Trypsin can activate the epithelial sodium channel (ENaC) in microdissected mouse distal nephron

American Journal of Physiology - Renal Physiology

Volumn 295, Issue 4, 2008, Pages

  Nesterov, Viatcheslav ^a   Dahlmann, Anke ^b   Bertog, Marko ^a   Korbmacher, Christoph ^a,c  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Amiloride; Epithelial sodium transport; Microdissected renal tubules; Serine proteases; Whole cell patch clamp recording

Indexed keywords

AMILORIDE; EPITHELIAL SODIUM CHANNEL; PROTEINASE; PROTEINASE INHIBITOR; SOYBEAN TRYPSIN INHIBITOR; TRYPSIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; KIDNEY COLLECTING TUBULE; KIDNEY CORTEX; KIDNEY DISTAL TUBULE; KIDNEY TUBULE; KIDNEY TUBULE CELL; MALE; MICRODISSECTION; MOUSE; NEPHRON; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SODIUM INTAKE; SODIUM RESTRICTION; WHOLE CELL;

EID: 57049187776     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00031.2008     Document Type: Article

References (60)

1. Adachi M, Kitamura K, Miyoshi T, Narikiyo T, Iwashita K, Shiraishi N, Nonoguchi H, Tomita K. Activation of epithelial sodium channels by prostasin in Xenopus oocytes. J Am Soc Nephrol 12: 1114-1121, 2001.
2. + transport. J Gen Physiol 130: 611-629, 2007.
3. + channel by trypsin. J Biol Chem 282: 26884-26896, 2007.
4. Bertog M, Cuffe JE, Pradervand S, Hummler E, Hartner A, Porst M, Hilgers KF, Rossier BC, Korbmacher C. Aldosterone responsiveness of the epithelial sodium channel (ENaC) in colon is increased in a mouse model for Liddle's syndrome. J Physiol 586: 459-475, 2008.
5. Bize V, Horisberger JD. Sodium self-inhibition of human epithelial sodium channel: Selectivity and affinity of the extracellular sodium sensing site. Am J Physiol Renal Physiol 293: F1137-F1146, 2007.
6. + transport in normal and CF human bronchial epithelial cells is inhibited by BAY 39-9437. Am J Physiol Lung Cell Mol Physiol 281: L16-L23, 2001.
7. + channels are fully activated by furin- and prostasin-dependent release of an inhibitory peptide from the gamma subunit. J Biol Chem 282: 6153-6160, 2007.
8. + transport. Am J Physiol Lung Cell Mol Physiol 288: L813-L819, 2005.
9. + channels. Am J Physiol Cell Physiol 286: C190-C194, 2004.
10. + channel is inhibited by a peptide derived from proteolytic processing of its alpha subunit. J Biol Chem 281: 18901-18907, 2006.
11. Chraibi A, Vallet V, Firsov D, Hess SK, Horisberger JD. Protease modulation of the activity of the epithelial sodium channel expressed in Xenopus oocytes. J Gen Physiol 111: 127-138, 1998.
12. + channels is maintained in a mouse model of Liddle's syndrome. Am J Physiol Renal Physiol 285: F310-F318, 2003.
13. Diakov A, Bera K, Mokrushina M, Krueger B, Korbmacher C. Cleavage in the γ-subunit of the epithelial sodium channel (ENaC) plays an important role in proteolytic activation of near-silent channels. J Physiol. In press.
14. Donaldson SH, Hirsh A, Li DC, Holloway G, Chao J, Boucher RC, Gabriel SE. Regulation of the epithelial sodium channel by serine proteases in human airways. J Biol Chem 277: 8338-8345, 2002.
15. Ergonul Z, Frindt G, Palmer LG. Regulation of maturation and processing of ENaC subunits in the rat kidney. Am J Physiol Renal Physiol 291: F683-F693, 2006.
16. Friis UG, Jensen BL, Jensen ON, Skott O. Activation of epithelial sodium channels by urinary plasmin contributes to NaCl retention in nephrotic syndrome (Abstract). J Am Soc Nephrol 17: 56A (F-FC094), 2006.
17. Frindt G, Ergonul Z, Palmer LG. Surface expression of epithelial Na channel protein in rat kidney. J Gen Physiol 131: 617-627, 2008.
