Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2014, Article ID 618652, 12 pages
http://dx.doi.org/10.1155/2014/618652
Review Article

Role of MicroRNAs in Islet Beta-Cell Compensation and Failure during Diabetes

1Lille 2 University, European Genomic Institute for Diabetes (EGID), FR 3508, UMR-8199 Lille, France
2Service of Internal Medicine, Hospital-University of Lausanne (CHUV), 1011 Lausanne, Switzerland
3Department of Fundamental Neurosciences, University of Lausanne, 1005 Lausanne, Switzerland

Received 24 October 2013; Accepted 24 January 2014; Published 5 March 2014

Academic Editor: Stephane Dalle

Copyright © 2014 Valérie Plaisance et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Prentki and C. J. Nolan, “Islet β cell failure in type 2 diabetes,” The Journal of Clinical Investigation, vol. 116, no. 7, pp. 1802–1812, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. G. C. Weir and S. Bonner-Weir, “Five of stages of evolving β-cell dysfunction during progression to diabetes,” Diabetes, vol. 53, supplement 3, pp. S16–S21, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. A. E. Butler, J. Janson, S. Bonner-Weir, R. Ritzel, R. A. Rizza, and P. C. Butler, “β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes,” Diabetes, vol. 52, no. 1, pp. 102–110, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. J. J. Meier, T. G. K. Breuer, R. C. Bonadonna et al., “Pancreatic diabetes manifests when beta cell area declines by approximately 65% in humans,” Diabetologia, vol. 55, no. 5, pp. 1346–1354, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. J. J. Meier, “Beta cell mass in diabetes: a realistic therapeutic target?” Diabetologia, vol. 51, no. 5, pp. 703–713, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Camastra, M. Manco, A. Mari et al., “β-cell function in morbidly obese subjects during free living: long-term effects of weight loss,” Diabetes, vol. 54, no. 8, pp. 2382–2389, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Y. Donath, J. A. Ehses, K. Maedler et al., “Mechanisms of β-cell death in type 2 diabetes,” Diabetes, vol. 54, supplement 2, pp. S108–S113, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Rahier, Y. Guiot, R. M. Goebbels, C. Sempoux, and J. C. Henquin, “Pancreatic β-cell mass in European subjects with type 2 diabetes,” Diabetes, Obesity & Metabolism, vol. 10, supplement 4, pp. 32–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Marselli, M. Suleiman, M. Masini et al., “Are we overestimating the loss of beta cells in type 2 diabetes?” Diabetologia, vol. 57, no. 2, pp. 362–365, 2014. View at Publisher · View at Google Scholar
  10. S. Gargani, J. Thevenet, J. E. Yuan et al., “Adaptive changes of human islets to an obesogenic environment in the mouse,” Diabetologia, vol. 56, no. 2, pp. 350–358, 2013. View at Publisher · View at Google Scholar
  11. B. Tyrberg, J. Ustinov, T. Otonkoski, and A. Andersson, “Stimulated endocrine cell proliferation and differentiation in transplanted human pancreatic islets: effects of the ob gene and compensatory growth of the implantation organ,” Diabetes, vol. 50, no. 2, pp. 301–307, 2001. View at Google Scholar · View at Scopus
  12. K. Maedler and M. Y. Donath, “Beta-cells in type 2 diabetes: a loss of function and mass,” Hormone Research, vol. 62, supplement 3, pp. 67–73, 2004. View at Google Scholar · View at Scopus
  13. K. Maedler, D. M. Schumann, F. Schulthess et al., “Aging correlates with decreased β-cell proliferative capacity and enhanced sensitivity to apoptosis: a potential role for fas and pancreatic duodenal homeobox-1,” Diabetes, vol. 55, no. 9, pp. 2455–2462, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. D. M. Nathan, “Long-term complications of diabetes mellitus,” The New England Journal of Medicine, vol. 328, no. 23, pp. 1676–1685, 1993. View at Publisher · View at Google Scholar · View at Scopus
