Proteases, cystic fibrosis and the epithelial sodium channel (ENaC)

Cell and Tissue Research

Volumn 351, Issue 2, 2013, Pages 309-323

  Thibodeau, P H ^a   Butterworth, Michael B ^a  

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

Author keywords

Cystic fibrosis (CF); Epithelial sodiumchannel (ENaC); Protease; Pseudomonas aeruginosa

Indexed keywords

EPITHELIAL SODIUM CHANNEL; PEPTIDE HYDROLASE;

ANIMAL; CYSTIC FIBROSIS; ENZYMOLOGY; HUMAN; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; REVIEW;

ANIMALS; CYSTIC FIBROSIS; EPITHELIAL SODIUM CHANNELS; HUMANS; PEPTIDE HYDROLASES; PSEUDOMONAS AERUGINOSA;

EID: 84885679220     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1439-z     Document Type: Review

References (188)

1. Abu-El-Haija M, Sinkora M, Meyerholz DK, Welsh MJ, McCray PB Jr, Butler J, Uc A (2011) An activated immune and inflammatory response targets the pancreas of newborn pigs with cystic fibrosis. Pancreatology 11:506-515
2. Adebamiro A, Johnson JP, Bridges RJ (2002) Aprotinin decreases the number of active Na+ channels in the apical membrane of A6 epithelia. Pediatr Pulmonol Suppl 24:211-212
3. Adebamiro A, Cheng Y, Johnson JP, Bridges RJ (2005) Endogenous protease activation of ENaC: effect of serine protease inhibition on ENaC single channel properties. J Gen Physiol 126:339-352
4. Adebamiro A, Cheng Y, Rao US, Danahay H, Bridges RJ (2007) A segment of gamma ENaC mediates elastase activation of Na+ transport. J Gen Physiol 130:611-629
5. Azad AK, Rauh R, Vermeulen F, Jaspers M, Korbmacher J, Boissier B, Bassinet L, Fichou Y, Georges M des, Stanke F, De Boeck K, Dupont L, Balascakova M, Hjelte L, Lebecque P, Radojkovic D, Castellani C, Schwartz M, Stuhrmann M, Schwarz M, Skalicka V, Monestrol I de, Girodon E, Ferec C, Claustres M, Tummler B, Cassiman JJ, Korbmacher C, Cuppens H (2009) Mutations in the amiloride-sensitive epithelial sodium channel in patients with cystic fibrosis-like disease. Hum Mutat 30:1093-1103
6. Azghani AO, Baker JW, Shetty S, Miller EJ, Bhat GJ (2002) Pseudomonas aeruginosa elastase stimulates ERK signaling pathway and enhances IL-8 production by alveolar epithelial cells in culture. Inflamm Res 51:506-510
7. Bainbridge T, Fick RB Jr (1989) Functional importance of cystic fibrosis immunoglobulin G fragments generated by Pseudomonas aeruginosa elastase. J Lab Clin Med 114:728-733
8. Baumann U (1994) Crystal structure of the 50 kDa metallo protease from Serratia marcescens. J Mol Biol 242:244-251
9. Baumann U, Wu S, Flaherty KM, McKay DB (1993) Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12:3357-3364
10. Bens M, Chassin C, Vandewalle A (2006) Regulation of NaCl transport in the renal collecting duct: lessons from cultured cells. Pflugers Arch 453:133-146
11. Bhalla V, Hallows KR (2008) Mechanisms of ENaC regulation and clinical implications. J Am Soc Nephrol 19:1845-1854
12. Bosshart H, Humphrey J, Deignan E, Davidson J, Drazba J, Yuan L, Oorschot V, Peters PJ, Bonifacino JS (1994) The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system. J Cell Biol 126:1157-1172
13. Boucher RC (2004) New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 23:146-158
14. Briel M, Greger R, Kunzelmann K (1998) Cl-transport by cystic fibrosis transmembrane conductance regulator (CFTR) contributes to the inhibition of epithelial Na+ channels (ENaCs) in Xenopus oocytes co-expressing CFTR and ENaC. J Physiol 508:825-836
15. Britigan BE, Hayek MB, Doebbeling BN, Fick RB Jr (1993) Transferrin and lactoferrin undergo proteolytic cleavage in the Pseudomonas aeruginosa-infected lungs of patients with cystic fibrosis. Infect Immun 61:5049-5055
16. Bruns JB, Carattino MD, Sheng S, Maarouf AB, Weisz OA, Pilewski JM, Hughey RP, Kleyman TR (2007) Epithelial Na+ channels are fully activated by furin- and prostasin-dependent release of an inhibitory peptide from the {gamma}-subunit. J Biol Chem 282:6153-6160
17. Burke V, Robinson JO, Richardson CJ, Bundell CS (1991) Longitudinal studies of virulence factors of Pseudomonas aeruginosa in cystic fibrosis. Pathology 23:145-148
18. Butterworth MB (2010) Regulation of the epithelial sodium channel (ENaC) by membrane trafficking. Biochim BiophysActa 1802:1166-1177
19. Butterworth MB, Edinger RS, Frizzell RA, Johnson JP (2009) Regulation of the epithelial sodium channel by membrane trafficking. Am J Physiol Renal Physiol 296:F10-F24
