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Kallikrein-related peptidases in lung diseases

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Published/Copyright: March 31, 2018

Abstract

Human tissue kallikreins (KLKs) are 15 members of the serine protease family and are present in various healthy human tissues including airway tissues. Multiple studies have revealed their crucial role in the pathophysiology of a number of chronic, infectious and tumour lung diseases. KLK1, 3 and 14 are involved in asthma pathogenesis, and KLK1 could be also associated with the exacerbation of this inflammatory disease caused by rhinovirus. KLK5 was demonstrated as an influenza virus activating protease in humans, and KLK1 and 12 could also be involved in the activation and spread of these viruses. KLKs are associated with lung cancer, with up- or downregulation of expression depending on the KLK, cancer subtype, stage of tumour and also the microenvironment. Functional studies showed that KLK12 is a potent pro-angiogenic factor. Moreover, KLK6 promotes malignant-cell proliferation and KLK13 invasiveness. In contrast, KLK8 and KLK10 reduce proliferation and invasion of malignant cells. Considering the involvement of KLKs in various physiological and pathological processes, KLKs appear to be potential biomarkers and therapeutic targets for lung diseases.

Acknowledgements

We particularly thank Laura Smales for editing the English text. Studies conducted by our team were supported by the ‘Ligue Contre le Cancer’ and we especially thank the Departmental committees of Indre et Loire, Morbihan, Maine et Loire, Deux-Sèvres, Indre, and Cher.

References

Abraham, W.M., Scuri, M., and Farmer, S.G. (2006). Peptide and non-peptide bradykinin receptor antagonists: role in allergic airway disease. Eur. J. Pharmacol. 533, 215–221.10.1016/j.ejphar.2005.12.071Search in Google Scholar PubMed

Aubier, M., Thabut, G., Hamidi, F., Guillou, N., Brard, J., Dombret, M.C., Borensztajn, K., Aitilaine, B., Poirier, I., Roland-Nicaise, P., et al. (2016). Airway smooth muscle enlargement is associated with protease-activated receptor 2/ligand overexpression in patients with difficult-to-control severe asthma. J. Allergy Clin. Immunol. 138, 729–739.10.1016/j.jaci.2015.12.1332Search 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, 801–818.10.1517/14728222.2016.1147560Search in Google Scholar PubMed

Bagdonas, E., Raudoniute, J., Bruzauskaite, I., and Aldonyte, R. (2015). Novel aspects of pathogenesis and regeneration mechanisms in COPD. Int. J. Chron. Obstruct. Pulmon. Dis. 10, 995–1013.10.2147/COPD.S82518Search in Google Scholar PubMed PubMed Central

Banville, N., Burgess, J.K., Jaffar, J., Tjin, G., Richeldi, L., Cerri, S., Persiani, E., Black, J.L., and Oliver, B.G. (2014). A quantitative proteomic approach to identify significantly altered protein networks in the serum of patients with lymphangioleiomyomatosis (LAM). PLoS One 9, e105365.10.1371/journal.pone.0105365Search in Google Scholar PubMed PubMed Central

Beaulieu, A., Gravel, É., Cloutier, A., Marois, I., Colombo, É., Désilets, A., Verreault, C., Leduc, R., Marsault, É., and Richter, M.V. (2013). Matriptase proteolytically activates influenza virus and promotes multicycle replication in the human airway epithelium. J. Virol. 87, 4237–4251.10.1128/JVI.03005-12Search in Google Scholar PubMed PubMed Central

Bertram, S., Glowacka, I., Blazejewska, P., Soilleux, E., Allen, P., Danisch, S., Steffen, I., Choi, S.Y., Park, Y., Schneider, H., et al. (2010). TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J. Virol. 84, 10016–10025.10.1128/JVI.00239-10Search in Google Scholar PubMed PubMed Central

Bhattacharjee, A., Richards, W.G., Staunton, J., Li, C., Monti, S., Vasa, P., Ladd, C., Beheshti, J., Bueno, R., Gillette, M., et al. (2001). Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc. Natl. Acad. Sci. USA 98, 13790–13795.10.1073/pnas.191502998Search in Google Scholar PubMed PubMed Central

Böttcher, E., Matrosovich, T., Beyerle, M., Klenk, H.D., Garten, W., and Matrosovich, M. (2006). Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J. Virol. 80, 9896–9898.10.1128/JVI.01118-06Search in Google Scholar PubMed PubMed Central

