. F. & Geimer, S. Distribution of polyglutamylated tubulin in the flagellar apparatus of green flagellates. Cell Motil. Cytoskeleton 47, 219-235 (2000).
42. Bobinnec, Y. et al. Glutamylation of centriole and cytoplasmic tubulin in proliferating non-neuronal cells. Cell Motil. Cytoskeleton 39, 223-232 (1998).
43. Regnard, C. et al. Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 275, 15969-15976 (2000). Identifies the nucleosome assembly proteins NAP1 and NAP2 as substrates for polyglutamylation, indicating that this is a more general protein modification.
44. Regnard, C., Audebert, S., Desbruyeres, Denoulet, P. & Edde, B. Tubulin polyglutamylase: partial purification and enzymatic properties. Biochemistry 37, 8395-8404 (1998).
45. Regnard, C. et al. Characterisation of PGs1, a subunit of a protein complex co-purifying with tubulin polyglutamylase. J. Cell Sci. 116, 4181-4190 (2003).
46. Regnard, C., Desbruyeres, E., Denoulet, P. & Edde, B. Tubulin polyglutamylase: isozymic variants and regulation during the cell cycle in HeLa cells. J. Cell Sci. 112, 4281-4289 (1999).
47. Westermann, S., Schneider, A., Horn, E. K. & Weber, K. Isolation of tubulin polyglutamylase from Crithidia; binding to microtubules and tubulin, and glutamylation of mammalian brain α- and β-tubulins. J. Cell. 112, 2185-2193 (1999).
48. Westermann, S., Plessmann, U. & Weber, K. Synthetic peptides identify the minimal substrate requirements of tubulin polyglutamylase in side chain elongation. FEBS Lett. 459, 90-94 (1999).
49. Westermann, S. & Weber, K. Identification of CfNek, a novel member of the NIMA family of cell cycle regulators, as a polypeptide copurifying with tubulin polyglutamylation activity in Crithidia. J. Cell Sci. 115, 5003-5012 (2002). Identifies a kinase of the NIMA family as the first enzyme involved in tubulin polyglutamylation.
50. Liu, S. et al. A defect in a novel Nek-family kinase causes cystic kidney disease in the mouse and in zebrafish. Development 129, 5839-5846 (2002).
51. Pazour, G. J. & Rosenbaum, J. L. Intraflagellar transport and cilia-dependent diseases. Trends Cell Biol. 12, 551-555 (2002).
52. Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934 (2002).
53. Upadhya, P., Birkenmeier, E. H., Birkenmeier, C. S. & Barker, J. E. Mutations in a NIMA-related kinase gene, Nek1, cause pleiotropic effects including a progressive polycystic kidney disease in mice. Proc. Natl Acad. Sci. USA 97, 217-221 (2000).
54. Audebert, S. et al. Reversible polyglutamylation of α- and β-tubulin and microtubule dynamics in mouse brain neurons. Mol. Biol. Cell 4, 615-626 (1993).
55. Larcher, J. C., Boucher, D., Lazereg, S., Gros, F. & Denoulet, P. Interaction of kinesin motor domains with α- and β-tubulin subunits at a tau-independent binding site. Regulation by polyglutamylation. J. Biol. Chem. 271, 22117-22124 (1996).
56. Bonnet, C. et al. Differential binding regulation of microtubule-associated proteins MAP1A, MAP1B, and MAP2 by tubulin polyglutamylation. J. Biol. Chem. 276, 12839-12848 (2001).
57. Okada, Y. & Hirokawa, N. Mechanism of the single-headed processivity: diffusional anchoring between the K-loop of kinesin and the C terminus of tubulin. Proc. Natl Acad. Sci. USA 97, 640-645 (2000).
58. Thorn, K. S., Ubersax, J. A. & Vale, R. D. Engineering the precessive run length of the kinesin motor. J. Cell Biol. 151, 1093-1100 (2000).
59. Gagnon, C. et al. The polyglutamylated lateral chain of α-tubulin plays a key role in flagellar motility. J. Cell Sci. 109, 1545-1553 (1996).
