RhoGTPases - A novel link between cytoskeleton organization and cisplatin resistance

Drug Resistance Updates

Volumn 19, Issue , 2015, Pages 22-32

  Mokady, Daphna ^a   Meiri, David ^b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Chemoresistance; Cisplatin; Cytoskeleton; Drug resistance; RhoA; RhoGTPases; Rock Cancer therapy

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL; CYTOSKELETON; DISEASE COURSE; DRUG DESIGN; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; NEOPLASMS; PATHOLOGY; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CISPLATIN; CYTOSKELETON; DISEASE PROGRESSION; DRUG DESIGN; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; RHO GTP-BINDING PROTEINS; UP-REGULATION;

EID: 84939981042     PISSN: 13687646     EISSN: 15322084     Source Type: Journal    
DOI: 10.1016/j.drup.2015.01.001     Document Type: Article

References (164)

1. M.T. Abraham, M.A. Kuriakose, P.G. Sacks, H. Yee, L. Chiriboga, E.L. Bearer, and M.D. Delacure Motility-related proteins as markers for head and neck squamous cell cancer Laryngoscope 111 2001 1285 1289 10.1097/00005537-200107000-00027
2. P. Adamson, C.J. Marshall, A. Hall, and P.A. Tilbrook Post-translational modifications of p21rho proteins J. Biol. Chem. 267 1992 20033 20038
3. I. Adini, I. Rabinovitz, J.F. Sun, G.C. Prendergast, and L.E. Benjamin RhoB controls Akt trafficking and stage-specific survival of endothelial cells during vascular development Genes Dev. 17 2003 2721 2732 10.1101/gad.1134603
4. J. Adnane, C. Muro-Cacho, L. Mathews, S.M. Sebti, and T. Muñoz-Antonia Suppression of rho B expression in invasive carcinoma from head and neck cancer patients Clin. Cancer Res. 8 2002 2225 2232
5. M. Amano, M. Nakayama, and K. Kaibuchi Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity Cytoskeleton (Hoboken) 67 2010 545 554 10.1002/cm.20472
6. N.M.G.M. Appels, J.H. Beijnen, and J.H.M. Schellens Development of farnesyl transferase inhibitors: a review Oncologist 10 2005 565 578 10.1634/theoncologist.10-8-565
7. W.T. Arthur, N.K. Noren, and K. Burridge Regulation of Rho family GTPases by cell-cell and cell-matrix adhesion Biol. Res. 35 2002 239 246
8. D. Bar-Sagi, and J.R. Feramisco Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins Science 233 1986 1061 1068
9. G. Benedetti, M. Fokkelman, K. Yan, L. Fredriksson, B. Herpers, J. Meerman, B. van de Water, and M. de Graauw The nuclear factor κB family member RelB facilitates apoptosis of renal epithelial cells caused by cisplatin/tumor necrosis factor α synergy by suppressing an epithelial to mesenchymal transition-like phenotypic switch Mol. Pharmacol. 84 2013 128 138 10.1124/mol.112.084053
10. A. Bernards, and J. Settleman GAP control: regulating the regulators of small GTPases Trends Cell Biol. 14 2004 377 385 10.1016/j.tcb.2004.05.003
11. E.J. Bernhard, G. Kao, A.D. Cox, S.M. Sebti, A.D. Hamilton, R.J. Muschel, and W.G. McKenna The farnesyltransferase inhibitor FTI-277 radiosensitizes H-ras-transformed rat embryo fibroblasts Cancer Res. 56 1996 1727 1730
12. E.J. Bernhard, W.G. McKenna, A.D. Hamilton, S.M. Sebti, Y. Qian, J.M. Wu, and R.J. Muschel Inhibiting Ras prenylation increases the radiosensitivity of human tumor cell lines with activating mutations of ras oncogenes Cancer Res. 58 1998 1754 1761
13. P.J. Bhavsar, E. Infante, A. Khwaja, and A.J. Ridley Analysis of Rho GTPase expression in T-ALL identifies RhoU as a target for Notch involved in T-ALL cell migration Oncogene 32 2013 198 208 10.1038/onc.2012.42
14. J.L. Bos, H. Rehmann, and A. Wittinghofer GEFs and GAPs: critical elements in the control of small G proteins Cell 129 2007 865 877 10.1016/j.cell.2007.05.018
15. J.J. Bravo-Cordero, M. Oser, X. Chen, R. Eddy, L. Hodgson, and J. Condeelis A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia Curr. Biol. 21 2011 635 644 10.1016/j.cub.2011.03.039
16. J.M. Brown, and A.J. Giaccia The unique physiology of solid tumors: opportunities (and problems) for cancer therapy Cancer Res. 58 1998 1408 1416
17. T.B. Brunner, S.M. Hahn, A.K. Gupta, R.J. Muschel, W.G. McKenna, and E.J. Bernhard Farnesyltransferase inhibitors: an overview of the results of preclinical and clinical investigations Cancer Res. 63 2003 5656 5668
18. Cancer Genome Atlas Research Network Comprehensive molecular characterization of gastric adenocarcinoma Nature 513 2014 202 209 10.1038/nature13480