20. Byrd MS, Pang B, Hong W, Waligora EA, Juneau RA, Armbruster CE, Weimer KE, Murrah K, Mann EE, Lu H, Sprinkle A, Parsek MR, Kock ND, Wozniak DJ, Swords WE (2011) Direct evaluation of Pseudomonas aeruginosa biofilm mediators in a chronic infection model. Infect Immun 79:3087-3095
21. Caballero AR, Moreau JM, Engel LS, Marquart ME, Hill JM, O'Callaghan RJ (2001) Pseudomonas aeruginosa protease IV enzyme assays and comparison to other Pseudomonas proteases. Anal Biochem 290:330-337
22. Caldwell RA, Boucher RC, Stutts MJ (2004) Serine protease activation of near-silent epithelial Na+ channels. Am J Physiol Cell Physiol 286:C190-C194
23. Caldwell RA, Boucher RC, Stutts MJ (2005) Neutrophil elastase activates near-silent epithelial Na+ channels and increases airway epithelial Na+ transport. Am J Physiol Lung Cell Mol Physiol 288:L813-L819
24. Capasso G, Cantone A, Evangelista C, Zacchia M, Trepiccione F, Acone D, Rizzo M (2005) Channels, carriers, and pumps in the pathogenesis of sodium-sensitive hypertension. Semin Nephrol 25:419-424
25. Carattino MD, Passero CJ, Steren CA, Maarouf AB, Pilewski JM, Myerburg MM, Hughey RP, Kleyman TR (2008) Defining an inhibitory domain in the alpha-subunit of the epithelial sodium channel. Am J Physiol Renal Physiol 294:F47-F52
26. Chambers LA, Rollins BM, Tarran R (2007) Liquid movement across the surface epithelium of large airways. Respir Physiol Neurobiol 159:256-270
27. Chen JH, Stoltz DA, Karp PH, Ernst SE, Pezzulo AA, Moninger TO, Rector MV, Reznikov LR, Launspach JL, Chaloner K, Zabner J, Welsh MJ (2010) Loss of anion transport without increased sodium absorption characterizes newborn porcine cystic fibrosis airway epithelia. Cell 143:911-923
28. Cheng SH, Rich DP, Marshall J, Gregory RJ, Welsh MJ, Smith AE (1991) Phosphorylation of the R domain by cAMP-dependent protein kinase regulates the CFTR chloride channel. Cell 66:1027-1036
29. Choi JY, Muallem D, Kiselyov K, Lee MG, Thomas PJ, Muallem S (2001) Aberrant CFTR-dependent HCO3 - transport in mutations associated with cystic fibrosis. Nature 410:94-97
30. Chow SC, Weis M, Kass GE, Holmstrom TH, Eriksson JE, Orrenius S (1995) Involvement of multiple proteases during Fas-mediated apoptosis in T lymphocytes. FEBS Lett 364:134-138
31. Ciechanover A (1998) The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J 17:7151-7160
32. Conese M, Copreni E, Di Gioia S, De Rinaldis P, Fumarulo R (2003) Neutrophil recruitment and airway epithelial cell involvement in chronic cystic fibrosis lung disease. J Cyst Fibros 2:129-135
33. Coraux C, Roux J, Jolly T, Birembaut P (2008) Epithelial cellextracellular matrix interactions and stem cells in airway epithelial regeneration. Proc Am Thorac Soc 5:689-694
34. Cottrell GS, Amadesi S, Grady EF, Bunnett NW (2004) Trypsin IV, a novel agonist of protease-activated receptors 2 and 4. J Biol Chem 279:13532-13539
35. Dean M, Hamon Y, Chimini G (2001) The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 42:1007-1017
36. Di Cera E, Cantwell AM (2001) Determinants of thrombin specificity. Ann N Y Acad Sci 936:133-146
37. Donaldson SH, Hirsh A, Li DC, Holloway G, Chao J, Boucher RC, Gabriel SE (2002) Regulation of the epithelial sodium channel by serine proteases in human airways. J Biol Chem 277:8338-8345
38. Downey DG, Brockbank S, Martin SL, Ennis M, Elborn JS (2007a) The effect of treatment of cystic fibrosis pulmonary exacerbations on airways and systemic inflammation. Pediatr Pulmonol 42:729-735
39. Downey DG, Martin SL, Dempster M, Moore JE, Keogan MT, Starcher B, Edgar J, Bilton D, Elborn JS (2007b) The relationship of clinical and inflammatory markers to outcome in stable patients with cystic fibrosis. Pediatr Pulmonol 42:216-220
40. Downey DG, Bell SC, Elborn JS (2009) Neutrophils in cystic fibrosis. Thorax 64:81-88
41. Drumm ML, Pope HA, Cliff WH, Rommens JM, Marvin SA, Tsui LC, Collins FS, Frizzell RA, Wilson JM (1990) Correction of the cystic fibrosis defect in vitro by retrovirus-mediated gene transfer. Cell 62:1227-1233
42. Duong F, Lazdunski A, Cami B, Murgier M (1992) Sequence of a cluster of genes controlling synthesis and secretion of alkaline protease in Pseudomonas aeruginosa: relationships to other secretory pathways. Gene 121:47-54
