Abstract
Carcinogenesis is accompanied by increased protein and activity levels of extracellular cell-surface proteases that are capable of modifying the tumor microenvironment by directly cleaving the extracellular matrix, as well as activating growth factors and proinflammatory mediators involved in proliferation and invasion of cancer cells, and recruitment of inflammatory cells. These complex processes ultimately potentiate neoplastic progression leading to local tumor cell invasion, entry into the vasculature, and metastasis to distal sites. Several members of the type II transmembrane serine protease (TTSP) family have been shown to play critical roles in cancer progression. In this review the knowledge collected over the past two decades about the molecular mechanisms underlying the pro-cancerous properties of selected TTSPs will be summarized. Furthermore, we will discuss how these insights may facilitate the translation into clinical settings in the future by specifically targeting TTSPs as part of novel cancer treatment regimens.
Acknowledgments
This work was supported by a NIH Ruth L. Kirschstein National Research Service Award T32-CA009531 (A.S.M.), NCI NIH RCA60565A (K.L.) and NCI NIH 3R01CA160565-04S grant (K.L., F.A.V.), and NIGMS/NIH grant R25 GM 058905-15 (F.A.V.).
References
Alef, T., Torres, S., Hausser, I., Metze, D., Türsen, U., Lestringant, G.G., and Hennies, H.C. (2008). Ichthyosis, follicular atrophoderma, and hypotrichosis caused by mutations in ST14 is associated with impaired profilaggrin processing. J. Invest. Dermatol 129, 862–869.10.1038/jid.2008.311Suche in Google Scholar PubMed
Antalis, T.M., Buzza, M.S., Hodge, K.M., Hooper, J.D., and Netzel-Arnett, S. (2010). The cutting edge: membrane-anchored serine protease activities in the pericellular microenvironment. Biochem. J. 428, 325–346.10.1042/BJ20100046Suche in Google Scholar PubMed PubMed Central
Avrahami, L., Maas, S., Pasmanik-Chor, M., Rainshtein, L., Magal, N., Smitt, J., van Marle, J., Shohat, M., and Basel-Vanagaite, L. (2008). Autosomal recessive ichthyosis with hypotrichosis syndrome: further delineation of the phenotype. Clin. Genet. 74, 47–53.10.1111/j.1399-0004.2008.01006.xSuche in Google Scholar PubMed
Baba, T., Kawaguchi, M., Fukushima, T., Sato, Y., Orikawa, H., Yorita, K., Tanaka, H., Lin, C.Y., Sakoda, S., and Kataoka, H. (2012). Loss of membrane-bound serine protease inhibitor HAI-1 induces oral squamous cell carcinoma cells’ invasiveness. J. Pathol. 228, 181–192.10.1002/path.3993Suche in Google Scholar PubMed
Basel-Vanagaite, L., Attia, R., Ishida-Yamamoto, A., Rainshtein, L., Ben Amitai, D., Lurie, R., Pasmanik-Chor, M., Indelman, M., Zvulunov, A., Saban, S., etal. (2007). Autosomal recessive ichthyosis with hypotrichosis caused by a mutation in ST14, encoding type II transmembrane serine protease matriptase. Am. J. Hum. Genet. 80, 467–477.10.1086/512487Suche in Google Scholar PubMed PubMed Central
Bergum, C. and List, K. (2010). Loss of the matriptase inhibitor HAI-2 during prostate cancer progression. Prostate 70, 1422–1428.10.1002/pros.21177Suche in Google Scholar PubMed
Betsunoh, H., Mukai, S., Akiyama, Y., Fukushima, T., Minamiguchi, N., Hasui, Y., Osada, Y., and Kataoka, H. (2007). Clinical relevance of hepsin and hepatocyte growth factor activator inhibitor type 2 expression in renal cell carcinoma. Cancer Sci. 98, 491–498.10.1111/j.1349-7006.2007.00412.xSuche in Google Scholar PubMed
Bocheva, G., Rattenholl, A., Kempkes, C., Goerge, T., Lin, C.Y., D’Andrea, M.R., Ständer, S., and Steinhoff, M. (2009). Role of matriptase and proteinase-activated receptor-2 in nonmelanoma skin cancer. J. Invest. Dermatol. 129, 1816–1823.10.1038/jid.2008.449Suche in Google Scholar PubMed
Bruxvoort, K.J., Charbonneau, H.M., Giambernardi, T.A., Goolsby, J.C., Qian, C.N., Zylstra, C.R., Robinson, D.R., Roy-Burman, P., Shaw, A.K., Buckner-Berghuis, B.D., et al. (2007). Inactivation of Apc in the mouse prostate causes prostate carcinoma. Cancer Res. 67, 2490–2496.10.1158/0008-5472.CAN-06-3028Suche in Google Scholar PubMed
Bugge, T.H., List, K., and Szabo, R. (2007). Matriptase-dependent cell surface proteolysis in epithelial development and pathogenesis. Front. Biosci. 12, 5060–5070.10.2741/2448Suche in Google Scholar PubMed
Bugge, T.H., Antalis, T.M., and Wu, Q. (2009). Type II transmembrane serine proteases. J. Biol. Chem. 284, 23177–23181.10.1074/jbc.R109.021006Suche in Google Scholar PubMed PubMed Central
Buzza, M.S., Netzel-Arnett, S., Shea-Donohue, T., Zhao, A., Lin, C.Y., List, K., Szabo, R., Fasano, A., Bugge, T.H., and Antalis, T.M. (2010). Membrane-anchored serine protease matriptase regulates epithelial barrier formation and permeability in the intestine. Proc. Natl. Acad. Sci. U.S.A. 107, 4200–4205.10.1073/pnas.0903923107Suche in Google Scholar PubMed PubMed Central
Cheng, M.F., Tzao, C., Tsai, W.C., Lee, W.H., Chen, A., Chiang, H., Sheu, L.F., and Jin, J.S. (2006). Expression of EMMPRIN and matriptase in esophageal squamous cell carcinoma: correlation with clinicopathological parameters. Dis. Esophagus 19, 482–486.10.1111/j.1442-2050.2006.00613.xSuche in Google Scholar PubMed