19. B. Canguilhem, A. Pradines, C. Baudouin, C. Boby, I. Lajoie-Mazenc, M. Charveron, and G. Favre RhoB protects human keratinocytes from UVB-induced apoptosis through epidermal growth factor receptor signaling J. Biol. Chem. 280 2005 43257 43263 10.1074/jbc.M508650200
20. M. Chatterjee, and K.L. van Golen Farnesyl transferase inhibitor treatment of breast cancer cells leads to altered RhoA and RhoC GTPase activity and induces a dormant phenotype Int. J. Cancer 129 2011 61 69 10.1002/ijc.25655
21. Y.-P. Ching, C.-M. Wong, S.-F. Chan, T.H.-Y. Leung, D.C.-H. Ng, D.-Y. Jin, and I.O. Ng Deleted in liver cancer (DLC) 2 encodes a RhoGAP protein with growth suppressor function and is underexpressed in hepatocellular carcinoma J. Biol. Chem. 278 2003 10824 10830 10.1074/jbc.M208310200
22. J.W. Choi, D.R. Herr, K. Noguchi, Y.C. Yung, C.-W. Lee, T. Mutoh, M.-E. Lin, S.T. Teo, K.E. Park, A.N. Mosley, and J. Chun LPA receptors: subtypes and biological actions Annu. Rev. Pharmacol. Toxicol. 50 2010 157 186 10.1146/annurev.pharmtox.010909.105753
23. T. Cimbora-Zovko, G. Fritz, N. Mikac, and M. Osmak Downregulation of RhoB GTPase confers resistance to cisplatin in human laryngeal carcinoma cells Cancer Lett. 295 2010 182 190 10.1016/j.canlet.2010.02.025
24. E.A. Clark, T.R. Golub, E.S. Lander, and R.O. Hynes Genomic analysis of metastasis reveals an essential role for RhoC Nature 406 2000 532 535 10.1038/35020106
25. F.M. Collier, C.C. Gregorio-King, T.J. Gough, C.D. Talbot, K. Walder, and M.A. Kirkland Identification and characterization of a lymphocytic Rho-GTPase effector: rhotekin-2 Biochem. Biophys. Res. Commun. 324 2004 1360 1369 10.1016/j.bbrc.2004.09.205
26. D.R. Croft, and M.F. Olson Transcriptional regulation of Rho GTPase signaling Transcription 2 2011 211 215 10.4161/trns.2.5.16904
27. J. Cullis, D. Meiri, M.J. Sandi, N. Radulovich, O.A. Kent, M. Medrano, D. Mokady, J. Normand, J. Larose, R. Marcotte, C.B. Marshall, M. Ikura, T. Ketela, J. Moffat, B.G. Neel, A.-C. Gingras, M.-S. Tsao, and R. Rottapel The RhoGEF GEF-H1 is required for oncogenic RAS signaling via KSR-1 Cancer Cell 25 2014 181 195 10.1016/j.ccr.2014.01.025
28. J.S. Damiano, A.E. Cress, L.A. Hazlehurst, A.A. Shtil, and W.S. Dalton Cell adhesion mediated drug resistance (CAM-DR): role of integrins and resistance to apoptosis in human myeloma cell lines Blood 93 1999 1658 1667
29. S. Dasari, and P. Bernard Tchounwou Cisplatin in cancer therapy: molecular mechanisms of action Eur. J. Pharmacol. 740 2014 364 378 10.1016/j.ejphar.2014.07.025
30. A. Davis, A.V. Tinker, and M. Friedlander "Platinum resistant" ovarian cancer: what is it, who to treat and how to measure benefit? Gynecol. Oncol. 133 2014 624 631 10.1016/j.ygyno.2014.02.038
31. W. Du, P.F. Lebowitz, and G.C. Prendergast Cell growth inhibition by farnesyltransferase inhibitors is mediated by gain of geranylgeranylated RhoB Mol. Cell. Biol. 19 1999 1831 1840
32. W. Du, and G.C. Prendergast Geranylgeranylated RhoB mediates suppression of human tumor cell growth by farnesyltransferase inhibitors Cancer Res. 59 1999 5492 5496
33. M.E. Engel, P.K. Datta, and H.L. Moses RhoB is stabilized by transforming growth factor beta and antagonizes transcriptional activation J. Biol. Chem. 273 1998 9921 9926
34. S. Etienne-Manneville, and A. Hall Rho GTPases in cell biology Nature 420 2002 629 635 10.1038/nature01148
35. M.-A. Forget, R.R. Desrosiers, M. Del, R. Moumdjian, D. Shedid, F. Berthelet, and R. Béliveau The expression of rho proteins decreases with human brain tumor progression: potential tumor markers Clin. Exp. Metastasis 19 2002 9 15
36. G. Fritz, I. Just, and B. Kaina Rho GTPases are over-expressed in human tumors Int. J. Cancer 81 1999 682 687 10.1002/(SICI)1097-0215(19990531)81:5<682::AID-IJC2>3.0.CO;2-B
37. G. Fritz, and B. Kaina rhoB encoding a UV-inducible Ras-related small GTP-binding protein is regulated by GTPases of the Rho family and independent of JNK, ERK, and p38 MAP kinase J. Biol. Chem. 272 1997 30637 30644
38. G. Fritz, and B. Kaina Ras-related GTPase RhoB forces alkylation-induced apoptotic cell death Biochem. Biophys. Res. Commun. 268 2000 784 789 10.1006/bbrc.2000.2211
39. G. Fritz, and B. Kaina Rho GTPases: promising cellular targets for novel anticancer drugs Curr. Cancer Drug Targets 6 2006 1 14
40. G. Fritz, B. Kaina, and K. Aktories The ras-related small GTP-binding protein RhoB is immediate-early inducible by DNA damaging treatments J. Biol. Chem. 270 1995 25172 25177