43. Eaton DC, Helms MN, Koval M, Bao HF, Jain L (2009) The contribution of epithelial sodium channels to alveolar function in health and disease. Annu Rev Physiol 71:403-423
44. Ecelbarger CA, Tiwari S (2006) Sodium transporters in the distal nephron and disease implications. Curr Hypertens Rep 8:158-165
45. Edelheit O, Hanukoglu I, Gizewska M, Kandemir N, Tenenbaum-Rakover Y, Yurdakok M, Zajaczek S, Hanukoglu A (2005) Novel mutations in epithelial sodium channel (ENaC) subunit genes and phenotypic expression of multisystem pseudohypoaldosteronism. Clin Endocrinol 62:547-553
46. Egnell P, Flock JI (1992) The autocatalytic processing of the subtilisin Carlsberg pro-region is independent of the primary structure of the cleavage site. Mol Microbiol 6:1115-1119
47. Elizur A, Cannon CL, Ferkol TW (2008) Airway inflammation in cystic fibrosis. Chest 133:489-495
48. Engel LS, Hobden JA, Moreau JM, Callegan MC, Hill JM, O'Callaghan RJ (1997) Pseudomonas deficient in protease IV has significantly reduced corneal virulence. Invest Ophthalmol Vis Sci 38:1535-1542
49. Engel LS, Hill JM, Caballero AR, Green LC, O'Callaghan RJ (1998) Protease IV, a unique extracellular protease and virulence factor from Pseudomonas aeruginosa. J Biol Chem 273:16792-16797
50. Erez E, Fass D, Bibi E (2009) How intramembrane proteases bury hydrolytic reactions in the membrane. Nature 459:371-378
51. Ergonul Z, Frindt G, Palmer LG (2006) Regulation of maturation and processing of ENaC subunits in the rat kidney. Am J Physiol Renal Physiol 291:F683-F693
52. Fleiszig SM, Evans DJ, Do N, Vallas V, Shin S, Mostov KE (1997) Epithelial cell polarity affects susceptibility to Pseudomonas aeruginosa invasion and cytotoxicity. Infect Immun 65:2861-2867
53. Freundlich M, Ludwig M (2005) A novel epithelial sodium channel beta-subunit mutation associated with hypertensive Liddle syndrome. Pediatr Nephrol 20:512-515
54. Fritz LC, Haidar MA, Arfsten AE, Schilling JW, Carilli C, Shine J, Baxter JD, Reudelhuber TL (1987) Human renin is correctly processed and targeted to the regulated secretory pathway in mouse pituitary AtT-20 cells. J Biol Chem 262:12409-12412
55. Gaillard EA, Kota P, Gentzsch M, Dokholyan NV, Stutts MJ, Tarran R (2010) Regulation of the epithelial Na+ channel and airway surface liquid volume by serine proteases. Pflugers Arch 460:1-17
56. Goldberg JB, Ohman DE (1987) Cloning and transcriptional regulation of the elastase lasA gene in mucoid and nonmucoid Pseudomonas aeruginosa. J Bacteriol 169:1349-1351
57. Gormley K, Dong Y, Sagnella GA (2003) Regulation of the epithelial sodium channel by accessory proteins. Biochem J 371:1-14
58. Gorogh T, Beier UH, Baumken J, Meyer JE, Hoffmann M, Gottschlich S, Maune S (2006) Metalloproteinases and their inhibitors: influence on tumor invasiveness and metastasis formation in head and neck squamous cell carcinomas. Head Neck 28:31-39
59. Granstrom M, Ericsson A, Strandvik B, Wretlind B, Pavlovskis OR, Berka R, Vasil ML (1984) Relation between antibody response to Pseudomonas aeruginosa exoproteins and colonization/infection in patients with cystic fibrosis. Acta Paediatr Scand 73:772-777
60. Gregory RJ, Cheng SH, Rich DP, Marshall J, Paul S, Hehir K, Ostedgaard L, Klinger KW, Welsh MJ, Smith AE (1990) Expression and characterization of the cystic fibrosis transmembrane conductance regulator. Nature 347:382-386
61. Griese M, Kappler M, Gaggar A, Hartl D (2008) Inhibition of airway proteases in cystic fibrosis lung disease. Eur Respir J 32:783-795
62. Guyot N, Butler MW, McNally P, Weldon S, Greene CM, Levine RL, O'Neill SJ, Taggart CC, McElvaney NG (2008) Elafin, an elastase-specific inhibitor, is cleaved by its cognate enzyme neutrophil elastase in sputum from individuals with cystic fibrosis. J Biol Chem 283:32377-32385
63. Guyot N, Bergsson G, Butler MW, Greene CM, Weldon S, Kessler E, Levine RL, O'Neill SJ, Taggart CC, McElvaney NG (2010) Functional study of elafin cleaved by Pseudomonas aeruginosa metalloproteinases. Biol Chem 391:705-716
64. Guzzo J, Murgier M, Filloux A, Lazdunski A (1990) Cloning of the Pseudomonas aeruginosa alkaline protease gene and secretion of the protease into the medium by Escherichia coli. J Bacteriol 172:942-948
65. Hamm LL, Feng Z, Hering-Smith KS (2010) Regulation of sodium transport by ENaC in the kidney. Curr Opin Nephrol Hypertens 19:98-105
