Islet β cell mass in diabetes and how it relates to function, birth, and death

Annals of the New York Academy of Sciences

Volumn 1281, Issue 1, 2013, Pages 92-105

  Weir, Gordon C ^a   Bonner Weir, Susan ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Beta cell; Diabetes; Insulin secretion; Islets; Neogenesis

Indexed keywords

AMYLOID; GLUCOSE; PROINSULIN;

ARTICLE; CELL DEATH; CELL DEDIFFERENTIATION; CELL FUNCTION; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; GLUCOSE BLOOD LEVEL; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INSULIN RESISTANCE; LIPOTOXICITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL;

EID: 84875684003     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12031     Document Type: Article

References (124)

1. Maclean, N. & R. F. Ogilvie. 1955. Quantitative estimation of the pancreatic islet tissue in diabetic subjects. Diabetes 4: 367-376.
2. Butler, A. E. et al. 2003. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102-110.
3. Yoon, K. H. et al. 2003. Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in Korea. J. Clin. Endocrinol. Metab. 88: 2300-2308.
4. Rahier, J. et al. 2008. Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes. Metab. 10(Suppl 4): 32-42.
5. Kloppel, G. et al. 1985. Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv. Synth. Pathol. Res. 4: 110-125.
6. Bruning, J. C. et al. 1999. Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 88: 561-572.
7. Herold, K. C. et al. 2005. A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes. Diabetes 54: 1763-1769.
8. Group, D. S. 1998. Effect of intensive therapy on residual beta-cell function in patients with type 1 diabetes in the diabetes control and complications trial. A randomized, controlled trial. The Diabetes Control and Complications Trial Research Group. Ann. Intern. Med. 128: 517-523.
9. Keenan, H. A. et al. 2010. Residual insulin production and pancreatic ss-cell turnover after 50 years of diabetes: Joslin Medalist Study. Diabetes 59: 2846-2853.
10. Goland, R. et al. 2009. 11C-dihydrotetrabenazine PET of the pancreas in subjects with long-standing type 1 diabetes and in healthy controls. J. Nucl. Med. 50: 382-389.
11. Reiner, T. et al. 2011. Accurate measurement of pancreatic islet beta-cell mass using a second-generation fluorescent exendin-4 analog. Proc. Natl. Acad. Sci. USA 108: 12815-12820.
12. Gaglia, J. L. et al. 2011. Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients. J. Clin. Invest. 121: 442-445.
13. Di Gialleonardo, V. et al. 2012. Imaging of beta-cell mass and insulitis in insulin-dependent (type 1) diabetes mellitus. Endocr. Rev. 33: 892-919.
14. De Vos, A. et al. 1995. Human and rat beta cells differ in glucose transporter but not in glucokinase gene expression. J. Clin. Invest. 96: 2489-2495.
15. van de Bunt, M. & A. L. Gloyn. 2012. A tale of two glucose transporters: how GLUT2 re-emerged as a contender for glucose transport into the human beta cell. Diabetologia 55: 2312-2315.
16. Matschinsky, F. M., B. Glaser & M. A. Magnuson. 1998. Pancreatic beta-cell glucokinase: closing the gap between theoretical concepts and experimental realities. Diabetes 47: 307-315.
17. Teff, K. L., R. D. Mattes & K. Engelman. 1991. Cephalic phase insulin release in normal weight males: verification and reliability. Am. J. Physiol. 261: E430-436.
18. Henquin, J. C. 2011. The dual control of insulin secretion by glucose involves triggering and amplifying pathways in beta-cells. Diabetes Res. Clin. Pract. 93(Suppl 1): S27-31.
19. Taborsky, G. J., Jr. & T. O. Mundinger. 2012. Minireview: the role of the autonomic nervous system in mediating the glucagon response to hypoglycemia. Endocrinology 153: 1055-1062.
