Tubulin folding pathways: Implication in the regulation of microtubule dynamics

Current Cancer Drug Targets

Volumn 7, Issue 8, 2007, Pages 697-703

  Beghin, A ^a,b   Galmarini, C M ^a   Dumontet, C ^a  

^a UNIVERSITÉ LYON 1   (France)

^b INSERM   (France)

Author keywords

Aneuploidy; Microtubule dynamics; Tubulin binding agents; Tubulin folding

Indexed keywords

ANTINEOPLASTIC AGENT; ARF PROTEIN; CHAPERONE; CYTOSOLIC CHAPERONE CONTAINING T COMPLEX PEPTIDE 1; GLYCOPROTEIN E1; PEPTIDE; POLYPEPTIDE; PREFOLDIN; TUBULIN; TUBULIN BINDING COFACTOR A; TUBULIN BINDING COFACTOR B; TUBULIN BINDING COFACTOR C; TUBULIN BINDING COFACTOR D; TUBULIN BINDING COFACTOR E; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONFORMATIONAL TRANSITION; DOWN SYNDROME; FACE DYSMORPHIA; GENE MUTATION; GENETIC DISORDER; HYPOPARATHYROIDISM; IN VITRO STUDY; KENNY CAFFREY SYNDROME; MENTAL DEFICIENCY; MICROTUBULE; MOTOR NEUROPATHY; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN FOLDING; RETINITIS PIGMENTOSA; REVIEW; RNA SEQUENCE; SANJAD SAKATI SYNDROME; SENSORY NEUROPATHY; SPASTIC PARAPLEGIA;

EID: 37449022408     PISSN: 15680096     EISSN: None     Source Type: Journal    
DOI: 10.2174/156800907783220426     Document Type: Review

References (61)