Broadley, K.J., Blair, A.E., Kidd, E.J., Bugert, J.J., and Ford, W.R. (2010). Bradykinin-induced lung inflammation and bronchoconstriction: role in parainfluenze-3 virus-induced inflammation and airway hyperreactivity. J. Pharmacol. Exp. Ther. 335, 681–692.10.1124/jpet.110.171876Search in Google Scholar PubMed

Casalino-Matsuda, S.M., Monzon, M.E., Conner, G.E., Salathe, M., and Forteza, R.M. (2004). Role of hyaluronan and reactive oxygen species in tissue kallikrein-mediated epidermal growth factor receptor activation in human airways. J. Biol. Chem. 279, 21606–21616.10.1074/jbc.M309950200Search in Google Scholar PubMed

Casalino-Matsuda, S.M., Monzón, M.E., and Forteza, R.M. (2006). Epidermal growth factor receptor activation by epidermal growth factor mediates oxidant-induced goblet cell metaplasia in human airway epithelium. Am. J. Respir. Cell. Mol. Biol. 34, 581–591.10.1165/rcmb.2005-0386OCSearch in Google Scholar PubMed PubMed Central

Castillo, J.R., Peters, S.P., and Busse, W.W. (2017). Asthma exacerbations: pathogenesis, prevention, and treatment. J. Allergy Clin. Immunol. Pract. 5, 918–927.10.1016/j.jaip.2017.05.001Search in Google Scholar PubMed PubMed Central

Chee, J., Singh, J., Naran, A., Misso, N.L., Thompson, P.J., and Bhoola, K.D. (2007). Novel expression of kallikreins, kallikrein-related peptidases and kinin receptors in human pleural mesothelioma. Biol. Chem. 388, 1235–1242.10.1515/BC.2007.139Search in Google Scholar PubMed

Chee, J., Naran, A., Misso, N.L., Thompson, P.J., and Bhoola, K.D. (2008). Expression of tissue and plasma kallikreins and kinin B1 and B2 receptors in lung cancer. Biol. Chem. 389, 1225–1233.10.1515/BC.2008.139Search in Google Scholar PubMed

Chou, R.H., Lin, S.C., Wen, H.C., Wu, C.W., and Chang, W.S. (2011). Epigenetic activation of human kallikrein 13 enhances malignancy of lung adenocarcinoma by promoting N-cadherin expression and laminin degradation. Biochem. Biophys. Res. Commun. 409, 442–447.10.1016/j.bbrc.2011.05.022Search in Google Scholar PubMed

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.2008.071Search in Google Scholar PubMed

Christiansen, S.C., Proud, D., Sarnoff, R.B., Juergens, U., Cochrane, C.G., and Zuraw, B.L. (1992). Elevation of tissue kallikrein and kinin in the airways of asthmatic subjects after endobronchial allergen challenge. Am. Rev. Respir. Dis 145, 900–905.10.1164/ajrccm/145.4_Pt_1.900Search in Google Scholar PubMed

Christiansen, S.C., Eddleston, J., Bengtson, S.H., Jenkins, G.R., Sarnoff, R.B., Turner, R.B., Gwaltney, J.M., and Zuraw, B.L. (2008). Experimental rhinovirus infection increases human tissue kallikrein activation in allergic subjects. Int. Arch. Allergy Immunol. 147, 299–304.10.1159/000144037Search in Google Scholar PubMed

Chung, H., Hamza, M., Oikonomopoulou, K., Gratio, V., Saifeddine, M., Virca, G.D., Diamandis, E.P., Hollenberg, M.D., and Darmoul, D. (2012). Kallikrein-related peptidase signaling in colon carcinoma cells: targeting proteinase-activated receptors. Biol. Chem. 393, 413–420.10.1515/bc-2011-231Search in Google Scholar PubMed

Diamandis, E.P., Goodglick, L., Planque, C., and Thornquist, M.D. (2011). Pentraxin-3 is a novel biomarker of lung carcinoma. Clin. Cancer Res. 17, 2395–2399.10.1158/1078-0432.CCR-10-3024Search in Google Scholar

Evans, D.M., Jones, D.M., Pitt, G.R., Ashworth, D., De Clerck, F., Verheyen, F., and Szelke, M. (1996). Synthetic inhibitors of human tissue kallikrein. Immunopharmacology 32, 117–118.10.1016/0162-3109(95)00069-0Search in Google Scholar

Evans, C.M., Raclawska, D.S., Ttofali, F., Liptzin, D.R., Fletcher, A.A., Harper, D.N., McGing, M.A., McElwee, M.M., Williams, O.W., Sanchez, E., et al. (2015). The polymeric mucin Muc5ac is required for allergic airway hyperreactivity. Nat. Commun. 6, 6281–6306.10.1038/ncomms7281Search in Google Scholar PubMed PubMed Central

