Albuminuria induces a proinflammatory and profibrotic response in cortical collecting ducts via the 24p3 receptor

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 7, 2013, Pages

  Dizin, Eva ^a   Hasler, Udo ^a   Nlandu Khodo, Stellor ^a   Fila, Marc ^b   Roth, Isabelle ^a   Ernandez, Thomas ^a   Doucet, Alain ^b   Martin, Pierre Yves ^a   Feraille, Eric ^a   de Seigneux, Sophie ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

24p3R; Collecting duct; Fibrosis; Proteinuria

Indexed keywords

ALBUMIN; CREATININE; I KAPPA B; I KAPPA B ALPHA; MESSENGER RNA; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; RANTES; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA1; VIMENTIN;

ALBUMIN BLOOD LEVEL; ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; ENDOCYTOSIS; ENZYME ACTIVATION; GLOMERULUS FILTRATION RATE; IMMUNOFLUORESCENCE MICROSCOPY; INFLAMMATION; INTERNALIZATION; KIDNEY COLLECTING TUBULE; KIDNEY CORTEX; KIDNEY FIBROSIS; KIDNEY MEDULLA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; RAT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84884926980     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00006.2013     Document Type: Article

References (40)

1. Abbate M, Zoja C, Remuzzi G. How does proteinuria cause progressive renal damage? J Am Soc Nephrol 17: 2974-2984, 2006.
2. Amsellem S, Gburek J, Hamard G, Nielsen R, Willnow TE, Devuyst O, Nexo E, Verroust PJ, Christensen EI, Kozyraki R. Cubilin is essential for albumin reabsorption in the renal proximal tubule. J Am Soc Nephrol 21: 1859-1867, 2010.
3. Apostol E, Ecelbarger CA, Terris J, Bradford AD, Andrews P, Knepper MA. Reduced renal medullary water channel expression in puromycin aminonucleoside-induced nephrotic syndrome. J Am Soc Nephrol 8: 15-24, 1997.
4. Astor BC, Matsushita K, Gansevoort RT, van der Velde M, Woodward M, Levey AS, Jong PE, Coresh J, de Jong PE, El-Nahas M, Eckardt KU, Kasiske BL, Wright J, Appel L, Greene T, Levin A, Djurdjev O, Wheeler DC, Landray MJ, Townend JN, Emberson J, Clark LE, Macleod A, Marks A, Ali T, Fluck N, Prescott G, Smith DH, Weinstein JR, Johnson ES, Thorp ML, Wetzels JF, Blankestijn PJ, van Zuilen AD, Menon V, Sarnak M, Beck G, Kronenberg F, Kollerits B, Froissart M, Stengel B, Metzger M, Remuzzi G, Ruggenenti P, Perna A, Heerspink HJ, Brenner B, de Zeeuw D, Rossing P, Parving HH, Auguste P, Veldhuis K, Wang Y, Camarata L, Thomas B, Manley T. Lower estimated glomerular filtration rate and higher albuminuria are associated with mortality and end-stage renal disease. A collaborative meta-analysis of kidney disease population cohorts. Kidney Int 79: 1331-1340, 2011.
5. Boger CA, Chen MH, Tin A, Olden M, Kottgen A, Deboer IH, Fuchsberger C, O'Seaghdha CM, Pattaro C, Teumer A, Liu CT, Glazer NL, Li M, O'Connell JR, Tanaka T, Peralta CA, Kutalik Z, Luan J, Zhao JH, Hwang SJ, Akylbekova E, Kramer H, van der Harst P, Smith AV, Lohman K, de Andrade M, Hayward C, Kollerits B, Tonjes A, Aspelund T, Ingelsson E, Eiriksdottir G, Launer LJ, Harris TB, Shuldiner AR, Mitchell BD, Arking DE, Franceschini N, Boerwinkle E, Egan J, Hernandez D, Reilly M, Townsend