Activation of the epithelial sodium channel (ENaC) by the alkaline protease from Pseudomonas aeruginosa

Journal of Biological Chemistry

Volumn 287, Issue 39, 2012, Pages 32556-32565

  Butterworth, Michael B ^a   Zhang, Liang ^a   Heidrich, Elisa M ^a   Myerburg, Michael M ^a   Thibodeau, Patrick H ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AIRWAY SURFACE LIQUID; ALKALINE PROTEASE; CHRONIC INFECTION; CYSTIC FIBROSIS; EPITHELIAL SODIUM CHANNELS; HOST DEFENSE; HUMAN BRONCHIAL EPITHELIAL CELLS; IMMORTALIZED CELLS; INFLAMMATORY RESPONSE; MULTIPLE MODES; P.AERUGINOSA; PROTEASE ACTIVITIES; PROTEOLYTIC ACTIVATION; PSEUDOMONAS AERUGINOSA; SUSTAINED ACTIVATION; VIRULENCE FACTORS;

ALKALINITY; BIOLOGICAL ORGANS; CELL CULTURE; CELLS; LIQUIDS; MONOLAYERS; PATHOGENS;

BACTERIA;

ALKALINE PROTEINASE; CALCIUM; EPITHELIAL SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; BACTERIAL VIRULENCE; BRONCHUS MUCOSA; CONTROLLED STUDY; CYSTIC FIBROSIS; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME RELEASE; EPITHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SUBUNIT; PSEUDOMONAS AERUGINOSA; RAT; SODIUM CURRENT;

ANIMALS; BACTERIAL PROTEINS; BRONCHI; CELL LINE; CELL POLARITY; CYSTIC FIBROSIS; ENDOPEPTIDASES; EPITHELIAL CELLS; EPITHELIAL SODIUM CHANNELS; HUMANS; MICE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 84866527762     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.369520     Document Type: Article

References (55)

