Potential role of serine proteases in modulating renal sodium transport in vivo

Nephron - Physiology

Volumn 119, Issue 2, 2011, Pages

  Jacquillet, G ^a   Rubera, I ^b   Unwin, R J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Epithelial sodium channel; Kidney; Protease; Protease activated receptor; Renal tubule; Sodium

Indexed keywords

FURIN; GENE PRODUCT; GENE PRODUCT CAP2; GENE PRODUCT CAP3; KALLIKREIN; PLASMIN; PROSTASIN; SERINE PROTEINASE; SODIUM; UNCLASSIFIED DRUG;

BRUSH BORDER; CELL MEMBRANE PERMEABILITY; EDEMA; FLUID BALANCE; HENLE LOOP; HOMEOSTASIS; HUMAN; HYPERTENSION; IN VIVO STUDY; KIDNEY COLLECTING TUBULE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE ABSORPTION; NEPHRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TRANSPORT; REVIEW; SODIUM ABSORPTION; SODIUM TRANSPORT;

ANIMALS; BIOLOGICAL TRANSPORT; FIBRINOLYSIN; HUMANS; KIDNEY; MODELS, BIOLOGICAL; NEPHRONS; NEPHROTIC SYNDROME; PLASMINOGEN; SERINE PROTEASES; SODIUM;

EID: 81155158685     PISSN: 16602110     EISSN: 16602137     Source Type: Journal    
DOI: 10.1159/000328926     Document Type: Review

References (46)

