Skip to main content
Top
Published in: Journal of Translational Medicine 1/2018

Open Access 01-12-2018 | Research

Urinary miR-196a predicts disease progression in patients with chronic kidney disease

Authors: Changming Zhang, Shaoshan Liang, Shuiqin Cheng, Wei Li, Xia Wang, Chunxia Zheng, Caihong Zeng, Shaolin Shi, Lu Xie, Ke Zen, Zhihong Liu

Published in: Journal of Translational Medicine | Issue 1/2018

Login to get access

Abstract

Background

Urinary miRNAs may potentially serve as noninvasive biomarkers in various kidney diseases to reflect disease activity, severity and progression, especially those correlated with the pathogenesis of kidney diseases. This study demonstrates that urinary miR-196a, a kidney-enriched miRNA, can predict progression of chronic kidney disease (CKD).

Methods

Focal segmental glomerulosclerosis (FSGS) cohorts were used as the representative example of CKD. First, correlation of miR-196a with disease activity was analyzed using paired urine and plasma samples from FSGS patients with nephrotic-range proteinuria (FSGS-A), complete remission (FSGS-CR) and normal controls (NCs). Then, the value of urinary miR-196a in predicting disease progression was validated using another cohort of 231 FSGS patients who were followed-up until over 36 months or reaching end-stage renal disease (ESRD). MiR-196a levels were analyzed by quantitative reverse transcription-polymerase chain reaction.

Results

The results showed that urinary miR-196a significantly increased in FSGS-A compared with FSGS-CR and NCs, clearly distinguishing FSGS-A from FSGS-CR and NCs, whereas plasma miR-196a showed no difference among these groups. Moreover, urinary miR-196a, which was associated with proteinuria, estimated glomerular filtration rate (eGFR), interstitial fibrosis and tubular atrophy, significantly increased in patients progressed to ESRD compared to those not. Furthermore, patients with higher urinary miR-196a displayed poorer renal survival than those with lower urinary miR-196a. Multivariate Cox analysis confirmed urinary miR-196a as an independent risk factor for FSGS progression after adjusting for age, sex, proteinuria and eGFR. Prediction accuracy of ESRD was significantly improved by combining urinary miR-196a with other indicators including eGFR and proteinuria.