Forteza, R., Lauredo, I., Abraham, W.M., and Conner, G.E. (1999). Bronchial tissue kallikrein activity is regulated by hyaluronic acid binding. Am. J. Respir. Cell. Mol. Biol. 21, 666–674.10.1165/ajrcmb.21.6.3651Search in Google Scholar PubMed

Forteza, R., Conner, G.E., and Salathe, M. (2004). Hyaluronan in the airways. In: Chemistry and Biology of Hyaluronan, Lung Biology in Health and Disease, H.G. Garg, and C.A. Hales, eds. (Oxford, UK: Elsevier), pp. 323–337.10.1016/B978-008044382-9/50046-7Search in Google Scholar

Gao, L., Chao, L., and Chao, J. (2010). A novel signaling pathway of tissue kallikrein in promoting keratinocyte migration: activation of proteinase-activated receptor 1 and epidermal growth factor receptor. Exp. Cell. Res. 316, 376–389.10.1016/j.yexcr.2009.10.022Search in Google Scholar PubMed PubMed Central

Goettig, P., Magdolen, V., and Brandstetter, H. (2010). Natural and synthetic inhibitors of kallikrein-related peptidases (KLKs). Biochimie 92, 1546–1567.10.1016/j.biochi.2010.06.022Search in Google Scholar PubMed PubMed Central

Gueugnon, F., Barascu, A., Mavridis, K., Petit-Courty, A., Marchand-Adam, S., Gissot, V., Scorilas, A., Guyetant, S., and Courty, Y. (2015). Kallikrein-related peptidase 13: an independent indicator of favorable prognosis for patients with nonsmall cell lung cancer. Tumour Biol. 36, 4979–4986.10.1007/s13277-015-3148-1Search in Google Scholar PubMed

Guillon-Munos, A., Oikonomopoulou, K., Michel, N., Smith, C.R., Petit-Courty, A., Canepa, S., Reverdiau, P., Heuzé-Vourc’h, N., Diamandis, E.P., and Courty, Y. (2011). Kallikrein-related peptidase 12 hydrolyzes matricellular proteins of the CCN family and modifies interactions of CCN1 and CCN5 with growth factors. J. Biol. Chem. 286, 25505–25518.10.1074/jbc.M110.213231Search in Google Scholar PubMed PubMed Central

Hamilton, B.S. and Whittaker, G.R. (2013). Cleavage activation of human-adapted influenza virus subtypes by kallikrein-related peptidases 5 and 12. J. Biol. Chem. 288, 17399–17407.10.1074/jbc.M112.440362Search in Google Scholar PubMed PubMed Central

Hamilton, B.S., Gludish, D.W., and Whittaker, G.R. (2012). Cleavage activation of the human-adapted influenza virus subtypes by matriptase reveals both subtype and strain specificities. J. Virol. 86, 10579–10586.10.1128/JVI.00306-12Search in Google Scholar PubMed PubMed Central

Harari, S., Torre, O., and Moss, J. (2011). Lymphangioleiomyomatosis: what do we know and what are we looking for? Eur. Respir. Rev. 20, 34–44.10.1183/09059180.00011010Search in Google Scholar PubMed PubMed Central

Hewson, C.A., Haas, J.J., Bartlett, N.W., Message, S.D., Laza-Stanca, V., Kebadze, T., Caramori, G., Zhu, J., Edbrooke, M.R., Stanciu, L.A., et al. (2010). Rhinovirus induces MUC5AC in a human infection model and in vitro via NF-κB and EGFR pathways. Eur. Respir. J. 36, 1425–1435.10.1183/09031936.00026910Search in Google Scholar PubMed

Ichinose, M. (2003). Inflamatory mechanisms in bronchial asthma and COPD. Tohoku J. Exp. Med. 200, 1–6.10.1620/tjem.200.1Search in Google Scholar PubMed

Johnson, J.J., Miller, D.L., Jiang, R., Liu, Y., Shi, Z., Tarwater, L., Williams, R., Balsara, R., Sauter, E.R., and Stack, M.S. (2016). Protease-activated receptor-2 (PAR-2)-mediated Nf-κB activation suppresses inflammation-associated tumor suppressor microRNAs in oral squamous cell carcinoma. J. Biol. Chem. 291, 6936–6945.10.1074/jbc.M115.692640Search in Google Scholar PubMed PubMed Central

