C-Met-induced epithelial carcinogenesis is initiated by the serine protease matriptase

Oncogene

Volumn 30, Issue 17, 2011, Pages 2003-2016

  Szabo, R ^a   Rasmussen, A L ^a   Moyer, A B ^a   Kosa, P ^a   Schafer, J M ^a   Molinolo, A A ^a   Gutkind, J S ^a   Bugge, T H ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

cell surface proteases; head and neck carcinoma; hepatocyte growth factor; mTor; protease activated signaling

Indexed keywords

GAB1 PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MATRIPTASE; PROTEIN; PROTEIN KINASE B; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EPIGENETICS; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HEPATOCYTE GROWTH FACTOR; HUMANS; KERATINOCYTES; MICE; PROTEIN PRECURSORS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MET; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UP-REGULATION;

MAMMALIA;

EID: 79955478095     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.586     Document Type: Article

References (50)

1. Amornphimoltham P, Patel V, Sodhi A, Nikitakis NG, Sauk JJ, Sausville EA et al. (2005). Mammalian target of rapamycin, a molecular target in squamous cell carcinomas of the head and neck. Cancer Res 65: 9953-9961. (Pubitemid 41541476)
2. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. (2003). Met, metastasis, motility and more. Nat Rev Mol Cell Biol 4: 915-925. (Pubitemid 37493640)
3. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C (1995). Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376: 768-771.
4. Bugge TH, Flick MJ, Daugherty CC, Degen JL. (1995). Plasminogen deficiency causes severe thrombosis but is compatible with devel-opment and reproduction. Genes Dev 9: 794-807.
5. Camerer E, Barker A, Duong DN, Ganesan R, Kataoka H, Cornelissen I et al. (2010). Local protease signaling contri-butes to neural tube closure in the mouse embryo. Dev Cell 18: 25-38.
6. Carmeliet P, Schoonjans L, Kieckens L, Ream B, Degen J, Bronson R et al. (1994). Physiological consequences of loss of plasminogen activator gene function in mice. Nature 368: 419-424. (Pubitemid 24115347)
7. Chmielowiec J, Borowiak M, Morkel M, Stradal T, Munz B, Werner S et al. (2007). c-Met is essential for wound healing in the skin. J Cell Biol 177: 151-162. (Pubitemid 46588409)
8. Dai C, Saleem MA, Holzman LB, Mathieson P, Liu Y. (2010). Hepatocyte growth factor signaling ameliorates podocyte injury and proteinuria. Kidney Int 77: 962-973.
9. Gailani D, Lasky NM, Broze Jr GJ. (1997). A murine model of factor XI deficiency. Blood Coagul Fibrinolysis 8: 134-144. (Pubitemid 27211727)
10. Gherardi E, Sandin S, Petoukhov MV, Finch J, Youles ME, Ofverstedt LG et al. (2006). Structural basis of hepatocyte growth factor/scatter factor and MET signalling. Proc Natl Acad Sci USA 103: 4046-4051.
11. Hanahan D, Weinberg RA. (2000). The hallmarks of cancer. Cell 100: 57-70. (Pubitemid 30046295)
12. Hartmann G, Prospero T, Brinkmann V, Ozcelik C, Winter G, Hepple J et al. (1998). Engineered mutants of HGF/SF with reduced binding to heparan sulphate proteoglycans, decreased clearance and enhanced activity in vivo. Curr Biol 8: 125-134. (Pubitemid 28091570)
13. Herter S, Piper DE, Aaron W, Gabriele T, Cutler G, Cao P et al. (2005). Hepatocyte growth factor is a preferred in vitro substrate for human Hepsin, a membrane-anchored serine protease implicated in prostate and ovarian cancers. Biochem J 390: 125-136. (Pubitemid 41192238)
14. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, Thorgeirsson SS. (2004). Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci USA 101: 4477-4482. (Pubitemid 38437436)
