Beta-Cell Fragility As a Common Underlying Risk Factor in Type 1 and Type 2 Diabetes

Trends in Molecular Medicine

Volumn 23, Issue 2, 2017, Pages 181-194

  Liston, Adrian ^a,b   Todd, John A ^c   Lagou, Vasiliki ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE;

BETA CELL FRAGILITY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; GLUCOSE METABOLISM; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OVERLAPPING GENE; PANCREAS ISLET BETA CELL; REGULATORY MECHANISM; REVIEW; RISK FACTOR; ANIMAL; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; GLUCOSE; HUMANS; INSULIN-SECRETING CELLS; RISK FACTORS;

EID: 85009932512     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2016.12.005     Document Type: Review

References (102)

1. 1 Cnop, M., et al. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 54:Suppl. 2 (2005), S97–S107.
2. 2 Anik, A., et al. Maturity-onset diabetes of the young (MODY): an update. J. Pediatr. Endocrinol. Metab. 28 (2015), 251–263.
3. 3 Roizen, J.D., et al. Progress in understanding type 1 diabetes through its genetic overlap with other autoimmune diseases. Curr. Diabetes Rep., 15, 2015, 102.
4. 4 Christoffersson, G., von Herrath, M.G., A deeper look into type 1 diabetes – imaging immune responses during onset of disease. Front. Immunol., 7, 2016, 313.
5. 5 Bonifacio, E., et al. Rebranding asymptomatic type 1 diabetes: the case for autoimmune beta cell disorder as a pathological and diagnostic entity. Diabetologia 60 (2016), 35–38.
6. 6 Oram, R.A., et al. The majority of patients with long-duration type 1 diabetes are insulin microsecretors and have functioning beta cells. Diabetologia 57 (2014), 187–191.
7. 7 Gitelman, S.E., Bluestone, J.A., Regulatory T cell therapy for type 1 diabetes: may the force be with you. J. Autoimmun. 71 (2016), 78–87.
8. 8 Kolb, H., von Herrath, M., Immunotherapy for type 1 diabetes: why do current protocols not halt the underlying disease process?. Cell Metab., 2016, 10.1016/j.cmet.2016.10.009 Published online November 5, 2016.
9. 9 Lee, Y.H., et al. Glucagon is the key factor in the development of diabetes. Diabetologia 59 (2016), 1372–1375.
10. 10 Unger, R.H., Cherrington, A.D., Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. J. Clin. Invest. 122 (2012), 4–12.
11. 1c and impaired fasting glucose: the Toranomon Hospital Health Management Center Study 4 (TOPICS 4). Diabet. Med. 29 (2012), e279–e285.
12. 12 Butler, A.E., et al. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52 (2003), 102–110.
13. 13 Munnee, K., et al. Comparing the clinical outcomes between insulin-treated and non-insulin-treated patients with type 2 diabetes mellitus after coronary artery bypass surgery: a systematic review and meta-analysis. Medicine, 95, 2016, e3006.
14. 14 Maedler, K., et al. Glucose induces beta-cell apoptosis via upregulation of the Fas receptor in human islets. Diabetes 50 (2001), 1683–1690.
15. 15 Back, S.H., Kaufman, R.J., Endoplasmic reticulum stress and type 2 diabetes. Annu. Rev. Biochem. 81 (2012), 767–793.
16. 16 Zhou, R., et al. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11 (2010), 136–140.
17. 17 Dooley, J., et al. Genetic predisposition for beta cell fragility underlies type 1 and type 2 diabetes. Nat. Genet. 48 (2016), 519–527.
18. 18 Todd, J.A., Intolerable secretion and diabetes in tolerant transgenic mice, revisited. Nat. Genet. 48 (2016), 476–477.
19. 19 Ikegami, H., et al. Mouse models of type 1 and type 2 diabetes derived from the same closed colony: genetic susceptibility shared between two types of diabetes. ILAR J. 45 (2004), 268–277.
20. 20 Wilkin, T., et al. Testing the accelerator hypothesis: a new approach to type 1 diabetes prevention (adAPT 1). Diabetes Obes. Metab. 18 (2016), 3–5.
21. 21 Nogueira, T.C., et al. GLIS3, a susceptibility gene for type 1 and type 2 diabetes, modulates pancreatic beta cell apoptosis via regulation of a splice variant of the BH3-only protein Bim. PLoS Genet., 9, 2013, e1003532.
22. 22 Herold, K.C., et al. Beta cell death and dysfunction during type 1 diabetes development in at-risk individuals. J. Clin. Invest. 125 (2015), 1163–1173.