  15. C. N. Street, J. R. T. Lakey, A. M. J. Shapiro et al., “Islet graft assessment in the Edmonton Protocol: implications for predicting long-term clinical outcome,” Diabetes, vol. 53, no. 12, pp. 3107–3114, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Wild, G. Roglic, A. Green, R. Sicree, and H. King, “Global prevalence of diabetes: estimates for the year 2000 and projections for 2030,” Diabetes Care, vol. 27, no. 5, pp. 1047–1053, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Safdar, A. Abadi, M. Akhtar, B. P. Hettinga, and M. A. Tarnopolsky, “miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57BI/6J male mice,” PLoS ONE, vol. 4, no. 5, Article ID e5610, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. D. P. Bartel, “MicroRNAs: target recognition and regulatory functions,” Cell, vol. 136, no. 2, pp. 215–233, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Baek, J. Villén, C. Shin, F. D. Camargo, S. P. Gygi, and D. P. Bartel, “The impact of microRNAs on protein output,” Nature, vol. 455, no. 7209, pp. 64–71, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. F. C. Lynn, P. Skewes-Cox, Y. Kosaka, M. T. McManus, B. D. Harfe, and M. S. German, “MicroRNA expression is required for pancreatic islet cell genesis in the mouse,” Diabetes, vol. 56, no. 12, pp. 2938–2945, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. M. V. Joglekar, V. M. Joglekar, and A. A. Hardikar, “Expression of islet-specific microRNAs during human pancreatic development,” Gene Expression Patterns, vol. 9, no. 2, pp. 109–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. M. N. Poy, L. Eliasson, J. Krutzfeldt et al., “A pancreatic islet-specific microRNA regulates insulin secretion,” Nature, vol. 432, no. 7014, pp. 226–230, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Guay, E. Roggli, V. Nesca, C. Jacovetti, and R. Regazzi, “Diabetes mellitus, a microRNA-related disease?” Translational Research, vol. 157, no. 4, pp. 253–264, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Lovis, S. Gattesco, and R. Regazzi, “Regulation of the expression of components of the exocytotic machinery of insulin-secreting cells by microRNAs,” Biological Chemistry, vol. 389, no. 3, pp. 305–312, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Baroukh, M. A. Ravier, M. K. Loder et al., “MicroRNA-124a regulates foxa2 expression and intracellular signaling in pancreatic β-cell lines,” The Journal of Biological Chemistry, vol. 282, no. 27, pp. 19575–19588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Plaisance, A. Abderrahmani, V. Perret-Menoud, P. Jacquemin, F. Lemaigre, and R. Regazzi, “MicroRNA-9 controls the expression of Granuphilin/Slp4 and the secretory response of insulin-producing cells,” The Journal of Biological Chemistry, vol. 281, no. 37, pp. 26932–26942, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. F. W. Pagliuca and D. A. Melton, “How to make a functional beta-cell,” Development, vol. 140, pp. 2472–2483, 2013. View at Publisher · View at Google Scholar
  28. L. Bouwens and I. Rooman, “Regulation of pancreatic beta-cell mass,” Physiological Reviews, vol. 85, no. 4, pp. 1255–1270, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. J. M. Rukstalis and J. F. Habener, “Neurogenin3: a master regulator of pancreatic islet differentiation and regeneration,” Islets, vol. 1, no. 3, pp. 177–184, 2009. View at Google Scholar · View at Scopus
  30. C. S. Lee, N. Perreault, J. E. Brestelli, and K. H. Kaestner, “Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity,” Genes & Development, vol. 16, no. 12, pp. 1488–1497, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. Å. Apelqvist, H. Li, L. Sommer et al., “Notch signalling controls pancreatic cell differentiation,” Nature, vol. 400, no. 6747, pp. 877–881, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Winter, S. Jung, S. Keller, R. I. Gregory, and S. Diederichs, “Many roads to maturity: microRNA biogenesis pathways and their regulation,” Nature Cell Biology, vol. 11, no. 3, pp. 228–234, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. M. V. Joglekar, V. S. Parekh, S. Mehta, R. R. Bhonde, and A. A. Hardikar, “MicroRNA profiling of developing and regenerating pancreas reveal post-transcriptional regulation of neurogenin3,” Developmental Biology, vol. 311, no. 2, pp. 603–612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. C. S. Lee, D. D. de León, K. H. Kaestner, and D. A. Stoffers, “Regeneration of pancreatic islets after partial pancreatectomy in mice does not involve the reactivation of neurogenin-3,” Diabetes, vol. 55, no. 2, pp. 269–272, 2006. View at Google Scholar · View at Scopus
