Startseite Kallikrein-related peptidases and associated microRNAs as promising prognostic biomarkers in gastrointestinal malignancies
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Kallikrein-related peptidases and associated microRNAs as promising prognostic biomarkers in gastrointestinal malignancies

  • Panagiotis G. Adamopoulos , Panagiotis Tsiakanikas und Andreas Scorilas ORCID logo EMAIL logo
Veröffentlicht/Copyright: 7. Juni 2018

Abstract

Gastrointestinal (GI) malignancies represent a wide spectrum of diseases of the GI tract and its accessory digestive organs, including esophageal (EC), gastric (GC), hepatocellular, pancreatic (PC) and colorectal cancers (CRC). Malignancies of the GI system are responsible for nearly 30% of cancer-related morbidity and approximately 40% of cancer-related mortality, worldwide. For this reason, the discovery of novel prognostic biomarkers that can efficiently provide a better prognosis, risk assessment and prediction of treatment response is an imperative need. Human kallikrein-related peptidases (KLKs) are a subgroup of trypsin and chymotrypsin-like serine peptidases that have emerged as promising prognosticators for many human types of cancer, being aberrantly expressed in cancerous tissues. The aberrant expression of KLKs in human malignancies is often regulated by KLK/microRNAs (miRNAs) interactions, as many miRNAs have been found to target KLKs and therefore alter their expression levels. The biomarker utility of KLKs has been elucidated not only in endocrine-related human malignancies, including those of the prostate and breast, but also in GI malignancies. The main purpose of this review is to summarize the existing information regarding the prognostic significance of KLKs in major types of GI malignancies and highlight the regulatory role of miRNAs on the expression levels of KLKs in these types of cancer.

References

Adamopoulos, P.G., Kontos, C.K., Papageorgiou, S.G., Pappa, V., and Scorilas, A. (2015a). KLKB1 mRNA overexpression: a novel molecular biomarker for the diagnosis of chronic lymphocytic leukemia. Clin. Biochem. 48, 849–854.10.1016/j.clinbiochem.2015.04.007Suche in Google Scholar PubMed

Adamopoulos, P.G., Kontos, C.K., Rapti, S.M., Papadopoulos, I.N., and Scorilas, A. (2015b). miR-224 overexpression is a strong and independent prognosticator of short-term relapse and poor overall survival in colorectal adenocarcinoma. Int. J. Oncol. 46, 849–859.10.3892/ijo.2014.2775Suche in Google Scholar PubMed

Adamopoulos, P.G., Kontos, C.K., Tsiakanikas, P., and Scorilas, A. (2016). Identification of novel alternative splice variants of the BCL2L12 gene in human cancer cells using next-generation sequencing methodology. Cancer Lett. 373, 119–129.10.1016/j.canlet.2016.01.019Suche in Google Scholar PubMed

Adamopoulos, P.G., Kontos, C.K., and Scorilas, A. (2017a). Identification and molecular cloning of novel transcripts of the human kallikrein-related peptidase 10 (KLK10) gene using next-generation sequencing. Biochem. Biophys. Res. Commun. 487, 776–781.10.1016/j.bbrc.2017.04.078Suche in Google Scholar PubMed

Adamopoulos, P.G., Kontos, C.K., and Scorilas, A. (2017b). Molecular cloning of novel transcripts of human kallikrein-related peptidases 5, 6, 7, 8 and 9 (KLK5–KLK9), using next-generation sequencing. Sci. Rep. 7, 17299.10.1038/s41598-017-16269-6Suche in Google Scholar PubMed PubMed Central

Adamopoulos, P.G., Kontos, C.K., and Scorilas, A. (2018a). Novel splice variants of the human kallikrein-related peptidases 11 (KLK11) and 12 (KLK12), unraveled by next-generation sequencing technology. Biol. Chem., doi: 10.1515/hsz-2017-0294.10.1515/hsz-2017-0294Suche in Google Scholar PubMed

Adamopoulos, P.G., Kontos, C.K., and Scorilas, A. (2018b). Discovery of novel transcripts of the human tissue kallikrein (KLK1) and kallikrein-related peptidase 2 (KLK2) in human cancer cells, exploiting next-generation sequencing technology. Genomics, doi: 10.1016/j.ygeno.2018.03.022.10.1016/j.ygeno.2018.03.022Suche in Google Scholar PubMed

Adamopoulos, P.G., Raptis, G.D., Kontos, C.K., and Scorilas, A. (2018c). Discovery and expression analysis of novel transcripts of the human SR-related CTD-associated factor 1 (SCAF1) gene in human cancer cells using Next-Generation Sequencing. Gene 670, 155–165.10.1016/j.gene.2018.05.044Suche in Google Scholar PubMed

Alexopoulou, D.K., Papadopoulos, I.N., and Scorilas, A. (2013). Clinical significance of kallikrein-related peptidase (KLK10) mRNA expression in colorectal cancer. Clin. Biochem. 46, 1453–1461.10.1016/j.clinbiochem.2013.03.002Suche in Google Scholar PubMed

Alexopoulou, D.K., Kontos, C.K., Christodoulou, S., Papadopoulos, I.N., and Scorilas, A. (2014). KLK11 mRNA expression predicts poor disease-free and overall survival in colorectal adenocarcinoma patients. Biomark. Med. 8, 671–685.10.2217/bmm.13.151Suche in Google Scholar PubMed

Anisowicz, A., Sotiropoulou, G., Stenman, G., Mok, S.C., and Sager, R. (1996). A novel protease homolog differentially expressed in breast and ovarian cancer. Mol. Med. 2, 624–636.10.1007/BF03401646Suche in Google Scholar

Anwar, S., Frayling, I.M., Scott, N.A., and Carlson, G.L. (2004). Systematic review of genetic influences on the prognosis of colorectal cancer. Br. J. Surg. 91, 1275–1291.10.1002/bjs.4737Suche in Google Scholar PubMed