18. Frindt G, Masilamani S, Knepper MA, Palmer LG. Activation of epithelial Na channels during short-term Na deprivation. Am J Physiol Renal Physiol 280: F112-F118, 2001.
19. Frindt G, Palmer LG. Na channels in the rat connecting tubule. Am J Physiol Renal Physiol 286: F669-F674, 2004.
20. Frindt G, Sackin H, Palmer LG. Whole-cell currents in rat cortical collecting tubule: low-Na diet increases amiloride-sensitive conductance. Am J Physiol Renal Fluid Electrolyte Physiol 258: F562-F567, 1990.
21. Garty H, Palmer LG. Epithelial sodium channels: function, structure, and regulation. Physiol Rev 77: 359-396, 1997.
22. Hamill P, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85-100, 1981.
23. Harris M, Firsov D, Vuagniaux G, Stutts MJ, Rossier BC. A novel neutrophil elastase inhibitor prevents elastase activation and surface cleavage of the epithelial sodium channel expressed in Xenopus laevis oocytes. J Biol Chem 282: 58-64, 2007.
24. Hu Y, Webb E, Singh J, Morgan BA, Gainor JA, Gordon TD, Siahaan TJ. Rapid determination of substrate specificity of clostridium histolyticum beta-collagenase using an immobilized peptide library. J Biol Chem 277: 8366-8371, 2002.
25. Hughey RP, Bruns JB, Kinlough CL, Harkleroad KL, Tong Q, Carattino MD, Johnson JP, Stockand JD, Kleyman TR. Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem 279: 18111-18114, 2004.
26. Hughey RP, Bruns JB, Kinlough CL, Kleyman TR. Distinct pools of epithelial sodium channels are expressed at the plasma membrane. J Biol Chem 279: 48491-48494, 2004.
27. Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 449: 316-323, 2007.
28. 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.
29. Kleyman TR, Myerburg MM, Hughey RP. Regulation of ENaCs by proteases: an increasingly complex story. Kidney Int 70: 1391-1392, 2006.
30. Korbmacher C, Segal AS, Fejes-Tóth G, Giebisch G, Boulpaep EL. Whole-cell currents in single and confluent M-1 mouse cortical collecting duct cells. J Gen Physiol 102: 761-793, 1993.
31. Letz B, Ackermann A, Canessa CM, Rossier BC, Korbmacher C. Amiloride-sensitive sodium channels in confluent M-1 mouse cortical collecting duct cells. J Membr Biol 148: 127-141, 1995.
32. + channels in mouse CCD cells. Am J Physiol Cell Physiol 272: C657-C666, 1997.
33. Liu L, Hering-Smith KS, Schiro FR, Hamm LL. Serine protease activity in M-1 cortical collecting duct cells. Hypertension 39: 860-864, 2002.
34. Lourdel S, Loffing J, Favre G, Paulais M, Nissant A, Fakitsas P, Creminon C, Feraille E, Verrey F, Teulon J, Doucet A, Deschenes G. Hyperaldosteronemia and activation of the epithelial sodium channel are not required for sodium retention in puromycin-induced nephrosis. J Am Soc Nephrol 16: 3642-3650, 2005.
35. Masilamani S, Kim GH, Mitchell C, Wade JB, Knepper MA. Aldosterone-mediated regulation of ENaC alpha, beta, and gamma subunit proteins in rat kidney. J Clin Invest 104: R19-R23, 1999.
36. Morimoto T, Liu W, Woda C, Carattino MD, Wei Y, Hughey RP, Apodaca G, Satlin LM, Kleyman TR. Mechanism underlying flow stimulation of sodium absorption in the mammalian collecting duct. Am J Physiol Renal Physiol 291: F663-F669, 2006.
37. Nakhoul NL, Hering-Smith KS, Gambala CT, Hamm LL. Regulation of sodium transport in M-1 cells. Am J Physiol Renal Physiol 275: F998-F1007, 1998.
38. Narikiyo T, Kitamura K, Adachi M, Miyoshi T, Iwashita K, Shiraishi N, Nonoguchi H, Chen LM, Chai KX, Chao J, Tomita K. Regulation of prostasin by aldosterone in the kidney. J Clin Invest 109: 401-408, 2002.