Conclusion

Urinary miR-196a may serve as a biomarker for predicting CKD progression
Appendix
Available only for authorised users
Literature
1.
go back to reference Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2095–128.CrossRefPubMed Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2095–128.CrossRefPubMed
2.
go back to reference Zhang L, Wang F, Wang L, Wang W, Liu B, Liu J, Chen M, He Q, Liao Y, Yu X, et al. Prevalence of chronic kidney disease in China: a cross-sectional survey. Lancet. 2012;379:815–22.CrossRefPubMed Zhang L, Wang F, Wang L, Wang W, Liu B, Liu J, Chen M, He Q, Liao Y, Yu X, et al. Prevalence of chronic kidney disease in China: a cross-sectional survey. Lancet. 2012;379:815–22.CrossRefPubMed
3.
go back to reference Nugent RA, Fathima SF, Feigl AB, Chyung D. The burden of chronic kidney disease on developing nations: a 21st century challenge in global health. Nephron Clin Pract. 2011;118:c269–77.CrossRefPubMed Nugent RA, Fathima SF, Feigl AB, Chyung D. The burden of chronic kidney disease on developing nations: a 21st century challenge in global health. Nephron Clin Pract. 2011;118:c269–77.CrossRefPubMed
4.
go back to reference Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS. Prevalence of chronic kidney disease in the United States. JAMA. 2007;298:2038–47.CrossRefPubMed Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS. Prevalence of chronic kidney disease in the United States. JAMA. 2007;298:2038–47.CrossRefPubMed
5.
go back to reference Whitman IR, Feldman HI, Deo R. CKD and sudden cardiac death: epidemiology, mechanisms, and therapeutic approaches. J Am Soc Nephrol. 2012;23:1929–39.CrossRefPubMedPubMedCentral Whitman IR, Feldman HI, Deo R. CKD and sudden cardiac death: epidemiology, mechanisms, and therapeutic approaches. J Am Soc Nephrol. 2012;23:1929–39.CrossRefPubMedPubMedCentral
6.
go back to reference Cattran DC, Coppo R, Cook HT, Feehally J, Roberts IS, Troyanov S, Alpers CE, Amore A, Barratt J, Berthoux F, et al. The Oxford classification of IgA nephropathy: rationale, clinicopathological correlations, and classification. Kidney Int. 2009;76:534–45.CrossRefPubMed Cattran DC, Coppo R, Cook HT, Feehally J, Roberts IS, Troyanov S, Alpers CE, Amore A, Barratt J, Berthoux F, et al. The Oxford classification of IgA nephropathy: rationale, clinicopathological correlations, and classification. Kidney Int. 2009;76:534–45.CrossRefPubMed
7.
go back to reference Zeng CH, Le W, Ni Z, Zhang M, Miao L, Luo P, Wang R, Lv Z, Chen J, Tian J, et al. A multicenter application and evaluation of the oxford classification of IgA nephropathy in adult chinese patients. Am J Kidney Dis. 2012;60:812–20.CrossRefPubMed Zeng CH, Le W, Ni Z, Zhang M, Miao L, Luo P, Wang R, Lv Z, Chen J, Tian J, et al. A multicenter application and evaluation of the oxford classification of IgA nephropathy in adult chinese patients. Am J Kidney Dis. 2012;60:812–20.CrossRefPubMed
8.
go back to reference Mise K, Hoshino J, Ueno T, Hazue R, Hasegawa J, Sekine A, Sumida K, Hiramatsu R, Hasegawa E, Yamanouchi M, et al. Prognostic value of tubulointerstitial lesions, urinary N-acetyl-beta-d-glucosaminidase, and urinary beta2-microglobulin in patients with type 2 diabetes and biopsy-proven diabetic nephropathy. Clin J Am Soc Nephrol. 2016;11:593–601.CrossRefPubMedPubMedCentral Mise K, Hoshino J, Ueno T, Hazue R, Hasegawa J, Sekine A, Sumida K, Hiramatsu R, Hasegawa E, Yamanouchi M, et al. Prognostic value of tubulointerstitial lesions, urinary N-acetyl-beta-d-glucosaminidase, and urinary beta2-microglobulin in patients with type 2 diabetes and biopsy-proven diabetic nephropathy. Clin J Am Soc Nephrol. 2016;11:593–601.CrossRefPubMedPubMedCentral