Kalinska, M., Meyer-Hoffert, U., Kantyka, T., and Potempa, J. (2016). Kallikreins – the melting pot of activity and function. Biochimie 122, 270–282.10.1016/j.biochi.2015.09.023Search in Google Scholar PubMed PubMed Central

Kimes, P.K. (2014). SigFuge: single gene clustering of RNA-seq reveals differential isoform usage among cancer samples. Nucleic Acids Res. 42, 1–12.10.1093/nar/gku521Search in Google Scholar PubMed PubMed Central

Kodak, J.A., Mann, D.L., Klyushnenkova, E.N., and Alexander, R.B. (2006). Activation of innate immunity by prostate specific antigen (PSA). Prostate 66, 1592–1599.10.1002/pros.20414Search in Google Scholar PubMed

Kryza, T., Lalmanach, G., Lavergne, M., Lecaille, F., Reverdiau, P., Courty, Y., and Heuzé-Vourc’h, N. (2013). Pro-angiogenic effect of human kallikrein-related peptidase 12 (KLK12) in lung endothelial cells does not depend on kinin-mediated activation of B2 receptor. Biol. Chem. 394, 385–391.10.1515/hsz-2012-0291Search in Google Scholar PubMed

Kryza, T., Achard, C., Parent, C., Marchand-Adam, S., Guillon-Munos, A., Iochmann, S., Korkmaz, B., Respaud, R., Courty, Y., and Heuzé-Vourc’h, N. (2014). Angiogenesis stimulated by human kallikrein-related peptidase 12 acting via a platelet-derived growth factor B-dependent paracrine pathway. FASEB J. 28, 740–751.10.1096/fj.13-237503Search in Google Scholar PubMed

Kryza, T., Silva, M.L., Loessner, D., Heuzé-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

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.2005.02.001Search in Google Scholar PubMed

Lai, J., An, J., Srinivasan, S., Clements, J.A., and Batra, J. (2016). A computational analysis of the genetic and transcript diversity at the kallikrein locus. Biol. Chem. 397, 1307–1313.10.1515/hsz-2016-0161Search in Google Scholar PubMed

Lauredo, I.T., Forteza, R.M., Botvinnikova, Y., and Abraham, W.M. (2004). Leukocytic cell sources of airway tissue kallikrein. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, 734–740.10.1152/ajplung.00129.2003Search in Google Scholar PubMed PubMed Central

Lee, M.K., Hong, Y., Kim, S.Y., Kim, W.J., and London, S.J. (2017). Epigenome-wide association study of chronic obstructive pulmonary disease and lungfunction in Koreans. Epigenomics 9, 971–984.10.2217/epi-2017-0002Search in Google Scholar PubMed PubMed Central

Leu, C.H., Yang, M.L., Chung, N.H., Huang, Y.J., Su, Y.C., Chen, Y.C., Lin, C.C., Shieh, G.S., Chang, M.Y., Wang, S.W., et al. (2015). Kallistatin ameliorates influenza virus pathogenesis by inhibition of kallikrein-related peptidase 1-mediated cleavage of viral hemagglutinin. Antimicrob. Agents Chemother. 59, 5619–5630.10.1128/AAC.00065-15Search in Google Scholar PubMed PubMed Central

Liu, C.J., Liu, T.Y., Kuo, L.T., Cheng, H.W., Chu, T.H., Chang, K.W., and Lin, S.C. (2008). Differential gene expression signature between primary and metastatic head and neck squamous cell carcinoma. J. Pathol. 214, 489–497.10.1002/path.2306Search 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

Magnen, M., Gueugnon, F., Guillon, A., Baranek, T., Thibault, V.C., Petit-Courty, A., de Veer, S.J., Harris, J., Humbles, A.A., Si-Tahar, M., et al. (2017). Kallikrein-related peptidase 5 contributes to H3N2 influenza virus infection in human lungs. J. Virol. 91, e00421–17.10.1128/JVI.00421-17Search in Google Scholar PubMed PubMed Central

Masurier, N., Arama, D.P., El Amri, C., and Lisowski, V. (2018). Inhibitors of kallikrein-related peptidases: an overview. Med. Res. Rev. 38, 655–683.10.1002/med.21451Search in Google Scholar PubMed

Michel, N., Heuzé-Vourc’h, N., Lavergne, E., Parent, C., Jourdan, M.L., Vallet, A., Iochmann, S., Musso, O., Reverdiau, P., and Courty, Y. (2014). Growth and survival of lung cancer cells: regulation by kallikrein-related peptidase 6 via activation of proteinase-activated receptor 2 and the epidermal growth factor receptor. Biol. Chem. 395, 1015–1025.10.1515/hsz-2014-0124Search in Google Scholar PubMed