Cheng, D., Kong, H., and Li, Y. (2013a). TMPRSS4 as a poor prognostic factor for triple-negative breast cancer. Int. J. Mol. Sci. 14, 14659–14668.10.3390/ijms140714659Suche in Google Scholar PubMed PubMed Central
Cheng, D., Liang, B., and Li, Y. (2013b). High TMPRSS4 expression is a predictor of poor prognosis in cervical squamous cell carcinoma. Cancer Epidemiol. 37, 993–997.10.1016/j.canep.2013.08.009Suche in Google Scholar PubMed
Cheng, M.F., Huang, M.S., Lin, C.S., Lin, L.H., Lee, H.S., Jiang, J.C., and Hsia, K.T. (2014). Expression of matriptase correlates with tumour progression and clinical prognosis in oral squamous cell carcinoma. Histopathology 65, 24–34.10.1111/his.12361Suche in Google Scholar PubMed
Chou, F.P., Chen, Y.W., Zhao, X.F., Xu-Monette, Z.Y., Young, K.H., Gartenhaus, R.B., Wang, J.K., Kataoka, H., Zuo, A.H., Barndt, R.J., et al. (2013). Imbalanced matriptase pericellular proteolysis contributes to the pathogenesis of malignant B-cell lymphomas. Am. J. Pathol. 183, 1306–1317.10.1016/j.ajpath.2013.06.024Suche in Google Scholar PubMed PubMed Central
Clark, J.P. and Cooper, C.S. (2009). ETS gene fusions in prostate cancer. Nat. Rev. Urol. 6, 429–439.10.1038/nrurol.2009.127Suche in Google Scholar PubMed
Colombo, E., Désilets, A., Duchêne, D., Chagnon, F., Najmanovich, R., Leduc, R., and Marsault, E. (2012). Design and synthesis of potent, selective inhibitors of matriptase. ACS Med. Chem. Lett. 3, 530–534.10.1021/ml3000534Suche in Google Scholar PubMed PubMed Central
Darragh, M.R., Schneider, E.L., Lou, J., Phojanakong, P.J., Farady, C.J., Marks, J.D., Hann, B.C., and Craik, C.S. (2010). Tumor detection by imaging proteolytic activity. Cancer Res. 70, 1505–1512.10.1158/0008-5472.CAN-09-1640Suche in Google Scholar PubMed PubMed Central
de Aberasturi, A.L. and Calvo, A. (2015). TMPRSS4: an emerging potential therapeutic target in cancer. Br. J. Cancer 112, 4–8.10.1038/bjc.2014.403Suche in Google Scholar
de Aberasturi, A.L., Redrado, M., Villalba, M., Larabal, L., Pajares, M.J., Garcia, J., Evans, S.R., Garcia-Ros, D., Bodegas, M.E., Lopez, L., et al. (2016). TMPRSS4 induces cancer stem cell-like properties in lung cancer cells and correlates with ALDH expression in NSCLC patients. Cancer Lett. 370, 165–176.10.1016/j.canlet.2015.10.012Suche in Google Scholar
Ellwood-Yen, K., Graeber, T.G., Wongvipat, J., Iruela-Arispe, M.L., Zhang, J., Matusik, R., Thomas, G.V., and Sawyers, C.L. (2003). Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 4, 223–238.10.1016/S1535-6108(03)00197-1Suche in Google Scholar
Förbs, D., Thiel, S., Stella, M.C., Stürzebecher, A., Schweinitz, A., Steinmetzer, T., Stürzebecher, J., and Uhland, K. (2005). In vitro inhibition of matriptase prevents invasive growth of cell lines of prostate and colon carcinoma. Int. J. Oncol. 27, 1061–1070.10.3892/ijo.27.4.1061Suche in Google Scholar
Galkin, A.V., Mullen, L., Fox, W.D., Brown, J., Duncan, D., Moreno, O., Madison, E.L., and Agus, D.B. (2004). CVS-3983, a selective matriptase inhibitor, suppresses the growth of androgen independent prostate tumor xenografts. Prostate 61, 228–235.10.1002/pros.20094Suche in Google Scholar PubMed
Gao, L., Liu, M., Dong, N., Jiang, Y., Lin, C.Y., Huang, M., Wu, D., and Wu, Q. (2012). Matriptase is highly upregulated in chronic lymphocytic leukemia and promotes cancer cell invasion. Leukemia 27, 1191–1194.10.1038/leu.2012.289Suche in Google Scholar PubMed
Garten, W., Braden, C., Arendt, A., Peitsch, C., Baron, J., Lu, Y., Pawletko, K., Hardes, K., Steinmetzer, T., and Böttcher-Friebertshäuser, E. (2015). Influenza virus activating host proteases: Identification, localization and inhibitors as potential therapeutics. Eur. J. Cell Biol. 94, 375–383.10.1016/j.ejcb.2015.05.013Suche in Google Scholar PubMed
Gray, K., Elghadban, S., Thongyoo, P., Owen, K.A., Szabo, R., Bugge, T.H., Tate, E.W., Leatherbarrow, R.J., and Ellis, V. (2014). Potent and specific inhibition of the biological activity of the type II transmembrane serine protease matriptase by the cyclic microprotein MCoTI-II. Thromb. Haemost. 112, 402–411.10.1160/TH13-11-0895Suche in Google Scholar PubMed
Guan, H., Liang, W., Liu, J., Wei, G., Li, H., Xiu, L., Xiao, H., and Li, Y. (2015). Transmembrane protease serine 4 promotes thyroid cancer proliferation via CREB phosphorylation. Thyroid 25, 85–94.10.1089/thy.2014.0155Suche in Google Scholar PubMed PubMed Central
Guipponi, M., Tan, J., Cannon, P.Z., Donley, L., Crewther, P., Clarke, M., Wu, Q., Shepherd, R.K., and Scott, H.S. (2007). Mice deficient for the type II transmembrane serine protease, TMPRSS1/hepsin, exhibit profound hearing loss. Am. J. Pathol. 171, 608–616.10.2353/ajpath.2007.070068Suche in Google Scholar PubMed PubMed Central
Hamamoto, J., Soejima, K., Naoki, K., Yasuda, H., Hayashi, Y., Yoda, S., Nakayama, S., Satomi, R., Terai, H., Ikemura, S., et al. (2015). Methylation-induced downregulation of TFPI-2 causes TMPRSS4 overexpression and contributes to oncogenesis in a subset of non-small-cell lung carcinoma. Cancer Sci. 106, 34–42.10.1111/cas.12569Suche in Google Scholar PubMed PubMed Central
