Von Hippel-Lindau tumor suppressor protein stimulation by thrombin involves RhoA activation

International Journal of Cancer

Volumn 112, Issue 5, 2004, Pages 777-786

  Turcotte, Sandra ^a   Desrosiers, Richard R ^a   Brand, Geneviève ^a   Béliveau, Richard ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

Protease activated receptors; Renal cell carcinoma; Thrombin, RhoA; Von Hippel Lindau protein

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CYTOPLASM PROTEIN; EXOTOXIN; EXOTOXIN C3; MATRIGEL; MESSENGER RNA; PROTEIN INHIBITOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 4; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL STIMULATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; KIDNEY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; UPREGULATION; WESTERN BLOTTING;

CARCINOMA, RENAL CELL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KIDNEY NEOPLASMS; NEOPLASM INVASIVENESS; RECEPTOR, PAR-1; RHOA GTP-BINDING PROTEIN; THROMBIN; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 7244261708     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.20468     Document Type: Article

References (49)

1. Maher ER, Kaelin WG. von Hippel-Lindau disease. Medicine 1997; 76:381-91.
2. Latif F, Tory K, Gnarra J, Yao M, Duh FM, Orcutt ML, Stackhouse T, Kuzmin I, Modi W, Geil L, Schmidt L, Zhou F, et al. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993;260:1317-20.
3. Siemeister G, Weindel K, Mohrs K, Barleon B, Martiny-Baron G, Marme D. Reversion of deregulated expression of vascular endothelial growth factor in human renal carcinoma cells by von Hippel-Lindau tumor suppressor protein. Cancer Res 1996;56:2299-301.
4. Takahashi A, Sasaki H, Kim SJ, Tobisu K, Kakizoe T, Tsukamoto T, Kumamoto Y, Sugimura T, Terada M. Markedly increased amounts of messenger RNAs for vascular endothelial growth factor and placenta growth factor in renal cell carcinoma associated with angiogenesis. Cancer Res 1994;54:4233-7.
5. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-5.
6. Kondo K, Kaelin WG. The von Hippel-Lindau tumor suppressor gene. Exp Cell Res 2001;264:117-125.
7. Ohh M, Yauch RL, Lonergan KM, Whaley JM. Stemmer-Rachamimov AO, Louis DN, Gavin BJ, Kley N, Kaelin WG. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol Cell 1998;1:959-68.
8. Hergovich A, Lisztwan J, Barry R, Ballschmieter P, Frek W. Regulation of microtubule stability by the von Hippel-Lindau tumor suppressor protein pVHL. Nature Cell Biol 2003;5:64-70.
9. Kamada M, Suzuki K, Kato Y, Okuda H, Shuin T. von Hippel-Lindau protein promotes the assembly of actin and vinculin and inhibits cell motility. Cancer Res 2001;61:4184-9.
10. Turcotte S, Desrosiers RR, Béliveau R. Hypoxia up-regulates von Hippel-Lindau tumor suppressor protein through RhoA-dependent activity in renal cell carcinoma. Am J Physiol Renal Physiol 2004; 286:F338-48.
11. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000;407:258-64.
12. Zacharski LR, Constantini V. Blood coagulation activation in cancer: challenges for cancer treatment. Hamostaseol. 1995;15:14-20.
13. Coughlin SR. How the protease thrombin talks to cells. Proc Natl Acad Sci USA 1999;96:11023-7.
14. Vu T-KH, Hung DT, Wheaton VL, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 1991;64:1057-68.
15. Ishihara H, Connolly AJ, Zeng D, Kahn ML, Zheng YW, Timmons C, Tram T, Coughlin SR. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature 1997;386:502-6.
16. Xu WF, Andersen H, Whitmore TE, Presnell SR, Yee DP, Ching A, Gilbert T, Davie EW, Foster DC. Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci USA 1998;95: 6642-6.
17. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinase-activated receptors. Pharmacol Rev 2001;53:245-82.
18. 2+ mobilization. FEbS Lett 1991;288:123-28.
19. Yin Y-J, Salah Z, Maoz M, Even Ram SC, Ochayon S, Neufeld G, Katzav S, Bar-Shavit R. Oncogen transformation induces tumor angiogenesis: a role for PAR activation. FASEB J 2003;17:163-74.
20. Darmoul D, Gratio V, Devaud H, Lehy T, Laburthe M. Aberrant expression and activation of the thrombin receptor-activated receptor-1 induces cell proliferation and motility in human colon cancer cells. Am J Pathol 2003;162:1503-13.
21. van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VWM. Activation of RhoA by thrombin in endothelial hypermeability: role of Rho kinase and protein tyrosine kinase. Circ Res 2000;87:335-40.
22. Klarenbach SW, Chipiuk A, Nelson RC, Hollenberg MD, Murray AG. Differential actions of PAR2 and PAR1 in stimulating human endothelial cell exocytosis and permeability: the role of Rho-GTPases. Circ Res 2003;92:272-8.
23. Vouret-Craviari V, Bourcier C, Boulter E, Van Obberghen-Schilling E. Distinct signals via Rho GTPases and Src drive shape changes by thrombin and sphingosine-1-phosphate in endothelial cells. J Cell Sci 2002;115:2475-84.
