Clinical relevance of kallikrein-related peptidase 6 (KLK6) and 8 (KLK8) mRNA expression in advanced serous ovarian cancer

References

Avgeris, M., Mavridis, K., and Scorilas, A. (2012). Kallikrein-related peptidases in prostate, breast, and ovarian cancers: from pathobiology to clinical relevance. Biol. Chem. 393, 301–317.10.1515/hsz-2011-0260Search in Google Scholar PubMed

Bayani, J. and Diamandis, E.P. (2012). The physiology and pathobiology of human kallikrein-related peptidase 6 (KLK6). Clin. Chem. Lab. Med. 50, 211–233.10.1515/cclm.2011.750Search in Google Scholar PubMed

Bayani, J., Paliouras, M., Planque, C., Shan, S.J., Graham, C., Squire, J.A., and Diamandis, E.P. (2008). Impact of cytogenetic and genomic aberrations of the kallikrein locus in ovarian cancer. Mol. Oncol. 2, 250–260.10.1016/j.molonc.2008.07.001Search in Google Scholar PubMed PubMed Central

Borgono, C.A., Kishi, T., Scorilas, A., Harbeck, N., Dorn, J., Schmalfeldt, B., Schmitt, M., and Diamandis, E.P. (2006). Human kallikrein 8 protein is a favorable prognostic marker in ovarian cancer. Clin. Cancer Res. 12, 1487–1493.10.1158/1078-0432.CCR-05-2106Search in Google Scholar PubMed

Bustin, A. and Nolan, T. (2013). Analysis of mRNA expression by real-time PCR. In: Real-Time PCR: Advanced Technologies and Applications, A. Saunders and A. Lee, eds. (Norfolk, UK: Caister Academic Press), pp. 51–88.10.21775/9781912530243.13Search in Google Scholar

Cané, S., Bignotti, E., Bellone, S., Palmieri, M., De las Casas, L., Roman, J.J., Pecorelli, S., Cannon, M.J., O’Brien, T., and Santin, A.D. (2004). The novel serine protease tumor-associated differentially expressed gene-14 (KLK8/Neuropsin/Ovasin) is highly overexpressed in cervical cancer. Am. J. Obstet. Gynecol. 190, 60–66.10.1016/j.ajog.2003.07.020Search in Google Scholar PubMed

Diamandis, E.P., Scorilas, A., Fracchioli, S., Van Gramberen, M., De Bruijn, H., Henrik, A., Soosaipillai, A., Grass, L., Yousef, G.M., Stenman, U.H., et al. (2003). Human kallikrein 6 (hK6): a new potential serum biomarker for diagnosis and prognosis of ovarian carcinoma. J. Clin. Oncol. 21, 1035–1043.10.1200/JCO.2003.02.022Search in Google Scholar PubMed

Dorn, J., Harbeck, N., Kates, R., Gkazepis, A., Scorilas, A., Soosaipillai, A., Diamandis, E., Kiechle, M., Schmalfeldt, B., and Schmitt, M. (2011). Impact of expression differences of kallikrein-related peptidases and of uPA and PAI-1 between primary tumor and omentum metastasis in advanced ovarian cancer. Ann. Oncol. 22, 877–883.10.1093/annonc/mdq462Search in Google Scholar PubMed

Dorn, J., Beaufort, N., Schmitt, M., Diamandis, E.P., Goettig, P., and Magdolen, V. (2014). Function and clinical relevance of kallikrein-related peptidases and other serine proteases in gynecological cancers. Crit. Rev. Clin. Lab. Sci. 51, 63–84.10.3109/10408363.2013.865701Search in Google Scholar PubMed

Dorn, J., Bronger, H., Kates, R., Slotta-Huspenina, J., Schmalfeldt, B., Kiechle, M., Diamandis, E.P., Soosaipillai, A., Schmitt, M., and Harbeck, N. (2015). OVSCORE – a validated score to identify ovarian cancer patients not suitable for primary surgery. Oncol. Lett. 9, 418–424.10.3892/ol.2014.2630Search in Google Scholar PubMed PubMed Central

