Proteolytic activation of pro-macrophage-stimulating protein by hepsin

Molecular Cancer Research

Volumn 9, Issue 9, 2011, Pages 1175-1186

  Ganesan, Rajkumar ^a   Kolumam, Ganesh A ^a   Lin, S Jack ^a   Xie, Ming Hong ^a   Santell, Lydia ^a   Wu, Thomas D ^a   Lazarus, Robert A ^a   Chaudhuri, Amitabha ^a   Kirchhofer, Daniel ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HEPSIN; HYBRID PROTEIN; LIPOPOLYSACCHARIDE; MATRIPTASE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PROTEIN ANTIBODY; PROTEIN KINASE; PROTEIN KINASE B; S6 KINASE; SCATTER FACTOR;

ANGIOGENESIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER CELL; CELL STRAIN LNCAP; CELL SURFACE; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME SUBSTRATE; HOMEOSTASIS; HUMAN; INCUBATION TEMPERATURE; LIVER CELL; MACROPHAGE; METASTASIS; OVARY CARCINOMA; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; FEMALE; HUMANS; MACROPHAGES; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; OVARIAN NEOPLASMS; PROSTATIC NEOPLASMS; PROTEIN PRECURSORS; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR PROTEIN-TYROSINE KINASES; RECOMBINANT FUSION PROTEINS; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 80052840444     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0004     Document Type: Article

References (60)

1. Leonard EJ, Danilkovitch A. Macrophage stimulating protein. Adv Cancer Res 2000;77:139-67. (Pubitemid 29439304)
2. Donate LE, Gherardi E, Srinivasan N, Sowdhamini R, Aparicio S, Blundell TL. Molecular evolution and domain structure of plasminogen-related growth factors (HGF/SF and HGF1/MSP). Protein Sci 1994;3:2378-94.
3. Carafoli F, Chirgadze DY, Blundell TL, Gherardi E. Crystal structure of the beta-chain of human hepatocyte growth factor-like/macrophage stimulating protein. FEBS J 2005;272:5799-807. (Pubitemid 41689352)
4. Rampino T, Collesi C, Gregorini M, Maggio M, Soccio G, Guallini P, et al. Macrophage-stimulating protein is produced by tubular cells and activates mesangial cells. J Am Soc Nephrol 2002;13:649-57. (Pubitemid 34183929)
5. Yoshimura T, Yuhki N, Wang MH, Skeel A, Leonard EJ. Cloning, sequencing, and expression of human macrophage stimulating protein (MSP, MST1) confirms MSP as a member of the family of kringle proteins and locates the MSP gene on chromosome 3. J Biol Chem 1993;268:15461-8. (Pubitemid 23222036)
6. Skeel A, Yoshimura T, Showalter SD, Tanaka S, Appella E, Leonard EJ. Macrophage stimulating protein: purification, partial amino acid sequence, and cellular activity. J Exp Med 1991;173:1227-34.
7. Maun HR, Kirchhofer D, Lazarus RA. Pseudo-active sites of protease domains: HGF/Met and Sonic hedgehog signaling in cancer. Biol Chem 2010;391:881-92.
8. Kirchhofer D, Lipari MT, Santell L, Billeci KL, Maun HR, Sandoval WN, et al. Utilizing the activation mechanism of serine proteases to engineer hepatocyte growth factor into a Met antagonist. Proc Natl Acad Sci U S A 2007;104:5306-11. (Pubitemid 47175676)
9. Kirchhofer D, Yao X, Peek M, Eigenbrot C, Lipari MT, Billeci KL, et al. Structural and functional basis of the serine protease-like hepatocyte growth factor beta-chain in Met binding and signaling. J Biol Chem 2004;279:39915-24. (Pubitemid 39258264)
10. 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;274:29937-43.
11. Bhatt AS, Welm A, Farady CJ, Vasquez M, Wilson K, Craik CS. Coordinate expression and functional profiling identify an extracellular proteolytic signaling pathway. Proc Natl Acad Sci U S A 2007;104:5771-6. (Pubitemid 47175609)
12. Kawaguchi M, Orikawa H, Baba T, Fukushima T, Kataoka H. Hepatocyte growth factor activator is a serum activator of single-chain precursor macrophage-stimulating protein. FEBS J 2009;276:3481-90.