Avgeris, M. and Scorilas, A. (2016). Kallikrein-related peptidases (KLKs) as emerging therapeutic targets: focus on prostate cancer and skin pathologies. Expert Opin. Ther. Targets 20, 801–818.10.1517/14728222.2016.1147560Suche in Google Scholar PubMed

Avgeris, M., Mavridis, K., and Scorilas, A. (2010). Kallikrein-related peptidase genes as promising biomarkers for prognosis and monitoring of human malignancies. Biol. Chem. 391, 505–511.10.1515/bc.2010.056Suche in Google Scholar PubMed

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-2011-0260Suche in Google Scholar PubMed

Bagaria, B., Sood, S., Sharma, R., and Lalwani, S. (2013). Comparative study of CEA and CA19-9 in esophageal, gastric and colon cancers individually and in combination (ROC curve analysis). Cancer Biol. Med. 10, 148–157.Suche in Google Scholar

Bartel, D.P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233.10.1016/j.cell.2009.01.002Suche in Google Scholar PubMed PubMed Central

Bayani, J. and Diamandis, E.P. (2011). The physiology and pathobiology of human kallikrein-related peptidase 6 (KLK6). Clin. Chem. Lab. Med. 50, 211–233.10.1515/cclm.2011.750Suche in Google Scholar PubMed

Bhoola, K., Ramsaroop, R., Plendl, J., Cassim, B., Dlamini, Z., and Naicker, S. (2001). Kallikrein and kinin receptor expression in inflammation and cancer. Biol. Chem. 382, 77–89.10.1515/BC.2001.013Suche in Google Scholar PubMed

Chen, D.L., Zhang, D.S., Lu, Y.X., Chen, L.Z., Zeng, Z.L., He, M.M., Wang, F.H., Li, Y.H., Zhang, H.Z., Pelicano, H., et al. (2015). microRNA-217 inhibits tumor progression and metastasis by downregulating EZH2 and predicts favorable prognosis in gastric cancer. Oncotarget 6, 10868–10879.10.18632/oncotarget.3451Suche in Google Scholar PubMed PubMed Central

Chow, T.F., Crow, M., Earle, T., El-Said, H., Diamandis, E.P., and Yousef, G.M. (2008). Kallikreins as microRNA targets: an in silico and experimental-based analysis. Biol. Chem. 389, 731–738.10.1515/BC.2008.071Suche in Google Scholar PubMed

Christodoulou, M.I., Kontos, C.K., Halabalaki, M., Skaltsounis, A.L., and Scorilas, A. (2014a). Nature promises new anticancer agents: Interplay with the apoptosis-related BCL2 gene family. Anticancer Agents Med. Chem. 14, 375–399.10.2174/18715206113139990089Suche in Google Scholar PubMed

Christodoulou, S., Alexopoulou, D.K., Kontos, C.K., Scorilas, A., and Papadopoulos, I.N. (2014b). Kallikrein-related peptidase-6 (KLK6) mRNA expression is an independent prognostic tissue biomarker of poor disease-free and overall survival in colorectal adenocarcinoma. Tumour Biol. 35, 4673–4685.10.1007/s13277-014-1612-ySuche in Google Scholar PubMed

Cidon, E.U. and Bustamante, R. (2011). Gastric cancer: tumor markers as predictive factors for preoperative staging. J. Gastrointest. Cancer 42, 127–130.10.1007/s12029-010-9161-0Suche in Google Scholar PubMed

Clements, J., Hooper, J., Dong, Y., and Harvey, T. (2001). The expanded human kallikrein (KLK) gene family: genomic organisation, tissue-specific expression and potential functions. Biol. Chem. 382, 5–14.10.1515/BC.2001.002Suche in Google Scholar PubMed

Consortium, E.P. (2012). An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57–74.10.1038/nature11247Suche in Google Scholar PubMed PubMed Central

D’Angelo, E., Vicentini, C., Agostini, M., Kiss, A., Baffa, R., Scarpa, A., and Fassan, M. (2015). MicroRNAs as tools and effectors for patient treatment in gastrointestinal carcinogenesis. Curr. Drug Targets 16, 383–392.10.2174/1389450116666141210091454Suche in Google Scholar PubMed

Dawsey, S.P., Tonui, S., Parker, R.K., Fitzwater, J.W., Dawsey, S.M., White, R.E., and Abnet, C.C. (2010). Esophageal cancer in young people: a case series of 109 cases and review of the literature. PLoS One 5, e14080.10.1371/journal.pone.0014080Suche in Google Scholar PubMed PubMed Central

Deng, S., Zhu, S., Wang, B., Li, X., Liu, Y., Qin, Q., Gong, Q., Niu, Y., Xiang, C., Chen, J., et al. (2014). Chronic pancreatitis and pancreatic cancer demonstrate active epithelial-mesenchymal transition profile, regulated by miR-217-SIRT1 pathway. Cancer Lett. 355, 184–191.10.1016/j.canlet.2014.08.007Suche in Google Scholar PubMed

Devetzi, M., Trangas, T., Scorilas, A., Xynopoulos, D., and Talieri, M. (2013). Parallel overexpression and clinical significance of kallikrein-related peptidases 7 and 14 (KLK7KLK14) in colon cancer. Thromb. Haemost. 109, 716–725.10.1160/TH12-07-0518Suche in Google Scholar PubMed

Di Tommaso, L., Franchi, G., Park, Y.N., Fiamengo, B., Destro, A., Morenghi, E., Montorsi, M., Torzilli, G., Tommasini, M., Terracciano, L., et al. (2007). Diagnostic value of HSP70, glypican 3, and glutamine synthetase in hepatocellular nodules in cirrhosis. Hepatology 45, 725–734.10.1002/hep.21531Suche in Google Scholar PubMed

