The Ron receptor tyrosine kinase positively regulates angiogenic chemokine production in prostate cancer cells

Oncogene

Volumn 29, Issue 2, 2010, Pages 214-226

  Thobe, M N ^a   Gurusamy, D ^a   Pathrose, P ^a   Waltz, S E ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Angiogenesis; Chemokines; Met receptor; Prostate cancer; Receptor tyrosine kinase; Ron receptor

Indexed keywords

CXCL1 CHEMOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; PROTEIN TYROSINE KINASE; RON RECEPTOR TYROSINE KINASE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL MIGRATION; CELL STRAIN LNCAP; CHEMOTAXIS; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE METASTASIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; ANTIGENS, CD31; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL1; CHEMOKINE CXCL5; CHEMOKINES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-8; MALE; MICE; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; PROSTATIC NEOPLASMS; RECEPTOR PROTEIN-TYROSINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSPLANTATION, HETEROLOGOUS;

EID: 74449090319     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.331     Document Type: Article

References (46)

1. Addison CL, Daniel TO, Burdick MD, Liu H, Ehlert JE, Xue YY et al. (2000). The CXC chemokine receptor 2, CXCR2, is the putative receptor for ELR+ CXC chemokine-induced angiogenic activity. J Immunol 165: 5269-5277.
2. Balbay MD, Pettaway CA, Kuniyasu H, Inoue K, Ramirez E, Li E et al. (1999). Highly metastatic human prostate cancer growing within the prostate of athymic mice overexpresses vascular endothelial growth factor. Clin Cancer Res 5: 783-789.
3. Best CJ, Gillespie JW, Yi Y, Chandramouli GV, Perlmutter MA, Gathright Y et al. (2005). Molecular alterations in primary prostate cancer after androgen ablation therapy. Clin Cancer Res 11: 6823-6834.
4. Bezerra JA, Carrick TL, Degen JL, Witte D, Degen SJ. (1998). Biological effects of targeted inactivation of hepatocyte growth factor-like protein in mice. J Clin Invest 101: 1175-1183.
5. Bezerra JA, Witte DP, Aronow BJ, Degen SJ. (1993). Hepatocyte-specific expression of the mouse hepatocyte growth factor-like protein. Hepatology 18: 394-399.
6. Chen YQ, Zhou YQ, Angeloni D, Kurtz AL, Qiang XZ, Wang MH. (2000). Overexpression and activation of the RON receptor tyrosine kinase in a panel of human colorectal carcinoma cell lines. Exp Cell Res 261: 229-238.
7. Collado B, Carmena MJ, Clemente C, Prieto JC, Bajo AM. (2007). Vasoactive intestinal peptide enhances growth and angiogenesis of human experimental prostate cancer in a xenograft model. Peptides 28: 1896-1901.
8. Craft PS, Harris AL. (1994). Clinical prognostic significance of tumour angiogenesis. Ann Oncol 5: 305-311.
9. Dhanasekaran SM, Dash A, Yu J, Maine IP, Laxman B, Tomlins SA et al. (2005). Molecular profiling of human prostate tissues: insights into gene expression patterns of prostate development during puberty. FASEB J 19: 243-245.
10. Greene GF, Kitadai Y, Pettaway CA, von Eschenbach AC, Bucana CD, Fidler IJ. (1997). Correlation of metastasis-related gene expression with metastatic potential in human prostate carcinoma cells implanted in nude mice using an in situ messenger RNA hybridization technique. Am J Pathol 150: 1571-1582.
11. Hepburn PJ, Griffiths K, Harper ME. (1997). Angiogenic factors expressed by human prostatic cell lines: effect on endothelial cell growth in vitro. Prostate 33: 123-132.