66. Harris M, Garcia-Caballero A, Stutts MJ, Firsov D, Rossier BC (2008) Preferential assembly of ENaC subunits in Xenopus oocyte: role of furin-mediated endogenous proteolysis. J Biol Chem 283:7455-7463
67. Heck LW, Alarcon PG, Kulhavy RM, Morihara K, Russell MW, Mestecky JF (1990) Degradation of IgA proteins by Pseudomonas aeruginosa elastase. J Immunol 144:2253-2257
68. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425-479
69. Hobden JA (2002) Pseudomonas aeruginosa proteases and corneal virulence. DNA Cell Biol 21:391-396
70. Hopf A, Schreiber R, Mall M, Greger R, Kunzelmann K (1999) Cystic fibrosis transmembrane conductance regulator inhibits epithelial Na+ channels carrying Liddle's syndrome mutations. J Biol Chem 274:13894-13899
71. Horvat RT, Clabaugh M, Duval-Jobe C, Parmely MJ (1989) Inactivation of human gamma interferon by Pseudomonas aeruginosa proteases: elastase augments the effects of alkaline protease despite the presence of alpha 2-macroglobulin. Infect Immun 57:1668-1674
72. Huber R, Krueger B, Diakov A, Korbmacher J, Haerteis S, Einsiedel J, Gmeiner P, Azad AK, Cuppens H, Cassiman JJ, Korbmacher C, Rauh R (2010) Functional characterization of a partial loss-offunction mutation of the epithelial sodium channel (ENaC) associated with atypical cystic fibrosis. Cell Physiol Biochem 25:145-158
73. Hughey RP, Mueller GM, Bruns JB, Kinlough CL, Poland PA, Harkleroad KL, Carattino MD, Kleyman TR (2003) Maturation of the epithelial Na+ channel involves proteolytic processing of the alpha- and gamma-subunits. J Biol Chem 278:37073-37082
74. Hughey RP, Bruns JB, Kinlough CL, Harkleroad KL, Tong Q, Carattino MD, Johnson JP, Stockand JD, Kleyman TR (2004a) Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem 279:18111-18114
75. Hughey RP, Bruns JB, Kinlough CL, Kleyman TR (2004b) Distinct pools of epithelial sodium channels are expressed at the plasma membrane. J Biol Chem 279:48491-48494
76. Hughey RP, Carattino MD, Kleyman TR (2007) Role of proteolysis in the activation of epithelial sodium channels. Curr Opin Nephrol Hypertens 16:444-450
77. Hummler E (1999) Implication of ENaC in salt-sensitive hypertension. J Steroid Biochem Mol Biol 69:385-390
78. Itani OA, Chen JH, Karp PH, Ernst S, Keshavjee S, Parekh K, Klesney-Tait J, Zabner J, Welsh MJ (2011) Human cystic fibrosis airway epithelia have reduced Cl-conductance but not increased Na+ conductance. Proc Natl Acad Sci USA 108:10260-10265
79. Jagger KS, Robinson DL, Franz MN, Warren RL (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
80. Jagger KS, Bahner DR, Warren RL (1983) Protease phenotypes of Pseudomonas aeruginosa isolated from patients with cystic fibrosis. J Clin Microbiol 17:55-59
81. Ji HL, Chalfant ML, Jovov B, Lockhart JP, Parker SB, Fuller CM, Stanton BA, Benos DJ (2000) The cytosolic termini of the betaand gamma-ENaC subunits are involved in the functional interactions between cystic fibrosis transmembrane conductance regulator and epithelial sodium channel. J Biol Chem 275:27947-27956
82. Jiang Q, Li J, Dubroff R, Ahn YJ, Foskett JK, Engelhardt J, Kleyman TR (2000) Epithelial sodium channels regulate cystic fibrosis transmembrane conductance regulator chloride channels in Xenopus oocytes. J Biol Chem 275:13266-13274
83. Johnson GG, Morris JM, Berk RS (1967) The extracellular protease from Pseudomonas aeruginosa exhibiting elastase activity. Can J Microbiol 13:711-719
84. Kametaka S, Shibata M, Moroe K, Kanamori S, Ohsawa Y, Waguri S, Sims PJ, Emoto K, Umeda M, Uchiyama Y (2003) Identification of phospholipid scramblase 1 as a novel interacting molecule with beta-secretase (beta-site amyloid precursor protein (APP) cleaving enzyme (BACE)). J Biol Chem 278:15239-15245
85. Kent G, Iles R, Bear CE, Huan LJ, Griesenbach U, McKerlie C, Frndova H, Ackerley C, Gosselin D, Radzioch D, O'Brodovich H, Tsui LC, Buchwald M, Tanswell AK (1997) Lung disease in mice with cystic fibrosis. J Clin Invest 100:3060-3069
86. Kercsmar CM, Davis PB (1993) Resistance of human tracheal epithelial cells to killing by neutrophils, neutrophil elastase, and Pseudomonas elastase. Am J Respir Cell Mol Biol 8:56-62
87. Kessler E, Safrin M (1988) Partial purification and characterization of an inactive precursor of Pseudomonas aeruginosa elastase. J Bacteriol 170:1215-1219
88. Kessler E, Safrin M (1994) The propeptide of Pseudomonas aeruginosa elastase acts an elastase inhibitor. J Biol Chem 269:22726-22731