20. Baggio, L. L. & D. J. Drucker. 2007. Biology of incretins: GLP-1 and GIP. Gastroenterology 132: 2131-2157.
21. Gaisano, H. Y., P. E. Macdonald & M. Vranic. 2012. Glucagon secretion and signaling in the development of diabetes. Front Physiol. 3: 349.
22. Cooperberg, B. A. & P. E. Cryer. 2010. Insulin reciprocally regulates glucagon secretion in humans. Diabetes 59: 2936-2940.
23. Goodner, C. J., B. C. Walike & D. J. Koerker. 1977. Insulin, glucagon, and glucose exhibit synchronous, sustained oscillations in fasting monkeys. Science 195: 177-179.
24. Song, S. H. et al. 2000. Direct measurement of pulsatile insulin secretion from the portal vein in human subjects. J. Clin. Endocrinol. Metab. 85: 4491-4499.
25. Stagner, J., E. Samols & G. C. Weir. 1980. Sustained oscillations of insulin, glucagon and somatostatin from the isolated canine pancreas during exposure to a constant glucose concentration. J. Clin. Invest. 65: 939-942.
26. Lang, D. A. et al. 1981. Brief, irregular oscillations of basal plasma insulin and glucose concentrations in diabetic man. Diabetes 30: 439.
27. Chen, L. et al. 1992. Factors regulating islet regeneration in the post-insulinoma NEDH rat. Adv. Exp. Med. Biol. 321: 71-80; discussion 81-74.
28. Bonner-Weir, S. et al. 1989. Compensatory growth of pancreatic beta-cells in adult rats after short-term glucose infusion. Diabetes 38: 49-53.
29. Jonas, J. C. et al. 1999. Chronic hyperglycemia triggers loss of pancreatic beta cell differentiation in an animal model of diabetes. J. Biol. Chem. 274: 14112-14121.
30. Swenne, I. 1982. The role of glucose in the in vitro regulation of cell cycle kinetics and proliferation of fetal pancreatic B-cells. Diabetes 31: 754-760.
31. Alonso, L. C. et al. 2007. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 56: 1792-1801.
32. Levitt, H. E. et al. 2011. Glucose stimulates human beta cell replication in vivo in islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia 54: 572-582.
33. Terauchi, Y. et al. 2007. Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance. J. Clin. Invest. 117: 246-257.
34. Okada, T. et al. 2007. Insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. Proc. Natl. Acad. Sci. USA 104: 8977-8982.
35. Chen, C. et al. 1994. Mechanism of compensatory hyperinsulinemia innormoglycemic insulin-resistant spontaneously hypertensive rats. J. Clin. Invest. 94: 399-404.
36. Brunzell, J. D. et al. 1976. Relationships between fasting plasma glucose levels and insulin secretion during intravenous glucose tolerance tests. J. Clin. Endocrinol. Metab. 42: 222-229.
37. Cerasi, E. & R. Luft. 1967. The plasma insulin response to glucose infusion in health subjects and in diabetes mellitus. Acta Endocrinol. 55: 278-304.
38. Ward, W. K. et al. 1984. Diminished B cell secretory capacity in patients with noninsulin-dependent diabetes mellitus. J. Clin. Invest. 74: 1318-1328.
39. Polyzogopoulou, E. V. et al. 2003. Restoration of euglycemia and normal acute insulin response to glucose in obese subjects with type 2 diabetes following bariatric surgery. Diabetes 52: 1098-1103.
40. Vague, P. & J. P. Moulin. 1982. The defective glucose sensitivity of the B-cell in noninsulin dependent diabetes: improvement after twenty hours of normoglycemia. Metabolism 31: 139-142.
41. Cnop, M. 2008. Fatty acids and glucolipotoxicity in the pathogenesis of Type 2 diabetes. Biochem. Soc. Trans. 36: 348-352.
42. Delghingaro-Augusto, V. et al. 2009. Islet beta cell failure in the 60% pancreatectomised obese hyperlipidaemic Zucker fatty rat: severe dysfunction with altered glycerolipid metabolism without steatosis or a falling beta cell mass. Diabetologia 52: 1122-1132.