Eissa, A., Cretu, D., Soosaipillai, A., Thavaneswaran, A., Pellett, F., Diamandis, A., Cevikbas, F., Steinhoff, M., Diamandis, E.P., Gladman, D., et al. (2013). Serum kallikrein-8 correlates with skin activity, but not psoriatic arthritis, in patients with psoriatic disease. Clin. Chem. Lab. Med. 51, 317–325.10.1515/cclm-2012-0251Search in Google Scholar

Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D.M., Forman, D., and Bray, F. (2015). Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136, E359–E386.10.1002/ijc.29210Search in Google Scholar

Ghosh, M.C., Grass, L., Soosaipillai, A., Sotiropoulou, G., and Diamandis, E.P. (2004). Human kallikrein 6 degrades extracellular matrix proteins and may enhance the metastatic potential of tumour cells. Tumour Biol. 25, 193–199.10.1159/000081102Search in Google Scholar

Henkhaus, R.S., Gerner, E.W., and Ignatenko, N.A. (2008). Kallikrein 6 is a mediator of K-RAS-dependent migration of colon carcinoma cells. Biol. Chem. 389, 757–764.10.1515/BC.2008.087Search in Google Scholar

Hibbs, K., Skubitz, K.M., Pambuccian, S.E., Casey, R.C., Burleson, K.M., Oegema, T.R., Jr., Thiele, J.J., Grindle, S.M., Bliss, R.L., and Skubitz, A.P. (2004). Differential gene expression in ovarian carcinoma: identification of potential biomarkers. Am. J. Pathol. 165, 397–414.10.1016/S0002-9440(10)63306-8Search in Google Scholar

Kim, J.T., Song, E.Y., Chung, K.S., Kang, M.A., Kim, J.W., Kim, S.J., Yeom, Y.I., Kim, J.H., Kim, K.H., and Lee, H.G. (2011). Up-regulation and clinical significance of serine protease kallikrein 6 in colon cancer. Cancer 117, 2608–2619.10.1002/cncr.25841Search in Google Scholar PubMed

Kipps, E., Tan, D.S., and Kaye, S.B. (2013). Meeting the challenge of ascites in ovarian cancer: new avenues for therapy and research. Nat. Rev. Cancer 13, 273–282.10.1038/nrc3432Search in Google Scholar PubMed PubMed Central

Kishi, T., Grass, L., Soosaipillai, A., Scorilas, A., Harbeck, N., Schmalfeldt, B., Dorn, J., Mysliwiec, M., Schmitt, M., and Diamandis, E.P. (2003). Human kallikrein 8, a novel biomarker for ovarian carcinoma. Cancer Res 63, 2771–2774.Search in Google Scholar

Kishibe, M., Bando, Y., Terayama, R., Namikawa, K., Takahashi, H., Hashimoto, Y., Ishida-Yamamoto, A., Jiang, Y.P., Mitrovic, B., Perez, D., et al. (2007). Kallikrein 8 is involved in skin desquamation in cooperation with other kallikreins. J. Biol. Chem. 282, 5834–5841.10.1074/jbc.M607998200Search in Google Scholar PubMed

Kishibe, M., Bando, Y., Tanaka, T., Ishida-Yamamoto, A., Iizuka, H., and Yoshida, S. (2012). Kallikrein-related peptidase 8-dependent skin wound healing is associated with upregulation of kallikrein-related peptidase 6 and PAR2. J. Invest. Dermatol. 132, 1717–1724.10.1038/jid.2012.18Search in Google Scholar PubMed

