Regulation of epithelial sodium channels in urokinase plasminogen activator deficiency

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 307, Issue 8, 2014, Pages L609-L617

  Chen, Zaixing ^a,b   Zhao, Runzhen ^a   Zhao, Meimi ^a,b   Liang, Xinrong ^a   Bhattarai, Deepa ^a   Dhiman, Rohan ^a   Shetty, Sreerama ^a   Idell, Steven ^a,c   Ji, Hong Long ^a  

^a UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

^b China Medical University   (Japan)

^c Baylor UT Houston Center for AIDS Research   (United States)

Author keywords

Airway surface fluid; Epithelial sodium channel; Knockout; Mouse tracheal epithelial cells; Proteolysis; Short circuit current; Urokinase

Indexed keywords

BENZAMIL; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL SODIUM CHANNEL; MITOGEN ACTIVATED PROTEIN KINASE 1; PLASMIN; PROTEIN KINASE B; UROKINASE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); SMALL INTERFERING RNA;

ANIMAL CELL; APICAL MEMBRANE; APOPTOSIS; ARTICLE; BASOLATERAL MEMBRANE; CELL SURVIVAL; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; FEMALE; HOMEOSTASIS; IMMUNOBLOTTING; INFLAMMATION; MALE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REGULATORY MECHANISM; UROKINASE PLASMINOGEN ACTIVATOR DEFICIENCY; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CHEMISTRY; CYTOLOGY; GENETICS; ION TRANSPORT; KNOCKOUT MOUSE; LUNG ALVEOLUS; METABOLISM; OOCYTE; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRACHEA; XENOPUS LAEVIS;

ANIMALS; APOPTOSIS; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; EPITHELIAL CELLS; EPITHELIAL SODIUM CHANNELS; IMMUNOBLOTTING; ION TRANSPORT; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OOCYTES; PHOSPHORYLATION; PROTEOLYSIS; PULMONARY ALVEOLI; RNA, SMALL INTERFERING; SODIUM-POTASSIUM-EXCHANGING ATPASE; TRACHEA; UROKINASE-TYPE PLASMINOGEN ACTIVATOR; XENOPUS LAEVIS;

EID: 84908066622     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00126.2014     Document Type: Article

References (84)

