BRAF and RAS oncogenes regulate Rho GTPase pathways to mediate migration and invasion properties in human colon cancer cells: A comparative study

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Makrodouli, Eleni ^a   Oikonomou, Eftychia ^a   Koc, Michal ^b   Andera, Ladislav ^b   Sasazuki, Takehiko ^c   Shirasawa, Senji ^d   Pintzas, Alexander ^a  

^a INSTITUTE OF BIOLOGY   (Greece)

^b INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

^c NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^d FUKUOKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; B RAF KINASE; H RAS PROTEIN; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN CDC42; RAC1 PROTEIN; RAS PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UO 126; WORTMANNIN; BRAF PROTEIN, HUMAN; CADHERIN; PROTEIN P21; RAC1 PROTEIN, HUMAN; RHO KINASE; RHOA PROTEIN, HUMAN;

ARTICLE; CANCER GROWTH; CANCER INVASION; CARCINOMA CELL; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL STRAIN CACO 2; CELL STRUCTURE; COLON ADENOCARCINOMA; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FILOPODIUM; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYME CELL; ONCOGENE H RAS; ONCOGENE K RAS; SIGNAL TRANSDUCTION; CELL MOTION; CELL SHAPE; COLON TUMOR; COMPARATIVE STUDY; DOWN REGULATION; DRUG EFFECT; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MISSENSE MUTATION; PHYSIOLOGY; PSEUDOPODIUM; TUMOR CELL LINE;

CADHERINS; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; COLONIC NEOPLASMS; DOWN-REGULATION; ENZYME ACTIVATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE KNOCKDOWN TECHNIQUES; HUMANS; MUTATION, MISSENSE; NEOPLASM INVASIVENESS; ONCOGENE PROTEIN P21(RAS); PROTO-ONCOGENE PROTEINS B-RAF; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA1;

EID: 80053172696     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-118     Document Type: Article

References (61)

1. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990, 61:759-767. 10.1016/0092-8674(90)90186-I, 2188735.
2. Pollock CB, Shirasawa S, Sasazuki T, Kolch W, Dhillon AS. Oncogenic K-RAS is required to maintain changes in cytoskeletal organization, adhesion, and motility in colon cancer cells. Cancer Res 2005, 65:1244-1250. 10.1158/0008-5472.CAN-04-1911, 15735008.
3. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 2003, 3:11-22. 10.1038/nrc969, 12509763.
4. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, et al. Mutations of the BRAF gene in human cancer. Nature 2002, 417:949-954. 10.1038/nature00766, 12068308.
5. Klein RM, Spofford LS, Abel EV, Ortiz A, Aplin AE. B-RAF regulation of Rnd3 participates in actin cytoskeletal and focal adhesion organization. Mol Biol Cell 2008, 19:498-508. 2230594, 18045987.
6. Vega FM, Ridley AJ. Rho GTPases in cancer cell biology. FEBS Lett 2008, 582:2093-2101. 10.1016/j.febslet.2008.04.039, 18460342.
7. Fritz G, Just I, Kaina B. Rho GTPases are over-expressed in human tumors. Int J Cancer 1999, 81:682-687. 10.1002/(SICI)1097-0215(19990531)81:5<682::AID-IJC2>3.0.CO;2-B, 10328216.
8. Chan AY, Coniglio S J, Chuang YY, Michaelson D, Knaus UG, Philips MR, Symons M. Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 2005, 24:7821-7829. 10.1038/sj.onc.1208909, 16027728.
9. Gadea G, Sanz-Moreno V, Self A, Godi A, Marshall CJ. DOCK10-mediated Cdc42 activation is necessary for amoeboid invasion of melanoma cells. Curr Biol 2008, 18:1456-1465. 10.1016/j.cub.2008.08.053, 18835169.
10. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, Sahai E. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 2007, 9:1392-1400. 10.1038/ncb1658, 18037882.
11. Vial E, Sahai E, Marshall CJ. ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 2003, 4:67-79. 10.1016/S1535-6108(03)00162-4, 12892714.
12. Tolias KF, Cantley LC, Carpenter CL. Rho Family GTPases Bind to Phosphoinositide Kinases. JBC 1995, 17656-17659.
13. Jiménez C, Portela RA, Mellado M, Rodríguez-Frade JM, Collard J, Serrano A, Avila J, Carrera AC. Role of the PI3K Regulatory Subunit in the Control of Actin Organization and Cell Migration. JCB 2000, 151:249-261. 10.1083/jcb.151.2.249, 2192656, 11038173.
14. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR. Cadherin switching. J Cell Sci 2008, 121:727-735. 10.1242/jcs.000455, 18322269.
15. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J, Beug H, Grunert S. Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 2002, 156:299-313. 10.1083/jcb.200109037, 2199233, 11790801.
16. Roberts ML, Drosopoulos KG, Vasileiou I, Stricker M, Taoufik E, Maercker C, Guialis A, Alexis MN, Pintzas A. Microarray analysis of the differential transformation mediated by Kirsten and Harvey Ras oncogenes in a human colorectal adenocarcinoma cell line. Int J Cancer 2006, 118:616-627. 10.1002/ijc.21386, 16152623.
17. Joyce T, Cantarella D, Isella C, Medico E, Pintzas A. A molecular signature for Epithelial to Mesenchymal transition in a human colon cancer cell system is revealed by large-scale microarray analysis. Clin Exp Metastasis 2009, 26:569-587. 10.1007/s10585-009-9256-9, 19340593.
18. Cicchini C, Laudadio I, Citarella F, Corazzari M, Steindler C, Conigliaro A, Fantoni A, Amicone L, Tripodi M. TGFbeta-induced EMT requires focal adhesion kinase (FAK) signaling. Exp Cell Res 2008, 314:143-152. 10.1016/j.yexcr.2007.09.005, 17949712.
19. Hashimoto Y, Parsons M, Adams JC. Dual actin-bundling and protein kinase C-binding activities of fascin regulate carcinoma cell migration downstream of Rac and contribute to metastasis. Mol Biol Cell 2007, 18:4591-4602. 10.1091/mbc.E07-02-0157, 2043557, 17855511.
20. Hashimoto Y, Skacel M, Lavery IC, Mukherjee AL, Casey G, Adams JC. Prognostic significance of fascin expression in advanced colorectal cancer: an immunohistochemical study of colorectal adenomas and adenocarcinomas. BMC Cancer 2006, 6:241. 10.1186/1471-2407-6-241, 1615879, 17029629.