Han, Z., Harris, P.K., Jones, D.E., Chugani, R., Kim, T., Agarwal, M., Shen, W., Wildman, S.A., and Janetka, J.W. (2014). Inhibitors of HGFA, matriptase, and hepsin serine proteases: a nonkinase strategy to block cell signaling in cancer. ACS Med. Chem. Lett. 5, 1219–1224.10.1021/ml500254rSuche in Google Scholar PubMed PubMed Central
Hanifa, S., Scott, H.S., Crewther, P., Guipponi, M., and Tan, J. (2010). Thyroxine treatments do not correct inner ear defects in tmprss1 mutant mice. Neuroreport 21, 897–901.10.1097/WNR.0b013e32833dbd2dSuche in Google Scholar PubMed PubMed Central
Hsu, Y.C., Huang, H.P., Yu, I.S., Su, K.Y., Lin, S.R., Lin, W.C., Wu, H.L., Shi, G.Y., Tao, M.H., Kao, C.H., et al. (2012). Serine protease hepsin regulates hepatocyte size and hemodynamic retention of tumor cells by hepatocyte growth factor signaling in mice. Hepatology 56, 1913–1923.10.1002/hep.25773Suche in Google Scholar PubMed
Hoang, C.D., D’Cunha, J., Kratzke, M.G., Casmey, C.E., Frizelle, S.P., Maddaus, M.A., and Kratzke, R.A. (2004). Gene expression profiling identifies matriptase overexpression in malignant mesothelioma. Chest 125, 1843–1852.10.1378/chest.125.5.1843Suche in Google Scholar PubMed
Hooper, J.D., Clements, J.A., Quigley, J.P., and Antalis, T.M. (2001). Type II transmembrane serine proteases. Insights into an emerging class of cell surface proteolytic enzymes. J. Biol. Chem. 276, 857–860.10.1074/jbc.R000020200Suche in Google Scholar PubMed
Huang, A., Zhou, H., Zhao, H., Quan, Y., Feng, B., and Zheng, M. (2013). TMPRSS4 correlates with colorectal cancer pathological stage and regulates cell proliferation and self-renewal ability. Cancer Biol. Ther. 15, 297–304.10.4161/cbt.27308Suche in Google Scholar PubMed PubMed Central
Jacquinet, E., Rao, N.V., Rao, G.V., Zhengming, W., Albertine, K.H., and Hoidal, J.R. (2001). Cloning and characterization of the cDNA and gene for human epitheliasin. Eur. J. Biochem. 268, 2687–2699.10.1046/j.1432-1327.2001.02165.xSuche in Google Scholar PubMed
Jin, J.S., Chen, A., Hsieh, D.S., Yao, C.W., Cheng, M.F., and Lin, Y.F. (2006). Expression of serine protease matriptase in renal cell carcinoma: correlation of tissue microarray immunohistochemical expression analysis results with clinicopathological parameters. Int. J. Surg. Pathol. 14, 65–72.10.1177/106689690601400111Suche in Google Scholar PubMed
Jung, H., Lee, K.P., Park, S.J., Park, J.H., Jang, Y.S., Choi, S.Y., Jung, J.G., Jo, K., Park, D.Y., Yoon, J.H., et al. (2007). TMPRSS4 promotes invasion, migration and metastasis of human tumor cells by facilitating an epithelial-mesenchymal transition. Oncogene 27, 2635–2647.10.1038/sj.onc.1210914Suche in Google Scholar PubMed
Kang, J.Y., Dolled-Filhart, M., Ocal, I.T., Singh, B., Lin, C.Y., Dickson, R.B., Rimm, D.L., and Camp, R.L. (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 progression of node-negative breast cancer. Cancer Res. 63, 1101–1105.Suche in Google Scholar
Kang, S., Min, H.J., Kang, M.S., Jung, M.G., and Kim, S. (2013). Discovery of novel 2-hydroxydiarylamide derivatives as TMPRSS4 inhibitors. Bioorg. Med. Chem. Lett. 23, 1748–1751.10.1016/j.bmcl.2013.01.055Suche in Google Scholar PubMed
Kebebew, E., Peng, M., Reiff, E., Duh, Q.Y., Clark, O.H., and McMillan, A. (2005). ECM1 and TMPRSS4 are diagnostic markers of malignant thyroid neoplasms and improve the accuracy of fine needle aspiration biopsy. Ann. Surg. 242, 363–361.10.1097/01.sla.0000179623.87329.6bSuche in Google Scholar PubMed PubMed Central
Kelly, K.A., Setlur, S.R., Ross, R., Anbazhagan, R., Waterman, P., Rubin, M.A., and Weissleder, R. (2008). Detection of early prostate cancer using a hepsin-targeted imaging agent. Cancer Res. 68, 2286–2291.10.1158/0008-5472.CAN-07-1349Suche in Google Scholar PubMed PubMed Central
Keppner, A., Andreasen, D., Mérillat, A.M., Bapst, J., Ansermet, C., Wang, Q., Maillard, M., Malsure, S., Nobile, A., and Hummler, E. (2015). Epithelial sodium channel-mediated sodium transport is not dependent on the membrane-bound serine protease CAP2/Tmprss4. PloS One 10, e0135224.10.1371/journal.pone.0135224Suche in Google Scholar PubMed PubMed Central
Kim, T.S., Heinlein, C., Hackman, R.C., and Nelson, P.S. (2006). Phenotypic analysis of mice lacking the TMPRSS2-encoded protease. Mol. Cell. Biol. 26, 965–975.10.1128/MCB.26.3.965-975.2006Suche in Google Scholar PubMed PubMed Central
Kim, S., Kang, H.Y., Nam, E.H., Choi, M.S., Zhao, X.F., Hong, C.S., Lee, J.W., Lee, J.H., and Park,Y.K. (2010). TMPRSS4 induces invasion and epithelial-mesenchymal transition through upregulation of integrin α5 and its signaling pathways. Carcinogenesis 31, 597–606.10.1093/carcin/bgq024Suche in Google Scholar PubMed
Klezovitch, O., Chevillet, J., Mirosevich, J., Roberts, R.L., Matusik, R.J., and Vasioukhin, V. (2004). Hepsin promotes prostate cancer progression and metastasis. Cancer Cell 6, 185–195.10.1016/j.ccr.2004.07.008Suche in Google Scholar PubMed