1. Lyczak, J. B., Cannon, C. L., and Pier, G. B. (2000) Establishment of Pseudomonas aeruginosa infection. Lessons from a versatile opportunist. Microbes Infect. 2, 1051-1060 (Pubitemid 30664219)
2. Lyczak, J. B., Cannon, C. L., and Pier, G. B. (2002) Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15, 194-222 (Pubitemid 34303763)
3. Hobden, J. A. (2002) Pseudomonas aeruginosa proteases and corneal virulence. DNA Cell Biol. 21, 391-396
4. Jaffar-Bandjee, M. C., Lazdunski, A., Bally, M., Carrère, J., Chazalette, J. P., and Galabert, C. (1995) Production of elastase, exotoxin A, and alkaline protease in sputa during pulmonary exacerbation of cystic fibrosis in patients chronically infected by Pseudomonas aeruginosa. J. Clin. Microbiol. 33, 924-929
5. Sarkisova, S., Patrauchan, M. A., Berglund, D., Nivens, D. E., and Franklin, M. J. (2005) Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J. Bacteriol. 187, 4327-4337 (Pubitemid 40880942)
6. Lazdunski, A., Guzzo, J., Filloux, A., Bally, M., and Murgier, M. (1990) Secretion of extracellular proteins by Pseudomonas aeruginosa. Biochimie 72, 147-156 (Pubitemid 20137356)
7. Parmely, M., Gale, A., Clabaugh, M., Horvat, R., and Zhou, W. W. (1990) Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect. Immun. 58, 3009-3014 (Pubitemid 20267696)
8. Horvat, R. T., Clabaugh, M., Duval-Jobe, C., and Parmely, M. J. (1989) Inactivation of human γ interferon by Pseudomonas aeruginosa proteases. Elastase augments the effects of alkaline protease despite the presence of α2-macroglobulin. Infect. Immun. 57, 1668-1674 (Pubitemid 19140125)
9. Horvat, R. T., and Parmely, M. J. (1988) Pseudomonas aeruginosa alkaline protease degrades human γ interferon and inhibits its bioactivity. Infect. Immun. 56, 2925-2932 (Pubitemid 18259950)
10. Jagger, K. S., Robinson, D. L., Franz, M. N., and Warren, R. L. (1982) Detection by enzyme-linked immunosorbent assays of antibody specific for Pseudomonas proteases and exotoxin A in sera from cystic fibrosis patients. J. Clin. Microbiol. 15, 1054-1058 (Pubitemid 12070853)
11. Burke, V., Robinson, J. O., Richardson, C. J., and Bundell, C. S. (1991) Longitudinal studies of virulence factors of Pseudomonas aeruginosa in cystic fibrosis. Pathology 23, 145-148
12. Tingpej, P., Smith, L., Rose, B., Zhu, H., Conibear, T., Al Nassafi, K., Manos, J., Elkins, M., Bye, P., Willcox, M., Bell, S., Wainwright, C., and Harbour, C. (2007) Phenotypic characterization of clonal and nonclonal Pseudomonas aeruginosa strains isolated from lungs of adults with cystic fibrosis. J. Clin. Microbiol. 45, 1697-1704 (Pubitemid 46933894)
13. Granström, M., Ericsson, A., Strandvik, B., Wretlind, B., Pavlovskis, O. R., Berka, R., and Vasil, M. L. (1984) Relation between antibody response to Pseudomonas aeruginosa exoproteins and colonization/infection in patients with cystic fibrosis. Acta Paediatr. Scand. 73, 772-777 (Pubitemid 15209679)
14. Jagger, K. S., Bahner, D. R., and Warren, R. L. (1983) Protease phenotypes of Pseudomonas aeruginosa isolated from patients with cystic fibrosis. J. Clin. Microbiol. 17, 55-59 (Pubitemid 13211577)
15. Suter, S. (1994) The role of bacterial proteases in the pathogenesis of cystic fibrosis. Am. J. Respir. Crit. Care Med. 150, S118-S122
16. Kharazmi, A., Döring, G., Høiby, N., and Valerius, N. H. (1984) Interaction of Pseudomonas aeruginosa alkaline protease and elastase with human polymorphonuclear leukocytes in vitro. Infect. Immun. 43, 161-165 (Pubitemid 14218019)
17. Kharazmi, A., Høiby, N., Döring, G., and Valerius, N. H. (1984) Pseudomonas aeruginosa exoproteases inhibit human neutrophil chemiluminescence. Infect. Immun. 44, 587-591 (Pubitemid 14112685)
18. Guyot, N., Bergsson, G., Butler, M. W., Greene, C. M., Weldon, S., Kessler, E., Levine, R. L., O'Neill, S. J., Taggart, C. C., and McElvaney, N. G. (2010) Functional study of elafin cleaved by Pseudomonas aeruginosa metalloproteinases. Biol. Chem. 391, 705-716
19. Leidal, K. G., Munson, K. L., Johnson, M. C., and Denning, G. M. (2003) Metalloproteases from Pseudomonas aeruginosa degrade human RANTES, MCP-1, and ENA-78. J. Interferon Cytokine Res. 23, 307-318 (Pubitemid 36760751)
