Endoplasmic Reticulum Stress Predicts Clinical Response to Cyclosporine Treatment in Primary Membranous Nephropathy

American Journal of Nephrology

Volumn 43, Issue 5, 2016, Pages 348-356

  Tao, Jianling ^a,b   Zhang, Wei ^a   Wen, Yubing ^a   Sun, Ying ^a   Chen, Limeng ^a   Li, Hang ^a   Li, Mingxi ^a   Li, Xuewang ^a   Lafayette, Richard A ^b   Li, Xuemei ^a  

^a PEKING UNION MEDICAL COLLEGE   (China)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcineurin; Cyclosporine; Endoplasmic reticulum stress; Glucose regulated protein 78; Primary membranous nephropathy

Indexed keywords

ALBUMIN; CALCINEURIN; CYCLOSPORIN; GLUCOSE REGULATED PROTEIN 78; PREDNISONE; CALCINEURIN INHIBITOR; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78;

ADULT; ALBUMIN BLOOD LEVEL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM STRESS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY DISTAL TUBULE; MAJOR CLINICAL STUDY; MALE; MEMBRANOUS GLOMERULONEPHRITIS; PODOCYTE; PREDICTION; PRIMARY MEMBRANOUS NEPHROPATHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEINURIA; REMISSION; RETROSPECTIVE STUDY; TREATMENT OUTCOME; AGED; BLOOD; KIDNEY; METABOLISM; MIDDLE AGED;

ADULT; AGED; CALCINEURIN; CALCINEURIN INHIBITORS; CYCLOSPORINE; ENDOPLASMIC RETICULUM STRESS; FEMALE; GLOMERULONEPHRITIS, MEMBRANOUS; HEAT-SHOCK PROTEINS; HUMANS; KIDNEY; MALE; MIDDLE AGED; RETROSPECTIVE STUDIES;

EID: 84966775976     PISSN: 02508095     EISSN: 14219670     Source Type: Journal    
DOI: 10.1159/000446293     Document Type: Article

References (34)

