Kinetic stabilization of microtubule dynamics by indanocine perturbs EB1 localization, induces defects in cell polarity and inhibits migration of MDA-MB-231 cells

Biochemical Pharmacology

Volumn 83, Issue 11, 2012, Pages 1495-1506

  Kapoor, Sonia ^a   Panda, Dulal ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

Cell migration; Indanocine; Metastasis; Microtubule dynamics

Indexed keywords

ALPHA TUBULIN; ANTIMETASTATIC AGENT; BINDING PROTEIN; CISPLATIN; INDANOCINE; MICROTUBULE PROTEIN; NOCODAZOLE; PACLITAXEL; PAXILLIN; PROTEIN EB1; TUBULIN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL POLARITY; CONTROLLED STUDY; DYNAMICS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; KINETICS; LAMELLIPODIUM; METASTASIS INHIBITION; MICROTUBULE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TUMOR CELL; WOUND HEALING;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; CELL POLARITY; HUMANS; INDANS; KINETICS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PROTEIN TRANSPORT;

EID: 84859492942     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.02.012     Document Type: Article

References (66)

1. H. Yamaguchi, J. Wyckoff, and J. Condeelis Cell migration in tumors Curr Opin Cell Biol 17 2005 559 564
2. M. Vicente-Manzanares, and A.R. Horwitz Cell migration: an overview Methods Mol Biol 769 2011 1 24
3. T. Watanabe, J. Noritake, and K. Kaibuchi Regulation of microtubules in cell migration Trends Cell Biol 15 2005 76 83
4. I. Kaverina, and A. Straube Regulation of cell migration by dynamic microtubules Semin Cell Dev Biol 22 2011 968 974
5. R.A. Walker, E.T. O'Brien, N.K. Pryer, M.F. Soboeiro, and W.A. Voter Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies J Cell Biol 107 1988 1437 1448
6. A. Desai, and T.J. Mitchison Microtubule polymerization dynamics Annu Rev Cell Dev Biol 13 1997 83 117
7. B. van der Vaart, A. Akhmanova, and A. Straube Regulation of microtubule dynamic instability Biochem Soc Trans 37 2009 1007 1013
8. G.G. Gundersen, and J.C. Bulinski Selective stabilization of microtubules oriented toward the direction of cell migration Proc Natl Acad Sci USA 85 1988 5946 5950
9. P. Wadsworth Regional regulation of microtubule dynamics in polarized, motile cells Cell Motil Cytoskeleton 42 1999 48 59
10. J.M. Vasiliev, I.M. Gelfand, L.V. Domnina, O.Y. Ivanova, S.G. Komm, and L.V. Olshevskaja Effect of colcemid on the locomotory behaviour of fibroblasts J Embryol Exp Morphol 24 1970 625 640
11. J.E. Glasgow, and R.P. Daniele Role of microtubules in random cell migration: stabilization of cell polarity Cell Motil Cytoskeleton 27 1994 88 96
12. A. Bershadsky, A. Chausovsky, E. Becker, A. Lyubimova, and B. Geiger Involvement of microtubules in the control of adhesion-dependent signal transduction Curr Biol 6 1996 1279 1289
13. B. Wehrle-Haller, and B.A. Imhof Actin, microtubules and focal adhesion dynamics during cell migration Int J Biochem Cell Biol 35 2003 39 50
14. C.M. Waterman-Storer, R.A. Worthylake, B.P. Liu, K. Burridge, and E.D. Salmon Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts Nat Cell Biol 1 1999 45 50
15. X.D. Ren, W.B. Kiosses, and M.A. Schwartz Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton EMBO J 18 1999 578 585
16. T. Wittmann, and C.M. Waterman-Storer Cell motility: can Rho GTPases and microtubules point the way J Cell Sci 114 2001 3795 3803
17. C. Dumontet, and M.A. Jordan Microtubule-binding agents: a dynamic field of cancer therapeutics Nat Rev Drug Discov 9 2010 790 803
18. P. Singh, K. Rathinasamy, R. Mohan, and D. Panda Microtubule assembly dynamics: an attractive target for anticancer drugs IUBMB Life 60 2008 368 375
19. M.E. Stearns, and M. Wang Taxol blocks processes essential for prostate tumor cell (PC-3 ML) invasion and metastases Cancer Res 52 1992 3776 3781
20. K.A. Hotchkiss, A.W. Ashton, R. Mahmood, R.G. Russell, J.A. Sparano, and E.L. Schwartz Inhibition of endothelial cell function in vitro and angiogenesis in vivo by docetaxel (Taxotere): association with impaired repositioning of the microtubule organizing center Mol Cancer Ther 1 2002 1191 1200
