MicroRNA-30 family members regulate calcium/calcineurin signaling in podocytes

Journal of Clinical Investigation

Volumn 125, Issue 11, 2015, Pages 4091-4106

  Wu, Junnan ^a   Zheng, Chunxia ^a   Wang, Xiao ^a   Yun, Shifeng ^a   Zhao, Yue ^a   Liu, Lin ^a   Lu, Yuqiu ^a   Ye, Yuting ^a   Zhu, Xiaodong ^a   Zhang, Changming ^a   Shi, Shaolin ^a   Liu, Zhihong ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; CALCINEURIN; CALCIUM; CYCLOSPORIN A; F ACTIN; MESSENGER RNA; MICRORNA; MICRORNA 30; NFATC3 PROTEIN; PEPTIDES AND PROTEINS; PPP3CA PROTEIN; PPP3CB PROTEIN; PPP3R1 PROTEIN; PROTEIN; PUROMYCIN AMINONUCLEOSIDE; TACROLIMUS; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; UNCLASSIFIED DRUG; CALCINEURIN INHIBITOR; DOXORUBICIN; MIRN30 MICRORNA, HUMAN; MIRN30 MICRORNA, RAT; MIRN30D MICRORNA, MOUSE; TRANSCRIPTION FACTOR NFAT; TRANSIENT RECEPTOR POTENTIAL CHANNEL C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FOCAL GLOMERULOSCLEROSIS; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; RAT; ANIMAL; APOPTOSIS; BIOSYNTHESIS; CARDIAC MUSCLE CELL; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; CALCINEURIN; CALCINEURIN INHIBITORS; CALCIUM SIGNALING; CELLS, CULTURED; DOXORUBICIN; GENE EXPRESSION REGULATION; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; HUMANS; MICE; MICE, TRANSGENIC; MICRORNAS; MYOCYTES, CARDIAC; NFATC TRANSCRIPTION FACTORS; PODOCYTES; PROTEINURIA; RATS; RNA, MESSENGER; TACROLIMUS; TRANSFECTION; TRPC CATION CHANNELS;

EID: 84946780880     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI81061     Document Type: Article

References (66)

