Hepatocyte growth factor activation inhibitors (HAI-1 and HAI-2) regulate HGF-induced invasion of human breast cancer cells

International Journal of Cancer

Volumn 119, Issue 5, 2006, Pages 1176-1183

  Parr, Christian ^a   Jiang, Wen G ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

HAI 1; HAI 2; HGF; HGFA; Matriptase

Indexed keywords

HEPSIN; MATRIPTASE; PROTEIN HAI 1; PROTEIN HAI 2; RIBOZYME; SCATTER FACTOR; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; UROKINASE;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER INVASION; CELL INTERACTION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FIBROBLAST; GENETIC RECOMBINATION; GROWTH REGULATION; HUMAN; HUMAN CELL; METASTASIS; PRIORITY JOURNAL; TRANSGENE; TUMOR GROWTH;

ANIMALS; ANTINEOPLASTIC AGENTS; BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; COLONIC NEOPLASMS; DOGS; FEMALE; FIBROBLASTS; HUMANS; KIDNEY; MALE; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; NEOPLASMS; PROSTATIC NEOPLASMS; RECOMBINANT PROTEINS; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, CATALYTIC; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; TRANSGENES; TRYPSIN INHIBITOR, KUNITZ SOYBEAN; URINARY PLASMINOGEN ACTIVATOR;

EID: 33746355289     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.21881     Document Type: Article

References (51)

