Essential role of X-box binding protein-1 during endoplasmic reticulum stress in podocytes

Journal of the American Society of Nephrology

Volumn 27, Issue 4, 2016, Pages 1055-1065

  Hassan, Hossam ^a   Tian, Xuefei ^a   Inoue, Kazunori ^a   Chai, Nathan ^a   Liu, Chang ^a   Soda, Keita ^a   Moeckel, Gilbert ^a   Tufro, Alda ^a   Lee, Ann Hwee ^b   Somlo, Stefan ^a   Fedeles, Sorin ^a   Ishibe, Shuta ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CHAPERONE; HISTONE H3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN SEC63; STRESS ACTIVATED PROTEIN KINASE; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; REGULATORY FACTOR X TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; XBP1 PROTEIN, MOUSE;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; END STAGE RENAL DISEASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GLOMERULOSCLEROSIS; HISTOLOGY; MOUSE; NEPHROTOXICITY; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MISFOLDING; RNA SPLICING; UNFOLDED PROTEIN RESPONSE; ANIMAL; CELL CULTURE; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; MICE; PODOCYTES; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; X-BOX BINDING PROTEIN 1;

EID: 85017085981     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015020191     Document Type: Article

References (41)

1. Cybulsky AV: The intersecting roles of endoplasmic reticulum stress, ubiquitin- proteasome system, and autophagy in the pathogenesis of proteinuric kidney disease. Kidney Int 84: 25–33, 2013
2. Inagi R, Ishimoto Y, Nangaku M: Proteostasis in endoplasmic reticulum—new mechanisms in kidney disease. Nat Rev Nephrol 10: 369–378, 2014
3. Inagi R: Endoplasmic reticulum stress as a progression factor for kidney injury. Curr Opin Pharmacol 10: 156–165, 2010
4. Walter P, Ron D: The unfolded protein response: from stress pathway to homeostatic regulation. Science 334: 1081–1086, 2011
5. Chen YM, Zhou Y, Go G, Marmerstein JT, Kikkawa Y, Miner JH: Laminin b2 gene missense mutation produces endoplasmic reticulum stress in podocytes. J Am Soc Nephrol 24: 1223–1233, 2013
6. Pieri M, Stefanou C, Zaravinos A, Erguler K, Stylianou K, Lapathitis G, Karaiskos C, Savva I, Paraskeva R, Dweep H, Sticht C, Anastasiadou N, Zouvani I, Goumenos D, Felekkis K, Saleem M, Voskarides K, Gretz N, Deltas C: Evidence for activation of the unfolded protein response in collagen IV nephropathies. J Am Soc Nephrol 25: 260–275, 2014
7. Ito N, Nishibori Y, Ito Y, Takagi H, Akimoto Y, Kudo A, Asanuma K, Sai Y, Miyamoto K, Takenaka H, Yan K: mTORC1 activation triggers the unfolded protein response in podocytes and leads to nephrotic syndrome. Lab Invest 91: 1584–1595, 2011
8. Inagi R, Nangaku M, Onogi H, Ueyama H, Kitao Y, Nakazato K, Ogawa S, Kurokawa K, Couser WG, Miyata T: Involvement of endoplasmic reticulum (ER) stress in podocyte injury induced by excessive protein accumulation. Kidney Int 68: 2639–2650, 2005
9. Fedeles SV, Tian X, Gallagher AR, Mitobe M, Nishio S, Lee SH, Cai Y, Geng L, Crews CM, Somlo S: A genetic interaction network of five genes for human polycystic kidney and liver diseases defines poly-cystin-1 as the central determinant of cyst formation. Nat Genet 43: 639–647, 2011
