Ron receptor tyrosine kinase signaling as a therapeutic target

Bibliography

• Ronsin C, Muscatelli F, Mattei MG, A novel putative receptor protein tyrosine kinase of the met family. Oncogene 1993;8(5):1195-202
   PubMed Web of Science ®Google Scholar
• Wagh PK, Peace BE, Waltz SE. Met-related receptor tyrosine kinase Ron in tumor growth and metastasis. Adv Cancer Res 2008;100:1-33
   PubMed Web of Science ®Google Scholar
• Iwama A, Okano K, Sudo T, Molecular cloning of a novel receptor tyrosine kinase gene, STK, derived from enriched hematopoietic stem cells. Blood 1994;83(11):3160-9
   Google Scholar
• Wang MH, Iwama A, Skeel A, The murine stk gene product, a transmembrane protein tyrosine kinase, is a receptor for macrophage-stimulating protein. Proc Natl Acad Sci USA 1995;92(9):3933-7
   Google Scholar
• Cottage A, Clark M, Hawker K, Three receptor genes for plasminogen related growth factors in the genome of the puffer fish Fugu rubripes. FEBS Lett 1999;443(3):370-4
   Google Scholar
• Lapraz F, Rottinger E, Duboc V, RTK and TGF-beta signaling pathways genes in the sea urchin genome. Dev Biol 2006;300(1):132-52
   Google Scholar
• Gaudino G, Follenzi A, Naldini L, RON is a heterodimeric tyrosine kinase receptor activated by the HGF homologue MSP. Embo J 1994;13(15):3524-32
   Google Scholar
• Wang MH, Yoshimura T, Skeel A, Proteolytic conversion of single chain precursor macrophage-stimulating protein to a biologically active heterodimer by contact enzymes of the coagulation cascade. J Biol Chem 1994;269(5):3436-40
   PubMed Web of Science ®Google Scholar
• Danilkovitch A, Miller M, Leonard EJ. Interaction of macrophage-stimulating protein with its receptor. Residues critical for beta chain binding and evidence for independent alpha chain binding. J Biol Chem 1999;274(42):29937-43
   Google Scholar
• Waltz SE, McDowell SA, Muraoka RS, Functional characterization of domains contained in hepatocyte growth factor-like protein. J Biol Chem 1997;272(48):30526-37
   Google Scholar
• Gaudino G, Avantaggiato V, Follenzi A, The proto-oncogene RON is involved in development of epithelial, bone and neuro-endocrine tissues. Oncogene 1995;11(12):2627-37
   Google Scholar
• Quantin B, Schuhbaur B, Gesnel MC, Restricted expression of the ron gene encoding the macrophage stimulating protein receptor during mouse development. Dev Dyn 1995;204(4):383-90
   Google Scholar
• Chodosh LA, Gardner HP, Rajan JV, Protein kinase expression during murine mammary development. Dev Biol 2000;219(2):259-76
   Google Scholar
• Meyer SE, Zinser GM, Stuart WD, The Ron receptor tyrosine kinase negatively regulates mammary gland branching morphogenesis. Dev Biol 2009;333(1):173-85
   Google Scholar
• Hess KA, Waltz SE, Chan EL, Receptor tyrosine kinase Ron is expressed in mouse reproductive tissues during embryo implantation and is important in trophoblast cell function. Biol Reprod 2003;68(4):1267-75
   Google Scholar
• Leonard EJ, Skeel A. A serum protein that stimulates macrophage movement, chemotaxis and spreading. Exp Cell Res 1976;102(2):434-8
   Google Scholar
• Leonard EJ, Skeel AH. Isolation of macrophage stimulating protein (MSP) from human serum. Exp Cell Res 1978;114(1):117-26
   Google Scholar
• Wang MH, Ronsin C, Gesnel MC, Identification of the ron gene product as the receptor for the human macrophage stimulating protein. Science 1994;266(5182):117-19
   Google Scholar
• Brunelleschi S, Penengo L, Lavagno L, Macrophage stimulating protein (MSP) evokes superoxide anion production by human macrophages of different origin. Br J Pharmacol 2001;134(6):1285-95
