Calcineurin (CN) activation promotes apoptosis of glomerular podocytes both in vitro and in vivo

Molecular Endocrinology

Volumn 25, Issue 8, 2011, Pages 1376-1386

  Wang, Liming ^a   Chang, Jae Hyung ^a   Paik, Seung Yeol ^b   Tang, Yuping ^a   Eisner, William ^a   Spurney, Robert F ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Chung Ang University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; CALCINEURIN; CYCLOOXYGENASE 2; ENDOTHELIN 1; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; PROSTAGLANDIN E2; PROSTAGLANDIN RECEPTOR; TACROLIMUS; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; REPORTER GENE; SIGNAL TRANSDUCTION;

ALBUMINURIA; ANIMALS; APOPTOSIS; BLOOD GLUCOSE; CALCINEURIN; CYCLOOXYGENASE 2; DENSITOMETRY; DINOPROSTONE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; KIDNEY GLOMERULUS; MICE; MODELS, BIOLOGICAL; NFATC TRANSCRIPTION FACTORS; OLIGOPEPTIDES; PODOCYTES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TACROLIMUS;

MUS;

EID: 79960972131     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-0029     Document Type: Article

References (52)

1. U.S. Renal Data System, USRDS 2010 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States. Bethesda, MD: NIH, National Institute of Diabetes and Digestive and Kidney Diseases
2. Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, Remuzzi G, Snapinn SM, Zhang Z, Shahinfar S 2001 Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 345:861-869
3. Wolf G, Chen S, Ziyadeh FN 2005 From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 54:1626-1634
4. Meyer TW, Bennett PH, Nelson RG 1999 Podocyte number predicts long-term urinary albumin excretion in Pima Indians with type II diabetes and microalbuminuria. Diabetologia 42:1341-1344
5. White KE, Bilous RW, Marshall SM, El-Nahas M, Remuzzi G, Piras G, De Cosmo S, Viberti G 2002 Podocyte number in normotensive type 1 diabetic patients with albuminuria. Diabetes 51:3083-3089
6. Dalla Vestra M, Masiero A, Roiter AM, Saller A, Crepaldi G, Fioretto P 2003 Is podocyte injury relevant in diabetic nephropathy? Studies in patients with type 2 diabetes. Diabetes 52:1031-1035
7. Wiggins RC 2007 The spectrum of podocytopathies: a unifying view of glomerular diseases. Kidney Int 71:1205-1214
8. Ronconi E, Sagrinati C, Angelotti ML, Lazzeri E, Mazzinghi B, Ballerini L, Parente E, Becherucci F, Gacci M, Carini M, Maggi E, Serio M, Vannelli GB, Lasagni L, Romagnani S, Romagnani P 2009 Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 20:322-332
9. Susztak K, Raff AC, Schiffer M, Bottinger EP 2006 Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 55:225-233
10. Verzola D, Gandolfo MT, Ferrario F, Rastaldi MP, Villaggio B, Gianiorio F, Giannoni M, Rimoldi L, Lauria F, Miji M, Deferrari G, Garibotto G 2007 Apoptosis in the kidneys of patients with type II diabetic nephropathy. Kidney Int 72:1262-1272
11. Gooch JL, Barnes JL, Garcia S, Abboud HE 2003 Calcineurin is activated in diabetes and is required for glomerular hypertrophy and ECM accumulation. Am J Physiol Renal Physiol 284:F144-F154
12. Gooch JL, Gorin Y, Zhang BX, Abboud HE 2004 Involvement of calcineurin in transforming growth factor-β-mediated regulation of extracellular matrix accumulation. J Biol Chem 279:15561-15570
13. Schiffer M, Bitzer M, Roberts IS, Kopp JB, ten Dijke P, Mundel P, Bottinger EP 2001 Apoptosis in podocytes induced by TGF-β and Smad7. J Clin Invest 108:807-816