12. Jimenez JA, Kao C, Raikwar S, Gardner TA. (2006). Current status of anti-angiogenesis therapy for prostate cancer. Urol Oncol 24: 260-268.
13. Keeley EC, Mehrad B, Strieter RM. (2008). Chemokines as mediators of neovascularization. Arterioscler Thromb Vasc Biol 28: 1928-1936.
14. Koch AE, Polverini PJ, Kunkel SL, Harlow LA, DiPietro LA, Elner VM et al. (1992). Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 258: 1798-1801.
15. Lapointe J, Li C, Giacomini CP, Salari K, Huang S, Wang P et al. (2007). Genomic profiling reveals alternative genetic pathways of prostate tumorigenesis. Cancer Res 67: 8504-8510.
16. Leonis MA, Thobe MN, Waltz SE. (2007). Ron-receptor tyrosine kinase in tumorigenesis and metastasis. Future Oncol 3: 441-448.
17. Li Y, Jin Y, Chen H, Jie G, Tobelem G, Caen JP et al. (2003). Suppression of tumor growth by viral vector-mediated gene transfer of N-terminal truncated platelet factor 4. Cancer Biother Radio-pharm 18: 829-840.
18. Lissbrant IF, Stattin P, Damber JE, Bergh A. (1997). Vascular density is a predictor of cancer-specific survival in prostatic carcinoma. Prostate 33: 38-45.
19. Loh SA, Chang EI, Galvez MG, Thangarajah H, El-ftesi S, Vial IN et al. (2009). SDF-1 alpha expression during wound healing in the aged is HIF dependent. Plast Reconstr Surg 123: 65S-75S.
20. Maggiora P, Marchio S, Stella MC, Giai M, Belfiore A, De Bortoli M et al. (1998). Overexpression of the RON gene in human breast carcinoma. Oncogene 16: 2927-2933.
21. Moore BB, Arenberg DA, Stoy K, Morgan T, Addison CL, Morris SB et al. (1999). Distinct CXC chemokines mediate tumorigenicity of prostate cancer cells. Am J Pathol 154: 1503-1512.
22. Nikolaidis NM, Gray JK, Gurusamy D, Fox W, Stuart WD, Huber N et al. (2009). Ron receptor tyrosine kinase negatively regulates TNFalpha production in alveolar macrophages by inhibiting NF-kappaB activity and ADAM17 production. Shock (in press).
23. O'Toole JM, Rabenau KE, Burns K, Lu D, Mangalampalli V, Balderes P et al. (2006). Therapeutic implications of a human neutralizing antibody to the macrophage-stimulating protein receptor tyrosine kinase (RON), a c-MET family member. Cancer Res 66: 9162-9170.
24. Peace BE, Hughes MJ, Degen SJ, Waltz SE. (2001). Point mutations and overexpression of Ron induce transformation, tumor formation, and metastasis. Oncogene 20: 6142-6151.
25. Peace BE, Toney-Earley K, Collins MH, Waltz SE. (2005). Ron receptor signaling augments mammary tumor formation and metastasis in a murine model of breast cancer. Cancer Res 65: 1285-1293.
26. Pound CR, Partin AW, Eisenberger MA, Chan DW, Pearson JD, Walsh PC. (1999). Natural history of progression after PSA elevation following radical prostatectomy. JAMA 281: 1591-1597.
27. Puri N, Khramtsov A, Ahmed S, Nallasura V, Hetzel JT, Jagadeeswaran R et al. (2007). A selective small molecule inhibitor of c-Met, PHA665752, inhibits tumorigenicity and angiogenesis in mouse lung cancer xenografts. Cancer Res 67: 3529-3534.
28. Ren Y, Cao B, Law S, Xie Y, Lee PY, Cheung L et al. (2005). Hepatocyte growth factor promotes cancer cell migration and angiogenic factors expression: a prognostic marker of human esophageal squamous cell carcinomas. Clin Cancer Res 11: 6190-6197.
29. Rollins BJ. (1997). Chemokines. Blood 90: 909-928.
30. Salcedo R, Resau JH, Halverson D, Hudson EA, Dambach M, Powell D et al. (2000). Differential expression and responsiveness of chemokine receptors (CXCR1-3) by human microvascular endothe-lial cells and umbilical vein endothelial cells. FASEB J 14: 2055-2064.
