Proximal tubules have the capacity to regulate uptake of albumin

Journal of the American Society of Nephrology

Volumn 27, Issue 2, 2016, Pages 482-494

  Wagner, Mark C ^a   Campos Bilderback, Silvia B ^a   Chowdhury, Mahboob ^b   Flores, Brittany ^a   Lai, Xianyin ^a   Myslinski, Jered ^a   Pandit, Sweekar ^a   Sandoval, Ruben M ^a   Wean, Sarah E ^a   Wei, Yuan ^c   Satlin, Lisa M ^c   Wiggins, Roger C ^b   Witzmann, Frank A ^a   Molitoris, Bruce A ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALBUMIN RECEPTOR; ANGIOPOIETIN 2; CALRETICULIN; TRANSCRIPTION FACTOR NRF2; ALBUMINOID;

ALBUMIN BLOOD LEVEL; ALBUMINURIA; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; INTRAVITAL MICROSCOPY; KIDNEY PROXIMAL TUBULE; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ANIMAL; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ALBUMINS; ANIMALS; FEMALE; KIDNEY TUBULES, PROXIMAL; RATS; RATS, WISTAR;

EID: 84970929781     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014111107     Document Type: Article

References (61)

1. Roscioni SS, Lambers Heerspink HJ, de Zeeuw D: Microalbuminuria: target for renoprotective therapy PRO. Kidney Int 86: 40-49, 2014
2. Dickson LE, Wagner MC, Sandoval RM, Molitoris BA: The proximal tubule and albuminuria: really! J Am Soc Nephrol 25: 443-453, 2014
3. Sandoval RM, Wagner MC, Patel M, Campos-Bilderback SB, Rhodes GJ, Wang E, Wean SE, Clendenon SS, Molitoris BA: Multiple factors influence glomerular albumin permeability in rats. J Am Soc Nephrol 23: 447-457, 2012
4. Tenten V, Menzel S, Kunter U, Sicking E-M, van Roeyen CRC, Sanden SK, Kaldenbach M, Boor P, Fuss A, Uhlig S, Lanzmich R, Willemsen B, Dijkman H, Grepl M, Wild K, Kriz W, Smeets B, Floege J, Moeller MJ: Albumin is recycled fromthe primary urine by tubular transcytosis. JAm Soc Nephrol 24: 1966-1980, 2013
5. Birn H, Christensen EI, Nielsen S: Kinetics of endocytosis in renal proximal tubule studied with rutheniumred asmembranemarker. AmJ Physiol 264: F239-F250, 1993
6. Christensen EI, Birn H: Megalin and cubilin: synergistic endocytic receptors in renal proximal tubule. Am J Physiol Renal Physiol 280: F562-F573, 2001
7. Anderson CL, Chaudhury C, Kim J, Bronson CL, Wani MA, Mohanty S: Perspective-FcRn transports albumin: relevance to immunology and medicine. Trends Immunol 27: 343-348, 2006
8. Schaeffer C, CreatoreA, Rampoldi L: Protein trafficking defects in inherited kidney diseases. Nephrol Dial Transplant 29[Suppl 4]: iv33-iv44, 2014
9. Weening JJ, Van Guldener C, DahaMR, KlarN, van der Wal A, Prins FA: The pathophysiology of protein-overload proteinuria. AmJ Pathol 129: 64-73, 1987
10. Yoshida S, Nagase M, Shibata S, Fujita T: Podocyte injury induced by albumin overload in vivo and in vitro: involvement of TGF-beta and p38 MAPK. Nephron Exp Nephrol 108: e57-e68, 2008
11. Wharram BL, Goyal M, Wiggins JE, Sanden SK, Hussain S, Filipiak WE, Saunders TL, Dysko RC, Kohno K, Holzman LB, Wiggins RC: Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol 16: 2941-2952, 2005
12. Sandoval RM, Molitoris BA: Quantifying endocytosis in vivo using intravital two-photon microscopy. MethodsMol Biol 440: 389-402, 2008
13. Russo LM, Sandoval RM, Campos SB, Molitoris BA, ComperWD, Brown D: Impaired tubular uptake explains albuminuria in early diabetic nephropathy. J Am Soc Nephrol 20: 489-494, 2009