41. K. Fukui, S. Tamura, A. Wada, Y. Kamada, Y. Sawai, K. Imanaka, T. Kudara, I. Shimomura, and N. Hayashi Expression and prognostic role of RhoA GTPases in hepatocellular carcinoma J. Cancer Res. Clin. Oncol. 132 2006 627 633 10.1007/s00432-006-0107-7
42. L. Galluzzi, L. Senovilla, I. Vitale, J. Michels, I. Martins, O. Kepp, M. Castedo, and G. Kroemer Molecular mechanisms of cisplatin resistance Oncogene 31 2012 1869 1883 10.1038/onc.2011.384
43. L. Galluzzi, I. Vitale, J. Michels, C. Brenner, G. Szabadkai, A. Harel-Bellan, M. Castedo, and G. Kroemer Systems biology of cisplatin resistance: past, present and future Cell Death Dis. 5 2014 e1257 10.1038/cddis.2013.428
44. R. Garcia-Mata, E. Boulter, and K. Burridge The "invisible hand": regulation of RHO GTPases by RHOGDIs Nat. Rev. Mol. Cell Biol. 12 2011 493 504 10.1038/nrm3153
45. T. Gómez del Pulgar, S.A. Benitah, P.F. Valerón, C. Espina, and J.C. Lacal Rho GTPase expression in tumourigenesis: evidence for a significant link BioEssays 27 2005 602 613 10.1002/bies.20238
46. W. Gou, Y. Zhao, H. Lu, X. Yang, Y. Xiu, S. Zhao, J. Liu, Z. Zhu, H. Sun, Y. Liu, F. Xu, Y. Takano, and H. Zheng The role of RhoC in epithelial-to-mesenchymal transition of ovarian carcinoma cells BMC Cancer 14 2014 477 10.1186/1471-2407-14-477
47. C. Guilluy, R. Garcia-Mata, and K. Burridge Rho protein crosstalk: another social network? Trends Cell Biol. 21 2011 718 726 10.1016/j.tcb.2011.08.002
48. A. Hakem, O. Sanchez-Sweatman, A. You-Ten, G. Duncan, A. Wakeham, R. Khokha, and T.W. Mak RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis Genes Dev. 19 2005 1974 1979 10.1101/gad.1310805
49. S. Hanna, B. Khalil, A. Nasrallah, B.A. Saykali, R. Sobh, S. Nasser, and M. El-Sibai StarD13 is a tumor suppressor in breast cancer that regulates cell motility and invasion Int. J. Oncol. 44 2014 1499 1511 10.3892/ijo.2014.2330
50. G.M. Hatch, Y. Gu, F.Y. Xu, J. Cizeau, S. Neumann, J.-S. Park, S. Loewen, and M.R.A. Mowat StARD13(Dlc-2) RhoGap mediates ceramide activation of phosphatidylglycerolphosphate synthase and drug response in Chinese hamster ovary cells Mol. Biol. Cell 19 2008 1083 1092 10.1091/mbc.E06-08-0737
51. D.M. Hayes, E. Cvitkovic, R.B. Golbey, E. Scheiner, L. Helson, and I.H. Krakoff High dose cis-platinum diammine dichloride: amelioration of renal toxicity by mannitol diuresis Cancer 39 1977 1372 1381
52. H. He, M. Yim, K.H. Liu, S.C. Cody, A. Shulkes, and G.S. Baldwin Involvement of G proteins of the Rho family in the regulation of Bcl-2-like protein expression and caspase 3 activation by Gastrins Cell. Signal. 20 2008 83 93 10.1016/j.cellsig.2007.08.018
53. A. Horiuchi, T. Imai, C. Wang, S. Ohira, Y. Feng, T. Nikaido, and I. Konishi Up-regulation of small GTPases, RhoA and RhoC, is associated with tumor progression in ovarian carcinoma Lab. Investig. 83 2003 861 870
54. M. Huang, and G.C. Prendergast RhoB in cancer suppression Histol. Histopathol. 21 2006 213 218
55. T. Igishi, M. Mikami, K. Murakami, S. Matsumoto, Y. Shigeoka, H. Nakanishi, K. Yasuda, J.S. Gutkind, Y. Hitsuda, and E. Shimizu Enhancement of cisplatin-induced cytotoxicity by ROCK inhibitor through suppression of focal adhesion kinase-independent mechanism in lung carcinoma cells Int. J. Oncol. 23 2003 1079 1085
56. D.E. Jaalouk, and J. Lammerding Mechanotransduction gone awry Nat. Rev. Mol. Cell Biol. 10 2009 63 73 10.1038/nrm2597
57. A.B. Jaffe, and A. Hall Rho GTPases: biochemistry and biology Annu. Rev. Cell Dev. Biol. 21 2005 247 269 10.1146/annurev.cellbio.21.020604.150721
58. L. Jiang, X. Liu, A. Kolokythas, J. Yu, A. Wang, C.E. Heidbreder, F. Shi, and X. Zhou Downregulation of the Rho GTPase signaling pathway is involved in the microRNA-138-mediated inhibition of cell migration and invasion in tongue squamous cell carcinoma Int. J. Cancer 127 2010 505 512 10.1002/ijc.25320
59. M. Karin, Y. Cao, F.R. Greten, and Z.-W. Li NF-kappaB in cancer: from innocent bystander to major culprit Nat. Rev. Cancer 2 2002 301 310 10.1038/nrc780
60. R. Karlsson, E.D. Pedersen, Z. Wang, and C. Brakebusch Rho GTPase function in tumorigenesis Biochim. Biophys. Acta 1796 2009 91 98 10.1016/j.bbcan.2009.03.003
61. J.E. Karp, and J.E. Lancet Development of farnesyltransferase inhibitors for clinical cancer therapy: focus on hematologic malignancies Cancer Invest. 25 2007 484 494 10.1080/07357900701359437
62. L. Kelland The resurgence of platinum-based cancer chemotherapy Nat. Rev. Cancer 7 2007 573 584 10.1038/nrc2167
63. R. Khosravi-Far, P.A. Solski, G.J. Clark, M.S. Kinch, and C.J. Der Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation Mol. Cell. Biol. 15 1995 6443 6453