1. Kriz W, Gretz N, Lemley KV. Progression of glomerular diseases: is the podocyte the culprit? Kidney Int. 1998;54(3):687-697.
2. Shankland SJ. The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int. 2006;69(12):2131-2147.
3. Schiffer M, et al. Apoptosis in podocytes induced by TGF-beta and Smad7. J Clin Invest. 2001;108(6):807-816.
4. Shi S, et al. Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol. 2008;19(11):2159-2169.
5. Harvey SJ, et al. Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol. 2008;19(11):2150-2158.
6. Ho J, Ng KH, Rosen S, Dostal A, Gregory RI, Kreidberg JA. Podocyte-specific loss of functional microRNAs leads to rapid glom-erular and tubular injury. J Am Soc Nephrol. 2008;19(11):2069-2075.
7. Gebeshuber CA, et al. Focal segmental glom-erulosclerosis is induced by microRNA-193a and its downregulation of WT1. Nat Med. 2013;19(4):481-487.
8. Lin CL, et al. MicroRNA-29a promotion of nephrin acetylation ameliorates hyperglyce-mia-induced podocyte dysfunction. J Am Soc Nephrol. 2014;25(8):1698-1709.
9. Wu J, et al. Downregulation of microRNA-30 facilitates podocyte injury and is prevented by gluco-corticoids. J Am Soc Nephrol. 2014;25(1):92-104.
10. Shi S, et al. Smad2-dependent downregulation of miR-30 is required for TGF-β-induced apoptosis in podocytes. PLoS One. 2013;8(9):e75572.
11. Welsh GI, Saleem MA. The podocyte cytoskele-ton - key to a functioning glomerulus in health and disease. Nat Rev Nephrol. 2012;8(1):14-21.
12. Garg P, Holzman LB. Podocytes: gaining a foothold. Exp Cell Res. 2012;318(9):955-963.
13. Chuang PY, He JC. Signaling in regulation of podocyte phenotypes. Nephron Physiol. 2009;111(2):p9-p15.
14. Greka A, Mundel P. Calcium regulates podocyte actin dynamics. Semin Nephrol. 2012;32(4):319-326.
15. Chen S, et al. Calcium entry via TRPC6 mediates albumin overload-induced endoplasmic reticulum stress and apoptosis in podocytes. Cell Calcium. 2011;50(6):523-529.
16. Wang Y, et al. Activation of NFAT signaling in podocytes causes glomerulosclerosis. J Am Soc Nephrol. 2010;21(10):1657-1666.
17. Wang L, Chang JH, Paik SY, Tang Y, Eisner W, Spurney RF. Calcineurin (CN) activation promotes apoptosis of glomerular podocytes both in vitro and in vivo. Mol Endocrinol. 2011;25(8):1376-1386.
18. Kincaid R. Calmodulin-dependent protein phos-phatases from microorganisms to man. Adv Second Messenger Phosphoprotein Res. 1993;27:1-23.
19. Ueki K, Muramatsu T, Kincaid RL. Structure and expression of two isoforms of the murine calm-odulin-dependent protein phosphatase regulatory subunit (calcineurin B). Biochem Biophys Res Commun. 1992;187(1):537-543.
20. Mukai H, Chang CD, Tanaka H, Ito A, Kuno T, Tanaka C. cDNA cloning of a novel testis-specific calcineurin B-like protein. Biochem Biophys Res Commun. 1991;179(3):1325-1330.
21. Jain J, et al. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature. 1993;365(6444):352-355.
22. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science. 1999;284(5412):339-343.
23. Shibasaki F, Kondo E, Akagi T, McKeon F. Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature. 1997;386(6626):728-731.
24. Molkentin JD, et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 1998;93(2):215-228.
25. Gomez AM, Ruiz-Hurtado G, Benitah JP, Dominguez-Rodriguez A. Ca(2+) fluxes involvement in gene expression during cardiac hypertrophy. Curr Vasc Pharmacol. 2013;11(4):497-506.
26. Xie J, Cha SK, An SW, Kuro OM, Birnbaumer L, Huang CL. Cardioprotection by Klotho through downregulation of TRPC6 channels in the mouse heart. Nat Commun. 2012;3:1238.
27. Seo K, et al. Combined TRPC3 and TRPC6 blockade by selective small-molecule or genetic deletion inhibits pathological cardiac hypertrophy. Proc Natl Acad Sci USA. 2014;111(4):1551-1556.
28. Wu X, Eder P, Chang B, Molkentin JD. TRPC channels are necessary mediators of pathologic cardiac hypertrophy. Proc Natl Acad Sci USA. 2010;107(15):7000-7005.
29. Mukherjee A, Soto C. Role of calcineurin in neu-rodegeneration produced by misfolded proteins and endoplasmic reticulum stress. Curr Opin Cell Biol. 2011;23(2):223-230.
30. Woods NK, Padmanabhan J. Neuronal calcium signaling and Alzheimer's disease. Adv Exp Med Biol. 2012;740:1193-1217.
31. Winn MP, et al. A mutation in the TRPC6 cation channel causes familial focal segmental glomeru-losclerosis. Science. 2005;308(5729):1801-1804.
32. Dietrich A, Chubanov V, Gudermann T. Renal TRPathies. J Am Soc Nephrol. 2010;21(5):736-744.
33. Faul C, et al. The actin cytoskeleton of kidney podocytes is a direct target of the antipro-teinuric effect of cyclosporine A. Nat Med. 2008;14(9):931-938.
34. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007;45(9):593-605.