14. Peti-Peterdi J, Sipos A: A high-powered view of the filtration barrier. J Am Soc Nephrol 21: 1835-1841, 2010
15. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB: Two gene fragments that direct podocyte-specific expression in transgenic mice. J Am Soc Nephrol 13: 1561-1567, 2002
16. Chaudhury C, Mehnaz S, Robinson JM, Hayton WL, Pearl DK, Roopenian DC, Anderson CL: The major histocompatibility complexrelated Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J ExpMed 197: 315-322, 2003
17. Andersen JT, Dee Qian J, Sandlie I: The conserved histidine 166 residue of the human neonatal Fc receptor heavy chain is critical for the pHdependent binDing to albumin. Eur J Immunol 36: 3044-3051, 2006
18. Tesar DB, Björkman PJ: An intracellular traffic jam: Fc receptor-mediated transport of immunoglobulin G. Curr Opin Struct Biol 20: 226-233, 2010
19. Newton EE, Wu Z, Simister NE: Characterization of basolateraltargeting signals in the neonatal Fc receptor. J Cell Sci 118: 2461-2469, 2005
20. Haymann JP, Levraud JP, Bouet S, Kappes V, Hagège J, Nguyen G, Xu Y, Rondeau E, Sraer JD: Characterization and localization of the neonatal Fc receptor in adult human kidney. J Am Soc Nephrol 11: 632-639, 2000
21. Lee D, Gleich K, Fraser SA, Katerelos M, Mount PF, Power DA: Limited capacity of proximal tubular proteolysis in mice with proteinuria. Am J Physiol Renal Physiol 304: F1009-F1019, 2013
22. Wang B-G, König K, Halbhuber K-J: Two-photon microscopy of deep intravital tissues and its merits in clinical research. JMicrosc 238: 1-20, 2010
23. Bliss DJ, Brewer DB: Increased albumin and normal dextran clearances in protein-overload proteinuria in the rat. Clin Sci (Lond) 69: 321-326, 1985
24. Lawrence GM, Brewer DB: Effect of strain and sex on the induction of hyperalbuminaemic proteinuria in the rat. Clin Sci (Lond) 61: 751-756, 1981
25. Davies DJ,Messina A, Thumwood CM, RyanGB:Glomerular podocytic injury in protein overload proteinuria. Pathology 17: 412-419, 1985
26. Nagai J, Yamamoto A, Yumoto R, TakanoM: Albumin overload induces expression of hypoxia-inducible factor 1a and its target genes in HK-2 human renal proximal tubular cell line. Biochem Biophys Res Commun 434: 670-675, 2013
27. Fang L, Xie D, Wu X, Cao H, SuW, Yang J: Involvement of endoplasmic reticulum stress in albuminuria induced inflammasome activation in renal proximal tubular cells. PLoS ONE 8: e72344, 2013
28. Gorostizaga A, Mori Sequeiros García MM, Acquier A, Gomez NV, Maloberti PM, Mendez CF, Paz C: Modulation of albumin-induced endoplasmic reticulum stress in renal proximal tubule cells by upregulation of mapk phosphatase-1. Chem Biol Interact 206: 47-54, 2013
29. KoltunM,ComperWD: Retentionof albumin in the circulation is governedby saturable renal cell-mediated processes. Microcirculation 11: 351-360, 2004
30. Leheste JR, Rolinski B, Vorum H, Hilpert J, Nykjaer A, Jacobsen C, Aucouturier P, Moskaug JO, Otto A, Christensen EI, Willnow TE: Megalin knockout mice as an animal model of low molecular weight proteinuria. Am J Pathol 155: 1361-1370, 1999
31. Nagai J, Christensen EI, Morris SM,Willnow TE, Cooper JA, Nielsen R: Mutually dependent localization of megalin and Dab2 in the renal proximal tubule. Am J Physiol Renal Physiol 289: F569-F576, 2005