Klucky, B., Mueller, R., Vogt, I., Teurich, S., Hartenstein, B., Breuhahn, K., Flechtenmacher, C., Angel, P., and Hess, J. (2007). Kallikrein 6 induces E-cadherin shedding and promotes cell proliferation, migration, and invasion. Cancer Res. 67, 8198–8206.10.1158/0008-5472.CAN-07-0607Search in Google Scholar PubMed

Kolin, D.L., Sy, K., Rotondo, F., Bassily, M.N., Kovacs, K., Brezden-Masley, C., Streutker, C.J., and Yousef, G.M. (2014). Prognostic significance of human tissue kallikrein-related peptidases 6 and 10 in gastric cancer. Biol. Chem. 395, 1087–1093.10.1515/hsz-2014-0143Search in Google Scholar PubMed

Kountourakis, P., Psyrri, A., Scorilas, A., Camp, R., Markakis, S., Kowalski, D., Diamandis, E.P., and Dimopoulos, M.A. (2008). Prognostic value of kallikrein-related peptidase 6 protein expression levels in advanced ovarian cancer evaluated by automated quantitative analysis (AQUA). Cancer Sci. 99, 2224–2229.10.1111/j.1349-7006.2008.00942.xSearch in Google Scholar PubMed

Kountourakis, P., Psyrri, A., Scorilas, A., Markakis, S., Kowalski, D., Camp, R.L., Diamandis, E.P., and Dimopoulos, M.A. (2009). Expression and prognostic significance of kallikrein-related peptidase 8 protein levels in advanced ovarian cancer by using automated quantitative analysis. Thromb. Haemost. 101, 541–546.10.1160/TH08-01-0052Search in Google Scholar

Kryza, T., Silva, M.L., Loessner, D., Heuze-Vourc’h, N., and Clements, J.A. (2016). The kallikrein-related peptidase family: dysregulation and functions during cancer progression. Biochimie 122, 283–299.10.1016/j.biochi.2015.09.002Search in Google Scholar PubMed

Kuzmanov, U., Jiang, N., Smith, C.R., Soosaipillai, A., and Diamandis, E.P. (2009). Differential N-glycosylation of kallikrein 6 derived from ovarian cancer cells or the central nervous system. Mol. Cell. Proteomics 8, 791–798.10.1074/mcp.M800516-MCP200Search in Google Scholar PubMed PubMed Central

Loessner, D., Quent, V.M., Kraemer, J., Weber, E.C., Hutmacher, D.W., Magdolen, V., and Clements, J.A. (2012). Combined expression of KLK4, KLK5, KLK6, and KLK7 by ovarian cancer cells leads to decreased adhesion and paclitaxel-induced chemoresistance. Gynecol. Oncol. 127, 569–578.10.1016/j.ygyno.2012.09.001Search in Google Scholar PubMed

Magklara, A., Scorilas, A., Katsaros, D., Massobrio, M., Yousef, G.M., Fracchioli, S., Danese, S., and Diamandis, E.P. (2001). The human KLK8 (neuropsin/ovasin) gene: identification of two novel splice variants and its prognostic value in ovarian cancer. Clin. Cancer Res. 7, 806–811.Search in Google Scholar

Nathalie, H.V., Chris, P., Serge, G., Catherine, C., Benjamin, B., Claire, B., Christelle, P., Briollais, L., Pascale, R., Marie-Lise, J., et al. (2009). High kallikrein-related peptidase 6 in non-small cell lung cancer cells: an indicator of tumour proliferation and poor prognosis. J. Cell. Mol. Med. 13, 4014–4022.10.1111/j.1582-4934.2009.00763.xSearch in Google Scholar PubMed PubMed Central

Pampalakis, G. and Sotiropoulou, G. (2007). Tissue kallikrein proteolytic cascade pathways in normal physiology and cancer. Biochim. Biophys. Acta. 1776, 22–31.10.1016/j.bbcan.2007.06.001Search in Google Scholar PubMed

