The Ron receptor tyrosine kinase is not required for adenoma formation in ApcMin/+ mice

Molecular Carcinogenesis

Volumn 48, Issue 11, 2009, Pages 995-1004

  Meyer, Sara E ^a   Waltz, Susan E ^a   Goss, Kathleen H ^b  

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

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Adenoma; Apc; Proliferation

Indexed keywords

BETA CATENIN; MESSENGER RNA; PROTEIN KINASE RON; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; COLON POLYPOSIS; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; INTESTINE CRYPT; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION; TUMOR VOLUME; WILD TYPE;

ADENOMA; ANIMALS; BASE SEQUENCE; CELL PROLIFERATION; COLONIC NEOPLASMS; DNA PRIMERS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; POLYMERASE CHAIN REACTION; RECEPTOR PROTEIN-TYROSINE KINASES;

MUS;

EID: 70350459060     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20551     Document Type: Article

References (62)

1. Powell SM, Zilz N, Beazer-Barclay Y, et al. APC mutations occur early during colorectal tumorigenesis. Nature 1992;359:235-237.
2. Groden J, Thliveris A, Samowitz W, et al. Identification and characterization of the familial adenomatous polyposis coli gene. Cell 1991;66:589-600. (Pubitemid 121001394)
3. Luongo C, Moser AR, Gledhill S, Dove WF. Loss of Apc+ in intestinal adenomas from Min mice. Cancer Res 1994;54:5947-5952. (Pubitemid 24375232)
4. Moser AR, Dove WF, Roth KA, Gordon JI. The Min (multiple intestinal neoplasia) mutation: Its effect on gut epithelial cell differentiation and interaction with a modifier system. J Cell Biol 1992;116:1517-1526.
5. Sodir NM, Chen X, Park R, et al. Smad3 deficiency promotes tumorigenesis in the distal colon of ApcMin/+ mice. Cancer Res 2006;66:8430-8438. (Pubitemid 44449154)
6. Suzui M, Okuno M, Tanaka T, Nakagama H, Moriwaki H. Enhanced colon carcinogenesis induced by azoxymethane in Min mice occurs via a mechanism independent of beta-catenin mutation. Cancer Lett 2002;183:31-41. (Pubitemid 34607349)
7. Sheng H, Shao J, Williams CS, et al. Nuclear translocation of beta-catenin in hereditary and carcinogen-induced intestinal adenomas. Carcinogenesis 1998;19:543-549. (Pubitemid 28376795)
8. Hao X, Tomlinson I, Ilyas M, Palazzo JP, Talbot IC. Reciprocity between membranous and nuclear expression of beta-catenin in colorectal tumours. Virchows Arch 1997;431:167-172. (Pubitemid 27440360)
9. Korinek V, Barker N, Morin PJ, et al. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/-colon carcinoma. Science 1997;275:1784-1787. (Pubitemid 27136714)
10. Ahn B, Ohshima H. Suppression of intestinal polyposis in Apc(Min/+) mice by inhibiting nitric oxide production. Cancer Res 2001;61:8357-8360. (Pubitemid 33131104)
11. Baker SM, Harris AC, Tsao JL, et al. Enhanced intestinal adenomatous polyp formation in Pms2-/-;Min mice. Cancer Res 1998;58:1087-1089.
12. Wilson CL, Heppner KJ, Labosky PA, Hogan BL, Matrisian LM. Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci USA 1997;94:1402-1407.
13. 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 2000;261:229-238. (Pubitemid 30943860)
14. Okino T, Egami H, Ohmachi H, et al. Presence of RON receptor tyrosine kinase and its splicing variant in malignant and non-malignant human colonic mucosa. Int J Oncol 1999;15:709-714.
15. Camp ER, Liu W, Fan F, Yang A, Somcio R, Ellis LM. RON, a tyrosine kinase receptor involved in tumor progression and metastasis. Ann Surg Oncol 2005;12:273-281. (Pubitemid 40616491)
16. Wang MH, Yao HP, Zhou YQ. Oncogenesis of RON receptor tyrosine kinase: A molecular target for malignant epithelial cancers. Acta Pharmacol Sin 2006;27:641-650.
17. Zhou YQ, He C, Chen YQ, Wang D, Wang MH. Altered expression of the RON receptor tyrosine kinase in primary human colorectal adenocarcinomas: Generation of different splicing RON variants and their oncogenic potential. Oncogene 2003;22:186-197. (Pubitemid 36174176)
18. Ronsin C, Muscatelli F, Mattei MG, Breathnach R. A novel putative receptor protein tyrosine kinase of the met family. Oncogene 1993;8:1195-1202. (Pubitemid 23129841)