10. Fedeles SV, So JS, Shrikhande A, Lee SH, Gallagher AR, Barkauskas CE, Somlo S, Lee AH: Sec63 and Xbp1 regulate IRE1a activity and polycystic disease severity. J Clin Invest 125: 1955–1967, 2015
11. Lang S, Benedix J, Fedeles SV, Schorr S, Schirra C, Schäuble N, Jalal C, Greiner M, Hassdenteufel S, Tatzelt J, Kreutzer B, Edelmann L, Krause E, Rettig J, Somlo S, Zimmermann R, Dudek J: Different effects of Sec61a, Sec62 and Sec63 depletion on transport of polypeptides into the endoplasmic reticulum of mammalian cells. J Cell Sci 125: 1958–1969, 2012
12. Lee AH, Scapa EF, Cohen DE, Glimcher LH: Regulation of hepatic lipo-genesis by the transcription factor XBP1. Science 320: 1492–1496, 2008
13. Jurczak MJ, Lee AH, Jornayvaz FR, Lee HY, Birkenfeld AL, Guigni BA, Kahn M, Samuel VT, Glimcher LH, Shulman GI: Dissociation of inositol-requiring enzyme (IRE1a)-mediated c-Jun N-terminal kinase activation from hepatic insulin resistance in conditional X-box-binding protein-1 (XBP1) knock-out mice. J Biol Chem 287: 2558–2567, 2012
14. Lee AS: Glucose-regulated proteins in cancer: Molecular mechanisms and therapeutic potential. Nat Rev Cancer 14: 263–276, 2014
15. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB: Podocyte-specific expression of cre recombinase in transgenic mice. Genesis 35: 39–42, 2003
16. Flanc RS, Ma FY, Tesch GH, Han Y, Atkins RC, Bennett BL, Friedman GC, Fan JH, Nikolic-Paterson DJ: A pathogenic role for JNK signaling in experimental anti-GBM glomerulonephritis. Kidney Int 72: 698–708, 2007
17. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D: Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664–666, 2000
18. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, Tohyama M: Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 276: 13935–13940, 2001
19. Tewari M, Quan LT, O’Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM: Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81: 801–809, 1995
20. Chaitanya GV, Steven AJ, Babu PP: PARP-1 cleavage fragments: Signatures of cell-death proteases in neurodegeneration. Cell Commun Signal 8: 31, 2010
21. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC: Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371: 346–347, 1994
22. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P: Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 5: a013169, 2013
23. He F, Chen S, Wang H, Shao N, Tian X, Jiang H, Liu J, Zhu Z, Meng X, Zhang C: Regulation of CD2-associated protein influences podocyte endoplasmic reticulum stress-mediated apoptosis induced by albumin overload. Gene 484: 18–25, 2011
24. Chen S, He FF, Wang H, Fang Z, Shao N, Tian XJ, Liu JS, Zhu ZH, Wang YM, Wang S, Huang K, Zhang C: Calcium entry via TRPC6 mediates albumin overload-induced endoplasmic reticulum stress and apoptosis in podocytes. Cell Calcium 50: 523–529, 2011
25. Cybulsky AV, Takano T, Papillon J, Bijian K: Role of the endoplasmic reticulum unfolded protein response in glomerular epithelial cell injury. J Biol Chem 280: 24396–24403, 2005
26. Zhang MZ, Wang Y, Paueksakon P, Harris RC: Epidermal growth factor receptor inhibition slows progression of diabetic nephropathy in association with a decrease in endoplasmic reticulum stress and an increase in autophagy. Diabetes 63: 2063–2072, 2014