9.
go back to reference An Y, Xu F, Le W, Ge Y, Zhou M, Chen H, Zeng C, Zhang H, Liu Z. Renal histologic changes and the outcome in patients with diabetic nephropathy. Nephrol Dial Transplant. 2015;30:257–66.CrossRefPubMed An Y, Xu F, Le W, Ge Y, Zhou M, Chen H, Zeng C, Zhang H, Liu Z. Renal histologic changes and the outcome in patients with diabetic nephropathy. Nephrol Dial Transplant. 2015;30:257–66.CrossRefPubMed
10.
go back to reference Zuo K, Wu Y, Li SJ, Xu F, Zeng CH, Liu ZH. Long-term outcome and prognostic factors of idiopathic membranous nephropathy in the Chinese population. Clin Nephrol. 2013;79:445–53.CrossRefPubMed Zuo K, Wu Y, Li SJ, Xu F, Zeng CH, Liu ZH. Long-term outcome and prognostic factors of idiopathic membranous nephropathy in the Chinese population. Clin Nephrol. 2013;79:445–53.CrossRefPubMed
11.
12.
go back to reference Creemers EE, Tijsen AJ, Pinto YM. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res. 2012;110:483–95.CrossRefPubMed Creemers EE, Tijsen AJ, Pinto YM. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res. 2012;110:483–95.CrossRefPubMed
13.
go back to reference Guay C, Regazzi R. Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol. 2013;9:513–21.CrossRefPubMed Guay C, Regazzi R. Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol. 2013;9:513–21.CrossRefPubMed
14.
go back to reference Grasedieck S, Sorrentino A, Langer C, Buske C, Dohner H, Mertens D, Kuchenbauer F. Circulating microRNAs in hematological diseases: principles, challenges, and perspectives. Blood. 2013;121:4977–84.CrossRefPubMed Grasedieck S, Sorrentino A, Langer C, Buske C, Dohner H, Mertens D, Kuchenbauer F. Circulating microRNAs in hematological diseases: principles, challenges, and perspectives. Blood. 2013;121:4977–84.CrossRefPubMed
15.
go back to reference Cheng G. Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Adv Drug Deliv Rev. 2015;81:75–93.CrossRefPubMed Cheng G. Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Adv Drug Deliv Rev. 2015;81:75–93.CrossRefPubMed
16.
go back to reference Wang K, Zhang S, Marzolf B, Troisch P, Brightman A, Hu Z, Hood LE, Galas DJ. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA. 2009;106:4402–7.CrossRefPubMedPubMedCentral Wang K, Zhang S, Marzolf B, Troisch P, Brightman A, Hu Z, Hood LE, Galas DJ. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA. 2009;106:4402–7.CrossRefPubMedPubMedCentral
17.
go back to reference Wang N, Zhou Y, Jiang L, Li D, Yang J, Zhang CY, Zen K. Urinary microRNA-10a and microRNA-30d serve as novel, sensitive and specific biomarkers for kidney injury. PLoS ONE. 2012;7:e51140.CrossRefPubMedPubMedCentral Wang N, Zhou Y, Jiang L, Li D, Yang J, Zhang CY, Zen K. Urinary microRNA-10a and microRNA-30d serve as novel, sensitive and specific biomarkers for kidney injury. PLoS ONE. 2012;7:e51140.CrossRefPubMedPubMedCentral
18.
go back to reference Zhang C, Zhang W, Chen H-M, Liu C, Wu J, Shi S, Liu Z-H. Plasma MicroRNA-186 and proteinuria in focal segmental glomerulosclerosis. Am J Kidney Dis. 2015;65:223–32.CrossRefPubMed Zhang C, Zhang W, Chen H-M, Liu C, Wu J, Shi S, Liu Z-H. Plasma MicroRNA-186 and proteinuria in focal segmental glomerulosclerosis. Am J Kidney Dis. 2015;65:223–32.CrossRefPubMed