  35. H.-L. C. Kaung, “Growth dynamics of pancreatic islet cell populations during fetal and neonatal development of the rat,” Developmental Dynamics, vol. 200, no. 2, pp. 163–175, 1994. View at Google Scholar · View at Scopus
  36. R. C. McEvoy and K. L. Madson, “Pancreatic insulin-, glucagon-, and somatostatin-positive islet cell populations during the perinatal development of the rat. I. Morphometric quantitation,” Biology of the Neonate, vol. 38, no. 5-6, pp. 248–254, 1980. View at Google Scholar · View at Scopus
  37. R. C. McEvoy, “Changes in the volumes of the A-, B-, and D-cell populations in the pancreatic islets during the postnatal development of the rat,” Diabetes, vol. 30, no. 10, pp. 813–817, 1981. View at Google Scholar · View at Scopus
  38. E. Montanya, V. Nacher, M. Biarnes, and J. Soler, “Linear correlation between β-cell mass and body weight throughout the lifespan in Lewis rats: role of β-cell hyperplasia and hypertrophy,” Diabetes, vol. 49, no. 8, pp. 1341–1346, 2000. View at Google Scholar · View at Scopus
  39. R. N. Wang, L. Bouwens, and G. Klöppel, “Beta-cell growth in adolescent and adult rats treated with streptozotocin during the neonatal period,” Diabetologia, vol. 39, no. 5, pp. 548–557, 1996. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Kalis, C. Bolmeson, J. L. S. Esguerra et al., “Beta-cell specific deletion of dicer1 leads to defective insulin secretion and diabetes mellitus,” PLoS ONE, vol. 6, no. 12, Article ID e29166, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. A. D. Mandelbaum, T. Melkman-Zehavi, R. Oren et al., “Dysregulation of Dicer1 in beta cells impairs islet architecture and glucose metabolism,” Experimental Diabetes Research, vol. 2012, Article ID 470302, 8 pages, 2012. View at Publisher · View at Google Scholar
  42. M. N. Poy, J. Hausser, M. Trajkovski et al., “miR-375 maintains normal pancreatic α- and β-cell mass,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 14, pp. 5813–5818, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. W. P. Kloosterman, A. K. Lagendijk, R. F. Ketting, J. D. Moulton, and R. H. A. Plasterk, “Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development,” PLoS Biology, vol. 5, no. 8, Article ID e203, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Correa-Medina, V. Bravo-Egana, S. Rosero et al., “MicroRNA miR-7 is preferentially expressed in endocrine cells of the developing and adult human pancreas,” Gene Expression Patterns, vol. 9, no. 4, pp. 193–199, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Wang, J. Liu, C. Liu, A. Naji, and D. A. Stoffers, “MicroRNA-7 regulates the mTOR pathway and proliferation in adult pancreatic beta-cells,” Diabetes, vol. 62, no. 3, pp. 887–895, 2013. View at Publisher · View at Google Scholar
  46. L. Rachdi, N. Balcazar, F. Osorio-Duque et al., “Disruption of Tsc2 in pancreatic β cells induces β cell mass expansion and improved glucose tolerance in a TORC1-dependent manner,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 27, pp. 9250–9255, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Hamada, K. Hara, T. Hamada et al., “Upregulation of the mammalian target of rapamycin complex 1 pathway by Ras homolog enriched in brain in pancreatic β-cells leads to increased β-cell mass and prevention of hyperglycemia,” Diabetes, vol. 58, no. 6, pp. 1321–1332, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Xie and T. P. Herbert, “The role of mammalian target of rapamycin (mTOR) in the regulation of pancreatic β-cell mass: implications in the development of type-2 diabetes,” Cellular and Molecular Life Sciences, vol. 69, no. 8, pp. 1289–1304, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Parnaud, D. Bosco, T. Berney et al., “Proliferation of sorted human and rat beta cells,” Diabetologia, vol. 51, no. 1, pp. 91–100, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. J. J. Meier, A. E. Butler, Y. Saisho