Smad2-Dependent Downregulation of miR-30 Is Required for TGF-β-Induced Apoptosis in Podocytes

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Shi, Shaolin ^a   Yu, Liping ^a   Zhang, Taoran ^a   Qi, Haiying ^a   Xavier, Sandhya ^a,b   Ju, Wenjun ^a,c   Bottinger, Erwin ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; MICRORNA; MICRORNA 192; MICRORNA 216A; MICRORNA 217; MICRORNA 30; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P53; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; GLOMERULOSCLEROSIS; IN VITRO STUDY; LENTIVIRINAE; MOUSE; NONHUMAN; PODOCYTE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; VIRUS EXPRESSION;

ANIMALS; APOPTOSIS; CASPASE 3; CELL LINE; DOWN-REGULATION; HUMANS; IN SITU NICK-END LABELING; MICE; MICE, TRANSGENIC; MICRORNAS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PODOCYTES; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84884633364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075572     Document Type: Article

References (39)

1. Roberts AB, Flanders KC, Heine UI, Jakowlew S, Kondaiah P, et al. (1990) Transforming growth factor-beta: Multifunctional regulator of differentiation and development. Philos Trans R Soc Lond B Biol Sci 327: 145-154. doi:10.1098/rstb.1990.0050. PubMed: 1969655.
2. Böttinger EP, (2007) TGF-beta in renal injury and disease. Semin Nephrol 27: 309-320. doi:10.1016/j.semnephrol.2007.02.009. PubMed: 17533008.
3. Kriz W, Hosser H, Hähnel B, Gretz N, Provoost AP, (1998) From segmental glomerulosclerosis to total nephron degeneration and interstitial fibrosis: A histopathological study in rat models and human glomerulopathies. Nephrol Dial Transplant 13: 2781-2798. doi:10.1093/ndt/13.11.2781. PubMed: 9829480.
4. Wiggins RC, (2007) The spectrum of podocytopathies: A unifying view of glomerular diseases. Kidney Int 71: 1205-1214. doi:10.1038/sj.ki.5002222. PubMed: 17410103.
5. Schiffer M, Mundel P, Shaw AS, Böttinger EP, (2004) A novel role for the adaptor molecule CD2-associated protein in transforming growth factor-beta-induced apoptosis. J Biol Chem 279: 37004-37012. doi:10.1074/jbc.M403534200. PubMed: 15213232.
6. Xavier S, Niranjan T, Krick S, Zhang T, Ju W, et al. (2009) TbetaRI independently activates smad- and CD2AP-dependent pathways in podocytes. J Am Soc Nephrol 20: 2127-2137. doi:10.1681/ASN.2008070806. PubMed: 19679673.
7. Wu DT, Bitzer M, Ju W, Mundel P, Böttinger EP, (2005) TGF-beta concentration specifies differential signaling profiles of growth arrest/differentiation and apoptosis in podocytes. J Am Soc Nephrol 16: 3211-3221. doi:10.1681/ASN.2004121055. PubMed: 16207831.
8. Schiffer M, Bitzer M, Roberts IS, Kopp JB, ten Dijke P, et al. (2001) Apoptosis in podocytes induced by TGF-beta and Smad7. J Clin Invest 108: 807-816. doi:10.1172/JCI200112367. PubMed: 11560950.
9. John B, Enright AJ, Aravin A, Tuschl T, Sander C, et al. (2004) Human MicroRNA targets. PLOS Biol 2: e363. doi:10.1371/journal.pbio.0020363. PubMed: 15502875.
10. Sequeira-Lopez ML, Weatherford ET, Borges GR, Monteagudo MC, Pentz ES, et al. (2010) The microRNA-processing enzyme dicer maintains juxtaglomerular cells. J Am Soc Nephrol 21: 460-467. doi:10.1681/ASN.2009090964. PubMed: 20056748.
11. Wei Q, Bhatt K, He HZ, Mi QS, Haase VH, et al. (2010) Targeted deletion of dicer from proximal tubules protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 21: 756-761. doi:10.1681/ASN.2009070718. PubMed: 20360310.
12. Kato M, Zhang J, Wang M, Lanting L, Yuan H, et al. (2007) MicroRNA-192 in diabetic kidney glomeruli and its function in TGF-beta-induced collagen expression via inhibition of E-box repressors. Proc Natl Acad Sci U S A 104: 3432-3437. doi:10.1073/pnas.0611192104. PubMed: 17360662.
13. Chung AC, Huang XR, Meng X, Lan HY, (2010) miR-192 mediates TGF-beta/Smad3-driven renal fibrosis. J Am Soc Nephrol 21: 1317-1325. doi:10.1681/ASN.2010020134. PubMed: 20488955.
14. Kato M, Putta S, Wang M, Yuan H, Lanting L, et al. (2009) TGF-beta activates akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 11: 881-889. doi:10.1038/ncb1897. PubMed: 19543271.
15. Long J, Wang Y, Wang W, Chang BH, Danesh FR, (2010) Identification of microRNA-93 as a novel regulator of vascular endothelial growth factor in hyperglycemic conditions. J Biol Chem 285: 23457-23465. doi:10.1074/jbc.M110.136168. PubMed: 20501654.
16. Shi S, Yu L, Chiu C, Sun Y, Chen J, et al. (2008) Podocyte-selective deletion of dicer induces proteinuria and glomerulosclerosis. J Am Soc Nephrol 19: 2159-2169. doi:10.1681/ASN.2008030312. PubMed: 18776119.