43. Poitout, V. 2008. Glucolipotoxicity of the pancreatic beta-cell: myth or reality? Biochem. Soc. Trans. 36: 901-904.
44. Leahy, J. L. et al. 1986. Chronic hyperglycemia is associated with impaired glucose influence on insulin secretion. A study in normal rats using chronic in vivo glucose infusions. J. Clin. Invest. 77: 908-915.
45. Laychock, S. G. 1995. Impaired cyclic AMP response to stimuli in glucose-desensitized rat pancreatic islets. Mol. Cell. Endocrinol. 113: 19-28.
46. Anello, M. et al. 1996. Fast reversibility of glucose-induced desensitization in rat pancreatic islets. Evidence for an involvement of ionic fluxes. Diabetes 45: 502-506.
47. Moffitt, J. H. et al. 2005. Adverse physicochemical properties of tripalmitin in beta cells lead to morphological changes and lipotoxicity in vitro. Diabetologia 48: 1819-1829.
48. Maedler, K. et al. 2002. Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. J. Clin. Invest. 110: 851-860.
49. Fontes, G. et al. 2010. Glucolipotoxicity age-dependently impairs beta cell function in rats despite a marked increase in beta cell mass. Diabetologia. 53: 2369-2379.
50. Laybutt, D. R. et al. 2002. Genetic regulation of metabolic pathways in beta-cells disrupted by hyperglycemia. J. Biol. Chem. 277: 10912-10921.
51. Kjorholt, C. et al. 2005. Chronic hyperglycemia, independent of plasma lipid levels, is sufficient for the loss of beta-cell differentiation and secretory function in the db/db mouse model of diabetes. Diabetes 54: 2755-2763.
52. Lee, Y. et al. 1994. B-Cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus of obese rats: impairment in adipocyte-B-cell relationships. Proc. Natl. Acad. Sci. USA 91: 10878-10882.
53. Wang, J. et al. 1997. Regulation of insulin preRNA splicing by glucose. Proc. Natl. Acad. Sci. USA. 94: 4360-4365.
54. Bonner-Weir, S. et al. 1981. Limited B cell regeneration in a B cell deficient rat model: studies with dexamethasone. Metabolism 30: 914-918.
55. Leibowitz, G. et al. 2002. Glucose-regulated proinsulin gene expression is required for adequate insulin production during chronic glucose exposure. Endocrinology 143: 3214-3220.
56. Alarcon, C. et al. 1995. Increased secretory demand rather than a defect in the proinsulin conversion mechanism causes hyperproinsulinemia in a glucose-infusion rat model of non-insulin-dependent diabetes mellitus. J. Clin. Invest. 95: 1032-1039.
57. Weir, G. C. & S. Bonner-Weir. 2004. Five stages of evolving beta-cell dysfunction during progression to diabetes. Diabetes 53(Suppl 3): S16-21.
58. Knowler, W. C. et al. 2002. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N. Engl. J. Med. 346: 393-403.
59. Tabak, A. G. et al. 2009. Trajectories of glycaemia, insulin sensitivity, and insulin secretion before diagnosis of type 2 diabetes: an analysis from the Whitehall II study. Lancet 373: 2215-2221.
60. Harrison, L. B. et al. 2012. Beta-cell function preservation after 3.5 years of intensive diabetes therapy. Diabetes Care 35: 1406-1412.
61. Xu, P. et al. 2012. Prognostic accuracy of immunologic and metabolic markers for type 1 diabetes in a high-risk population: receiver operating characteristic analysis. Diabetes Care 35: 1975-1980.
62. Couri, C. E. et al. 2009. C-peptide levels and insulin independence following autologous nonmyeloablative hematopoietic stem cell transplantation in newly diagnosed type 1 diabetes mellitus. JAMA 301: 1573-1579.
63. Bonner-Weir, S. et al. 2010. Beta-cell growth and regeneration: replication is only part of the story. Diabetes 59: 2340-2348.
64. Rovira, M. et al. 2010. Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas. Proc. Natl. Acad. Sci. USA 107: 75-80.