et al., “β-cell replication is the primary mechanism subserving the postnatal expansion of β-cell mass in humans,” Diabetes, vol. 57, no. 6, pp. 1584–1594, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. P. I. Veld, N. de Munck, K. van Belle et al., “β-cell replication is increased in donor organs from young patients after prolonged life support,” Diabetes, vol. 59, no. 7, pp. 1702–1708, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Bar, H. A. Russ, S. Knoller, L. Ouziel-Yahalom, and S. Efrat, “HES-1 is involved in adaptation of adult human β-cells to proliferation in vitro,” Diabetes, vol. 57, no. 9, pp. 2413–2420, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Rutti, N. S. Sauter, K. Bouzakri, R. Prazak, P. A. Halban, and M. Y. Donath, “In vitro proliferation of adult human beta-cells,” PLoS ONE, vol. 7, no. 4, Article ID e35801, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. D. J. Drucker, “The biology of incretin hormones,” Cell Metabolism, vol. 3, no. 3, pp. 153–165, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. D. J. Hodson, R. K. Mitchell, E. A. Bellomo et al., “Lipotoxicity disrupts incretin-regulated human beta cell connectivity,” The Journal of Clinical Investigation, vol. 123, no. 10, pp. 4182–4194, 2013. View at Publisher · View at Google Scholar
  56. M. Ferdaoussi, S. Abdelli, J.-Y. Yang et al., “Exendin-4 protects β-cells from interleukin-1β-induced apoptosis by interfering with the c-Jun NH2-terminal kinase pathway,” Diabetes, vol. 57, no. 5, pp. 1205–1215, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. D. M. Keller, E. A. Clark, and R. H. Goodman, “Regulation of microRNA-375 by cAMP in pancreatic beta-cells,” Molecular Endocrinology, vol. 26, no. 6, pp. 989–999, 2012. View at Publisher · View at Google Scholar
  58. A. El Ouaamari, N. Baroukh, G. A. Martens, P. Lebrun, D. Pipeleers, and E. van Obberghen, “MiR-375 targets 3′-phosphoinositide-dependent protein kinase-1 and regulates glucose-induced biological responses in pancreatic β-Cells,” Diabetes, vol. 57, no. 10, pp. 2708–2717, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. A. M. Krichevsky, K.-C. Sonntag, O. Isacson, and K. S. Kosik, “Specific MicroRNAs modulate embryonic stem cell-derived neurogenesis,” Stem Cells, vol. 24, no. 4, pp. 857–864, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Abderrahmani, V. Plaisance, P. Lovis, and R. Regazzi, “Mechanisms controlling the expression of the components of the exocytotic apparatus under physiological and pathological conditions,” Biochemical Society Transactions, vol. 34, no. 5, pp. 696–700, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. F. C. Schuit, P. A. I. Veld, and D. G. Pipeleers, “Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 11, pp. 3865–3869, 1988. View at Google Scholar · View at Scopus
  62. J. Suckale and M. Solimena, “Pancreas islets in metabolic signaling—focus on the beta-cell,” Frontiers in Bioscience, vol. 13, no. 18, pp. 7156–7171, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. X. Tang, L. Muniappan, G. Tang, and S. Özcan, “Identification of glucose-regulated miRNAs from pancreatic β cells reveals a role for miR-30d in insulin transcription,” RNA, vol. 15, no. 2, pp. 287–293, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. S. S. Andrali, M. L. Smapley, N. L. Vanderford, and S. Özcan, “Glucose regulation of insulin gene expression in pancreatic β-cells,” Biochemical Journal, vol. 415, no. 1, pp. 1–10, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Xu, J. Chen, G. Jing, and A. Shalev, “Thioredoxin-interacting protein regulates insulin transcription through microRNA-204,” Nature Medicine, vol. 19, pp. 1141–1146, 2013. View at Publisher · View at Google Scholar