21. Oikonomou E, Makrodouli E, Evagelidou M, Joyce T, Probert L, Pintzas A. BRAFV600E efficient transformation and induction of MSI versus KRASG12V induction of senescence markers in human colon cancer cells. Neoplasia 2009, 11:1116-1131. 2767214, 19881948.
22. Jaffe AB, Kaji N, Durgan J, Hall A. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J Cell Biol 2008, 183:625-633. 10.1083/jcb.200807121, 2582895, 19001128.
23. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003, 30:256-268. 10.1016/S1046-2023(03)00032-X, 12798140.
24. Petersen OW, Ronnov-Jessen L, Howlett AR, Bissell MJ. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci USA 1992, 89:9064-9068. 10.1073/pnas.89.19.9064, 50065, 1384042.
25. Andreolas C, Kalogeropoulou M, Voulgari A, Pintzas A. Fra-1 regulates vimentin during Ha-RAS-induced epithelial mesenchymal transition in human colon carcinoma cells. Int J Cancer 2008, 122:1745-1756.
26. Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 2000, 148:779-790. 10.1083/jcb.148.4.779, 2169367, 10684258.
27. Nieman MT, Prudoff RS, Johnson KR, Wheelock MJ. N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J Cell Biol 1999, 147:631-644. 10.1083/jcb.147.3.631, 2151177, 10545506.
28. Shirasawa S, Furuse M, Yokoyama N, Sasazuki T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 1993, 260:85-88. 10.1126/science.8465203, 8465203.
29. Khosravi-Far R, Solski PA, Clark GJ, Kinch MS, Der CJ. Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation. Mol Cell Biol 1995, 15:6443-6453. 230895, 7565796.
30. Qiu RG, Abo A, McCormick F, Symons M. Cdc42 regulates anchorage-independent growth and is necessary for Ras transformation. Mol Cell Biol 1997, 17:3449-3458. 232198, 9154844.
31. Cox EA, Sastry SK, Huttenlocher A. Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol Biol Cell 2001, 12:265-277. 30942, 11179414.
32. Radisky DC, Levy DD, Littlepage LE, Liu H, Nelson CM, Fata JE, Leake D, Godden EL, Albertson DG, Nieto MA, Werb Z, Bissell MJ. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 2005, 436:123-127. 10.1038/nature03688, 2784913, 16001073.
33. Sanders LC, Matsumura F, Bokoch GM, de Lanerolle P. Inhibition of myosin light chain kinase by p21-activated kinase. Science 1999, 283:2083-2085. 10.1126/science.283.5410.2083, 10092231.
34. Akbar H, Cancelas J, Williams DA, Zheng J, Zheng Y. Rational design and applications of a Rac GTPase-specific small molecule inhibitor. Methods Enzymol 2006, 406:554-565.
35. Wu WJ, Hirsch DS. Mechanism of E-cadherin lysosomal degradation. Nat Rev Cancer 2009, 9:143.
36. De Bosscher K, Hill CS, Nicolás FJ. Molecular and functional consequences of Smad4 C-terminal missense mutations in colorectal tumour cells. Biochem J 2004, 379:209-16. 10.1042/BJ20031886, 1224058, 14715079.
37. Fleming YM, Ferguson GJ, Spender LC, Larsson J, Karlsson S, Ozanne BW, Grosse R, Inman GJ. TGF-beta-mediated activation of RhoA signalling is required for efficient (V12)HaRas and (V600E)BRAF transformation. Oncogene 2009, 28:983-993. 10.1038/onc.2008.449, 19079344.
38. Moustakas A, Heldin CH. Non-Smad TGF-ß signals. Journal of Cell Science 2005, 118:3573-84. 10.1242/jcs.02554, 16105881.
39. Xu J, Lamouille S, Derynck R. TGF-β-induced epithelial to mesenchymal transition. Cell Research 2009, 19:156-72. 10.1038/cr.2009.5, 19153598.
40. Kuroda S, Fukata M, Nakagawa M, Fujii K, Nakamura T, Ookubo T, Izawa I, Nagase T, Nomura N, Tani H, Shoji I, Matsuura Y, Yonehara S, Kaibuchi K. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin- mediated cell-cell adhesion. Science 1998, 281:832-835.
41. Nobes CD, Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81:53-62. 10.1016/0092-8674(95)90370-4, 7536630.
42. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?. Nat Rev Cancer 2007, 7:415-428. 10.1038/nrc2131, 17508028.
43. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002, 2:442-454. 10.1038/nrc822, 12189386.