1. Schieppati A, Mosconi L, Perna A, Mecca G, Bertani T, Garattini S, Remuzzi G: Prognosis of untreated patients with idiopathic membranous nephropathy. N Engl J Med 1993; 329: 85-89.
2. Cattran DC, Alexopoulos E, Heering P, Hoyer PF, Johnston A, Meyrier A, Ponticelli C, Saito T, Choukroun G, Nachman P, Praga M, Yoshikawa N: Cyclosporin in idiopathic glomerular disease associated with the nephrotic syndrome: workshop recommendations. Kidney Int 2007; 72: 1429-1447.
3. Radhakrishnan J, Cattran DC: The KDIGO practice guideline on glomerulonephritis: reading between the (guide)lines-application to the individual patient. Kidney Int 2012; 82: 840-856.
4. Chapman JR, Nankivell BJ: Nephrotoxicity of ciclosporin A: short-term gain, long-term pain? Nephrol Dial Transplant 2006; 21: 2060-2063.
5. Wakamatsu A, Fukusumi Y, Hasegawa E, Tomita M, Watanabe T, Narita I, Kawachi H: Role of calcineurin (CN) in kidney glomerular podocyte: CN inhibitor ameliorated proteinuria by inhibiting the redistribution of CN at the slit diaphragm. Physiol Rep 2016; 4:pii:e12679.
6. Kung L, Batiuk TD, Palomo-Pinon S, Noujaim J, Helms LM, Halloran PF: Tissue distribution of calcineurin and its sensitivity to inhibition by cyclosporine. Am J Transplant 2001; 1: 325-333.
7. Naesens M, Kuypers DR, Sarwal M: Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009; 4: 481-508.
8. Taniguchi M, Yoshida H: Endoplasmic reticulum stress in kidney function and disease. Curr Opin Nephrol Hypertens 2015; 24: 345-350.
9. Hendershot LM, Valentine VA, Lee AS, Morris SW, Shapiro DN: Localization of the gene encoding human BiP/GRP78, the endoplasmic reticulum cognate of the HSP70 family, to chromosome 9q34. Genomics 1994; 20: 281-284.
10. Wang M, Wey S, Zhang Y, Ye R, Lee AS: Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders. Antioxid Redox Signal 2009; 11: 2307-2316.
11. Rao RV, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T, Goldsmith PC, Ellerby LM, Ellerby HM, Bredesen DE: Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett 2002; 514: 122-128.
12. Ohse T, Inagi R, Tanaka T, Ota T, Miyata T, Kojima I, Ingelfinger JR, Ogawa S, Fujita T, Nangaku M: Albumin induces endoplasmic reticulum stress and apoptosis in renal proximal tubular cells. Kidney Int 2006; 70: 1447-1455.
13. Fang L, Xie D, Wu X, Cao H, Su W, Yang J: Involvement of endoplasmic reticulum stress in albuminuria induced inflammasome activation in renal proximal tubular cells. PLoS One 2013; 8:e72344.
14. Gorostizaga A, Mori Sequeiros Garcia 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 2013; 206: 47-54.
15. 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 2011; 50: 523-529.
16. Hu RR, Ma J, Tao JL, Wen YB, Zhao C, Zhang W, Li H, Li MX, Li XM, Li XW: [Expression of calcineurin in podocytes in response to endoplasmic reticulum stress in diabetic nephropathy]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 2014; 36: 477-481.
17. Pallet N, Bouvier N, Bendjallabah A, Rabant M, Flinois JP, Hertig A, Legendre C, Beaune P, Thervet E, Anglicheau D: Cyclosporine-induced endoplasmic reticulum stress triggers tubular phenotypic changes and death. Am J Transplant 2008; 8: 2283-2296.
18. Sarro E, Jacobs-Cacha C, Itarte E, Meseguer A: A pharmacologically-based array to identify targets of cyclosporine A-induced toxicity in cultured renal proximal tubule cells. Toxicol Appl Pharmacol 2012; 258: 275-287.
19. Xie G, Xu J, Ye C, Chen D, Xu C, Yang L, Ma Y, Hu X, Li L, Sun L, Zhao X, Mao Z, Mei C: Immunosuppressive treatment for nephrotic idiopathic membranous nephropathy: a meta-analysis based on Chinese adults. PLoS One 2012; 7:e44330.
20. Cattran DC, Appel GB, Hebert LA, Hunsicker LG, Pohl MA, Hoy WE, Maxwell DR, Kunis CL; North America Nephrotic Syndrome Study Group: Cyclosporine in patients with steroid-resistant membranous nephropathy: a randomized trial. Kidney Int 2001; 59: 1484-1490.
21. Tran TH, Hughes GJ, Greenfeld C, Pham JT: Overview of current and alternative therapies for idiopathic membranous nephropathy. Pharmacotherapy 2015; 35: 396-411.
22. Yoshida H: ER stress and diseases. FEBS J 2007; 274: 630-658.
23. Markan S, Kohli HS, Joshi K, Minz RW, Sud K, Ahuja M, Anand S, Khullar M: Up regulation of the GRP-78 and GADD-153 and down regulation of Bcl-2 proteins in primary glomerular diseases: a possible involvement of the ER stress pathway in glomerulonephritis. Mol Cell Biochem 2009; 324: 131-138.
24. Inagi R: Endoplasmic reticulum stress as a progression factor for kidney injury. Curr Opin Pharmacol 2010; 10: 156-165.
25. Cybulsky AV: The intersecting roles of endoplasmic reticulum stress, ubiquitin-proteasome system, and autophagy in the pathogenesis of proteinuric kidney disease. Kidney Int 2013; 84: 25-33.
26. Fervenza FC: Overcoming calcineurin dependence in membranous nephropathy: is rituximab the answer? Clin J Am Soc Nephrol 2009; 4: 1017-1019.
27. Zhang B, Shi W: Is the antiproteinuric effect of cyclosporine A independent of its immunosuppressive function in T cells? Int J Nephrol 2012; 2012: 809456.
28. Faul C, Donnelly M, Merscher-Gomez S, Chang YH, Franz S, Delfgaauw J, Chang JM, Choi HY, Campbell KN, Kim K, Reiser J, Mundel P: The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine A. Nat Med 2008; 14: 931-938.
29. Descazeaud V, Mestre E, Marquet P, Essig M: Calcineurin regulation of cytoskeleton organization: a new paradigm to analyse the effects of calcineurin inhibitors on the kidney. J Cell Mol Med 2012; 16: 218-227.
30. Gooch JL, Toro JJ, Guler RL, Barnes JL: Calcineurin A-alpha but not A-beta is required for normal kidney development and function. Am J Pathol 2004; 165: 1755-1765.
31. Sankaranarayanan TK, Sethi BK, Subramanyam C: Serum calcineurin activity in relation to oxidative stress and glycemic control in type II diabetes mellitus. Clin Biochem 2005; 38: 218-222.
32. Cybulsky AV: Endoplasmic reticulum stress in proteinuric kidney disease. Kidney Int 2010; 77: 187-193.
33. Kurji K, Sharma RK: Potential role of calcineurin in pathogenic conditions. Mol Cell Biochem 2010; 338: 133-141.
34. McQuarrie EP, Stirling CM, Geddes CC: Idiopathic membranous nephropathy and nephrotic syndrome: outcome in the era of evidence-based therapy. Nephrol Dial Transplant 2012; 27: 235-242.