64. B. Köberle, M.T. Tomicic, S. Usanova, and B. Kaina Cisplatin resistance: preclinical findings and clinical implications Biochim. Biophys. Acta 1806 2010 172 182 10.1016/j.bbcan.2010.07.004
65. P.A. Konstantinopoulos, M.V. Karamouzis, and A.G. Papavassiliou Post-translational modifications and regulation of the RAS superfamily of GTPases as anticancer targets Nat. Rev. Drug Discov. 6 2007 541 555 10.1038/nrd2221
66. C.M. Kraning-Rush, J.P. Califano, and C.A. Reinhart-King Cellular traction stresses increase with increasing metastatic potential PLoS ONE 7 2012 e32572 10.1371/journal.pone.0032572
67. Y. Kureishi, S. Kobayashi, M. Amano, K. Kimura, H. Kanaide, T. Nakano, K. Kaibuchi, and M. Ito Rho-associated kinase directly induces smooth muscle contraction through myosin light chain phosphorylation J. Biol. Chem. 272 1997 12257 12260
68. J. Lane, T.A. Martin, G. Watkins, R.E. Mansel, and W.G. Jiang The expression and prognostic value of ROCK I and ROCK II and their role in human breast cancer Int. J. Oncol. 33 2008 585 593
69. G. Lazer, and S. Katzav Guanine nucleotide exchange factors for RhoGTPases: good therapeutic targets for cancer therapy? Cell. Signal. 23 2011 969 979 10.1016/j.cellsig.2010.10.022
70. P.F. Lebowitz, J.P. Davide, and G.C. Prendergast Evidence that farnesyltransferase inhibitors suppress Ras transformation by interfering with Rho activity Mol. Cell. Biol. 15 1995 6613 6622
71. E.C. Lessey, C. Guilluy, and K. Burridge From mechanical force to RhoA activation Biochemistry (Mosc.) 51 2012 7420 7432 10.1021/bi300758e
72. A.X. Liu, G.J. Cerniglia, E.J. Bernhard, and G.C. Prendergast RhoB is required to mediate apoptosis in neoplastically transformed cells after DNA damage Proc. Natl. Acad. Sci. U. S. A. 98 2001 6192 6197 10.1073/pnas.111137198
73. A.X. Liu, N. Rane, J.P. Liu, and G.C. Prendergast RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells Mol. Cell. Biol. 21 2001 6906 6912 10.1128/MCB.21.20.6906-6912.2001
74. C.-A. Liu, M.-J. Wang, C.-W. Chi, C.-W. Wu, and J.-Y. Chen Rho/Rhotekin-mediated NF-kappaB activation confers resistance to apoptosis Oncogene 23 2004 8731 8742 10.1038/sj.onc.1208106
75. M. Liu, F. Bi, X. Zhou, and Y. Zheng Rho GTPase regulation by miRNAs and covalent modifications Trends Cell Biol. 22 2012 365 373 10.1016/j.tcb.2012.04.004
76. S. Liu, R.H. Goldstein, E.M. Scepansky, and M. Rosenblatt Inhibition of rho-associated kinase signaling prevents breast cancer metastasis to human bone Cancer Res. 69 2009 8742 8751 10.1158/0008-5472.CAN-09-1541
77. A.X. Liu, W. Du, J.P. Liu, T.M. Jessell, and G.C. Prendergast RhoB alteration is necessary for apoptotic and antineoplastic responses to farnesyltransferase inhibitors Mol. Cell. Biol. 20 2000 6105 6113
78. X. Liu, E. Choy, F.J. Hornicek, S. Yang, C. Yang, D. Harmon, H. Mankin, and Z. Duan ROCK1 as a potential therapeutic target in osteosarcoma J. Orthop. Res. 29 2011 1259 1266 10.1002/jor.21403
79. X.R. Li, F. Ji, J. Ouyang, W. Wu, L.Y. Qian, and K.Y. Yang Overexpression of RhoA is associated with poor prognosis in hepatocellular carcinoma Eur. J. Surg. Oncol. 32 2006 1130 1134 10.1016/j.ejso.2006.05.012
80. A. Lombet, V. Zujovic, M. Kandouz, C. Billardon, S. Carvajal-Gonzalez, A. Gompel, and W. Rostène Resistance to induced apoptosis in the human neuroblastoma cell line SK-N-SH in relation to neuronal differentiation. Role of Bcl-2 protein family Eur. J. Biochem. 268 2001 1352 1362
81. K. Mamouni, A. Cristini, J. Guirouilh-Barbat, S. Monferran, A. Lemarié, J.-C. Faye, B.S. Lopez, G. Favre, and O. Sordet RhoB promotes γH2AX dephosphorylation and DNA double-strand break repair Mol. Cell. Biol. 34 2014 3144 3155 10.1128/MCB.01525-13
82. P.H. Maxwell, M.S. Wiesener, G.W. Chang, S.C. Clifford, E.C. Vaux, M.E. Cockman, C.C. Wykoff, C.W. Pugh, E.R. Maher, and P.J. Ratcliffe The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis Nature 399 1999 271 275 10.1038/20459
83. J. Mazieres, T. Antonia, G. Daste, C. Muro-Cacho, D. Berchery, V. Tillement, A. Pradines, S. Sebti, and G. Favre Loss of RhoB expression in human lung cancer progression Clin. Cancer Res. 10 2004 2742 2750
84. D.J. McGrail, Q.M.N. Kieu, and M.R. Dawson The malignancy of metastatic ovarian cancer cells is increased on soft matrices through a mechanosensitive Rho-ROCK pathway J. Cell Sci. 127 2014 2621 2626 10.1242/jcs.144378