1. Ahn YJ, Brooker DR, Kosari F, Harte BJ, Li J, Mackler SA, Kleyman TR. Cloning and functional expression of the mouse epithelial sodium channel. Am J Physiol Renal Physiol 277: F121-F129, 1999.
2. Angelici E, Contini C, Spezzano M, Romani R, Carfagna P, Serra P, Canipari R. Plasminogen activator production in a rat model of Pneumocystis carinii pneumonia. Microbiol Immunol 45: 605-611, 2001.
3. Arteaga MF, Canessa CM. Functional specificity of Sgk1 and Akt1 on ENaC activity. Am J Physiol Renal Physiol 289: F90-F96, 2005.
4. Barazzone C, Belin D, Piguet PF, Vassalli JD, Sappino AP. Plasminogen activator inhibitor-1 in acute hyperoxic mouse lung injury. J Clin Invest 98: 2666-2673, 1996.
5. Barker PM, Nguyen MS, Gatzy JT, Grubb B, Norman H, Hummler E, Rossier B, Boucher RC, Koller B. Role of ENaC subunit in lung liquid clearance and electrolyte balance in newborn mice. Insights into perinatal adaptation and pseudohypoaldosteronism. J Clin Invest 102: 1634-1640, 1998.
6. Beck JM, Preston AM, Gyetko MR. Urokinase-type plasminogen activator in inflammatory cell recruitment and host defense against Pneumocystis carinii in mice. Infect Immun 67: 879-884, 1999.
7. Benos DJ, Stanton BA. Functional domains within the degenerin/epithelial sodium channel (Deg/ENaC) superfamily of ion channels. J Physiol 520: 631-644, 1999.
8. Bertozzi P, Astedt B, Zenzius L, Lynch K, LeMaire F, Zapol W, Chapman HA, Jr. Depressed bronchoalveolar urokinase activity in patients with adult respiratory distress syndrome. N Engl J Med 322: 890-897, 1990.
9. Booth RE, Stockand JD. Targeted degradation of ENaC in response to PKC activation of the ERK1/2 cascade. Am J Physiol Renal Physiol 284: F938-F947, 2003.
10. Bove PF, Grubb BR, Okada SF, Ribeiro CM, Rogers TD, Randell SH, O’Neal WK, Boucher RC. Human alveolar type II cells secrete and absorb liquid in response to local nucleotide signaling. J Biol Chem 285: 34939-34949, 2010.
11. Bruns JB, Carattino MD, Sheng S, Maarouf AB, Weisz OA, Pilewski JM, Hughey RP, Kleyman TR. 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, 2007.
12. Canessa CM, Schild L, Buell G, Thorens B, Gautschi I, Horisberger JD, Rossier BC. Amiloride-sensitive epithelial Na channel is made of three homologous subunits. Nature 367: 463-467, 1994.
13. Chen L, Song W, Davis IC, Shrestha K, Schwiebert E, Sullender WM, Matalon S. Inhibition of Na transport in lung epithelial cells by respiratory syncytial virus infection. Am J Respir Cell Mol Biol 40: 588-600, 2009.
14. Drapkin PT, O’Riordan CR, Yi SM, Chiorini JA, Cardella J, Zabner J, Welsh MJ. Targeting the urokinase plasminogen activator receptor enhances gene transfer to human airway epithelia. J Clin Invest 105: 589-596, 2000.
15. Du A, Zhao B, Yin D, Zhang S, Miao J. Safrole oxide induces apoptosis by activating caspase-3,-8, and-9 in A549 human lung cancer cells. Bioorg Med Chem Lett 16: 81-83, 2006.
16. Du B, Leung H, Khan KM, Miller CG, Subbaramaiah K, Falcone DJ, Dannenberg AJ. Tobacco smoke induces urokinase-type plasminogen activator and cell invasiveness: evidence for an epidermal growth factor receptor dependent mechanism. Cancer Res 67: 8966-8972, 2007.
17. Eaton DC, Chen J, Ramosevac S, Matalon S, Jain L. Regulation of Na channels in lung alveolar type II epithelial cells. Proc Am Thorac Soc 1: 10-16, 2004.
18. Egli M, Duplain H, Lepori M, Cook S, Nicod P, Hummler E, Sartori C, Scherrer U. Defective respiratory amiloride-sensitive sodium transport predisposes to pulmonary oedema and delays its resolution in mice. J Physiol 560: 857-865, 2004.
