The multidomain protooncogenic protein c-Cbl binds to tubulin and stabilizes microtubules

Experimental Cell Research

Volumn 306, Issue 1, 2005, Pages 114-127

  Teckchandani, Anjali M ^a   Birukova, Anna A ^b   Tar, Krisztina ^b   Verin, Alexander D ^b   Tsygankov, Alexander Y ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylation; c Cbl; Endothelial cells; Microtubules; Polymerization; Stabilization; Tubulin

Indexed keywords

CBL PROTEIN; PROTEIN TYROSINE KINASE; TUBULIN;

ANIMAL CELL; ARTICLE; CELL STRAIN COS7; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MICROTUBULE; MUTATION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY;

EID: 18844455052     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2005.02.014     Document Type: Article

References (74)

1. E. Nogales Structural insights into microtubule function Annu. Rev. Biochem. 69 2000 277 302
2. T. Mitchison, and M. Kirschner Dynamic instability of microtubule growth Nature 312 1984 237 242
3. R.A. Walker, E.T. O'Brien, N.K. Pryer, M.F. Soboeiro, W.A. Voter, H.P. Erickson, and E.D. Salmon Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies J. Cell Biol. 107 1988 1437 1448
4. A. Desai, and T.J. Mitchison Microtubule polymerization dynamics Annu. Rev. Cell Dev. Biol. 13 1997 83 117
5. T.H. MacRae Microtubule organization by cross-linking and bundling proteins Biochim. Biophys. Acta 1160 1992 145 155
6. A.Y. Tsygankov, A.M. Teckchandani, E.A. Feshchenko, and G. Swaminathan Beyond the RING: CBL proteins as multivalent adapters Oncogene 20 2001 6382 6402
7. C.B. Thien, and W.Y. Langdon Cbl: many adaptations to regulate protein tyrosine kinases Nat. Rev., Mol. Cell Biol. 2 2001 294 307
8. N. Rao, I. Dodge, and H. Band The Cbl family of ubiquitin ligases: critical negative regulators of tyrosine kinase signaling in the immune system J. Leukocyte Biol. 71 2002 753 763
9. M.L. Galisteo, I. Dikic, A.G. Batzer, W.Y. Langdon, and J. Schlessinger Tyrosine phosphorylation of the c-cbl proto-oncogene protein product and association with epidermal growth factor (EGF) receptor upon EGF stimulation J. Biol. Chem. 270 1995 20242 20245
10. M.L. Lupher Jr., K.A. Reedquist, S. Miyake, W.Y. Langdon, and H. Band A novel phosphotyrosine-binding domain in the N-terminal transforming region of Cbl interacts directly and selectively with ZAP-70 in T cells J. Biol. Chem. 271 1996 24063 24068
11. D.P. Bonita, S. Miyake, M.L. Lupher Jr., W.Y. Langdon, and H. Band Phosphotyrosine binding domain-dependent upregulation of the platelet-derived growth factor receptor alpha signaling cascade by transforming mutants of Cbl: implications for Cbl's function and oncogenicity Mol. Cell. Biol. 17 1997 4597 4610
12. M.L. Lupher Jr., N. Rao, N.L. Lill, C.E. Andoniou, S. Miyake, E.A. Clark, B. Druker, and H. Band Cbl-mediated negative regulation of the Syk tyrosine kinase. A critical role for Cbl phosphotyrosine-binding domain binding to Syk phosphotyrosine 323 J. Biol. Chem. 273 1998 35273 35281
13. M. Deckert, C. Elly, A. Altman, and Y.C. Liu Coordinated regulation of the tyrosine phosphorylation of Cbl by Fyn and Syk tyrosine kinases J. Biol. Chem. 273 1998 8867 8874
14. C.A. Joazeiro, S.S. Wing, H. Huang, J.D. Leverson, T. Hunter, and Y.C. Liu The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase Science 286 1999 309 312
15. G. Levkowitz, H. Waterman, S.A. Ettenberg, M. Katz, A.Y. Tsygankov, I. Alroy, S. Lavi, K. Iwai, Y. Reiss, A. Ciechanover, S. Lipkowitz, and Y. Yarden Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1 Mol. Cell 4 1999 1029 1040
16. H. Waterman, G. Levkowitz, I. Alroy, and Y. Yarden The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor J. Biol. Chem. 274 1999 22151 22154