Minor, D.M. and Proud, D. (2017). Role of human rhinovirus in triggering human airway epithelial-mesenchymal transition. Respir. Res. 18, 1–16.10.1186/s12931-017-0595-9Search in Google Scholar PubMed PubMed Central

Mize, G.J., Wang, W., and Takayama, T.K. (2008). Prostate-specific kallikreins-2 and -4 enhance the proliferation of DU-145 prostate cancer cells through protease-activated receptors-1 and -2. Mol. Cancer Res. 6, 1043–1051.10.1158/1541-7786.MCR-08-0096Search in Google Scholar PubMed

Monzón, M.E., Manzanares, D., Schmid, N., Casalino-Matsuda, S.M., and Forteza, R.M. (2008). Hyaluronidase expression and activity is regulated by pro-inflammatory cytokines in human airway epithelial cells. Am. J. Respir. Cell. Mol. Biol. 39, 289–295.10.1165/rcmb.2007-0361OCSearch in Google Scholar PubMed PubMed Central

Myers, R.A., Himes, B.E., Gignoux, G.R., Yang, J.J., Gauderman, W.J., Rebordosa, C., Xie, J., Torgerson, D.G., Levin, A.M., Baurley, J., et al. (2012). Further replication studies of the EVE Consortium meta-analysis identifies 2 asthma risk loci in European Americans. J. Allergy Clin. Immunol. 130, 1294–1301.10.1016/j.jaci.2012.07.054Search in Google Scholar PubMed PubMed Central

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

Naveed, S.U., Clements, D., Jackson, D.J., Philp, C., Billington, C.K., Soomro, I., Reynolds, C., Harrison, T.W., Johnston, S.L., Shaw, D.E., et al. (2017). Matrix metalloproteinase-1 activation contributes to airway smooth muscle growth and asthma severity. Am. J. Respir. Crit. Care Med. 195, 1000–1009.10.1164/rccm.201604-0822OCSearch in Google Scholar PubMed PubMed Central

Neumann, G. and Kawaoka, Y. (2015). Transmission of influenza A viruses. Virology 1, 234–246.10.1016/j.virol.2015.03.009Search in Google Scholar PubMed PubMed Central

Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Tea, I., Blaber, M., Blaber, S.I., Scarisbrick, I., Andrade-Gordon, P., Cottrell, G.S., Bunnett, N.W., et al. (2006). Proteinase-activated receptors, targets for kallikrein signaling. J. Biol. Chem. 281, 32095–32112.10.1074/jbc.M513138200Search in Google Scholar PubMed

O’Riordan, T.G., Weinstein, M.D., Abraham, W.M., and Forteza, R. (2003). Elevated tissue kallikrein activity in airway secretions from patients with tracheobronchitis associated with prolonged mechanical ventilation. Lung 181, 237–244.10.1007/s00408-003-1019-9Search in Google Scholar PubMed

Ozge, C., Bozlu, M., Ozgur, E.S., Tek, M., Tunckiran, A., Muslu, N., and Ilvan, A. (2015). The impact of hypoxemia on serum total and free prostate-specific antigen levels in patients with chronic obstructive pulmonary disease. Med. Oncol. 32, 156–159.10.1007/s12032-015-0602-2Search in Google Scholar PubMed

Pais, F., Fayed, M., and Evans, T. (2017). Lymphangioleiomyomatosis: an explosive presentation of a rare disease. Oxf. Med. Case Reports 6, 92–94.10.1093/omcr/omx023Search in Google Scholar PubMed PubMed Central

Pasic, M.D., Sotiropoulou, G., and Yousef, G.M. (2015). The miRNA-kallikrein interactions: adding a new dimension. Cell Cycle 14, 691–692.10.1080/15384101.2015.1006541Search in Google Scholar PubMed PubMed Central

Petraki, C.D., Papanastasiou, P.A., Karavana, V.N., and Diamandis, E.P. (2006). Cellular distribution of human tissue kallikreins: immunohistochemical localization. Biol. Chem. 387, 653–663.10.1515/BC.2006.084Search in Google Scholar PubMed

Planque, C., de Monte, M., Guyetant, S., Rollin, J., Desmazes, C., Panel, V., Lemarié, E., and Courty, Y. (2005). KLK5 and KLK7, two members of the human tissue kallikrein family, are differentially expressed in lung cancer. Biochem. Biophys. Res. Commun. 329, 1260–1266.10.1016/j.bbrc.2005.02.100Search in Google Scholar PubMed