21. C. Hayot, S. Farinelle, R. De Decker, C. Decaestecker, F. Darro, and R. Kiss In vitro pharmacological characterizations of the anti-angiogenic and anti-tumor cell migration properties mediated by microtubule-affecting drugs, with special emphasis on the organization of the actin cytoskeleton Int J Oncol 21 2002 417 425
22. E. Pasquier, S. Honoré, and D. Braguer Microtubule-targeting agents in angiogenesis: where do we stand Drug Resist Updat 9 2006 74 86
23. G. Liao, T. Nagasaki, and G.G. Gundersen Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: implications for the role of dynamic microtubules in cell locomotion J Cell Sci 108 1995 3473 3483
24. A. Mikhailov, and G.G. Gundersen Relationship between microtubule dynamics and lamellipodium formation revealed by direct imaging of microtubules in cells treated with nocodazole or taxol Cell Motil Cytoskeleton 41 1998 325 340
25. H. Yang, A. Ganguly, and F. Cabral Inhibition of cell migration and cell division correlates with distinct effects of microtubule inhibiting drugs J Biol Chem 285 2010 32242 32250
26. S. Honoré, A. Pagano, G. Gauthier, V. Bourgarel-Rey, P. Verdier-Pinard, and K. Civiletti Antiangiogenic vinflunine affects EB1 localization and microtubule targeting to adhesion sites Mol Cancer Ther 7 2008 2080 2089
27. A. Ganguly, H. Yang, and F. Cabral Class III β-tubulin counteracts the ability of paclitaxel to inhibit cell migration Oncotarget 2 2011 368 377
28. L.M. Leoni, E. Hamel, D. Genini, H. Shih, C.J. Carrera, and H.B. Cottam Indanocine, a microtubule-binding indanone and a selective inducer of apoptosis in multidrug-resistant cancer cells J Natl Cancer Inst 92 2000 217 224
29. X.H. Hua, D. Genini, R. Gussio, R. Tawatao, H. Shih, and T.J. Kipps Biochemical genetic analysis of indanocine resistance in human leukemia Cancer Res 61 2001 7248 7254
30. L. Das, S. Gupta, D. Dasgupta, A. Poddar, M.E. Janik, and B. Bhattacharyya Binding of indanocine to the colchicine site on tubulin promotes fluorescence, and its binding parameters resemble those of the colchicine analogue AC Biochemistry 48 2009 1628 1635
31. P. Skehan, R. Storeng, D. Scudiero, A. Monks, J. McMahon, and D. Vistica New colorimetric cytotoxicity assay for anticancer-drug screening J Natl Cancer Inst 82 1990 1107 1112
32. R. Mohan, and D. Panda Kinetic stabilization of microtubule dynamics by estramustine is associated with tubulin acetylation, spindle abnormalities, and mitotic arrest Cancer Res 68 2008 6181 6189
33. C.C. Liang, A.Y. Park, and J.L. Guan In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro Nat Protoc 2 2007 329 333
34. K. Rathinasamy, and D. Panda Kinetic stabilization of microtubule dynamic instability by benomyl increases the nuclear transport of p53 Biochem Pharmacol 15 2008 1669 1680
35. S.J. Haggarty, K.M. Koeller, J.C. Wong, C.M. Grozinger, and S.L. Schreiber Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation Proc Natl Acad Sci USA 100 2003 4389 4394
36. A.D. Tran, T.P. Marmo, A.A. Salam, S. Che, E. Finkelstein, and R. Kabarriti HDAC6 deacetylation of tubulin modulates dynamics of cellular adhesions J Cell Sci 120 2007 1469 1479
37. B. Bisel, Y. Wang, J.H. Wei, Y. Xiang, D. Tang, and M. Miron-Mendoza ERK regulates Golgi and centrosome orientation towards the leading edge through GRASP65 J Cell Biol 182 2008 837 843
38. D.J. Webb, K. Donais, L.A. Whitmore, S.M. Thomas, C.E. Turner, and J.T. Parsons FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly Nat Cell Biol 6 2004 154 161
39. E. Schulze, D.J. Asai, J.C. Bulinski, and M. Kirschner Posttranslational modification and microtubule stability J Cell Biol 105 1987 2167 2177
40. D.R. Webster, and G.G. Borisy Microtubules are acetylated in domains that turn over slowly J Cell Sci 92 1989 57 65
41. J.S. Tirnauer, and B.E. Bierer EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability J Cell Biol 149 2000 761 766