17. J.A. Fernandez, L.M. Keshvara, J.D. Peters, M.T. Furlong, M.L. Harrison, and R.L. Geahlen Phosphorylation- and activation-independent association of the tyrosine kinase Syk and the tyrosine kinase substrates Cbl and Vav with tubulin in B-cells J. Biol. Chem. 274 1999 1401 1406
18. T.M. Yankee, L.M. Keshvara, S. Sawasdikosol, M.L. Harrison, and R.L. Geahlen Inhibition of signaling through the B cell antigen receptor by the protooncogene product, c-Cbl, requires Syk tyrosine 317 and the c-Cbl phosphotyrosine-binding domain J. Immunol. 163 1999 5827 5835
19. E.A. Feshchenko, E.V. Smirnova, G. Swaminathan, A.M. Teckchandani, R. Agrawal, H. Band, X. Zhang, R.S. Annan, S.A. Carr, and A.Y. Tsygankov TULA: An SH3- and UBA-containing protein that binds to c-Cbl and ubiquitin Oncogene 23 2004 4690 4706
20. S.W. L'Hernault, and J.L. Rosenbaum Chlamydomonas alpha-tubulin is posttranslationally modified by acetylation on the epsilon-amino group of a lysine Biochemistry 24 1985 473 478
21. I.A. Khan, and R.F. Luduena Phosphorylation of beta III-tubulin Biochemistry 35 1996 3704 3711
22. V. Redeker, N. Levilliers, J.M. Schmitter, J.P. Le Caer, J. Rossier, A. Adoutte, and M.H. Bre Polyglycylation of tubulin: a posttranslational modification in axonemal microtubules Science 266 1994 1688 1691
23. B. Edde, J. Rossier, J.P. LeCaer, E. Desbruyeres, F. Gros, and P. Denoulet Posttranslational glutamylation of alpha-tubulin Science 247 1990 83 85
24. J.A. Rodriguez, and G.G. Borisy Modification of the C-terminus of brain tubulin during development Biochem. Biophys. Res. Commun. 83 1978 579 586
25. L. Paturle-Lafanechere, B. Edde, P. Denoulet, A. Van Dorsselaer, H. Mazarguil, J.P. Le Caer, J. Wehland, and D. Jod Characterization of a major brain tubulin variant which cannot be tyrosinated Biochemistry 30 1991 10523 10528
26. E.A. Feshchenko, W.Y. Langdon, and A.Y. Tsygankov Fyn, Yes, and Syk phosphorylation sites in c-Cbl map to the same tyrosine residues that become phosphorylated in activated T cells J. Biol. Chem. 273 1998 8323 8331
27. K.G. Birukov, A.A. Birukova, S.M. Dudek, A.D. Verin, M.T. Crow, X. Zhan, N. DePaola, and J.G. Garcia Shear stress-mediated cytoskeletal remodeling and cortactin translocation in pulmonary endothelial cells Am. J. Respir. Cell Mol. Biol. 26 2002 453 464
28. I. Tint, T. Slaughter, I. Fischer, and M.M. Black Acute inactivation of tau has no effect on dynamics of microtubules in growing axons of cultured sympathetic neurons J. Neurosci. 18 1998 8660 8673
29. Y. Gachet, S. Tournier, M. Lee, A. Lazaris-Karatzas, T. Poulton, and U.A. Bommer The growth-related, translationally controlled protein P23 has properties of a tubulin binding protein and associates transiently with microtubules during the cell cycle J. Cell Sci. 112 Pt. 8 1999 1257 1271
30. J.D. Jiang, A.S. Davis, K.M. Middleton, Y.H. Ling, R. Perez-Soler, J.F. Holland, and J.G. Bekesi 3-(Iodoacetamido)-benzoylurea: a novel cancericidal tubulin ligand that inhibits microtubule polymerization, phosphorylates bcl-2, and induces apoptosis in tumor cells Cancer Res. 58 1998 5389 5395
31. A. Davis, J.D. Jiang, K.M. Middleton, Y. Wang, I. Weisz, Y.H. Ling, and J.G. Bekesi Novel suicide ligands of tubulin arrest cancer cells in S-phase Neoplasia 1 1999 498 507
32. J.D. Jiang, L. Denner, Y.H. Ling, J.N. Li, A. Davis, Y. Wang, Y. Li, J. Roboz, L.G. Wang, R. Perez-Soler, M. Marcelli, G. Bekesi, and J.F. Holland Double blockade of cell cycle at g(1)-s transition and m phase by 3-iodoacetamido benzoyl ethyl ester, a new type of tubulin ligand Cancer Res. 62 2002 6080 6088
