HAI-2 suppresses the invasive growth and metastasis of prostate cancer through regulation of matriptase

Oncogene

Volumn 33, Issue 38, 2014, Pages 4643-4652

  Tsai, C H ^a   Teng, C H ^b   Tu, Y T ^b   Cheng, T S ^b   Wu, S R ^b   Ko, C J ^b   Shyu, H Y ^c   Lan, S W ^b   Huang, H P ^b   Tzeng, S F ^a   Johnson, M D ^d   Lin, C Y ^d   Hsiao, P W ^a   Lee, M S ^b  

^a AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c MINISTRY OF JUSTICE   (Taiwan)

^d GEORGETOWN UNIVERSITY   (United States)

Author keywords

cancer cell invasion; hepatocyte growth factor activator inhibitor 2; metastasis; prostate cancer; tumorigenicity

Indexed keywords

MEMBRANE PROTEIN; SERINE PROTEINASE; SPINT2 PROTEIN, HUMAN; ST14 PROTEIN, HUMAN;

ANIMAL; ARTICLE; CANCER TRANSPLANTATION; CARCINOGENESIS; CELL MOTION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LUNG TUMOR; LYMPH NODE METASTASIS; MALE; METABOLISM; METASTASIS; MOUSE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; TUMOR INVASION; TUMOR VOLUME;

ANIMALS; CARCINOGENESIS; CELL MOVEMENT; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; LYMPHATIC METASTASIS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; PROSTATIC NEOPLASMS; SERINE ENDOPEPTIDASES; TUMOR BURDEN;

EID: 84885199880     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.412     Document Type: Article

References (46)