14. Ding G, Reddy K, Kapasi AA, Franki N, Gibbons N, Kasinath BS, Singhal PC 2002 Angiotensin II induces apoptosis in rat glomerular epithelial cells. Am J Physiol Renal Physiol 283:F173-F180
15. Jia J, Ding G, Zhu J, Chen C, Liang W, Franki N, Singhal PC 2008 Angiotensin II infusion induces nephrin expression changes and podocyte apoptosis. Am J Nephrol 28:500-507
16. Winn MP, Daskalakis N, Spurney RF, Middleton JP 2006 Unexpected role of TRPC6 channel in familial nephrotic syndrome: does it have clinical implications? J Am Soc Nephrol 17:378-387
17. Makino H, Tanaka I, Mukoyama M, Sugawara A, Mori K, Muro S, Suganami T, Yahata K, Ishibashi R, Ohuchida S, Maruyama T, Narumiya S, Nakao K 2002 Prevention of diabetic nephropathy in rats by prostaglandin E receptor EP1-selective antagonist. J Am Soc Nephrol 13:1757-1765
18. Wenzel RR, Littke T, Kuranoff S, Jurgens C, Bruck H, Ritz E, Philipp T, Mitchell A 2009 Avosentan reduces albumin excretion in diabetics with macroalbuminuria. J Am Soc Nephrol 20:655-664
19. Kontessis PS, Jones SL, Barrow SE, Stratton PD, Alessandrini P, De Cosmo S, Ritter JM, Viberti GC 1993 Effect of selective inhibition of thromboxane synthesis on renal function in diabetic nephropathy. J Lab Clin Med 121:415-423
20. Rao A, Luo C, Hogan PG 1997 Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15:707-747
21. Wang L, Flannery PJ, Rosenberg PB, Fields TA, Spurney RF 2008 Gq-dependent signaling upregulates COX2 in glomerular podo-cytes. J Am Soc Nephrol 19:2108-2118
22. Asai M, Iwasaki Y, Yoshida M, Mutsuga-Nakayama N, Arima H, Ito M, Takano K, Oiso Y 2004 Nuclear factor of activated T cells (NFAT) is involved in the depolarization-induced activation of growth hormone-releasing hormone gene transcription in vitro. Mol Endocrinol 18:3011-3019
23. Becker-Hapak M, McAllister SS, Dowdy SF 2001 TAT-mediated protein transduction into mammalian cells. Methods 24:247-256
24. Kalinec G, Nazarali AJ, Hermouet S, Xu N, Gutkind JS 1992 Mutated a subunit of the Gq protein induces malignant transformation in NIH 3T3 cells. Mol Cell Biol 12:4687-4693
25. Boss V, Abbott KL, Wang XF, Pavlath GK, Murphy TJ 1998 The cyclosporin A-sensitive nuclear factor of activated T cells (NFAT) proteins are expressed in vascular smooth muscle cells. Differential localization of NFAT isoforms and induction of NFAT-mediated transcription by phospholipase C-coupled cell surface receptors. J Biol Chem 273:19664-19671
26. Ruff VA, Leach KL 1995 Direct demonstration of NFATp dephos-phorylation and nuclear localization in activated HT-2 cells using a specific NFATp polyclonal antibody. J Biol Chem 270:22602-22607
27. Rothermel BA, McKinsey TA, Vega RB, Nicol RL, Mammen P, Yang J, Antos CL, Shelton JM, Bassel-Duby R, Olson EN, Williams RS 2001 Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc Natl Acad Sci USA 98: 3328-3333
28. Kuwahara K, Wang Y, McAnally J, Richardson JA, Bassel-Duby R, Hill JA, Olson EN 2006 TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J Clin Invest 116:3114-3126
29. Ortmann J, Amann K, Brandes RP, Kretzler M, Münter K, Parekh N, Traupe T, Lange M, Lattmann T, Barton M 2004 Role of podocytes for reversal of glomerulosclerosis and proteinuria in the aging kidney after endothelin inhibition. Hypertension 44:974-981
30. Akhter SA, Luttrell LM, Rockman HA, Iaccarino G, Lefkowitz RJ, Koch WJ 1998 Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy. Science 280:574-577