Planque, C., Aïnciburu, M., Heuzé-Vourc’h, N., Régina, S., de Monte, M., and Courty, Y. (2006). Expression of the human kallikrein genes 10 (KLK10) and 11 (KLK11) in cancerous and non-cancerous lung tissues. Biol. Chem. 387, 783–788.10.1515/BC.2006.098Search in Google Scholar PubMed

Planque, C., Bléchet, C., Ayadi-Kaddour, A., Heuzé-Vourc’h, N., Dumont, P., Guyétant, S., Diamandis, E.P., El Mezni, F., and Courty, Y. (2008a). Quantitative RT-PCR analysis and immunohistochemical localization of the kallikrein-related peptidases 13 and 14 in lung. Biol. Chem. 389, 781–786.10.1515/BC.2008.089Search in Google Scholar PubMed

Planque, C., Li, L., Zheng, Y., Soosaipillai, A., Reckamp, K., Chia, D., Diamandis, E.P., and Goodglick, L. (2008b). A multiparametric serum kallikrein panel for diagnosis of non-small cell lung carcinoma. Clin. Cancer Res. 14, 1355–1362.10.1158/1078-0432.CCR-07-4117Search in Google Scholar PubMed

Planque, C., Choi, Y.H., Guyetant, S., Heuzé-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

Proud, D. (1998). The kinin system in rhinitis and asthma. Clin. Rev. Allergy Immunol. 16, 351–364.10.1007/BF02737656Search in Google Scholar PubMed

Ramachandran, R., Altier, C., Oikonomopoulou, K., and Hollenberg, M.D. (2016). Proteinases, their extracellular targets, and inflammatory signaling. Pharmacol. Rev. 68, 1110–1142.10.1124/pr.115.010991Search in Google Scholar PubMed

Ramsay, A.J., Dong, Y., Hunt, M.L., Linn, M., Samaratunga, H., Clements, J.A., and Hooper, J.D. (2008). Kallikrein-related peptidase 4 (KLK4) initiates intracellular signaling via protease-activated receptors (PARs). KLK4 and PAR-2 are co-expressed during prostate cancer progression. J. Biol. Chem. 283, 12293–12304.10.1074/jbc.M709493200Search in Google Scholar PubMed

Ricciardolo, F.L.M., Sabatini, F., Sorbello, V., Benedetto, S., Dephilippi, I., Petecchia, L., Usai, C., Gnemmi, I., Balbi, B., De Rose, V., et al. (2013). Expression of vascular remodeling markers in relation to bradykinin receptors in asthma and COPD. Thorax 68, 803–811.10.1136/thoraxjnl-2012-202741Search in Google Scholar PubMed

Ricciardolo, F.L., Petecchia, L., Sorbello, V., Di Stefano, A., Usai, C., Massaglia, G.M., Gnemmi, I., Mognetti, B., Hiemstra, P.S., Sterk, P.J., et al. (2015). Bradykinin B2 receptor expression in the bronchial mucosa of allergic asthmatics: the role of NF-κB. Clin. Exp. Allergy 46, 428–438.10.1111/cea.12676Search in Google Scholar PubMed

Sasaki, H., Kawano, O., Endo, K., Suzuki, E., Haneda, H., Yukiue, H., Kobayashi, Y., Yano, M., and Fujii, Y. (2006). Decreased kallikrein 11 messenger RNA expression in lung cancer. Clin. Lung Cancer 8, 45–48.10.3816/CLC.2006.n.032Search in Google Scholar PubMed

Seiz, L., Kotzsch, M., Grebenchtchikov, N.I., Geurts-Moespot, A.J., Fuessel, S., Goettig, P., Gkazepis, A., Wirth, M.P., Schmitt, M., Lossnitzer, A., et al. (2010). Polyclonal antibodies against kallikrein-related peptidase 4 (KLK4): immunohistochemical assessment of KLK4 expression in healthy tissues and prostate cancer. Biol. Chem. 391, 391–401.10.1515/bc.2010.033Search in Google Scholar

Sexton, D.J., Chen, T., Martik, D., Kuzmic, P., Kuang, G., Chen, J., Nixon, A.E., Zuraw, B.L., Forteza, R.M., Abraham, W.M., et al. (2009). Specific inhibition of tissue kallikrein 1 with a human monoclonal antibody reveals a potential role in airway diseases. Biochem. J. 422, 383–392.10.1042/BJ20090010Search in Google Scholar PubMed