Ko, C.J., Huang, C.C., Lin, H.Y., Juan, C.P., Lan, S.W., Shyu, H.Y., Wu, S.R., Hsiao, P.W., Huang, H.P., Shun, C.T., et al. (2015). Androgen-induced TMPRSS2 activates matriptase and promotes extracellular matrix degradation, prostate cancer cell invasion, tumor growth, and metastasis. Cancer Res. 75, 2949–2960.10.1158/0008-5472.CAN-14-3297Suche in Google Scholar PubMed
Kosa, P., Szabo, R., Molinolo, A.A., and Bugge, T.H. (2011). Suppression of Tumorigenicity-14, encoding matriptase, is a critical suppressor of colitis and colitis-associated colon carcinogenesis. Oncogene 31, 3679–3695.10.1038/onc.2011.545Suche in Google Scholar PubMed PubMed Central
Lahiry, P., Racacho, L., Wang, J., Robinson, J.F., Gloor, G.B., Rupar, C.A, Siu, V.M., Bulman, D.E., and Hegele, R.A. (2013). A mutation in the serine protease TMPRSS4 in a novel pediatric neurodegenerative disorder. Orphanet J. Rare Dis. 8, 126.10.1186/1750-1172-8-126Suche in Google Scholar PubMed PubMed Central
Larzabal, L., Nguewa, P.A., Pio, R., Blanco, D., Sanchez, B., Roriguez, M.J., Pajares, M.J., Catena, R., Montuenga, L.M., and Calvo, A. (2011). Overexpression of TMPRSS4 in non-small cell lung cancer is associated with poor prognosis in patients with squamous histology. Br. J. Cancer 105, 1608–1614.10.1038/bjc.2011.432Suche in Google Scholar PubMed PubMed Central
Larzabal, L., de Aberasturi, A.L., Redrado, M., Rueda, P., Rodriguez, M.J., Bodegas, M.E., Montuenga, L.M., and Calvo, A. (2014). TMPRSS4 regulates levels of integrin α5 in NSCLC through miR-205 activity to promote metastasis. Br. J. Cancer 110, 764–774.10.1038/bjc.2013.761Suche in Google Scholar PubMed PubMed Central
LeBeau, A.M., Lee, M., Murphy, S.T., Hann, B.C., Warren, R.S., Delos Santos, R., Kurhanewicz, J., Hanash, S.M., VanBrocklin, H.F., and Craik, C.S. (2013). Imaging a functional tumorigenic biomarker in the transformed epithelium. Proc. Natl. Acad. Sci. U.S.A. 110, 93–98.10.1073/pnas.1218694110Suche in Google Scholar PubMed PubMed Central
Lee, J.W., Yong Song, S., Choi, J.J., Lee, S.J., Kim, B.G.,Park, C.S., Lee, J.H., Lin, C.Y., Dickson, R.B., and Bae, D.S. (2005). Increased expression of matriptase is associated with histopathologic grades of cervical neoplasia. Hum. Pathol. 36, 626–633.10.1016/j.humpath.2005.03.003Suche in Google Scholar PubMed
Leytus, S.P., Loeb, K.R., Hagen, F.S., Kurachi, K., and Davie, E.W. (1988). A novel trypsin-like serine protease (hepsin) with a putative transmembrane domain expressed by human liver and hepatoma cells. Biochemistry 27, 1067–1074.10.1021/bi00403a032Suche in Google Scholar PubMed
Li, W., Wang, B.E., Moran, P., Lipari, T., Ganesan, R., Corpuz, R., Ludlam, M.J., Gogineni, A., Koeppen, H., Bunting, S., et al. (2009). Pegylated kunitz domain inhibitor suppresses hepsin-mediated invasive tumor growth and metastasis. Cancer Res. 69, 8395–8402.10.1158/0008-5472.CAN-09-1995Suche in Google Scholar PubMed
Li, T., Zeng, Z.C., Wang, L., Qiu, S.J., Zhou, J.W., Zh, X.T., Yu, H.H., and Tang, Z.Y. (2011). Radiation enhances long-term metastasis potential of residual hepatocellular carcinoma in nude mice through TMPRSS4-induced epithelial-mesenchymal transition. Cancer Gene Ther. 18, 617–626.10.1038/cgt.2011.29Suche in Google Scholar PubMed
Liang, B., Wu, M., Bu, Y., Zhao, A., and Xie, F. (2013). Prognostic value of TMPRSS4 expression in patients with breast cancer. Med. Oncol. 30, 497.10.1007/s12032-013-0497-8Suche in Google Scholar PubMed
List, K. (2009). Matriptase: a culprit in cancer? Future Oncol. 5, 97–104.10.2217/14796694.5.1.97Suche in Google Scholar PubMed
List, K., Haudenschild, C.C., Szabo, R., Chen, W., Wahl, S.M., Swaim, W., Engelholm, L.H., Behrendt, N., and Bugge, T.H. (2002). Matriptase/MT-SP1 is required for postnatal survival, epidermal barrier function, hair follicle development, and thymic homeostasis. Oncogene 21, 3765–3779.10.1038/sj.onc.1205502Suche in Google Scholar PubMed
List, K., Szabo, R., Wertz, P.W., Segre, J., Haudenschild, C.C., Kim, S.Y., and Bugge, T.H. (2003). Loss of proteolytically processed filaggrin caused by epidermal deletion of Matriptase/MT-SP1. J. Cell Biol. 163, 901–910.10.1083/jcb.200304161Suche in Google Scholar PubMed PubMed Central
List, K., Szabo, R., Molinolo, A., Sriuranpong, V., Redeye, V., Murdock, T., Burke, B., Nielsen, B.S., Gutkind, J.S., and Bugge, T.H. (2005). Deregulated matriptase causes ras-independent multistage carcinogenesis and promotes ras-mediated malignant transformation. Genes Dev. 19, 1934–1935.10.1101/gad.1300705Suche in Google Scholar PubMed PubMed Central
List, K., Currie, B., Scharschmidt, T.C., Szabo, R., Shireman, J., Molinolo, A., Cravatt, B.F., Segre, J., and Bugge, T.H. (2007). Autosomal ichthyosis with hypotrichosis syndrome displays low matriptase proteolytic activity and is phenocopied in ST14 hypomorphic mice. J. Biol. Chem. 282, 36714–36723.10.1074/jbc.M705521200Suche in Google Scholar PubMed