RR, Lumley T, Siscovick DS, Psaty BM, Kestenbaum B, Haritunians T, Bergmann S, Vollenweider P, Waeber G, Mooser V, Waterworth D, Johnson AD, Florez JC, Meigs JB, Lu X, Turner ST, Atkinson EJ, Leak TS, Aasarod K, Skorpen F, Syvanen AC, Illig T, Baumert J, Koenig W, Kramer BK, Devuyst O, Mychaleckyj JC, Minelli C, Bakker SJ, Kedenko L, Paulweber B, Coassin S, Endlich K, Kroemer HK, Biffar R, Stracke S, Volzke H, Stumvoll M, Magi R, Campbell H, Vitart V, Hastie ND, Gudnason V, Kardia SL, Liu Y, Polasek O, Curhan G, Kronenberg F, Prokopenko I, Rudan I, Arnlov J, Hallan S, Navis G, Parsa A, Ferrucci L, Coresh J, Shlipak MG, Bull SB, Paterson AD, Wichmann HE, Wareham NJ, Loos RJ, Rotter JI, Pramstaller PP, Cupples LA, Beckmann JS, Yang Q, Heid IM, Rettig R, Dreisbach AW, Bochud M, Fox CS, Kao WH. CUBN is a gene locus for albuminuria. J Am Soc Nephrol 22: 555-570, 2011.
6. Chasman DI, Fuchsberger C, Pattaro C, Teumer A, Boger CA, Endlich K, Olden M, Chen MH, Tin A, Taliun D, Li M, Gao X, Gorski M, Yang Q, Hundertmark C, Foster MC, O'Seaghdha CM, Glazer N, Isaacs A, Liu CT, Smith AV, O'Connell JR, Struchalin M, Tanaka T, Li G, Johnson AD, Gierman HJ, Feitosa MF, Hwang SJ, Atkinson EJ, Lohman K, Cornelis MC, Johansson A, Tonjes A, Dehghan A, Lambert JC, Holliday EG, Sorice R, Kutalik Z, Lehtimaki T, Esko T, Deshmukh H, Ulivi S, Chu AY, Murgia F, Trompet S, Imboden M, Coassin S, Pistis G, Harris TB, Launer LJ, Aspelund T, Eiriksdottir G, Mitchell BD, Boerwinkle E, Schmidt H, Cavalieri M, Rao M, Hu F, Demirkan A, Oostra BA, de Andrade M, Turner ST, Ding J, Andrews JS, Freedman BI, Giulianini F, Koenig W, Illig T, Meisinger C, Gieger C, Zgaga L, Zemunik T, Boban M, Minelli C, Wheeler HE, Igl W, Zaboli G, Wild SH, Wright AF, Campbell H, Ellinghaus D, Nothlings U, Jacobs G, Biffar R, Ernst F, Homuth G, Kroemer HK, Nauck M, Stracke S, Volker U, Volzke H, Kovacs P, Stumvoll M, Magi R, Hofman A, Uitterlinden AG, Rivadeneira F, Aulchenko YS, Polasek O, Hastie N, Vitart V, Helmer C, Wang JJ, Stengel B, Ruggiero D, Bergmann S, Kahonen M, Viikari J, Nikopensius T, Province M, Ketkar S, Colhoun H, Doney A, Robino A, Kramer BK, Portas L, Ford I, Buckley BM, Adam M, Thun GA, Paulweber B, Haun M, Sala C, Mitchell P, Ciullo M, Kim SK, Vollenweider P, Raitakari O, Metspalu A, Palmer C, Gasparini P, Pirastu M, Jukema JW, Probst-Hensch NM, Kronenberg F, Toniolo D, Gudnason V, Shuldiner AR, Coresh J, Schmidt R, Ferrucci L, Siscovick DS, van Duijn CM, Borecki IB, Kardia SL, Liu Y, Curhan GC, Rudan I, Gyllensten U, Wilson JF, Franke A, Pramstaller PP, Rettig R, Prokopenko I, Witteman J, Hayward C, Ridker PM, Parsa A, Bochud M, Heid IM, Kao WH, Fox CS, Kottgen A. Integration of genome-wide association studies with biological knowledge identifies six novel genes related to kidney function. Hum Mol Genet 21: 5329-5343, 2012.
7. Christensen EI, Verroust PJ, Nielsen R. Receptor-mediated endocytosis in renal proximal tubule. Pflügers Arch 458: 1039-1048, 2009.
8. de Seigneux S, Nielsen J, Olesen ET, Dimke H, Kwon TH, Frokiaer J, Nielsen S. Long-term aldosterone treatment induces decreased apical but increased basolateral expression of AQP2 in CCD of rat kidney. Am J Physiol Renal Physiol 293: F87-F99, 2007.