19.
go back to reference Maluf DG, Dumur CI, Suh JL, Scian MJ, King AL, Cathro H, Lee JK, Gehrau RC, Brayman KL, Gallon L, Mas VR. The urine microRNA profile may help monitor post-transplant renal graft function. Kidney Int. 2014;85:439–49.CrossRefPubMed Maluf DG, Dumur CI, Suh JL, Scian MJ, King AL, Cathro H, Lee JK, Gehrau RC, Brayman KL, Gallon L, Mas VR. The urine microRNA profile may help monitor post-transplant renal graft function. Kidney Int. 2014;85:439–49.CrossRefPubMed
20.
go back to reference van de Vrie M, Deegens JK, Eikmans M, van der Vlag J, Hilbrands LB. Urinary microRNA as biomarker in renal transplantation. Am J Transplant. 2016;17:1160–6.CrossRefPubMedPubMedCentral van de Vrie M, Deegens JK, Eikmans M, van der Vlag J, Hilbrands LB. Urinary microRNA as biomarker in renal transplantation. Am J Transplant. 2016;17:1160–6.CrossRefPubMedPubMedCentral
21.
go back to reference Nassirpour R, Homer BL, Mathur S, Li Y, Li Z, Brown T, Carraher D, Warneke J, Bailey S, Percival K, et al. Identification of promising urinary MicroRNA biomarkers in two rat models of glomerular injury. Toxicol Sci. 2015;148:35–47.CrossRefPubMed Nassirpour R, Homer BL, Mathur S, Li Y, Li Z, Brown T, Carraher D, Warneke J, Bailey S, Percival K, et al. Identification of promising urinary MicroRNA biomarkers in two rat models of glomerular injury. Toxicol Sci. 2015;148:35–47.CrossRefPubMed
22.
go back to reference Sole C, Cortes-Hernandez J, Felip ML, Vidal M, Ordi-Ros J. miR-29c in urinary exosomes as predictor of early renal fibrosis in lupus nephritis. Nephrol Dial Transplant. 2015;30:1488–96.CrossRefPubMed Sole C, Cortes-Hernandez J, Felip ML, Vidal M, Ordi-Ros J. miR-29c in urinary exosomes as predictor of early renal fibrosis in lupus nephritis. Nephrol Dial Transplant. 2015;30:1488–96.CrossRefPubMed
23.
go back to reference Zhang W, Zhang C, Chen H, Li L, Tu Y, Liu C, Shi S, Zen K, Liu Z. Evaluation of microRNAs miR-196a, miR-30a-5P, and miR-490 as biomarkers of disease activity among patients with FSGS. Clin J Am Soc Nephrol. 2014;9:1545–52.CrossRefPubMedPubMedCentral Zhang W, Zhang C, Chen H, Li L, Tu Y, Liu C, Shi S, Zen K, Liu Z. Evaluation of microRNAs miR-196a, miR-30a-5P, and miR-490 as biomarkers of disease activity among patients with FSGS. Clin J Am Soc Nephrol. 2014;9:1545–52.CrossRefPubMedPubMedCentral
24.
go back to reference Meng J, Li L, Zhao Y, Zhou Z, Zhang M, Li D, Zhang CY, Zen K, Liu Z. MicroRNA-196a/b mitigate renal fibrosis by targeting TGF-beta receptor 2. J Am Soc Nephrol. 2016;27:3006–21.CrossRefPubMedPubMedCentral Meng J, Li L, Zhao Y, Zhou Z, Zhang M, Li D, Zhang CY, Zen K, Liu Z. MicroRNA-196a/b mitigate renal fibrosis by targeting TGF-beta receptor 2. J Am Soc Nephrol. 2016;27:3006–21.CrossRefPubMedPubMedCentral
25.
go back to reference Honda N, Jinnin M, Kajihara I, Makino T, Makino K, Masuguchi S, Fukushima S, Okamoto Y, Hasegawa M, Fujimoto M, Ihn H. TGF-beta-mediated downregulation of microRNA-196a contributes to the constitutive upregulated type I collagen expression in scleroderma dermal fibroblasts. J Immunol. 2012;188:3323–31.CrossRefPubMed Honda N, Jinnin M, Kajihara I, Makino T, Makino K, Masuguchi S, Fukushima S, Okamoto Y, Hasegawa M, Fujimoto M, Ihn H. TGF-beta-mediated downregulation of microRNA-196a contributes to the constitutive upregulated type I collagen expression in scleroderma dermal fibroblasts. J Immunol. 2012;188:3323–31.CrossRefPubMed