19. Fang X, Song Y, Hirsch J, Galietta LJ, Pedemonte N, Zemans RL, Dolganov G, Verkman AS, Matthay MA. Contribution of CFTR to apical-basolateral fluid transport in cultured human alveolar epithelial type II cells. Am J Physiol Lung Cell Mol Physiol 290: L242-L249, 2006.
20. Garcia-Caballero A, Dang Y, He H, Stutts MJ. ENaC proteolytic regulation by channel-activating protease 2. J Gen Physiol 132: 521-535, 2008.
21. Gyetko MR, Sud S, Chen GH, Fuller JA, Chensue SW, Toews GB. Urokinase-type plasminogen activator is required for the generation of a type 1 immune response to pulmonary Cryptococcus neoformans infection. J Immunol 168: 801-809, 2002.
22. Haerteis S, Krappitz M, Diakov A, Krappitz A, Rauh R, Korbmacher C. Plasmin and chymotrypsin have distinct preferences for channel activating cleavage sites in the gamma subunit of the human epithelial sodium channel. J Gen Physiol 140: 375-389, 2012.
23. Han DY, Nie HG, Gu X, Nayak RC, Su XF, Fu J, Chang Y, Rao V, Ji HL. K channel openers restore verapamil-inhibited lung fluid resolution and transepithelial ion transport. Respir Res 11: 65, 2010.
24. Hildenbrand R, Gandhari M, Stroebel P, Marx A, Allgayer H, Arens N. The urokinase-system - role of cell proliferation and apoptosis. Histol Histopathol 23: 227-236, 2008.
25. Hobbs CA, Da Tan C, Tarran R. Does epithelial sodium channel hyperactivity contribute to cystic fibrosis lung disease? J Physiol 591: 4377-4387, 2013.
26. Hughey RP, Mueller GM, Bruns JB, Kinlough CL, Poland PA, Harkleroad KL, Carattino MD, Kleyman TR. Maturation of the epithelial Na channel involves proteolytic processing of the alpha- and gamma-subunits. J Biol Chem 278: 37073-37082, 2003.
27. Hummler E, Barker P, Gatzy J, Beermann F, Verdumo C, Schmidt A, Boucher R, Rossier BC. Early death due to defective neonatal lung liquid clearance in ENaC-deficient mice. Nat Genet 12: 325-328, 1996.
28. Hummler E, Planes C. Importance of ENaC-mediated sodium transport in alveolar fluid clearance using genetically-engineered mice. Cell Physiol Biochem 25: 63-70, 2010.
29. Idell S. Coagulation, fibrinolysis, and fibrin deposition in acute lung injury. Crit Care Med 31: S213-S220, 2003.
30. Idell S. The matrix unloaded: aerosolized heparin or urokinase for pulmonary fibrosis. Am J Respir Crit Care Med 168: 1268-1269, 2003.
31. Idell S, Girard W, Koenig KB, McLarty J, Fair DS. Abnormalities of pathways of fibrin turnover in the human pleural space. Am Rev Respir Dis 144: 187-194, 1991.
32. Idell S, James KK, Levin EG, Schwartz BS, Manchanda N, Maunder RJ, Martin TR, McLarty J, Fair DS. Local abnormalities in coagulation and fibrinolytic pathways predispose to alveolar fibrin deposition in the adult respiratory distress syndrome. J Clin Invest 84: 695-705, 1989.
33. Idell S, Mazar A, Cines D, Kuo A, Parry G, Gawlak S, Juarez J, Koenig K, Azghani A, Hadden W, McLarty J, Miller E. Single-chain urokinase alone or complexed to its receptor in tetracycline-induced pleuritis in rabbits. Am J Respir Crit Care Med 166: 920-926, 2002.
34. Ji HL, Parker S, Langloh AL, Fuller CM, Benos DJ. Point mutations in the post-M2 region of human-ENaC regulate cation selectivity. Am J Physiol Cell Physiol 281: C64-C74, 2001.
35. Kashlan OB, Kleyman TR. ENaC structure and function in the wake of a resolved structure of a family member. Am J Physiol Renal Physiol 301: F684-F696, 2011.