Pfaffl, W. (2012). Quantification strategies in real-time polymerase chain reaction. In: Quantitative Real-Time PCR in Applied Microbiology, M. Filion, ed. (Norfolk, UK: Caister Academic Press), pp. 53–61.10.21775/9781912530243.05Search in Google Scholar

Planque, C., Choi, Y.H., Guyetant, S., Heuze-Vourc’h, N., Briollais, L., and Courty, Y. (2010). Alternative splicing variant of kallikrein-related peptidase 8 as an independent predictor of unfavorable prognosis in lung cancer. Clin. Chem. 56, 987–997.10.1373/clinchem.2009.138917Search in Google Scholar PubMed

Prassas, I., Eissa, A., Poda, G., and Diamandis, E.P. (2015). Unleashing the therapeutic potential of human kallikrein-related serine proteases. Nat. Rev. Drug. Discov. 14, 183–202.10.1038/nrd4534Search in Google Scholar PubMed

Prat, J. (2012). Ovarian carcinomas: five distinct diseases with different origins, genetic alterations, and clinicopathological features. Virchow’s Arch. 460, 237–249.10.1007/s00428-012-1203-5Search in Google Scholar PubMed

Prat, J. (2014). Staging classification for cancer of the ovary, fallopian tube, and peritoneum. Int. J. Gynaecol. Obstet. 124, 1–5.10.1016/j.ijgo.2013.10.001Search in Google Scholar PubMed

Prezas, P., Arlt, M.J., Viktorov, P., Soosaipillai, A., Holzscheiter, L., Schmitt, M., Talieri, M., Diamandis, E.P., Kruger, A., and Magdolen, V. (2006). Overexpression of the human tissue kallikrein genes KLK4, 5, 6, and 7 increases the malignant phenotype of ovarian cancer cells. Biol. Chem. 387, 807–811.10.1515/BC.2006.102Search in Google Scholar PubMed

Ruckert, F., Hennig, M., Petraki, C.D., Wehrum, D., Distler, M., Denz, A., Schroder, M., Dawelbait, G., Kalthoff, H., Saeger, H.D., et al. (2008). Co-expression of KLK6 and KLK10 as prognostic factors for survival in pancreatic ductal adenocarcinoma. Br. J. Cancer 99, 1484–1492.10.1038/sj.bjc.6604717Search in Google Scholar PubMed PubMed Central

Scarisbrick, I.A. (2012). Physiological and pathophysiological roles of kallikrein-related peptidases in the central nervous system. In: Kallikrein-Related Peptidases. Characterization, Regulation, and Interactions within the Protease Web, Vol. 1, V. Magdolen, C.P. Sommerhoff, H. Fritz, M. Schmitt, M. (eds.) (Berlin, Germany: DeGruyter), pp. 349–372.10.1515/9783110260373.349Search in Google Scholar

Seiz, L., Dorn, J., Kotzsch, M., Walch, A., Grebenchtchikov, N.I., Gkazepis, A., Schmalfeldt, B., Kiechle, M., Bayani, J., Diamandis, E.P., et al. (2012). Stromal cell-associated expression of kallikrein-related peptidase 6 (KLK6) indicates poor prognosis of ovarian cancer patients. Biol. Chem. 393, 391–401.10.1515/hsz-2011-0264Search in Google Scholar PubMed

Sher, Y.P., Chou, C.C., Chou, R.H., Wu, H.M., Wayne Chang, W.S., Chen, C.H., Yang, P.C., Wu, C.W., Yu, C.L., and Peck, K. (2006). Human kallikrein 8 protease confers a favorable clinical outcome in non-small cell lung cancer by suppressing tumor cell invasiveness. Cancer Res. 66, 11763–11770.10.1158/0008-5472.CAN-06-3165Search in Google Scholar PubMed

Shigemasa, K., Tian, X., Gu, L., Tanimoto, H., Underwood, L.J., O’Brien, T.J., and Ohama, K. (2004). Human kallikrein 8 (hK8/TADG-14) expression is associated with an early clinical stage and favorable prognosis in ovarian cancer. Oncol Rep 11, 1153–1159.10.3892/or.11.6.1153Search in Google Scholar