26.
go back to reference Makino K, Jinnin M, Aoi J, Hirano A, Kajihara I, Makino T, Sakai K, Fukushima S, Inoue Y, Ihn H. Discoidin domain receptor 2-microRNA 196a-mediated negative feedback against excess type I collagen expression is impaired in scleroderma dermal fibroblasts. J Invest Dermatol. 2013;133:110–9.CrossRefPubMed Makino K, Jinnin M, Aoi J, Hirano A, Kajihara I, Makino T, Sakai K, Fukushima S, Inoue Y, Ihn H. Discoidin domain receptor 2-microRNA 196a-mediated negative feedback against excess type I collagen expression is impaired in scleroderma dermal fibroblasts. J Invest Dermatol. 2013;133:110–9.CrossRefPubMed
27.
go back to reference Shah N, Singh I. MicroRNA profiling identifies miR-196a as differentially expressed in childhood adrenoleukodystrophy and adult adrenomyeloneuropathy. Mol Neurobiol. 2017;54:1392–403.CrossRefPubMed Shah N, Singh I. MicroRNA profiling identifies miR-196a as differentially expressed in childhood adrenoleukodystrophy and adult adrenomyeloneuropathy. Mol Neurobiol. 2017;54:1392–403.CrossRefPubMed
28.
go back to reference Zhang Q, Zeng C, Fu Y, Cheng Z, Zhang J, Liu Z. Biomarkers of endothelial dysfunction in patients with primary focal segmental glomerulosclerosis. Nephrology (Carlton). 2012;17:338–45.CrossRef Zhang Q, Zeng C, Fu Y, Cheng Z, Zhang J, Liu Z. Biomarkers of endothelial dysfunction in patients with primary focal segmental glomerulosclerosis. Nephrology (Carlton). 2012;17:338–45.CrossRef
29.
go back to reference Coresh J, Turin TC, Matsushita K, Sang Y, Ballew SH, Appel LJ, Arima H, Chadban SJ, Cirillo M, Djurdjev O, et al. Decline in estimated glomerular filtration rate and subsequent risk of end-stage renal disease and mortality. JAMA. 2014;311:2518–31.CrossRefPubMedPubMedCentral Coresh J, Turin TC, Matsushita K, Sang Y, Ballew SH, Appel LJ, Arima H, Chadban SJ, Cirillo M, Djurdjev O, et al. Decline in estimated glomerular filtration rate and subsequent risk of end-stage renal disease and mortality. JAMA. 2014;311:2518–31.CrossRefPubMedPubMedCentral
30.
go back to reference Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150:604–12.CrossRefPubMedPubMedCentral Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150:604–12.CrossRefPubMedPubMedCentral
31.
go back to reference Chen X, Hu Z, Wang W, Ba Y, Ma L, Zhang C, Wang C, Ren Z, Zhao Y, Wu S, et al. Identification of ten serum microRNAs from a genome-wide serum microRNA expression profile as novel noninvasive biomarkers for nonsmall cell lung cancer diagnosis. Int J Cancer. 2012;130:1620–8.CrossRefPubMed Chen X, Hu Z, Wang W, Ba Y, Ma L, Zhang C, Wang C, Ren Z, Zhao Y, Wu S, et al. Identification of ten serum microRNAs from a genome-wide serum microRNA expression profile as novel noninvasive biomarkers for nonsmall cell lung cancer diagnosis. Int J Cancer. 2012;130:1620–8.CrossRefPubMed
32.
go back to reference Luo Y, Wang C, Chen X, Zhong T, Cai X, Chen S, Shi Y, Hu J, Guan X, Xia Z, et al. Increased serum and urinary microRNAs in children with idiopathic nephrotic syndrome. Clin Chem. 2013;59:658–66.CrossRefPubMed Luo Y, Wang C, Chen X, Zhong T, Cai X, Chen S, Shi Y, Hu J, Guan X, Xia Z, et al. Increased serum and urinary microRNAs in children with idiopathic nephrotic syndrome. Clin Chem. 2013;59:658–66.CrossRefPubMed