Shariff, S., Shelfoon, C., Holden, N.S., Traves, S.L., Wiehler, S., Kooi, C., Proud, D., and Leigh, R. (2017). Human rhinovirus infection of epithelial cells modulates airway smooth muscle migration. Am. J. Respir. Cell. Mol. Biol. 56, 796–803.10.1165/rcmb.2016-0252OCSearch in Google Scholar PubMed

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.2007.088104Search in Google Scholar PubMed

Shelfoon, C., Shariff, S., Traves, S.L., Kooi, C., Leigh, R., and Proud, D. (2016). Chemokine release from human rhinovirus-infected airway epithelial cells promotes fibroblast migration. J. Allergy Clin. Immunol. 138, 114–122.10.1016/j.jaci.2015.12.1308Search in Google Scholar PubMed

Sher, Y.P., Chou, C.C., Chou, R.H., Wu, H.M., 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

Singh, J., Naran, A., Misso, N.L., Rigby, P.J., Thompson, P.J., and Bhoola, K.D. (2008). Expression of kallikrein-related peptidases (KRP/hK5, 7, 6, 8) in subtypes of human lung carcinoma. Int. Immunopharmacol. 8, 300–306.10.1016/j.intimp.2007.08.015Search in Google Scholar PubMed

Sotiropoulou, G. and Pampalakis, G. (2012). Targeting the kallikrein-related peptidases for drug development. Trends Pharmacol. Sci. 33, 623–634.10.1016/j.tips.2012.09.005Search in Google Scholar PubMed

Stefansson, K., Brattsand, M., Roosterman, D., Kempkes, C., Bocheva, G., Steinhoff, M., and Egelrud, T. (2008). Activation of proteinase-activated receptor-2 by human kallikrein-related peptidases. J. Invest. Dermatol. 128, 18–25.10.1038/sj.jid.5700965Search in Google Scholar PubMed

Straus, M.R. and Whittaker, G.R. (2017). A peptide-based approach to evaluate the adaptability of influenza A virus to humans based on its hemagglutinin proteolytic cleavage site. PLoS One 12, e0174827.10.1371/journal.pone.0174827Search in Google Scholar PubMed PubMed Central

Swarts, D.R., Van Neste, L., Henfling, M.E., Eijkenboom, I., Eijk, P.P., van Velthuysen, M.L., Vink, A., Volante, M., Ylstra, B., Van Criekinge, W., et al. (2013). An exploration of pathways involved in lung carcinoid progression using gene expression profiling. Carcinogenesis 34, 2726–2737.10.1093/carcin/bgt271Search in Google Scholar PubMed

Tacon, C.E., Wiehler, S., Holden, N.S., Newton, R., Proud, D., and Leigh, R. (2010). Human rhinovirus infection up-regulates MMP-9 production in airway epithelial cells via NF-κB. Am. J. Respir. Cell. Mol. Biol. 243, 201–209.10.1165/rcmb.2009-0216OCSearch in Google Scholar PubMed

Taggart, C., Mall, M.A., Lalmanach, G., Cataldo, D., Ludwig, A., Janciauskiene, S., Heath, N., Meiners, S., Overall, C.M., Schultz, C., et al. (2017). Protean proteases: at the cutting edge of lung diseases. Eur. Respir. J. 49, 1–12.10.1183/13993003.01200-2015Search in Google Scholar PubMed

Talieri, M., Devetzi, M., Scorilas, A., Pappa, E., Tsapralis, N., Missitzis, I., and Ardavanis, A. (2012). Human kallikrein-related peptidase 12 (KLK12) splice variants expression in breast cancer and their clinical impact. Tumour Biol. 33, 1075–1084.10.1007/s13277-012-0347-xSearch in Google Scholar PubMed

Unal, D., Eroglu, C., Tasdemir, A., Karaman, H., Kurtul, N., Oguz, A., Goksu, S.S., and Kaplan, B. (2016). Is human kallikrein 11 in non-small cell lung cancer treated chemoradiotherapy associated with survival? Cancer Res. Treat. 48, 98–105.10.4143/crt.2014.364Search in Google Scholar PubMed PubMed Central

Van Leuven, J.T., Ridenhour, B.J., Gonzalez, A.J., Miller, C.R., and Miura, T.A. (2017). Lung epithelial cells have virus-specific and shared gene expression responses to infection by diverse respiratory viruses. PLoS One 12, e0178408.10.1371/journal.pone.0178408Search in Google Scholar PubMed PubMed Central