23. 23 Basile, K.J., et al. Overlap of genetic susceptibility to type 1 diabetes, type 2 diabetes, and latent autoimmune diabetes in adults. Curr. Diabetes Rep., 14, 2014, 550.
24. 24 Prasad, R.B., Groop, L., Genetics of type 2 diabetes—pitfalls and possibilities. Genes 6 (2015), 87–123.
25. 25 Qu, H.Q., et al. Association analysis of type 2 diabetes loci in type 1 diabetes. Diabetes 57 (2008), 1983–1986.
26. 26 Raj, S.M., et al. No association of multiple type 2 diabetes loci with type 1 diabetes. Diabetologia 52 (2009), 2109–2116.
27. 27 Barrett, J.C., et al. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat. Genet. 41 (2009), 703–707.
28. 28 Dupuis, J., et al. New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat. Genet. 42 (2010), 105–116.
29. 29 Li, H., et al. A genome-wide association study identifies GRK5 and RASGRP1 as type 2 diabetes loci in Chinese Hans. Diabetes 62 (2013), 291–298.
30. 30 Cho, Y.S., et al. Meta-analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in East Asians. Nat. Genet. 44 (2011), 67–72.
31. 31 Somers, E.C., et al. Are individuals with an autoimmune disease at higher risk of a second autoimmune disorder?. Am. J. Epidemiol. 169 (2009), 749–755.
32. 32 Karaderi, T., et al. Insights into the genetic susceptibility to type 2 diabetes from genome-wide association studies of obesity-related traits. Curr. Diabetes Rep., 15, 2015, 83.
33. 33 Dauriz, M., Meigs, J.B., Current insights into the joint genetic basis of type 2 diabetes and coronary heart disease. Curr. Cardiovasc. Risk Rep., 8, 2014, 368.
34. 34 Ligthart, S., et al. Pleiotropy among common genetic loci identified for cardiometabolic disorders and C-reactive protein. PLoS One, 10, 2015, e0118859.
35. 35 Teslovich, T.M., et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466 (2010), 707–713.
36. 36 Ridker, P.M., et al. Loci related to metabolic-syndrome pathways including LEPRHNF1AIL6R, and GCKR associate with plasma C-reactive protein: the Women's Genome Health Study. Am. J. Hum. Genet. 82 (2008), 1185–1192.
37. 37 Replication, D.I.G., Genome-wide trans-ancestry meta-analysis provides insight into the genetic architecture of type 2 diabetes susceptibility. Nat. Genet. 46 (2014), 234–244.
38. 38 Locke, A.E., et al. Genetic studies of body mass index yield new insights for obesity biology. Nature 518 (2015), 197–206.
39. 39 Frayling, T.M., et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 316 (2007), 889–894.
40. 40 Morris, A.P., et al. Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat. Genet. 44 (2012), 981–990.
41. 41 Scott, R.A., et al. Large-scale association analyses identify new loci influencing glycemic traits and provide insight into the underlying biological pathways. Nat. Genet. 44 (2012), 991–1005.
42. 42 Lotta, L.A., et al. Integrative genomic analysis implicates limited peripheral adipose storage capacity in the pathogenesis of human insulin resistance. Nat. Genet., 2016, 10.1038/ng.3714 Published online November 14, 2016.
43. 43 Frayling, T.M., et al. A genetic link between type 2 diabetes and prostate cancer. Diabetologia 51 (2008), 1757–1760.
44. 44 van de Bunt, M., An alternative effector gene at the type 2 diabetes-associated TCF7L2 locus?. Diabetologia 59 (2016), 2292–2294.
45. 45 Eizirik, D.L., et al. The human pancreatic islet transcriptome: expression of candidate genes for type 1 diabetes and the impact of pro-inflammatory cytokines. PLoS Genet., 8, 2012, e1002552.
46. 46 Welter, D., et al. The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res. 42 (2014), D1001–D1006.
47. 47 Farh, K.K., et al. Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature 518 (2015), 337–343.
48. 48 Group, D.P., Incidence and trends of childhood type 1 diabetes worldwide 1990–1999. Diabet. Med. 23 (2006), 857–866.
49. 49 Onkamo, P., et al. Worldwide increase in incidence of type I diabetes—the analysis of the data on published incidence trends. Diabetologia 42 (1999), 1395–1403.