33.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative pcr and the 2 (− ΔΔCT) method. Methods. 2001;25:402–8.CrossRefPubMed Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative pcr and the 2 (− ΔΔCT) method. Methods. 2001;25:402–8.CrossRefPubMed
34.
go back to reference Nicholson ML, McCulloch TA, Harper SJ, Wheatley TJ, Edwards CM, Feehally J, Furness PN. Early measurement of interstitial fibrosis predicts long-term renal function and graft survival in renal transplantation. Br J Surg. 1996;83:1082–5.CrossRefPubMed Nicholson ML, McCulloch TA, Harper SJ, Wheatley TJ, Edwards CM, Feehally J, Furness PN. Early measurement of interstitial fibrosis predicts long-term renal function and graft survival in renal transplantation. Br J Surg. 1996;83:1082–5.CrossRefPubMed
35.
go back to reference Hayek SS, Sever S, Ko YA, Trachtman H, Awad M, Wadhwani S, Altintas MM, Wei C, Hotton AL, French AL, et al. Soluble urokinase receptor and chronic kidney disease. N Engl J Med. 2015;373:1916–25.CrossRefPubMedPubMedCentral Hayek SS, Sever S, Ko YA, Trachtman H, Awad M, Wadhwani S, Altintas MM, Wei C, Hotton AL, French AL, et al. Soluble urokinase receptor and chronic kidney disease. N Engl J Med. 2015;373:1916–25.CrossRefPubMedPubMedCentral
36.
go back to reference Nair V, Robinson-Cohen C, Smith MR, Bellovich KA, Bhat ZY, Bobadilla M, Brosius F, de Boer IH, Essioux L, Formentini I, et al. Growth differentiation factor-15 and risk of CKD progression. J Am Soc Nephrol. 2017;28:2233–40.CrossRefPubMed Nair V, Robinson-Cohen C, Smith MR, Bellovich KA, Bhat ZY, Bobadilla M, Brosius F, de Boer IH, Essioux L, Formentini I, et al. Growth differentiation factor-15 and risk of CKD progression. J Am Soc Nephrol. 2017;28:2233–40.CrossRefPubMed
37.
go back to reference Rasmussen DGK, Fenton A, Jesky M, Ferro C, Boor P, Tepel M, Karsdal MA, Genovese F, Cockwell P. Urinary endotrophin predicts disease progression in patients with chronic kidney disease. Sci Rep. 2017;7:17328.CrossRefPubMedPubMedCentral Rasmussen DGK, Fenton A, Jesky M, Ferro C, Boor P, Tepel M, Karsdal MA, Genovese F, Cockwell P. Urinary endotrophin predicts disease progression in patients with chronic kidney disease. Sci Rep. 2017;7:17328.CrossRefPubMedPubMedCentral
38.
go back to reference Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129:1401–14.CrossRefPubMedPubMedCentral Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129:1401–14.CrossRefPubMedPubMedCentral
39.
go back to reference Nikolic-Paterson DJ, Wang S, Lan HY. Macrophages promote renal fibrosis through direct and indirect mechanisms. Kidney Int Suppl. 2014;4:34–8.CrossRef Nikolic-Paterson DJ, Wang S, Lan HY. Macrophages promote renal fibrosis through direct and indirect mechanisms. Kidney Int Suppl. 2014;4:34–8.CrossRef
40.
go back to reference Edeling M, Ragi G, Huang S, Pavenstadt H, Susztak K. Developmental signalling pathways in renal fibrosis: the roles of Notch, Wnt and Hedgehog. Nat Rev Nephrol. 2016;12:426–39.CrossRefPubMedPubMedCentral Edeling M, Ragi G, Huang S, Pavenstadt H, Susztak K. Developmental signalling pathways in renal fibrosis: the roles of Notch, Wnt and Hedgehog. Nat Rev Nephrol. 2016;12:426–39.CrossRefPubMedPubMedCentral
41.
go back to reference Yiu WH, Lin M, Tang SC. Toll-like receptor activation: from renal inflammation to fibrosis. Kidney Int Suppl. 2014;4:20–5.CrossRef Yiu WH, Lin M, Tang SC. Toll-like receptor activation: from renal inflammation to fibrosis. Kidney Int Suppl. 2014;4:20–5.CrossRef