19. Rubin JS, Bottaro DP, Aaronson SA. Hepatocyte growth factor/scatter factor and its receptor, the c-met protooncogene product. Biochim Biophys Acta 1993;1155:357-371. (Pubitemid 24012300)
20. Danilkovitch-Miagkova A. Oncogenic signaling pathways activated by RON receptor tyrosine kinase. Curr Cancer Drug Targets 2003;3:31-40. (Pubitemid 36119419)
21. 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 2004;23:8464-8474. (Pubitemid 39540797)
22. Wang MH, Wang D, Chen YQ. Oncogenic and invasive potentials of human macrophage-stimulating protein receptor, the RON receptor tyrosine kinase. Carcinogenesis 2003;24:1291-1300. (Pubitemid 37038819)
23. Zinser GM, Leonis MA, Toney K, et al. Mammary-specific Ron receptor overexpression induces highly metastatic mammary tumors associated with beta-catenin activation. Cancer Res 2006;66:11967-11974. (Pubitemid 46094210)
24. Peace BE, Toney-Earley K, Collins MH,Waltz SE. Ron receptor signaling augments mammary tumor formation and metastasis in a murine model of breast cancer. Cancer Res 2005;65:1285-1293. (Pubitemid 40270155)
25. Ichii S, Horii A, Nakatsuru S, Furuyama J, Utsunomiya J, Nakamura Y. Inactivation of bothAPCalleles in an early stage of colon adenomas in a patient with familial adenomatous polyposis (FAP). Hum Mol Genet 1992;1:387-390.
26. Levy DB, Smith KJ, Beazer-Barclay Y, Hamilton SR, Vogelstein B, Kinzler KW. Inactivation of both APC alleles in human and mouse tumors. Cancer Res 1994;54:5953-5958. (Pubitemid 24375233)
27. Waltz SE, Eaton L, Toney-Earley K, et al. Ron-mediated cytoplasmic signaling is dispensable for viability but is required to limit inflammatory responses. J Clin Invest 2001;108:567-576. (Pubitemid 32777736)
28. Boivin GP, Washington K, Yang K, et al. Pathology of mouse models of intestinal cancer: Consensus report and recommendations. Gastroenterology 2003;124:762-777. (Pubitemid 36268493)
29. Okino T, Egami H, Ohmachi H, et al. Immunohistochemical analysis of distribution of RON receptor tyrosine kinase in human digestive organs. Dig Dis Sci 2001;46:424-429. (Pubitemid 32242694)
30. Kim SH, Roth KA, Moser AR, Gordon JI. Transgenic mouse models that explore the multistep hypothesis of intestinal neoplasia. J Cell Biol 1993;123:877-893. (Pubitemid 23333577)
31. Paulsen JE, Namork E, Steffensen IL, Eide TJ, Alexander J. Identification and quantification of aberrant crypt foci in the colon of Min mice - A murine model of familial adenomatous polyposis. Scand J Gastroenterol 2000;35:534-539. (Pubitemid 30354095)
32. Paulsen JE, Steffensen IL, Loberg EM, Husoy T, Namork E, Alexander J. Qualitative and quantitative relationship between dysplastic aberrant crypt foci and tumorigenesis in the Min/+ mouse colon. Cancer Res 2001;61:5010-5015. (Pubitemid 32681528)
33. Wang D, Shen Q, Xu XM, Chen YQ, Wang MH. Activation of the RON receptor tyrosine kinase attenuates transforming growth factor-beta1-induced apoptotic death and promotes phenotypic changes in mouse intestinal epithelial cells. Carcinogenesis 2005;26:27-36. (Pubitemid 40207696)
34. Leonis MA, Toney-Earley K, Degen SJ, Waltz SE. Deletion of the Ron receptor tyrosine kinase domain in mice provides protection from endotoxin-induced acute liver failure. Hepatology 2002;36:1053-1060. (Pubitemid 35253420)
35. Danilkovitch-Miagkova A, Miagkov A, Skeel A, Nakaigawa N, Zbar B, Leonard EJ. Oncogenic mutants of RON and MET receptor tyrosine kinases cause activation of the beta-catenin pathway. Mol Cell Biol 2001;21:5857-5868. (Pubitemid 32737803)
36. Iwama A, Yamaguchi N, Suda T. STK/RON receptor tyrosine kinase mediates both apoptotic and growth signals via the multifunctional docking site conserved among the HGF receptor family. EMBO J 1996;15:5866-5875. (Pubitemid 26375508)
37. Harada N, Tamai Y, Ishikawa T, et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 1999;18:5931-5942. (Pubitemid 29515670)
38. Crawford HC, Fingleton BM, Rudolph-Owen LA, et al. The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene 1999;18:2883-2891.
39. O'Toole JM, Rabenau KE, Burns K, et al. Therapeutic implications of a human neutralizing antibody to the macrophage-stimulating protein receptor tyrosine kinase (RON), a c-MET family member. Cancer Res 2006;66:9162-9170. (Pubitemid 44521136)
