Identification and Characterization of microRNAs Associated With Human β-Cell Loss in a Mouse Model

American Journal of Transplantation

Volumn 17, Issue 4, 2017, Pages 992-1007

  Roat, R ^a   Hossain, M M ^a   Christopherson, J ^a   Free, C ^a   Jain, S ^a   Guay, C ^b   Regazzi, R ^b   Guo, Z ^a,c  

^a SANFORD RESEARCH   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

basic (laboratory) research science; cell death; diabetes: type 1; endocrinology diabetology; islet transplantation; islets of Langerhans; molecular biology; molecular biology: microRNA

Indexed keywords

MICRORNA; MICRORNA 375;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL LOSS; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; HYPERGLYCEMIA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE TRANSFER; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET TRANSPLANTATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TUNEL ASSAY; ADOPTIVE TRANSFER; ANIMAL; BLOOD; DISEASE MODEL; EXPERIMENTAL DIABETES MELLITUS; GENETICS; GRAFT SURVIVAL; HUMAN; IMMUNOLOGY; LYMPHOCYTE; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; FEMALE; GRAFT SURVIVAL; HUMANS; HYPERGLYCEMIA; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS TRANSPLANTATION; LYMPHOCYTES; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MICRORNAS;

EID: 85000434635     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.14073     Document Type: Article

References (50)