42. B. Vitre, F.M. Coquelle, C. Heichette, C. Garnier, D. Chrétien, and I. Arnal EB1 regulates microtubule dynamics and tubulin sheet closure in vitro Nat Cell Biol 10 2008 415 421
43. J.M. Schober, J.M. Cain, Y.A. Komarova, and G.G. Borisy Migration and actin protrusion in melanoma cells are regulated by EB1 protein Cancer Lett 284 2009 30 36
44. I. Kaverina, K. Rottner, and J.V. Small Targeting, capture, and stabilization of microtubules at early focal adhesions J Cell Biol 142 1998 181 190
45. I. Kaverina, O. Krylyshkina, and J.V. Small Microtubule targeting of substrate contacts promotes their relaxation and dissociation J Cell Biol 146 1999 1033 1044
46. J.V. Small, and I. Kaverina Microtubules meet substrate adhesions to arrange cell polarity Curr Opin Cell Biol 15 2003 40 47
47. A. Efimov, N. Schiefermeier, I. Grigoriev, R. Ohi, M.C. Brown, and C.E. Turner Paxillin-dependent stimulation of microtubule catastrophes at focal adhesion sites J Cell Sci 121 2008 196 204
48. V.J. Fincham, M. James, M.C. Frame, and S.J. Winder Active ERK/MAP kinase is targeted to newly forming cell-matrix adhesions by integrin engagement and v-Src EMBO J 19 2000 2911 2923
49. M.C. Mendoza, E.E. Er, W. Zhang, B.A. Ballif, H.L. Elliott, and G. Danuser ERK-MAPK drives lamellipodia protrusion by activating the WAVE2 regulatory complex Mol Cell 41 2011 661 671
50. K.J. Salaycik, C.J. Fagerstrom, K. Murthy, U.S. Tulu, and P. Wadsworth Quantification of microtubule nucleation, growth and dynamics in wound-edge cells J Cell Sci 118 2005 4113 4122
51. A. Kupfer, D. Louvard, and S.J. Singer Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound Proc Natl Acad Sci USA 79 1982 2603 2607
52. J.A. Broussard, D.J. Webb, and I. Kaverina Asymmetric focal adhesion disassembly in motile cells Curr Opin Cell Biol 20 2008 85 90
53. I.R. Nabi The polarization of the motile cell J Cell Sci 112 1999 1803 1811
54. Y. Wen, C.H. Eng, J. Schmoranzer, N. Cabrera-Poch, E.J. Morris, and M. Chen EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration Nat Cell Biol 6 2004 820 830
55. Y. Mimori-Kiyosue, I. Grigoriev, G. Lansbergen, H. Sasaki, C. Matsui, and F. Severin CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex J Cell Biol 168 2005 141 153
56. T. Watanabe, J. Noritake, M. Kakeno, T. Matsui, T. Harada, and S. Wang Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules J Cell Sci 122 2009 2969 2979
57. A. Akhmanova, and C.C. Hoogenraad Microtubule plus-end-tracking proteins: mechanisms and functions Curr Opin Cell Biol 17 2005 47 54
58. M. Zanic, J.H. Stear, A.A. Hyman, and J. Howard EB1 recognizes the nucleotide state of tubulin in the microtubule lattice PLoS One 4 2009 e7585
59. D. Panda, H.P. Miller, and L. Wilson Determination of the size and chemical nature of the stabilizing cap at microtubule ends using modulators of polymerization dynamics Biochemistry 41 2002 1609 1617
60. O. Krylyshkina, I. Kaverina, W. Kranewitter, W. Steffen, M.C. Alonso, and R.A. Cross Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1 J Cell Biol 156 2002 349 359
61. N.A. Reed, D. Cai, T.L. Blasius, G.T. Jih, E. Meyhofer, and J. Gaertig Microtubule acetylation promotes kinesin-1 binding and transport Curr Biol 16 2006 2166 2172
62. K.C. Slep Structural and mechanistic insights into microtubule end-binding proteins Curr Opin Cell Biol 22 2010 88 95
63. A. Nakano, H. Kato, T. Watanabe, K.D. Min, S. Yamazaki, and Y. Asano AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation Nat Cell Biol 12 2010 583 590
64. S. Etienne-Manneville APC in cell migration Adv Exp Med Biol 656 2009 30 40
65. K. Drabek, M. van Ham, T. Stepanova, K. Draegestein, R. van Horssen, and C.L. Sayas Role of CLASP2 in microtubule stabilization and the regulation of persistent motility Curr Biol 16 2006 2259 2264
66. X. Wu, A. Kodama, and E. Fuchs ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity Cell 135 2008 137 148