RhoGDIα-dependent balance between RhoA and RhoC is a key regulator of cancer cell tumorigenesis

Molecular Biology of the Cell

Volumn 22, Issue 17, 2011, Pages 3263-3275

  Giang Ho, T T ^a   Stultiens, Audrey ^a   Dubail, Johanne ^a   Lapier̀e, Charles M ^a   Nusgens, Betty V ^a   Colige, Alain C ^a   Deroanne, Christophe F ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; PROTEIN NAG 1; PROTEIN RHOC; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR ALPHA; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; TUMOR SUPPRESSOR GENE; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GROWTH DIFFERENTIATION FACTOR 15; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; OSTEONECTIN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE;

EID: 80052242837     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-01-0020     Document Type: Article

References (50)

1. Bauskin AR, Brown DA, Kuffner T, Johnen H, Luo XW, Hunter M, Breit SN (2006). Role of macrophage inhibitory cytokine-1 in tumorigenesis and diagnosis of cancer. Cancer Res 66, 4983-4986. (Pubitemid 43852864)
2. Bellovin DI, Simpson KJ, Danilov T, Maynard E, Rimm DL, Oettgen P, Mercurio AM (2006). Reciprocal regulation of RhoA and RhoC characterizes the EMT and identifies RhoC as a prognostic marker of colon carcinoma. Oncogene 25, 6959-6967. (Pubitemid 44684836)
3. Berenjeno IM, Nunez F, Bustelo XR (2007). Transcriptomal profiling of the cellular transformation induced by Rho subfamily GTPases. Oncogene 26, 4295-4305. (Pubitemid 46975793)
4. Bielek H, Anselmo A, Dermardirossian C (2009). Morphological and proliferative abnormalities in renal mesangial cells lacking RhoGDI. Cell Signal 21, 1974-1983.
5. Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, Brennwald PJ, Burridge K (2010). Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat Cell Biol 12, 477-483.
6. Carracedo A et al. (2006). The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells. Cancer Cell 9, 301-312.
7. Chen N, Ye XC, Chu K, Navone NM, Sage EH, Yu-Lee LY, Logothetis CJ, Lin SH (2007). A secreted isoform of ErbB3 promotes osteonectin expression in bone and enhances the invasiveness of prostate cancer cells. Cancer Res 67, 6544-6548. (Pubitemid 47105497)
8. Chiba Y, Tanabe M, Goto K, Sakai H, Misawa M (2009). Down-regulation of miR-133a contributes to up-regulation of Rhoa in bronchial smooth muscle cells. Am J Respir Crit Care Med 180, 713-719.
9. Clark DW, Mitra A, Fillmore RA, Jiang WG, Samant RS, Fodstad O, Shevde LA (2008). NUPR1 interacts with p53, transcriptionally regulates p21 and rescues breast epithelial cells from doxorubicin-induced genotoxic stress. Curr Cancer Drug Targets 8, 421-430.
10. Clark EA, Golub TR, Lander ES, Hynes RO (2000). Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406, 532-535. (Pubitemid 30625739)
11. Coso OA, Chiariello M, Yu JC, Teramoto H, Crespo P, Xu N, Miki T, Gutkind JS (1995). The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
12. DerMardirossian C, Rocklin G, Seo JY, Bokoch GM (2006). Phosphorylation of RhoGDI by Src regulates Rho GTPase binding and cytosol-membrane cycling. Mol Biol Cell 17, 4760-4768. (Pubitemid 44665745)
13. Deroanne C, Vouret-Craviari V, Wang B, Pouyssegur J (2003). EphrinA1 inactivates integrin-mediated vascular smooth muscle cell spreading via the Rac/PAK pathway. J Cell Sci 116, 1367-1376. (Pubitemid 36410674)