1. Visscher, D. W.; Wallis, T. L.; Crissman, J. D. Evaluation of chromosome aneuploidy in tissue sections of preinvasive breast carcinomas using interphase cytogenetics. Cancer 1996, 77, 315-320.
2. Segers, P.; Haesen, S.; Castelain, P.; Amy, J. J.; De Sutter, P.; Van Dam, P.; Kirsch-Volders, M. Study of numerical aberrations of chromosome 1 by fluorescent in situ hybridization and DNA content by densitometric analysis on (pre)-malignant cervical lesions. Histochem. J. 1995, 27, 24-34.
3. Feinberg, A. P.; Rainier, S.; DeBaun, M. R. Genomic imprinting, DNA methylation, and cancer. J. Natl. Cancer Inst. Monogr. 1995, 21-26.
4. Duesberg, P. D.; Rasnick, R.; Li, L.; Winters, R. C.; Hehlmann, R.; How aneuploidy may cause cancer and genetic instability. Anticancer Res. 1999, 19, 4887-4906.
5. Lasko, D.; Cavenee, W.; Nordenskjold, M. Loss of constitutional heterozygosity in human cancer. Annu. Rev. Genet. 1991, 25, 281-314.
6. Pihan, G. A.; Doxsey, S. J. The mitotic machinery as a source of genetic instability in cancer. Semin. Cancer Biol, 1999, 9, 289-302.
7. Storchova, Z.; Pellman, D. From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell Biol. 2004, 5, 45-54.
8. Jordan, M. A. Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr. Med. Chem - Anti-Cancer Agents 2002, 2, 1-17.
9. Cleveland, D. W.; Lopata, M. A.; Sherline, P.; Kirschner, M. W. Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 1981, 25, 537-546.
10. Yen, T. J.; Machlin, P. S.; Cleveland, D. W. Autoregulated instability of beta-tubulin mRNAs by recognition of the nascent amino terminus of beta-tubulin. Nature 1988, 334, 580-585.
11. Schwarz, P. M.; Liggins, J. R.; Luduena, R. F. Beta-tubulin isotypes purified from bovine brain have different relative stabilities. Biochemistry 1998, 37, 4687-4692.
12. Wang, Y.; Tian, G.; Cowan, N. J.; Cabral, F. Mutations affecting beta-tubulin folding and degradation. J. Biol. Chem. 2006, 281, 13628-13635.
13. Vainberg, I. E.; Lewis, S. A.; Rommelaere, H.; Ampe, C.; Vandekerckhove, J.; Klein, H. L.; Cowan, N. J. Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 1998, 93, 863-873.
14. Rommelaere, H.; Van Troys, M.; Gao, Y.; Melki, R.; Cowan, N. J.; Vandekerckhove, J.; Ampe, C. Eukaryotic cytosolic chaperonin contains t-complex polypeptide 1 and seven related subunits. Proc. Natl. Acad. Sci. USA 1993, 90, 11975-11979.
15. Lewis, S. A.; Tian, G.; Vainberg, I. E.; Cowan, N. J. Chaperonin-mediated folding of actin and tubulin. J. Cell Biol. 1996, 132, 1-4.
16. Tian, G.; Vainberg, I. E.; Tap, W. D.; Lewis, S. A.; Cowan, N. J. Quasi-native chaperonin-bound intermediates in facilitated protein folding. J. Biol. Chem. 1995, 270, 23910-23913.
17. Tian, G.; Vainberg, I. E.; Tap, W. D.; Lewis, S. A.; Cowan, N. J. Specificity in chaperonin-mediated protein folding. Nature 1995, 375, 250-253.
18. Lopez-Fanarraga, M.; Avila, J.; Guasch, A.; Coll, M.; Zabala, J. C. Review: postchaperonin tubulin folding cofactors and their role in microtubule dynamics. J. Struct. Biol. 2001, 135, 219-229.
19. Fontalba, A.; Paciucci, R.; Avila, J.; Zabala, J. C. Incorporation of tubulin subunits into dimers requires GTP hydrolysis. J. Cell Sci. 1993, 106(Pt 2), 627-632.
20. Simons, C. T.; Staes, A.; Rommelaere, H.; Ampe, C.; Lewis, S. A.; Cowan, N. J. Selective contribution of eukaryotic prefoldin subunits to actin and tubulin binding. J. Biol. Chem. 2004, 279, 4196-4203.
21. Sternlicht, H.; Farr, G. W.; Sternlicht, M. L.; Driscoll, J. K.; Willison, K.; Yaffe, M. B. The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc. Natl. Acad. Sci. USA 1993, 90, 9422-9426.
22. Chen, X.; Sullivan, D. S.; Huffaker, T. C. Two yeast genes with similarity to TCP-1 are required for microtubule and actin function in vivo. Proc. Natl. Acad. Sci. USA 1994, 91, 9111-9115.
23. Gao, Y.; Vainberg, I. E.; Chow, R. L.; Cowan, N. J. Two cofactors and cytoplasmic chaperonin are required for the folding of alpha- and beta-tubulin. Mol. Cell Biol. 1993, 13, 2478-2485.