85. C. Médale-Giamarchi, I. Lajoie-Mazenc, E. Malissein, E. Meunier, B. Couderc, Y. Bergé, T. Filleron, L. Keller, C. Marty, M. Lacroix-Triki, F. Dalenc, S.F. Doisneau-Sixou, and G. Favre RhoB modifies estrogen responses in breast cancer cells by influencing expression of the estrogen receptor Breast Cancer Res. 15 2013 R6 10.1186/bcr3377
86. D. Meiri, M.A. Greeve, A. Brunet, D. Finan, C.D. Wells, J. LaRose, and R. Rottapel Modulation of Rho guanine exchange factor Lfc activity by protein kinase A-mediated phosphorylation Mol. Cell. Biol. 29 2009 5963 5973 10.1128/MCB.01268-08
87. D. Meiri, C.B. Marshall, M.A. Greeve, B. Kim, M. Balan, F. Suarez, C. Bakal, C. Wu, J. Larose, N. Fine, M. Ikura, and R. Rottapel Mechanistic insight into the microtubule and actin cytoskeleton coupling through dynein-dependent RhoGEF inhibition Mol. Cell 45 2012 642 655 10.1016/j.molcel.2012.01.027
88. D. Meiri, C.B. Marshall, D. Mokady, J. LaRose, M. Mullin, A.-C. Gingras, M. Ikura, and R. Rottapel Mechanistic insight into GPCR-mediated activation of the microtubule-associated RhoA exchange factor GEF-H1 Nat. Commun. 5 2014 4857 10.1038/ncomms5857
89. D. Michaelson, J. Silletti, G. Murphy, P. D'Eustachio, M. Rush, and M.R. Philips Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding J. Cell Biol. 152 2001 111 126
90. T. Miki, C.L. Smith, J.E. Long, A. Eva, and T.P. Fleming Oncogene ect2 is related to regulators of small GTP-binding proteins Nature 362 1993 462 465 10.1038/362462a0
91. S. Monferran, N. Skuli, C. Delmas, G. Favre, J. Bonnet, E. Cohen-Jonathan-Moyal, and C. Toulas Alphavbeta3 and alphavbeta5 integrins control glioma cell response to ionising radiation through ILK and RhoB Int. J. Cancer 123 2008 357 364 10.1002/ijc.23498
92. M. Morgan-Fisher, U.M. Wewer, and A. Yoneda Regulation of ROCK activity in cancer J. Histochem. Cytochem. 61 2013 185 198 10.1369/0022155412470834
93. P.J. Morin Drug resistance and the microenvironment: nature and nurture Drug Resist. Updat. 6 2003 169 172
94. J.A. Moscow, R. He, J.R. Gnarra, T. Knutsen, Y. Weng, W.P. Zhao, J. Whang-Peng, W.M. Linehan, and K.H. Cowan Examination of human tumors for rhoA mutations Oncogene 9 1994 189 194
95. K. Nakamichi, M. Saiki, H. Kitani, Y. Kuboyama, K. Morimoto, M. Takayama-Ito, and I. Kurane Roles of NF-kappaB and MAPK signaling pathways in morphological and cytoskeletal responses of microglia to double-stranded RNA Neurosci. Lett. 414 2007 222 227 10.1016/j.neulet.2006.12.058
96. T. Nakamura, Y. Kato, H. Fuji, T. Horiuchi, Y. Chiba, and K. Tanaka E-cadherin-dependent intercellular adhesion enhances chemoresistance Int. J. Mol. Med. 12 2003 693 700
97. S. Narumiya, M. Tanji, and T. Ishizaki Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion Cancer Metastasis Rev. 28 2009 65 76 10.1007/s10555-008-9170-7
98. A. Nasrallah, B. Saykali, S. Al Dimassi, N. Khoury, S. Hanna, and M. El-Sibai Effect of StarD13 on colorectal cancer proliferation, motility and invasion Oncol. Rep. 31 2014 505 515 10.3892/or.2013.2861
99. C.D. Nobes, and A. Hall Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia Cell 81 1995 53 62
100. T. Ohta, T. Takahashi, T. Shibuya, M. Amita, N. Henmi, K. Takahashi, and H. Kurachi Inhibition of the Rho/ROCK pathway enhances the efficacy of cisplatin through the blockage of hypoxia-inducible factor-1α in human ovarian cancer cells Cancer Biol. Ther. 13 2012 25 33 10.4161/cbt.13.1.18440
101. L.V. Parise, J. Lee, and R.L. Juliano New aspects of integrin signaling in cancer Semin. Cancer Biol. 10 2000 407 414 10.1006/scbi.2000.0337
102. B. Park, N.T. Nguyen, P. Dutt, K.D. Merdek, M. Bashar, P. Sterpetti, A. Tosolini, J.R. Testa, and D. Toksoz Association of Lbc Rho guanine nucleotide exchange factor with alpha-catenin-related protein, alpha-catulin/CTNNAL1, supports serum response factor activation J. Biol. Chem. 277 2002 45361 45370 10.1074/jbc.M202447200
103. M.J. Paszek, N. Zahir, K.R. Johnson, J.N. Lakins, G.I. Rozenberg, A. Gefen, C.A. Reinhart-King, S.S. Margulies, M. Dembo, D. Boettiger, D.A. Hammer, and V.M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 8 2005 241 254 10.1016/j.ccr.2005.08.010
104. V. Paulitschke, V. Haudek-Prinz, J. Griss, W. Berger, T. Mohr, H. Pehamberger, R. Kunstfeld, and C. Gerner Functional classification of cellular proteome profiles support the identification of drug resistance signatures in melanoma cells J. Proteome Res. 12 2013 3264 3276 10.1021/pr400124w