13. Wang MH, Gonias SL, Skeel A, Wolf BB, Yoshimura T, Leonard EJ. Proteolytic activation of single-chain precursor macrophage-stimulating protein by nerve growth factor-gamma and epidermal growth factor-binding protein, members of the kallikrein family. J Biol Chem 1994;269:13806-10. (Pubitemid 24191124)
14. Wang MH, Skeel A, Leonard EJ. Proteolytic cleavage and activation of pro-macrophage-stimulating protein by resident peritoneal macrophage membrane proteases. J Clin Invest 1996;97:720-7. (Pubitemid 26057091)
15. Wang MH, Yoshimura T, Skeel A, Leonard EJ. 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;269:3436-40. (Pubitemid 24237662)
16. Netzel-Arnett S, Hooper JD, Szabo R, Madison EL, Quigley JP, Bugge TH, et al. Membrane anchored serine proteases: a rapidly expanding group of cell surface proteolytic enzymes with potential roles in cancer. Cancer Metastasis Rev 2003;22:237-58. (Pubitemid 36561060)
17. Wu Q, Parry G. Hepsin and prostate cancer. Front Biosci 2007;12:5052-9.
18. Somoza JR, Ho JD, Luong C, Ghate M, Sprengeler PA, Mortara K, et al. The structure of the extracellular region of human hepsin reveals a serine protease domain and a novel scavenger receptor cysteine-rich (SRCR) domain. Structure 2003;11:1123-31. (Pubitemid 37103073)
19. Herter S, Piper DE, Aaron W, Gabriele T, Cutler G, Cao P, et al. 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 2005;390:125-36. (Pubitemid 41192238)
20. Dhanasekaran SM, Barrette TR, Ghosh D, Shah R, Varambally S, Kurachi K, et al. Delineation of prognostic biomarkers in prostate cancer. Nature 2001;412:822-6. (Pubitemid 32801464)
21. Luo J, Duggan DJ, Chen Y, Sauvageot J, Ewing CM, Bittner ML, et al. Human prostate cancer and benign prostatic hyperplasia: molecular dissection by gene expression profiling. Cancer Res 2001;61:4683-8. (Pubitemid 32691876)
22. Magee JA, Araki T, Patil S, Ehrig T, True L, Humphrey PA, et al. Expression profiling reveals hepsin overexpression in prostate cancer. Cancer Res 2001;61:5692-6. (Pubitemid 32769078)
23. Stamey TA, Warrington JA, Caldwell MC, Chen Z, Fan Z, Mahadevappa M, et al. Molecular genetic profiling of Gleason grade 4/5 prostate cancers compared to benign prostatic hyperplasia. J Urol 2001;166:2171-7. (Pubitemid 33065250)
24. Stephan C, Yousef GM, Scorilas A, Jung K, Jung M, Kristiansen G, et al. Hepsin is highly over expressed in and a new candidate for a prognostic indicator in prostate cancer. J Urol 2004;171:187-91. (Pubitemid 37549120)
25. Welsh JB, Sapinoso LM, Su AI, Kern SG, Wang-Rodriguez J, Moskaluk CA, et al. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res 2001;61:5974-8. (Pubitemid 32762523)
26. Xuan JA, Schneider D, Toy P, Lin R, Newton A, Zhu Y, et al. Antibodies neutralizing hepsin protease activity do not impact cell growth but inhibit invasion of prostate and ovarian tumor cells in culture. Cancer Res 2006;66:3611-9.
27. Morrissey C, True LD, Roudier MP, Coleman IM, Hawley S, Nelson PS, et al. Differential expression of angiogenesis associated genes in prostate cancer bone, liver and lymph node metastases. Clin Exp Metastasis 2008;25:377-88.
28. Klezovitch O, Chevillet J, Mirosevich J, Roberts RL, Matusik RJ, Vasioukhin V. Hepsin promotes prostate cancer progression and metastasis. Cancer Cell 2004;6:185-95. (Pubitemid 39485690)
29. Li W, Wang BE, Moran P, Lipari T, Ganesan R, Corpuz R, et al. Pegylated kunitz domain inhibitor suppresses hepsin-mediated invasive tumor growth and metastasis. Cancer Res 2009;69:8395-402.