   Google Scholar
• Wang MH, Cox GW, Yoshimura T, Macrophage-stimulating protein inhibits induction of nitric oxide production by endotoxin- or cytokine-stimulated mouse macrophages. J Biol Chem 1994;269(19):14027-31
   Google Scholar
• Chen YQ, Fisher JH, Wang MH. Activation of the RON receptor tyrosine kinase inhibits inducible nitric oxide synthase (iNOS) expression by murine peritoneal exudate macrophages: phosphatidylinositol-3 kinase is required for RON-mediated inhibition of iNOS expression. J Immunol 1998;161(9):4950-9
   Google Scholar
• Correll PH, Iwama A, Tondat S, Deregulated inflammatory response in mice lacking the STK/RON receptor tyrosine kinase. Genes Funct 1997;1(1):69-83
   Google Scholar
• Lentsch AB, Pathrose P, Kader S, The Ron receptor tyrosine kinase regulates acute lung injury and suppresses nuclear factor kappaB activation. Shock 2007;27(3):274-80
   Google Scholar
• Morrison AC, Wilson CB, Ray M, Macrophage-stimulating protein, the ligand for the stem cell-derived tyrosine kinase/RON receptor tyrosine kinase, inhibits IL-12 production by primary peritoneal macrophages stimulated with IFN-gamma and lipopolysaccharide. J Immunol 2004;172(3):1825-32
   PubMed Web of Science ®Google Scholar
• O'Toole JM, Rabenau KE, Burns K, 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(18):9162-70
   Google Scholar
• Eckerich C, Schulte A, Martens T, RON receptor tyrosine kinase in human gliomas: expression, function, and identification of a novel soluble splice variant. J Neurochem 2009;109(4):969-80
   Google Scholar
• Molhoek KR, Shada AL, Smolkin M, Comprehensive analysis of receptor tyrosine kinase activation in human melanomas reveals autocrine signaling through IGF-1R. Melanoma Res 2011;21(4):274-84
   Google Scholar
• Nagahama J, Daa T, Yada N, Tyrosine kinase receptor RON and its ligand MSP in Merkel cell carcinoma. Pathol Res Pract 2011;207(8):463-7
   Google Scholar
• Feres KJ, Ischenko I, Hayman MJ. The RON receptor tyrosine kinase promotes MSP-independent cell spreading and survival in breast epithelial cells. Oncogene 2009;28(2):279-88
   Google Scholar
• Jaquish DV, Yu PT, Shields DJ, IGF1-R signals through the RON receptor to mediate pancreatic cancer cell migration. Carcinogenesis 2011;32(8):1151-6
   Google Scholar
• Peace BE, Hill KJ, Degen SJ, Cross-talk between the receptor tyrosine kinases Ron and epidermal growth factor receptor. Exp Cell Res 2003;289(2):317-25
   Google Scholar
• Chen YQ, Zhou YQ, Angeloni D, Overexpression and activation of the RON receptor tyrosine kinase in a panel of human colorectal carcinoma cell lines. Exp Cell Res 2000;261(1):229-38
   Google Scholar
• Collesi C, Santoro MM, Gaudino G, A splicing variant of the RON transcript induces constitutive tyrosine kinase activity and an invasive phenotype. Mol Cell Biol 1996;16(10):5518-26
   PubMedGoogle Scholar
• Ghigna C, Giordano S, Shen H, Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol Cell 2005;20(6):881-90
   PubMed Web of Science ®Google Scholar
• Wei X, Hao L, Ni S, Altered exon usage in the juxtamembrane domain of mouse and human RON regulates receptor activity and signaling specificity. J Biol Chem 2005;280(48):40241-51
   Google Scholar
• Persons DA, Paulson RF, Loyd MR, Fv2 encodes a truncated form of the Stk receptor tyrosine kinase. Nat Genet 1999;23(2):159-65
   Google Scholar
• Wetzel CC, Leonis MA, Dent A, Short-form Ron receptor is required for normal IFN-gamma production in concanavalin A-induced acute liver injury. Am J Physiol Gastrointest Liver Physiol 2007;292(1):G253-G61
   Google Scholar