105. J.-Y. Pillé, C. Denoyelle, J. Varet, J.-R. Bertrand, J. Soria, P. Opolon, H. Lu, L.-L. Pritchard, J.-P. Vannier, C. Malvy, C. Soria, and H. Li Anti-RhoA and anti-RhoC siRNAs inhibit the proliferation and invasiveness of MDA-MB-231 breast cancer cells in vitro and in vivo Mol. Ther. 11 2005 267 274 10.1016/j.ymthe.2004.08.029
106. G.C. Prendergast Farnesyltransferase inhibitors: antineoplastic mechanism and clinical prospects Curr. Opin. Cell Biol. 12 2000 166 173
107. G.C. Prendergast Actin' up: RhoB in cancer and apoptosis Nat. Rev. Cancer 1 2001 162 168 10.1038/35101096
108. Y.-W. Qiang, Y. Endo, J.S. Rubin, and S. Rudikoff Wnt signaling in B-cell neoplasia Oncogene 22 2003 1536 1545 10.1038/sj.onc.1206239
109. Y.-W. Qiang, L. Yao, G. Tosato, and S. Rudikoff Insulin-like growth factor I induces migration and invasion of human multiple myeloma cells Blood 103 2004 301 308 10.1182/blood-2003-06-2066
110. N. Rath, and M.F. Olson Rho-associated kinases in tumorigenesis: re-considering ROCK inhibition for cancer therapy EMBO Rep. 13 2012 900 908 10.1038/embor.2012.127
111. R. Rattan, S. Giri, A.K. Singh, and I. Singh Rho/ROCK pathway as a target of tumor therapy J. Neurosci. Res. 83 2006 243 255 10.1002/jnr.20707
112. T. Reid, T. Furuyashiki, T. Ishizaki, G. Watanabe, N. Watanabe, K. Fujisawa, N. Morii, P. Madaule, and S. Narumiya Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain J. Biol. Chem. 271 1996 13556 13560
113. Y. Ren, R. Li, Y. Zheng, and H. Busch Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases J. Biol. Chem. 273 1998 34954 34960
114. C. Reynaud, S. Fabre, and P. Jalinot The PDZ protein TIP-1 interacts with the Rho effector rhotekin and is involved in Rho signaling to the serum response element J. Biol. Chem. 275 2000 33962 33968 10.1074/jbc.M000465200
115. A.J. Ridley Rho family proteins: coordinating cell responses Trends Cell Biol. 11 2001 471 477
116. A.J. Ridley Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking Trends Cell Biol. 16 2006 522 529 10.1016/j.tcb.2006.08.006
117. A.J. Ridley RhoA, RhoB and RhoC have different roles in cancer cell migration J. Microsc. 251 2013 242 249 10.1111/jmi.12025
118. A.J. Ridley, and A. Hall The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors Cell 70 1992 389 399
119. A.J. Ridley, H.F. Paterson, C.L. Johnston, D. Diekmann, and A. Hall The small GTP-binding protein rac regulates growth factor-induced membrane ruffling Cell 70 1992 401 410
120. S. Rihet, P. Vielh, J. Camonis, B. Goud, S. Chevillard, and J. de Gunzburg Mutation status of genes encoding RhoA, Rac1, and Cdc42 GTPases in a panel of invasive human colorectal and breast tumors J. Cancer Res. Clin. Oncol. 127 2001 733 738
121. M. Rohde, J. Richter, M. Schlesner, M.J. Betts, A. Claviez, B.R. Bonn, M. Zimmermann, C. Damm-Welk, R.B. Russell, A. Borkhardt, R. Eils, J.I. Hoell, M. Szczepanowski, I. Oschlies, W. Klapper, B. Burkhardt, R. Siebert, I.C.G.C. German, and MMML-Seq-Project and the NHL-BFM Study Group Recurrent RHOA mutations in pediatric Burkitt lymphoma treated according to the NHL-BFM protocols Genes. Chromosomes Cancer 53 2014 911 916 10.1002/gcc.22202
122. B. Rosenberg Platinum coordination complexes in cancer chemotherapy Naturwissenschaften 60 1973 399 406 10.1007/BF00623551
123. A. Routhier, M. Astuccio, D. Lahey, N. Monfredo, A. Johnson, W. Callahan, A. Partington, K. Fellows, L. Ouellette, S. Zhidro, C. Goodrow, A. Smith, K. Sullivan, P. Simone, L. Le, B. Vezuli, M. Zohni, E. West, D. Gleason, and B. Bryan Pharmacological inhibition of Rho-kinase signaling with Y-27632 blocks melanoma tumor growth Oncol. Rep. 23 2010 861 867
124. E. Sahai, and C.J. Marshall RHO-GTPases and cancer Nat. Rev. Cancer 2 2002 133 142 10.1038/nrc725
125. M. Sakamoto, A. Kondo, K. Kawasaki, T. Goto, H. Sakamoto, K. Miyake, Y. Koyamatsu, T. Akiya, H. Iwabuchi, T. Muroya, K. Ochiai, T. Tanaka, Y. Kikuchi, and Y. Tenjin Analysis of gene expression profiles associated with cisplatin resistance in human ovarian cancer cell lines and tissues using cDNA microarray Hum. Cell 14 2001 305 315
126. M.S. Samuel, J.I. Lopez, E.J. McGhee, D.R. Croft, D. Strachan, P. Timpson, J. Munro, E. Schröder, J. Zhou, V.G. Brunton, N. Barker, H. Clevers, O.J. Sansom, K.I. Anderson, V.M. Weaver, and M.F. Olson Actomyosin-mediated cellular tension drives increased tissue stiffness and β-catenin activation to induce epidermal hyperplasia and tumor growth Cancer Cell 19 2011 776 791 10.1016/j.ccr.2011.05.008
127. H.A. Sansing, A. Sarkeshik, J.R. Yates, V. Patel, J.S. Gutkind, K.M. Yamada, and A.L. Berrier Integrin αβ1, αvβ, α6β effectors p130Cas, Src and talin regulate carcinoma invasion and chemoresistance Biochem. Biophys. Res. Commun. 406 2011 171 176 10.1016/j.bbrc.2011.01.109