Diamantopoulos, M.A., Kontos, C.K., Kerimis, D., Papadopoulos, I.N., and Scorilas, A. (2017). Upregulated miR-16 expression is an independent indicator of relapse and poor overall survival of colorectal adenocarcinoma patients. Clin. Chem. Lab. Med. 55, 737–747.10.1515/cclm-2016-0756Suche in Google Scholar

Dou, R., Nishihara, R., Cao, Y., Hamada, T., Mima, K., Masuda, A., Masugi, Y., Shi, Y., Gu, M., Li, W., et al. (2016). MicroRNA let-7, T cells, and patient survival in colorectal cancer. Cancer Immunol. Res. 4, 927–935.10.1158/2326-6066.CIR-16-0112Suche in Google Scholar

Duffy, M.J., Sturgeon, C., Lamerz, R., Haglund, C., Holubec, V.L., Klapdor, R., Nicolini, A., Topolcan, O., and Heinemann, V. (2010). Tumor markers in pancreatic cancer: a European Group on Tumor Markers (EGTM) status report. Ann. Oncol. 21, 441–447.10.1093/annonc/mdp332Suche in Google Scholar

Duffy, M.J., Lamerz, R., Haglund, C., Nicolini, A., Kalousova, M., Holubec, L., and Sturgeon, C. (2014). Tumor markers in colorectal cancer, gastric cancer and gastrointestinal stromal cancers: European group on tumor markers 2014 guidelines update. Int. J. Cancer 134, 2513–2522.10.1002/ijc.28384Suche in Google Scholar

Feng, B., Xu, W.B., Zheng, M.H., Ma, J.J., Cai, Q., Zhang, Y., Ji, J., Lu, A.G., Qu, Y., Li, J.W., et al. (2006). Clinical significance of human kallikrein 10 gene expression in colorectal cancer and gastric cancer. J. Gastroenterol. Hepatol. 21, 1596–1603.10.1111/j.1440-1746.2006.04228.xSuche 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, E359–386.10.1002/ijc.29210Suche in Google Scholar

Ferraro, A., Kontos, C.K., Boni, T., Bantounas, I., Siakouli, D., Kosmidou, V., Vlassi, M., Spyridakis, Y., Tsipras, I., Zografos, G., et al. (2014). Epigenetic regulation of miR-21 in colorectal cancer: ITGB4 as a novel miR-21 target and a three-gene network (miR-21-ITGBeta4-PDCD4) as predictor of metastatic tumor potential. Epigenetics 9, 129–141.10.4161/epi.26842Suche in Google Scholar

Fiorentino, M., Altimari, A., Ravaioli, M., Gruppioni, E., Gabusi, E., Corti, B., Vivarelli, M., Bringuier, P.P., Scoazec, J.Y., Grigioni, W.F., et al. (2004). Predictive value of biological markers for hepatocellular carcinoma patients treated with orthotopic liver transplantation. Clin. Cancer Res. 10, 1789–1795.10.1158/1078-0432.CCR-1149-3Suche in Google Scholar

Forner, A., Llovet, J.M., and Bruix, J. (2012). Hepatocellular carcinoma. Lancet 379, 1245–1255.10.1016/S0140-6736(11)61347-0Suche in Google Scholar

Foteinou, E., Kontos, C.K., Giotakis, A.I., and Scorilas, A. (2014). Low mRNA expression levels of kallikrein-related peptidase 4 (KLK4) predict short-term relapse in patients with laryngeal squamous cell carcinoma. Biol. Chem. 395, 1051–1062.10.1515/hsz-2014-0139Suche in Google Scholar PubMed

Goonetilleke, K.S. and Siriwardena, A.K. (2007). Systematic review of carbohydrate antigen (CA 19-9) as a biochemical marker in the diagnosis of pancreatic cancer. Eur. J. Surg. Oncol. 33, 266–270.10.1016/j.ejso.2006.10.004Suche in Google Scholar PubMed

Grin, A., Samaan, S., Tripathi, M., Rotondo, F., Kovacs, K., Bassily, M.N., and Yousef, G.M. (2015). Evaluation of human tissue kallikrein-related peptidases 6 and 10 expression in early gastroesophageal adenocarcinoma. Hum. Pathol. 46, 541–548.10.1016/j.humpath.2014.12.005Suche in Google Scholar PubMed

Hayashi, Y., Tsujii, M., Wang, J., Kondo, J., Akasaka, T., Jin, Y., Li, W., Nakamura, T., Nishida, T., Iijima, H., et al. (2013). CagA mediates epigenetic regulation to attenuate let-7 expression in Helicobacter pylori-related carcinogenesis. Gut 62, 1536–1546.10.1136/gutjnl-2011-301625Suche in Google Scholar PubMed

He, F.C., Meng, W.W., Qu, Y.H., Zhou, M.X., He, J., Lv, P., and Ming, L. (2015). Expression of circulating microRNA-20a and let-7a in esophageal squamous cell carcinoma. World J. Gastroenterol. 21, 4660–4665.10.3748/wjg.v21.i15.4660Suche in Google Scholar PubMed PubMed Central

Hu, C.J., Chen, K.X., Zheng, J.F., and Chen, Y.J. (2013). Expression and biological significance of human kallikrein 6 in gastric cancer tissues. Contemp. Oncol. (Pozn.) 17, 64–67.10.5114/wo.2013.33776Suche in Google Scholar PubMed PubMed Central

Huang, W., Zhong, J., Wu, L.Y., Yu, L.F., Tian, X.L., Zhang, Y.F., and Li, B. (2007). Downregulation and CpG island hypermethylation of NES1/hK10 gene in the pathogenesis of human gastric cancer. Cancer Lett. 251, 78–85.10.1016/j.canlet.2006.11.006Suche in Google Scholar PubMed