50. 50 Patterson, C.C., et al. Trends in childhood type 1 diabetes incidence in Europe during 1989-2008: evidence of non-uniformity over time in rates of increase. Diabetologia 55 (2012), 2142–2147.
51. 51 Patterson, C.C., et al. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet 373 (2009), 2027–2033.
52. 52 Dabelea, D., et al. Prevalence of type 1 and type 2 diabetes among children and adolescents from 2001 to 2009. JAMA 311 (2014), 1778–1786.
53. 53 Harjutsalo, V., et al. Incidence of type 1 diabetes in Finland. JAMA 310 (2013), 427–428.
54. 54 Harjutsalo, V., et al. Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet 371 (2008), 1777–1782.
55. 55 Niemi, M., Winell, K., Diabetes in Finland: Prevalence and Variation in Quality of Care. 2006, Finnish Diabetes Association.
56. 56 Eder, W., et al. The asthma epidemic. N. Engl. J. Med. 355 (2006), 2226–2235.
57. 57 Cosnes, J., et al. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology 140 (2011), 1785–1794.
58. 58 Virta, L.J., et al. Inflammatory bowel disease incidence is on the continuous rise among all paediatric patients except for the very young: a nationwide registry-based study on 28-year follow-up. J. Crohns Colitis., 2016, 10.1093/ecco-jcc/jjw148 Published online August 23, 2016.
59. 59 Rautiainen, H., et al. Prevalence and incidence of primary biliary cirrhosis are increasing in Finland. Scand. J. Gastroenterol. 42 (2007), 1347–1353.
60. 60 Okada, H., et al. The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 160 (2010), 1–9.
61. 61 Versini, M., et al. Unraveling the hygiene hypothesis of Helminthes and autoimmunity: origins, pathophysiology, and clinical applications. BMC Med., 13, 2015, 81.
62. 62 Kondrashova, A., et al. The ‘hygiene hypothesis’ and the sharp gradient in the incidence of autoimmune and allergic diseases between Russian Karelia and Finland. APMIS 121 (2013), 478–493.
63. 63 Haahtela, T., et al. Hunt for the origin of allergy—comparing the Finnish and Russian Karelia. Clin. Exp. Allergy 45 (2015), 891–901.
64. 64 Pinhas-Hamiel, O., Zeitler, P., Who is the wise man? The one who foresees consequences: childhood obesity, new associated comorbidity and prevention. Prev. Med. 31 (2000), 702–705.
65. 65 Pozzilli, P., et al. Obesity, autoimmunity, and double diabetes in youth. Diabetes Care 34:Suppl. 2 (2011), S166–S170.
66. 66 Betts, P., et al. Increasing body weight predicts the earlier onset of insulin-dependant diabetes in childhood: testing the ‘accelerator hypothesis’ (2). Diabet. Med. 22 (2005), 144–151.
67. 67 Hamman, R.F., et al. The SEARCH for Diabetes in Youth study: rationale, findings, and future directions. Diabetes Care 37 (2014), 3336–3344.
68. 68 Berhan, Y., et al. Thirty years of prospective nationwide incidence of childhood type 1 diabetes: the accelerating increase by time tends to level off in Sweden. Diabetes 60 (2011), 577–581.
69. 69 Bergstrom, E., Blomquist, H.K., Is the prevalence of overweight and obesity declining among 4-year-old Swedish children?. Acta Paediatr. 98 (2009), 1956–1958.
70. 70 Hussen, H.I., et al. Maternal overweight and obesity are associated with increased risk of type 1 diabetes in offspring of parents without diabetes regardless of ethnicity. Diabetologia 58 (2015), 1464–1473.
71. 71 Selmi, C., et al. The X chromosome and the sex ratio of autoimmunity. Autoimmun. Rev. 11 (2012), A531–A537.
72. 72 Soltesz, G., et al. Worldwide childhood type 1 diabetes incidence—what can we learn from epidemiology?. Pediatr. Diabetes 8:Suppl. 6 (2007), 6–14.
73. 73 Gale, E.A., Gillespie, K.M., Diabetes and gender. Diabetologia 44 (2001), 3–15.
74. 74 Wandell, P.E., Carlsson, A.C., Time trends and gender differences in incidence and prevalence of type 1 diabetes in Sweden. Curr. Diabetes Rev. 9 (2013), 342–349.
75. 75 Wandell, P.E., Carlsson, A.C., Gender differences and time trends in incidence and prevalence of type 2 diabetes in Sweden—a model explaining the diabetes epidemic worldwide today?. Diabetes Res. Clin. Pract. 106 (2014), e90–e92.
76. 76 Donahue, R.P., et al. Insulin response in a triethnic population: effects of sex, ethnic origin, and body fat. Miami Community Health Study. Diabetes Care 20 (1997), 1670–1676.
