Activated Gα13 impairs cell invasiveness through p190RhoGAP-mediated inhibition of RhoA activity

Cancer Research

Volumn 68, Issue 20, 2008, Pages 8221-8230

  Bartolomé, Rubén A ^a   Wright, Natalia ^a   Molina Ortiz, Isabel ^a   Sánchez Luque, Francisco J ^a,b   Teixidó, Joaquin ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA 13 SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; LYSOPHOSPHATIDYLCHOLINE; PROTEIN P190; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL ACTIVATION; CELL INVASION; CELL MIGRATION; CELL TYPE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LUNG METASTASIS; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCID MOUSE; STRESS FIBER; SURVIVAL;

ANIMALS; CELL LINE, TUMOR; CHEMOKINE CXCL12; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; LUNG NEOPLASMS; LYSOPHOSPHATIDYLCHOLINES; MELANOMA; MICE; MICE, SCID; NEOPLASM INVASIVENESS; PROTO-ONCOGENE PROTEINS C-VAV; REPRESSOR PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; SWISS 3T3 CELLS; THROMBOXANE A2;

EID: 54249083160     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0561     Document Type: Article

References (50)

1. Ridley AJ, Schwartz MA, Burridge K, et al. Cell migration: integrating signals from front to back. Science 2003;302:1704-9.
2. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005;21:247-69.
3. Schmidt A, Hall A. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 2002;16:1587-609.
4. Bos JL, Rehmann H, Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007;129:865-77.
5. Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2002;2:563-72.
6. Fidler IJ. The pathogenesis of cancer metastasis: the "seed and soil" hypothesis revisited. Nat Rev Cancer 2003;3:453-8.
7. Sahai E, Marshall CJ. RHO-GTPases and cancer. Nat Rev Cancer 2002;2:133-42.
8. Fritz G, Just I, Kaina B. Rho GTPases are overexpressed in human tumors. Int J Cancer 1999;81:682-7.
9. van Golen KL, Wu ZF, Qiao XT, Bao LW, Merajver SD. RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype. Cancer Res 2000;60:5832-8.
10. Clark EA, Golub TR, Lander ES, Hynes RO. Genomic analysis of metastasis reveals an essential role for RhoC. Nature 2000;406:532-5.
11. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000;18:217-42.
12. Proudfoot AE. Chemokine receptors: multifaceted therapeutic targets. Nat Rev Immunol 2002;2:106-15.
13. Muller A, Homey B, Soto H, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-6.
14. Epstein RJ. The CXCL12-4 chemotactic pathway as a target of adjuvant breast cancer therapies. Nat Rev Cancer 2004;4:901-9.
15. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004;4:540-50.
16. Miller AJ, Mihm MC, Jr. Melanoma. N Engl J Med 2006;355:51-65.
17. Robledo MM, Bartolome RA, Longo N, et al. Expression of functional chemokine receptors CXCR3 and CXCR4 on human melanoma cells. J Biol Chem 2001;276:45098-105.
18. Bartolome RA, Galvez BG, Longo N, et al. Stromal cell-derived factor-1a promotes melanoma cell invasion across basement membranes involving stimulation of membrane-type 1 matrix metalloproteinase and Rho GTPase activities. Cancer Res 2004;64:2534-43.
19. Murakami T, Maki W, Cardones AR, et al. Expression of CXC chemokine receptor-4 enhances the pulmonary metastatic potential of murine B16 melanoma cells. Cancer Res 2002;62:7328-34.
20. Bartolome RA, Molina-Ortiz I, Samaniego R, Sanchez-Mateos P, Bustelo XR, Teixido J. Activation of Vav/Rho GTPase signaling by CXCL12 controls membrane-type matrix metalloproteinase-dependent melanoma cell invasion. Cancer Res 2006;66:248-58.
21. Neves SR, Ram PT, Iyengar R. G protein pathways. Science 2002;296:1636-9.
22. Pierce KL, Premont RT, Lefkowitz RJ. Seven-transmembrane receptors. Nat Rev Mol Cell Biol 2002;3:639-50.
23. Kelly P, Casey PJ, Meigs TE. Biologic functions of the G12 subfamily of heterotrimeric g proteins: growth, migration, and metastasis. Biochemistry 2007;46:6677-87.
24. Buhl AM, Johnson NL, Dhanasekaran N, Johnson GL. G α 12 and G α 13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J Biol Chem 1995;270:24631-4.
25. Gohla A, Offermanns S, Wilkie TM, Schultz G. Differential involvement of Gα12 and Gα13 in receptor-mediated stress fiber formation. J Biol Chem 1999; 274:17901-7.