65. Dor, Y. et al. 2004. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429: 41-46.
66. Nir, T., D. A. Melton & Y. Dor. 2007. Recovery from diabetes in mice by beta cell regeneration. J. Clin. Invest. 117: 2553-2561.
67. Inada, A. et al. 2008. Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc. Natl. Acad. Sci. USA 105: 19915-19919.
68. Chintinne, M. et al. 2010. Contribution of postnatally formed small beta cell aggregates to functional beta cell mass in adult rat pancreas. Diabetologia 53: 2380-2388.
69. Li, W. C. et al. 2010. Activation of pancreatic-duct-derived progenitor cells during pancreas regeneration in adult rats. J. Cell. Sci. 123: 2792-2802.
70. Peshavaria, M. et al. 2006. Regulation of pancreatic beta-cell regeneration in the normoglycemic 60% partial-pancreatectomy mouse. Diabetes 55: 3289-3298.
71. Gregg, B. E. et al. 2012. Formation of a human beta-cell population within pancreatic islets is set early in life. J. Clin. Endocrinol. Metab. 97: 3197-3206.
72. In't Veld, P. et al. 2010. Beta-cell replication is increased in donor organs from young patients after prolonged life support. Diabetes 59: 1702-1708.
73. Perl, S. et al. 2010. Significant human beta-cell turnover is limited to the first three decades of life as determined by in vivo thymidine analog incorporation and radiocarbon dating. J. Clin. Endocrinol. Metab. 95: E234-E239.
74. Caballero, F. et al. 2013. Birth and death of human β-cells in pancreas from cadaver donors, autopsies, surgical specimens, and islets transplanted into mice. Cell Transplan. In press.
75. Menge, B. A. et al. 2008. Partial pancreatectomy in adult humans does not provoke beta-cell regeneration. Diabetes 57: 142-149.
76. Patti, M. E. et al. 2005. Severe hypoglycaemia post-gastric bypass requiring partial pancreatectomy: evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia 48: 2236-2240.
77. Jorgensen, N. B. et al. 2012. Acute and long-term effects of Roux-en-Y gastric bypass on glucose metabolism in subjects with Type 2 diabetes and normal glucose tolerance. Am. J. Physiol. Endocrinol. Metab. 303: E122-131.
78. Cnop, M. et al. 2010. The long lifespan and low turnover of human islet beta cells estimated by mathematical modelling of lipofuscin accumulation. Diabetologia 53: 321-330.
79. Robertson, R. P. 2010. Antioxidant drugs for treating beta-cell oxidative stress in type 2 diabetes: glucose-centric versus insulin-centric therapy. Discov. Med. 9: 132-137.
80. Mailloux, R. J. et al. 2012. Glutathionylation state of uncoupling protein-2 and the control of glucose-stimulated insulin secretion. J. Biol. Chem. 287: 39673-39685.
81. Kaneto, H. et al. 1999. Beneficial effects of antioxidants in diabetes-possible protection of pancreatic beta-cells against glucose toxicity. Diabetes 48: 2398-2406.
82. Tanaka, Y. et al. 1999. Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc. Natl. Acad. Sci. USA 96: 10857-10862.
83. Opie, E. L. 1900. The relation of diabetes mellitus to lesions of the pancreas: hyaline degeneration of the islands of Langerhans. J. Exp. Med. 5: 527-540.
84. Cooper, G. J. S. et al. 1987. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. USA 84: 8628-8632.
85. Westermark, P. & E. Wilander. 1978. The influence of amyloid deposits on the islet volume in maturity onset diabetes mellitus. Diabetologia 15: 417-421.
86. Hull, R. L. et al. 2004. Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes. J. Clin. Endocrinol. Metab. 89: 3629-3643.
87. Verchere, C. B. et al. 1996. Islet amyloid formation associated with hyperglycemia in transgenic mice with pancreatic beta cell expression of human islet amyloid polypeptide. Proc. Natl. Acad. Sci. USA 93: 3492-3496.