33. T.S. Panetti, J. Nowlen, and D.F. Mosher Sphingosine-1-phosphate and lysophosphatidic acid stimulate endothelial cell migration Arterioscler., Thromb., Vasc. Biol. 20 2000 1013 1019
34. A.D. Verin, A. Birukova, P. Wang, F. Liu, P. Becker, K. Birukov, and J.G. Garcia Microtubule disassembly increases endothelial cell barrier dysfunction: role of MLC phosphorylation Am. J. Physiol.: Lung Cell. Mol. Physiol. 281 2001 L565 L574
35. I. Petrache, A. Birukova, S.I. Ramirez, J.G. Garcia, and A.D. Verin The role of the microtubules in tumor necrosis factor-alpha-induced endothelial cell permeability Am. J. Respir. Cell Mol. Biol. 28 2003 574 581
36. T.M. Fournier, L. Lamorte, C.R. Maroun, M. Lupher, H. Band, W. Langdon, and M. Park Cbl-transforming variants trigger a cascade of molecular alterations that lead to epithelial mesenchymal conversion Mol. Biol. Cell 11 2000 3397 3410
37. C. Dong, Z. Li, R. Alvarez Jr., X.H. Feng, and P.J. Goldschmidt-Clermont Microtubule binding to Smads may regulate TGF beta activity Mol. Cell 5 2000 27 34
38. A. Nieto, J. Avila, and M.M. Valdivia Comparative measurement by radioimmunoassay of the brain microtubule-associated protein MAP2 Mol. Cell. Biochem. 37 1981 185 189
39. M. Goedert, R.A. Crowther, and C.C. Garner Molecular characterization of microtubule-associated proteins tau and MAP2 Trends Neurosci. 14 1991 193 199
40. F. Meng, and C.A. Lowell A beta 1 integrin signaling pathway involving Src-family kinases, Cbl and PI-3 kinase is required for macrophage spreading and migration EMBO J. 17 1998 4391 4403
41. E.A. Feshchenko, S.K. Shore, and A.Y. Tsygankov Tyrosine phosphorylation of C-Cbl facilitates adhesion and spreading while suppressing anchorage-independent growth of V-Abl-transformed NIH3T3 fibroblasts Oncogene 18 1999 3703 3715
42. R.M. Scaife, and W.Y. Langdon c-Cbl localizes to actin lamellae and regulates lamellipodia formation and cell morphology J. Cell Sci. 113 Pt. 2 2000 215 226
43. A.M. Teckchandani, E.A. Feshchenko, and A.Y. Tsygankov c-Cbl facilitates fibronectin matrix production by v-Abl-transformed NIH3T3 cells via activation of small GTPases Oncogene 20 2001 1739 1755
44. R.M. Scaife, S.A. Courtneidge, and W.Y. Langdon The multi-adaptor proto-oncoprotein Cbl is a key regulator of Rac and actin assembly J. Cell Sci. 116 2003 463 473
45. R.M. Scaife, D. Job, and W.Y. Langdon Rapid microtubule-dependent induction of neurite-like extensions in NIH 3T3 fibroblasts by inhibition of ROCK and Cbl Mol. Biol. Cell 14 2003 4605 4617
46. W.C. Thompson, D.J. Asai, and D.H. Carney Heterogeneity among microtubules of the cytoplasmic microtubule complex detected by a monoclonal antibody to alpha tubulin J. Cell Biol. 98 1984 1017 1025
47. G. Piperno, M. LeDizet, and X.J. Chang Microtubules containing acetylated alpha-tubulin in mammalian cells in culture J. Cell Biol. 104 1987 289 302
48. E. Schulze, D.J. Asai, J.C. Bulinski, and M. Kirschner Posttranslational modification and microtubule stability J. Cell Biol. 105 1987 2167 2177
49. J.C. Bulinski, J.E. Richards, and G. Piperno Posttranslational modifications of alpha tubulin: detyrosination and acetylation differentiate populations of interphase microtubules in cultured cells J. Cell Biol. 106 1988 1213 1220
50. M. LeDizet, and G. Piperno Identification of an acetylation site of chlamydomonas alpha-tubulin Proc. Natl. Acad. Sci. U. S. A. 84 1987 5720 5724
51. W. Meng, S. Sawasdikosol, S.J. Burakoff, and M.J. Eck Structure of the amino-terminal domain of Cbl complexed to its binding site on ZAP-70 kinase Nature 398 1999 84 90