• Zhang K, Zhou YQ, Yao HP, Alterations in a defined extracellular region of the RON receptor tyrosine kinase promote RON-mediated motile and invasive phenotypes in epithelial cells. Int J Oncol 2010;36(1):255-64
   Google Scholar
• Golan-Gerstl R, Cohen M, Shilo A, Splicing factor hnRNP A2/B1 regulates tumor suppressor gene splicing and is an oncogenic driver in glioblastoma. Cancer Res 2011;71(13):4464-72
   PubMed Web of Science ®Google Scholar
• Lefave CV, Squatrito M, Vorlova S, Splicing factor hnRNPH drives an oncogenic splicing switch in gliomas. EMBO J 2011;30(19):4084-97
   PubMed Web of Science ®Google Scholar
• Ghigna C, De Toledo M, Bonomi S, Pro-metastatic splicing of Ron proto-oncogene mRNA can be reversed: therapeutic potential of bifunctional oligonucleotides and indole derivatives. RNA Biol 2010;7(4):495-503
   Web of Science ®Google Scholar
• Ma Q, Guin S, Padhye SS, Ribosomal protein S6 kinase (RSK)-2 as a central effector molecule in RON receptor tyrosine kinase mediated epithelial to mesenchymal transition induced by macrophage-stimulating protein. Mol Cancer 2011;10:66
   Google Scholar
• Xiangming X, Yun Q, Guoliang Z, Mechanisms of RON-mediated epithelial-mesenchymal transition in MDCK cells through the MAPK pathway. Braz J Med Biol Res 2011;44(7):634-41
   Google Scholar
• Danilkovitch-Miagkova A, Miagkov A, Skeel A, Oncogenic mutants of RON and MET receptor tyrosine kinases cause activation of the beta-catenin pathway. Mol Cell Biol 2001;21(17):5857-68
   PubMed Web of Science ®Google Scholar
• Wagh PK, Gray JK, Zinser GM, Beta-Catenin is required for Ron receptor-induced mammary tumorigenesis. Oncogene 2011;30(34):3694-704
   Google Scholar
• Wagh PK, Zinser GM, Gray JK, Conditional deletion of beta-catenin in mammary epithelial cells of ron receptor, mst1r, overexpressing mice alters mammary tumorigenesis. Endocrinology 2012;153(6):2735-46
   Google Scholar
• Gray JK, Paluch AM, Stuart WD, Ron receptor overexpression in the murine prostate induces prostate intraepithelial neoplasia. Cancer Lett 2012;314(1):92-101
   Google Scholar
• Zinser GM, Leonis MA, Toney K, Mammary-specific Ron receptor overexpression induces highly metastatic mammary tumors associated with beta-catenin activation. Cancer Res 2006;66(24):11967-74
   Google Scholar
• Thobe MN, Gurusamy D, Pathrose P, The Ron receptor tyrosine kinase positively regulates angiogenic chemokine production in prostate cancer cells. Oncogene 2010;29(2):214-26
   Google Scholar
• Thobe MN, Gray JK, Gurusamy D, The Ron receptor promotes prostate tumor growth in the TRAMP mouse model. Oncogene 2011;30(50):4990-8
   Google Scholar
• Thomas RM, Jaquish DV, French RP, The RON tyrosine kinase receptor regulates vascular endothelial growth factor production in pancreatic cancer cells. Pancreas 2010;39(3):301-7
   Google Scholar
• Logan-Collins J, Thomas RM, Yu P, Silencing of RON receptor signaling promotes apoptosis and gemcitabine sensitivity in pancreatic cancers. Cancer Res 2010;70(3):1130-40
   Google Scholar
• Jayson GC, Hicklin DJ, Ellis LM. Antiangiogenic therapy-evolving view based on clinical trial results. Nat Rev Clin Oncol 2012;9(5):297-303
   PubMed Web of Science ®Google Scholar
• Santoro MM, Gaudino G, Marchisio PC. The MSP receptor regulates alpha6beta4 and alpha3beta1 integrins via 14-3-3 proteins in keratinocyte migration. Dev Cell 2003;5(2):257-71
   PubMed Web of Science ®Google Scholar
• Yu PT, Babicky M, Jaquish D, The RON-receptor regulates pancreatic cancer cell migration through phosphorylation-dependent breakdown of the hemidesmosome. Int J Cancer 2012; doi: 10.1002/ijc.27447
