Association of serum microRNAs with islet autoimmunity, disease progression and metabolic impairment in relatives at risk of type 1 diabetes

Diabetologia

Volumn 60, Issue 8, 2017, Pages 1409-1422

  Snowhite, Isaac V ^a   Allende, Gloria ^a   Sosenko, Jay ^a   Pastori, Ricardo L ^a   Messinger Cayetano, Shari ^a   Pugliese, Alberto ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Clinical science; Microarray; Prediction and prevention of type 1 diabetes

Indexed keywords

AUTOANTIBODY; C PEPTIDE; GLUCOSE; INSULIN ANTIBODY; MICRORNA; MICRORNA 106A; MICRORNA 143; MICRORNA 15A; MICRORNA 16; MICRORNA 185; MICRORNA 19A; MICRORNA 20A; MICRORNA 21; MICRORNA 25; MICRORNA 29A; MICRORNA 31; MICRORNA 3P; MICRORNA 424; MICRORNA 451A; MICRORNA 485; MICRORNA 523; MICRORNA 524; MICRORNA 619; MICRORNA 92A; UNCLASSIFIED DRUG;

ANTIBODY BLOOD LEVEL; ARTICLE; AUTOIMMUNITY; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; FOLLOW UP; GLUCOSE BLOOD LEVEL; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; ORAL GLUCOSE TOLERANCE TEST; PANCREAS ISLET; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY; SIBLING; ADOLESCENT; BLOOD; CHILD; FEMALE; GLUCOSE TOLERANCE TEST; IMMUNOLOGY; INFANT; MALE; PHYSIOLOGY; PRESCHOOL CHILD; RECEIVER OPERATING CHARACTERISTIC;

ADOLESCENT; AUTOANTIBODIES; AUTOIMMUNITY; CHILD; CHILD, PRESCHOOL; DIABETES MELLITUS, TYPE 1; FEMALE; GLUCOSE TOLERANCE TEST; HUMANS; INFANT; ISLETS OF LANGERHANS; MALE; MICRORNAS; RETROSPECTIVE STUDIES; ROC CURVE;

EID: 85019199700     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-017-4294-3     Document Type: Article

References (50)

