Proteolytic activation of the human epithelial sodium channel by trypsin IV and trypsin i involves distinct cleavage sites

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 19067-19078

  Haerteis, Silke ^a   Krappitz, Annabel ^a   Krappitz, Matteus ^a   Murphy, Jane E ^b   Bertog, Marko ^a   Krueger, Bettina ^a   Nacken, Regina ^a   Chung, Hyunjae ^c   Hollenberg, Morley D ^c   Knecht, Wolfgang ^d   Bunnett, Nigel W ^e,f   Korbmacher, Christoph ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d ASTRAZENECA R AND D   (Sweden)

^e MONASH UNIVERSITY   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TISSUE;

CLEAVAGE SITES; EPITHELIAL SODIUM CHANNELS; EPITHELIAL TISSUE; IN-VIVO; PROTEOLYTIC ACTIVATION; TISSUE SPECIFICS;

CHEMICAL ACTIVATION;

LEUKOCYTE ELASTASE; TRYPSIN; TRYPSIN I; TRYPSIN IV; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOTINYLATION; CELL DIFFERENTIATION; CELL SURFACE; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; SODIUM TRANSPORT;

EPITHELIAL SODIUM CHANNEL (ENAC); ION CHANNEL; OOCYTE; PROTEASE; PROTEOLYTIC CHANNEL ACTIVATION; SERINE PROTEASE; TRYPSIN; TRYPSIN IV; TWO-ELECTRODE VOLTAGE CLAMP;

AMINO ACID SEQUENCE; ANIMALS; AZETIDINES; BENZYLAMINES; BINDING SITES; EPITHELIAL CELLS; EPITHELIAL SODIUM CHANNELS; EXTRACELLULAR SPACE; HUMANS; KIDNEY; MOLECULAR SEQUENCE DATA; MUTATION; OOCYTES; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; TRYPSIN; XENOPUS LAEVIS;

EID: 84903823511     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.538470     Document Type: Article

References (47)