44. Du J, Jiang B, Coffey RJ, Barnard J. Raf and RhoA cooperate to transform intestinal epithelial cells and induce growth resistance to transforming growth factor beta. Mol Cancer Res 2004, 2:233-241.
45. Sumimoto H, Hirata K, Yamagata S, Miyoshi H, Miyagishi M, Taira K, Kawakami Y. Effective inhibition of cell growth and invasion of melanoma by combined suppression of BRAF (V599E) and Skp2 with lentiviral RNAi. Int J Cancer 2006, 118:472-476. 10.1002/ijc.21286, 16052531.
46. Kurokawa K, Matsuda M. Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol Biol Cell 2005, 16:4294-4303. 10.1091/mbc.E04-12-1076, 1196338, 15987744.
47. Blomquist A, Schworer G, Schablowski H, Psoma A, Lehnen M, Jakobs KH, Rumenapp U. Identification and characterization of a novel Rho-specific guanine nucleotide exchange factor. Biochem J 2000, 352(2):319-325. 10.1042/0264-6021:3520319, 1221462, 11085924.
48. Oleksy A, Opalinski L, Derewenda U, Derewenda ZS, Otlewski J. The molecular basis of RhoA specificity in the guanine nucleotide exchange factor PDZ-RhoGEF. J Biol Chem 2006, 281:32891-32897. 10.1074/jbc.M606220200, 16954208.
49. Pullikuth AK, Catling AD. ERK promotes Rho dependent focal adhesion formation by suppressing p190A RhoGAP. Mol Cell Biol 2010, 30(13):3233-48. 10.1128/MCB.01178-09, 2897570, 20439493.
50. Darenfed H, Dayanandan B, Zhang T, Hsieh SH, Fournier AE, Mandato CA. Molecular Characterization of the Effects of Y-27632. Cell Motility and the Cytoskeleton 2007, 64(2):97-109. 10.1002/cm.20168, 17009325.
51. Grewal S, Carver JG, Ridley AJ, Mardon HJ. Implantation of the human embryo requires Rac1-dependent endometrial stromal cell migration. PNAS 2008, 105(42):16189-94. 10.1073/pnas.0806219105, 2562412, 18838676.
52. Sahai E, Marshall CJ. ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nature Cell Biol 2002, 4:408-415. 10.1038/ncb796, 11992112.
53. Holeiter G, Heering J, Erlmann P, Schmid S, Jähne R, Olayioye MA. Deleted in liver cancer 1 controls cell migration through a Dia1-dependent signaling pathway. Cancer Res 2008, 68(21):8743-51. 10.1158/0008-5472.CAN-08-0984, 18974116.
54. Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, Brennwald PJ, Burridge K. Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat Cell Biol 2010, 12:477-83. 10.1038/ncb2049, 2866742, 20400958.
55. Malchinkhuu E, Sato K, Horiuchi Y, Mogi C, Ohwada S, Ishiuchi S, Saito N, Kurose H, Tomura H, Okajima F. Role of p38 mitogen-activated kinase and c-Jun terminal kinase in migration response to lysophosphatidic acid and sphingosine-1-phosphate in glioma cells. Oncogene 2005, 24:6676-6688. 10.1038/sj.onc.1208805, 16007180.
56. Shin I, Kim S, Song H, Kim HR, Moon A. H-Ras-specific activation of Rac-MKK3/6-p38 pathway: its critical role in invasion and migration of breast epithelial cells. J Biol Chem 2005, 280:14675-14683. 10.1074/jbc.M411625200, 15677464.
57. Li Q, Mattingly RR. Restoration of E-cadherin cell-cell junctions requires both expression of E-cadherin and suppression of ERK MAP kinase activation in Ras-transformed breast epithelial cells. Neoplasia 2008, 10:1444-1458. 2586695, 19048123.
58. Kwei KA, Finch JS, Ranger-Moore J, Bowden GT. The role of Rac1 in maintaining malignant phenotype of mouse skin tumor cells. Cancer Lett 2006, 231:326-338. 10.1016/j.canlet.2005.02.031, 15893875.
59. Zheng Y, Xia Y, Hawke D, Halle M, Tremblay ML, Gao X, Zhou XZ, Aldape K, Cobb MH, Xie K, He J, Lu Z. FAK phosphorylation by ERK primes ras-induced tyrosine dephosphorylation of FAK mediated by PIN1 and PTP-PEST. Mol Cell 2009, 35:11-25. 10.1016/j.molcel.2009.06.013, 2715139, 19595712.
60. Kalogeropoulou M, Voulgari A, Kostourou V, Sandaltzopoulos R, Dikstein R, Davidson I, Tora L, Pintzas A. TAF4b and Jun/AP-1 collaborate to regulate expression of Integrin α6 and cancer cell migration properties. Mol Cancer Res 2010, 8:554-568. 10.1158/1541-7786.MCR-09-0159, 20353996.
61. Voulgari A, Pintzas A. Epithelial-Mesenchymal Transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. BBA Reviews on Cancer 2009, 1796:75-90.