20. + self-inhibition. J. Physiol. 588, 1211-1225
21. Azad, A. K., Rauh, R., Vermeulen, F., Jaspers, M., Korbmacher, J., Boissier, B., Bassinet, L., Fichou, Y., des Georges, M., Stanke, F., De Boeck, K., Dupont, L., Balascáková, M., Hjelte, L., Lebecque, P., Radojkovic, D., Castellani, C., Schwartz, M., Stuhrmann, M., Schwarz, M., Skalicka, V., de Monestrol, I., Girodon, E., Férec, C., Claustres, M., Tümmler, B., Cassiman, J. J., Korbmacher, C., and Cuppens, H. (2009) Mutations in the amiloride-sensitive epithelial sodium channel in patients with cystic fibrosis-like disease. Hum. Mutat. 30, 1093-1103
22. + conductance in human colon is defective in cystic fibrosis. Am. J. Physiol. 277, G709-G716
23. Garcia-Caballero, A., Rasmussen, J. E., Gaillard, E., Watson, M. J., Olsen, J. C., Donaldson, S. H., Stutts, M. J., and Tarran, R. (2009) SPLUNC1 regulates airway surface liquid volume by protecting ENaC from proteolytic cleavage. Proc. Natl. Acad. Sci. U.S.A. 106, 11412-11417
24. Riordan, J. R., Rommens, J. M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N., and Chou, J. L. (1989) Identification of the cystic fibrosis gene. Cloning and characterization of complementary DNA. Science 245, 1066-1073 (Pubitemid 19231814)
25. Thibodeau, P. H., Richardson, J. M., 3rd, Wang, W., Millen, L., Watson, J., Mendoza, J. L., Du, K., Fischman, S., Senderowitz, H., Lukacs, G. L., Kirk, K., and Thomas, P. J. (2010) The cystic fibrosis-causing mutation ΔF508 affects multiple steps in cystic fibrosis transmembrane conductance regulator biogenesis. J. Biol. Chem. 285, 35825-35835
26. Myerburg, M. M., McKenna, E. E., Luke, C. J., Frizzell, R. A., Kleyman, T. R., and Pilewski, J. M. (2008) Prostasin expression is regulated by airway surface liquid volume and is increased in cystic fibrosis. Am. J. Physiol. Lung Cell Mol. Physiol. 294, L932-L941
27. Myerburg, M. M., Butterworth, M. B., McKenna, E. E., Peters, K. W., Frizzell, R. A., Kleyman, T. R., and Pilewski, J. M. (2006) Airway surface liquid volume regulates ENaC by altering the serine protease-protease inhibitor balance. A mechanism for sodium hyperabsorption in cystic fibrosis. J. Biol. Chem. 281, 27942-27949 (Pubitemid 44414506)
28. Tarran, R., Trout, L., Donaldson, S. H., and Boucher, R. C. (2006) Soluble mediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia. J. Gen. Physiol. 127, 591-604
29. + transport. Am. J. Physiol. Lung Cell Mol. Physiol. 288, L813-L819
30. 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
31. Tan, C. D., Selvanathar, I. A., and Baines, D. L. (2011) Cleavage of endogenous γENaC and elevated abundance of αENaC are associated with increased Na transport in response to apical fluid volume expansion in human H441 airway epithelial cells. Pflugers Arch. 462, 431-441
32. 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
33. Jasti, J., Furukawa, H., Gonzales, E. B., and Gouaux, E. (2007) Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 449, 316-323 (Pubitemid 47443482)
34. + channel through peptide binding at peripheral finger and thumb domains. J. Biol. Chem. 285, 35216-35223
35. Vuagniaux, G., Vallet, V., Jaeger, N. F., Hummler, E., and Rossier, B. C. (2002) Synergistic activation of ENaC by three membrane-bound channel- activating serine proteases (mCAP1, mCAP2, and mCAP3) and serum- and glucocorticoid-regulated kinase (Sgk1) in Xenopus oocytes. J. Gen. Physiol. 120, 191-201 (Pubitemid 34857968)
36. Guipponi, M., Vuagniaux, G., Wattenhofer, M., Shibuya, K., Vazquez, M., Dougherty, L., Scamuffa, N., Guida, E., Okui, M., Rossier, C., Hancock, M., Buchet, K., Reymond, A., Hummler, E., Marzella, P. L., Kudoh, J., Shimizu, N., Scott, H. S., Antonarakis, S. E., and Rossier, B. C. (2002) The transmembrane serine protease (TMPRSS3) mutated in deafness DFNB8/10 activates the epithelial sodium channel (ENaC) in vitro. Hum. Mol. Genet. 11, 2829-2836 (Pubitemid 35331815)
37. Planes, C., Leyvraz, C., Uchida, T., Angelova, M. A., Vuagniaux, G., Hummler, E., Matthay, M., Clerici, C., and Rossier, B. (2005) In vitro and in vivo regulation of transepithelial lung alveolar sodium transport by serine proteases. Am. J. Physiol. Lung Cell Mol. Physiol. 288, L1099-L1109 (Pubitemid 40695435)