1. Leviel F, Hubner CA, Houillier P, Morla L, El Moghrabi S, Brideau G, Hatim H, Parker MD, Kurth I, Kougioumtzes A, Sinning A, Pech V, Riemondy KA, Miller RL, Hummler E, Shull GE, Aronson PS, Doucet A, Wall SM, Chambrey R, Eladari D: The Na + -dependent chloride-bicarbonate exchanger SLC4A8 mediates an electroneutral Na + reabsorption process in the renal cortical collecting ducts of mice. J Clin Invest 2010; 120: 1627-1635.
2. Naray-Fejes-Toth A, Helms MN, Stokes JB, Fejes-Toth G: Regulation of sodium transport in mammalian collecting duct cells by aldosterone-induced kinase, SGK1: Structure/ function studies. Mol Cell Endocrinol 2004; 217: 197-202. (Pubitemid 38596644)
3. Rozansky DJ, Cornwall T, Subramanya AR, Rogers S, Yang YF, David LL, Zhu X, Yang CL, Ellison DH: Aldosterone mediates activation of the thiazide-sensitive Na-Cl cotransporter through an SGK1 and WNK4 signaling pathway. J Clin Invest 2009; 119: 2601-2612.
4. Debonneville C, Flores SY, Kamynina E, Plant PJ, Tauxe C, Thomas MA, Munster C, Chraibi A, Pratt JH, Horisberger JD, Pearce D, Loffing J, Staub O: Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na + channel cell surface expression. EMBO J 2001; 20: 7052-7059. (Pubitemid 34062297)
5. Heise CJ, Xu BE, Deaton SL, Cha SK, Cheng CJ, Earnest S, Sengupta S, Juang YC, Stippec S, Xu Y, Zhao Y, Huang CL, Cobb MH: Serum and glucocorticoid-induced kinase (SGK)-1 and the epithelial sodium channel are regulated by multiple with no lysine (WNK) family members. J Biol Chem 2010; 285: 25161-25167.
6. Diakov A, Korbmacher C: A novel pathway of epithelial sodium channel activation involves a serum- and glucocorticoid-inducible kinase consensus motif in the C terminus of the channel'sγ-subunit. J Biol Chem 2004; 279: 38134-38142. (Pubitemid 39295959)
7. Neurath H: Proteolytic enzymes, past and future. Proc Natl Acad Sci USA 1999; 96: 10962-10963. (Pubitemid 29487312)
8. 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 2002; 109: 401-408. (Pubitemid 34141814)
9. Passero CJ, Mueller GM, Rondon-Berrios H, Tofovic SP, Hughey RP, Kleyman TR: Plasmin activates epithelial Na + channels by cleaving theγ-subunit. J Biol Chem 2008; 283: 36586-36591.
10. 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 2008; 283: 4602-4611.
11. 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 2000; 11: 828-834. (Pubitemid 30241716)
12. Wang JK, Lee MS, Tseng IC, Chou FP, Chen YW, Fulton A, Lee HS, Chen CJ, Johnson MD, Lin CY: Polarized epithelial cells secrete matriptase as a consequence of zymogen activation and HAI-1-mediated inhibition. Am J Physiol Cell Physiol 2009; 297:C459-C470.
13. Girardi AC, Degray BC, Nagy T, Biemesderfer D, Aronson PS: Association of Na + -H + exchanger isoform NHE3 and dipeptidyl peptidase IV in the renal proximal tubule. J Biol Chem 2001; 276: 46671-46677.
14. Sabolic I, Shi LB, Brown D, Ausiello DA, Verkman AS: Proteinases inhibit H + -ATPase and Na + /H + exchange but not water transport in apical and endosomal membranes from rat proximal tubule. Biochim Biophys Acta 1992; 1103: 137-147.
15. Weinman EJ, Dubinsky WP, Dinh Q, Steplock D, Shenolikar S: Effect of limited trypsin digestion on the renal Na + -H + exchanger and its regulation by cAMP-dependent protein kinase. J Membr Biol 1989; 109: 233-241. (Pubitemid 19191213)
16. Augustyns K, Bal G, Thonus G, Belyaev A, Zhang XM, Bollaert W, Lambeir AM, Durinx C, Goossens F, Haemers A: The unique properties of dipeptidyl-peptidase IV (DPP IV/CD26) and the therapeutic potential of DPP IV inhibitors. Curr Med Chem 1999; 6: 311-327. (Pubitemid 29226115)
17. Sedo A, Duke-Cohan JS, Balaziova E, Sedova LR: Dipeptidyl peptidase IV activity and/or structure homologs: Contributing factors in the pathogenesis of rheumatoid arthritis? Arthritis Res Ther 2005; 7: 253-269. (Pubitemid 41646256)
18. Antonyan AA, Sharoyan SG, Mardanyan SS, Galoyan AA: Proline-rich cytokine from neurosecretory granules: A new natural substrate for dipeptidyl peptidase IV. Neurochem Res 2011; 36: 34-38.
19. Reinhold D, Kahne T, Steinbrecher A, Wrenger S, Neubert K, Ansorge S, Brocke S: The role of dipeptidyl peptidase IV enzymatic activity in T-cell activation and autoimmunity. Biol Chem 2002; 383: 1133-1138. (Pubitemid 35215059)
20. Girardi AC, Fukuda LE, Rossoni LV, Malnic G, Reboucas NA: Dipeptidyl peptidase IV inhibition downregulates Na + -H + exchanger NHE3 in rat renal proximal tubule. Am J Physiol Renal Physiol 2008; 294:F414-F422. (Pubitemid 351199407)
21. Carattino MD, Sheng S, Bruns JB, Pilewski JM, Hughey RP, Kleyman TR: The epithelial Na + channel is inhibited by a peptide derived from proteolytic processing of itsγ-subunit. J Biol Chem 2006; 281: 18901-18907. (Pubitemid 44035549)
22. 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 theγ-subunit. J Biol Chem 2007; 282: 6153-6160. (Pubitemid 47100869)