36. Kellenberger S, Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 82: 735-767, 2002.
37. Kleyman TR, Carattino MD, Hughey RP. ENaC at the cutting edge: regulation of epithelial sodium channels by proteases. J Biol Chem 284: 20447-20451, 2009.
38. Kleyman TR, Sheng S, Kosari F, Kieber-Emmons T. Mechanism of action of amiloride: a molecular prospective. Semin Nephrol 19: 524-532, 1999.
39. Koren HS, Hatch GE, Graham DE. Nasal lavage as a tool in assessing acute inflammation in response to inhaled pollutants. Toxicology 60: 15-25, 1990.
40. Kuramoto E, Nishiuma T, Kobayashi K, Yamamoto M, Kono Y, Funada Y, Kotani Y, Sisson TH, Simon RH, Nishimura Y. Inhalation of urokinase-type plasminogen activator reduces airway remodeling in a murine asthma model. Am J Physiol Lung Cell Mol Physiol 296: L337-L346, 2009.
41. Lardot C, Delos M, Lison D. Upregulation of urokinase in alveolar macrophages and lung tissue in response to silica particles. Am J Physiol Lung Cell Mol Physiol 274: L1040-L1048, 1998.
42. Lardot CG, Huaux FA, Broeckaert FR, Declerck PJ, Delos M, Fubini B, Lison DF. Role of urokinase in the fibrogenic response of the lung to mineral particles. Am J Respir Crit Care Med 157: 617-628, 1998.
43. Lazrak A, Chen L, Jurkuvenaite A, Doran SF, Liu G, Li Q, Lancaster JR, Jr., Matalon S. Regulation of alveolar epithelial Na channels by ERK1/2 in chlorine-breathing mice. Am J Respir Cell Mol Biol 46: 342-354, 2012.
44. Lazrak A, Jurkuvenaite A, Chen L, Keeling KM, Collawn JF, Bedwell DM, Matalon S. Enhancement of alveolar epithelial sodium channel activity with decreased cystic fibrosis transmembrane conductance regulator expression in mouse lung. Am J Physiol Lung Cell Mol Physiol 301: L557-L567, 2011.
45. Lee IH, Dinudom A, Sanchez-Perez A, Kumar S, Cook DI. Akt mediates the effect of insulin on epithelial sodium channels by inhibiting Nedd4-2. J Biol Chem 282: 29866-29873, 2007.
46. Lingueglia E, Voilley N, Waldmann R, Lazdunski M, Barbry P. Expression cloning of an epithelial amiloride-sensitive Na channel. A new channel type with homologies to Caenorhabditis elegans degenerins. FEBS Lett 318: 95-99, 1993.
47. Mall M, Grubb BR, Harkema JR, O’Neal WK, Boucher RC. Increased airway epithelial Na absorption produces cystic fibrosis-like lung disease in mice. Nat Med 10: 487-493, 2004.
48. Mall MA, Button B, Johannesson B, Zhou Z, Livraghi A, Caldwell RA, Schubert SC, Schultz C, O’Neal WK, Pradervand S, Hummler E, Rossier BC, Grubb BR, Boucher RC. Airway surface liquid volume regulation determines different airway phenotypes in Liddle compared with ENaC-overexpressing mice. J Biol Chem 285: 26945-26955, 2010.
49. Mall MA, Harkema JR, Trojanek JB, Treis D, Livraghi A, Schubert S, Zhou Z, Kreda SM, Tilley SL, Hudson EJ, O’Neal WK, Boucher RC. Development of chronic bronchitis and emphysema in-epithelial Na channel-overexpressing mice. Am J Respir Crit Care Med 177: 730-742, 2008.
50. Matalon S, Lazrak A, Jain L, Eaton DC. Invited review: biophysical properties of sodium channels in lung alveolar epithelial cells. J Appl Physiol 93: 1852-1859, 2002.
51. Matalon S, O’Brodovich H. Sodium channels in alveolar epithelial cells: molecular characterization, biophysical properties, and physiological significance. Annu Rev Physiol 61: 627-661, 1999.
52. Matsuo O, Sakai T, Bando H, Okada K, Nakajima S, Takagi O, Izaki S. Plasminogen activator in bronchoalveolar fluid. Haemostasis 16: 43-50, 1986.