1. Garty, H., and Palmer, L. G. (1997) Epithelial sodium channels: function, structure, and regulation. Physiol. Rev. 77, 359-396
2. Kellenberger, S., and Schild, L. (2002) Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82, 735-767
3. Jasti, J., Furukawa, H., Gonzales, E. B., and Gouaux, E. (2007) Structure of acid-sensing ion channel 1 at 1. 9 Åresolution and low pH. Nature 449, 316-323
4. Stockand, J. D., Staruschenko, A., Pochynyuk, O., Booth, R. E., and Silverthorn, D. U. (2008) Insight toward epithelial Na- channel mechanism revealed by the acid-sensing ion channel 1 structure. IUBMB Life 60, 620-628
5. Stewart, A. P., Haerteis, S., Diakov, A., Korbmacher, C., and Edwardson, J. M. (2011) Atomic force microscopy reveals the architecture of the epithelial sodium channel (ENaC). J. Biol. Chem. 286, 31944-31952
6. Kleyman, T. R., Carattino, M. D., and Hughey, R. P. (2009) ENaC at the cutting edge: regulation of epithelial sodium channels by proteases. J. Biol. Chem. 284, 20447-20451
7. Rossier, B. C., and Stutts, M. J. (2009) Activation of the epithelial sodium channel (ENaC) by serine proteases. Annu. Rev. Physiol. 71, 361-379
8. Haerteis, S., Krappitz, M., Diakov, A., Krappitz, A., Rauh, R., and Korbmacher, C. (2012) Plasmin and chymotrypsin have distinct preferences for channel activating cleavage sites in the -subunit of the human epithelial sodium channel. J. Gen. Physiol. 140, 375-389
9. Bruns, J. B., Carattino, M. D., Sheng, S., Maarouf, A. B., Weisz, O. A., Pilewski, J. M., Hughey, R. P., and Kleyman, T. R. (2007) Epithelial Na- channels are fully activated by furin- and prostasin-dependent release of an inhibitory peptide from the - subunit. J. Biol. Chem. 282, 6153-6160
10. Passero, C. J., Mueller, G. M., Rondon-Berrios, H., Tofovic, S. P., Hughey, R. P., and Kleyman, T. R. (2008) Plasmin activates epithelial Na- channels by cleaving the - subunit. J. Biol. Chem. 283, 36586-36591
11. Adebamiro, A., Cheng, Y., Rao, U. S., Danahay, H., and Bridges, R. J. (2007) Asegment of-ENaC mediates elastase activation of Na- transport. J. Gen. Physiol. 130, 611-629
12. Patel, A. B., Chao, J., and Palmer, L. G. (2012) Tissue kallikrein activation of the epithelial Na channel. Am. J. Physiol. Renal Physiol. 303, F540-F550
13. Diakov, A., Bera, K., Mokrushina, M., Krueger, B., and Korbmacher, C. (2008) Cleavage in the -subunit of the epithelial sodium channel (ENaC) plays an important role in the proteolytic activation of near-silent channels. J. Physiol. 586, 4587-4608
14. Nesterov, V., Dahlmann, A., Bertog, M., and Korbmacher, C. (2008) Trypsin can activate the epithelial sodium channel (ENaC) in microdissected mouse distal nephron. Am. J. Physiol. Renal Physiol. 295, F1052-F1062
15. Koshikawa, N., Hasegawa, S., Nagashima, Y., Mitsuhashi, K., Tsubota, Y., Miyata, S., Miyagi, Y., Yasumitsu, H., and Miyazaki, K. (1998) Expression of trypsin by epithelial cells of various tissues, leukocytes, and neurons in human and mouse. Am. J. Pathol. 153, 937-944
16. Navarrete, M., Ho, J., Krokhin, O., Ezzati, P., Rigatto, C., Reslerova, M., Rush, D. N., Nickerson, P., and Wilkins, J. A. (2013) Proteomic characterization of serine hydrolase activity and composition in normal urine. Clin. Proteomics 10, 17
17. Emi, M., Nakamura, Y., Ogawa, M., Yamamoto, T., Nishide, T., Mori, T., and Matsubara, K. (1986) Cloning, characterization and nucleotide sequences of two cDNAs encoding human pancreatic trypsinogens. Gene 41, 305-310
18. Wiegand, U., Corbach, S., Minn, A., Kang, J., and Müller-Hill, B. (1993) Cloning of the cDNA encoding human brain trypsinogen and characterization of its product. Gene 136, 167-175
19. Nyaruhucha, C. N., Kito, M., and Fukuoka, S. I. (1997) Identification and expression of the cDNA-encoding human mesotrypsin(ogen), an isoform of trypsin with inhibitor resistance. J. Biol. Chem. 272, 10573-10578
20. Gallatz, K., Medveczky, P., Németh, P., Szilágyi, L., Gráf, L., and Palkovits, M. (2007) Human trypsin(ogen) 4-like immunoreactivity in the white matter of the cerebral cortex and the spinal cord. Ideggyogyaszati szemle 60, 118-123
21. Tóth, J., Siklódi, E., Medveczky, P., Gallatz, K., Németh, P., Szilágyi, L., Gráf, L., and Palkovits, M. (2007) Regional distribution of human trypsinogen 4 in human brain at mRNA and protein level. Neurochem. Res. 32, 1423-1433
22. Knecht, W., Cottrell, G. S., Amadesi, S., Mohlin, J., Skåregärde, A., Gedda, K., Peterson, A., Chapman, K., Hollenberg, M. D., Vergnolle, N., and Bunnett, N. W. (2007) Trypsin IV or mesotrypsin and p23 cleave proteaseactivated receptors 1 and 2 to induce inflammation and hyperalgesia. J. Biol. Chem. 282, 26089-26100
23. Ceppa, E. P., Lyo, V., Grady, E. F., Knecht, W., Grahn, S., Peterson, A., Bunnett, N. W., Kirkwood, K. S., and Cattaruzza, F. (2011) Serine proteases mediate inflammatory pain in acute pancreatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G1033-G1042
24. Cattaruzza, F., Amadesi, S., Carlsson, J. F., Murphy, J. E., Lyo, V., Kirkwood, K., Cottrell, G. S., Bogyo, M., Knecht, W., and Bunnett, N. W. (2014) Serine proteases and protease-activated receptor 2 mediate the proinflammatory and algesic actions of diverse stimulants. Br. J. Pharmacol. 10. 1111/bph. 12738
25. Hockla, A., Miller, E., Salameh, M. A., Copland, J. A., Radisky, D. C., and Radisky, E. S. (2012) PRSS3/mesotrypsin is a therapeutic target for metastatic prostate cancer. Mol. Cancer Res. 10, 1555-1566