  66. E. Tweedie, I. Artner, L. Crawford et al., “Maintenance of hepatic nuclear factor 6 in postnatal islets impairs terminal differentiation and function of β-cells,” Diabetes, vol. 55, no. 12, pp. 3264–3270, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. I. Rafiq, G. da Silva Xavier, S. Hooper, and G. A. Rutter, “Glucose-stimulated preproinsulin gene expression and nuclear trans-location of pancreatic duodenum homeobox-1 require activation of phosphatidylinositol 3-kinase but not p38 MAPK/SAPK2,” The Journal of Biological Chemistry, vol. 275, no. 21, pp. 15977–15984, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. C. J. Rhodes, M. F. White, J. L. Leahy, and S. E. Kahn, “Direct autocrine action of insulin on beta-cells: does it make physiological sense?” Diabetes, vol. 62, no. 7, pp. 2157–2163, 2013. View at Publisher · View at Google Scholar
  69. N. Hashimoto, Y. Kido, T. Uchida et al., “Ablation of PDK1 in pancreatic β cells induces diabetes as a result of loss of β cell mass,” Nature Genetics, vol. 38, no. 5, pp. 589–593, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. T. J. Pullen and G. A. Rutter, “When less is more: the forbidden fruits of gene repression in the adult beta-cell,” Diabetes, Obesity & Metabolism, vol. 15, no. 6, pp. 503–512, 2013. View at Publisher · View at Google Scholar
  71. T. J. Pullen, L. Sylow, G. Sun, A. P. Halestrap, E. A. Richter, and G. A. Rutter, “Overexpression of monocarboxylate transporter-1 (SLC16A1) in mouse pancreatic beta-cells leads to relative hyperinsulinism during exercise,” Diabetes, vol. 61, no. 7, pp. 1719–1725, 2012. View at Publisher · View at Google Scholar
  72. J. A. Parsons, T. C. Brelje, and R. L. Sorenson, “Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion,” Endocrinology, vol. 130, no. 3, pp. 1459–1466, 1992. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Rieck and K. H. Kaestner, “Expansion of β-cell mass in response to pregnancy,” Trends in Endocrinology and Metabolism, vol. 21, no. 3, pp. 151–158, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. C. Jacovetti, A. Abderrahmani, G. Parnaud et al., “MicroRNAs contribute to compensatory beta cell expansion during pregnancy and obesity,” The Journal of Clinical Investigation, vol. 122, no. 10, pp. 3541–3551, 2012. View at Publisher · View at Google Scholar
  75. C. Jacovetti and R. Regazzi, “Compensatory beta-cell mass expansion: a big role for a tiny actor,” Cell Cycle, vol. 12, no. 2, pp. 197–198, 2013. View at Publisher · View at Google Scholar
  76. A. E. Butler, L. Cao-Minh, R. Galasso et al., “Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy,” Diabetologia, vol. 53, no. 10, pp. 2167–2176, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. P. L. Brubaker and D. J. Drucker, “Minireview: glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system,” Endocrinology, vol. 145, no. 6, pp. 2653–2659, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. G. Valsamakis, A. Margeli, N. Vitoratos et al., “The role of maternal gut hormones in normal pregnancy: fasting plasma active glucagon-like peptide 1 level is a negative predictor of fetal abdomen circumference and maternal weight change,” European Journal of Endocrinology, vol. 162, no. 5, pp. 897–903, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. A. Nadal, P. Alonso-Magdalena, S. Soriano, A. B. Ropero, and I. Quesada, “The role of oestrogens in the adaptation of islets to insulin resistance,” The Journal of Physiology, vol. 587, no. 21, pp. 5031–5037, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. R. C. Vasavada, A. Garcia-Ocaña, W. S. Zawalich et al., “Targeted expression of placental lactogen in the beta cells of transgenic mice results in beta cell proliferation, islet mass augmentation, and hypoglycemia,” The Journal of Biological Chemistry, vol. 275, no. 20, pp. 15399–15406, 2000. View at Publisher · View at Google Scholar · View at Scopus
  81. G. C. Weir, D. R. Laybutt, H. Kaneto, S. Bonner-Weir, and A. Sharma, “β-cell adaptation and decompensation during the progression of diabetes,” Diabetes, vol. 50, supplement 1, pp. S154–S159, 2001. View at Google Scholar · View at Scopus
  82. J. Y. Chan, J. Luzuriaga, M. Bensellam, T. J. Biden, and D. R. Laybutt, “Failure of the adaptive unfolded protein response in islets of obese mice is linked with abnormalities in beta-cell gene expression and progression to diabetes,” Diabetes, vol. 62, no. 5, pp. 1557–1568, 2013. View at Publisher · View at Google Scholar