Huang, W., Tian, X.L., Wu, Y.L., Zhong, J., Yu, L.F., Hu, S.P., and Li, B. (2008). Suppression of gastric cancer growth by baculovirus vector-mediated transfer of normal epithelial cell specific-1 gene. World J. Gastroenterol. 14, 5810–5815.10.3748/wjg.14.5810Suche in Google Scholar PubMed PubMed Central

Iacobuzio-Donahue, C.A., Ashfaq, R., Maitra, A., Adsay, N.V., Shen-Ong, G.L., Berg, K., Hollingsworth, M.A., Cameron, J.L., Yeo, C.J., Kern, S.E., et al. (2003). Highly expressed genes in pancreatic ductal adenocarcinomas: a comprehensive characterization and comparison of the transcription profiles obtained from three major technologies. Cancer Res. 63, 8614–8622.Suche in Google Scholar

Iakovlev, V., Siegel, E.R., Tsao, M.S., and Haun, R.S. (2012). Expression of kallikrein-related peptidase 7 predicts poor prognosis in patients with unresectable pancreatic ductal adenocarcinoma. Cancer Epidemiol. Biomarkers Prev. 21, 1135–1142.10.1158/1055-9965.EPI-11-1079Suche in Google Scholar PubMed

Inoue, Y., Yokobori, T., Yokoe, T., Toiyama, Y., Miki, C., Mimori, K., Mori, M., and Kusunoki, M. (2010). Clinical significance of human kallikrein7 gene expression in colorectal cancer. Ann. Surg. Oncol. 17, 3037–3042.10.1245/s10434-010-1132-ySuche in Google Scholar PubMed

Jiao, X., Lu, H.J., Zhai, M.M., Tan, Z.J., Zhi, H.N., Liu, X.M., Liu, C.H., and Zhang, D.P. (2013). Overexpression of kallikrein gene 10 is a biomarker for predicting poor prognosis in gastric cancer. World J. Gastroenterol. 19, 9425–9431.10.3748/wjg.v19.i48.9425Suche in Google Scholar PubMed PubMed Central

Johnson, S.K., Ramani, V.C., Hennings, L., and Haun, R.S. (2007). Kallikrein 7 enhances pancreatic cancer cell invasion by shedding E-cadherin. Cancer 109, 1811–1820.10.1002/cncr.22606Suche in Google Scholar PubMed

Kerimis, D., Kontos, C.K., Christodoulou, S., Papadopoulos, I.N., and Scorilas, A. (2017). Elevated expression of miR-24-3p is a potentially adverse prognostic factor in colorectal adenocarcinoma. Clin. Biochem. 50, 285–292.10.1016/j.clinbiochem.2016.11.034Suche in Google Scholar PubMed

Kim, J.J., Kim, J.T., Yoon, H.R., Kang, M.A., Kim, J.H., Lee, Y.H., Kim, J.W., Lee, S.J., Song, E.Y., Myung, P.K., et al. (2012). Upregulation and secretion of kallikrein-related peptidase 6 (KLK6) in gastric cancer. Tumour Biol. 33, 731–738.10.1007/s13277-011-0267-1Suche 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-2014-0143Suche in Google Scholar PubMed

Konstantoudakis, G., Florou, D., Mavridis, K., Papadopoulos, I.N., and Scorilas, A. (2010). Kallikrein-related peptidase 13 (KLK13) gene expressional status contributes significantly in the prognosis of primary gastric carcinomas. Clin. Biochem. 43, 1205–1211.10.1016/j.clinbiochem.2010.07.016Suche in Google Scholar PubMed

Kontos, C.K. and Scorilas, A. (2012a). Kallikrein-related peptidases (KLKs): a gene family of novel cancer biomarkers. Clin. Chem. Lab. Med. 50, 1877–1891.10.1515/cclm-2012-0247Suche in Google Scholar PubMed

Kontos, C.K. and Scorilas, A. (2012b). Molecular cloning of novel alternatively spliced variants of BCL2L12, a new member of the BCL2 gene family, and their expression analysis in cancer cells. Gene 505, 153–166.10.1016/j.gene.2012.04.084Suche in Google Scholar PubMed

Kontos, C.K., Papadopoulos, I.N., and Scorilas, A. (2008). Quantitative expression analysis and prognostic significance of the novel apoptosis-related gene BCL2L12 in colon cancer. Biol. Chem. 389, 1467–1475.10.1515/BC.2008.173Suche in Google Scholar PubMed

Kontos, C.K., Papadopoulos, I.N., Fragoulis, E.G., and Scorilas, A. (2010). Quantitative expression analysis and prognostic significance of L-DOPA decarboxylase in colorectal adenocarcinoma. Br. J. Cancer 102, 1384–1390.10.1038/sj.bjc.6605654Suche in Google Scholar PubMed PubMed Central

Kontos, C.K., Chantzis, D., Papadopoulos, I.N., and Scorilas, A. (2013a). Kallikrein-related peptidase 4 (KLK4) mRNA predicts short-term relapse in colorectal adenocarcinoma patients. Cancer Lett. 330, 106–112.10.1016/j.canlet.2012.11.036Suche in Google Scholar PubMed

Kontos, C.K., Mavridis, K., Talieri, M., and Scorilas, A. (2013b). Kallikrein-related peptidases (KLKs) in gastrointestinal cancer: mechanistic and clinical aspects. Thromb. Haemost. 110, 450–457.10.1160/TH12-11-0791Suche in Google Scholar

Kontos, C.K., Christodoulou, M.I., and Scorilas, A. (2014). Apoptosis-related BCL2-family members: key players in chemotherapy. Anticancer Agents Med. Chem. 14, 353–374.10.2174/18715206113139990091Suche in Google Scholar