Venanzi, S., Malerba, G., Galavotti, R., Lauciello, M.C., Trabetti, E., Zanoni, G., Pescollderungg, L., Martinati, L.C., Boner, A.L., and Pignatti, P.F. (2001). Linkage to atopy on chromosome 19 in north-eastern Italian families with allergic asthma. Clin. Exp. Allergy 31, 1220–1224.10.1046/j.1365-2222.2001.01132.xSearch in Google Scholar PubMed

Wadsworth, S., Sin, D., and Dorscheid, D. (2011). Clinical update on the use of biomarkers of airway inflammation in the management of asthma. J. Asthma Allergy 4, 77–86.10.2147/JAA.S15081Search in Google Scholar PubMed PubMed Central

Xu, C.H., Zhang, Y., Yu, L.K. (2014). The diagnostic and prognostic value of serum human kallikrein-related peptidases 11 in non-small cell lung cancer. Tumour Biol. 35, 5199–5203.10.1007/s13277-014-1674-xSearch in Google Scholar PubMed PubMed Central

Yiu, W.H., Wong, D.W., Chan, L.Y., Leung, J.C., Chan, K.W., Lan, H.Y., Lai, K.N., and Tang, S.C. (2014). Tissue kallikrein mediates pro-inflammatory pathways and activation of protease-activated receptor-4 in proximal tubular epithelial cells. PLoS One 9, e88894.10.1371/journal.pone.0088894Search in Google Scholar PubMed PubMed Central

Zhang, Y., Song, H., Miao, Y., Wang, R., and Chen, L. (2010). Frequent transcriptional inactivation of Kallikrein 10 gene by CpG island hypermethylation in non-small cell lung cancer. Cancer Sci. 101, 934–940.10.1111/j.1349-7006.2009.01486.xSearch in Google Scholar PubMed

Zhang, Y., Wang, R., Song, H., Huang, G., Yi, J., Zheng, Y., Wang, J., and Chen, L. (2011). Methylation of multiple genes as a candidate biomarker in non-small cell lung cancer. Cancer Lett. 303, 21–28.10.1016/j.canlet.2010.12.011Search in Google Scholar PubMed

Zhu, S.P., Wang, J.Y., Wang, X.G., and Zhao, J.P. (2017). Long intergenic non-protein coding RNA 00858 functions as a competing endogenous RNA for miR-422a to facilitate the cell growth in non-small cell lung cancer. Aging 9, 475–486.10.18632/aging.101171Search in Google Scholar PubMed PubMed Central

Received: 2018-01-11
Accepted: 2018-03-26
Published Online: 2018-03-31
Published in Print: 2018-09-25

©2018 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Highlight: The 7th International Symposium on Kallikreins and Kallikrein-Related Peptidases
  3. Obituary
  4. Manfred Schmitt (1947–2018)
  5. Functional interrelationships between the kallikrein-related peptidases family and the classical kinin system in the human neutrophil
  6. Overview of tissue kallikrein and kallikrein-related peptidases in breast cancer
  7. Kallikrein-related peptidases in lung diseases
  8. The miRNA-kallikrein interaction: a mosaic of epigenetic regulation in cancer
  9. Mining human cancer datasets for kallikrein expression in cancer: the ‘KLK-CANMAP’ Shiny web tool
  10. Specificity profiling of human trypsin-isoenzymes
  11. Activation and activity of glycosylated KLKs 3, 4 and 11
  12. Microenvironment proteinases, proteinase-activated receptor regulation, cancer and inflammation
  13. Kallikrein-related peptidase 6 orchestrates astrocyte form and function through proteinase activated receptor-dependent mechanisms
  14. Kallikrein-related peptidase 5 and seasonal influenza viruses, limitations of the experimental models for activating proteases
  15. Novel splice variants of the human kallikrein-related peptidases 11 (KLK11) and 12 (KLK12), unraveled by next-generation sequencing technology
  16. Insights into the activity control of the kallikrein-related peptidase 6: small-molecule modulators and allosterism
  17. Kallikrein-related peptidase 14 is the second KLK protease targeted by the serpin vaspin
  18. Profiling system for skin kallikrein proteolysis applied in gene-deficient mouse models
  19. Evidence that cell surface localization of serine protease activity facilitates cleavage of the protease activated receptor CDCP1
  20. Kallikrein-related peptidase 7 overexpression in melanoma cells modulates cell adhesion leading to a malignant phenotype
  21. KLK5, a novel potential suppressor of vaginal carcinogenesis
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