β-Arrestin-1-dependent activation of extracellular signal-regulated kinases in RON receptor-mediated tumorigenic activities in colon cancer cells

Journal of Cancer Molecules

Volumn 5, Issue 2, 2009, Pages 55-62

  Zhou, Yong Qing ^a   Luo, Yu Lan ^b   Zhou, Wendy ^b   Yao, Hang Ping ^a   Wang, Ming Hai ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

arrestin 1; RON; RON160; Signal transduction; Tumorigenic phenotype

Indexed keywords

BETA ARRESTIN 1; MITOGEN ACTIVATED PROTEIN KINASE; TYROSINE KINASE RECEPTOR; TYROSINE KINASE RECEPTOR RON; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CARCINOGENIC ACTIVITY; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CELL TRANSFORMATION; COLON CANCER; COMPLEX FORMATION; CONTROLLED STUDY; DNA PROTEIN COMPLEX; ENZYME ACTIVATION; GENE DISRUPTION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 79251530772     PISSN: 18160735     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (41)

1. Buchanan FG, DuBois RN. Emerging roles of β-arrestins. Cell Cycle 5: 2060-2063, 2006.
2. Lefkowitz RJ, Shenoy SK. Transduction of receptor signals by β-arrestins. Science 308: 512-517, 2005.
3. Lefkowitz RJ, Rajagopal K, Whalen EJ. New roles for β-arrestins in cell signaling: not just for seven-transmembrane receptors. Mol Cell 24: 643-652, 2006.
4. Hupfeld CJ, Olefsky JM. Regulation of receptor tyrosine kinase signaling by GRKs and β-arrestins. Annu Rev Physiol 69: 561- 577, 2007.
5. Luttrell LM, Roudabush FL, Choy EW, Miller WE, Field ME, Pierce KL, Lefkowitz RJ. Activation and targeting of extracellular signal-regulated kinases by β-arrestin scaffolds. Proc Natl Acad Sci USA 98: 2449-2454, 2001.
6. Noma T, Lemaire A, Naga Prasad SV, Barki-Harrington L, Tilley DG, Chen J, Le Corvoisier P, Violin JD, Wei H, Lefkowitz RJ, Rockman HA. β-arrestin-mediated β1-adrenergic receptor transactivation of the EGFR confers cardioprotection. J Clin Invest 117: 2445-2458, 2007.
7. Girnita L, Shenoy SK, Sehat B, Vasilcanu R, Vasilcanu D, Girnita A, Lefkowitz RJ, Larsson O. β-arrestin and Mdm2 mediate IGF-1 receptor-stimulated ERK activation and cell cycle progression. J Biol Chem 282: 11329-11338, 2007.
8. Povsic TJ, Kohout TA, Lefkowitz RJ. β-arrestin 1 mediates insulin-like growth factor 1 (IGF-1) activation of phosphatidylinositol 3-kinase (PI3K) and anti-apoptosis. J Biol Chem 278: 51334-51339, 2003.
9. Defea KA. Stop β-arrestin-dependent chemotaxis: a tale of localized actin assembly and receptor desensitization. Annu Rev Physiol 69: 2.1-2.26, 2007.
10. Buchanan FG, Gorden DL, Matta P, Shi Q, Matrisian LM, DuBois RN. Role of β-arrestin 1 in the metastatic progression of colorectal cancer. Proc Natl Acad Sci USA 103: 1492-1497, 2006.
11. Ge L, Shenoy SK, Lefkowitz RJ, DeFea K. Constitutive proteaseactivated receptor-2-mediated migration of MDA MB-231 breast cancer cells requires both β-arrestin-1 and -2. J Biol Chem 279: 55419-5524, 2004.
12. Wang M-H, Wang D, Chen Y-Q: Oncogenic and metastatic potentials of human macrophage stimulating protein receptor, the RON receptor tyrosine kinase. Carcinogenesis 24:1291- 1300, 2003.