27. Chen J, Guo Y, Zeng W, Huang L, Pang Q, Nie L, Mu J, Yuan F, Feng B: ER stress triggers MCP-1 expression through SET7/9-induced histone methylation in the kidneys of db/db mice. Am J Physiol Renal Physiol 306: F916–F925, 2014
28. Cybulsky AV, Kennedy CR: Podocyte injury associated with mutant a-actinin-4. J Signal Transduct 2011: 563128, 2011
29. Cybulsky AV, Takano T, Papillon J, Bijian K, Guillemette J, Kennedy CR: Glomerular epithelial cell injury associated with mutant alpha-actinin-4. Am J Physiol Renal Physiol 297: F987–F995, 2009
30. Hartleben B, Gödel M, Meyer-Schwesinger C, Liu S, Ulrich T, Köbler S, Wiech T, Grahammer F, Arnold SJ, Lindenmeyer MT, Cohen CD, Pavenstädt H, Kerjaschki D, Mizushima N, Shaw AS, Walz G, Huber TB: Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J Clin Invest 120: 1084–1096, 2010
31. Inoki K, Mori H, Wang J, Suzuki T, Hong S, Yoshida S, Blattner SM, Ikenoue T, Rüegg MA, Hall MN, Kwiatkowski DJ, Rastaldi MP, Huber TB, Kretzler M, Holzman LB, Wiggins RC, Guan KL: mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Invest 121: 2181–2196, 2011
32. Cheng Y, Yang JM: Survival and death of endoplasmic-reticulum-stressed cells: role of autophagy. World J Biol Chem 2: 226–231, 2011
33. Ijaz A, Tejada T, Catanuto P, Xia X, Elliot SJ, Lenz O, Jauregui A, Saenz MO, Molano RD, Pileggi A, Ricordi C, Fornoni A: Inhibition of C-jun N-terminal kinase improves insulin sensitivity but worsens albuminuria in experimental diabetes. Kidney Int 75: 381–388, 2009
34. Gebeshuber CA, Kornauth C, Dong L, Sierig R, Seibler J, Reiss M, Tauber S, Bilban M, Wang S, Kain R, Böhmig GA, Moeller MJ, Gröne HJ, Englert C, Martinez J, Kerjaschki D: Focal segmental glomerulosclerosis is induced by microRNA-193a and its downregulation of WT1. Nat Med 19: 481–487, 2013
35. Guo G, Morrison DJ, Licht JD, Quaggin SE: WT1 activates a glomerular-specific enhancer identified from the human nephrin gene. J Am Soc Nephrol 15: 2851–2856, 2004
36. 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
37. Matsusaka T, Xin J, Niwa S, Kobayashi K, Akatsuka A, Hashizume H, Wang QC, Pastan I, Fogo AB, Ichikawa I: Genetic engineering of glomerular sclerosis in the mouse via control of onset and severity of podocyte-specific injury. J Am Soc Nephrol 16: 1013–1023, 2005
38. Guo JK, Marlier A, Shi H, Shan A, Ardito TA, Du ZP, Kashgarian M, Krause DS, Biemesderfer D, Cantley LG: Increased tubular proliferation as an adaptive response to glomerular albuminuria. J Am Soc Nephrol 23: 429–437, 2012
39. Soda K, Balkin DM, Ferguson SM, Paradise S, Milosevic I, Giovedi S, Volpicelli-Daley L, Tian X, Wu Y, Ma H, Son SH, Zheng R, Moeckel G, Cremona O, Holzman LB, De Camilli P, Ishibe S: Role of dynamin, synaptojanin, and endophilin in podocyte foot processes. J Clin Invest 122: 4401–4411, 2012
40. Tian X, Kim JJ, Monkley SM, Gotoh N, Nandez R, Soda K, Inoue K, Balkin DM, Hassan H, Son SH, Lee Y, Moeckel G, Calderwood DA, Holzman LB, Critchley DR, Zent R, Reiser J, Ishibe S: Podocyte-associated talin1 is critical for glomerular filtration barrier maintenance. J Clin Invest 124: 1098–1113, 2014
41. Ma H, Togawa A, Soda K, Zhang J, Lee S, Ma M, Yu Z, Ardito T, Czyzyk J, Diggs L, Joly D, Hatakeyama S, Kawahara E, Holzman L, Guan JL, Ishibe S: Inhibition of podocyte FAK protects against proteinuria and foot process effacement. J Am Soc Nephrol 21: 1145–1156, 2010