1. Weiss L. Metastasis of cancer: a conceptual history from antiquity to the 1990s. Cancer Metastasis Rev 2000; 19: I-XI 193-383.
2. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003; 3: 453-458.
3. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature 2001; 411: 375-379.
4. Antalis TM, Buzza MS, Hodge KM, Hooper JD, Netzel-Arnett S. The cutting edge: membrane-anchored serine protease activities in the pericellular microenvironment. Biochem J 2010; 428: 325-346.
5. 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: 237-258.
6. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002; 2: 161-174.
7. Shi YE, Torri J, Yieh L, Wellstein A, Lippman ME, Dickson RB. Identification and characterization of a novel matrix-degrading protease from hormone-dependent human breast cancer cells. Cancer Res 1993; 53: 1409-1415.
8. Lin CY, Anders J, Johnson M, Sang QA, Dickson RB. Molecular cloning of cDNA for matriptase, a matrix-degrading serine protease with trypsin-like activity. J Biol Chem 1999; 274: 18231-18236.
9. Oberst M, Anders J, Xie B, Singh B, Ossandon M, Johnson M et al. Matriptase and HAI-1 are expressed by normal and malignant epithelial cells in vitro and in vivo. Am J Pathol 2001; 158: 1301-1311.
10. Lee MS, Kiyomiya K, Benaud C, Dickson RB, Lin CY. Simultaneous activation and hepatocyte growth factor activator inhibitor 1-mediated inhibition of matriptase induced at activation foci in human mammary epithelial cells. Am J Physiol Cell Physiol 2005; 288: C932-C941.
11. Lin CY, Anders J, Johnson M, Dickson RB. Purification and characterization of a complex containing matriptase and a Kunitz-type serine protease inhibitor from human milk. J Biol Chem 1999; 274: 18237-18242.
12. Szabo R, Molinolo A, List K, Bugge TH. Matriptase inhibition by hepatocyte growth factor activator inhibitor-1 is essential for placental development. Oncogene 2007; 26: 1546-1556.
13. Kang JY, Dolled-Filhart M, Ocal IT, Singh B, Lin CY, Dickson RB et al. 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 progression of node-negative breast cancer. Cancer Res 2003; 63: 1101-1105.
14. Saleem M, Adhami VM, Zhong W, Longley BJ, Lin CY, Dickson RB et al. A novel biomarker for staging human prostate adenocarcinoma: overexpression of matriptase with concomitant loss of its inhibitor, hepatocyte growth factor activator inhibitor-1. Cancer Epidemiol Biomarkers Prev 2006; 15: 217-227.
15. Wu SR, Cheng TS, Chen WC, Shyu HY, Ko CJ, Huang HP et al. Matriptase is involved in ErbB-2-induced prostate cancer cell invasion. Am J Pathol 2010; 177: 3145-3158.
16. List K, Szabo R, Molinolo A, Sriuranpong V, Redeye V, Murdock T et al. Deregulated matriptase causes ras-independent multistage carcinogenesis and promotes rasmediated malignant transformation. Genes Dev 2005; 19: 1934-1950.
17. Lin CY, Tseng IC, Chou FP, Su SF, Chen YW, Johnson MD et al. Zymogen activation, inhibition, and ectodomain shedding of matriptase. Front Biosci 2008; 13: 621-635.
18. Lee MS. Matrix-degrading type II transmembrane serine protease matriptase: its role in cancer development and malignancy. J Cancer Molecules 2006; 2: 183-190.
19. 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: 36720-36725.
20. 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: 26333-26342.
21. Jin X, Yagi M, Akiyama N, Hirosaki T, Higashi S, Lin CY et al. Matriptase activates stromelysin (MMP-3) and promotes tumor growth and angiogenesis. Cancer Sci 2006; 97: 1327-1334.
22. Satomi S, Yamasaki Y, Tsuzuki S, Hitomi Y, Iwanaga T, Fushiki T. A role for membrane-type serine protease (MT-SP1) in intestinal epithelial turnover. Biochem Biophys Res Commun 2001; 287: 995-1002.
23. Kawaguchi T, Qin L, Shimomura T, Kondo J, Matsumoto K, Denda K et al. Purification and cloning of hepatocyte growth factor activator inhibitor type 2, a Kunitz-type serine protease inhibitor. J Biol Chem 1997; 272: 27558-27564.
24. Marlor CW, Delaria KA, Davis G, Muller DK, Greve JM, Tamburini PP. Identification and cloning of human placental bikunin, a novel serine protease inhibitor containing two Kunitz domains. J Biol Chem 1997; 272: 12202-12208.
25. 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: 29495-29504.
26. Heinz-Erian P, Muller T, Krabichler B, Schranz M, Becker C, Ruschendorf F et al. Mutations in SPINT2 cause a syndromic form of congenital sodium diarrhea. Am J Hum Genet 2009; 84: 188-196.
27. Huang HP, Chang MH, Chen YT, Hsu HY, Chiang CL, Cheng TS et al. Persistent elevation of hepatocyte growth factor activator inhibitors in cholangiopathies affects liver fibrosis and differentiation. Hepatology 2012; 55: 161-172.
28. Szabo R, Hobson JP, Christoph K, Kosa P, List K, Bugge TH. Regulation of cell surface protease matriptase by HAI2 is essential for placental development, neural tube closure and embryonic survival in mice. Development 2009; 136: 2653-2663.
29. Parr C, Watkins G, Mansel RE, Jiang WG. The hepatocyte growth factor regulatory factors in human breast cancer. Clin Cancer Res 2004; 10: 202-211.
30. Bergum C, List K. Loss of the matriptase inhibitor HAI-2 during prostate cancer progression. Prostate 2010; 70: 1422-1428.
31. Muller-Pillasch F, Wallrapp C, Bartels K, Varga G, Friess H, Buchler M et al. Cloning of a new Kunitz-type protease inhibitor with a putative transmembrane domain overexpressed in pancreatic cancer. Biochim Biophys Acta 1998; 1395: 88-95.
32. Kongkham PN, Northcott PA, Ra YS, Nakahara Y, Mainprize TG, Croul SE et al. An epigenetic genome-wide screen identifies SPINT2 as a novel tumor suppressor gene in pediatric medulloblastoma. Cancer Res 2008; 68: 9945-9953.
33. Morris MR, Gentle D, Abdulrahman M, Maina EN, Gupta K, Banks RE et al. Tumor suppressor activity and epigenetic inactivation of hepatocyte growth factor activator inhibitor type 2/SPINT2 in papillary and clear cell renal cell carcinoma. Cancer Res 2005; 65: 4598-4606.
34. Fukai K, Yokosuka O, Chiba T, Hirasawa Y, Tada M, Imazeki F et al. Hepatocyte growth factor activator inhibitor 2/placental bikunin (HAI-2/PB) gene is frequently hypermethylated in human hepatocellular carcinoma. Cancer Res 2003; 63: 8674-8679.
35. Parr C, Jiang WG. Hepatocyte growth factor activation inhibitors (HAI-1 and HAI-2) regulate HGF-induced invasion of human breast cancer cells. Int J Cancer 2006; 119: 1176-1183.
36. 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: 1945-1950.
37. Tsai C.H, Lin FM, Yang YC, Lee MT, Cha TL, Wu GJ et al. Herbal extract of Wedelia chinensis attenuates androgen receptor activity and orthotopic growth of prostate cancer in nude mice. Clin Cancer Res 2009; 15: 5435-5444.
38. Chen CJ, Wu BY, Tsao PI, Chen CY, Wu MH, Chan YL et al. Increased matriptase zymogen activation in inflammatory skin disorders. Am J Physiol Cell Physiol 2011; 300: C406-C415.
39. Oberst MD, Singh B, Ozdemirli M, Dickson RB, Johnson MD, Lin CY. Characterization of matriptase expression in normal human tissues. J Histochem Cytochem 2003; 51: 1017-1025.
40. List K, Bugge TH, Szabo R. Matriptase: potent proteolysis on the cell surface. Mol Med 2006; 12: 1-7.
41. Uhland K. Matriptase and its putative role in cancer. Cell Mol Life Sci 2006; 63: 2968-2978.
42. Cheng TS, Chen WC, Lin YY, Tsai C.H, Liao CI, Shyu HY et al. Curcumin-targeting pericellular serine protease matriptase role in suppression of prostate cancer cell invasion, tumor growth, and metastasis. Cancer Prev Res 2013; 6: 495-505.
43. Lee MS, Tseng IC, Wang Y, Kiyomiya K, Johnson MD, Dickson RB et al. Autoactivation of matriptase in vitro: requirement for biomembrane and LDL receptor domain. Am J Physiol Cell Physiol 2007; 293: C95-105.
44. Szabo R, Rasmussen AL, Moyer AB, Kosa P, Schafer JM, Molinolo AA et al. c-Met-induced epithelial carcinogenesis is initiated by the serine protease matriptase. Oncogene 2011; 30: 2003-2016.
45. Nagakawa O, Yamagishi T, Fujiuchi Y, Junicho A, Akashi T, Nagaike K et al. Serum hepatocyte growth factor activator (HGFA) in benign prostatic hyperplasia and prostate cancer. Eur Urol 2005; 48: 686-690.
46. Oberst MD, Williams CA, Dickson RB, Johnson MD, Lin CY. The activation of matriptase requires its noncatalytic domains, serine protease domain, and its cognate inhibitor. J Biol Chem 2003; 278: 26773-26779.