1. Grant DS, Kleinman HK, Goldberg ID, Bhargava MM, Nickoloff BJ, Kinsella JL, Polverini P, Rosen EM. Scatter factor induces blood-vessel formation in vivo. Proc Natl Acad Sci USA 1993;90:1937-41.
2. Sugawara J, Fukaya T, Murakami T, Yoshida H, Yajima A. Hepatocyte growth factor stimulates proliferation, migration, and lumen formation of human endometrial epithelial cells in vitro. Biol Reprod 1997;57:936-42.
3. Jiang WG, Martin TA, Parr C, Davies G, Matsumoto K, Nakamura T. Hepatocyte growth factor, its receptor, and their potential value in cancer therapies. Crit Rev Oncol Hematol 2005;53:35-69.
4. Tuck AB, Park M, Sterns EE, Boag A, Elliott BE. Coexpression of hepatocyte growth factor and receptor (Met) in human breast carcinoma. Am J Pathol 1996;148:225-32.
5. Toi M, Taniguchi T, Ueno T, Asano M, Funata N, Sekiguchi K, Iwanari H, Tominaga T. Significance of circulating hepatocyte growth factor level as a prognostic indicator in primary breast cancer. Clin Cancer Res 1998;4:659-64.
6. Taniguchi T, Toi M, Inada K, Imazawa T, Yamamoto Y, Tominaga T. Serum concentrations of hepatocyte growth factor in breast cancer patients. Clin Cancer Res 1995;1:1031-4.
7. Woodbury RL, Varnum SM, Zangar RC. Elevated HGF levels in sera from breast cancer patients detected using a protein microarray ELISA. J Proteome Res 2002;1:233-7.
8. Elliot BE, Hung WL, Boag AH, Tuck AB. The role of hepatocyte growth factor (scatter factor) in epithelial-mesenchymal transition in breast cancer. Can J Physiol Pharmacol 2002;80:91-102.
9. Narita T, Toi M, Sekiguchi K, Iwanari H, Matsuura N, Kimura N, Mitsuoka C, Kannagi R. Hepatocyte growth factor in the sera of patients with gastrointestinal and breast cancer. Gan To Kagaku Ryoho 1997;24:2159-62.
10. Fukuura T, Mik C, Inoue T, Matsumoto K, Suzuki H. Serum hepatocyte growth factor as an index of disease status of patients with colorectal carcinoma. Br J Cancer 1998;78:454-9.
11. Yamashita J, Ogawa M, Yamashita S, Nomura K, Kuramoto M, Saishoji T, Shin S. Immunoreactive hepatocyte growth-factor is a strong and independent predictor of recurrence and survival in human breast-cancer. Cancer Res 1994;54:1630-3.
12. Grey AM, Schor AM, Rushton G, Ellis I, Schor SL. Purification of the migration stimulating factor produced by fetal and breast cancer patient fibroblasts. Proc Natl Acad Sci USA 1989;86:2438-42.
13. Camps JL, Chang SM, Hsu TC, Freeman MR, Hong SJ, Zhau HE, von Eschenbach AC, Chung LW. Fibroblast-mediated acceleration of human epithelial tumour growth in vivo. Proc Natl Acad Sci USA 1990;87:75-9.
14. Ohuchida K, Mizumoto K, Murakami M, Qian LW, Sato N, Nagai E, Matsumoto K, Nakamura T, Tanaka M. Radiation to stromal fibroblasts increases invasiveness of pancreatic cancer cells through tumor-stromal interactions. Cancer Res 2004;64:3215-22.
15. Hartmann G, Naldini L, Weidner KM, Sachs M, Vigna E, Comoglio PM, Birchmeier W. A functional domain in the heavy-chain of scatter/factor hepatocyte growth-factor binds the c-Met receptor and induces cell-dissociation but not mitogenesis. Proc Natl Acad Sci USA 1992;89:11574-8.
16. Gak E, Taylor WG, Chan AM, Rubin JS. Processing of hepatocyte growth factor to the heterodimeric form is required for biological activity. FEBS Lett 1992;311:17-21.
17. Miyazawa K, Shimomura T, Kitamura A, Kondo J, Morimoto Y, Kitamura N. Molecular-cloning and sequence-analysis of the cDNA for a human serine protease responsible for activation of hepatocyte growth-factor. Structural similarity of the protease precursor to blood-coagulation factor-XII. J Biol Chem 1993;268:10024-8.
18. Parr C, Jiang WG. Expression of hepatocyte growth factor/scatter factor, its activator, inhibitors and the c-Met receptor in human cancer cells. Int J Oncol 2001;19:857-63.
19. Parr C, Watkins G, Mansel RE, Jiang WG. The hepatocyte growth factor regulatory factors and human breast cancer. Clin Cancer Res 2004; 10:202-11.
20. Shimomura T, Denda K, Kitamura A, Kawaguchi T, Kito M, Kondo J, Kagaya S, Qin L, Takata H, Miyazawa K, Kitamura N. Hepatocyte growth factor activator inhibitor, a novel Kunitz-type serine protease inhibitor. J Biol Chem 1997;272:6370-6.
21. Kawaguchi T, Qin L, Shimomura T, Kondo J, Matsumoto K, Denda K, Kitamura N. Purification and cloning of hepatocyte growth factor activator inhibitor type 2, a Kunitz-type serine protease inhibitor. J Biol Chem 1997;272:27558-64.
22. Oberst M, Anders J, Xie B, Singh B, Ossandon M, Johnson M, Dickson RB, Lin CY. Matriptase and HAI-1 are expressed by normal and malignant epithelial cells in vitro and in vivo. Am J Pathol 2001;158: 1301-11.
23. Kirchhofer D, Peek M, Li W, Stamos J, Eigenbrot C, Kadkhodayan S, Elliott JM, Corpuz RT, Lazarus RA, Moran P. 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.
24. Shia S, Stamos J, Kirchhofer D, Fan B, Wu J, Corpuz RT, Santell L, Lazarus RA, Eigenbrot C. 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.
25. Lee S, 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.
26. Naldini L, Vigna E, Bardelli A, Follenzi A, Galimi F, Comoglio PM. Biological activation of pro-HGF (hepatocyte growth factor) by urokinase is controlled by a stoichiometric reaction. J Biol Chem 1995;270: 603-11.
27. Herter S, Piper DE, Aaron W, Gabriele T, Cutler G, Cao P, Bhatt AS, Choe Y, Craik CS, Walker N, Meininger D, Hoey T, 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.
