Aberrant glomerular filtration of urokinase-type plasminogen activator in nephrotic syndrome leads to amiloride-sensitive plasminogen activation in urine

American Journal of Physiology - Renal Physiology

Volumn 309, Issue 3, 2015, Pages F235-F241

  Stæhr, Mette ^a   Buhl, Kristian B ^a   Andersen, René F ^b   Svenningsen, Per ^a   Nielsen, Flemming ^a   Hinrichs, Gitte Rye ^c   Bistrup, Claus ^a,c   Jensen, Boye L ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Edema; ENaC; Proteinuria; Proteolysis; Sodium

Indexed keywords

AMILORIDE; PLASMIN; PROTEINASE; PUROMYCIN AMINONUCLEOSIDE; UROKINASE; EPITHELIAL SODIUM CHANNEL; EPITHELIAL SODIUM CHANNEL BLOCKING AGENT; PLASMINOGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GLOMERULUS FILTRATION; HUMAN; MALE; NEPHROTIC SYNDROME; NONHUMAN; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEINURIA; RAT; SODIUM RETENTION; URINARY EXCRETION; URINE; ADULT; ANIMAL; CHEMICALLY INDUCED; CHILD; GLOMERULUS; METABOLISM; SPRAGUE DAWLEY RAT;

ADULT; AMILORIDE; ANIMALS; CHILD; EPITHELIAL SODIUM CHANNEL BLOCKERS; EPITHELIAL SODIUM CHANNELS; HUMANS; KIDNEY GLOMERULUS; MALE; NEPHROTIC SYNDROME; PLASMINOGEN; PUROMYCIN AMINONUCLEOSIDE; RATS; RATS, SPRAGUE-DAWLEY; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84938575786     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00138.2015     Document Type: Article

References (45)