53. Matthay MA, Folkesson HG, Clerici C. Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 82: 569-600, 2002.
54. Matthay MA, Idell S. Update on acute lung injury and critical care medicine 2009. Am J Respir Crit Care Med 181: 1027-1032, 2010.
55. McDonald FJ, Price MP, Snyder PM, Welsh MJ. Cloning and expression of the - and -subunits of the human epithelial sodium channel. Am J Physiol Cell Physiol 268: C1157-C1163, 1995.
56. Molina R, Han DY, Su XF, Zhao RZ, Zhao M, Sharp GM, Chang Y, Ji HL. Cpt-cAMP activates human epithelial sodium channels via relieving self-inhibition. Biochim Biophys Acta 1808: 1818-1826, 2011.
57. Nie HG, Chen L, Han DY, Li J, Song WF, Wei SP, Fang XH, Gu X, Matalon S, Ji HL. Regulation of epithelial sodium channels by cGMP/ PKGII. J Physiol 587: 2663-2676, 2009.
58. Nie HG, Tucker T, Su XF, Na T, Peng JB, Smith PR, Idell S, Ji HL. Expression and regulation of epithelial Na channels by nucleotides in pleural mesothelial cells. Am J Respir Cell Mol Biol 40: 543-554, 2009.
59. Nishiuma T, Sisson TH, Subbotina N, Simon RH. Localization of plasminogen activator activity within normal and injured lungs by in situ zymography. Am J Respir Cell Mol Biol 31: 552-558, 2004.
60. Passero CJ, Mueller GM, Rondon-Berrios H, Tofovic SP, Hughey RP, Kleyman TR. Plasmin activates epithelial Na channels by cleaving the subunit. J Biol Chem 283: 36586-36591, 2008.
61. Planes C, Caughey GH. Regulation of the epithelial Na channel by peptidases. Curr Top Dev Biol 78: 23-46, 2007.
62. Prabhakaran P, Ware LB, White KE, Cross MT, Matthay MA, Olman MA. Elevated levels of plasminogen activator inhibitor-1 in pulmonary edema fluid are associated with mortality in acute lung injury. Am J Physiol Lung Cell Mol Physiol 285: L20-L28, 2003.
63. Prager GW, Mihaly J, Brunner PM, Koshelnick Y, Hoyer-Hansen G, Binder BR. Urokinase mediates endothelial cell survival via induction of the X-linked inhibitor of apoptosis protein. Blood 113: 1383-1390, 2009.
64. Randrianarison N, Clerici C, Ferreira C, Fontayne A, Pradervand S, Fowler-Jaeger N, Hummler E, Rossier BC, Planes C. Low expression of the-ENaC subunit impairs lung fluid clearance in the mouse. Am J Physiol Lung Cell Mol Physiol 294: L409-L416, 2008.
65. Randrianarison N, Escoubet B, Ferreira C, Fontayne A, Fowler-Jaeger N, Clerici C, Hummler E, Rossier BC, Planes C. Middle mutation of the epithelial sodium channel increases alveolar fluid clearance and reduces the severity of hydrostatic pulmonary oedema in mice. J Physiol 582: 777-788, 2007.
66. Rossier BC, Pradervand S, Schild L, Hummler E. Epithelial sodium channel and the control of sodium balance: interaction between genetic and environmental factors. Annu Rev Physiol 64: 877-897, 2002.
67. Rossier BC, Stutts MJ. Activation of the epithelial sodium channel (ENaC) by serine proteases. Annu Rev Physiol 71: 361-379, 2009.
68. Ruppert C, Mahavadi P, Wygrecka M, Weaver TE, Magdolen V, Idell S, Preissner KT, Seeger W, Gunther A, Markart P. Recombinant production of a hybrid plasminogen activator composed of surfactant protein B and low-molecular-weight urokinase. Thromb Haemost 100: 1185-1192, 2008.
69. Schermuly RT, Gunther A, Ermert M, Ermert L, Ghofrani HA, Weissmann N, Grimminger F, Seeger W, Walmrath D. Conebulization of surfactant and urokinase restores gas exchange in perfused lungs with alveolar fibrin formation. Am J Physiol Lung Cell Mol Physiol 280: L792-L800, 2001.