23. Maekawa A, Kakizoe Y, Miyoshi T, Wakida N, Ko T, Shiraishi N, Adachi M, Tomita K, Kitamura K: Camostat mesilate inhibits prostasin activity and reduces blood pressure and renal injury in salt-sensitive hypertension. J Hypertens 2009; 27: 181-189.
24. 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 2002; 120: 191-201. (Pubitemid 34857968)
25. Garcia-Caballero A, Dang Y, He H, Stutts MJ: ENaC proteolytic regulation by channelactivating protease 2. J Gen Physiol 2008; 132: 521-535.
26. Friis S, Godiksen S, Bornholdt J, Selzer-Plon J, Rasmussen HB, Bugge TH, Lin CY, Vogel LK: Transport via the transcytotic pathway makes prostasin available as a substrate for matriptase. J Biol Chem 2011; 286: 5793-5802.
27. 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 2009; 297:R1733-R1741.
28. Svenningsen P, Bistrup C, Friis UG, Bertog M, Haerteis S, Krueger B, Stubbe J, Jensen ON, Thiesson HC, Uhrenholt TR, Jespersen B, Jensen BL, Korbmacher C, Skott O: Plasmin in nephrotic urine activates the epithelial sodium channel. J Am Soc Nephrol 2009; 20: 299-310.
29. Valles P, Ebner S, Manucha W, Gutierrez L, Marin-Grez M: Effect of glandular kallikrein on distal nephron HCO 3 - secretion in rats and on HCO 3 - secretion in MDCK cells. Am J Physiol 1997; 273:F807-F816. (Pubitemid 27508378)
30. El Moghrabi S, Houillier P, Picard N, Sohet F, Wootla B, Bloch-Faure M, Leviel F, Cheval L, Frische S, Meneton P, Eladari D, Chambrey R: Tissue kallikrein permits early renal adaptation to potassium load. Proc Natl Acad Sci USA 2010; 107: 13526-13531.
31. Vesey DA, Hooper JD, Gobe GC, Johnson DW: Potential physiological and pathophysiological roles for protease-activated receptor- 2 in the kidney. Nephrology (Carlton) 2007; 12: 36-43.
32. Bertog M, Letz B, Kong W, Steinhoff M, Higgins MA, Bielfeld-Ackermann A, Fromter E, Bunnett NW, Korbmacher C: Basolateral proteinase-activated receptor (PAR-2) induces chloride secretion in M-1 mouse renal cortical collecting duct cells. J Physiol 1999; 521: 3-17.
33. Grandaliano G, Pontrelli P, Cerullo G, Monno R, Ranieri E, Ursi M, Loverre A, Gesualdo L, Schena FP: Protease-activated receptor-2 expression in IgA nephropathy: A potential role in the pathogenesis of interstitial fibrosis. J Am Soc Nephrol 2003; 14: 2072-2083. (Pubitemid 36909915)
34. Morla L, Crambert G, Mordasini D, Favre G, Doucet A, Imbert-Teboul M: Proteinase-activated receptor 2 stimulates Na,K-ATPase and sodium reabsorption in native kidney epithelium. J Biol Chem 2008; 283: 28020-28028.
35. Liu L, Hering-Smith KS, Schiro FR, Hamm LL: Serine protease activity in m-1 cortical collecting duct cells. Hypertension 2002; 39: 860-864. (Pubitemid 34437540)
36. Verghese GM, Gutknecht MF, Caughey GH: Prostasin regulates epithelial monolayer function: Cell-specific Gpld1-mediated secretion and functional role for GPI anchor. Am J Physiol Cell Physiol 2006; 291:C1258-C1270. (Pubitemid 44878597)
37. Steensgaard M, Svenningsen P, Tinning AR, Nielsen TD, Jorgensen F, Kjaersgaard G, Madsen K, Jensen BL: Apical serine protease activity is necessary for assembly of a highresistance renal collecting duct epithelium. Acta Physiol (Oxf) 2010; 200: 347-359.
38. Leyvraz C, Charles RP, Rubera I, Guitard M, Rotman S, Breiden B, Sandhoff K, Hummler E: The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J Cell Biol 2005; 170: 487-496. (Pubitemid 41126947)
39. Buzza MS, Netzel-Arnett S, Shea-Donohue T, Zhao A, Lin CY, List K, Szabo R, Fasano A, Bugge TH, Antalis TM: Membrane-anchored serine protease matriptase regulates epithelial barrier formation and permeability in the intestine. Proc Natl Acad Sci USA 2010; 107: 4200-4205.
40. Belo AA, Sousa Mde O, Machado EL, Figueiredo AF: On human tissue kallikrein activity in urine of Brazilian White and Black primary hypertensive patients. Ethn Dis 2009; 19: 265-270.
41. Margolis HS, Geller R, Pisano JJ, Sjoerdsma A: Altered urinary kallikrein excretion in human hypertension. Lancet 1971;ii:1063-1065.
42. 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 2005; 46: 683-688. (Pubitemid 43191838)
43. Geller RG, Margolius HS, Pisano JJ, Keiser HR: Effects of mineralocorticoids, altered sodium intake, and adrenalectomy on urinary kallikrein in rats. Circ Res 1972; 31: 857-861.
44. Ergonul Z, Frindt G, Palmer LG: Regulation of maturation and processing of ENaC subunits in the rat kidney. Am J Physiol Renal Physiol 2006; 291:F683-F693. (Pubitemid 44343751)
45. Frindt G, Ergonul Z, Palmer LG: Surface expression of epithelial Na channel protein in rat kidney. J Gen Physiol 2008; 131: 617-627. (Pubitemid 351749201)
46. Masilamani S, Kim GH, Mitchell C, Wade JB, Knepper MA: Aldosterone-mediated regulation of ENaCγ-,γ-, andγ-subunit proteins in rat kidney. J Clin Invest 1999; 104:R19-R23. (Pubitemid 29536348)