13. Wang M-H, Wei L, Luo Y-L, Weis MT, Yao H-P. Altered expression of the RON receptor tyrosine kinase in various epithelial cancers and its contribution to tumorigenic phenotypes in thyroid cancer cells. J Pathol 213: 401-411, 2007.
14. Zhou YQ, He C, Chen YQ, Wang D, Wang MH. Altered expression of the RON receptor tyrosine kniase in primary human colorectal adenocarcinomas: generation of different splicing variants and their oncogenic potential. Oncogene 22: 186-197, 2003.
15. Maggiora P, Marchio S, Stella MC, Giai M, Belfiore A, De Bortoli M, Di Renzo MF, Costantino A, Sismondi P, Comoglio PM. Overexpression of the RON gene in human breast carcinoma. Oncogene 16: 2927-2933, 1998.
16. Lee WY, Chen HH, Chow NH, Su WC, Lin PW, Guo HR. Prognostic significance of co-expression of RON and MET receptors in node-negative breast cancer patients. Clin Cancer Res 11: 2222- 2228, 2005.
17. Thomas RM, Toney K, Fenoglio-Preiser C, Revelo-Penafiel MP, Hingorani SR, Tuveson DA, Waltz SE, Lowy AM. The RON receptor tyrosine kinase mediates oncogenic phenotypes in pancreatic cancer cells and is increasingly expressed during pancreatic cancer progression. Cancer Res 67: 6075-6082, 2007.
18. Camp ER, Yang A, Gray MJ, Fan F, Hamilton SR, Evans DB, Hooper AT, Pereira DS, Hicklin DJ, Ellis LM. Tyrosine kinase receptor RON in human pancreatic cancer: expression, function, and validation as a target. Cancer 109: 1030-1039, 2007.
19. Wang MH, Yao HP, Zhou YQ. Oncogenesis of RON receptor tyrosine kinase: a molecular target for malignant epithelial cancers. Acta Pharmacol Sin 27: 641-650, 2006.
20. Lu Y, Yao PH, Wang MH. Multiple variants of the RON receptor tyrosine kinase: biochemical properties, tumorigenic activities, and potential drug targets. Cancer Lett 257: 157-164, 2007.
21. Wang M-H, Kurtz AL, Chen YQ. Identification of a novel splicing product of the RON receptor tyrosine kinase in human colorectal carcinoma cells. Carcinogenesis 21: 1507-1512, 2000.
22. Finkelstein LD, Ney PA, Liu QP, Paulson RF, Correll PH. Sf-Stk kinase activity and the Grb2 binding site are required for Epoindependent growth of primary erythroblasts infected with Friend virus. Oncogene 21: 3562-3570, 2002.
23. Li BQ, Wang MH, Kung HF, Ronsin C, Breathnach R, Leonard EJ, Kamata T. Macrophage-stimulating protein activates Ras by both activation and translocation of SOS nucleotide exchange factor. Biochem Biophys Res Commun 216: 110-118, 1995.
24. Kohout TA, Lin FS, Perry SJ, Conner DA, Lefkowitz RJ. β-arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc Natl Acad Sci USA 98: 1601-1606, 2001.
25. Williams AC, Harper SJ, Paraskeva C. Neoplastic transformation of a human colonic epithelial cell line: in vitro evidence for the adenoma to carcinoma sequence. Cancer Res 50: 4724-4730, 1990.
26. Xu XM, Wang D, Shen Q, Chen YQ, Wang MH. RNA-mediated gene silencing of the RON receptor tyrosine kinase alters oncogenic phenotypes of human colorectal carcinoma cells. Oncogene 23: 8464-8474, 2004.
27. Manning AM, Williams AC, Game SM, Paraskeva C. Differential sensitivity of human colonic adenoma and carcinoma cells to transforming growth factor β (TGF-β): conversion of an adenoma cell line to a tumorigenic phenotype is accompanied by a reduced response to the inhibitory effects of TGF-β. Oncogene 6: 1471-1476, 1991.