   Google Scholar
• Song YA, Park YL, Kim KY, RON is associated with tumor progression via the inhibition of apoptosis and cell cycle arrest in human gastric cancer. Pathol Int 2012;62(2):127-36
   Google Scholar
• Park JS, Park JH, Khoi PN, MSP-induced RON activation upregulates uPAR expression and cell invasiveness via MAPK, AP-1 and NF-kappaB signals in gastric cancer cells. Carcinogenesis 2011;32(2):175-81
   Google Scholar
• Roychowdhury S, Talpaz M. Managing resistance in chronic myeloid leukemia. Blood Rev 2011;25(6):279-90
   PubMed Web of Science ®Google Scholar
• Waltz SE, Toms CL, McDowell SA, Characterization of the mouse Ron/Stk receptor tyrosine kinase gene. Oncogene 1998;16(1):27-42
   Google Scholar
• McClaine RJ, Marshall AM, Wagh PK, Ron receptor tyrosine kinase activation confers resistance to tamoxifen in breast cancer cell lines. Neoplasia 2010;12(8):650-8
   Google Scholar
• Ferrandina G, Martinelli E, Petrillo M, Prognostic role of the recepteur d'origine nantais (RON) expression in ovarian cancer patients. Gynecol Oncol 2008;111(2):237-43
   Google Scholar
• Lee CT, Chow NH, Su PF, The prognostic significance of RON and MET receptor coexpression in patients with colorectal cancer. Dis Colon Rectum 2008;51(8):1268-74
   Google Scholar
• Lee WY, Chen HH, Chow NH, Prognostic significance of co-expression of RON and MET receptors in node-negative breast cancer patients. Clin Cancer Res 2005;11(6):2222-8
   PubMed Web of Science ®Google Scholar
• Qian F, Engst S, Yamaguchi K, Inhibition of tumor cell growth, invasion, and metastasis by EXEL-2880 (XL880, GSK1363089), a novel inhibitor of HGF and VEGF receptor tyrosine kinases. Cancer Res 2009;69(20):8009-16
   PubMed Web of Science ®Google Scholar
• Norman RA, Toader D, Ferguson AD. Structural approaches to obtain kinase selectivity. Trends Pharmacol Sci 2012;33(5):273-8
   PubMed Web of Science ®Google Scholar
• Eder JP, Shapiro GI, Appleman LJ, A phase I study of foretinib, a multi-targeted inhibitor of c-Met and vascular endothelial growth factor receptor 2. Clin Cancer Res 2010;16(13):3507-16
   PubMed Web of Science ®Google Scholar
• Li Z, Yao H, Guin S, Monoclonal antibody (mAb)-induced down-regulation of RON receptor tyrosine kinase diminishes tumorigenic activities of colon cancer cells. Int J Oncol 2010;37(2):473-82
   Google Scholar
• Guin S, Yao HP, Wang MH. RON receptor tyrosine kinase as a target for delivery of chemodrugs by antibody directed pathway for cancer cell cytotoxicity. Mol Pharm 2010;7(2):386-97
   Google Scholar
• Padhye SS, Guin S, Yao HP, Sustained expression of the RON receptor tyrosine kinase by pancreatic cancer stem cells as a potential targeting moiety for antibody-directed chemotherapeutics. Mol Pharm 2011;8(6):2310-19
   PubMedGoogle Scholar
• Yao HP, Zhou YQ, Ma Q, The monoclonal antibody Zt/f2 targeting RON receptor tyrosine kinase as potential therapeutics against tumor growth-mediated by colon cancer cells. Mol Cancer 2011;10:82
   Google Scholar
• Ray M, Yu S, Sharda DR, Inhibition of TLR4-induced IkappaB kinase activity by the RON receptor tyrosine kinase and its ligand, macrophage-stimulating protein. J Immunol 2010;185(12):7309-16
   Google Scholar
• Sharda DR, Yu S, Ray M, Regulation of macrophage arginase expression and tumor growth by the Ron receptor tyrosine kinase. J Immunol 2011;187(5):2181-92
   Google Scholar
• Nikolaidis NM, Gray JK, Gurusamy D, Ron receptor tyrosine kinase negatively regulates TNFalpha production in alveolar macrophages by inhibiting NF-kappaB activity and Adam17 production. Shock 2010;33(2):197-204
   Google Scholar