89. Kessler E, Safrin M, Olson JC, Ohman DE (1993) Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268:7503-7508
90. Kessler E, Safrin M, Gustin JK, Ohman DE (1998) Elastase and the LasA protease of Pseudomonas aeruginosa are secreted with their propeptides. J Biol Chem 273:30225-30231
91. Kharazmi A, Doring G, Hoiby N, Valerius NH (1984a) Interaction of Pseudomonas aeruginosa alkaline protease and elastase with human polymorphonuclear leukocytes in vitro. Infect Immun 43:161-165
92. Kharazmi A, Hoiby N, Doring G, Valerius NH (1984b) Pseudomonas aeruginosa exoproteases inhibit human neutrophil chemiluminescence. Infect Immun 44:587-591
93. Kleyman TR, Myerburg MM, Hughey RP (2006) Regulation of ENaCs by proteases: an increasingly complex story. Kidney Int 70:1391-1392
94. Kleyman TR, Carattino MD, Hughey RP (2009) ENaC at the cutting edge: regulation of epithelial sodium channels by proteases. J Biol Chem 284:20447-20451
95. Ko SB, Shcheynikov N, Choi JY, Luo X, Ishibashi K, Thomas PJ, Kim JY, Kim KH, Lee MG, Naruse S, Muallem S (2002) A molecular mechanism for aberrant CFTR-dependent HCO3- transport in cystic fibrosis. EMBO J 21:5662-5672
96. Kobayashi H (2005) Airway biofilms: implications for pathogenesis and therapy of respiratory tract infections. Treat Respir Med 4:241-253
97. Kudoh I, Wiener-Kronish JP, Hashimoto S, Pittet JF, Frank D (1994) Exoproduct secretions of Pseudomonas aeruginosa strains influence severity of alveolar epithelial injury. Am J Physiol 267:L551-L556
98. Kunzelmann K, Kiser GL, Schreiber R, Riordan JR (1997) Inhibition of epithelial Na+ currents by intracellular domains of the cystic fibrosis transmembrane conductance regulator. FEBS Lett 400:341-344
99. Lang F, Huang DY, Vallon V (2010) SGK, renal function and hypertension. J Nephrol 23 (Suppl 16):S124-S129
100. Lazdunski A, Guzzo J, Filloux A, Bally M, Murgier M (1990) Secretion of extracellular proteins by Pseudomonas aeruginosa. Biochimie 72:147-156
101. Lee B, Schjerling CK, Kirkby N, Hoffmann N, Borup R, Molin S, Hoiby N, Ciofu O (2011) Mucoid Pseudomonas aeruginosa isolates maintain the biofilm formation capacity and the gene expression profiles during the chronic lung infection of CF patients. APMIS 119:263-274
102. Leidal KG, Munson KL, Johnson MC, Denning GM (2003) Metalloproteases from Pseudomonas aeruginosa degrade human RANTES, MCP-1, and ENA-78. J Interferon Cytokine Res 23:307-318
103. Levene PA (1905) The cleavage of products of proteoses. J Biol Chem 1:45-58
104. Li J, Wang DH (2007) Function and regulation of epithelial sodium transporters in the kidney of a salt-sensitive hypertensive rat model. J Hypertens 25:1065-1072
105. Liu L, Hering-Smith KS, Schiro FR, Hamm LL (2002) Serine protease activity in m-1 cortical collecting duct cells. Hypertension 39:860-864
106. Lopez-Otin C, Bond JS (2008) Proteases: multifunctional enzymes in life and disease. J Biol Chem 283:30433-30437
107. Lopez-Otin C, Matrisian LM (2007) Emerging roles of proteases in tumour suppression. Nat Rev Cancer 7:800-808
108. Louis D, Bernillon J, Wallach JM (1998) Specificity of Pseudomonas aeruginosa serralysin revisited, using biologically active peptides as substrates. Biochim Biophys Acta 1387:378-386
109. Lyczak JB, Cannon CL, Pier GB (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2:1051-1060
110. Lyczak JB, Cannon CL, Pier GB (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15:194-222
111. Mall MA (2008) Role of cilia, mucus, and airway surface liquid in mucociliary dysfunction: lessons from mouse models. J Aerosol Med Pulm Drug Deliv 21:13-24
112. Mall M, Bleich M, Kuehr J, Brandis M, Greger R, Kunzelmann K (1999) CFTR-mediated inhibition of epithelial Na+ conductance in human colon is defective in cystic fibrosis. Am J Physiol 277: G709-G716
113. Mall M, Grubb BR, Harkema JR, O'Neal WK, Boucher RC (2004) Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat Med 10:487-493
114. Malloy JL, Veldhuizen RA, Thibodeaux BA, O'Callaghan RJ, Wright JR (2005) Pseudomonas aeruginosa protease IV degrades surfactant proteins and inhibits surfactant host defense and biophysical functions. Am J Physiol Lung Cell Mol Physiol 288:L409-L418