26. Radisky, E. S. (2013) PRSS3/mesotrypsin in prostate cancer progression: implications for translational medicine. Asian J. Androl. 15, 439-440
27. Svenningsen, P., Bistrup, C., Friis, U. G., Bertog, M., Haerteis, S., Krueger, B., Stubbe, J., Jensen, O. N., Thiesson, H. C., Uhrenholt, T. R., Jespersen, B., Jensen, B. L., Korbmacher, C., and Skøtt, O. (2009) Plasmin in nephrotic urine activates the epithelial sodium channel. J. Am. Soc. Nephrol. 20, 299-310
28. Zeissig, S., Bergann, T., Fromm, A., Bojarski, C., Heller, F., Guenther, U., Zeitz, M., Fromm, M., and Schulzke, J. D. (2008) Altered ENaC expression leads to impaired sodium absorption in the noninflamed intestine in Crohn's disease. Gastroenterology 134, 1436-1447
29. Haerteis, S., Krappitz, M., Bertog, M., Krappitz, A., Baraznenok, V., Henderson, I., Lindström, E., Murphy, J. E., Bunnett, N. W., and Korbmacher, C. (2012) Proteolytic activation of the epithelial sodium channel (ENaC) by the cysteine protease cathepsin-S. Pflügers Arch. 464, 353-365
30. Haerteis, S., Krueger, B., Korbmacher, C., and Rauh, R. (2009) The -subunit of the epithelial sodium channel (ENaC) enhances channel activity and alters proteolytic ENaC activation. J. Biol. Chem. 284, 29024-29040
31. Rauh, R., Diakov, A., Tzschoppe, A., Korbmacher, J., Azad, A. K., Cuppens, H., Cassiman, J. J., Dötsch, J., Sticht, H., and Korbmacher, C. (2010) A mutation of the epithelial sodium channel associated with atypical cystic fibrosis increases channel open probability and reduces Na- self inhibition. J. Physiol. 588, 1211-1225
32. Krueger, B., Schlötzer-Schrehardt, U., Haerteis, S., Zenkel, M., Chankiewitz, V. E., Amann, K. U., Kruse, F. E., and Korbmacher, C. (2012) Four subunits (-) of the epithelial sodium channel (ENaC) are expressed in the human eye in various locations. Invest. Ophthalmol. Vis. Sci. 53, 596-604
33. Chung, H., Ramachandran, R., Hollenberg, M. D., and Muruve, D. A. (2013) Proteinase- activated receptor-2 transactivation of epidermal growth factor receptor and transforming growth factor- receptor signaling pathways contributes to renal fibrosis. J. Biol. Chem. 288, 37319-37331
34. Cottrell, G. S., Amadesi, S., Grady, E. F., and Bunnett, N. W. (2004) Trypsin IV, a novel agonist of protease-activated receptors 2 and 4. J. Biol. Chem. 279, 13532-13539
35. Woollhead, A. M., Scott, J. W., Hardie, D. G., and Baines, D. L. (2005) Phenformin and 5-aminoimidazole-4-carboxamide-1-D-ribofurano-side (AICAR) activation of AMP-activated protein kinase inhibits transepithelial Na- transport across H441 lung cells. J. Physiol. 566, 781-792
36. Bertog, M., Letz, B., Kong, W., Steinhoff, M., Higgins, M. A., Bielfeld- Ackermann, A., Frömter, E., Bunnett, N. W., and Korbmacher, C. (1999) Basolateral proteinase-activated receptor (PAR-2) induces chloride secretion in M-1 mouse renal cortical collecting duct cells. J. Physiol. 521, 3-17
37. Tan, C. D., Selvanathar, I. A., and Baines, D. L. (2011) Cleavage of endogenous -ENaC and elevated abundance of -ENaC are associated with increased Na- transport in response to apical fluid volume expansion in human H441 airway epithelial cells. Pflügers Arch. 462, 431-441
38. Volk, T., Konstas, A. A., Bassalaý, P., Ehmke, H., and Korbmacher, C. (2004) Extracellular Na- removal attenuates rundown of the epithelial Na-channel (ENaC) by reducing the rate of channel retrieval. Pflügers Arch. 447, 884-894
39. Eaton, D. C., Helms, M. N., Koval, M., Bao, H. F., and Jain, L. (2009) The contribution of epithelial sodium channels to alveolar function in health and disease. Annu. Rev. Physiol. 71, 403-423
40. Hummler, E., and Planès, C. (2010) Importance of ENaC-mediated sodium transport in alveolar fluid clearance using genetically-engineered mice. Cell Physiol. Biochem. 25, 63-70
41. Lazrak, A., and Matalon, S. (2003) cAMP-induced changes of apical membrane potentials of confluent H441 monolayers. Am. J. Physiol. Lung Cell Mol. Physiol. 285, L443-L450
42. Ji, H. L., Su, X. F., Kedar, S., Li, J., Barbry, P., Smith, P. R., Matalon, S., and Benos, D. J. (2006) -Subunit confers novel biophysical features to - human ENaC via a physical interaction. J. Biol. Chem. 281, 8233-8241
43. Szmola, R., Kukor, Z., and Sahin-Tóth, M. (2003) Human mesotrypsin is a unique digestive protease specialized for the degradation of trypsin inhibitors. J. Biol. Chem. 278, 48580-48589
44. Sahin-Tóth, M. (2005) Human mesotrypsin defies natural trypsin inhibitors: from passive resistance to active destruction. Protein Pept. Lett. 12, 457-464
45. Chen, J. M., Radisky, E. S., and Ferec, C. (2012) Human trypsins. in Handbook of Proteolytic Enzymes (Rawlings, N. D., and Salvesen, G. S., eds) pp. 2600-2609, Elsevier, Amsterdam
46. Diederichs, S., Bulk, E., Steffen, B., Ji, P., Tickenbrock, L., Lang, K., Zänker, K. S., Metzger, R., Schneider, P. M., Gerke, V., Thomas, M., Berdel, W. E., Serve, H., and Müller-Tidow, C. (2004) S100 family members and trypsinogens are predictors of distant metastasis and survival in early-stage non-small cell lung cancer. Cancer Res. 64, 5564-5569
47. Ghilardi, C., Chiorino, G., Dossi, R., Nagy, Z., Giavazzi, R., and Bani, M. (2008) Identification of novel vascular markers through gene expression profiling of tumor-derived endothelium. BMC Genomics 9, 201