40. Zhang Y, Kaplan-Lefko PJ, Rex K, et al. Identification of a novel recepteur d'origine nantais/c-met small-molecule kinase inhibitor with antitumor activity in vivo. Cancer Res 2008;68:6680-6687.
41. Moser AR, Luongo C, Gould KA, McNeley MK, Shoemaker AR, Dove WF. ApcMin: A mouse model for intestinal and mammary tumorigenesis. Eur J Cancer 1995;31:1061-1064.
42. Kartheuser A, West S, Walon C, et al. The genetic background of familial adenomatous polyposis. Linkage analysis, the APC gene identification and mutation screening. Acta Gastroenterol Belg 1995;58:433-451.
43. Su LK, Kinzler KW, Vogelstein B, et al. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992;256:668-670.
44. Boon EM, Pouwels W, Redeker S, et al. Activation of Wnt signaling in the intestinal mucosa of Apc+/min mice does not cause overexpression of the receptor tyrosine kinase Met. Cancer Sci 2006;97:710-715. (Pubitemid 43983782)
45. Leonis MA, Thobe MN, Waltz SE. Ron-receptor tyrosine kinase in tumorigenesis and metastasis. Future Oncol 2007;3:441-448. (Pubitemid 47250161)
46. Wang MH, Lee W, Luo YL, Weis MT, Yao HP. Altered expression of the RON receptor tyrosine kinase in various epithelial cancers and its contribution to tumourigenic phenotypes in thyroid cancer cells. J Pathol 2007;213:402-411. (Pubitemid 350206512)
47. Chan EL, Peace BE, Collins MH, Toney-Earley K, Waltz SE. Ron tyrosine kinase receptor regulates papilloma growth and malignant conversion in a murine model of skin carcinogenesis. Oncogene 2005;24:479-488. (Pubitemid 40188595)
48. Rudolph KL, Millard M, Bosenberg MW, DePinho RA. Telomere dysfunction and evolution of intestinal carcinoma in mice and humans. Nat Genet 2001;28:155-159. (Pubitemid 32538061)
49. Goss KH, Risinger MA, Kordich JJ, et al. Enhanced tumor formation in mice heterozygous for Blm mutation. Science 2002;297:2051-2053.
50. Goss KJ, Brown PD, Matrisian LM. Differing effects of endogenous and synthetic inhibitors of metalloproteinases on intestinal tumorigenesis. Int J Cancer 1998;78:629-635.
51. Silverman KA, Koratkar R, Siracusa LD, Buchberg AM. Identification of the modifier of Min 2 (Mom2) locus, a new mutation that influences Apc-induced intestinal neoplasia. Genome Res 2002;12:88-97. (Pubitemid 34065592)
52. Gould KA, Dove WF. Analysis of the Mom1 modifier of intestinal neoplasia inmice. Exp Lung Res 1998;24:437-453.
53. Kwong LN, Shedlovsky A, Biehl BS, Clipson L, Pasch CA, Dove WF. Identification of Mom7, a novel modifier of Apc(Min/+) on mouse chromosome 18. Genetics 2007;176:1237-1244. (Pubitemid 46961118)
54. Thomas RM, Toney K, Fenoglio-Preiser C, et al. The RON receptor tyrosine kinase mediates oncogenic phenotypes in pancreatic cancer cells and is increasingly expressed during pancreatic cancer progression. Cancer Res 2007;67:6075-6082. (Pubitemid 47037486)
55. He TC, Sparks AB, Rago C, et al. Identification of c-MYC as a target of the APC pathway. Science 1998;281:1509-1512. (Pubitemid 28425575)
56. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999;398:422-426. (Pubitemid 29180374)
57. Correll PH, Iwama A, Tondat S, Mayrhofer G, Suda T, Bernstein A. Deregulated inflammatory response in mice lacking the STK/RON receptor tyrosine kinase. Genes Funct 1997;1:69-83.
58. Zhou YQ, Chen YQ, Fisher JH, Wang MH. Activation of the RON receptor tyrosine kinase by macrophage-stimulating protein inhibits inducible cyclooxygenase-2 expression in murine macrophages. J BiolChem2002;277:38104- 38110.
59. Hull MA, Booth JK, Tisbury A, et al. Cyclooxygenase 2 is upregulated and localized to macrophages in the intestine of Min mice. Br J Cancer 1999;79:1399-1405. (Pubitemid 29116796)
60. Chen LC, Hao CY, Chiu YS, et al. Alteration of gene expression in normal-appearing colon mucosa of APC(min) mice and human cancer patients. Cancer Res 2004;64:3694-3700.
61. Williams CS, Luongo C, Radhika A, et al. Elevated cyclooxygenase-2 levels in Min mouse adenomas. Gastroenterology 1996;111:1134-1140. (Pubitemid 26327618)
62. Oshima M, Dinchuk JE, Kargman SL, et al. Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 1996;87:803-809. (Pubitemid 26404280)