70. Sheng S, Carattino MD, Bruns JB, Hughey RP, Kleyman TR. Furin cleavage activates the epithelial Na channel by relieving Na self-inhibition. Am J Physiol Renal Physiol 290: F1488-F1496, 2006.
71. Shetty S., Bhandary YP, Marudamuthu AS, Abernathy D, Velusamy T, Starcher B, Shetty S. Regulation of airway and alveolar epithelial cell apoptosis by p53-Induced plasminogen activator inhibitor-1 during cigarette smoke exposure injury. Am J Respir Cell Mol Biol 47: 474-483, 2012.
72. Shetty S., Marudamuthu AS, Abernathy D, Shetty RS, Shetty P, Fu J, Idell S, Bhandary YP, Ji H, Liu MC, Shetty S. Regulation of urokinase expression at the posttranscription level by lung epithelial cells. Biochemistry 51: 205-213, 2012.
73. Sisson TH, Hanson KE, Subbotina N, Patwardhan A, Hattori N, Simon RH. Inducible lung-specific urokinase expression reduces fibrosis and mortality after lung injury in mice. Am J Physiol Lung Cell Mol Physiol 283: L1023-L1032, 2002.
74. Smith HW, Marshall CJ. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 11: 23-36, 2010.
75. Snyder PM, Olson DR, Kabra R, Zhou R, Steines JC. cAMP and serum and glucocorticoid-inducible kinase (SGK) regulate the epithelial Na channel through convergent phosphorylation of Nedd4-2. J Biol Chem 279: 45753-45758, 2004.
76. Soukup B, Benjamin A, Orogo-Wenn M, Walters D. Physiological effect of protein kinase C on ENaC-mediated lung liquid regulation in the adult rat lung. Am J Physiol Lung Cell Mol Physiol 302: L133-L139, 2012.
77. Stutts MJ, Rossier BC, Boucher RC. Cystic fibrosis transmembrane conductance regulator inverts protein kinase A-mediated regulation of epithelial sodium channel single channel kinetics. J Biol Chem 272: 14037-14040, 1997.
78. Svenningsen P, Uhrenholt TR, Palarasah Y, Skjodt K, Jensen BL, Skott O. Prostasin-dependent activation of epithelial Na channels by low plasmin concentrations. Am J Physiol Regul Integr Comp Physiol 297: R1733-R1741, 2009.
79. Tarran R, Button B, Picher M, Paradiso AM, Ribeiro CM, Lazarowski ER, Zhang L, Collins PL, Pickles RJ, Fredberg JJ, Boucher RC. Normal and cystic fibrosis airway surface liquid homeostasis. The effects of phasic shear stress and viral infections. J Biol Chem 280: 35751-35759, 2005.
80. Tong Q, Gamper N, Medina JL, Shapiro MS, Stockand JD. Direct activation of the epithelial Na channel by phosphatidylinositol 3,4,5-trisphosphate and phosphatidylinositol 3,4-bisphosphate produced by phosphoinositide 3-OH kinase. J Biol Chem 279: 22654-22663, 2004.
81. Tsangaris I, Tsantes A, Bonovas S, Lignos M, Kopterides P, Gialeraki A, Rapti E, Orfanos S, Dimopoulou I, Travlou A, Armaganidis A. The impact of the PAI-1 4G/5G polymorphism on the outcome of patients with ALI/ARDS. Thromb Res 123: 832-836, 2009.
82. Xie C, Jiang XH, Zhang JT, Sun TT, Dong JD, Sanders AJ, Diao RY, Wang Y, Fok KL, Tsang LL, Yu MK, Zhang XH, Chung YW, Ye L, Zhao MY, Guo JH, Xiao ZJ, Lan HY, Ng CF, Lau KM, Cai ZM, Jiang WG, Chan HC. CFTR suppresses tumor progression through miR-193b targeting urokinase plasminogen activator (uPA) in prostate cancer. Oncogene 32: 2282-2291.e1-7, 2013.
83. Yang LM, Rinke R, Korbmacher C. Stimulation of the epithelial sodium channel (ENaC) by cAMP involves putative ERK phosphorylation sites in the C termini of the channel’s - and -subunit. J Biol Chem 281: 9859-9868, 2006.
84. Zhao RZ, Nie HG, Su XF, Han DY, Lee A, Huang Y, Chang Y, Matalon S, Ji HL. Characterization of a novel splice variant of ENaC subunit in human lungs. Am J Physiol Lung Cell Mol Physiol 302: L1262-L1272, 2012.