77. 77 Amiel, S.A., et al. Impaired insulin action in puberty. A contributing factor to poor glycemic control in adolescents with diabetes. N. Engl. J. Med. 315 (1986), 215–219.
78. 78 Schwenk, R.W., et al. GLP-1–oestrogen attenuates hyperphagia and protects from beta cell failure in diabetes-prone New Zealand obese (NZO) mice. Diabetologia 58 (2015), 604–614.
79. 79 Wicker, L.S., et al. Type 1 diabetes genes and pathways shared by humans and NOD mice. J. Autoimmun. 25:Suppl (2005), 29–33.
80. 80 Lindahl, M., et al. MANF is indispensable for the proliferation and survival of pancreatic beta cells. Cell Rep. 7 (2014), 366–375.
81. 81 Senee, V., et al. Mutations in GLIS3 are responsible for a rare syndrome with neonatal diabetes mellitus and congenital hypothyroidism. Nat. Genet. 38 (2006), 682–687.
82. 82 Hakonarson, H., et al. A genome-wide association study identifies KIAA0350 as a type 1 diabetes gene. Nature 448 (2007), 591–594.
83. 83 Soleimanpour, S.A., The diabetes susceptibility gene Clec16a regulates mitophagy. Cell 157 (2014), 1577–1590.
84. 84 Davison, L.J., et al. Long-range DNA looping and gene expression analyses identify DEXI as an autoimmune disease candidate gene. Hum. Mol. Genet. 21 (2012), 322–333.
85. 85 Onengut-Gumuscu, S., Fine mapping of type 1 diabetes susceptibility loci and evidence for colocalization of causal variants with lymphoid gene enhancers. Nat. Genet. 47 (2015), 381–386.
86. 86 Santin, I., et al. Pancreatic beta cell survival and signaling pathways: effects of type 1 diabetes-associated genetic variants. Methods Mol. Biol. 1433 (2016), 21–54.
87. 87 Marroqui, L., et al. BACH2, a candidate risk gene for type 1 diabetes, regulates apoptosis in pancreatic beta-cells via JNK1 modulation and crosstalk with the candidate gene PTPN2. Diabetes 63 (2014), 2516–2527.
88. 88 Santin, I., et al. PTPN2, a candidate gene for type 1 diabetes, modulates pancreatic beta-cell apoptosis via regulation of the BH3-only protein Bim. Diabetes 60 (2011), 3279–3288.
89. 89 Marroqui, L., et al. TYK2, a candidate gene for type 1 diabetes, modulates apoptosis and the innate immune response in human pancreatic beta-cells. Diabetes 64 (2015), 3808–3817.
90. 90 Laybutt, D.R., et al. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50 (2007), 752–763.
91. 91 Lupi, R., et al. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 51 (2002), 1437–1442.
92. 92 El-Assaad, W., et al. Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death. Endocrinology 144 (2003), 4154–4163.
93. 93 Cunha, D.A., et al. Thrombospondin 1 protects pancreatic beta-cells from lipotoxicity via the PERK–NRF2 pathway. Cell Death Differ. 23 (2016), 1995–2006.
94. 94 Hall, E., et al. Effects of palmitate on genome-wide mRNA expression and DNA methylation patterns in human pancreatic islets. BMC Med., 12, 2014, 103.
95. 95 Cnop, M., et al. RNA sequencing identifies dysregulation of the human pancreatic islet transcriptome by the saturated fatty acid palmitate. Diabetes 63 (2014), 1978–1993.
96. 96 Planas, R., et al. Global gene expression changes in type 1 diabetes: insights into autoimmune response in the target organ and in the periphery. Immunol. Lett. 133 (2010), 55–61.
97. 97 Engin, F., et al. Restoration of the unfolded protein response in pancreatic beta cells protects mice against type 1 diabetes. Sci. Transl. Med., 5, 2013, 211ra156.
98. 98 Endesfelder, D., et al. Gut immunity and type 1 diabetes: a melange of microbes, diet, and host interactions?. Curr. Diabetes Rep., 16, 2016, 60.
99. 99 Vetere, A., et al. Targeting the pancreatic beta-cell to treat diabetes. Nat. Rev. Drug Discov. 13 (2014), 278–289.
100. 100 Fisher, M.M., et al. Elevations in circulating methylated and unmethylated preproinsulin DNA in new-onset type 1 diabetes. Diabetes 64 (2015), 3867–3872.
101. 101 Cole, T.J., et al. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320 (2000), 1240–1243.
102. 102 School of Health Sciences, Adolescent Health and Lifestyle Survey. 2011, University of Tampere.