42.
go back to reference Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–79.CrossRefPubMed Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–79.CrossRefPubMed
43.
go back to reference Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19:43–51.CrossRefPubMed Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009;19:43–51.CrossRefPubMed
44.
go back to reference Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13:423–33.CrossRefPubMedPubMedCentral Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13:423–33.CrossRefPubMedPubMedCentral
45.
go back to reference Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005;65:7065–70.CrossRefPubMed Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005;65:7065–70.CrossRefPubMed
46.
go back to reference Hagrass HA, Sharaf S, Pasha HF, Tantawy EA, Mohamed RH, Kassem R. Circulating microRNAs-a new horizon in molecular diagnosis of breast cancer. Genes Cancer. 2015;6:281–7.PubMedPubMedCentral Hagrass HA, Sharaf S, Pasha HF, Tantawy EA, Mohamed RH, Kassem R. Circulating microRNAs-a new horizon in molecular diagnosis of breast cancer. Genes Cancer. 2015;6:281–7.PubMedPubMedCentral
47.
go back to reference Mar-Aguilar F, Mendoza-Ramirez JA, Malagon-Santiago I, Espino-Silva PK, Santuario-Facio SK, Ruiz-Flores P, Rodriguez-Padilla C, Resendez-Perez D. Serum circulating microRNA profiling for identification of potential breast cancer biomarkers. Dis Markers. 2013;34:163–9.CrossRefPubMedPubMedCentral Mar-Aguilar F, Mendoza-Ramirez JA, Malagon-Santiago I, Espino-Silva PK, Santuario-Facio SK, Ruiz-Flores P, Rodriguez-Padilla C, Resendez-Perez D. Serum circulating microRNA profiling for identification of potential breast cancer biomarkers. Dis Markers. 2013;34:163–9.CrossRefPubMedPubMedCentral
48.
go back to reference Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133–44.CrossRefPubMed Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010;39:133–44.CrossRefPubMed
49.
go back to reference Ju W, Nair V, Smith S, Zhu L, Shedden K, Song PX, Mariani LH, Eichinger FH, Berthier CC, Randolph A, et al. Tissue transcriptome-driven identification of epidermal growth factor as a chronic kidney disease biomarker. Sci Transl Med. 2015;7:316193.CrossRef Ju W, Nair V, Smith S, Zhu L, Shedden K, Song PX, Mariani LH, Eichinger FH, Berthier CC, Randolph A, et al. Tissue transcriptome-driven identification of epidermal growth factor as a chronic kidney disease biomarker. Sci Transl Med. 2015;7:316193.CrossRef
50.
51.
go back to reference Aregger F, Uehlinger DE, Witowski J, Brunisholz RA, Hunziker P, Frey FJ, Jorres A. Identification of IGFBP-7 by urinary proteomics as a novel prognostic marker in early acute kidney injury. Kidney Int. 2014;85:909–19.CrossRefPubMed Aregger F, Uehlinger DE, Witowski J, Brunisholz RA, Hunziker P, Frey FJ, Jorres A. Identification of IGFBP-7 by urinary proteomics as a novel prognostic marker in early acute kidney injury. Kidney Int. 2014;85:909–19.CrossRefPubMed
52.
go back to reference Wang X, Shen E, Wang Y, Jiang Z, Gui D, Cheng D, Chen T, Wang N. MiR-196a regulates high glucose-induced mesangial cell hypertrophy by targeting p27kip1. J Lab Autom. 2015;20:491–9.CrossRefPubMed Wang X, Shen E, Wang Y, Jiang Z, Gui D, Cheng D, Chen T, Wang N. MiR-196a regulates high glucose-induced mesangial cell hypertrophy by targeting p27kip1. J Lab Autom. 2015;20:491–9.CrossRefPubMed