24. Fanarraga, M. L.; Parraga, M.; Aloria, K.; del Mazo, J.; Avila, J.; Zabala, J. C. Regulated expression of p14 (cofactor A) during spermatogenesis. Cell Motil. Cytoskeleton 1999, 43, 243-254.
25. Archer, J. E.; Magendantz, M.; Vega, L. R.; Solomon, F. Formation and function of the Rbl2p-beta-tubulin complex. Mol. Cell Biol. 1998, 18, 1757-1762.
26. Archer, J. E.; Vega, L. R.; Solomon, F. Rbl2p, a yeast protein that binds to beta-tubulin and participates in microtubule function in vivo. Cell 1995, 82, 425-434.
27. Radcliffe, P. A.; Toda, T. Characterisation of fission yeast alp11 mutants defines three functional domains within tubulin-folding cofactor B. Mol. Gen. Genet. 2000, 263, 752-760.
28. Velculescu, V. E.; Zhang, L.; Zhou, W.; Vogelstein, J.; Basrai, M. A.; Bassett, D. E.; Hieter, P., Jr.; Vogelstein, B.; Kinzler, K. W. Characterization of the yeast transcriptome. Cell 1997, 88, 243-251.
29. Tian, G.; Lewis, S. A.; Feierbach, B.; Stearns, T.; Rommelaere, H.; Ampe, C.; Cowan, N. J. Tubulin subunits exist in an activated conformational state generated and maintained by protein cofactors. J. Cell Biol. 1997, 138, 821-832.
30. Feierbach, B.; Nogales, E.; Downing, K. H.; Stearns, T. Alf1p, a CLIP-170 domain-containing protein, is functionally and physically associated with alpha-tubulin. J. Cell Biol. 1999, 144, 113-124.
31. Tian, G.; Bhamidipati, A.; Cowan, N. J.; Lewis, S. A. Tubulin folding cofactors as GTPase-activating proteins. GTP hydrolysis and the assembly of the alpha/beta-tubulin heterodimer. J. Biol. Chem. 1999, 274, 24054-24058.
32. Fleming, J. A.; Vega, L. R.; Solomon, F. Function of tubulin binding proteins in vivo. Genetics 2000, 156, 69-80.
33. Bartolini, F.; Bhamidipati, A.; Thomas, S.; Schwahn, U.; Lewis, S. A.; Cowan, N. J. Functional overlap between retinitis pigmentosa 2 protein and the tubulin-specific chaperone cofactor C. J. Biol. Chem. 2002, 277, 14629-14634.
34. Martin, L.; Fanarraga, M. L.; Aloria, K.; Zabala, J. C. Tubulin folding cofactor D is a microtubule destabilizing protein. FEBS Lett. 2000, 470, 93-95.
35. Hoyt, M. A.; Stearns, T.; Botstein, D. Chromosome instability mutants of Saccharomyces cerevisiae that are defective in microtubule-mediated processes. Mol. Cell Biol. 1990, 10, 223-234.
36. Radcliffe, P.; Hirata, D.; Childs, D.; Vardy, L.; Toda, T. Identification of novel temperature-sensitive lethal alleles in essential beta-tubulin and nonessential alpha 2-tubulin genes as fission yeast polarity mutants. Mol. Biol. Cell 1998, 9, 1757-1771.
37. Hoyt, M. A.; Macke, J. P.; Roberts, B. T.; Geiser, J. R. Saccharomyces cerevisiae PAC2 functions with CIN1, 2 and 4 in a pathway leading to normal microtubule stability. Genetics 1997, 146, 849-857.
38. Grishchuk, E. L.; McIntosh, J. R. Sto1p, a fission yeast protein similar to tubulin folding cofactor E, plays an essential role in mitotic microtubule assembly. J. Cell Sci. 1999, 112(Pt 12), 1979-1988.
39. Vega, L. R.; Fleming, J.; Solomon, F. An alpha-tubulin mutant destabilizes the heterodimer: phenotypic consequences and interactions with tubulin-binding proteins. Mol. Biol. Cell 1998, 9, 2349-2360.
40. Keller, C. E.; Lauring, B. P. Possible regulation of microtubules through destabilization of tubulin. Trends Cell Biol. 2005, 15, 571-573.
41. Schuller, E.; Gulesserian, T.; Seidl, R.; Cairns, N. Lube, G. Brain t-complex polypeptide 1 (TCP- 1) related to its natural substrate beta1 tubulin is decreased in Alzheimer's disease. Life Sci. 2001, 69, 263-270.
42. Yoo, B. C.; Fountoulakis, M.; Dierssen, M.; Lubec, G. Expression patterns of chaperone proteins in cerebral cortex of the fetus with Down syndrome: dysregulation of T-complex protein 1. J. Neural. Transm. Suppl. 2001, 321-334.
43. Lee, M. J.; Stephenson, D. A.; Groves, M. J.; Sweeney, M. G.; Davis, M. B.; An, S. F.; Houlden, H.; Salih, M. A.; Timmerman, V.; de Jonghe, P.; Auer-Grumbach, M.; Di Maria, E.; Scaravilli, F. N.; Wood, W.; Reilly, M. M. Hereditary sensory neuropathy is caused by a mutation in the delta subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct4 ) gene. Hum. Mol. Genet. 2003, 12, 1917-1925.