Shimizu-Okabe, C., Yousef, G.M., Diamandis, E.P., Yoshida, S., Shiosaka, S., and Fahnestock, M. (2001). Expression of the kallikrein gene family in normal and Alzheimer’s disease brain. Neuroreport 12, 2747–2751.10.1097/00001756-200108280-00031Search in Google Scholar PubMed

Tatebe, H., Watanabe, Y., Kasai, T., Mizuno, T., Nakagawa, M., Tanaka, M., and Tokuda, T. (2010). Extracellular neurosin degrades alpha-synuclein in cultured cells. Neurosci Res 67, 341–346.10.1016/j.neures.2010.04.008Search in Google Scholar

Terayama, R., Bando, Y., Takahashi, T., and Yoshida, S. (2004). Differential expression of neuropsin and protease M/neurosin in oligodendrocytes after injury to the spinal cord. Glia 48, 91–101.10.1002/glia.20058Search in Google Scholar

Underwood, L.J., Tanimoto, H., Wang, Y., Shigemasa, K., Parmley, T.H., and O’Brien, T.J. (1999). Cloning of tumor-associated differentially expressed gene-14, a novel serine protease overexpressed by ovarian carcinoma. Cancer Res. 59, 4435–4439.Search in Google Scholar

Vakrakou, A., Devetzi, M., Papachristopoulou, G., Malachias, A., Scorilas, A., Xynopoulos, D., and Talieri, M. (2014). Kallikrein-related peptidase 6 (KLK6) expression in the progression of colon adenoma to carcinoma. Biol. Chem. 395, 1105–1117.10.1515/hsz-2014-0166Search in Google Scholar

Wang, S.M., Mao, J., Li, B., Wu, W., and Tang, L.L. (2008). Expression of KLK6 protein and mRNA in primary breast cancer and its clinical significance. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 24, 1087–1089.Search in Google Scholar

White, N.M., Mathews, M., Yousef, G.M., Prizada, A., Popadiuk, C., and Dore, J.J. (2009). KLK6 and KLK13 predict tumor recurrence in epithelial ovarian carcinoma. Br. J. Cancer 101, 1107–1113.10.1038/sj.bjc.6605280Search in Google Scholar

Yoshida, S. (2003). Kallikrein-family serine protease in the central nervous system. Kaibogaku Zasshi 78, 77–82.Search in Google Scholar

Yousef, G.M., Kishi, T., and Diamandis, E.P. (2003a). Role of kallikrein enzymes in the central nervous system. Clin. Chim. Acta 329, 1–8.10.1016/S0009-8981(03)00004-4Search in Google Scholar

Yousef, G.M., Polymeris, M.E., Yacoub, G.M., Scorilas, A., Soosaipillai, A., Popalis, C., Fracchioli, S., Katsaros, D., and Diamandis, E.P. (2003b). Parallel overexpression of seven kallikrein genes in ovarian cancer. Cancer Res. 63, 2223–2227.Search in Google Scholar

Yousef, G.M., Borgono, C.A., Popalis, C., Yacoub, G.M., Polymeris, M.E., Soosaipillai, A., and Diamandis, E.P. (2004). In-silico analysis of kallikrein gene expression in pancreatic and colon cancers. Anticancer Res. 24, 43–51.Search in Google Scholar

Zheng, Y., Katsaros, D., Shan, S.J., de la Longrais, I.R., Porpiglia, M., Scorilas, A., Kim, N.W., Wolfert, R.L., Simon, I., Li, L., et al. (2007). A multiparametric panel for ovarian cancer diagnosis, prognosis, and response to chemotherapy. Clin. Cancer Res. 13, 6984–6992.10.1158/1078-0432.CCR-07-1409Search in Google Scholar PubMed