Accessible Requires Authentication Published by De Gruyter March 31, 2018

Kallikrein-related peptidases in lung diseases

Woodys Lenga Ma Bonda, Sophie Iochmann, Mélia Magnen, Yves Courty and Pascale Reverdiau
From the journal Biological Chemistry

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search 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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search in Google Scholar

Goettig, P., Magdolen, V., and Brandstetter, H. (2010). Natural and synthetic inhibitors of kallikrein-related peptidases (KLKs). Biochimie 92, 1546–1567. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Ichinose, M. (2003). Inflamatory mechanisms in bronchial asthma and COPD. Tohoku J. Exp. Med. 200, 1–6. Search in Google Scholar

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. Search in Google Scholar

Kalinska, M., Meyer-Hoffert, U., Kantyka, T., and Potempa, J. (2016). Kallikreins – the melting pot of activity and function. Biochimie 122, 270–282. Search in Google Scholar

Kimes, P.K. (2014). SigFuge: single gene clustering of RNA-seq reveals differential isoform usage among cancer samples. Nucleic Acids Res. 42, 1–12. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Minor, D.M. and Proud, D. (2017). Role of human rhinovirus in triggering human airway epithelial-mesenchymal transition. Respir. Res. 18, 1–16. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. 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. Search in Google Scholar

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. Search in Google Scholar

Neumann, G. and Kawaoka, Y. (2015). Transmission of influenza A viruses. Virology 1, 234–246. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Pais, F., Fayed, M., and Evans, T. (2017). Lymphangioleiomyomatosis: an explosive presentation of a rare disease. Oxf. Med. Case Reports 6, 92–94. Search in Google Scholar

Pasic, M.D., Sotiropoulou, G., and Yousef, G.M. (2015). The miRNA-kallikrein interactions: adding a new dimension. Cell Cycle 14, 691–692. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

Proud, D. (1998). The kinin system in rhinitis and asthma. Clin. Rev. Allergy Immunol. 16, 351–364. Search in Google Scholar

Ramachandran, R., Altier, C., Oikonomopoulou, K., and Hollenberg, M.D. (2016). Proteinases, their extracellular targets, and inflammatory signaling. Pharmacol. Rev. 68, 1110–1142. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search in Google Scholar

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. Search in Google Scholar

Shaw, J.L. and Diamandis, E.P. (2007). Distribution of 15 human kallikreins in tissues and biological fluids. Clin. Chem. 53, 1423–1432. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search 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. Search in Google Scholar

Sotiropoulou, G. and Pampalakis, G. (2012). Targeting the kallikrein-related peptidases for drug development. Trends Pharmacol. Sci. 33, 623–634. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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. Search in Google Scholar

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