128. K. Sawada, K.i. Morishige, M. Tahara, Y. Ikebuchi, R. Kawagishi, K. Tasaka, and Y. Murata Lysophosphatidic acid induces focal adhesion assembly through Rho/Rho-associated kinase pathway in human ovarian cancer cells Gynecol. Oncol. 87 2002 252 259
129. L. Sepp-Lorenzino, G. Tjaden, M.M. Moasser, N. Timaul, Z. Ma, N.E. Kohl, J.B. Gibbs, A. Oliff, N. Rosen, and H.I. Scher Farnesyl:protein transferase inhibitors as potential agents for the management of human prostate cancer Prostate Cancer Prostatic Dis. 4 2001 33 43 10.1038/sj.pcan.4500491
130. S. Sharma, C. Santiskulvong, L.A. Bentolila, J. Rao, O. Dorigo, and J.K. Gimzewski Correlative nanomechanical profiling with super-resolution F-actin imaging reveals novel insights into mechanisms of cisplatin resistance in ovarian cancer cells Nanomed. Nanotechnol. Biol. Med. 8 2012 757 766 10.1016/j.nano.2011.09.015
131. S. Sharma, C. Santiskulvong, J. Rao, J.K. Gimzewski, and O. Dorigo The role of Rho GTPase in cell stiffness and cisplatin resistance in ovarian cancer cells Integr. Biol. Quant. Biosci. Nano Macro 6 2014 611 617 10.1039/c3ib40246k
132. D.-W. Shen, L.M. Pouliot, M.D. Hall, and M.M. Gottesman Cisplatin resistance: a cellular self-defense mechanism resulting from multiple epigenetic and genetic changes Pharmacol. Rev. 64 2012 706 721 10.1124/pr.111.005637
133. K. Shen, C.E. Tolbert, C. Guilluy, V.S. Swaminathan, M.E. Berginski, K. Burridge, R. Superfine, and S.L. Campbell The vinculin C-terminal hairpin mediates F-actin bundle formation, focal adhesion, and cell mechanical properties J. Biol. Chem. 286 2011 45103 45115 10.1074/jbc.M111.244293
134. J. Shi, and L. Wei Rho kinase in the regulation of cell death and survival Arch. Immunol. Ther. Exp. (Warsz.) 55 2007 61 75 10.1007/s00005-007-0009-7
135. Z.H. Siddik Cisplatin: mode of cytotoxic action and molecular basis of resistance Oncogene 22 2003 7265 7279 10.1038/sj.onc.1206933
136. K.S.M. Smalley, and T.G. Eisen Farnesyl transferase inhibitor SCH66336 is cytostatic, pro-apoptotic and enhances chemosensitivity to cisplatin in melanoma cells Int. J. Cancer 105 2003 165 175 10.1002/ijc.11064
137. A.V. Somlyo, D. Bradshaw, S. Ramos, C. Murphy, C.E. Myers, and A.P. Somlyo Rho-kinase inhibitor retards migration and in vivo dissemination of human prostate cancer cells Biochem. Biophys. Res. Commun. 269 2000 652 659 10.1006/bbrc.2000.2343
138. M.C. Srougi, and K. Burridge The nuclear guanine nucleotide exchange factors Ect2 and Net1 regulate RhoB-mediated cell death after DNA damage PLoS ONE 6 2011 e17108 10.1371/journal.pone.0017108
139. P. Sterpetti, L. Marucci, C. Candelaresi, D. Toksoz, G. Alpini, L. Ugili, G.S. Baroni, G. Macarri, and A. Benedetti Cell proliferation and drug resistance in hepatocellular carcinoma are modulated by Rho GTPase signals Am. J. Physiol. Gastrointest. Liver Physiol. 290 2006 G624 G632 10.1152/ajpgi.00128.2005
140. C.A. Street, A.A. Routhier, C. Spencer, A.L. Perkins, K. Masterjohn, A. Hackathorn, J. Montalvo, E.A. Dennstedt, and B.A. Bryan Pharmacological inhibition of Rho-kinase (ROCK) signaling enhances cisplatin resistance in neuroblastoma cells Int. J. Oncol. 37 2010 1297 1305
141. H. Sun, J. Ren, Q. Zhu, F.-Z. Kong, L. Wu, and B.-R. Pan Effects of lysophosphatidic acid on human colon cancer cells and its mechanisms of action World J. Gastroenterol. 15 2009 4547 4555
142. J. Sun, M.A. Blaskovich, D. Knowles, Y. Qian, J. Ohkanda, R.D. Bailey, A.D. Hamilton, and S.M. Sebti Antitumor efficacy of a novel class of non-thiol-containing peptidomimetic inhibitors of farnesyltransferase and geranylgeranyltransferase I: combination therapy with the cytotoxic agents cisplatin, Taxol, and gemcitabine Cancer Res. 59 1999 4919 4926
143. H. Suwa, G. Ohshio, T. Imamura, G. Watanabe, S. Arii, M. Imamura, S. Narumiya, H. Hiai, and M. Fukumoto Overexpression of the rhoC gene correlates with progression of ductal adenocarcinoma of the pancreas Br. J. Cancer 77 1998 147 152
144. K. Takata, K.-I. Morishige, T. Takahashi, K. Hashimoto, S. Tsutsumi, L. Yin, T. Ohta, J. Kawagoe, K. Takahashi, and H. Kurachi Fasudil-induced hypoxia-inducible factor-1alpha degradation disrupts a hypoxia-driven vascular endothelial growth factor autocrine mechanism in endothelial cells Mol. Cancer Ther. 7 2008 1551 1561 10.1158/1535-7163.MCT-07-0428