15. Itoh H, Naganuma S, Takeda N, Miyata S, Uchinokura S, Fukushima T et al. (2004). Regeneration of injured intestinal mucosa is impaired in hepatocyte growth factor activator-deficient mice. Gastroenterology 127: 1423-1435. (Pubitemid 39457769)
16. Jin X, Yagi M, Akiyama N, Hirosaki T, Higashi S, Lin CY et al. (2006). Matriptase activates stromelysin (MMP-3) and promotes tumor growth and angiogenesis. Cancer Sci 97: 1327-1334. (Pubitemid 44614984)
17. Kang JY, Dolled-Filhart M, Ocal IT, Singh B, Lin CY, Dickson RB et al. (2003). Tissue microarray analysis of hepatocyte growth factor/Met pathway components reveals a role for Met, matriptase, and hepatocyte growth factor activator inhibitor 1 in the progres-sion of node-negative breast cancer. Cancer Res 63: 1101-1105. (Pubitemid 36278444)
18. Kirchhofer D, Lipari MT, Santell L, Billeci KL, Maun HR, Sandoval WN et al. (2007). Utilizing the activation mechanism of serine proteases to engineer hepatocyte growth factor into a Met antagonist. Proc Natl Acad Sci USA 104: 5306-5311. (Pubitemid 47175676)
19. Knudsen BS, Vande Woude G (2008). Showering c-MET-dependent cancers with drugs. Curr Opin Genet Dev 18: 87-96. (Pubitemid 351694452)
20. Lee SL, Dickson RB, Lin CY. (2000). Activation of hepatocyte growth factor and urokinase/plasminogen activator by matriptase, an epithelial membrane serine protease. J Biol Chem 275: 36720-36725. (Pubitemid 32002078)
21. Lichti U, Weinberg WC, Goodman L, Ledbetter S, Dooley T, Morgan D et al. (1993). in vivo regulation of murine hair growth: insights from grafting defined cell populations onto nude mice. J Invest Dermatol 101: 124S-129S. (Pubitemid 23216896)
22. List K, Bugge TH, Szabo R. (2006a). Matriptase: potent proteolysis on the cell surface. Mol Med 12: 1-7. (Pubitemid 44128372)
23. List K, Haudenschild CC, Szabo R, Chen W, Wahl SM, Swaim W et al. (2002). Matriptase/MT-SP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene 21: 3765-3779. (Pubitemid 34620539)
24. List K, Szabo R, Molinolo A, Nielsen BS, Bugge TH. (2006b). Delineation of matriptase protein expression by enzymatic gene trapping suggests diverging roles in barrier function, hair formation, and squamous cell carcinogenesis. Am J Pathol 168: 1513-1525.
25. List K, Szabo R, Molinolo A, Sriuranpong V, Redeye V, Murdock T et al. (2005). Deregulated matriptase causes ras-independent multi-stage carcinogenesis and promotes ras-mediated malignant trans-formation. Genes Dev 19: 1934-1950. (Pubitemid 41186993)
26. Lopez-Otin C, Hunter T. (2010). The regulatory crosstalk between kinases and proteases in cancer. Nat Rev Cancer 10: 278-292.
27. Ma H, Saenko M, Opuko A, Togawa A, Soda K, Marlier A et al. (2009). Deletion of the Met receptor in the collecting duct decreases renal repair following ureteral obstruction. Kidney Int 76: 868-876.
28. McCawley LJ, Crawford HC, King Jr LE, Mudgett J, Matrisian LM. (2004). A protective role for matrix metalloproteinase-3 in squamous cell carcinoma. Cancer Res 64: 6965-6972. (Pubitemid 39331006)
29. Molinolo AA, Amornphimoltham P, Squarize CH, Castilho RM, Patel V, Gutkind JS. (2009). Dysregulated molecular networks in head and neck carcinogenesis. Oral Oncol 45: 324-334.
30. Molinolo AA, Hewitt SM, Amornphimoltham P, Keelawat S, Rangdaeng S, Meneses Garcia A et al. (2007). Dissecting the Akt/mammalian target of rapamycin signaling network: emerging results from the head and neck cancer tissue array initiative. Clin Cancer Res 13: 4964-4973. (Pubitemid 47502060)
31. Naldini L, Tamagnone L, Vigna E, Sachs M, Hartmann G, Birchmeier W et al. (1992). Extracellular proteolytic cleavage by urokinase is required for activation of hepatocyte growth factor/scatter factor. EMBO J 11: 4825-4833. (Pubitemid 23023425)