26. Kelly P, Stemmle LN, Madden JF, Fields TA, Daaka Y, Casey PJ. A role for the G12 family of heterotrimeric G proteins in prostate cancer invasion. J Biol Chem 2006;281:26483-90.
27. Kelly P, Moeller BJ, Juneja J, et al. The G12 family of heterotrimeric G proteins promotes breast cancer invasion and metastasis. Proc Natl Acad Sci U S A 2006;103:8173-8.
28. Van Muijen GN, Cornelissen LM, Jansen CF, et al. Antigen expression of metastasizing and non-metastasizing human melanoma cells xenografted into nude mice. Clin Exp Metastasis 1991;9:259-72.
29. Garcia-Bernal D, Wright N, Sotillo-Mallo E, et al. Vav1 and Rac Control Chemokine-promoted T Lymphocyte Adhesion Mediated by the Integrin {α}4{β}1. Mol Biol Cell 2005;16:3223-35.
30. Ticchioni M, Charvet C, Noraz N, et al. Signaling through ZAP-70 is required for CXCL12-mediated T-cell transendothelial migration. Blood 2002;99:3111-8.
31. Sander EE, van Delft S, ten Klooster JP, et al. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J Cell Biol 1998;14:1385-98.
32. Federman AD, Conklin BR, Schrader KA, Reed RR, Bourne HR. Hormonal stimulation of adenylyl cyclase through Gi-protein β γ subunits. Nature 1992;356:159-61.
33. Pitcher JA, Inglese J, Higgins JB, et al. Role of β γ subunits of G proteins in targeting the β-adrenergic receptor kinase to membrane-bound receptors. Science 1992;257:1264-7.
34. Settleman J, Narasimhan V, Foster LC, Weinberg RA. Molecular cloning of cDNAs encoding the GAP-associated protein p190: implications for a signaling pathway from ras to the nucleus. Cell 1992;69:539-49.
35. Tikoo A, Czekay S, Viars C, et al. p190-A, a human tumor suppressor gene, maps to the chromosomal region 19q13.3 that is reportedly deleted in some gliomas. Gene 2000;257:23-31.
36. Roof RW, Haskell MD, Dukes BD, Sherman N, Kinter M, Parsons SJ. Phosphotyrosine (p-Tyr)-dependent and -independent mechanisms of p190 RhoGAP-p120 Ras-GAP interaction: Tyr 1105 of p190, a substrate for c-Src, is the sole p-Tyr mediator of complex formation. Mol Cell Biol 1998;18:7052-63.
37. Moran MF, Polakis P, McCormick F, Pawson T, Ellis C. Protein-tyrosine kinases regulate the phosphorylation, protein interactions, subcellular distribution, and activity of p21ras GTPase-activating protein. Mol Cell Biol 1991;11:1804-12.
38. Settleman J, Albright CF, Foster LC, Weinberg RA. Association between GTPase activators for Rho and Ras families. Nature 1992;359:153-4.
39. Bustelo XR. Regulatory and signaling properties of the Vav family. Mol Cell Biol 2000;20:1461-77.
40. Offermanns S. G-proteins as transducers in trans-membrane signalling. Prog Biophys Mol Biol 2003;83:101-30.
41. Meyer zu Heringdorf D, Jakobs KH. Lysophospholipid receptors: signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim Biophys Acta 2007;1768:923-40.
42. Hirata M, Hayashi Y, Ushikubi F, et al. Cloning and expression of cDNA for a human thromboxane A2 receptor. Nature 1991;349:617-20.
43. Raychowdhury MK, Yukawa M, Collins LJ, McGrail SH, Kent KC, Ware JA. Alternative splicing produces a divergent cytoplasmic tail in the human endothelial thromboxane A2 receptor. J Biol Chem1994;269:19256-61.
44. Ridley AJ, Self AJ, Kasmi F, et al. rho family GTPase activating proteins p190, bcr and rhoGAP show distinct specificities in vitro and in vivo. EMBO J 1993;12:5151-60.
45. Lepley D, Paik JH, Hla T, Ferrer F. The G protein-coupled receptor S1P2 regulates Rho/Rho kinase pathway to inhibit tumor cell migration. Cancer Res 2005;65:3788-95.
46. Meigs TE, Fields TA, McKee DD, Casey PJ. Interaction of Gα 12 and Gα 13 with the cytoplasmic domain of cadherin provides a mechanism for β-catenin release. Proc Natl Acad Sci U S A 2001;98:519-24.
47. Wildenberg GA, Dohn MR, Carnahan RH, et al. p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 2006;127:1027-39.
48. Offermanns S, Laugwitz KL, Spicher K, Schultz G. G proteins of the G12 family are activated via thromboxane A2 and thrombin receptors in human platelets. Proc Natl Acad Sci U S A 1994;91:504-8.
49. Wolf RM, Draghi N, Liang X, et al. p190RhoGAP can act to inhibit PDGF-induced gliomas in mice: a putative tumor suppressor encoded on human chromosome 19q13.3. Genes Dev 2003;17:476-87.
50. Dorsam RT, Gutkind JS. G-protein-coupled receptors and cancer. Nat Rev Cancer 2007;7:79-94.