1. Pugliese A (2013) The multiple origins of type 1 diabetes. Diabet Med 30:135–146
2. Yates LA, Norbury CJ, Gilbert RJ (2013) The long and short of microRNA. Cell 153:516–519
3. Cobb BS, Hertweck A, Smith J et al (2006) A role for dicer in immune regulation. J Exp Med 203:2519–2527
4. Poy MN, Eliasson L, Krutzfeldt J et al (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432:226–230
5. Correa-Medina M, Bravo-Egana V, Rosero S et al (2009) MicroRNA miR-7 is preferentially expressed in endocrine cells of the developing and adult human pancreas. Gene Expr Patterns 9:193–199
6. Joglekar MV, Joglekar VM, Hardikar AA (2009) Expression of islet-specific microRNAs during human pancreatic development. Gene Expr Patterns 9:109–113
7. Joglekar MV, Parekh VS, Mehta S, Bhonde RR, Hardikar AA (2007) MicroRNA profiling of developing and regenerating pancreas reveal post-transcriptional regulation of neurogenin3. Dev Biol 311:603–612
8. Belgardt BF, Ahmed K, Spranger M et al (2015) The microRNA-200 family regulates pancreatic beta cell survival in type 2 diabetes. Nat Med 21:619–627
9. Sebastiani G, Po A, Miele E et al (2015) MicroRNA-124a is hyperexpressed in type 2 diabetic human pancreatic islets and negatively regulates insulin secretion. Acta Diabetol 52:523–530
10. Sebastiani G, Grieco FA, Spagnuolo I, Galleri L, Cataldo D, Dotta F (2011) Increased expression of microRNA miR-326 in type 1 diabetic patients with ongoing islet autoimmunity. Diabetes Metab Res Rev 27:862–866
11. Salas-Perez F, Codner E, Valencia E, Pizarro C, Carrasco E, Perez-Bravo F (2013) MicroRNAs miR-21a and miR-93 are down regulated in peripheral blood mononuclear cells (PBMCs) from patients with type 1 diabetes. Immunobiology 218:733–737
12. Hezova R, Slaby O, Faltejskova P et al (2010) microRNA-342, microRNA-191 and microRNA-510 are differentially expressed in T regulatory cells of type 1 diabetic patients. Cell Immunol 260:70–74
13. Mi QS, He HZ, Dong Z, Isales C, Zhou L (2010) microRNA deficiency in pancreatic islet cells exacerbates streptozotocin-induced murine autoimmune diabetes. Cell Cycle 9:3127–3129
14. Roggli E, Gattesco S, Caille D et al (2012) Changes in microRNA expression contribute to pancreatic beta-cell dysfunction in prediabetic NOD mice. Diabetes 61:1742–1751
15. Osmai M, Osmai Y, Bang-Berthelsen CH et al (2016) MicroRNAs as regulators of beta-cell function and dysfunction. Diabetes Metab Res Rev 32:334–349
16. Seyhan AA, Nunez Lopez YO, Xie H et al (2016) Pancreas-enriched miRNAs are altered in the circulation of subjects with diabetes: a pilot cross-sectional study. Sci Report 6:31479
17. Kroh EM, Parkin RK, Mitchell PS, Tewari M (2010) Analysis of circulating microRNA biomarkers in plasma and serum using quantitative reverse transcription-PCR (qRT-PCR). Methods (San Diego, Calif) 50:298–301
18. Wang K, Zhang S, Marzolf B et al (2009) Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci U S A 106:4402–4407
19. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659
20. Guay C, Regazzi R (2013) Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol 9:513–521
21. Latreille M, Herrmanns K, Renwick N et al (2015) miR-375 gene dosage in pancreatic beta-cells: implications for regulation of beta-cell mass and biomarker development. J Mol Med (Berlin, Germany) 93:1159–1169
22. Kanak MA, Takita M, Shahbazov R et al (2015) Evaluation of microRNA375 as a novel biomarker for graft damage in clinical islet transplantation. Transplantation 99:1568–1573
23. Nielsen LB, Wang C, Sorensen K et al (2012) Circulating levels of microRNA from children with newly diagnosed type 1 diabetes and healthy controls: evidence that miR-25 associates to residual beta-cell function and glycaemic control during disease progression. Exp Diabetes Res 2012:896362
24. Marchand L, Jalabert A, Meugnier E et al (2016) miRNA-375 a sensor of glucotoxicity is altered in the serum of children with newly diagnosed type 1 diabetes. J Diabetes Res 2016:1869082
25. Mahon JL, Sosenko JM, Rafkin-Mervis L et al (2009) The TrialNet natural history study of the development of type 1 diabetes: objectives, design, and initial results. Pediatr Diabetes 10:97–104
26. Lampasona V, Schlosser M, Mueller PW et al (2011) Diabetes antibody standardization program: first proficiency evaluation of assays for autoantibodies to zinc transporter 8. Clin Chem 57:1693–1702