60. Million, K. et al. Polyglutamylation and polyglycylation of α- and β-tubulins during in vitro ciliated cell differentiation of human respiratory epithelial cells. J. Cell Sci. 112, 4357-4366 (1999).
61. Bobinnec, Y. et al. Centdole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J. Cell Biol. 143, 1575-1589 (1998). Antibody-microinjection studies identify tubulin polyglutamylation as being essential for centriole stability and centrosome structure.
62. Bornens, M. Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25-34 (2002).
63. 14C]tyrosine by brain extract. Separation of a carboxypeptidase from tubulin-tyrosine ligase. Mol. Cell. Biochem. 19, 17-21 (1978).
64. 14C)tyrosine by a ribonuclease-insensitive system. J. Neurochem. 20, 97-108 (1973).
65. Arce, C. A., Rodriguez, J. A., Barra, H. S. & Caputo, R. Incorporation of L-tyrosine, L-phenylalanine and L-3,4-dihydroxyphenylalanine as single units into rat brain tubulin. Eur. J. Biochem. 59, 145-149 (1975).
66. 14C]tyrosine into the C-terminal position of the α subunit of tubulin. Arch. Biochem. Biophys. 180, 264-268 (1977).
67. Paturle-Lafanechere, L. et al. Characterization of a major brain tubulin variant which cannot be tyrosinated. Biochemistry 30, 10523-10528 (1991).
68. Rudiger, M., Wehland, J. & Weber, K. The carboxy-terminal peptide of detyrosinated α tubulin provides a minimal system to study the substrate specificity of tubulin-tyrosine ligase. Eur. J. Biochem. 220, 309-320 (1994).
69. Banerjee, A. Coordination of posttranslational modifications of bovine brain α-tubulin. Polyglycylation of δ2 tubulin. J. Biol. Chem. 277, 46140-46144 (2002).
70. Multigner, L. et al. The A and B tubules of the outer doublets of sea urchin sperm axonemes are composed of different tubulin variants. Biochemistry 35, 10862-10871 (1996).
71. Johnson, K. A. The axonemal microtubules of the Chlamydomonas flagelium differ in tubulin isoform content. J. Cell Sci. 111, 313-320 (1998).
72. Bre, M. H. et al. Axonemal tubulin polyglycylation probed with two monoclonal antibodies: widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J. CellSci. 109, 727-738 (1996).
73. Hultorel, P. et al. Differential distribution of glutamylated tubulin isoforms along the sea urchin sperm axoneme. Mol. Reprod. Dev. 62, 139-148 (2002).
74. Murofushi, H. Purification and characterization of tubulin-tyrosine ligase from porcine brain. J. Biochem. 87, 979-984 (1980).
75. Ersfeld, K. et al. Characterization of the tubulin-tyrosine ligase. J. Cell Biol. 120, 725-732 (1993).
76. Galperin, M. Y. & Koonin, E. V. A diverse superfamily of enzymes with ATP-dependent carboxylate-amine/thiol ligase activity. Protein Sci. 6, 2639-2643 (1997).
77. Argarana, C. E., Barra, H. S. & Caputto, R. Tubulinyl-tyrosine carboxypeptidase from chicken brain: properties and partial purification. J. Neurochem. 34, 114-118 (1980).
78. Wehland, J. & Weber, K. Turnover of the carboxy-terminal tyrosine of α-tubulin and means of reaching elevated levels of detyrosination in living cells. J. Cell Sci. 88, 185-203 (1987).
79. Webster, D. R., Gundersen, G. G., Bulinski, J. C. & Borisy, G. G. Assembly and turnover of detyrosinated tubulin in vivo. J. Cell Biol. 105, 265-276 (1987).
80. Webster, D. R., Wehland, J., Weber, K. & Borisy, G. G. Detyrosination of α tubulin does not stabilize microtubules in vivo. J Cell Biol. 111, 113-122 (1990).
81. Cook, T. A., Nagasaki, T. & Gundersen, G. G. Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J. Cell Biol. 141, 175-185 (1998).