115. Manos J, Arthur J, Rose B, Tingpej P, Fung C, Curtis M, Webb JS, Hu H, Kjelleberg S, Gorrell MD, Bye P, Harbour C (2008) Transcriptome analyses and biofilm-forming characteristics of a clonal seudomonas aeruginosa from the cystic fibrosis lung. J Med Microbiol 57:1454-1465
116. Manos J, Arthur J, Rose B, Bell S, Tingpej P, Hu H, Webb J, Kjelleberg S, Gorrell MD, Bye P, Harbour C (2009) Gene expression characteristics of a cystic fibrosis epidemic strain of Pseudomonas aeruginosa during biofilm and planktonic growth. FEMS Microbiol Lett 292:107-114
117. Mariencheck WI, Alcorn JF, Palmer SM, Wright JR (2003) Pseudomonas aeruginosa elastase degrades surfactant proteins A and D. Am J Respir Cell Mol Biol 28:528-537
118. Marino CR, Matovcik LM, Gorelick FS, Cohn JA (1991) Localization of the cystic fibrosis transmembrane conductance regulator in pancreas. J Clin Invest 88:712-716
119. Matthay MA, Robriquet L, Fang X (2005) Alveolar epithelium: role in lung fluid balance and acute lung injury. Proc Am Thorac Soc 2:206-213
120. Mirghomizadeh F, Bullwinkel J, Orinska Z, Janssen O, Petersen A, Singh PB, Bulfone-Paus S (2009) Transcriptional regulation of mouse mast cell protease-2 by interleukin-15. J Biol Chem 284:32635-32641
121. Mossessova E, Lima CD (2000) Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell 5:865-876
122. Muzio M, Salvesen GS, Dixit VM (1997) FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J Biol Chem 272:2952-2956
123. Myerburg MM, Butterworth MB, McKenna EE, Peters KW, Frizzell RA, Kleyman TR, Pilewski JM (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
124. Myerburg MM, Harvey PR, Heidrich EM, Pilewski JM, Butterworth MB (2010) Acute regulation of the epithelial sodium channel in airway epithelia by proteases and trafficking. Am J Respir Cell Mol Biol 43:712-719
125. O'Callaghan RJ, Engel LS, Hobden JA, Callegan MC, Green LC, Hill JM (1996) Pseudomonas keratitis. The role of an uncharacterized exoprotein, protease IV, in corneal virulence. Invest Ophthalmol Vis Sci 37:534-543
126. Oda K (2012) New families of carboxyl peptidases: serine-carboxyl peptidases and glutamic peptidases. J Biochem 151:13-25
127. Orce GG, Castillo GA, Margolius HS (1980) Inhibition of short-circuit current in toad urinary bladder by inhibitors of glandular kallikrein. Am J Physiol 239:F459-F465
128. Orce GG, Castillo GA, Margolius HS (1981) Kallikrein inhibitors decrease short-circuit current by inhibiting sodium uptake. Hypertension 3:92-95
129. Overall CM, Tam EM, Kappelhoff R, Connor A, Ewart T, Morrison CJ, Puente X, Lopez-Otin C, Seth A (2004) Protease degradomics: mass spectrometry discovery of protease substrates and the CLIP-CHIP, a dedicated DNA microarray of all human proteases and inhibitors. Biol Chem 385:493-504
130. Parmely MJ, Horvat RT (1986) Antigenic specificities of seudomonas aeruginosa alkaline protease and elastase defined by human T cell clones. J Immunol 137:988-994
131. Parmely MJ, Iglewski BH, Horvat RT (1984) Identification of the principal T lymphocyte-stimulating antigens of Pseudomonas aeruginosa. J Exp Med 160:1338-1349
132. Parmely MJ, Horvat RT, Iglewski BH, Kanarek J, Furtado D, Van Enk R (1987) The antigenicity of a pulmonary pathogen defined by monoclonal T cells. Adv Exp Med Biol 216B:1043-1051
133. Parmely M, Gale A, Clabaugh M, Horvat R, Zhou WW (1990) Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect Immun 58:3009-3014
134. Passero CJ, Mueller GM, Rondon-Berrios H, Tofovic SP, Hughey RP, Kleyman TR (2008) Plasmin activates epithelial Na+ channels by cleaving the gamma subunit. J Biol Chem 283:36586-36591
135. Planes C, Caughey GH (2007) Regulation of the epithelial Na+ channel by peptidases. Curr Top Dev Biol 78:23-46
136. Planes C, Leyvraz C, Uchida T, Angelova MA, Vuagniaux G, Hummler E, Matthay M, Clerici C, 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
137. Pochynyuk O, Tong Q, Staruschenko A, Ma HP, Stockand JD (2006) Regulation of the epithelial Na+ channel (ENaC) by phosphatidylinositides. Am J Physiol Renal Physiol 290:F949-F957
138. Puente XS, Sanchez LM, Overall CM, Lopez-Otin C (2003) Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 4:544-558
139. Quesada V, Ordonez GR, Sanchez LM, Puente XS, Lopez-Otin C (2009) The Degradome database: mammalian proteases and diseases of proteolysis. Nucleic Acids Res 37:D239-D243
140. Rauh R, Diakov A, Tzschoppe A, Korbmacher J, Azad AK, Cuppens H, Cassiman JJ, Dotsch J, Sticht H, 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