28. Stoker M, Gherardi E, Perryman M, Gray J. Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature 1987;327: 239-42.
29. Jiang WG, Puntis MCA, Hallett MB. Monocyte-conditioned media possess a novel factor which increases motility of cancer-cells. Int J Cancer 1993;53:426-31.
30. Jiang WG, Grimshaw D, Lane J, Martin TA, Abounader R, Laterra J, Mansel RE. A hammerhead ribozyme suppresses expression of hepatocyte growth factor/scatter factor receptor c-MET and reduces migration and invasiveness of breast cancer cells. Clin Cancer Res 2001;7: 2555-62.
31. Jiang WG, Davies G, Fodstad O. Com-1/P8 in oestrogen regulated growth of breast cancer cells, the ER-β connection. Biochem Biophys Res Commun 2005;330:253-62.
32. Parr C, Hiscox S, Nakamura T, Matsumoto K, Jiang WG. NK4, a new HGF/SF variant, is an antagonist to the influence of HGF/SF on the motility and invasion of colon cancer cells. Int J Cancer 2000;85:563-70.
33. Ueda K, Iwahashi M, Matsuura I, Nakamori M, Nakamura M, Ojima T, Naka T, Ishida K, Matsumoto K, Nakamura T, Yamaue H. Adenoviral-mediated gene transduction of the hepatocyte growth factor (HGF) antagonist, NK4, suppresses peritoneal metastases of gastric cancer in nude mice. Eur J Cancer 2004;40:2135-42.
34. Kubota T, Fujiwara H, Amaike H, Takashima K, Inada S, Atsuji K, Yoshimura M, Matsumoto K, Nakamura T, Yamagishi H. Reduced HGF expression in subcutaneous CT26 tumor genetically modified to secrete NK4 and its possible relation with antitumor effects. Cancer Sci 2004;95:321-7.
35. Wen J, Matsumoto K, Taniura N, Tomioka D, Nakamura T. Hepatic gene expression of NK4, an HGF-antagonist/angiogenesis inhibitor, suppresses liver metastasis and invasive growth of colon cancer in mice. Cancer Gene Ther 2004;11:419-30.
36. Brockmann MA, Papadimitriou A, Brandt M, Fillbrandt R, Westphal M, Lamszus K. Inhibition of intracerebral glioblastoma growth by local treatment with the scatter factor/hepatocyte growth factor-antagonist NK4. Clin Cancer Res 2003;9:4578-85.
37. Davies G, Mason MD, Martin TA, Parr C, Watkins G, Lane J, Matsumoto K, Nakamura T, Jiang WG. The HGF/SF antagonist NK4 reverses fibroblast- and HGF-induced prostate tumor growth and angiogenesis in vivo. Int J Cancer 2003;106:348-54.
38. Martin TA, Parr C, Davies G, Watkins G, Lane J, Matsumoto K, Nakamura T, Mansel RE, Jiang WG. Growth and angiogenesis of human breast cancer in a nude mouse tumour model is reduced by NK4, a HGF/SF antagonist. Carcinogenesis 2003;24:1317-23.
39. Parr C, Davies G, Nakamura T, Matsumoto K, Mason MD, Jiang WG. The HGF/SF-induced phosphorylation of paxillin, matrix adhesion, and invasion of prostate cancer cells were suppressed by NK4, an HGF/SF variant. Biochem Biophys Res Commun 2001;285:1330-7.
40. Jiang WG, Hiscox SE, Parr C, Martin TA, Matsumoto K, Nakamura T, Mansel RE. Antagonistic effect of NK4, a novel hepatocyte growth factor variant, on in vitro angiogenesis of human vascular endothelial cells. Clin Cancer Res 1999;5:3695-703.
41. Miyazawa K, Shimomura T, Kitamura N. Activation of hepatocyte growth factor, in the injured tissues, is mediated by hepatocyte growth factor activator. J Biol Chem 1996;271:3615-8.
42. Matsubara Y, Ichinose M, Yahagi N, Tsukada S, Oka M, Miki K, Kimura S, Omata M, Shiokawa K, Kitamura N, Kaneko Y, Fukamachi H. Hepatocyte growth factor activator: a possible regulator of morphogenesis during fetal development of the rat gastrointestinal tract. Biochem Biophys Res Commun 1998;253:477-84.
43. Kataoka H, Hamasuna R, Itoh H, Kitamura N, Koono M. Activation of hepatocyte growth factor/scatter factor in colorectal carcinoma. Cancer Res 2000;60:6148-59.
44. van Adelsberg J, Sehgal S, Kukes A, Brady C, Barasch J, Yang J, Huan Y. Activation of hepatocyte growth factor (HGF) by endogenous HGF activator is required for metanephric kidney morphogenesis in vitro. J Biol Chem 2001;18:15099-106.
45. Mazzone M, Basilico C, Cavassa S, Pennacchietti S, Risio M, Naldini L, Comoglio PM, Michieli P. An uncleavable form of pro-scatter factor suppresses tumor growth and dissemination in mice. J Clin Invest 2004;114:1418-32.
46. Suzuki M, Kobayashi H, Tanaka Y, Hirashima Y, Kanayama N, Takei Y, Saga Y, Suzuki M, Itoh H, Terao T. Suppression of invasion and peritoneal carcinomatosis of ovarian cancer cell line by overexpression of bikunin. Int J Cancer 2003;104:289-302.
47. Denda K, Shimomura T, Kawaguchi T, Miyazawa K, Kitamura N. Functional characterisation of Kunitz domains in hepatocyte growth factor activator inhibitor type-1. J Biol Chem 2002;277:14053-9.
48. Kobayashi H, Suzuki M, Kanayama N, Takashi N, Takigawa M, Terao T. Suppression of urokinase receptor expression by bikunin is associated with inhibition of upstream targets of extracellular signal-regulated kinase-dependant cascade. Eur J Biochem 2002;269:3945-57.
49. Takeuchi T, Harris JL, Huang W, Yan KW, Coughlin SR, Craik CS. 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 2000;275:26333-42.
50. Forbs D, Thiel S, Stella MC, Sturzebecher A, Schweinitz A, Steinmetzer T, Sturzebecher J, Uhland K. In vitro inhibition of matriptase prevents invasive growth of cell lines of prostate and colon carcinoma. Int J Oncol 2005;27:1061-70.
51. 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.