14. Deroanne CF, Hamelryckx D, Ho TT, Lambert CA, Catroux P, Lapiere CM, Nusgens BV (2005). Cdc42 downregulates MMP-1 expression by inhibiting the ERK1/2 pathway. J Cell Sci 118, 1173-1183. (Pubitemid 40528688)
15. Dovas A, Choi Y, Yoneda A, Multhaupt HA, Kwon SH, Kang D, Oh ES, Couchman JR (2010). Serine34 phosphorylation of RHO guanine dissociation inhibitor (RHOGDIalpha) links signaling from conventional protein kinase C to RHO GTPase in cell adhesion. J Biol Chem 285, 23296-23308.
16. Editors (2003). Whither RNAi? Nat Cell Biol 5, 489-490.
17. Fei F, Kweon SM, Haataja L, De Sepulveda P, Groffen J, Heisterkamp N (2010). The Fer tyrosine kinase regulates interactions of Rho GDP-dissociation inhibitor alpha with the small GTPase Rac. BMC Biochem 11, 48.
18. Hill CS, Wynne J, Treisman R (1995). The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81, 1159-1170.
19. Ho TT, Merajver SD, Lapiere CM, Nusgens BV, Deroanne CF (2008). RhoA-GDP regulates RhoB protein stability. Potential involvement of RhoGDIalpha. J Biol Chem 283, 21588-21598.
20. Hooi CF et al. (2006). ST7-mediated suppression of tumorigenicity of prostate cancer cells is characterized by remodeling of the extracellular matrix. Oncogene 25, 3924-3933.
21. Huelsenbeck J, Dreger SC, Gerhard R, Fritz G, Just I, Genth H (2007). Upregulation of the immediate early gene product RhoB by exoenzyme C3 from Clostridium limosum and toxin B from Clostridium difficile. Biochemistry 46, 4923-4931. (Pubitemid 46651213)
22. Iiizumi M et al. (2008). RhoC promotes metastasis via activation of the Pyk2 pathway in prostate cancer. Cancer Res 68, 7613-7620.
23. Jaffe AB, Hall A (2005). Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21, 247-269.
24. Jiang HY, Wek SA, McGrath BC, Lu D, Hai T, Harding HP, Wang X, Ron D, Cavener DR, Wek RC (2004). Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol Cell Biol 24, 1365-1377. (Pubitemid 38112196)
25. Jiang L, Liu X, Kolokythas A, Yu J, Wang A, Heidbreder CE, Shi F, Zhou X (2010). 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, 505-512.
26. Kim JS, Baek SJ, Sali T, Eling TE (2005). The conventional nonsteroidal anti-inflammatory drug sulindac sulfide arrests ovarian cancer cell growth via the expression of NAG-1/MIC-1/GDF-15. Mol Cancer Ther 4, 487-493. (Pubitemid 40443934)
27. Kleer CG, van Golen KL, Zhang Y, Wu ZF, Rubin MA, Merajver SD (2002). Characterization of RhoC expression in benign and malignant breast disease: a potential new marker for small breast carcinomas with metastatic ability. Am J Pathol 160, 579-584. (Pubitemid 34160335)
28. Kong W, Yang H, He L, Zhao JJ, Coppola D, Dalton WS, Cheng JQ (2008). MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol 28, 6773-6784.
29. Kostenko EV, Olabisi OO, Sahay S, Rodriguez PL, Whitehead IP (2006). Ccpg1, a novel scaffold protein that regulates the activity of the Rho guanine nucleotide exchange factor Dbs. Mol Cell Biol 26, 8964-8975. (Pubitemid 44851953)
30. Laboisse CL, Augeron C, Potet F (1981). Growth and differentiation of human gastrointestinal adenocarcinoma stem cells in soft agarose. Cancer Res 41, 310-315. (Pubitemid 11218835)
31. Liu A, Cerniglia GJ, Bernhard EJ, Prendergast GC (2001). RhoB is required to mediate apoptosis in neoplastically transformed cells after DNA damage. Proc Natl Acad Sci USA 98, 6192-6197.
32. Ma L, Teruya-Feldstein J, Weinberg RA (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682-688. (Pubitemid 47552092)