  83. K. Kobayashi, T. M. Forte, S. Taniguchi, B. Y. Ishida, K. Oka, and L. Chan, “The db/dbdb/db mouse, a model for diabetic dyslipidemia: molecular characterization and effects of Western diet feeding,” Metabolism, vol. 49, no. 1, pp. 22–31, 2000. View at Publisher · View at Google Scholar · View at Scopus
  84. V. Nesca, C. Guay, C. Jacovetti et al., “Identification of particular groups of microRNAs that positively or negatively impact on beta cell function in obese models of type 2 diabetes,” Diabetologia, vol. 56, no. 10, pp. 2203–2212, 2013. View at Publisher · View at Google Scholar
  85. J. M. Locke, G. da Silva Xavier, H. R. Dawe, G. A. Rutter, and L. W. Harries, “Increased expression of miR-187 in human islets from individuals with type 2 diabetes is associated with reduced glucose-stimulated insulin secretion,” Diabetologia, vol. 57, no. 1, pp. 122–128, 2014. View at Publisher · View at Google Scholar
  86. G. Boden, “Obesity and free fatty acids,” Endocrinology and Metabolism Clinics of North America, vol. 37, no. 3, pp. 635–646, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. M. A. Charles, E. Eschwège, N. Thibult et al., “The role of non-esterified fatty acids in the deterioration of glucose tolerance in Caucasian subjects: results of the Paris prospective study,” Diabetologia, vol. 40, no. 9, pp. 1101–1106, 1997. View at Publisher · View at Google Scholar · View at Scopus
  88. C. Kjørholt, M. C. Åkerfeldt, T. J. Biden, and D. R. Laybutt, “Chronic hyperglycemia, independent of plasma lipid levels, is sufficient for the loss of β-cell differentiation and secretory function in the db/db mouse model of diabetes,” Diabetes, vol. 54, no. 9, pp. 2755–2763, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Y. Donath, D. M. Schumann, M. Faulenbach, H. Ellingsgaard, A. Perren, and J. A. Ehses, “Islet inflammation in type 2 diabetes: from metabolic stress to therapy,” Diabetes Care, vol. 31, supplement 2, pp. S161–S164, 2008. View at Google Scholar · View at Scopus
  90. V. Poitout, “Glucolipotoxicity of the pancreatic β-cell: myth or reality?” Biochemical Society Transactions, vol. 36, no. 5, pp. 901–904, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. P. Lovis, E. Roggli, D. R. Laybutt et al., “Alterations in microRNA expression contribute to fatty acid-induced pancreatic β-Cell dysfunction,” Diabetes, vol. 57, no. 10, pp. 2728–2736, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. K. Eguchi, I. Manabe, Y. Oishi-Tanaka et al., “Saturated fatty acid and TLR signaling link β cell dysfunction and islet inflammation,” Cell Metabolism, vol. 15, no. 4, pp. 518–533, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. E. Roggli, A. Britan, S. Gattesco et al., “Involvement of microRNAs in the cytotoxic effects exerted by proinflammatory cytokines on pancreatic β-cells,” Diabetes, vol. 59, no. 4, pp. 978–986, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Abderrahmani, G. Niederhauser, D. Favre et al., “Human high-density lipoprotein particles prevent activation of the JNK pathway induced by human oxidised low-density lipoprotein particles in pancreatic beta cells,” Diabetologia, vol. 50, no. 6, pp. 1304–1314, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. D. Favre, G. Niederhauser, D. Fahmi et al., “Role for inducible cAMP early repressor in promoting pancreatic beta cell dysfunction evoked by oxidative stress in human and rat islets,” Diabetologia, vol. 54, no. 9, pp. 2337–2346, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. J. A. Haefliger, D. Martin, D. Favre et al., “Reduction of connexin36 content by ICER-1 contributes to insulin-secreting cells apoptosis induced by oxidized LDL particles,” PloS ONE, vol. 8, no. 1, Article ID e55198, 2013. View at Publisher · View at Google Scholar