32. Tojo A, Kinugasa S: Mechanisms of glomerular albumin filtration and tubular reabsorption. Int J Nephrol 481520: 2012
33. Guasch A, Deen WM, Myers BD: Charge selectivity of the glomerular filtration barrier in healthy and nephrotic humans. J Clin Invest 92: 2274-2282, 1993
34. Storm T, Tranebjærg L, Frykholm C, Birn H, Verroust PJ, Nevéus T, Sundelin B, Hertz JM, Holmström G, Ericson K, Christensen EI, Nielsen R: Renal phenotypic investigations of megalin-deficient patients: novel insights into tubular proteinuria and albumin filtration. Nephrol Dial Transplant 28: 585-591, 2013
35. Böger CA, Chen M-H, Tin A, Olden M, Köttgen A, de Boer IH, Fuchsberger C, O'Seaghdha CM, Pattaro C, Teumer A, Liu CT, Glazer NL, LiM,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, Tönjes 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, ReillyM, 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, Aasarød K, Skorpen F, Syvänen AC, Illig T, Baumert J, Koenig W, Krämer BK, Devuyst O, Mychaleckyj JC, Minelli C, Bakker SJ, Kedenko L, Paulweber B, Coassin S, Endlich K, Kroemer HK, Biffar R, Stracke S, Völzke H, StumvollM,Mägi R, Campbell H, Vitart V, Hastie ND, Gudnason V, Kardia SL, Liu Y, Polasek O, Curhan G, Kronenberg F, Prokopenko I, Rudan I, Arnlöv J, Hallan S, Navis G, Parsa A, Ferrucci L, Coresh J, Shlipak MG, Bull SB, Paterson NJ, 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; CKDGen Consortium: CUBN is a gene locus for albuminuria. J Am Soc Nephrol 22: 555-570, 2011
36. Ovunc B,Otto EA, Vega-Warner V, Saisawat P, Ashraf S, Ramaswami G, Fathy HM, Schoeb D, Chernin G, Lyons RH, Yilmaz E, Hildebrandt F: Exome sequencing reveals cubilin mutation as a single-gene cause of proteinuria. J Am Soc Nephrol 22: 1815-1820, 2011
37. 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
38. Kuo TT, de Muinck EJ, Claypool SM, Yoshida M, Nagaishi T, Aveson VG, LencerWI, Blumberg RS:N-glycanmoieties in neonatal Fc receptor determine steady-state membrane distribution and directional transport of IgG. J Biol Chem284: 8292-8300, 2009
39. McCarthy KM, Lam M, Subramanian L, Shakya R, Wu Z, Newton EE, Simister NE: Effects of mutations in potential phosphorylation sites on transcytosis of FcRn. J Cell Sci 114: 1591-1598, 2001
40. Dickinson BL, Claypool SM, D'Angelo JA, AikenML, Venu N, Yen EH, Wagner JS, Borawski JA, Pierce AT, Hershberg R, Blumberg RS, Lencer WI: Ca2+-dependent calmodulin binDing to FcRn affects immunoglobulin G transport in the transcytotic pathway. Mol Biol Cell 19: 414-423, 2008
41. MarzoloM-P, Yuseff MI, Retamal C, DonosoM, Ezquer F, Farfán P, Li Y, Bu G: Differential distribution of low-density lipoproteinreceptor-related protein (LRP) and megalin in polarized epithelial cells is determined by their cytoplasmic domains. Traffic 4: 273-288, 2003
42. Zhang H, Yoshioka S, Miyazaki M, Kannagi R, Suzuki A: Core 2 GlcNAc modification and megalin ligand-binDing activity. Biochim Biophys Acta 1780: 479-485, 2008
43. Yuseff MI, Farfan P, Bu G, Marzolo M-P: A cytoplasmic PPPSP motif determines megalin's phosphorylation and regulates receptor's recycling and surface expression. Traffic 8: 1215-1230, 2007