27. Mestdagh P, Van Vlierberghe P, De Weer A et al (2009) A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol 10:R64
28. Mukherjee SN, Sykacek P, Roberts SJ, Gurr SJ (2003) Gene ranking using bootstrapped P-values. SIGKDD Explor 5:14–18
29. Sosenko JM, Palmer JP, Rafkin LE et al (2010) Trends of earlier and later responses of C-peptide to oral glucose challenges with progression to type 1 diabetes in diabetes prevention trial-type 1 participants. Diabetes Care 33:620–625
30. Sosenko JM, Skyler JS, DiMeglio LA et al (2015) A new approach for diagnosing type 1 diabetes in autoantibody-positive individuals based on prediction and natural history. Diabetes Care 38:271–276
31. Wherrett DK, Chiang JL, Delamater AM et al (2015) Defining pathways for development of disease-modifying therapies in children with type 1 diabetes: a consensus report. Diabetes Care 38:1975–1985
32. Ziegler AG, Rewers M, Simell O et al (2013) Seroconversion to multiple islet autoantibodies and risk of progression to diabetes in children. JAMA 309:2473–2479
33. Yan M, Chen C, Gong W et al (2015) miR-21-3p regulates cardiac hypertrophic response by targeting histone deacetylase-8. Cardiovasc Res 105:340–352
34. Christensen DP, Dahllof M, Lundh M et al (2011) Histone deacetylase (HDAC) inhibition as a novel treatment for diabetes mellitus. Mol Med (Camb, Mass) 17:378–390
35. Nerup J, Pociot F (2001) A genomewide scan for type 1-diabetes susceptibility in Scandinavian families: identification of new loci with evidence of interactions. Am J Hum Genet 69:1301–1313
36. Bang C, Batkai S, Dangwal S et al (2014) Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Investig 124:2136–2146
37. Roggli E, Britan A, Gattesco S et al (2010) Involvement of microRNAs in the cytotoxic effects exerted by proinflammatory cytokines on pancreatic beta-cells. Diabetes 59:978–986
38. Bravo-Egana V, Rosero S, Klein D et al (2012) Inflammation-mediated regulation of microRNA expression in transplanted pancreatic islets. J Transp Secur 2012:723614
39. Ruan Q, Wang T, Kameswaran V et al (2011) The microRNA-21-PDCD4 axis prevents type 1 diabetes by blocking pancreatic beta cell death. Proc Natl Acad Sci U S A 108:12030–12035
40. Klein D, Misawa R, Bravo-Egana V et al (2013) MicroRNA expression in alpha and beta cells of human pancreatic islets. PLoS One 8:e55064
41. Dooley J, Garcia-Perez JE, Sreenivasan J et al (2016) The microRNA-29 family dictates the balance between homeostatic and pathological glucose handling in diabetes and obesity. Diabetes 65:53–61
42. Bagge A, Clausen TR, Larsen S et al (2012) MicroRNA-29a is up-regulated in beta-cells by glucose and decreases glucose-stimulated insulin secretion. Biochem Biophys Res Commun 426:266–272
43. Bagge A, Dahmcke CM, Dalgaard LT (2013) Syntaxin-1a is a direct target of miR-29a in insulin-producing beta-cells. Horm Metab Res 45:463–466
44. Pullen TJ, da Silva XG, Kelsey G, Rutter GA (2011) miR-29a and miR-29b contribute to pancreatic beta-cell-specific silencing of monocarboxylate transporter 1 (Mct1). Mol Cell Biol 31:3182–3194
45. Kim KW, Ho A, Alshabee-Akil A et al (2016) Coxsackievirus B5 infection induces dysregulation of microRNAs predicted to target known type 1 diabetes risk genes in human pancreatic islets. Diabetes 65:996–1003
46. Sims EK, Chaudhry Z, Watkins R et al (2016) Elevations in the fasting serum proinsulin-to-C-peptide ratio precede the onset of type 1 diabetes. Diabetes Care 39:1519–1526
47. Akirav EM, Lebastchi J, Galvan EM et al (2011) Detection of beta cell death in diabetes using differentially methylated circulating DNA. Proc Natl Acad Sci U S A 108:19018–19023
48. Estrella S, Garcia-Diaz DF, Codner E, Camacho-Guillen P, Perez-Bravo F (2016) Expression of miR-22 and miR-150 in type 1 diabetes mellitus: possible relationship with autoimmunity and clinical characteristics. Med Clin 147:245–247
49. Abuhatzira L, Xu H, Tahhan G, Boulougoura A, Schaffer AA, Notkins AL (2015) Multiple microRNAs within the 14q32 cluster target the mRNAs of major type 1 diabetes autoantigens IA-2, IA-2beta, and GAD65. FASEB J 29:4374–4383
50. Wang L, Qin Y, Tong L et al (2012) MiR-342-5p suppresses coxsackievirus B3 biosynthesis by targeting the 2C-coding region. Antivir Res 93:270–279