39. Oda T, Hotta O, Taguma Y, Kitamura H, Sudo K, Horigome I, Chiba S, Yoshizawa N, Nagura H. Involvement of neutrophil elastase in crescentic glomerulonephritis. Hum Pathol 28: 720-728, 1997.
40. Olivieri O, Castagna A, Guarini P, Chiecchi L, Sabaini G, Pizzolo F, Corrocher R, Righetti PG. Urinary prostasin: a candidate marker of epithelial sodium channel activation in humans. Hypertension 46: 683-688, 2005.
41. Passero CJ, Rondon-Berrios H, Hughey RP, Kleyman TR. Plasmin activates the epithelial sodium channel (Abstract). J Am Soc Nephrol 18: F-PO051, 2007.
42. Picard N, Eladari D, El Moghrabi S, Planes C, Bourgeois S, Houillier P, Wang Q, Burnier M, Deschenes G, Knepper MA, Meneton P, Chambrey R. Defective ENaC processing and function in tissue-kallikrein deficient mice. J Biol Chem 283: 4602-4611, 2008.
43. + channel by peptidases. Curr Top Dev Biol 78: 23-46, 2007.
44. Planes C, Leyvraz C, Uchida T, Angelova MA, Vuagniaux G, Hummler E, Matthay M, Clerici C, Rossier B. 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, 2005.
45. Rossier BC. The epithelial sodium channel: activation by membrane-bound serine proteases. Proc Am Thorac Soc 1: 4-9, 2004.
46. 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.
47. + self-inhibition. Am J Physiol Renal Physiol 290: F1488-F1496, 2006.
48. Steinbrink DR, Bond MD, Van Wart HE. Substrate specificity of beta-collagenase from clostridium histolyticum. J Biol Chem 260: 2771-2776, 1985.
49. Stoos BA, Náray-Fejes-Tóth A, Carretero OA, Ito S, Fejes-Tóth G. Characterization of a mouse cortical collecting duct cell line. Kidney Int 39: 1168-1175, 1991.
50. Sugrue RJ, Brown C, Brown G, Aitken J, Mc LRHW. Furin cleavage of the respiratory syncytial virus fusion protein is not a requirement for its transport to the surface of virus-infected cells. J Gen Virol 82: 1375-1386, 2001.
51. Svenningsen P, Jensen BL, Skott O. Plasmin stimulates the epithelial sodium channel via interaction with prostasin (Abstract). J Am Soc Nephrol 18: SA-FC019, 2007.
52. Thomas G. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat Rev Mol Cell Biol 3: 753-766, 2002.
53. Tong Z, Illek B, Bhagwandin VJ, Verghese GM, Caughey GH. 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, 2004.
54. Vallet V, Chraibi A, Gaeggeler HP, Horisberger JD, Rossier BC. An epithelial serine protease activates the amiloride-sensitive sodium channel. Nature 389: 607-610, 1997.
55. Vallet V, Pfister C, Loffing J, Rossier BC. Cell-surface expression of the channel activating protease xCAP-1 is required for activation of ENaC in the Xenopus oocyte. J Am Soc Nephrol 13: 588-594, 2002.
56. +-channel (ENaC) by reducing the rate of channel retrieval. Pflügers Arch 447: 884-894, 2004.
57. Vuagniaux G, Vallet V, Jaeger NF, Hummler E, Rossier BC. 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, 2002.
58. Vuagniaux G, Vallet V, Jaeger NF, Pfister C, Bens M, Farman N, Courtois-Coutry N, Vandewalle A, Rossier BC, Hummler E. 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, 2000.
59. Wakida N, Kitamura K, Tuyen DG, Maekawa A, Miyoshi T, Adachi M, Shiraishi N, Ko T, Ha V, Nonoguchi H, Tomita K. Inhibition of prostasin-induced ENaC activities by PN-1 and regulation of PN-1 expression by TGF-β1 and aldosterone. Kidney Int 70: 1432-1438, 2006.
60. Yagil C, Hubner N, Monti J, Schulz H, Sapojnikov M, Luft FC, Ganten D, Yagil Y. Identification of hypertension-related genes through an integrated genomic-transcriptomic approach. Circ Res 96: 617-625, 2005.