31. Sawa Y, Tsuruga E, Iwasawa K, Ishikawa H, Yoshida S. (2008). Leukocyte adhesion molecule and chemokine production through lipoteichoic acid recognition by toll-like receptor 2 in cultured human lymphatic endothelium. Cell Tissue Res 333: 237-252.
32. Shen H, Lentsch AB. (2004). Progressive dysregulation of transcription factors NF-kappa B and STAT1 in prostate cancer cells causes proangiogenic production of CXC chemokines. Am J Physiol Cell Physiol 286: C840-C847.
33. Shen H, Schuster R, Stringer KF, Waltz SE, Lentsch AB. (2006). The Duffy antigen/receptor for chemokines (DARC) regulates prostate tumor growth. FASEB J 20: 59-64.
34. Strieter RM, Burdick MD, Mestas J, Gomperts B, Keane MP, Belperio JA. (2006). Cancer CXC chemokine networks and tumour angiogenesis. Eur J Cancer 42: 768-778.
35. Thomas RM, Toney K, Fenoglio-Preiser C, Revelo-Penafiel MP, Hingorani SR, Tuveson DA et al. (2007). 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.
36. Tomlins SA, Mehra R, Rhodes DR, Cao X, Wang L, Dhanasekaran SM et al. (2007). Integrative molecular concept modeling of prostate cancer progression. Nat Genet 39: 41-51.
37. Varambally S, Yu J, Laxman B, Rhodes DR, Mehra R, Tomlins SA et al. (2005). Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression. Cancer Cell 8: 393-406.
38. Verras M, Lee J, Xue H, Li TH, Wang Y, Sun Z. (2007). The androgen receptor negatively regulates the expression of c-Met: implications for a novel mechanism of prostate cancer progression. Cancer Res 67: 967-975.
39. Wagh PK, Peace BE, Waltz SE. (2008). Met-related receptor tyrosine kinase Ron in tumor growth and metastasis. Adv Cancer Res 100: 1-33.
40. Wang MH, Lee W, Luo YL, Weis MT, Yao HP. (2007). Altered expression of the RON receptor tyrosine kinase in various epithelial cancers and its contribution to tumourigenic phenotypes in thyroid cancer cells. J Pathol 213: 402-411.
41. Waugh DJ, Wilson C, Seaton A, Maxwell PJ. (2008). Multi-faceted roles for CXC-chemokines in prostate cancer progression. Front Biosci 13: 4595-4604.
42. Welm AL, Sneddon JB, Taylor C, Nuyten DS, van de Vijver MJ, Hasegawa BH et al. (2007). The macrophage-stimulating protein pathway promotes metastasis in a mouse model for breast cancer and predicts poor prognosis in humans. Proc Natl Acad Sci USA 104: 7570-7575.
43. Wilson C, Purcell C, Seaton A, Oladipo O, Maxwell PJ, O'Sullivan JM et al. (2008). Chemotherapy-induced CXC-chemokine/CXC-che-mokine receptor signaling in metastatic prostate cancer cells confers resistance to oxaliplatin through potentiation of nuclear factor-kappaB transcription and evasion of apoptosis. J Pharmacol Exp Ther 327: 746-759.
44. Yoshida S, Harada T, Iwabe T, Taniguchi F, Fujii A, Sakamoto Y et al. (2002). Induction of hepatocyte growth factor in stromal cells by tumor-derived basic fibroblast growth factor enhances growth and invasion of endometrial cancer. J Clin Endocrinol Metab 87: 2376-2383.
45. Zhou YQ, He C, Chen YQ, Wang D, Wang MH. (2003). Altered expression of the RON receptor tyrosine kinase in primary human colorectal adenocarcinomas: generation of different splicing RON variants and their oncogenic potential. Oncogene 22: 186-197.
46. Zinser GM, Leonis MA, Toney K, Pathrose P, Thobe M, Kader SA et al. (2006). Mammary-specific Ron receptor overexpression induces highly metastatic mammary tumors associated with beta-catenin activation. Cancer Res 66: 11967-11974.