141. Ravaud S, Gouet P, Haser R, Aghajari N (2003) Probing the role of divalent metal ions in a bacterial psychrophilic metalloprotease: binding studies of an enzyme in the crystalline state by X-ray crystallography. J Bacteriol 185:4195-4203
142. Rawlings ND, Barrett AJ, Bateman A (2010) MEROPS: the peptidase database. Nucleic Acids Res 38:D227-D233
143. Rawlings ND, Barrett AJ, Bateman A (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40:D343-D350
144. Reddy MM, Quinton PM (2003) Functional interaction of CFTR and ENaC in sweat glands. Pflugers Arch 445:499-503
145. Reddy MM, Light MJ, Quinton PM (1999) Activation of the epithelial Na+ channel (ENaC) requires CFTR Cl-channel function. Nature 402:301-304
146. Reeves EP, McElvaney NG (2012) The facilitating effect of hypertonic saline on resolution of airway inflammation in cystic fibrosis. Am J Respir Crit Care Med 185:226-227
147. Rich DP, Anderson MP, Gregory RJ, Cheng SH, Paul S, Jefferson DM, McCann JD, Klinger KW, Smith AE, Welsh MJ (1990) Expression of cystic fibrosis transmembrane conductance regulator corrects defective chloride channel regulation in cystic fibrosis airway epithelial cells. Nature 347:358-363
148. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, Chou JL et al (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066-1073
149. Rollins BM, Garcia-Caballero A, Stutts MJ, Tarran R (2010) SPLUNC1 expression reduces surface levels of the epithelial sodium channel (ENaC) in Xenopus laevis oocytes. Channels (Austin) 4:255-259
150. Rossier BC (2002) Hormonal regulation of the epithelial sodium channel ENaC: N or Po? J Gen Physiol 120:67-70
151. Rossier BC (2004) The epithelial sodium channel: activation by membrane-bound serine proteases. Proc Am Thorac Soc 1:4-9
152. Rossier BC, Stutts MJ (2009) Activation of the epithelial sodium channel (ENaC) by serine proteases. Annu Rev Physiol 71:361-379
153. Rust L, Pesci EC, Iglewski BH (1996) Analysis of the Pseudomonas aeruginosa elastase (lasB) regulatory region. J Bacteriol 178:1134-1140
154. Saadane A, Soltys J, Berger M (2006) Acute Pseudomonas challenge in cystic fibrosis mice causes prolonged nuclear factor-kappa B activation, cytokine secretion, and persistent lung inflammation. J Allergy Clin Immunol 117:1163-1169
155. Sagel SD, Sontag MK, Wagener JS, Kapsner RK, Osberg I, Accurso FJ (2002) Induced sputum inflammatory measures correlate with lung function in children with cystic fibrosis. J Pediatr 141:811-817
156. Salunkhe P, Smart CH, Morgan JA, Panagea S, Walshaw MJ, Hart CA, Geffers R, Tummler B, Winstanley C (2005) A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance. J Bacteriol 187:4908-4920
157. Salvesen GS, Riedl SJ (2008) Caspase mechanisms. Adv Exp Med Biol 615:13-23
158. Sarkisova S, Patrauchan MA, Berglund D, Nivens DE, Franklin MJ (2005a) Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J Bacteriol 187:4327-4337
159. Sarkisova S, Patrauchan MA, Berglund D, Nivens DE, Franklin MJ (2005b) Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. J Bacteriol 187:4327-4337
160. Saulnier JM, Curtil FM, Duclos MC, Wallach JM (1989) Elastolytic activity of Pseudomonas aeruginosa elastase. Biochim Biophys Acta 995:285-290
161. Schafer W, Stroh A, Berghofer S, Seiler J, Vey M, Kruse ML, Kern HF, Klenk HD, Garten W (1995) Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin. EMBO J 14:2424-2435
162. Schreiber R, Hopf A, Mall M, Greger R, Kunzelmann K (1999) The first-nucleotide binding domain of the cystic-fibrosis transmembrane conductance regulator is important for inhibition of the epithelial Na+ channel. Proc Natl Acad Sci USA 96:5310-5315
163. Sheng S, Carattino MD, Bruns JB, Hughey RP, Kleyman TR (2006) Furin cleavage activates the epithelialNa+ channels by relievingNa+ self-inhibition. Am J Physiol Renal Physiol 290:F1488-F1496
164. Song HK, Bochtler M, Azim MK, Hartmann C, Huber R, Ramachandran R (2003) Isolation and characterization of the prokaryotic proteasome homolog HslVU (ClpQY) fromThermotoga maritima and the crystal structure of HslV. Biophys Chem 100:437-452
165. Studholme DJ, Rawlings ND, Barrett AJ, Bateman A (2003) A comparison of Pfam and MEROPS: two databases, one comprehensive, and one specialised. BMC Bioinformatics 4:17