  97. P. Holvoet, S. B. Kritchevsky, R. P. Tracy et al., “The metabolic syndrome, circulating oxidized LDL, and risk of myocardial infarction in well-functioning elderly people in the health, aging, and body composition cohort,” Diabetes, vol. 53, no. 4, pp. 1068–1073, 2004. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Nakhjavani, O. Khalilzadeh, L. Khajeali et al., “Serum oxidized-LDL is associated with diabetes duration independent of maintaining optimized levels of LDL-cholesterol,” Lipids, vol. 45, no. 4, pp. 321–327, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. G. Bellomo, E. Maggi, M. Poli, F. G. Agosta, P. Bollati, and G. Finardi, “Antoantibodies against oxidatively modified low-density lipoproteins in NIDDM,” Diabetes, vol. 44, no. 1, pp. 60–66, 1995. View at Google Scholar · View at Scopus
  100. L. R. Brunham, J. K. Kruit, C. B. Verchere, and M. R. Hayden, “Cholesterol in islet dysfunction and type 2 diabetes,” The Journal of Clinical Investigation, vol. 118, no. 2, pp. 403–408, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. B. G. Drew, S. J. Duffy, M. F. Formosa et al., “High-density lipoprotein modulates glucose metabolism in patients with type 2 diabetes mellitus,” Circulation, vol. 119, no. 15, pp. 2103–2111, 2009. View at Publisher · View at Google Scholar · View at Scopus
  102. F. Okajima, M. Kurihara, C. Ono et al., “Oxidized but not acetylated low-density lipoprotein reduces preproinsulin mRNA expression and secretion of insulin from HIT-T15 cells,” Biochimica et Biophysica Acta, vol. 1687, no. 1–3, pp. 173–180, 2005. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Rütti, J. A. Ehses, R. A. Sibler et al., “Low- and high-density lipoproteins modulate function, apoptosis, and proliferation of primary human and murine pancreatic β-cells,” Endocrinology, vol. 150, no. 10, pp. 4521–4530, 2009. View at Publisher · View at Google Scholar · View at Scopus
  104. M.-E. Roehrich, V. Mooser, V. Lenain et al., “Insulin-secreting β-cell dysfunction induced by human lipoproteins,” The Journal of Biological Chemistry, vol. 278, no. 20, pp. 18368–18375, 2003. View at Publisher · View at Google Scholar · View at Scopus
  105. A. Bonnefond, P. Froguel, and M. Vaxillaire, “The emerging genetics of type 2 diabetes,” Trends in Molecular Medicine, vol. 16, no. 9, pp. 407–416, 2010. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Vaxillaire, A. Abderrahmani, P. Boutin et al., “Anatomy of a homeoprotein revealed by the analysis of human MODY3 mutations,” The Journal of Biological Chemistry, vol. 274, no. 50, pp. 35639–35646, 1999. View at Publisher · View at Google Scholar · View at Scopus
  107. C. Bonner, K. C. Nyhan, S. Bacon et al., “Identification of circulating microRNAs in HNF1A-MODY carriers,” Diabetologia, vol. 56, no. 8, pp. 1743–1751, 2013. View at Publisher · View at Google Scholar
  108. H. Wang, P. A. Antinozzi, K. A. Hagenfeldt, P. Maechler, and C. B. Wollheim, “Molecular targets of a human HNF1α mutation responsible for pancreatic β-cell dysfunction,” The EMBO Journal, vol. 19, no. 16, pp. 4257–4264, 2000. View at Google Scholar · View at Scopus
  109. C. Guay, C. Jacovetti, V. Nesca, A. Motterle, K. Tugay, and R. Regazzi, “Emerging roles of non-coding RNAs in pancreatic beta-cell function and dysfunction,” Diabetes, Obesity & Metabolism, vol. 14, supplement 3, pp. 12–21, 2012. View at Publisher · View at Google Scholar
  110. A. Zampetaki, S. Kiechl, I. Drozdov et al., “Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes,” Circulation Research, vol. 107, no. 6, pp. 810–817, 2010. View at Publisher · View at Google Scholar · View at Scopus
  111. I. Moran, I. Akerman, M. van de Bunt et al., “Human beta cell transcriptome analysis uncovers lncRNAs that are tissue-specific, dynamically regulated, and abnormally expressed in type 2 diabetes,” Cell Metabolism, vol. 16, no. 4, pp. 435–448, 2012. View at Publisher · View at Google Scholar
  112. C. Wahlestedt, “Targeting long non-coding RNA to therapeutically upregulate gene expression,” Nature Reviews Drug Discovery, vol. 12, pp. 433–446, 2013. View at Publisher · View at Google Scholar
  113. J. T. Lee and M. S. Bartolomei, “X-inactivation, imprinting, and long noncoding RNAs in health and disease,” Cell, vol. 152, no. 6, pp. 1308–1323, 2013. View at Publisher · View at Google Scholar
  114. P. J. Batista and H. Y. Chang, “Long noncoding RNAs: cellular address codes in development and disease,” Cell, vol. 152, no. 6, pp. 1298–1307, 2013. View at Publisher · View at Google Scholar