9. Eddy AA. Interstitial nephritis induced by protein-overload proteinuria. Am J Pathol 135: 719-733, 1989.
10. secretion in the distal nephron in nephrotic syndrome: possible role of albuminuria. J Physiol 589: 3611-3621, 2011.
11. Fujita T, Nolan GP, Liou HC, Scott ML, Baltimore D. The candidate proto-oncogene bcl-3 encodes a transcriptional coactivator that activates through NF-kappa B p50 homodimers. Genes Dev 7: 1354-1363, 1993.
12. Fujiu K, Manabe I, Nagai R. Renal collecting duct epithelial cells regulate inflammation in tubulointerstitial damage in mice. J Clin Invest 121: 3425-3441, 2011.
13. Garcia-Sanchez O, Lopez-Hernandez FJ, Lopez-Novoa JM. An integrative view on the role of TGF-beta in the progressive tubular deletion associated with chronic kidney disease. Kidney Int 77: 950-955, 2010.
14. Hasler U, Leroy V, Jeon US, Bouley R, Dimitrov M, Kim JA, Brown D, Kwon HM, Martin PY, Feraille E. NF-kappaB modulates aquaporin-2 transcription in renal collecting duct principal cells. J Biol Chem 283: 28095-28105, 2008.
15. Hasler U, Vinciguerra M, Vandewalle A, Martin PY, Feraille E. Dual effects of hypertonicity on aquaporin-2 expression in cultured renal collecting duct principal cells. J Am Soc Nephrol 16: 1571-1582, 2005.
16. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 176: 85-97, 2010.
17. Koesters R, Kaissling B, Lehir M, Picard N, Theilig F, Gebhardt R, Glick AB, Hahnel B, Hosser H, Grone HJ, Kriz W. Tubular overexpression of transforming growth factor-beta1 induces autophagy and fibrosis but not mesenchymal transition of renal epithelial cells. Am J Pathol 177: 632-643, 2010.
18. Langelueddecke C, Roussa E, Fenton RA, Wolff NA, Lee WK, Thevenod F. Lipocalin-2 [24p3/neutrophil gelatinase-associated lipocalin (NGAL)] receptor is expressed in distal nephron and mediates protein endocytosis. J Biol Chem 287: 159-169, 2012.
19. Leroy V, De Seigneux S, Agassiz V, Hasler U, Rafestin-Oblin ME, Vinciguerra M, Martin PY, Feraille E. Aldosterone activates NFkappaB in the collecting duct. J Am Soc Nephrol 20: 131-144, 2009.
20. Levey AS, Coresh J. Chronic kidney disease. Lancet 379: 165-180, 2012.
21. Levey AS, de Jong PE, Coresh J, Nahas ME, Astor BC, Matsushita K, Gansevoort RT, Kasiske BL, Eckardt KU. The definition, classification and prognosis of chronic kidney disease: a KDIGO Controversies Conference report. Kidney Int 80: 17-28, 2011.
22. Li Y, Wen X, Liu Y. Tubular cell dedifferentiation and peritubular inflammation are coupled by the transcription regulator Id1 in renal fibrogenesis. Kidney Int 81: 880-891, 2012.
23. Maunsbach AB. Albumin absorption by renal proximal tubule cells. Nature 212: 546-547, 1966.
24. Maunsbach AB. Cellular mechanisms of tubular protein transport. Int Rev Physiol 11: 145-167, 1976.
25. Mogensen CE. Microalbuminuria predicts clinical proteinuria and early mortality in maturity-onset diabetes. N Engl J Med 310: 356-360, 1984.
26. Nielsen R, Christensen EI. Proteinuria and events beyond the slit. Pediatr Nephrol 25: 813-822, 2010.