44. Bouhouche, A.; Benomar, A.; Bouslam, N.; Chkili, T.; Yahyaoui, M. Mutation in the epsilon subunit of the cytosolic chaperonin-containing tcomplex peptide-1 (Cct5) gene causes autosomal recessive mutilating sensory neuropathy with spastic paraplegia. J. Med. Genet. 2006, 43, 441-443.
45. Barral, J. M.; Broadley, S. A.; Schaffar, G.; Hartl, F. U. Roles of molecular chaperones in protein misfolding diseases. Semin. Cell Dev. Biol. 2004, 15, 17-29.
46. Parvari, R.; Hershkovitz, E.; Grossman, N.; Gorodischer, R.; Loeys, B.; Zecic, A.; Mortier, G.; Gregory, S.; Sharony, R.; Kambouris, M.; Sakati, N.; Meyer, B. F.; Al Aqeel, A. I.; Al Humaidan, A. K.; Al Zanhrani, F.; Al Swaid, A.; Al Othman, J.; Diaz, G. A.; Weiner, R.; Khan, K. T.; Gordon, R.; Gelb, B. D. Mutation of TBCE causes hypoparathyroidism-retardation-dysmorphism and autosomal recessive Kenny-Caffey syndrome. Nat. Genet. 2002, 32, 448-452.
47. Martin, N.; Jaubert, J.; Gounon, P.; Salido, E.; Haase, G.; Szatanik, M.; Guenet, J. L. A missense mutation in Tbce causes progressive motor neuronopathy in mice. Nat. Genet., 2002, 32, 443-447.
48. Schwahn, U.; Lenzner, S.; Dong, J.; Feil, S.; Hinzmann, B.; van Duijnhoven, G.; Kirschner, R.; Hemberger, M.; Bergen, A. A.; Rosenberg, T. Pinckers, A. J.; Fundele, R.; Rosenthal, A.; Cremers, F. P.; Ropers, H. H.; Berger, W. Positional cloning of the gene for X-linked retinitis pigmentosa 2. Nat. Genet. 1998, 19, 327-332.
49. Boman, A. L.; Kahn, R. A. Arf proteins: the membrane traffic police? Trends Biochem. Sci. 1995, 20, 147-150.
50. Kahn, R. A.; Randazzo, P.; Serafini, T.; Weiss, O.; Rulka, C.; Clark, J.; Amherdt, M.; Roller, P.; Orci, L.; Rothman, J. E. The amino terminus of ADP-ribosylation factor (ARF) is a critical determinant of ARF activities and is a potent and specific inhibitor of protein transport. J. Biol. Chem. 1992, 267, 13039-13046.
51. Clark, J.; Moore, L.; Krasinskas, A.; Way, J.; Battey, J.; Tamkun, J.; Kahn, R. A. Selective amplification of additional members of the ADP-ribosylation factor (ARF) family: cloning of additional human and Drosophila ARF-like genes. Proc. Natl. Acad. Sci. USA 1993, 90, 8952-8956.
52. Sharer, J. D.; Shern, J. F.; Van Valkenburgh, H.; Wallace, D. C.; Kahn, R. A. ARL2 and BART enter mitochondria and bind the adenine nucleotide transporter. Mol. Biol. Cell 2002, 13, 71-83.
53. Bhamidipati, A.; Lewis, S. A.; Cowan, N. J. ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin. J. Cell Biol. 2000, 149, 1087-1096.
54. Shern, J. F.; Sharer, J. D.; Pallas, D. C.; Bartolini, F.; Cowan, N. J.; Reed, M. S.; Pohl, J. Kahn, R. A. Cytosolic Arl2 is complexed with cofactor D and protein phosphatase 2A. J. Biol. Chem. 2003, 278, 40829-40836.
55. Lechward, K.; Awotunde, O. S.; Swiatek, W.; Muszynska, G. Protein phosphatase 2A: variety of forms and diversity of functions. Acta Biochim. Pol. 2001, 48, 921-933.
56. Van Hoof, C.; Goris, J. Phosphatases in apoptosis: to be or not to be, PP2A is in the heart of the question. Biochim. Biophys. Acta 2003, 1640, 97-104.
57. MacKintosh, C.; MacKintosh, R. W. Inhibitors of protein kinases and phosphatases. Trends Biochem. Sci. 1994, 19, 444-448.
58. Cegielska, A.; Shaffer, S.; Derua, R.; Goris, J.; Virshup, D. M. Different oligomeric forms of protein phosphatase 2A activate and inhibit simian virus 40 DNA replication. Mol. Cell Biol. 1994, 14, 4616-4623.
59. Pallas, D. C.; Shahrik, L. K.; Martin, B. L.; Jaspers, S.; Miller, T. B.; Brautigan, D. L.; Roberts, T. M. Polyoma small and middle T antigens and SV40 small t antigen form stable complexes with protein phosphatase 2A. Cell 1990, 60, 167-176.
60. Sontag, E.; Nunbhakdi-Craig, V.; Lee, G.; Brandt, R.; Kamibayashi, C.; Kuret, J.; White, C. L. 3rd.; Mumby, M. C.; Bloom, G. S. Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J. Biol. Chem. 1999, 274, 25490-25498.
61. Radcliffe, P. A.; Vardy, L.; Toda, T. A conserved small GTP-binding protein Alp41 is essential for the cofactor-dependent biogenesis of microtubules in fission yeast. FEBS Lett. 2000, 468, 84-88.