38. Myerburg, M. M., Harvey, P. R., Heidrich, E. M., Pilewski, J. M., and Butterworth, M. B. (2010) Acute regulation of the epithelial sodium channel in airway epithelia by proteases and trafficking. Am. J. Respir. Cell Mol. Biol. 43, 712-719
39. Bens, M., Vallet, V., Cluzeaud, F., Pascual-Letallec, L., Kahn, A., Rafestin-Oblin, M. E., Rossier, B. C., and Vandewalle, A. (1999) Corticosteroid-dependent sodium transport in a novel immortalized mouse collecting duct principal cell line. J. Am. Soc. Nephrol. 10, 923-934 (Pubitemid 29203078)
40. Zhang, L., Conway, J. F., and Thibodeau, P. H. (2012) Calcium-induced folding and stabilization of the Pseudomonas aeruginosa alkaline protease. J. Biol. Chem. 287, 4311-4322
41. Jozic, D., Bourenkov, G., Lim, N. H., Visse, R., Nagase, H., Bode, W., and Maskos, K. (2005) X-ray structure of human proMMP-1. New insights into procollagenase activation and collagen binding. J. Biol. Chem. 280, 9578-9585 (Pubitemid 40409653)
42. Edman, K., Furber, M., Hemsley, P., Johansson, C., Pairaudeau, G., Petersen, J., Stocks, M., Tervo, A., Ward, A., Wells, E., and Wissler, L. (2011) The discovery of MMP7 inhibitors exploiting a novel selectivity trigger. ChemMedChem 6, 769-773
43. Bertini, I., Calderone, V., Fragai, M., Jaiswal, R., Luchinat, C., Melikian, M., Mylonas, E., and Svergun, D. I. (2008) Evidence of reciprocal reorientation of the catalytic and hemopexin-like domains of full-length MMP-12. J. Am. Chem. Soc. 130, 7011-7021 (Pubitemid 351770143)
44. Butterworth, M. B., Frizzell, R. A., Johnson, J. P., Peters, K. W., and Edinger, R. S. (2005) PKA-dependent ENaC trafficking requires the SNARE-binding protein complexin. Am. J. Physiol. Renal Physiol. 289, F969-F977 (Pubitemid 41447051)
45. Passero, C. J., Carattino, M. D., Kashlan, O. B., Myerburg, M. M., Hughey, R. P., and Kleyman, T. R. (2010) Defining an inhibitory domain in the γ subunit of the epithelial sodium channel. Am. J. Physiol. Renal Physiol. 299, F854-F861
46. Passero, C. J., Mueller, G. M., Myerburg, M. M., Carattino, M. D., Hughey, R. P., and Kleyman, T. R. (2012) TMPRSS4-dependent activation of the epithelial sodium channel requires cleavage of the γ-subunit distal to the furin cleavage site. Am. J. Physiol. Renal Physiol. 302, F1-F8
47. Carattino, M. D., Hughey, R. P., and Kleyman, T. R. (2008) Proteolytic processing of the epithelial sodium channel γ subunit has a dominant role in channel activation. J. Biol. Chem. 283, 25290-25295
48. Bardoel, B. W., van der Ent, S., Pel, M. J., Tommassen, J., Pieterse, C. M., van Kessel, K. P., and van Strijp, J. A. (2011) Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7, e1002206
49. Xiong, L., Montplaisir, J., Desautels, A., Barhdadi, A., Turecki, G., Levchenko, A., Thibodeau, P., Dube, M. P., Gaspar, C., and Rouleau, G. A. (2010) Family study of restless legs syndrome in Quebec, Canada. Clinical characterization of 671 familial cases. Arch. Neurol. 67, 617-622
50. + conductance. Proc. Natl. Acad. Sci. U.S.A. 108, 10260-10265
51. + transport in cystic fibrosis respiratory epithelia. Abnormal basal rate and response to adenylate cyclase activation. J. Clin. Invest. 78, 1245-1252
52. Gowen, C. W., Lawson, E. E., Gingras-Leatherman, J., Gatzy, J. T., Boucher, R. C., and Knowles, M. R. (1986) Increased nasal potential difference and amiloride sensitivity in neonates with cystic fibrosis. J. Pediatr. 108, 517-521 (Pubitemid 16115510)
53. Catalan, M. A., Nakamoto, T., Gonzalez-Begne, M., Camden, J. M., Wall, S. M., Clarke, L. L., and Melvin, J. E. (2010) Cftr and ENaC ion channels mediate NaCl absorption in the mouse submandibular gland. J. Physiol. 588, 713-724
54. Zhou, Z., Duerr, J., Johannesson, B., Schubert, S. C., Treis, D., Harm, M., Graeber, S. Y., Dalpke, A., Schultz, C., and Mall, M. A. (2011) The ENaC-overexpressing mouse as a model of cystic fibrosis lung disease. J. Cyst. Fibros. 10, S172-S182
55. Knowles, M., Gatzy, J., and Boucher, R. (1981) Increased bioelectric potential difference across respiratory epithelia in cystic fibrosis. N. Engl. J. Med. 305, 1489-1495 (Pubitemid 12244203)