24. Greenberg DL, Mize GJ, Takayama TK. Protease-activated receptor mediated RhoA signaling and cytoskeletal reorganization in LNCaP cells. Biochemistry 2003;42:702-9
25. Matozaki T, Nakanishi H, Takai Y. Small G-protein networks: their crosstalk and signal cascades. Cell Signal 2000;12:515-24.
26. Forget M-A, Desrosiers RR, Béliveau R. Phosphorylation states of Cdc42 and RhoA regulate their interactions with Rho GDP dissociation inhibitor and their extraction from biological membranes. Biochem J 2002;361:243-54.
27. Whitehead IP, Zohn IE, Der CJ. Rho GTPase-dependent transformation by G protein-coupled receptors. Oncogene 2001;20:1547-55.
28. Hu E, Lee D. Rho kinase inhibitors as potential therapeutic agents for cardiovascular diseases. Curr Opin Investig Drugs 2003;4:1065-75.
29. Sharpe CC, Hendry BM. Signaling: Focus on Rho in renal disease. J Am Soc Nephrol 2003;14:261-4.
30. Iliopoulos O, Kibel A, Gray S, Kaelin WG. Tumor suppression by the human von Hippel-Lindau gene product. Nat Med 1995;1:822-6.
31. Turcotte S, Desrosiers RR, Béliveau R. HIF-1α mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. J Cell Sci 2003;115:2247-60.
32. Okuda H, Hirai S, Takaki Y, Kamada M, Baba M, Sakai N, Kishida T, Kaneko S, Yao M, Ohno S, Shuin T. Direct interaction of the beta-domain of VHL tumor suppressor protein with the regulatory domain of atypical PKC isotypes. Biochem Biophys Res Commun. 1999;263:491-7.
33. Pal S, Claffey K, Dvorak H, Mukhopadhyay D. The von Hippel-Lindau gene product inhibits vascular permeability factor/vascular endothelial growth factor expression in renal cell carcinoma. J Biol Chem 1997;272:27509-12.
34. Tellez C, McCarty M, Ruiz M, Bar-Eli M. Loss of activator protein-2alpha results in overexpression of protease-activated receptor-1 and correlates with the malignant phenotype of human melanoma. J Biol Chem 2003;278:46632-42.
35. Even-Ram S, Uziely B, Cohen P, Grisaru-Granovsky S, Maoz M, Ginzburg Y, Reich R, Vlodavsky I, Bar-Shavit R. Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med 1998;4:909-14.
36. Richard DE, Berra E, Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1α in vascular smooth muscle cells. J Biol Chem 2000;275:26765-71.
37. Gorlach A, Diebold I, Schini-Kerth VB, Berchner-Pfannschmidt U, Roth U, Brandes RP, Kietzmann T, Busse R. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells Role of the p22phox-containing NADPH oxidase. Circ Res 2001;89:47-54.
38. Schoenfeld AR, Davidowitz EJ, Burk RD. Endoplasmic reticulum/ cytosolic localization of von Hippel-Lindau gene products is mediated by a 64-amino acid region. Int J Cancer 2001;91:457-67.
39. Lee S, Chen DYT, Humphrey J S, Gnarra JR, Linehan WM, Klausner RD. Nuclear/cytoplasmic localization of the von Hippel-Lindau tumor suppressor gene product is determined by cell density. Proc Natl Acad Sci U S A 1996;93:1770-5.
40. Lee S, Neumann M, Stearman R, Stauber R, Pause A, Pavlakis GN, Klausner RD. Transcription-dependent nuclear-cytoplasmic trafficking is required for the function of the von Hippel-Lindau tumor suppressor protein. Mol. Cell Biol. 1999;19:1486-97.
41. Vouret-Craviari V, Boquet P, Pouyssegur J, van Obberghen-Schilling E. Regulation of the actin cytoskeleton by thrombin in human endothelial cells: role of Rho proteins in endothelial barrier functions. Mol Biol Cell 1998;9:2639-53.
42. 11. J Biol Chem 2003;278:28743-9.
43. Bauer M, Retzer M, Wilde JI, Maschberger P, Essler M, Aepfelbacher M, Watson SP, Siess W. Dichotomous regulation of myosin phosphorylation and shape change by Rho-kinase and calcium in intact human platelets. Blood 1999;94:1665-72.
44. Yamashiro S, Totsukawa G, Yamakita Y, Sasaki Y, Madaule P, Ishizaki T, Narumiya S, Matsumura F. Citron kinase, a Rho-dependent kinase, induces di-phosphorylation of regulatory light chain of myosin II. Mol Biol Cell 2003;14:1745-56.
45. Zacharski LR, Memoli VA, Morain WD, Schlaeppi JM, Rousseau SM. Cellular localization of enzymatically active thrombin in intact human tissues by hirudin binding. Thromb Haemost 1995;73:793-7.
46. Kaufmann R, Junker U, Junker K, Nuske K, Ranke C, Zieger M, Scheele J. The serine proteinase thrombin promotes migration of human renal carcinoma cells by a PKA-dependent mechanism. Cancer Lett 2002;180:183-90.
47. Ziger M, Tausch S, Henklein P, Nowak G, Kaufmann RA novel PAR-1-type thrombin receptor signaling pathway: cyclic AMP-independent activation of PKA in SNB-19 glioblastoma cells. Biochem Biophys Res Commun 2001;13:282-4.
48. Koochekpour S, Jeffers M, Wang PH, Gong C, Taylor GA, Roessler LM, Stearman R, Vasselli JR, Stetler-Stevenson WG, Kaelin WG Jr, Linehan WM, Klausner RD, et al. The von Hippel-Lindau tumor suppressor gene inhibits hepatocyte growth factor/scatter factor-induced invasion and branching morphogenesis in renal carcinoma cells. Mol Cell Biol 1999;19:5902-12.
49. Lewis MD, Roberts BJ. Role of nuclear and cytoplasmic localization in the tumor suppressor activity of the von Hippel-Lindau protein. Oncogene 2003;22:3992-97.