List, K., Kosa, P., Szabo, R., Bey, A.L., Wang, C.B., Molinolo, A., and Bugge, T.H. (2009). Epithelial integrity is maintained by a matriptase-dependent proteolytic pathway. Am. J. Pathol. 175, 1453–1463.10.2353/ajpath.2009.090240Suche in Google Scholar PubMed PubMed Central
Lucas, J.M., True, L., Hawley, S., Matsumura, M., Morrissey, C., Vessella, R., and Nelson, P.S. (2008). The androgen-regulated type II serine protease TMPRSS2 is differentially expressed and mislocalized in prostate adenocarcinoma. J. Pathol. 215, 118–125.10.1002/path.2330Suche in Google Scholar PubMed
Lucas, J.M., Heinlein, C., Kim, T., Hernandez, S.A., Malik, M.S., True, L.D., Morrissey, C., Corey, E., Montgomery, B., Mostaghel, E., et al. (2014). The androgen-regulated protease TMPRSS2 activates a proteolytic cascade involving components of the tumor microenvironment and promotes prostate cancer metastasis. Cancer Discov. 4, 1310–1325.10.1158/2159-8290.CD-13-1010Suche in Google Scholar PubMed PubMed Central
Matsuo, T., Nakamura, K., Takamoto, N., Kodama, J., Hongo, A., Abrzua, F., Nasu, Y., Kumon, H., and Hiramatsu, Y. (2008). Expression of the serine protease hepsin and clinical outcome of human endometrial cancer. Anticancer Res. 28, 159–164.Suche in Google Scholar
Meyer, D., Sielaff, F., Hammami, M., Bottcher-Friebertshauser, E., Garten, W., and Steinmetzer, T. (2013). Identification of the first synthetic inhibitors of the type II transmembrane serine protease TMPRSS2 suitable for inhibition of influenza virus activation. Biochem. J. 452, 331–343.10.1042/BJ20130101Suche in Google Scholar PubMed
Miao, J., Mu, D., Ergel, B., Singavarapu, R., Duan, Z., Powers, S., Oliva, E., and Orsulic, S. (2008). Hepsin colocalizes with desmosomes and induces progression of ovarian cancer in a mouse model. Int. J. Cancer 123, 2041–2047.10.1002/ijc.23726Suche in Google Scholar PubMed PubMed Central
Nakamura, K., Hongo, A., Kodama, J., Abarzua, F., Nasu, Y., Kumon, H., and Hiramatsu, Y. (2009). Expression of matriptase and clinical outcome of human endometrial cancer. Anticancer Res. 29, 1685–1690.Suche in Google Scholar
Nakamura, K., Hongo, A., Kodama, J., and Hiramatsu, Y. (2011). The role of hepatocyte growth factor activator inhibitor (HAI)-1 and HAI-2 in endometrial cancer. Int. J. Cancer 128, 2613–2624.10.1002/ijc.25606Suche in Google Scholar PubMed
Nandana, S., Ellwood-Yen, K., Sawyers, C., Wills, M., Weidow, B., Case, T., Vasioukhin, V., and Matusik, R. (2010). Hepsin cooperates with MYC in the progression of adenocarcinoma in a prostate cancer mouse model. Prostate 70, 591–600.10.1002/pros.21093Suche in Google Scholar PubMed PubMed Central
Napp, J., Dullin, C., Müller, F., Uhland, K., Petri, J.B., van de Locht, A., Steinmetzer, T., and Alves, F. (2010). Time-domain in vivo near infrared fluorescence imaging for evaluation of matriptase as a potential target for the development of novel, inhibitor-based tumor therapies. Int. J. Cancer 127, 1958–1974.10.1002/ijc.25405Suche in Google Scholar PubMed
Netzel-Arnett, S., Hooper, J.D., Szabo, R., Madison, E.L., Quigley, J.P., Bugge, T.H., and Antalis, T.M. (2003). Membrane anchored serine proteases: a rapidly expanding group of cell surface proteolytic enzymes with potential roles in cancer. Cancer Metastasis Rev. 22, 237–258.10.1023/A:1023003616848Suche in Google Scholar
Netzel-Arnett, S., Currie, B.M., Szabo, R., Lin, C.Y., Chen, L.M., Chai, K.X., Antalis, T.M., Bugge, T.H., and List, K. (2006). Evidence for a matriptase-prostasin proteolytic cascade regulating terminal epidermal differentiation. J. Biol. Chem. 281, 32941–32945.10.1074/jbc.C600208200Suche in Google Scholar PubMed
Netzel-Arnett, S., Buzza, M.S., Shea-Donohue, T., Désilets, A., Leduc, R., Fasano, A., Bugge, T.H., and Antalis, T.M. (2012). Matriptase protects against experimental colitis and promotes intestinal barrier recovery. Inflamm. Bowel Dis. 18, 1303–1314.10.1002/ibd.21930Suche in Google Scholar PubMed PubMed Central
Oberst, M.D., Johnson, M.D., Dickson, R.B., Lin, C.Y., Singh, B., Stewart, M., Williams, A., al-Nafussi, A., Smyth, J.F., Gabra, H., et al. (2002). Expression of the serine protease matriptase and its inhibitor HAI-1 in epithelial ovarian cancer: correlation with clinical outcome and tumor clinicopathological parameters. Clin. Cancer Res. 8, 1101–1107.Suche in Google Scholar
Owen, K.A., Qiu, D., Alves, J., Schumacher, A.M., Kilpatrick, L.M., Li, J., Harris, J.L., and Ellis, V. (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, 219–228.10.1042/BJ20091448Suche in Google Scholar PubMed
Riddick, A.C., Shukla, C.J., Pennington, C.J., Bass, R., Nuttall, R.K., Hogan, A., Sethia, K.K., Ellis, V., Collins, A.T., Maitland, N.J., et al. (2005). Identification of degradome components associated with prostate cancer progression by expression analysis of human prostatic tissues. Br. J. Cancer 92, 2171–2180.10.1038/sj.bjc.6602630Suche in Google Scholar PubMed PubMed Central
Saleem, M., Adhami, V.M., Zhong, W., Longley, B.J., Lin, C.Y., Dickson, R.B., Reagan-Shaw, S., Jarrard, D.F., and Mukhtar, H. (2006). 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. 15, 217–227.10.1158/1055-9965.EPI-05-0737Suche in Google Scholar PubMed