35. Moeller MJ, Sanden SK, Soofi A, Wiggins RC, Holzman LB. Podocyte-specific expression of cre recombinase in transgenic mice. Genesis. 2003;35(1):39-42.
36. Schiffer M, et al. Inhibitory smads and tgf-Beta signaling in glomerular cells. J Am Soc Nephrol. 2002;13(11):2657-2666.
37. Brukamp K, Jim B, Moeller MJ, Haase VH. Hypoxia and podocyte-specific Vhlh deletion confer risk of glomerular disease. Am J Physiol Renal Physiol. 2007;293(4):F1397-F1407.
38. Kambham N, et al. Congenital focal segmental glomerulosclerosis associated with beta4 integrin mutation and epidermolysis bullosa. Am J Kidney Dis. 2000;36(1):190-196.
39. Woroniecka KI, Park AS, Mohtat D, Thomas DB, Pullman JM, Susztak K. Transcriptome analysis of human diabetic kidney disease. Diabetes. 2011;60(9):2354-2369.
40. Obad S, et al. Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet. 2011;43(4):371-378.
41. Wei C, et al. Modification of kidney barrier function by the urokinase receptor. Nat Med. 2008;14(1):55-63.
42. Yu F, Deng H, Yao H, Liu Q, Su F, Song E. Mir-30 reduction maintains self-renewal and inhibits apoptosis in breast tumor-initiating cells. Oncogene. 2010;29(29):4194-4204.
43. Zhang B, et al. The calcineurin-NFAT pathway allows for urokinase receptor-mediated β3 integ-rin signaling to cause podocyte injury. J Mol Med (Berl). 2012;90(12):1407-1420.
44. Mallipattu SK, et al. Kruppel-like factor 6 regulates mitochondrial function in the kidney. J Clin Invest. 2015;125(3):1347-1361.
45. Li J, Donath S, Li Y, Qin D, Prabhakar BS, Li P. miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet. 2010;6(1):e1000795.
46. Nijenhuis T, et al. Angiotensin II contributes to podocyte injury by increasing TRPC6 expression via an NFAT-mediated positive feedback signaling pathway. Am J Pathol. 2011;179(4):1719-1732.
47. 2+ current impairs salivary gland fluid secretion in TRPC1(-/-) mice. Proc Natl Acad Sci USA. 2007;104(44):17542-17547.
48. Sonneveld R, et al. Glucose specifically regulates TRPC6 expression in the podocyte in an AngII-dependent manner. Am J Pathol. 2014;184(6):1715-1726.
49. Yang H, et al. High glucose-induced apoptosis in cultured podocytes involves TRPC6-dependent calcium entry via the RhoA/ROCK pathway. Biochem Biophys Res Commun. 2013;434(2):394-400.
50. Dietrich A, Fahlbusch M, Gudermann T. Classical Transient Receptor Potential 1 (TRPC1): channel or channel regulator? Cells. 2014;3(4):939-962.
51. Wiggins RC. The spectrum of podocytopathies: a unifying view of glomerular diseases. Kidney Int. 2007;71(12):1205-1214.
52. Ma F, et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat Immunol. 2011;12(9):861-869.
53. Wharram BL, et al. Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. J Am Soc Nephrol. 2005;16(10):2941-2952.
54. Moller CC, et al. Induction of TRPC6 channel in acquired forms of proteinuric kidney disease. J Am Soc Nephrol. 2007;18(1):29-36.
55. Croce N, et al. NPY modulates miR-30a-5p and BDNF in opposite direction in an in vitro model of Alzheimer disease: a possible role in neuroprotection? Mol Cell Biochem. 2013;376(1-2):189-195.
56. Mellios N, Huang HS, Grigorenko A, Rogaev E, Akbarian S. A set of differentially expressed miRNAs, including miR-30a-5p, act as post-tran-scriptional inhibitors of BDNF in prefrontal cortex. Hum Mol Genet. 2008;17(19):3030-3042.
57. Rastaldi MP, et al. Glomerular podocytes contain neuron-like functional synaptic vesicles. FASEB J. 2006;20(7):976-978.
58. Boerries M, et al. Molecular fingerprinting of the podocyte reveals novel gene and protein regulatory networks. Kidney Int. 2013;83(6):1052-1064.
59. Nakamura A, Imaizumi A, Yanagawa Y, Kohsaka T, Johns EJ. β(2)-Adrenoceptor activation attenuates endotoxin-induced acute renal failure. J Am Soc Nephrol. 2004;15(2):316-325.
60. Wang X, et al. Histone deacetylase 4 selectively contributes to podocyte injury in diabetic neph-ropathy. Kidney Int. 2014;86(4):712-725.
61. van den Berg JG, van den Bergh Weerman MA, Assmann KJ, Weening JJ, Florquin S. Podocyte foot process effacement is not correlated with the level of proteinuria in human glomerulopathies. Kidney Int. 2004;66(5):1901-1906.
62. Zhou Y, et al. Peroxisome proliferator-activated receptor-alpha is renoprotective in doxoru-bicin-induced glomerular injury. Kidney Int. 2011;79(12):1302-1311.
63. Venkatareddy M, et al. Estimating podocyte number and density using a single histologic section. J Am Soc Nephrol. 2014;25(5):1118-1129.
64. Saleem MA, et al. A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol. 2002;13(3):630-638.
65. 2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985;260(6):3440-3450.
66. Asano T, Matsusaka T, Mizutani S, Ichikawa I. Rapid downregulation of β-actin-based CAG promoter and filamentous actin in injured podocytes. J Med Dent Sci. 2005;52(2):129-134.