166. Stuhrmann M, Macek M Jr, Reis A, Schmidtke J, Tummler B, Dork T, Vavrova V, Macek M, Krawczak M (1990) Genotype analysis of cystic fibrosis patients in relation to pancreatic sufficiency. Lancet 335:738-739
167. Stutts MJ, Rossier BC, Boucher RC (1997) Cystic fibrosis transmembrane conductance regulator inverts protein kinase A-mediated regulation of epithelial sodium channel single channel kinetics. J Biol Chem 272:14037-14040
168. Sun Y, Zhang JN, Zhao D, Wang QS, Gu YC, Ma HP, Zhang ZR (2011) Role of the epithelial sodium channel in salt-sensitive hypertension. Acta Pharmacol Sin 32:789-797
169. Suter S (1994) The role of bacterial proteases in the pathogenesis of cystic fibrosis. Am J Respir Crit Care Med 150:S118-S122
170. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, Banach D, Ghayur T, Brady KD, Wong WW (1997) Substrate specificities of caspase family proteases. J Biol Chem 272:9677-9682
171. Tan CD, Selvanathar IA, Baines DL (2011) Cleavage of endogenous gammaENaC and elevated abundance of alphaENaC are associated with increased Na transport in response to apical fluid volume expansion in human H441 airway epithelial cells. Pflugers Arch 462:431-441
172. Tarran R, Trout L, Donaldson SH, Boucher RC (2006) Solublemediators, not cilia, determine airway surface liquid volume in normal and cystic fibrosis superficial airway epithelia. J Gen Physiol 127:591-604
173. Terheggen-Lagro SW, Rijkers GT, Ent CK van der (2005) The role of airway epithelium and blood neutrophils in the inflammatory response in cystic fibrosis. J Cyst Fibros 4 (Suppl 2):15-23
174. Toder DS, Ferrell SJ, Nezezon JL, Rust L, Iglewski BH (1994) lasA and lasB genes of Pseudomonas aeruginosa: analysis of transcription and gene product activity. Infect Immun 62:1320-1327
175. Tomisugi Y, Unno M, Mizushima T, Morimoto Y, Tanahashi N, Tanaka K, Tsukihara T, Yasuoka N (2000) New crystal forms and low resolution structure analysis of 20 S proteasomes from bovine liver. J Biochem 127:941-943
176. Tomlin KL, Coll OP, Ceri H (2001) Interspecies biofilms of Pseudomonas aeruginosa and Burkholderia cepacia. Can J Microbiol 47:949-954
177. Tong Z, Illek B, Bhagwandin VJ, Verghese GM, Caughey GH (2004) Prostasin, a membrane-anchored serine peptidase, regulates sodium currents in JME/CF15 cells, a cystic fibrosis airway epithelial cell line. Am J Physiol Lung Cell Mol Physiol 287:L928-L935
178. Unno M, Mizushima T, Morimoto Y, Tomisugi Y, Tanaka K, Yasuoka N, Tsukihara T (2002) The structure of the mammalian 20 S proteasome at 2.75 Å resolution. Structure 10:609-618
179. Uss RH, Fenton JW 2nd, Muraschi TF, Miller KD (1969) Two distinct elastases from different strains of Pseudomonas aeruginosa. Biochim Biophys Acta 191:179-181
180. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC (1997) An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389:607-610
181. Voynow JA, Fischer BM, Zheng S (2008) Proteases and cystic fibrosis. Int J Biochem Cell Biol 40:1238-1245
182. Vuagniaux G, Vallet V, Jaeger NF, Pfister C, Bens M, Farman N, Courtois-Coutry N, Vandewalle A, Rossier BC, Hummler E (2000) Activation of the amiloride-sensitive epithelial sodium channel by the serine protease mCAP1 expressed in a mouse cortical collecting duct cell line. J Am Soc Nephrol 11:828-834
183. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC (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
184. Wagner CA, Loffing-Cueni D, Yan Q, Schulz N, Fakitsas P, Carrel M, Wang T, Verrey F, Geibel JP, Giebisch G, Hebert SC, Loffing J (2008) Mouse model of type II Bartter's syndrome. II. Altered expression of renal sodium- and water-transporting proteins. Am J Physiol Ren Physiol 294:F1373-F1380
185. Wiener-Kronish JP, Sakuma T, Kudoh I, Pittet JF, Frank D, Dobbs L, Vasil ML, Matthay MA (1993) Alveolar epithelial injury and pleural empyema in acute P. aeruginosa pneumonia in anesthetized rabbits. J Appl Physiol 75:1661-1669
186. Wynn TA (2008) Cellular and molecular mechanisms of fibrosis. J Pathol 214:199-210
187. Zhang L, Conway JF, Thibodeau PH (2012) Calcium-induced folding and stabilization of the Pseudomonas aeruginosa alkaline protease. J Biol Chem 287:4311-4322
188. Zhou Z, Duerr J, Johannesson B, Schubert SC, Treis D, Harm M, Graeber SY, Dalpke A, Schultz C, Mall MA (2011) The ENaCoverexpressing mouse as a model of cystic fibrosis lung disease. J Cyst Fibros 10 (Suppl 2):S172-S182