Sales, K.U., Friis, S., Konkel, J.E., Godiksen, S., Hatakeyama, M., Hansen, K.K., Rogatto, S.R., Szabo, R., Vogel, L.K., Chen, W., et al. (2014). Non-hematopoietic PAR-2 is essential for matriptase-driven pre-malignant progression and potentiation of ras-mediated squamous cell carcinogenesis. Oncogene 34, 346–356.10.1038/onc.2013.563Suche in Google Scholar PubMed PubMed Central
Sales, K.U., Friis, S., Abusleme, L., Moutsopoulos, N.M., and Bugge, T.H. (2015). Matriptase promotes inflammatory cell accumulation and progression of established epidermal tumors. Oncogene 34, 4664–4672.10.1038/onc.2014.391Suche in Google Scholar PubMed PubMed Central
Sanders, A.J., Parr, C., Davies, G., Martin, T.A., Lane, J., Mason, M.D., and Jiang, W.G. (2006). Genetic reduction of matriptase-1 expression is associated with a reduction in the aggressive phenotype of prostate cancer cells in vitro and in vivo. J. Exp. Ther. Oncol. 6, 39–48.Suche in Google Scholar
Sanman, L.E. and Bogyo. M. (2014). Activity-based profiling of proteases. Annu. Rev. Biochem. 83, 249–273.10.1146/annurev-biochem-060713-035352Suche in Google Scholar PubMed
Shah, S. and Small, E. (2010). Emerging biological observations in prostate cancer. Expert Rev. Anticancer Ther. 10, 89–101.10.1586/era.09.161Suche in Google Scholar PubMed
Srikantan, V., Valladares, M., Rhim, J.S., Moul, J.W., and Srivastava, S. (2002). HEPSIN inhibits cell growth/invasion in prostate cancer cells. Cancer Res. 62, 6812–6816.Suche in Google Scholar
Steinmetzer, T., Schweinitz, A., Stürzebecher, A., Dönnecke, D., Uhland, K., Schuster, O., Steinmetzer, P., Müller, F., Friedrich, R., Than, M.E., et al. (2006). Secondary amides of sulfonylated 3-amidinophenylalanine. New potent and selective inhibitors of matriptase. J. Med. Chem. 49, 4116–4126.10.1021/jm051272lSuche in Google Scholar PubMed
Szabo, R. and Bugge, T.H. (2008). Type II transmembrane serine proteases in development and disease. Int. J. Biochem. Cell Biol. 40, 1297–1316.10.1016/j.biocel.2007.11.013Suche in Google Scholar PubMed
Szabo, R. and Bugge, T.H. (2011). Membrane-anchored serine proteases in vertebrate cell and developmental biology. Annu. Rev. Cell Dev. Biol. 27, 213–235.10.1146/annurev-cellbio-092910-154247Suche in Google Scholar PubMed PubMed Central
Szabo, R., Molinolo, A., List, K., and Bugge, T.H. (2007). Matriptase inhibition by hepatocyte growth factor activator inhibitor-1 is essential for placental development. Oncogene 26, 1546–1556.10.1038/sj.onc.1209966Suche in Google Scholar PubMed
Szabo, R., Hobson, J.P., List, K., Molinolo, A., Lin, C.Y., and Bugge, T.H. (2008). 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. 283, 29495–29504.10.1074/jbc.M801970200Suche in Google Scholar PubMed PubMed Central
Szabo, R., Hobson, J.P., Christoph, K., Kosa, P., List, K., and Bugge, T.H. (2009a). Regulation of cell surface protease matriptase by HAI2 is essential for placental development, neural tube closure and embryonic survival in mice. Development 136, 2653–2663.10.1242/dev.038430Suche in Google Scholar PubMed PubMed Central
Szabo, R., Kosa, P., List, K., and Bugge, T.H. (2009b). Loss of matriptase suppression underlies spint1 mutation-associated ichthyosis and postnatal lethality. Am. J. Pathol. 174, 2015–2022.10.2353/ajpath.2009.090053Suche in Google Scholar PubMed PubMed Central
Szabo, R., Rasmussen, A.L., Moyer, A.B., Kosa, P., Schafer, J.M., Molinolo, A.A., Gutkind, J.S., and Bugge, T.H. (2011). c-Met-induced epithelial carcinogenesis is initiated by the serine protease matriptase. Oncogene 30, 2003–2016.10.1038/onc.2010.586Suche in Google Scholar PubMed PubMed Central
Tang, X., Mahajan, S.S., Nguyen, L.T., Béliveau, F., Leduc, R., Simon, J.A., and Vasioukhin, V. (2014). Targeted inhibition of cell-surface serine protease Hepsin blocks prostate cancer bone metastasis. Oncotarget 5, 1352–1362.10.18632/oncotarget.1817Suche in Google Scholar PubMed PubMed Central
Tanimoto, H., Yan, Y., Clarke, J., Korourian, S., Shigemasa, K., Parmley, T.H., Parham, G.P., and O’Brien, T.J. (1997). Hepsin, a cell surface serine protease identified in hepatoma cells, is overexpressed in ovarian cancer. Cancer Res. 57, 2884–2887.Suche in Google Scholar
Tanimoto, H., Underwood, L.J., Wang, Y., Shigemasa, K., Parmley, T.H., and O’Brien, T.J. (2001). Ovarian tumor cells express a transmembrane serine protease: a potential candidate for early diagnosis and therapeutic intervention. Tumour Biol. 22, 104–114.10.1159/000050604Suche in Google Scholar
Tanimoto, H., Shigemasa, K., Tian, X., Gu, L., Beard, J.B., Sawasaki, T., and O’Brien, T.J. (2005). Transmembrane serine protease TADG-15 (ST14/Matriptase/MT-SP1): expression and prognostic value in ovarian cancer. Br. J. Cancer 92, 278–283.10.1038/sj.bjc.6602320Suche in Google Scholar