53.
go back to reference Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, Natarajan R. 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 USA. 2007;104:3432–7.CrossRefPubMedPubMedCentral Kato M, Zhang J, Wang M, Lanting L, Yuan H, Rossi JJ, Natarajan R. 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 USA. 2007;104:3432–7.CrossRefPubMedPubMedCentral
54.
go back to reference Oba S, Kumano S, Suzuki E, Nishimatsu H, Takahashi M, Takamori H, Kasuya M, Ogawa Y, Sato K, Kimura K, et al. miR-200b precursor can ameliorate renal tubulointerstitial fibrosis. PLoS ONE. 2010;5:e13614.CrossRefPubMedPubMedCentral Oba S, Kumano S, Suzuki E, Nishimatsu H, Takahashi M, Takamori H, Kasuya M, Ogawa Y, Sato K, Kimura K, et al. miR-200b precursor can ameliorate renal tubulointerstitial fibrosis. PLoS ONE. 2010;5:e13614.CrossRefPubMedPubMedCentral
55.
go back to reference Wang G, Kwan BC, Lai FM, Choi PC, Chow KM, Li PK, Szeto CC. Intrarenal expression of microRNAs in patients with IgA nephropathy. Lab Invest. 2010;90:98–103.CrossRefPubMed Wang G, Kwan BC, Lai FM, Choi PC, Chow KM, Li PK, Szeto CC. Intrarenal expression of microRNAs in patients with IgA nephropathy. Lab Invest. 2010;90:98–103.CrossRefPubMed
56.
go back to reference Wang G, Kwan BC, Lai FM, Chow KM, Kam-Tao Li P, Szeto CC. Expression of microRNAs in the urinary sediment of patients with IgA nephropathy. Dis Markers. 2010;28:79–86.CrossRefPubMedPubMedCentral Wang G, Kwan BC, Lai FM, Chow KM, Kam-Tao Li P, Szeto CC. Expression of microRNAs in the urinary sediment of patients with IgA nephropathy. Dis Markers. 2010;28:79–86.CrossRefPubMedPubMedCentral
57.
go back to reference Zhou TB, Jiang ZP. Role of miR-21 and its signaling pathways in renal diseases. J Recept Signal Transduct Res. 2014;34:335–7.CrossRefPubMed Zhou TB, Jiang ZP. Role of miR-21 and its signaling pathways in renal diseases. J Recept Signal Transduct Res. 2014;34:335–7.CrossRefPubMed
58.
go back to reference Kato M, Wang L, Putta S, Wang M, Yuan H, Sun G, Lanting L, Todorov I, Rossi JJ, Natarajan R. 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. 2010;285:34004–15.CrossRefPubMedPubMedCentral Kato M, Wang L, Putta S, Wang M, Yuan H, Sun G, Lanting L, Todorov I, Rossi JJ, Natarajan R. 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. 2010;285:34004–15.CrossRefPubMedPubMedCentral
59.
go back to reference Szeto CC, Ching-Ha KB, Ka-Bik L, Mac-Moune LF, Cheung-Lung CP, Gang W, Kai-Ming C, Kam-Tao LP. Micro-RNA expression in the urinary sediment of patients with chronic kidney diseases. Dis Markers. 2012;33:137–44.CrossRefPubMedPubMedCentral Szeto CC, Ching-Ha KB, Ka-Bik L, Mac-Moune LF, Cheung-Lung CP, Gang W, Kai-Ming C, Kam-Tao LP. Micro-RNA expression in the urinary sediment of patients with chronic kidney diseases. Dis Markers. 2012;33:137–44.CrossRefPubMedPubMedCentral
Metadata
Title
Urinary miR-196a predicts disease progression in patients with chronic kidney disease
Authors
Changming Zhang
Shaoshan Liang
Shuiqin Cheng
Wei Li
Xia Wang
Chunxia Zheng
Caihong Zeng
Shaolin Shi
Lu Xie
Ke Zen
Zhihong Liu
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2018
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-018-1470-2

Other articles of this Issue 1/2018

Journal of Translational Medicine 1/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.