• Tong XM, Wang JC, Shen Y, Inhibition of inflammatory mediators and related signaling pathways by macrophage-stimulating protein in rheumatoid arthritis synovial fibroblasts. Inflamm Res 2011;60(9):823-9
   Google Scholar
• Marquez A, Cenit MC, Nunez C, Effect of BSN-MST1 locus on inflammatory bowel disease and multiple sclerosis susceptibility. Genes Immun 2009;10(7):631-5
   Google Scholar
• Beckly JB, Hancock L, Geremia A, Two-stage candidate gene study of chromosome 3p demonstrates an association between nonsynonymous variants in the MST1R gene and Crohn's disease. Inflamm Bowel Dis 2008;14(4):500-7
   Google Scholar
• Gorlatova N, Chao K, Pal LR, Protein characterization of a candidate mechanism SNP for Crohn's disease: the macrophage stimulating protein R689C substitution. PLoS One 2011;6(11):e27269
   Google Scholar
• Goyette P, Lefebvre C, Ng A, Gene-centric association mapping of chromosome 3p implicates MST1 in IBD pathogenesis. Mucosal Immunol 2008;1(2):131-8
   PubMed Web of Science ®Google Scholar
• Latiano A, Palmieri O, Corritore G, Variants at the 3p21 locus influence susceptibility and phenotype both in adults and early-onset patients with inflammatory bowel disease. Inflamm Bowel Dis 2010;16(7):1108-17
   Google Scholar
• Bernstein CN, Blanchard JF, Rawsthorne P, The prevalence of extraintestinal diseases in inflammatory bowel disease: a population-based study. Am J Gastroenterol 2001;96(4):1116-22
   PubMed Web of Science ®Google Scholar
• Hauser F, Deyle C, Berard D, Macrophage-stimulating protein polymorphism rs3197999 is associated with a gain of function: implications for inflammatory bowel disease. Genes Immun 2012;13(4):321-7
   Google Scholar
• Stuart WD, Kulkarni RM, Gray JK, Ron receptor regulates Kupffer cell-dependent cytokine production and hepatocyte survival following endotoxin exposure in mice. Hepatology 2011;53(5):1618-28
   Google Scholar
• Franks AL, Slansky JE. Multiple associations between a broad spectrum of autoimmune diseases, chronic inflammatory diseases and cancer. Anticancer Res 2012;32(4):1119-36
   PubMed Web of Science ®Google Scholar
• Chan ES, Cronstein BN. Methotrexate–how does it really work? Nat Rev Rheumatol 2010;6(3):175-8
   PubMed Web of Science ®Google Scholar
• Rosen JM, Jordan CT. The increasing complexity of the cancer stem cell paradigm. Science 2009;324(5935):1670-3
   PubMed Web of Science ®Google Scholar
• Kanneganti M, Mino-Kenudson M, Mizoguchi E. Animal models of colitis-associated carcinogenesis. J Biomed Biotechnol 2011;2011:342637
   PubMedGoogle Scholar
• Moser AR, Luongo C, Gould KA, ApcMin: a mouse model for intestinal and mammary tumorigenesis. Eur J Cancer 1995;31A(7-8):1061-4
   Google Scholar
• Meyer SE, Waltz SE, Goss KH. The Ron receptor tyrosine kinase is not required for adenoma formation in Apc(Min/+) mice. Mol Carcinog 2009;48(11):995-1004
   Google Scholar
• Danilkovitch A, Leonard EJ. Kinases involved in MSP/RON signaling. J Leukoc Biol Suppl 1998:9-35
   Google Scholar
• 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(21):5866-75
   Google Scholar
• Santoro MM, Penengo L, Minetto M, Point mutations in the tyrosine kinase domain release the oncogenic and metastatic potential of the Ron receptor. Oncogene 1998;17(6):741-9
   Google Scholar
• Danilkovitch A, Leonard EJ. Kinases involved in MSP/RON signaling. J Leukoc Biol 1999;65(3):345-8
   Google Scholar
• Li BQ, Wang MH, Kung HF, Macrophage-stimulating protein activates Ras by both activation and translocation of SOS nucleotide exchange factor. Biochem Biophys Res Commun 1995;216(1):110-18
   Google Scholar