Kontos, C.K., Adamopoulos, P.G., Papageorgiou, S.G., Pappa, V., and Scorilas, A. (2016). mRNA overexpression of kallikrein-related peptidase 14 (KLK14) is an independent predictor of poor overall survival in chronic lymphocytic leukemia patients. Clin. Chem. Lab. Med. 54, 315–324.10.1515/cclm-2015-0456Suche in Google Scholar

Kontos, C.K., Tsiakanikas, P., Avgeris, M., Papadopoulos, I.N., and Scorilas, A. (2017). miR-15a-5p, a novel prognostic biomarker, predicting recurrent colorectal adenocarcinoma. Mol. Diagn. Ther. 21, 453–464.10.1007/s40291-017-0270-3Suche in Google Scholar

Kosaka, N., Iguchi, H., and Ochiya, T. (2010). Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 101, 2087–2092.10.1111/j.1349-7006.2010.01650.xSuche in Google Scholar

Kurlender, L., Borgono, C., Michael, I.P., Obiezu, C., Elliott, M.B., Yousef, G.M., and Diamandis, E.P. (2005). A survey of alternative transcripts of human tissue kallikrein genes. Biochim. Biophys. Acta 1755, 1–14.10.1016/j.bbcan.2005.02.001Suche in Google Scholar

Li, X.S. and He, X.L. (2016). Kallikrein 12 downregulation reduces AGS gastric cancer cell proliferation and migration. Genet Mol Res. 15, doi: 10.4238/gmr.15038452.10.4238/gmr.15038452Suche in Google Scholar

Li, D., Mallory, T., and Satomura, S. (2001). AFP-L3: a new generation of tumor marker for hepatocellular carcinoma. Clin. Chim. Acta 313, 15–19.10.1016/S0009-8981(01)00644-1Suche in Google Scholar

Li, L., Xu, N., Fan, N., Meng, Q., Luo, W., Lv, L., Ma, W., Liu, X., Liu, L., Xu, F., et al. (2015). Upregulated KLK10 inhibits esophageal cancer proliferation and enhances cisplatin sensitivity in vitro. Oncol. Rep. 34, 2325–2332.10.3892/or.2015.4211Suche in Google Scholar PubMed

Liang, S., He, L., Zhao, X., Miao, Y., Gu, Y., Guo, C., Xue, Z., Dou, W., Hu, F., Wu, K., et al. (2011). MicroRNA let-7f inhibits tumor invasion and metastasis by targeting MYH9 in human gastric cancer. PLoS One 6, e18409.10.1371/journal.pone.0018409Suche in Google Scholar PubMed PubMed Central

Liu, X., Xiong, H., Li, J., He, Y., and Yuan, X. (2013). Correlation of hK6 expression with tumor recurrence and prognosis in advanced gastric cancer. Diagn. Pathol. 8, 62.10.1186/1746-1596-8-62Suche in Google Scholar PubMed PubMed Central

Liu, X., Quan, B., Tian, Z., Xi, H., Jia, G., Wang, H., Zhang, L., Liu, R., Ma, C., Han, F., et al. (2017). Elevated expression of KLK8 predicts poor prognosis in colorectal cancer. Biomed. Pharmacother. 88, 595–602.10.1016/j.biopha.2017.01.112Suche in Google Scholar PubMed

Lok, A.S., Sterling, R.K., Everhart, J.E., Wright, E.C., Hoefs, J.C., Di Bisceglie, A.M., Morgan, T.R., Kim, H.Y., Lee, W.M., Bonkovsky, H.L., et al. (2010). Des-gamma-carboxy prothrombin and α-fetoprotein as biomarkers for the early detection of hepatocellular carcinoma. Gastroenterology 138, 493–502.10.1053/j.gastro.2009.10.031Suche in Google Scholar PubMed PubMed Central

Lu, C.Y., Hsieh, S.Y., Lu, Y.J., Wu, C.S., Chen, L.C., Lo, S.J., Wu, C.T., Chou, M.Y., Huang, T.H., and Chang, Y.S. (2009). Aberrant DNA methylation profile and frequent methylation of KLK10 and OXGR1 genes in hepatocellular carcinoma. Genes Chromosomes Cancer 48, 1057–1068.10.1002/gcc.20708Suche in Google Scholar PubMed

Lu, L., Yang, Z., Zhu, B., Fang, S., Yang, X., Cai, W., Li, C., Ma, J.X., and Gao, G. (2007). Kallikrein-binding protein suppresses growth of hepatocellular carcinoma by anti-angiogenic activity. Cancer Lett. 257, 97–106.10.1016/j.canlet.2007.07.008Suche in Google Scholar PubMed

Matsushima, K., Isomoto, H., Inoue, N., Nakayama, T., Hayashi, T., Nakayama, M., Nakao, K., Hirayama, T., and Kohno, S. (2011). MicroRNA signatures in Helicobacter pylori-infected gastric mucosa. Int. J. Cancer 128, 361–370.10.1002/ijc.25348Suche in Google Scholar PubMed

Mavridis, K., Avgeris, M., and Scorilas, A. (2014). Targeting kallikrein-related peptidases in prostate cancer. Expert Opin. Ther. Targets 18, 365–383.10.1517/14728222.2014.880693Suche in Google Scholar PubMed

Nagahara, H., Mimori, K., Utsunomiya, T., Barnard, G.F., Ohira, M., Hirakawa, K., and Mori, M. (2005). Clinicopathologic and biological significance of kallikrein 6 overexpression in human gastric cancer. Clin. Cancer Res. 11, 6800–6806.10.1158/1078-0432.CCR-05-0943Suche in Google Scholar PubMed