30. Tanimoto H, Yan Y, Clarke J, Korourian S, Shigemasa K, Parmley TH, et al. Hepsin, a cell surface serine protease identified in hepatoma cells, is overexpressed in ovarian cancer. Cancer Res 1997;57:2884-7. (Pubitemid 27315033)
31. Zacharski LR, Ornstein DL, Memoli VA, Rousseau SM, Kisiel W. Expression of the factor VII activating protease, hepsin, in situ in renal cell carcinoma. Thromb Haemost 1998;79:876-7.
32. Betsunoh H, Mukai S, Akiyama Y, Fukushima T, Minamiguchi N, Hasui Y, et al. Clinical relevance of hepsin and hepatocyte growth factor activator inhibitor type 2 expression in renal cell carcinoma. Cancer Sci 2007;98:491-8. (Pubitemid 46562738)
33. Matsuo T, Nakamura K, Takamoto N, Kodama J, Hongo A, Abrzua F, et al. Expression of the serine protease hepsin and clinical outcome of human endometrial cancer. Anticancer Res 2008;28:159-64. (Pubitemid 351362896)
34. Kirchhofer D, Peek M, Lipari MT, Billeci K, Fan B, Moran P. Hepsin activates pro-hepatocyte growth factor and is inhibited by hepatocyte growth factor activator inhibitor-1B (HAI-1B) and HAI-2. FEBS Lett 2005;579:1945-50. (Pubitemid 40404036)
35. Moran P, Li W, Fan B, Vij R, Eigenbrot C, Kirchhofer D. Pro-urokinasetype plasminogen activator is a substrate for hepsin. J Biol Chem 2006;281:30439-46. (Pubitemid 44596152)
36. Tripathi M, Nandana S, Yamashita H, Ganesan R, Kirchhofer D, Quaranta V. Laminin-332 is a substrate for hepsin, a protease associated with prostate cancer progression. J Biol Chem 2008;283:30576-84.
37. Kazama Y, Hamamoto T, Foster DC, Kisiel W. Hepsin, a putative membrane-associated serine protease, activates human factor VII and initiates a pathway of blood coagulation on the cell surface leading to thrombin formation. J Biol Chem 1995;270:66-72.
38. Chen M, Chen LM, Lin CY, Chai KX. Hepsin activates prostasin and cleaves the extracellular domain of the epidermal growth factor receptor. Mol Cell Biochem 2010;337:259-66.
39. Wahl RC, Costigan VJ, Batac JP, Chen K, Cam L, Courchesne PL, et al. Mutation of Cys672 allows recombinant expression of activatible macrophage-stimulating protein. J Biol Chem 1997;272:15053-6. (Pubitemid 27255515)
40. Shia S, Stamos J, Kirchhofer D, Fan B, Wu J, Corpuz RT, et al. Conformational lability in serine protease active sites: structures of hepatocyte growth factor activator (HGFA) alone and with the inhibitory domain from HGFA inhibitor-1B. J Mol Biol 2005;346:1335-49. (Pubitemid 40248833)
41. Kirchhofer D, Peek M, Li W, Stamos J, Eigenbrot C, Kadkhodayan S, et al. Tissue expression, protease specificity, and Kunitz domain functions of hepatocyte growth factor activator inhibitor-1B (HAI-1B), a new splice variant of HAI-1. J Biol Chem 2003;278:36341-9. (Pubitemid 37139961)
42. Ganesan R, Eigenbrot C, Wu Y, Liang WC, Shia S, Lipari MT, et al. Unraveling the allosteric mechanism of serine protease inhibition by an antibody. Structure 2009;17:1614-24.
43. Schechter I, Berger A. On the active site of proteases. 3. Mapping the active site of papain; specific peptide inhibitors of papain. Biochem Biophys Res Commun 1968;32:898-902.