44. Coudroy G, Gburek J, Kozyraki R,Madsen M, Trugnan G,Moestrup SK, Verroust PJ, Maurice M: Contribution of cubilin and amnionless to processing and membrane targeting of cubilin-amnionless complex. J Am Soc Nephrol 16: 2330-2337, 2005
45. AseemO, Barth JL, Klatt SC, Smith BT, ArgravesWS:Cubilin expression is monoallelic and epigenetically augmented via PPARs. BMC Genomics 14: 405, 2013
46. SaravM,Wang Y, Hack BK, Chang A, Jensen M, Bao L,Quigg RJ: Renal FcRn reclaims albumin but facilitates elimination of IgG. J Am Soc Nephrol 20: 1941-1952, 2009
47. Hosaka K, Takeda T, Iino N, Hosojima M, Sato H, Kaseda R, Yamamoto K, Kobayashi A,Gejyo F, Saito A:Megalin and nonmuscle myosin heavy chain IIA interact with the adaptor protein Disabled-2 in proximal tubule cells. Kidney Int 75: 1308-1315, 2009
48. Koral K, Erkan E: PKB/Akt partners with Dab2 in albumin endocytosis. Am J Physiol Renal Physiol 302: F1013-F1024, 2012
49. Williams DB: Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J Cell Sci 119: 615-623, 2006
50. Wu VY, Shearman CW, Cohen MP: Identification of calnexin as a binDing protein for Amadori-modified glycated albumin. Biochem Biophys Res Commun 284: 602-606, 2001
51. Hall AM, Campanella M, Loesch A, Duchen MR, Unwin RJ: Albumin uptake in OK cells exposed to rotenone: a model for studying the effects of mitochondrial dysfunction on endocytosis in the proximal tubule? Nephron Physiol 115: p9-p19, 2010
52. Shelton LM, Park BK, Copple IM: Role of Nrf2 in protection against acute kidney injury. Kidney Int 84: 1090-1095, 2013
53. KurniatiNF, vanMeursM, VomHagen F, Jongman RM,Moser J, Zwiers PJ, Struys MMRF, Westra J, Zijlstra JG, Hammes H-P, Molema G, Heeringa P: Pleiotropic effects of angiopoietin-2 deficiency do not protect mice against endotoxin-induced acute kidney injury. Nephrol Dial Transplant 28: 567-575, 2013
54. Yuan HT, Khankin EV, Karumanchi SA, Parikh SM: Angiopoietin 2 is a partial agonist/antagonist of Tie2 signaling in the endothelium. Mol Cell Biol 29: 2011-2022, 2009
55. Molnar MZ, Kümpers P, Kielstein JT, Schiffer M, Czira ME, Ujszaszi A, Kovesdy CP, Mucsi I: Circulating Angiopoietin-2 levels predict mortality in kidney transplant recipients: a 4-year prospective case-cohort study. Transpl Int 27: 541-552, 2014
56. Zahr NM, Bell RL, Ringham HN, Sullivan EV,Witzmann FA, Pfefferbaum A: Ethanol-induced changes in the expression of proteins related to neurotransmission and metabolism in different regions of the rat brain. Pharmacol Biochem Behav 99: 428-436, 2011
57. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG: Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333, 2004
58. KoehlerG, Wilson RC,Goodpaster JV, Sønsteby A, Lai X,Witzmann FA, You J-S, Rohloff J, Randall SK, Alsheikh M: Proteomic study of lowtemperature responses in strawberry cultivars (Fragaria x ananassa) that differ in cold tolerance. Plant Physiol 159: 1787-1805, 2012
59. Keller A, Nesvizhskii AI, Kolker E, Aebersold R: Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392, 2002
60. Nesvizhskii AI, Keller A, Kolker E, Aebersold R: A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658, 2003
61. Najjar F, ZhouH,MorimotoT, Bruns JB, Li H-S, LiuW,KleymanTR,SatlinLM: DietaryK+regulates apicalmembraneexpressionof maxi-K channels in rabbit cortical collecting duct. Am J Physiol Renal Physiol 289: F922-F932, 2005