17. Ho J, Ng KH, Rosen S, Dostal A, Gregory RI, et al. (2008) Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J Am Soc Nephrol 19: 2069-2075. doi:10.1681/ASN.2008020162. PubMed: 18832437.
18. Harvey SJ, Jarad G, Cunningham J, Goldberg S, Schermer B, et al. (2008) Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 19: 2150-2158. doi:10.1681/ASN.2008020233. PubMed: 18776121.
19. Yao J, Liang L, Huang S, Ding J, Tan N, et al. (2010) MicroRNA-30d promotes tumor invasion and metastasis by targeting Galphai2 in hepatocellular carcinoma. Hepatology 51: 846-856. PubMed: 20054866.
20. Li J, Donath S, Li Y, Qin D, Prabhakar BS, et al. (2010) miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLOS Genet 6: e1000795. PubMed: 20062521.
21. Yu F, Deng H, Yao H, Liu Q, Su F, et al. (2010) Mir-30 reduction maintains self-renewal and inhibits apoptosis in breast tumor-initiating cells. Oncogene 29: 4194-4204. doi:10.1038/onc.2010.167. PubMed: 20498642.
22. Braun J, Hoang-Vu C, Dralle H, Hüttelmaier S, (2010) Downregulation of microRNAs directs the EMT and invasive potential of anaplastic thyroid carcinomas. Oncogene 29: 4237-4244. doi:10.1038/onc.2010.169. PubMed: 20498632.
23. Hand NJ, Master ZR, Eauclaire SF, Weinblatt DE, Matthews RP, et al. (2009) The microRNA-30 family is required for vertebrate hepatobiliary development. Gastroenterology 136: 1081-1090. doi:10.1053/j.gastro.2008.12.006. PubMed: 19185580.
24. Agrawal R, Tran U, Wessely O, (2009) The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development 136: 3927-3936. doi:10.1242/dev.037432. PubMed: 19906860.
25. Sanderson N, Factor V, Nagy P, Kopp J, Kondaiah P, et al. (1995) Hepatic expression of mature transforming growth factor beta 1 in transgenic mice results in multiple tissue lesions. Proc Natl Acad Sci U S A 92: 2572-2576. doi:10.1073/pnas.92.7.2572. PubMed: 7708687.
26. Ashcroft GS, Yang X, Glick AB, Weinstein M, Letterio JL, et al. (1999) Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1: 260-266. doi:10.1038/12971. PubMed: 10559937.
27. Ju W, Ogawa A, Heyer J, Nierhof D, Yu L, et al. (2006) Deletion of Smad2 in mouse liver reveals novel functions in hepatocyte growth and differentiation. Mol Cell Biol 26: 654-667. doi:10.1128/MCB.26.2.654-667.2006. PubMed: 16382155.
28. Takeuchi A, Yoshizawa N, Yamamoto M, Sawasaki Y, Oda T, et al. (1992) Basic fibroblast growth factor promotes proliferation of rat glomerular visceral epithelial cells in vitro. Am J Pathol 141: 107-116. PubMed: 1632456.
29. Saleem MA, O'Hare MJ, Reiser J, Coward RJ, Inward CD, et al. (2002) A conditionally immortalized human podocyte cell line demonstrating nephrin and podocin expression. J Am Soc Nephrol 13: 630-638. PubMed: 11856766.
30. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, et al. (2005) Combinatorial microRNA target predictions. Nat Genet 37: 495-500. doi:10.1038/ng1536. PubMed: 15806104.
31. Kato M, Wang L, Putta S, Wang M, Yuan H, et al. (2010) Post-transcriptional up-regulation of Tsc-22 by Ybx1, a target of miR-216a, mediates TGF-{beta}-induced collagen expression in kidney cells. J Biol Chem 285: 34004-34015. doi:10.1074/jbc.M110.165027. PubMed: 20713358.
32. Winbanks CE, Wang B, Beyer C, Koh P, White L, et al. (2011) TGF-beta regulates miR-206 and miR-29 to control myogenic differentiation through regulation of HDAC4. J Biol Chem 286: 13805-13814. doi:10.1074/jbc.M110.192625. PubMed: 21324893.
33. Davis BN, Hilyard AC, Lagna G, Hata A, (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454: 56-61. doi:10.1038/nature07086. PubMed: 18548003.
34. Zavadil J, Böttinger EP, (2005) TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24: 5764-5774. doi:10.1038/sj.onc.1208927. PubMed: 16123809.
35. Kong W, Yang H, He L, Zhao JJ, Coppola D, et al. (2008) MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol 28: 6773-6784. doi:10.1128/MCB.00941-08. PubMed: 18794355.
36. Louafi F, Martinez-Nunez RT, Sanchez-Elsner T, (2010) MicroRNA-155 targets SMAD2 and modulates the response of macrophages to transforming growth factor-{beta}. J Biol Chem 285: 41328-41336. doi:10.1074/jbc.M110.146852. PubMed: 21036908.
37. Park SM, Gaur AB, Lengyel E, Peter ME, (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22: 894-907. doi:10.1101/gad.1640608. PubMed: 18381893.
38. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601. doi:10.1038/ncb1722. PubMed: 18376396.
39. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, et al. (2009) Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137: 1005-1017. doi:10.1016/j.cell.2009.04.021. PubMed: 19524505.