Circulating TGF-β1-Regulated MiRNAs and the Risk of Rapid Progression to ESRD in Type 1 Diabetes

Overview

Journal Diabetes

Specialty Endocrinology

Date 2015 May 2

PMID 25931475

Citations 54

Authors

Marcus G Pezzolesi

Eiichiro Satake

Kevin P McDonnell

Melissa Major

Adam M Smiles

Andrzej S Krolewski

Affiliations

Soon will be listed here.

Abstract

We investigated whether circulating TGF-β1-regulated miRNAs detectable in plasma are associated with the risk of rapid progression to end-stage renal disease (ESRD) in a cohort of proteinuric patients with type 1 diabetes (T1D) and normal eGFR. Plasma specimens obtained at entry to the study were examined in two prospective subgroups that were followed for 7-20 years (rapid progressors and nonprogressors), as well as a reference panel of normoalbuminuric T1D patients. Of the five miRNAs examined in this study, let-7c-5p and miR-29a-3p were significantly associated with protection against rapid progression and let-7b-5p and miR-21-5p were significantly associated with the increased risk of ESRD. In logistic analysis, controlling for HbA1c and other covariates, let-7c-5p and miR-29a-3p were associated with more than a 50% reduction in the risk of rapid progression (P ≤ 0.001), while let-7b-5p and miR-21-5p were associated with a >2.5-fold increase in the risk of ESRD (P ≤ 0.005). This study is the first prospective study to demonstrate that circulating TGF-β1-regulated miRNAs are deregulated early in T1D patients who are at risk for rapid progression to ESRD.

Citing Articles

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References

Arroyo J, Chevillet J, Kroh E, Ruf I, Pritchard C, Gibson D . Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A. 2011; 108(12):5003-8. PMC: 3064324. DOI: 10.1073/pnas.1019055108. View

Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C . Circulating microRNAs in patients with coronary artery disease. Circ Res. 2010; 107(5):677-84. DOI: 10.1161/CIRCRESAHA.109.215566. View

Kato M, Arce L, Wang M, Putta S, Lanting L, Natarajan R . A microRNA circuit mediates transforming growth factor-β1 autoregulation in renal glomerular mesangial cells. Kidney Int. 2011; 80(4):358-68. PMC: 3337779. DOI: 10.1038/ki.2011.43. View

Qin W, Chung A, Huang X, Meng X, Hui D, Yu C . TGF-β/Smad3 signaling promotes renal fibrosis by inhibiting miR-29. J Am Soc Nephrol. 2011; 22(8):1462-74. PMC: 3148701. DOI: 10.1681/ASN.2010121308. View

Zhong X, Chung A, Chen H, Meng X, Lan H . Smad3-mediated upregulation of miR-21 promotes renal fibrosis. J Am Soc Nephrol. 2011; 22(9):1668-81. PMC: 3171938. DOI: 10.1681/ASN.2010111168. View

Weber J, Baxter D, Zhang S, Huang D, Huang K, Lee M . The microRNA spectrum in 12 body fluids. Clin Chem. 2010; 56(11):1733-41. PMC: 4846276. DOI: 10.1373/clinchem.2010.147405. View

Zhou Q, Fan J, Ding X, Peng W, Yu X, Chen Y . TGF-{beta}-induced MiR-491-5p expression promotes Par-3 degradation in rat proximal tubular epithelial cells. J Biol Chem. 2010; 285(51):40019-27. PMC: 3000984. DOI: 10.1074/jbc.M110.141341. View

Rosolowsky E, Skupien J, Smiles A, Niewczas M, Roshan B, Stanton R . Risk for ESRD in type 1 diabetes remains high despite renoprotection. J Am Soc Nephrol. 2011; 22(3):545-53. PMC: 3060448. DOI: 10.1681/ASN.2010040354. View

Turchinovich A, Weiz L, Langheinz A, Burwinkel B . Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011; 39(16):7223-33. PMC: 3167594. DOI: 10.1093/nar/gkr254. View

10.

Heegaard N, Schetter A, Welsh J, Yoneda M, Bowman E, Harris C . Circulating micro-RNA expression profiles in early stage nonsmall cell lung cancer. Int J Cancer. 2011; 130(6):1378-86. PMC: 3259258. DOI: 10.1002/ijc.26153. View

11.

Wang B, Komers R, Carew R, Winbanks C, Xu B, Herman-Edelstein M . Suppression of microRNA-29 expression by TGF-β1 promotes collagen expression and renal fibrosis. J Am Soc Nephrol. 2011; 23(2):252-65. PMC: 3269175. DOI: 10.1681/ASN.2011010055. View

12.

Kriegel A, Liu Y, Cohen B, Usa K, Liu Y, Liang M . MiR-382 targeting of kallikrein 5 contributes to renal inner medullary interstitial fibrosis. Physiol Genomics. 2011; 44(4):259-67. PMC: 3289118. DOI: 10.1152/physiolgenomics.00173.2011. View

13.

Putta S, Lanting L, Sun G, Lawson G, Kato M, Natarajan R . Inhibiting microRNA-192 ameliorates renal fibrosis in diabetic nephropathy. J Am Soc Nephrol. 2012; 23(3):458-69. PMC: 3294315. DOI: 10.1681/ASN.2011050485. View

14.

Schaeffer V, Hansen K, Morris D, LeBoeuf R, Abrass C . RNA-binding protein IGF2BP2/IMP2 is required for laminin-β2 mRNA translation and is modulated by glucose concentration. Am J Physiol Renal Physiol. 2012; 303(1):F75-82. PMC: 3431147. DOI: 10.1152/ajprenal.00185.2012. View

15.

Dey N, Ghosh-Choudhury N, Kasinath B, Ghosh Choudhury G . TGFβ-stimulated microRNA-21 utilizes PTEN to orchestrate AKT/mTORC1 signaling for mesangial cell hypertrophy and matrix expansion. PLoS One. 2012; 7(8):e42316. PMC: 3411779. DOI: 10.1371/journal.pone.0042316. View

16.

Skupien J, Warram J, Smiles A, Niewczas M, Gohda T, Pezzolesi M . The early decline in renal function in patients with type 1 diabetes and proteinuria predicts the risk of end-stage renal disease. Kidney Int. 2012; 82(5):589-97. PMC: 3425658. DOI: 10.1038/ki.2012.189. View

17.

Argyropoulos C, Wang K, McClarty S, Huang D, Bernardo J, Ellis D . Urinary microRNA profiling in the nephropathy of type 1 diabetes. PLoS One. 2013; 8(1):e54662. PMC: 3554645. DOI: 10.1371/journal.pone.0054662. View

18.

Zhong X, Chung A, Chen H, Dong Y, Meng X, Li R . miR-21 is a key therapeutic target for renal injury in a mouse model of type 2 diabetes. Diabetologia. 2013; 56(3):663-74. DOI: 10.1007/s00125-012-2804-x. View

19.

Brennan E, Nolan K, Borgeson E, Gough O, McEvoy C, Docherty N . Lipoxins attenuate renal fibrosis by inducing let-7c and suppressing TGFβR1. J Am Soc Nephrol. 2013; 24(4):627-37. PMC: 3609134. DOI: 10.1681/ASN.2012060550. View

20.

DiStefano J, Taila M, Alvarez M . Emerging roles for miRNAs in the development, diagnosis, and treatment of diabetic nephropathy. Curr Diab Rep. 2013; 13(4):582-91. DOI: 10.1007/s11892-013-0386-8. View