Tervonen, T.A., Belitškin, D., Pant, S.M., Englund, J.I., Marques, E., Ala-Hongisto, H., Nevalaita, L., Sihto, H., Heikkilä, P., Leidenius, M., et al. (2016). Deregulated hepsin protease activity confers oncogenicity by concomitantly augmenting HGF/MET signalling and disrupting epithelial cohesion. Oncogene 92, 278–283.10.1038/onc.2015.248Suche in Google Scholar
Tripathi, M., Potdar, A.A., Yamashita, H., Weidow, B., Cummings, P.T., Kirchhofer, D., and Quaranta, V. (2011). Laminin-332 cleavage by matriptase alters motility parameters of prostate cancer cells. Prostate 71, 184–196.10.1002/pros.21233Suche in Google Scholar
Tsai, W.C., Chao, Y.C., Lee, W.H., Chen, A., Sheu, L.F., and Jin, J.S. (2006). Increasing EMMPRIN and matriptase expression in hepatocellular carcinoma: tissue microarray analysis of immunohistochemical scores with clinicopathological parameters. Histopathology 49, 388–395.10.1111/j.1365-2559.2006.02516.xSuche in Google Scholar
Tsai, C.H., Teng, C.H., Tu, Y.T., Cheng, T.S., Wu, S.R., Ko, C.J., Shyu, H.Y., Lan, S.W., Huang, H.P., Tzeng, S.F., et al. (2014). HAI-2 suppresses the invasive growth and metastasis of prostate cancer through regulation of matriptase. Oncogene 33, 4643–4652.10.1038/onc.2013.412Suche in Google Scholar
Tsuji, A., Torres-Rosado, A., Arai, T., Le Beau, M.M., Lemons, R.S., Chou, S.H., and Kurachi, K. (1991a). Hepsin, a cell membrane-associated protease. Characterization, tissue distribution, and gene localization. J. Biol. Chem. 266, 16948–16953.10.1016/S0021-9258(18)55395-3Suche in Google Scholar
Tsuji, A., Torres-Rosado, A., Arai, T., Chou, S.H., and Kurachi, K. (1991b). Characterization of hepsin, a membrane bound protease. Biomed. Biochim. Acta 50, 791–793.Suche in Google Scholar
Uhland, K., Siphos, B., Arkona, C., Schuster, M., Petri, B., Steinmetzer, P., Mueller, F., Schweinitz, A., Steinmetzer, T., and Van De Locht, A. (2009). Use of IHC and newly designed matriptase inhibitors to elucidate the role of matriptase in pancreatic ductal adenocarcinoma. Int. J. Oncol. 35, 347–357.Suche in Google Scholar
Valkenburg, K.C., Yu, X., De marzo, A.M., Spiering, T.J., Matusik, R.J., and Williams, B.O. (2014). Activation of Wnt/β-catenin signaling in a subpopulation of murine prostate luminal epithelial cells induces high grade prostate intraepithelial neoplasia. Prostate 74, 1506–1520.10.1002/pros.22868Suche in Google Scholar PubMed PubMed Central
Valkenburg, K.C., Hostetter, G., and Williams, B.O. (2015). Concurrent Hepsin overexpression and denomatous polyposis coli deletion causes invasive prostate carcinoma in mice. Prostate 75, 1579–1585.10.1002/pros.23032Suche in Google Scholar PubMed
Vogel, L.K., Saebo, M., Skjelbred, C.F., Abell, K., Pedersen, E.D., Vogel, U., and Kure, E.H. (2006). The ratio of Matriptase/HAI-1 mRNA is higher in colorectal cancer adenomas and carcinomas than corresponding tissue from control individuals. BMC Cancer 6, 176.10.1111/j.1538-7836.2006.00310.xSuche in Google Scholar
Wallrapp, C., Uehara, H., and K Izumi. (2000). A novel transmembrane serine protease (TMPRSS3) overexpressed in pancreatic cancer. Cancer Res 60, 2602–2606.Suche in Google Scholar
Wang, C.H., Guo, Z.Y., Chen, Z.T., Zhi, X.T., Li, D.K., Dong, Z.R., Chen, Z.Q., Hu, S.y., and Li, T. (2015). TMPRSS4 facilitates epithelial-mesenchymal transition of hepatocellular carcinoma and is a predictive marker for poor prognosis of patients after curative resection. Sci. Rep. 5, 12366.10.1038/srep12366Suche in Google Scholar PubMed PubMed Central
Webb, S.L., Sanders, A.J., Mason, M.D., and Jiang, W.G. (2011). Type II transmembrane serine protease (TTSP) deregulation in cancer. Front. Biosci. 16, 539–552.10.2741/3704Suche in Google Scholar PubMed
Welman, A., Sproul, D., Mullen, P., Muir, M., Kinnaird, A.R., Harrison, D.J., Faratian, D., Brunton, V.G., and Frame, M.C. (2012). Diversity of matriptase expression level and function in breast cancer. PloS One 7, e34182.10.1371/journal.pone.0034182Suche in Google Scholar PubMed PubMed Central
Wilson, S.R., Gallagher, S., Warpeha, K., and Hawthorne, S.J. (2004). Amplification of MMP-2 and MMP-9 production by prostate cancer cell lines via activation of protease-activated receptors. Prostate 60, 168–174.10.1002/pros.20047Suche in Google Scholar PubMed
Wilson, S., Greer, B., Hooper, J., Zijlstra, A., Walker, B., Quigley, J., and S Hawthorne. (2005). The membrane-anchored serine protease, TMPRSS2, activates PAR-2 in prostate cancer cells. Biochem. J. 388, 967–972.10.1042/BJ20041066Suche in Google Scholar PubMed PubMed Central
Wu, S.R., Cheng, T.S., Chen, W.C., Shyu, H.Y., Ko, C.J., Huang, H.P., Teng, C.H., Lin, C.H., Johnson, M.D., Lin, C.Y., et al. (2010). Matriptase is involved in ErbB-2-induced prostate cancer cell invasion. Am. J. Pathol. 177, 3145–3158.10.2353/ajpath.2010.100228Suche in Google Scholar PubMed PubMed Central
Wu, X.Y., Zhang, L., Zhang, K.M., Zhang, M.H., Ruan, T.Y., Liu, C.Y., and JY, Xu. (2014). Clinical implication of TMPRSS4 expression in human gallbladder cancer. Tumour Biol. 35, 5481–5486.10.1007/s13277-014-1716-4Suche in Google Scholar PubMed