1. Sherry NA, Tsai EB, Herold KC. Natural history of beta-cell function in type 1 diabetes. Diabetes 2005; 54(Suppl 2): S32–S39.
2. Chhabra P, Brayman KL. Stem cell therapy to cure type 1 diabetes: From hype to hope. Stem Cells Transl Med 2013; 2: 328–336.
3. Watkins RA, Evans-Molina C, Blum JS, DiMeglio LA. Established and emerging biomarkers for the prediction of type 1 diabetes: A systematic review. Transl Res 2014; 164: 110–121.
4. Bonifacio E. Predicting type 1 diabetes using biomarkers. Diabetes Care 2015; 38: 989–996.
5. Shapiro AM, Lakey JR, Ryan EA, et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med 2000; 343: 230–238.
6. Hering BJ, Bellin MD. Transplantation: Sustained benefits of islet transplants for T1DM. Nat Rev Endocrinol 2015; 11: 572–574.
7. Brennan DC, Kopetskie HA, Sayre PH, et al. Long-term follow-up of the Edmonton protocol of islet transplantation in the United States. Am J Transplant 2015; 16: 509–517.
8. Lablanche S, Borot S, Wojtusciszyn A, et al. Five-year metabolic, functional, and safety results of patients with type 1 diabetes transplanted with allogenic islets within the Swiss-French GRAGIL network. Diabetes Care 2015; 38: 1714–1722.
9. Krogvold L, Edwin B, Buanes T, et al. Pancreatic biopsy by minimal tail resection in live adult patients at the onset of type 1 diabetes: Experiences from the DiViD study. Diabetologia 2014; 57: 841–843.
10. Brissova M, Fowler MJ, Nicholson WE, et al. Assessment of human pancreatic islet architecture and composition by laser scanning confocal microscopy. J Histochem Cytochem 2005; 53: 1087–1097.
11. Cabrera O, Berman DM, Kenyon NS, Ricordi C, Berggren PO, Caicedo A. The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc Natl Acad Sci USA 2006; 103: 2334–2339.
12. Kim A, Miller K, Jo J, Kilimnik G, Wojcik P, Hara M. Islet architecture: A comparative study. Islets 2009; 1: 129–136.
13. Brehm MA, Shultz LD, Greiner DL. Humanized mouse models to study human diseases. Curr Opin Endocrinol Diabetes Obes 2010; 17: 120–125.
14. Luo J, Nguyen K, Chen M, et al. Evaluating insulin secretagogues in a humanized mouse model with functional human islets. Metabolism 2013; 62: 90–99.
15. Liu B, Hao J, Pan Y, et al. Increasing donor chimerism and inducing tolerance to islet allografts by post-transplant donor lymphocyte infusion. Am J Transplant 2006; 6(5 Pt 1): 933–946.
16. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29: e45.
17. Tian L, Gao J, Weng G, et al. Comparison of exendin-4 on beta-cell replication in mouse and human islet grafts. Transpl Int 2011; 24: 856–864.
18. Ansarullah, Free C, Christopherson J, et al. Activation of GPR119 stimulates human β-cell replication and neogenesis in humanized mice with functional human islets. J Diabetes Res 2016; 2016: 12.
19. Wicker LS, Miller BJ, Mullen Y. Transfer of autoimmune diabetes mellitus with splenocytes from nonobese diabetic (NOD) mice. Diabetes 1986; 35: 855–860.
20. Christianson SW, Shultz LD, Leiter EH. Adoptive transfer of diabetes into immunodeficient NOD-scid/scid mice. Relative contributions of CD4 + and CD8 + T-cells from diabetic versus prediabetic NOD.NON-Thy-1a donors. Diabetes 1993; 42: 44–55.
21. Rohane PW, Shimada A, Kim DT, et al. Islet-infiltrating lymphocytes from prediabetic NOD mice rapidly transfer diabetes to NOD-scid/scid mice. Diabetes 1995; 44: 550–554.
22. Tian B, Hao J, Zhang Y, et al. Upregulating CD4 + CD25 + FOXP3 + regulatory T cells in pancreatic lymph nodes in diabetic NOD mice by adjuvant immunotherapy. Transplantation 2009; 87: 198–206.
23. Eizirik DL, Pipeleers DG, Ling Z, Welsh N, Hellerstrom C, Andersson A. Major species differences between humans and rodents in the susceptibility to pancreatic beta-cell injury. Proc Natl Acad Sci USA 1994; 91: 9253–9256.
24. Yang H, Wright Jr JR. Human beta cells are exceedingly resistant to streptozotocin in vivo. Endocrinology 2002; 143: 2491–2495.
25. Poy MN, Eliasson L, Krutzfeldt J, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004; 432: 226–230.
26. Keller DM, Clark EA, Goodman RH. Regulation of microRNA-375 by cAMP in pancreatic beta-cells. Mol Endocrinol 2012; 26: 989–999.
27. Poy MN, Hausser J, Trajkovski M, et al. miR-375 maintains normal pancreatic alpha- and beta-cell mass. Proc Natl Acad Sci USA 2009; 106: 5813–5818.
28. Erener S, Mojibian M, Fox JK, Denroche HC, Kieffer TJ. Circulating miR-375 as a biomarker of beta-cell death and diabetes in mice. Endocrinology 2013; 154: 603–608.
29. Kanak MA, Takita M, Shahbazov R, et al. Evaluation of microRNA375 as a novel biomarker for graft damage in clinical islet transplantation. Transplantation 2015; 99: 1568–1573.
30. Yoshimatsu G, Takita M, Kanak MA, et al. MiR-375 and miR-200c as predictive biomarkers of islet isolation and transplantation in total pancreatectomy with islet autotransplantation. J Hepatobiliary Pancreat Sci 2016; 23: 585–594.
31. Marchand L, Jalabert A, Meugnier E, et al. miRNA-375 a sensor of glucotoxicity is altered in the serum of children with newly diagnosed type 1 diabetes. J Diabetes Res 2016; 2016: 1869082.
32. Seyhan AA, Nunez Lopez YO, Xie H, et al. Pancreas-enriched miRNAs are altered in the circulation of subjects with diabetes: A pilot cross-sectional study. Sci Rep 2016; 6: 31479.
33. Zhou F, Wang W, Xing Y, Wang T, Xu X, Wang J. NF-kappaB target microRNAs and their target genes in TNFalpha-stimulated HeLa cells. Biochim Biophys Acta 2014; 1839: 344–354.
34. Armstrong DA, Green BB, Seigne JD, Schned AR, Marsit CJ. MicroRNA molecular profiling from matched tumor and bio-fluids in bladder cancer. Mol Cancer 2015; 14: 194.
35. Polytarchou C, Oikonomopoulos A, Mahurkar S, et al. Assessment of circulating microRNAs for the diagnosis and disease activity evaluation in patients with ulcerative colitis by using the nanostring technology. Inflamm Bowel Dis 2015; 21: 2533–2539.
36. Ji H, Chen M, Greening DW, et al. Deep sequencing of RNA from three different extracellular vesicle (EV) subtypes released from the human LIM1863 colon cancer cell line uncovers distinct miRNA-enrichment signatures. PLoS ONE 2014; 9: e110314.
37. Morita K, Shirabe K, Taketomi A, et al. Relevance of MicroRNA-18a and MicroRNA-199a-5p to hepatocellular carcinoma recurrence after living donor liver transplantation. Liver Transpl 2016; 22: 665–676.
38. Petrillo M, Zannoni G, Beltrame L, et al. Identification of high-grade serous ovarian cancer miRNA species associated with survival and drug response in patients receiving neo-adjuvant chemotherapy: A retrospective longitudinal analysis using matched tumor biopsies. Ann Oncol 2016; 27: 625–634.
39. Byrnes KA, Phatak P, Mansour D, et al. Overexpression of miR-199a-5p decreases esophageal cancer cell proliferation through repression of mitogen-activated protein kinase kinase kinase-11 (MAP3K11). Oncotarget 2016; 7: 8756–8770.
40. Mata R, Palladino C, Nicolosi ML, et al. IGF-I induces upregulation of DDR1 collagen receptor in breast cancer cells by suppressing MIR-199a-5p through the PI3K/AKT pathway. Oncotarget 2015; 7: 7683–7700.
41. Collares CV, Evangelista AF, Xavier DJ, et al. Identifying common and specific microRNAs expressed in peripheral blood mononuclear cell of type 1, type 2, and gestational diabetes mellitus patients. BMC Res Notes 2013; 6: 491.
42. Brase JC, Johannes M, Schlomm T, et al. Circulating miRNAs are correlated with tumor progression in prostate cancer. Int J Cancer 2011; 128: 608–616.
43. Yin J, Hou P, Wu Z, Wang T, Nie Y. Circulating miR-375 and miR-199a-3p as potential biomarkers for the diagnosis of hepatocellular carcinoma. Tumour Biol 2015; 36: 4501–4507.
44. Chen X, Ba Y, Ma L, et al. Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 2008; 18: 997–1006.
45. Gilad S, Meiri E, Yogev Y, et al. Serum microRNAs are promising novel biomarkers. PLoS ONE 2008; 3: e3148.
46. Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 2008; 105: 10513–10518.
47. Moran I, Akerman I, van de Bunt M, et al. Human beta cell transcriptome analysis uncovers lncRNAs that are tissue-specific, dynamically regulated, and abnormally expressed in type 2 diabetes. Cell Metab 2012; 16: 435–448.
48. Kameswaran V, Kaestner KH. The Missing lnc(RNA) between the pancreatic beta-cell and diabetes. Front Genet 2014; 5: 200.
49. Esguerra JL, Eliasson L. Functional implications of long non-coding RNAs in the pancreatic islets of Langerhans. Front Genet 2014; 5: 209.
50. Engin F, Yermalovich A, Nguyen T, et al. Restoration of the unfolded protein response in pancreatic beta cells protects mice against type 1 diabetes. Sci Transl Med 2013; 5: 211ra156.