82. Palazzo, A. F., Cook, T. A., Alberts, A. S. & Gundersen, G. G. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nature Cell Biol. 3, 723-729 (2001).
83. Infante, A. S., Stein, M. S., Zhai, Y., Borisy, G. G. & Gundersen, G. G. Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap. J. Cell Sci. 113, 3907-3919 (2000).
84. Gurland, G. & Gundersen, G. G. Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J. Cell Biol. 131, 1275-1290 (1995).
85. Liao, G. & Gundersen, G. G. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273, 9797-9803 (1998).
86. Kreitzer, G., Liao, G. & Gundersen, G. G. Detyrosination of tubulin regulates the interaction of intermediate filaments with microtubules in vivo via a kinesin-dependent mechanism. Mol. Biol. Cell 10, 1105-1118 (1999).
87. Lafanechere, L. et al. Suppression of tubulin tyrosine ligase during tumor growth. J. Cell Sci. 111, 171-181 (1998).
88. Mialhe, A. et al. Tubulin detyrosination is a frequent occurrence in breast cancers of poor prognosis. Cancer Res. 61, 5024-5027 (2001).
89. Eiserich, J. P. et al. Microtubule dysfunction by posttranslational nitrotyrosination of α-tubulin: a nitric oxide-dependent mechanism of cellular injury. Proc. Natl Acad. Sci. USA 96, 6365-6370 (1999).
90. Kalisz, H. M., Erck, C., Plessmann, U. & Wehland, J. Incorporation of nitrotyrosine into α-tubulin by recombinant mammalian tubulin-tyrosine ligase. Biochim. Biophys. Acta 1481, 131-138 (2000).
91. Chang, W. et al. Alteration of the C-terminal amino acid of tubulin specifically inhibits myogenic differentiation. J. Biol. Chem. 277, 30690-30698 (2002).
92. Eipper, B. A. Properties of rat brain tubulin. J. Biol. Chem. 249, 1407-1416 (1974).
93. Gard, D. L. & Kirschner, M. W. A polymer-dependent increase in phosphorylation of β-tubulin accompanies differentiation of a mouse neuroblastoma cell line. J. Cell Biol. 100, 764-774 (1985).
94. Caron, J. M. Posttranslational modification of tubulin by palmitoylation: I. In vivo and cell-free studies. Mol. Biol. Cell 8, 621-636 (1997).
95. Ozols, J. & Caron, J. M. Posttranslational modification of tubulin by palmitoylation: II. Identification of sites of palmitoylation. Mol. Biol. Cell 8, 637-645 (1997).
96. Caron, J. M., Vega, L. R., Fleming, J., Bishop, R. & Solomon, F. Single site α-tubulin mutation affects astral microtubules and nuclear positioning during anaphase in Saccharomyces cerevisae: possible role for palmitoylation of α-tubulin. Mol. Biol. Cell 12, 2672-2687 (2001).
97. Sisson, J. C., Ho, K. S., Suyama, K. & Scott, M. P. Costal2, a novel kinesin-related protein in the Hedgehog signaling pathway. Cell 90, 235-245 (1997).
98. Nogales, E., Downing, K. H., Amos, L. A. & Lowe, J. Tubulin and FtsZ form a distinct family of GTPases. Nature Struct. Biol. 5, 451-458 (1998).
99. McKean, P. G., Vaughan, S. & Gull, K. The extended tubulin superfamiiy. J. Cell Sci. 114, 2723-2733 (2001).
100. Dupuis-Williams, P. et al. Functional role of ε-tubulin in the assembly of the centriolar microtubule scaffold. J. Cell Biol. 158, 1183-1193 (2002).
101. Vinh, J. et al. Structural characterization by tandem mass spectrometry of the posttranslational polyglycylation of tubulin. Biochemistry 38, 3133-3139 (1999).
102. Vinh, J., Loyaux, D., Redeker, V. & Rossier, J. Sequencing branched peptides with CID/PSD MALDI-TOF in the low-picomole range: application to the structural study of the posttranslational polyglycylation of tubulin. Anal. Chem. 69, 3979-3985 (1997).