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. Andersen RF, Buhl KB, Jensen BL, Svenningsen P, Friis UG, Jespersen B, Rittig S. Remission of nephrotic syndrome diminishes urinary plasmin content and abolishes activation of ENaC. Pediatr Nephrol 28: 1227-1234, 2013.
3. Andreenko GV, Podoroldskaya LV, Polyantseva LP. Plasminogen activator in nephrotic syndrome. Folia Haematol Int Mag Klin Morphol Blutforsch 115: 351-355, 1988.
4. Bistrup C, Thiesson HC, Jensen BL, Skott O. Reduced activity of 11beta-hydroxysteroid dehydrogenase type 2 is not responsible for sodium retention in nephrotic rats. Acta Physiol Scand 184: 161-169, 2005.
5. Boer P, Roos JC, Geyskes GG, Dorhaut Mees EF. Observations on plasma renin substrate in the nephrotic syndrome. Nephron 26: 121-125, 1980.
6. Brown EA, Markandu ND, Roulston JE, Jones BE, Squires M, MacGregor GA. Is the renin-angiotensin-aldosterone system involved in the sodium retention in the nephrotic syndrome? Nephron 32: 102-107, 1982.
7. Brown EA, Markandu ND, Sagnella GA, Squires M, Jones BE, MacGregor GA. Evidence that some mechanism other than the renin system causes sodium retention in nephrotic syndrome. Lancet 2: 1237- 1240, 1982.
8. + 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.
9. + channels. Am J Physiol Cell Physiol 286: C190-C194, 2004.
10. Carattino MD, Hughey RP, Kleyman TR. Proteolytic processing of the epithelial sodium channel gamma subunit has a dominant role in channel activation. J Biol Chem 283: 25290-25295, 2008.
11. Chen Z, Zhao R, Zhao M, Liang X, Bhattarai D, Dhiman R, Shetty S, Idell S, Ji HL. Regulation of epithelial sodium channels in urokinase plasminogen activator deficiency. Am J Physiol Lung Cell Mol Physiol 307: L609-L617, 2014.
12. Cubellis MV, Nolli ML, Cassani G, Blasi F. Binding of single-chain prourokinase to the urokinase receptor of human U937 cells. J Biol Chem 261: 15819-15822, 1986.
13. +)-ATPase activity is correlated with urinary sodium excretion in rat nephrotic syndromes. J Am Soc Nephrol 11: 604-615, 2000.
14. Deschenes G, Guigonis V, Doucet A. Molecular mechanism of edema formation in nephrotic syndrome. Arch Pediatr 11: 1084-1094, 2004.
15. Deschenes G, Wittner M, Stefano A, Jounier S, Doucet A. Collecting duct is a site of sodium retention in PAN nephrosis: a rationale for amiloride therapy. J Am Soc Nephrol 12: 598-601, 2001.
16. 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.
17. Frindt G, Ergonul Z, Palmer LG. Na channel expression and activity in the medullary collecting duct of rat kidney. Am J Physiol Renal Physiol 292: F1190-F1196, 2007.
18. Holmberg L, Bladh B, Astedt B. Purification of urokinase by affinity chromatography. Biochim Biophys Acta 445: 215-222, 1976.
19. 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.
20. Ichikawa I, Rennke HG, Hoyer JR, Badr KF, Schor N, Troy JL, Lechene CP, Brenner BM. Role for intrarenal mechanisms in the impaired salt excretion of experimental nephrotic syndrome. J Clin Invest 71: 91-103, 1983.
21. Ji HL, Zhao R, Komissarov AA, Chang Y, Liu Y, Matthay MA. Proteolytic regulation of epithelial sodium channels by urokinase plasminogen activator: cutting edge and cleavage sites. J Biol Chem 290: 5241- 5255, 2015.
22. Kenichi M, Masanobu M, Takehiko K, Shoko T, Akira F, Katsushige A, Takashi H, Yoshiyuki O, Shigeru K. Renal synthesis of urokinase type-plasminogen activator, its receptor, and plasminogen activator inhibitor- 1 in diabetic nephropathy in rats: modulation by angiotensin-converting- enzyme inhibitor. J Lab Clin Med 144: 69-77, 2004.
23. Kerlin BA, Ayoob R, Smoyer WE. Epidemiology and pathophysiology of nephrotic syndrome-associated thromboembolic disease. Clin J Am Soc Nephrol 7: 513-520, 2012.
24. Koomans HA, Geers AB, vd Meiracker AH, Roos JC, Boer P, Dorhout Mees EJ. Effects of plasma volume expansion on renal salt handling in patients with the nephrotic syndrome. Am J Nephrol 4: 227-234, 1984.
25. 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.
26. Navarrete M, Ho J, Krokhin O, Ezzati P, Rigatto C, Reslerova M, Rush DN, Nickerson P, Wilkins JA. Proteomic characterization of serine hydrolase activity and composition in normal urine. Clin Proteomics 10: 17, 2013.
27. Nicholas SB, Aguiniga E, Ren Y, Kim J, Wong J, Govindarajan N, Noda M, Wang W, Kawano Y, Collins A, Hsueh WA. Plasminogen activator inhibitor-1 deficiency retards diabetic nephropathy. Kidney Int 67: 1297-1307, 2005.
28. Nielsen LS, Hansen JG, Skriver L, Wilson EL, Kaltoft K, Zeuthen J, Dano K. Purification of zymogen to plasminogen activator from human glioblastoma cells by affinity chromatography with monoclonal antibody. Biochemistry 21: 6410-6415, 1982.
29. + channels by cleaving the gamma subunit. J Biol Chem 283: 36586-36591, 2008.
30. Rabelink TJ, Bijlsma JA, Koomans HA. Iso-oncotic volume expansion in the nephrotic syndrome. Clin Sci (Lond) 84: 627-632, 1993.
31. Sappino AP, Huarte J, Vassalli JD, Belin D. Sites of synthesis of urokinase and tissue-type plasminogen activators in the murine kidney. J Clin Invest 87: 962-970, 1991.
32. Schild L, Schneeberger E, Gautschi I, Firsov D. Identification of amino acid residues in the alpha, beta, and gamma subunits of the epithelial sodium channel (ENaC) involved in amiloride block and ion permeation. J Gen Physiol 109: 15-26, 1997.
33. Siddall EC, Radhakrishnan J. The pathophysiology of edema formation in the nephrotic syndrome. Kidney Int 82: 635-642, 2012.
34. Smith AJ, Smith RN. Kinetics and bioavailability of two formulations of amiloride in man. Br J Pharmacol 48: 646-649, 1973.
35. 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 20: 299-310, 2009.
36. + channels by low plasmin concentrations. Am J Physiol Regul Integr Comp Physiol 297: R1733-R1741, 2009.
37. Tudpor K, Lainez S, Kwakernaak AJ, Kovalevskaya NV, Verkaart S, van Genesen S, van der Kemp A, Navis G, Bindels RJ, Hoenderop JG. Urinary plasmin inhibits TRPV5 in nephrotic-range proteinuria. J Am Soc Nephrol 23: 1824-1834, 2012.
38. Uchimura K, Kakizoe Y, Onoue T, Hayata M, Morinaga J, Yamazoe R, Ueda M, Mizumoto T, Adachi M, Miyoshi T, Shiraishi N, Sakai Y, Tomita K, Kitamura K. In vivo contribution of serine proteases to the proteolytic activation of γENaC in aldosterone-infused rats. Am J Physiol Renal Physiol 303: F939-F943, 2012.
39. 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.
40. Vassalli JD, Belin D. Amiloride selectively inhibits the urokinase-type plasminogen activator. FEBS Lett 214: 187-191, 1987.
41. 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.
42. Wagner SN, Atkinson MJ, Wagner C, Hofler H, Schmitt M, Wilhelm O. Sites of urokinase-type plasminogen activator expression and distribution of its receptor in the normal human kidney. Histochem Cell Biol 105: 53-60, 1996.
43. Wang Y, Jones CJ, Dang J, Liang X, Olsen JE, Doe WF. Human urokinase receptor expression is inhibited by amiloride and induced by tumor necrosis factor and phorbol ester in colon cancer cells. FEBS Lett 353: 138-142, 1994.
44. Yu Z, Schumacher M, Frey BM, Frey FJ, Vogt B. Regulation of epithelial sodium channel in puromycin aminonucleoside-induced unilateral experimental nephrotic syndrome in normal and analbuminemic Nagase rats. Nephron Physiol 101: 51-62, 2005.
45. Zhang B, Xie S, Shi W, Yang Y. Amiloride off-target effect inhibits podocyte urokinase receptor expression and reduces proteinuria. Nephrol Dial Transplant 27: 1746-1755, 2012.