27. Nlandu Khodo S, Dizin E, Sossauer G, Szanto I, Martin PY, Feraille E, Krause KH, de Seigneux S. NADPH-oxidase 4 protects against kidney fibrosis during chronic renal injury. J Am Soc Nephrol 23: 1967-1976, 2012.
28. Olesen ET, de Seigneux S, Wang G, Lutken SC, Frokiaer J, Kwon TH, Nielsen S. Rapid and segmental specific dysregulation of AQP2, S256-pAQP2 and renal sodium transporters in rats with LPS-induced endotoxaemia. Nephrol Dial Transplant 24: 2338-2349, 2009.
29. Roth I, Leroy V, Kwon HM, Martin PY, Feraille E, Hasler U. Osmoprotective transcription factor NFAT5/TonEBP modulates nuclear factor-kappaB activity. Mol Biol Cell 21: 3459-3474, 2010.
30. Ruggenenti P, Perna A, Zoccali C, Gherardi G, Benini R, Testa A, Remuzzi G. Chronic proteinuric nephropathies. II. Outcomes and response to treatment in a prospective cohort of 352 patients: differences between women and men in relation to the ACE gene polymorphism Gruppo Italiano di Studi Epidemologici in Nefrologia (Gisen). J Am Soc Nephrol 11: 88-96, 2000.
31. Russo LM, Sandoval RM, Campos SB, Molitoris BA, Comper WD, Brown D. Impaired tubular uptake explains albuminuria in early diabetic nephropathy. J Am Soc Nephrol 20: 489-494, 2009.
32. Russo LM, Sandoval RM, McKee M, Osicka TM, Collins AB, Brown D, Molitoris BA, Comper WD. The normal kidney filters nephrotic levels of albumin retrieved by proximal tubule cells: retrieval is disrupted in nephrotic states. Kidney Int 71: 504-513, 2007.
33. Schainuck LI, Striker GE, Cutler RE, Benditt EP. Structural-functional correlations in renal disease. II. The correlations. Hum Pathol 1: 631-641, 1970.
34. Suzuki T, Kimura M, Asano M, Fujigaki Y, Hishida A. Role of atrophic tubules in development of interstitial fibrosis in microembolisminduced renal failure in rat. Am J Pathol 158: 75-85, 2001.
35. Suzuki Y, Ito Y, Mizuno M, Kinashi H, Sawai A, Noda Y, Mizuno T, Shimizu H, Fujita Y, Matsui K, Maruyama S, Imai E, Matsuo S, Takei Y. Transforming growth factor-beta induces vascular endothelial growth factor-C expression leading to lymphangiogenesis in rat unilateral ureteral obstruction. Kidney Int 81: 865-879, 2012.
36. Tonelli M, Muntner P, Lloyd A, Manns BJ, James MT, Klarenbach S, Quinn RR, Wiebe N, Hemmelgarn BR. Using proteinuria and estimated glomerular filtration rate to classify risk in patients with chronic kidney disease: a cohort study. Ann Intern Med 154: 12-21, 2011.
37. Xiao G, Fu J. NF-kappaB and cancer: a paradigm of Yin-Yang. Am J Cancer Res 1: 192-221, 2011.
38. Yard BA, Chorianopoulos E, Herr D, van der Woude FJ. Regulation of endothelin-1 and transforming growth factor-beta1 production in cultured proximal tubular cells by albumin and heparan sulphate glycosaminoglycans. Nephrol Dial Transplant 16: 1769-1775, 2001.
39. Zoja C, Donadelli R, Colleoni S, Figliuzzi M, Bonazzola S, Morigi M, Remuzzi G. Protein overload stimulates RANTES production by proximal tubular cells depending on NF-kappa B activation. Kidney Int 53: 1608-1615, 1998.
40. Zoja C, Morigi M, Remuzzi G. Proteinuria and phenotypic change of proximal tubular cells. J Am Soc Nephrol 14, Suppl 1: S36-41, 2003.