32. Owen KA, Qiu D, Alves J, Schumacher AM, Kilpatrick LM, Li J et al. (2010). Pericellular activation of hepatocyte growth factor by the transmembrane serine proteases matriptase and hepsin, but not by the membrane-associated protease uPA. Biochem J 426: 219-228.
33. Park M, Dean M, Cooper CS, Schmidt M, O'Brien SJ, Blair DG et al. (1986). Mechanism of met oncogene activation. Cell 45: 895-904. (Pubitemid 16083694)
34. Pauer HU, Renne T, Hemmerlein B, Legler T, Fritzlar S, Adham I et al. (2004). Targeted deletion of murine coagulation factor XII gene-a model for contact phase activation in vivo. Thromb Haemost 92: 503-508. (Pubitemid 39248007)
35. Peek M, Moran P, Mendoza N, Wickramasinghe D, Kirchhofer D. (2002). Unusual proteolytic activation of pro-hepatocyte growth factor by plasma kallikrein and coagulation factor XIa. J Biol Chem 277: 47804-47809. (Pubitemid 36159306)
36. Raimondi AR, Molinolo A, Gutkind JS. (2009). Rapamycin prevents early onset of tumorigenesis in an oral-specific K-ras and p53 two-hit carcinogenesis model. Cancer Res 69: 4159-4166.
37. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. (2004). ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6: 1-6. (Pubitemid 38391943)
38. Schmidt C, Bladt F, Goedecke S, Brinkmann V, Zschiesche W, Sharpe M et al. (1995). Scatter factor/hepatocyte growth factor is essential for liver development. Nature 373: 699-702.
39. Seiwert TY, Jagadeeswaran R, Faoro L, Janamanchi V, Nallasura V, El Dinali M et al. (2009). The MET receptor tyrosine kinase is a potential novel therapeutic target for head and neck squamous cell carcinoma. Cancer Res 69: 3021-3031.
40. Shanmukhappa K, Matte U, Degen JL, Bezerra JA. (2009). Plasmin-mediated proteolysis is required for hepatocyte growth factor activation during liver repair. J Biol Chem 284: 12917-12923.
41. Shimomura T, Miyazawa K, Komiyama Y, Hiraoka H, Naka D, Morimoto Y et al. (1995). Activation of hepatocyte growth factor by two homologous proteases, blood-coagulation factor XIIa and hepatocyte growth factor activator. Eur J Biochem 229: 257-261.
42. Squarize CH, Castilho RM, Gutkind JS. (2008). Chemoprevention and treatment of experimental Cowden's disease by mTOR inhibition with rapamycin. Cancer Res 68: 7066-7072.
43. Szabo R, Bugge TH. (2008). Type II transmembrane serine proteases in development and disease. Int J Biochem Cell Biol 40: 1297-1316.
44. Takeuchi T, Harris JL, Huang W, Yan KW, Coughlin SR, Craik CS. (2000). Cellular localization of membrane-type serine protease 1 and identification of protease-activated receptor-2 and single-chain urokinase-type plasminogen activator as substrates. J Biol Chem 275: 26333-26342.
45. Uehara Y, Minowa O, Mori C, Shiota K, Kuno J, Noda T et al. (1995). Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373: 702-705.
46. Uhland K (2006). Matriptase and its putative role in cancer. Cell Mol Life Sci 63: 2968-2978. (Pubitemid 46072302)
47. Vivanco I, Sawyers CL. (2002). The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2: 489-501. (Pubitemid 37328931)
48. Williams-Simons L, Westphal H. (1999). EIIaCre\utility of a general deleter strain. Transgenic Res 8: 53-54.
49. Wu Q, Yu D, Post J, Halks-Miller M, Sadler JE, Morser J. (1998). Generation and characterization of mice deficient in hepsin, a hepatic transmembrane serine protease. J Clin Invest 101: 321-326. (Pubitemid 28067328)
50. Zhou HM, Nichols A, Meda P, Vassalli JD. (2000). Urokinase-type plasminogen activator and its receptor synergize to promote pathogenic proteolysis. Embo J 19: 4817-4826.