Navaneethan, U., Lourdusamy, V., Gk Venkatesh, P., Willard, B., Sanaka, M.R., and Parsi, M.A. (2015). Bile proteomics for differentiation of malignant from benign biliary strictures: a pilot study. Gastroenterol. Rep. (Oxf) 3, 136–143.10.1093/gastro/gou066Suche in Google Scholar PubMed PubMed Central

Ni, X.G., Bai, X.F., Mao, Y.L., Shao, Y.F., Wu, J.X., Shan, Y., Wang, C.F., Wang, J., Tian, Y.T., Liu, Q., et al. (2005). The clinical value of serum CEA, CA19-9, and CA242 in the diagnosis and prognosis of pancreatic cancer. Eur. J. Surg. Oncol. 31, 164–169.10.1016/j.ejso.2004.09.007Suche in Google Scholar PubMed

Ogawa, K., Utsunomiya, T., Mimori, K., Tanaka, F., Inoue, H., Nagahara, H., Murayama, S., and Mori, M. (2005). Clinical significance of human kallikrein gene 6 messenger RNA expression in colorectal cancer. Clin. Cancer Res. 11, 2889–2893.10.1158/1078-0432.CCR-04-2281Suche in Google Scholar PubMed

Pasic, M.D., Olkhov, E., Bapat, B., and Yousef, G.M. (2012). Epigenetic regulation of kallikrein-related peptidases: there is a whole new world out there. Biol. Chem. 393, 319–330.10.1515/hsz-2011-0273Suche in Google Scholar PubMed

Patsis, C., Yiotakis, I., and Scorilas, A. (2012). Diagnostic and prognostic significance of human kallikrein 11 (KLK11) mRNA expression levels in patients with laryngeal cancer. Clin. Biochem. 45, 623–630.10.1016/j.clinbiochem.2012.03.005Suche in Google Scholar PubMed

Pectasides, D., Mylonakis, A., Kostopoulou, M., Papadopoulou, M., Triantafillis, D., Varthalitis, J., Dimitriades, M., and Athanassiou, A. (1997). CEA, CA 19-9, and CA-50 in monitoring gastric carcinoma. Am. J. Clin. Oncol. 20, 348–353.10.1097/00000421-199708000-00005Suche in Google Scholar PubMed

Petraki, C., Dubinski, W., Scorilas, A., Saleh, C., Pasic, M.D., Komborozos, V., Khalil, B., Gabril, M.Y., Streutker, C., Diamandis, E.P., et al. (2012a). Evaluation and prognostic significance of human tissue kallikrein-related peptidase 6 (KLK6) in colorectal cancer. Pathol. Res. Pract. 208, 104–108.10.1016/j.prp.2011.12.010Suche in Google Scholar PubMed

Petraki, C., Youssef, Y.M., Dubinski, W., Lichner, Z., Scorilas, A., Pasic, M.D., Komborozos, V., Khalil, B., Streutker, C., Diamandis, E.P., et al. (2012b). Evaluation and prognostic significance of human tissue kallikrein-related peptidase 10 (KLK10) in colorectal cancer. Tumour Biol. 33, 1209–1214.10.1007/s13277-012-0368-5Suche in Google Scholar PubMed

Ramani, V.C. and Haun, R.S. (2008a). Expression of kallikrein 7 diminishes pancreatic cancer cell adhesion to vitronectin and enhances urokinase-type plasminogen activator receptor shedding. Pancreas 37, 399–404.10.1097/MPA.0b013e31817f76f7Suche in Google Scholar PubMed

Ramani, V.C. and Haun, R.S. (2008b). The extracellular matrix protein fibronectin is a substrate for kallikrein 7. Biochem. Biophys. Res. Commun. 369, 1169–1173.10.1016/j.bbrc.2008.03.021Suche in Google Scholar PubMed

Ramani, V.C., Hennings, L., and Haun, R.S. (2008). Desmoglein 2 is a substrate of kallikrein 7 in pancreatic cancer. BMC Cancer 8, 373.10.1186/1471-2407-8-373Suche in Google Scholar PubMed PubMed Central

Ramani, V.C., Kaushal, G.P., and Haun, R.S. (2011). Proteolytic action of kallikrein-related peptidase 7 produces unique active matrix metalloproteinase-9 lacking the C-terminal hemopexin domains. Biochim. Biophys. Acta 1813, 1525–1531.10.1016/j.bbamcr.2011.05.007Suche in Google Scholar PubMed PubMed Central

Rapti, S.M., Kontos, C.K., Papadopoulos, I.N., and Scorilas, A. (2014). Enhanced miR-182 transcription is a predictor of poor overall survival in colorectal adenocarcinoma patients. Clin. Chem. Lab. Med. 52, 1217–1227.10.1515/cclm-2013-0950Suche in Google Scholar

Rapti, S.M., Kontos, C.K., Papadopoulos, I.N., and Scorilas, A. (2016). High miR-96 levels in colorectal adenocarcinoma predict poor prognosis, particularly in patients without distant metastasis at the time of initial diagnosis. Tumour Biol. 37, 11815–11824.10.1007/s13277-016-5023-0Suche in Google Scholar

Rapti, S.M., Kontos, C.K., Christodoulou, S., Papadopoulos, I.N., and Scorilas, A. (2017). miR-34a overexpression predicts poor prognostic outcome in colorectal adenocarcinoma, independently of clinicopathological factors with established prognostic value. Clin. Biochem. 50, 918–924.10.1016/j.clinbiochem.2017.06.004Suche in Google Scholar

Reddy, S., Cameron, J.L., Scudiere, J., Hruban, R.H., Fishman, E.K., Ahuja, N., Pawlik, T.M., Edil, B.H., Schulick, R.D., and Wolfgang, C.L. (2009). Surgical management of solid-pseudopapillary neoplasms of the pancreas (Franz or Hamoudi tumors): a large single-institutional series. J. Am. Coll. Surg. 208, 950–957; discussion 957–959.10.1016/j.jamcollsurg.2009.01.044Suche in Google Scholar