44. Lee SL, Dickson RB, Lin CY. Activation of hepatocyte growth factor and urokinase/plasminogen activator by matriptase, an epithelial membrane serine protease. J Biol Chem 2000;275:36720-5. (Pubitemid 32002078)
45. Iwama A, Wang MH, Yamaguchi N, Ohno N, Okano K, Sudo T, et al. Terminal differentiation of murine resident peritoneal macrophages is characterized by expression of the STK protein tyrosine kinase, a receptor for macrophage-stimulating protein. Blood 1995;86:3394-403.
46. Hess KA, Waltz SE, Toney-Earley K, Degen SJ. The receptor tyrosine kinase Ron is expressed in the mouse ovary and regulates inducible nitric oxide synthase levels and ovulation. Fertil Steril 2003;80Suppl 2:747-54. (Pubitemid 37152389)
47. Wang MH, Cox GW, Yoshimura T, Sheffler LA, Skeel A, Leonard EJ. Macrophage-stimulating protein inhibits induction of nitric oxide production by endotoxin- or cytokine-stimulated mouse macrophages. J Biol Chem 1994;269:14027-31. (Pubitemid 24191155)
48. Beliveau F, Desilets A, Leduc R. Probing the substrate specificities of matriptase, matriptase-2, hepsin and DESC1 with internally quenched fluorescent peptides. FEBS J 2009;276:2213-26.
49. Andreasen PA, Kjoller L, Christensen L, Duffy MJ. The urokinase-type plasminogen activator system in cancer metastasis: a review. Int J Cancer 1997;72:1-22. (Pubitemid 27314632)
50. Danø K, Behrendt N, Høyer-Hansen G, Johnsen M, Lund LR, Ploug M, et al. Plasminogen activation and cancer. Thromb Haemost 2005;93:676-81. (Pubitemid 40485402)
51. O'Toole JM, Rabenau KE, Burns K, Lu D, Mangalampalli V, Balderes P, 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;66:9162-70. (Pubitemid 44521136)
52. Thobe MN, Gurusamy D, Pathrose P, Waltz SE. The Ron receptor tyrosine kinase positively regulates angiogenic chemokine production in prostate cancer cells. Oncogene 2009;29:214-26.
53. Thomas RM, Jaquish DV, French RP, Lowy AM. The RON tyrosine kinase receptor regulates vascular endothelial growth factor production in pancreatic cancer cells. Pancreas 2010;39:301-7.
54. Szabo R, Hobson JP, List K, Molinolo A, Lin CY, Bugge TH. Potent inhibition and global co-localization implicate the transmembrane Kunitz-type serine protease inhibitor hepatocyte growth factor activator inhibitor-2 in the regulation of epithelial matriptase activity. J Biol Chem 2008;283:29495-504.
55. Wang MH, Skeel A, Yoshimura T, Copeland TD, Sakaguchi K, Leonard EJ. Antibodies to macrophage stimulating protein (MSP): specificity, epitope interactions, and immunoassay of MSP in human serum. J Leukoc Biol 1993;54:289-95. (Pubitemid 23317695)
56. 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 1996;226:39-46. (Pubitemid 26238925)
57. Naldini L, Tamagnone L, Vigna E, Sachs M, Hartmann G, Birchmeier W, et al. Extracellular proteolytic cleavage by urokinase is required for activation of hepatocyte growth factor/scatter factor. EMBO J 1992;11:4825-33. (Pubitemid 23023425)
58. Hooper JD, Campagnolo L, Goodarzi G, Truong TN, Stuhlmann H, Quigley JP. Mouse matriptase-2: identification, characterization and comparative mRNA expression analysis with mouse hepsin in adult and embryonic tissues. Biochem J 2003;373:689-702. (Pubitemid 36981079)
59. Bezerra JA, Witte DP, Aronow BJ, Degen SJ. Hepatocyte-specific expression of the mouse hepatocyte growth factor-like protein. Hepatology 1993;18:394-9. (Pubitemid 23225112)
60. Cantaluppi V, Biancone L, Romanazzi GM, Figliolini F, Beltramo S, Galimi F, et al. Macrophage stimulating protein may promote tubular regeneration after acute injury. J Am Soc Nephrol 2008;19:1904-18.