31. Shibasaki F, Hallin U, Uchino H 2002 Calcineurin as a multifunctional regulator. J Biochem 131:1-15
32. Aramburu J, Yaffe MB, Lopez-Rodriguez C, Cantley LC, Hogan PG, Rao A 1999 Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 285:2129-2133
33. O'Keefe SJ, Tamura J, Kincaid RL, Tocci MJ, O'Neill EA 1992 FK-506- and CsA-sensitive activation of the interleukin-2 promoter by calcineurin. Nature 357:692-694
34. Iniguez MA, Martinez-Martinez S, Punzon C, Redondo JM, Fresno M 2000 An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J Biol Chem 275:23627-23635
35. Parashar B, Latha Shankar S, O'Guin K, Butler J, Vikram B, Shafit-Zagardo B 2005 Inhibition of human neuroblastoma cell growth by CAY10404, a highly selective Cox-2 inhibitor. J Neurooncol 71: 141-148
36. Lee SH, Williams MV, Dubois RN, Blair IA 2005 Cyclooxygenase-2-mediated DNA damage. J Biol Chem 280:28337-28346
37. Wilcox CS, Pearlman A 2008 Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 60:418-469
38. Matsuo M, Yoshida N, Zaitsu M, Ishii K, Hamasaki Y 2004 Inhibition of human glioma cell growth by a PHS-2 inhibitor, NS398, and a prostaglandin E receptor subtype EP1-selective antagonist, SC51089. J Neurooncol 66:285-292
39. Serfling E, Chuvpilo S, Liu J, Hofer T, Palmetshofer A 2006 NFATc1 autoregulation: a crucial step for cell-fate determination. Trends Immunol 27:461-469
40. Armbruster DA 1987 Fructosamine: structure, analysis, and clinical usefulness. Clin Chem 33:2153-2163
41. Mathieson PW 2008 Proteinuria and immunity-an overstated relationship? N Engl J Med 359:2492-2494
42. Faul C, Donnelly M, Merscher-Gomez S, Chang YH, Franz S, Delf-gaauw J, Chang JM, Choi HY, Campbell KN, Kim K, Reiser J, Mundel P 2008 The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine A. Nat Med 14:931-938
43. Czirjak G, Enyedi P 2006 Targeting of calcineurin to anNFAT-like docking site is required for the calcium-dependent activation of the background K+ channel, TRESK. J Biol Chem 281:14677-14682
44. Hogan PG, Chen L, Nardone J, Rao A 2003 Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 17:2205-2232
45. Cheng HF, Wang CJ, Moeckel GW, Zhang MZ, McKanna JA, Harris RC 2002 Cyclooxygenase-2 inhibitor blocks expression of mediators of renal injury in a model of diabetes and hypertension. Kidney Int 62:929-939
46. FitzGerald GA, Patrono C 2001 The coxibs, selective inhibitors of cyclooxygenase-2. N Engl J Med 345:433-442
47. Wang Y, Jarad G, Tripathi P, Pan M, Cunningham J, Martin DR, Liapis H, Miner JH, Chen F 2010 Activation of NFAT signaling in podocytes causes glomerulosclerosis. J Am Soc Nephrol 21:1657-1666
48. Cheng H, Wang S, Jo YI, Hao CM, Zhang M, Fan X, Kennedy C, Breyer MD, Moeckel GW, Harris RC 2007 Overexpression of cyclooxygenase-2 predisposes to podocyte injury. J Am Soc Nephrol 18:551-559
49. Gaston RS 2009 Chronic calcineurin inhibitor nephrotoxicity: reflections on an evolving paradigm. Clin J Am Soc Nephrol 4:2029-2034
50. Lee JI, Burckart GJ 1998 Nuclear factor k B: important transcription factor and therapeutic target. J Clin Pharmacol 38:981-993
51. Noguchi H, Matsushita M, Okitsu T, Moriwaki A, Tomizawa K, Kang S, Li ST, Kobayashi N, Matsumoto S, Tanaka K, Tanaka N, Matsui H 2004 A new cell-permeable peptide allows successful allogeneic islet transplantation in mice. Nat Med 10:305-309
52. Wang L, Gesty-Palmer D, Fields TA, Spurney RF 2009 Inhibition of WNT signaling by G protein-coupled receptor (GPCR) kinase 2 (GRK2). Mol Endocrinol 23:1455-1465