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.6604717Suche in Google Scholar

Salmena, L., Poliseno, L., Tay, Y., Kats, L., and Pandolfi, P.P. (2011). A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146, 353–358.10.1016/j.cell.2011.07.014Suche in Google Scholar

Samaan, S., Lichner, Z., Ding, Q., Saleh, C., Samuel, J., Streutker, C., and Yousef, G.M. (2014). Kallikreins are involved in an miRNA network that contributes to prostate cancer progression. Biol. Chem. 395, 991–1001.10.1515/hsz-2013-0288Suche in Google Scholar

Sawant, S., Snyman, C., and Bhoola, K. (2001). Comparison of tissue kallikrein and kinin receptor expression in gastric ulcers and neoplasms. Int. Immunopharmacol. 1, 2063–2080.10.1016/S1567-5769(01)00118-7Suche in Google Scholar

Sells, E., Pandey, R., Chen, H., Skovan, B.A., Cui, H., and Ignatenko, N.A. (2017). Specific microRNA-mRNA regulatory network of colon cancer invasion mediated by tissue kallikrein-related peptidase 6. Neoplasia 19, 396–411.10.1016/j.neo.2017.02.003Suche in Google Scholar PubMed PubMed Central

Shaw, J.L. and Diamandis, E.P. (2007). Distribution of 15 human kallikreins in tissues and biological fluids. Clin. Chem. 53, 1423–1432.10.1373/clinchem.2007.088104Suche in Google Scholar PubMed

Shi, T., Gao, G., and Cao, Y. (2016). Long noncoding RNAs as novel biomarkers have a promising future in cancer diagnostics. Dis. Markers. 2016, 9085195.10.1155/2016/9085195Suche in Google Scholar

Sidiropoulos, K.G., White, N.M., Bui, A., Ding, Q., Boulos, P., Pampalakis, G., Khella, H., Samuel, J.N., Sotiropoulou, G., and Yousef, G.M. (2014). Kallikrein-related peptidase 5 induces miRNA-mediated anti-oncogenic pathways in breast cancer. Oncoscience 1, 709–724.10.18632/oncoscience.91Suche in Google Scholar

Sidiropoulos, K.G., Ding, Q., Pampalakis, G., White, N.M., Boulos, P., Sotiropoulou, G., and Yousef, G.M. (2016). KLK6-regulated miRNA networks activate oncogenic pathways in breast cancer subtypes. Mol. Oncol. 10, 993–1007.10.1016/j.molonc.2016.03.008Suche in Google Scholar

Sugimura, K., Miyata, H., Tanaka, K., Hamano, R., Takahashi, T., Kurokawa, Y., Yamasaki, M., Nakajima, K., Takiguchi, S., Mori, M., et al. (2012). Let-7 expression is a significant determinant of response to chemotherapy through the regulation of IL-6/STAT3 pathway in esophageal squamous cell carcinoma. Clin. Cancer Res. 18, 5144–5153.10.1158/1078-0432.CCR-12-0701Suche in Google Scholar

Sun, Y., Gao, G., Cai, J., Wang, Y., Qu, X., He, L., Liu, F., Zhang, Y., Lin, K., Ma, S., et al. (2013). Annexin A2 is a discriminative serological candidate in early hepatocellular carcinoma. Carcinogenesis 34, 595–604.10.1093/carcin/bgs372Suche in Google Scholar

Talieri, M., Li, L., Zheng, Y., Alexopoulou, D.K., Soosaipillai, A., Scorilas, A., Xynopoulos, D., and Diamandis, E.P. (2009a). The use of kallikrein-related peptidases as adjuvant prognostic markers in colorectal cancer. Br. J. Cancer 100, 1659–1665.10.1038/sj.bjc.6605033Suche in Google Scholar

Talieri, M., Mathioudaki, K., Prezas, P., Alexopoulou, D.K., Diamandis, E.P., Xynopoulos, D., Ardavanis, A., Arnogiannaki, N., and Scorilas, A. (2009b). Clinical significance of kallikrein-related peptidase 7 (KLK7) in colorectal cancer. Thromb. Haemost. 101, 741–747.10.1160/TH08-07-0471Suche in Google Scholar

Talieri, M., Alexopoulou, D.K., Scorilas, A., Kypraios, D., Arnogiannaki, N., Devetzi, M., Patsavela, M., and Xynopoulos, D. (2011). Expression analysis and clinical evaluation of kallikrein-related peptidase 10 (KLK10) in colorectal cancer. Tumour Biol. 32, 737–744.10.1007/s13277-011-0175-4Suche in Google Scholar

Tokas, T., Avgeris, M., Alamanis, C., Scorilas, A., Stravodimos, K.G., and Constantinides, C.A. (2017). Downregulated KLK13 expression in bladder cancer highlights tumor aggressiveness and unfavorable patients’ prognosis. J. Cancer. Res. Clin. Oncol. 143, 521–532.10.1007/s00432-016-2301-6Suche in Google Scholar

Trevisani, F., D’Intino, P.E., Morselli-Labate, A.M., Mazzella, G., Accogli, E., Caraceni, P., Domenicali, M., De Notariis, S., Roda, E., and Bernardi, M. (2001). Serum alpha-fetoprotein for diagnosis of hepatocellular carcinoma in patients with chronic liver disease: influence of HBsAg and anti-HCV status. J. Hepatol. 34, 570–575.10.1016/S0168-8278(00)00053-2Suche in Google Scholar

Tsiakanikas, P., Kontos, C.K., Kerimis, D., Papadopoulos, I.N., and A., S. (2018). High microRNA-28-5p expression in colorectal adenocarcinoma predicts short-term relapse of node-negative patients and poor overall survival of patients with non-metastatic disease. Clin. Chem. Lab. Med. 56, 990–1000.10.1515/cclm-2017-0430Suche in Google Scholar PubMed