52. T. Itoh, K. Miura, H. Miki, and T. Takenawa Beta-tubulin binds Src homology 2 domains through a region different from the tyrosine-phosphorylated protein-recognizing site J. Biol. Chem. 271 1996 27931 27935
53. A. Marie-Cardine, H. Kirchgessner, C. Eckerskorn, S.C. Meuer, and B. Schraven Human T lymphocyte activation induces tyrosine phosphorylation of alpha-tubulin and its association with the SH2 domain of the p59fyn protein tyrosine kinase Eur. J. Immunol. 25 1995 3290 3297
54. E.P. Sablin Kinesins and microtubules: their structures and motor mechanisms Curr. Opin. Cell Biol. 12 2000 35 41
55. K. Hirose, and L.A. Amos Three-dimensional structure of motor molecules Cell. Mol. Life Sci. 56 1999 184 199
56. R. Takemura, S. Okabe, T. Umeyama, Y. Kanai, N.J. Cowan, and N. Hirokawa Increased microtubule stability and alpha tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau J. Cell Sci. 103 Pt. 4 1992 953 964
57. H. Maruta, K. Greer, and J.L. Rosenbaum The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules J. Cell Biol. 103 1986 571 579
58. D.R. Webster, and G.G. Borisy Microtubules are acetylated in domains that turn over slowly J. Cell Sci. 92 Pt. 1 1989 57 65
59. C. Hubbert, A. Guardiola, R. Shao, Y. Kawaguchi, A. Ito, A. Nixon, M. Yoshida, X.F. Wang, and T.P. Yao HDAC6 is a microtubule-associated deacetylase Nature 417 2002 455 458
60. A. Palazzo, B. Ackerman, and G.G. Gundersen Cell biology: tubulin acetylation and cell motility Nature 421 2003 230
61. M. Somers, Y. Engelborghs, and J. Baert Analysis of the binding of glyceraldehyde-3-phosphate dehydrogenase to microtubules, the mechanism of bundle formation and the linkage effect Eur. J. Biochem. 193 1990 437 444
62. V.T. Marchesi, and N. Ngo In vitro assembly of multiprotein complexes containing alpha, beta, and gamma tubulin, heat shock protein HSP70, and elongation factor 1 alpha Proc. Natl. Acad. Sci. U. S. A. 90 1993 3028 3032
63. V.I. Muronetz, Z.X. Wang, T.J. Keith, H.R. Knull, and D.K. Srivastava Binding constants and stoichiometries of glyceraldehyde 3-phosphate dehydrogenase-tubulin complexes Arch. Biochem. Biophys. 313 1994 253 260
64. N.A. Durso, and R.J. Cyr A calmodulin-sensitive interaction between microtubules and a higher plant homolog of elongation factor-1 alpha Plant Cell 6 1994 893 905
65. R.C. Moore, N.A. Durso, and R.J. Cyr Elongation factor-1alpha stabilizes microtubules in a calcium/calmodulin-dependent manner Cell Motil. Cytoskeleton 41 1998 168 180
66. N. Shiina, Y. Gotoh, N. Kubomura, A. Iwamatsu, and E. Nishida Microtubule severing by elongation factor 1 alpha Science 266 1994 282 285
67. C.M. Waterman-Storer, and E. Salmon Positive feedback interactions between microtubule and actin dynamics during cell motility Curr. Opin. Cell Biol. 11 1999 61 67
68. D.M. Suter, and P. Forscher Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance J. Neurobiol. 44 2000 97 113
69. B.L. Goode, D.G. Drubin, and G. Barnes Functional cooperation between the microtubule and actin cytoskeletons Curr. Opin. Cell Biol. 12 2000 63 71
70. F. Entschladen, and K.S. Zanker Locomotion of tumor cells: a molecular comparison to migrating pre- and postmitotic leukocytes J. Cancer Res. Clin. Oncol. 126 2000 671 681
71. E. Karsenti, and I. Vernos The mitotic spindle: a self-made machine Science 294 2001 543 547
72. S.P. Blagden, and D.M. Glover Polar expeditions-provisioning the centrosome for mitosis Nat. Cell Biol. 5 2003 505 511
73. Y. Volkov, A. Long, S. McGrath, D. Ni Eidhin, and D. Kelleher Crucial importance of PKC-beta(I) in LFA-1-mediated locomotion of activated T cells Nat. Immunol. 2 2001 508 514
74. J.R. Kuhn, and M. Poenie Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing Immunity 16 2002 111 121