Xing, P., Li, J.G., Jin, F., Zhao, T.T., Liu, Q., Dong, H.T., and Wei, X.L. (2011). Clinical and biological significance of hepsin overexpression in breast cancer. J. Investig. Med. 59, 803–810.10.2310/JIM.0b013e31821451a1Suche in Google Scholar PubMed
Xuan, J.A., Schneider, D., Toy, P., Lin, R., Newton, A., Zhu, Y., Finster, S., Vogel, D., Mintzer, B., Dinter, H., et al. (2006). Antibodies neutralizing hepsin protease activity do not impact cell growth but inhibit invasion of prostate and ovarian tumor cells in culture. Cancer Res. 66, 3611–3619.10.1158/0008-5472.CAN-05-2983Suche in Google Scholar PubMed
Ye, J., Kawaguchi, M., Haruyama, Y., Kanemaru, A., Fukushima, T., Yamamoto, K., Lin, C.Y., and Kataoka, H. (2014). Loss of hepatocyte growth factor activator inhibitor type 1 participates in metastatic spreading of human pancreatic cancer cells in a mouse orthotopic transplantation model. Cancer Sci. 105, 44–51.10.1111/cas.12306Suche in Google Scholar PubMed PubMed Central
Yin, H., Kosa, P., Liu, X., Swaim, W.D., Lai, Z., Cabrera-Perez, J., Di Pasquale, G., Ambudkar, I.S., Bugge, T.H., and Chiorini, J.A. (2014). Matriptase deletion initiates a Sjögren’s syndrome-like disease in mice. PLoS One 9, e82852.10.1371/journal.pone.0082852Suche in Google Scholar PubMed PubMed Central
Zeng, L., Cao, J., and Zhang, X. (2005). Expression of serine protease SNC19/matriptase and its inhibitor hepatocyte growth factor activator inhibitor type 1 in normal and malignant tissues of gastrointestinal tract. World J. Gastroenterol. 11, 6202–6207.10.3748/wjg.v11.i39.6202Suche in Google Scholar PubMed PubMed Central
Zoratti, G.L., Tanabe, L.M., Varela, F.A., Murray, A.S., Bergum, C., Colombo, É., Lang, J.E., Molinolo, A.A., Leduc, R., Marsault, E., et al. (2015). Targeting matriptase in breast cancer abrogates tumour progression via impairment of stromal-epithelial growth factor signalling. Nat. Commun. 6, 6776.10.1038/ncomms7776Suche in Google Scholar PubMed PubMed Central
©2016 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Guest Editorial
- Highlight: proteolytic networks across cellular boundaries
- HIGHLIGHT: IPS 2015 – 9TH GENERAL MEETING OF THE INTERNATIONAL PROTEOLYSIS SOCIETY
- A personal journey with matrix metalloproteinases
- Type II transmembrane serine proteases as potential targets for cancer therapy
- Membrane trafficking and proteolytic activity of γ-secretase in Alzheimer’s disease
- Dipeptidyl peptidase 9 substrates and their discovery: current progress and the application of mass spectrometry-based approaches
- Tetraspanin 8 is an interactor of the metalloprotease meprin β within tetraspanin-enriched microdomains
- Procathepsin E is highly abundant but minimally active in pancreatic ductal adenocarcinoma tumors
- Granzyme B inhibits keratinocyte migration by disrupting epidermal growth factor receptor (EGFR)-mediated signaling
- Myeloid conditional deletion and transgenic models reveal a threshold for the neutrophil survival factor Serpinb1
- Probing catalytic rate enhancement during intramembrane proteolysis
- Human 20S proteasome activity towards fluorogenic peptides of various chain lengths
- Research Articles/Short Communications
- Protein Structure and Function
- Biophysical analysis of three novel profilin-1 variants associated with amyotrophic lateral sclerosis indicates a correlation between their aggregation propensity and the structural features of their globular state
- The potential of the Galleria mellonella innate immune system is maximized by the co-presentation of diverse antimicrobial peptides
Artikel in diesem Heft
- Frontmatter
- Guest Editorial
- Highlight: proteolytic networks across cellular boundaries
- HIGHLIGHT: IPS 2015 – 9TH GENERAL MEETING OF THE INTERNATIONAL PROTEOLYSIS SOCIETY
- A personal journey with matrix metalloproteinases
- Type II transmembrane serine proteases as potential targets for cancer therapy
- Membrane trafficking and proteolytic activity of γ-secretase in Alzheimer’s disease
- Dipeptidyl peptidase 9 substrates and their discovery: current progress and the application of mass spectrometry-based approaches
- Tetraspanin 8 is an interactor of the metalloprotease meprin β within tetraspanin-enriched microdomains
- Procathepsin E is highly abundant but minimally active in pancreatic ductal adenocarcinoma tumors
- Granzyme B inhibits keratinocyte migration by disrupting epidermal growth factor receptor (EGFR)-mediated signaling
- Myeloid conditional deletion and transgenic models reveal a threshold for the neutrophil survival factor Serpinb1
- Probing catalytic rate enhancement during intramembrane proteolysis
- Human 20S proteasome activity towards fluorogenic peptides of various chain lengths
- Research Articles/Short Communications
- Protein Structure and Function
- Biophysical analysis of three novel profilin-1 variants associated with amyotrophic lateral sclerosis indicates a correlation between their aggregation propensity and the structural features of their globular state
- The potential of the Galleria mellonella innate immune system is maximized by the co-presentation of diverse antimicrobial peptides