Unal, D., Tasdemir, A., Oguz, A., Eroglu, C., Cihan, Y.B., Turak, E.E., Karaman, H., and Soyuer, S. (2013). Is human kallikrein-11 in gastric cancer treated with surgery and adjuvant chemoradiotherapy associated with survival? Pathol. Res. Pract. 209, 779–783.10.1016/j.prp.2013.09.004Suche in Google Scholar PubMed

Wang, B., Shen, Z.L., Jiang, K.W., Zhao, G., Wang, C.Y., Yan, Y.C., Yang, Y., Zhang, J.Z., Shen, C., Gao, Z.D., et al. (2015). MicroRNA-217 functions as a prognosis predictor and inhibits colorectal cancer cell proliferation and invasion via an AEG-1 dependent mechanism. BMC Cancer 15, 437.10.1186/s12885-015-1438-zSuche in Google Scholar PubMed PubMed Central

Wen, Y.G., Wang, Q., Zhou, C.Z., Yan, D.W., Qiu, G.Q., Yang, C., Tang, H.M., and Peng, Z.H. (2011). Identification and validation of Kallikrein-ralated peptidase 11 as a novel prognostic marker of gastric cancer based on immunohistochemistry. J. Surg. Oncol. 104, 516–524.10.1002/jso.21981Suche in Google Scholar PubMed

White, N.M., Bui, A., Mejia-Guerrero, S., Chao, J., Soosaipillai, A., Youssef, Y., Mankaruos, M., Honey, R.J., Stewart, R., Pace, K.T., et al. (2010a). Dysregulation of kallikrein-related peptidases in renal cell carcinoma: potential targets of miRNAs. Biol. Chem. 391, 411–423.10.1515/bc.2010.041Suche in Google Scholar PubMed

White, N.M., Chow, T.F., Mejia-Guerrero, S., Diamandis, M., Rofael, Y., Faragalla, H., Mankaruous, M., Gabril, M., Girgis, A., and Yousef, G.M. (2010b). Three dysregulated miRNAs control kallikrein 10 expression and cell proliferation in ovarian cancer. Br. J. Cancer 102, 1244–1253.10.1038/sj.bjc.6605634Suche in Google Scholar PubMed PubMed Central

White, N.M., Youssef, Y.M., Fendler, A., Stephan, C., Jung, K., and Yousef, G.M. (2012). The miRNA-kallikrein axis of interaction: a new dimension in the pathogenesis of prostate cancer. Biol. Chem. 393, 379–389.10.1515/hsz-2011-0246Suche in Google Scholar PubMed

Wu, Y., Chen, Y., Li, Q., Gong, Y., Liu, X., Bi, L., and Hu, C. (2016). Upregulation of kallikreinrelated peptidase 5 is associated with the malignant behavior of colorectal cancer. Mol. Med. Rep. 14, 2164–2170.10.3892/mmr.2016.5516Suche in Google Scholar PubMed

Xi, S., Inchauste, S., Guo, H., Shan, J., Xiao, Z., Xu, H., Miettenen, M., Zhang, M.R., Hong, J.A., Raiji, M.T., et al. (2015). Cigarette smoke mediates epigenetic repression of miR-217 during esophageal adenocarcinogenesis. Oncogene 34, 5548–5559.10.1038/onc.2015.10Suche in Google Scholar PubMed PubMed Central

Yousef, G.M., Chang, A., Scorilas, A., and Diamandis, E.P. (2000). Genomic organization of the human kallikrein gene family on chromosome 19q13.3-q13.4. Biochem. Biophys. Res. Commun. 276, 125–133.10.1006/bbrc.2000.3448Suche in Google Scholar PubMed

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

Yousef, G.M., Borgono, C.A., White, N.M., Robb, J.D., Michael, I.P., Oikonomopoulou, K., Khan, S., and Diamandis, E.P. (2004b). In silico analysis of the human kallikrein gene 6. Tumour Biol. 25, 282–289.10.1159/000081393Suche in Google Scholar PubMed

Yousef, G.M., White, N.M., Michael, I.P., Cho, J.C., Robb, J.D., Kurlender, L., Khan, S., and Diamandis, E.P. (2005). Identification of new splice variants and differential expression of the human kallikrein 10 gene, a candidate cancer biomarker. Tumour Biol. 26, 227–235.10.1159/000087377Suche in Google Scholar PubMed

Zhang, M., Li, M., Li, N., Zhang, Z., Liu, N., Han, X., Liu, Q., and Liao, C. (2017). miR-217 suppresses proliferation, migration, and invasion promoting apoptosis via targeting MTDH in hepatocellular carcinoma. Oncol. Rep. 37, 1772–1778.10.3892/or.2017.5401Suche in Google Scholar PubMed

Zhao, E.H., Shen, Z.Y., Liu, H., Jin, X., and Cao, H. (2012). Clinical significance of human kallikrein 12 gene expression in gastric cancer. World J. Gastroenterol. 18, 6597–6604.10.3748/wjg.v18.i45.6597Suche in Google Scholar PubMed PubMed Central

Zhu, B., Lu, L., Cai, W., Yang, X., Li, C., Yang, Z., Zhan, W., Ma, J.X., and Gao, G. (2007). Kallikrein-binding protein inhibits growth of gastric carcinoma by reducing vascular endothelial growth factor production and angiogenesis. Mol. Cancer Ther. 6, 3297–3306.10.1158/1535-7163.MCT-06-0798Suche in Google Scholar PubMed

Received: 2017-12-30
Accepted: 2018-04-17
Published Online: 2018-06-07
Published in Print: 2018-07-26

©2018 Walter de Gruyter GmbH, Berlin/Boston

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