33. Marinissen MJ, Chiariello M, Tanos T, Bernard O, Narumiya S, Gutkind JS (2004). The small GTP-binding protein RhoA regulates c-jun by a ROCK-JNK signaling axis. Mol Cell 14, 29-41. (Pubitemid 38469907)
34. Mazieres J, Antonia T, Daste G, Muro-Cacho C, Berchery D, Tillement V, Pradines A, Sebti S, Favre G (2004). Loss of RhoB expression in human lung cancer progression. Clin Cancer Res 10, 2742-2750. (Pubitemid 38509150)
35. Mazieres J, Tillement V, Allal C, Clanet C, Bobin L, Chen Z, Sebti SM, Favre G, Pradines A (2005). Geranylgeranylated, but not farnesylated, RhoB suppresses Ras transformation of NIH-3T3 cells. Exp Cell Res 304, 354-364. (Pubitemid 40321115)
36. Michaelson D, Silletti J, Murphy G, D'Eustachio P, Rush M, Philips MR (2001). Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 152, 111-126. (Pubitemid 32102441)
37. Miralles F, Posern G, Zaromytidou AI, Treisman R (2003). Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329-342. (Pubitemid 36556115)
38. Sahai E, Marshall CJ (2002). ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat Cell Biol 4, 408-415. (Pubitemid 34746158)
39. Sander EE, ten Klooster JP, van Delft S, van der Kammen RA, Collard JG (1999). Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J Cell Biol 147, 1009-1022.
40. Shikada Y, Yoshino I, Okamoto T, Fukuyama S, Kameyama T, Maehara Y (2003). Higher expression of RhoC is related to invasiveness in non-small cell lung carcinoma. Clin Cancer Res 9, 5282-5286. (Pubitemid 37413580)
41. Shim M, Eling TE (2005). Protein kinase C-dependent regulation of NAG-1/placental bone morphogenic protein/MIC-1 expression in LNCaP prostate carcinoma cells. J Biol Chem 280, 18636-18642. (Pubitemid 41379563)
42. Simpson KJ, Dugan AS, Mercurio AM (2004). Functional analysis of the contribution of RhoA and RhoC GTPases to invasive breast carcinoma. Cancer Res 64, 8694-8701. (Pubitemid 39552085)
43. Steffan JJ, Snider JL, Skalli O, Welbourne T, Cardelli JA (2009). Na/H Exchangers and RhoA regulate acidic extracellular pH-induced lysosome trafficking in prostate cancer cells. Traffic 10, 737-753.
44. Teramoto H, Malek RL, Behbahani B, Castellone MD, Lee NH, Gutkind JS (2003). Identification of H-Ras, RhoA, Rac1 and Cdc42 responsive genes. Oncogene 22, 2689-2697. (Pubitemid 36605616)
45. Tillement V, Lajoie-Mazenc I, Casanova A, Froment C, Penary M, Tovar D, Marquez R, Monsarrat B, Favre G, Pradines A (2008). Phosphorylation of RhoB by CK1 impedes actin stress fiber organization and epidermal growth factor receptor stabilization. Exp Cell Res 314, 2811-2821.
46. Wang W, Wu F, Fang F, Tao Y, Yang L (2008). Inhibition of invasion and metastasis of hepatocellular carcinoma cells via targeting RhoC in vitro and in vivo. Clin Cancer Res 14, 6804-6812.
47. Wang W, Yang LY, Huang GW, Lu WQ, Yang ZL, Yang JQ, Liu HL (2004). Genomic analysis reveals RhoC as a potential marker in hepatocellular carcinoma with poor prognosis. Br J Cancer 90, 2349-2355. (Pubitemid 38961899)
48. Wu M, Wu ZF, Kumar-Sinha C, Chinnaiyan A, Merajver SD (2004). RhoC induces differential expression of genes involved in invasion and metastasis in MCF10A breast cells. Breast Cancer Res Treat 84, 3-12. (Pubitemid 38388855)
49. Yao H, Dashner EJ, van Golen CM, van Golen KL (2006). RhoC GTPase is required for PC-3 prostate cancer cell invasion but not motility. Oncogene 25, 2285-2296.
50. Zu K, Bihani T, Lin A, Park YM, Mori K, Ip C (2006). Enhanced selenium effect on growth arrest by BiP/GRP78 knockdown in p53-null human prostate cancer cells. Oncogene 25, 546-554. (Pubitemid 43164465)