28. Yao HP, Luo YL, Feng L, Cheng LF, Lu Y, Li W, Wang MH. Agonistic monoclonal antibodies potentiate tumorigenic and invasive activities of splicing variant of the RON receptor tyrosine kinase. Cancer Biol Ther 5: 1179-1186, 2006.
29. Ahn S, Nelson CD, Garrison TR, Miller WE, Lefkowitz RJ. Desensitization, internalization, and signaling functions of β-arrestins demonstrated by RNA interference. Proc Natl Acad Sci USA 100: 1740-1744, 2003.
30. Wang MH, Dlugosz AA, Sun Y, Suda T, Skeel A, Leonard EJ. Macrophage-stimulating protein induces proliferation and migration of murine keratinocytes. Exp Cell Res 226: 39-46, 1996.
31. Chen YQ, Zhou YQ, Angeloni D, Kurtz AL, Qiang XZ, Wang MH. Overexpression and activation of the RON receptor tyrosine kinase in a panel of human colorectal carcinoma cell lines. Exp Cell Res 261: 229-238, 2000.
32. Ponzetto C, Bardelli A, Zhen Z, Maina F, dalla Zonca P, Giordano S, Graziani A, Panayotou G, Comoglio PM. A multifunctional docking site mediates signaling and transformation by the hepatocyte growth factor/scatter factor receptor family. Cell 77: 261-271, 1994.
33. Penengo L, Rubin C, Yarden Y, Gaudino G. c-Cbl is a critical modulator of the Ron tyrosine kinase receptor. Oncogene 22: 3669-3679, 2003.
34. Santoro MM, Gaudino G, Villa-Moruzzi E. Protein phosphatase 1 binds to phospho-Ser-1394 of the macrophage-stimulating protein receptor. Biochem J 376: 587-594, 2003.
35. Germano S, Barberis D, Santoro MM, Penengo L, Citri A, Yarden Y, Gaudino G. Geldanamycins trigger a novel Ron degradative pathway, hampering oncogenic signaling. J Biol Chem 281: 21710-21719, 2006.
36. Alderton F, Rakhit S, Kong KC, Palmer T, Sambi B, Pyne S, Pyne NJ. Tethering of the platelet-derived growth factor β receptor to G-protein-coupled receptors. A novel platform for integrative signaling by these receptor classes in mammalian cells. J Biol Chem 276: 28578-28585, 2001.
37. Wang MH, Montero-Julian FA, Dauny I, Leonard EJ. Requirement of phosphatidylinositol-3 kinase for epithelial cell migration activated by human macrophage-stimulating protein. Oncogene 13: 2167-2175, 1996.
38. Xiao ZQ, Chen YQ, Wang MH. Requirement of both tyrosine residues 1330 and 1337 in the C-terminal tail of the RON receptor tyrosine kinase for epithelial cell scattering and migration. Biochem Biophys Res Commun 267: 669-675, 2000.
39. Wang J, Rajput A, Kan JL, Rose R, Liu XQ, Kuropatwinski K, Hauser J, Beko A, Dominquez I, Sharratt EA, Brattain L, Levea C, Sun FL, Keane DM, Gibson NW, Brattain MG. Knockdown of Ron kinase inhibits mutant phosphatidylinositol 3-kinase and reduces metastasis in human colon carcinoma. J Biol Chem 284: 10912-10922, 2009.
40. Wang D, Shen Q, Chen YQ, Wang MH. Collaborative activities of macrophage-stimulating protein and transforming growth factor- β1 in induction of epithelial to mesenchymal transition: roles of the RON receptor tyrosine kinase. Oncogene 23: 1668- 1680, 2004.
41. Wang D, Shen Q, Xu XM, Chen YQ, Wang MH. Activation of the RON receptor tyrosine kinase attenuates transforming growth factor-β1-induced apoptotic death and promotes phenotypic changes in mouse intestinal epithelial cells. Carcinogenesis 26: 27-36, 2005.