145. D. Toksoz, and D.A. Williams Novel human oncogene lbc detected by transfection with distinct homology regions to signal transduction products Oncogene 9 1994 621 628
146. K. Ueno, H. Hirata, S. Majid, S. Yamamura, V. Shahryari, Z.L. Tabatabai, Y. Hinoda, and R. Dahiya Tumor suppressor microRNA-493 decreases cell motility and migration ability in human bladder cancer cells by downregulating RhoC and FZD4 Mol. Cancer Ther. 11 2012 244 253 10.1158/1535-7163.MCT-11-0592
147. S. Valastyan, N. Benaich, A. Chang, F. Reinhardt, and R.A. Weinberg Concomitant suppression of three target genes can explain the impact of a microRNA on metastasis Genes Dev. 23 2009 2592 2597 10.1101/gad.1832709
148. K.L. Van Golen, Z.F. Wu, X.T. Qiao, L.W. Bao, and S.D. Merajver RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype Cancer Res. 60 2000 5832 5838
149. K.A. Varker, S.H. Phelps, M.M. King, and C.L. Williams The small GTPase RhoA has greater expression in small cell lung carcinoma than in non-small cell lung carcinoma and contributes to their unique morphologies Int. J. Oncol. 22 2003 671 681
150. F.M. Vega, and A.J. Ridley SnapShot: Rho family GTPases Cell 129 2007 1430 10.1016/j.cell.2007.06.021
151. W. Wang, F. Wu, F. Fang, Y. Tao, and L. Yang Inhibition of invasion and metastasis of hepatocellular carcinoma cells via targeting RhoC in vitro and in vivo Clin. Cancer Res. 14 2008 6804 6812 10.1158/1078-0432.CCR-07-4820
152. W. Wang, L.-Y. Yang, G.-W. Huang, W.-Q. Lu, Z.-L. Yang, J.-Q. Yang, and H.-L. Liu Genomic analysis reveals RhoC as a potential marker in hepatocellular carcinoma with poor prognosis Br. J. Cancer 90 2004 2349 2355 10.1038/sj.bjc.6601749
153. W. Wang, L.-Y. Yang, Z.-L. Yang, G.-W. Huang, and W.-Q. Lu Expression and significance of RhoC gene in hepatocellular carcinoma World J. Gastroenterol. 9 2003 1950 1953
154. K. Watanabe, M. Ueno, D. Kamiya, A. Nishiyama, M. Matsumura, T. Wataya, J.B. Takahashi, S. Nishikawa, S. Nishikawa, K. Muguruma, and Y. Sasai A ROCK inhibitor permits survival of dissociated human embryonic stem cells Nat. Biotechnol. 25 2007 681 686 10.1038/nbt1310
155. N. Watanabe, T. Kato, A. Fujita, T. Ishizaki, and S. Narumiya Cooperation between mDia1 and ROCK in Rho-induced actin reorganization Nat. Cell Biol. 1 1999 136 143 10.1038/11056
156. J. Wesierska-Gadek, M.P. Kramer, and G. Schmid A combined treatment of HeLa cells with the farnesyl protein transferase inhibitor L-744,832 and cisplatin significantly increases the therapeutic effect as compared to cisplatin monotherapy J. Cell. Biochem. 104 2008 189 201 10.1002/jcb.21612
157. I. Whitehead, H. Kirk, C. Tognon, G. Trigo-Gonzalez, and R. Kay Expression cloning of lfc, a novel oncogene with structural similarities to guanine nucleotide exchange factors and to the regulatory region of protein kinase C J. Biol. Chem. 270 1995 18388 18395
158. C.C.-L. Wong, C.-M. Wong, E.K.-K. Tung, K. Man, and I.O.-L. Ng Rho-kinase 2 is frequently overexpressed in hepatocellular carcinoma and involved in tumor invasion Hepatology (Baltim. MD) 49 2009 1583 1594 10.1002/hep.22836
159. F. Xue, T. Takahara, Y. Yata, Q. Xia, K. Nonome, E. Shinno, M. Kanayama, S. Takahara, and T. Sugiyama Blockade of Rho/Rho-associated coiled coil-forming kinase signaling can prevent progression of hepatocellular carcinoma in matrix metalloproteinase-dependent manner Hepatol. Res. 38 2008 810 817 10.1111/j.1872-034X.2008.00333.x
160. H. Ying, S.L. Biroc, W.-W. Li, B. Alicke, J.-A. Xuan, R. Pagila, Y. Ohashi, T. Okada, Y. Kamata, and H. Dinter The Rho kinase inhibitor fasudil inhibits tumor progression in human and rat tumor models Mol. Cancer Ther. 5 2006 2158 2164 10.1158/1535-7163.MCT-05-0440
161. H.Y. Yoo, M.K. Sung, S.H. Lee, S. Kim, H. Lee, S. Park, S.C. Kim, B. Lee, K. Rho, J.-E. Lee, K.-H. Cho, W. Kim, H. Ju, J. Kim, S.J. Kim, W.S. Kim, S. Lee, and Y.H. Ko A recurrent inactivating mutation in RHOA GTPase in angioimmunoblastic T cell lymphoma Nat. Genet. 46 2014 371 375 10.1038/ng.2916
162. T. Yoshida, M.F. Clark, and P.H. Stern The small GTPase RhoA is crucial for MC3T3-E1 osteoblastic cell survival J. Cell. Biochem. 106 2009 896 902 10.1002/jcb.22059
163. G. Zalcman, V. Closson, G. Linarès-Cruz, F. Lerebours, N. Honoré, A. Tavitian, and B. Olofsson Regulation of Ras-related RhoB protein expression during the cell cycle Oncogene 10 1995 1935 1945
164. J. Zhou, Y. Hayakawa, T.C. Wang, and A.J. Bass RhoA mutations identified in diffuse gastric cancer Cancer Cell 26 2014 9 11 10.1016/j.ccr.2014.06.022