88. Costes, S. et al. 2011. beta-cell dysfunctional ERAD/ ubiquitin/proteasome system in type 2 diabetes mediated by islet amyloid polypeptide-induced UCH-L1 deficiency. Diabetes 60: 227-238.
89. Gurlo, T. et al. 2010. Evidence for proteotoxicity in beta cells in type 2 diabetes: toxic islet amyloid polypeptide oligomers form intracellularly in the secretory pathway. Am. J. Pathol. 176: 861-869.
90. Lorenzo, A. et al. 1994. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368: 756-760.
91. Kaufman, R. J. 2011. Beta-cell failure, stress, and type 2 diabetes. N. Engl. J. Med. 365: 1931-1933.
92. Oslowski, C. M. et al. 2012. Thioredoxin-interacting protein mediates ER stress-induced beta cell death through initiation of the inflammasome. Cell Metab. 16: 265-273.
93. Lerner, A. G. et al. 2012. IRE1alpha induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab. 16: 250-264.
94. Kennedy, J. et al. 2010. Protective unfolded protein response in human pancreatic beta cells transplanted into mice. PLoS ONE 5: e11211.
95. Marselli, L. et al. 2010. Gene expression profiles of Beta-cell enriched tissue obtained by laser capture microdissection from subjects with type 2 diabetes. PLoS ONE 5: e11499.
96. Huang, C. J. et al. 2007. High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress mediated beta-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 56: 2016-2027.
97. Laybutt, D. R. et al. 2003. Critical reduction in beta-cell mass results in two distinct outcomes over time. Adaptation with impaired glucose tolerance or decompensated diabetes. J. Biol. Chem. 278: 2997-3005.
98. Laybutt, D. R. et al. 2002. Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to beta-cell survival during chronic hyperglycemia. Diabetes 51: 413-423.
99. Kondo, T. et al. 2009. p38 MAPK is a major regulator of MafA protein stability under oxidative stress. Mol. Endocrinol. 23: 1281-1290.
100. Talchai, C. et al. 2012. Pancreatic beta Cell dedifferentiation as a mechanism of diabetic beta cell failure. Cell 150: 1223-1234.
101. Henquin, J. C. & J. Rahier. 2011. Pancreatic alpha cell mass in European subjects with type 2 diabetes. Diabetologia 54: 1720-1725.
102. Olsson, R. & P. O. Carlsson. 2011. A low-oxygenated subpopulation of pancreatic islets constitutes a functional reserve of endocrine cells. Diabetes 60: 2068-2075.
103. Harlan, D. M. et al. 2009. Current advances and travails in islet transplantation. Diabetes 58: 2175-2184.
104. Nath, D. S. et al. 2005. Outcomes of pancreas transplants for patients with type 2 diabetes mellitus. Clin. Transplant. 19: 792-797.
105. Schulz, T. C. et al. 2012. A scalable system for production of functional pancreatic progenitors from human embryonic stem cells. PLoS ONE 7: e37004.
106. Alipio, Z. et al. 2010. Reversal of hyperglycemia in diabetic mouse models using induced-pluripotent stem (iPS)-derived pancreatic beta-like cells. Proc. Natl. Acad. Sci. USA 107: 13426-13431.
107. Rezania, A. et al. 2012. Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice. Diabetes 61: 2016-2029.
108. Ouziel-Yahalom, L. et al. 2006. Expansion and redifferentiation of adult human pancreatic islet cells. Biochem. Biophys. Res. Commun. 341: 291-298.
109. Lysy, P. A. et al. 2012. Functional in vivo β-cell differentiation of expanded human pancreatic duct cells. Diabetes 61(Suppl 1): A73.
110. Annes, J. P. et al. 2012. Adenosine kinase inhibition selectively promotes rodent and porcine islet beta-cell replication. Proc. Natl. Acad. Sci. USA 109: 3915-3920.
111. Andersson, O. et al. 2012. Adenosine signaling promotes regeneration of pancreatic beta cells in vivo. Cell Metab. 15: 885-894.
112. Rao, P. et al. 2005. Gene transfer of constitutively active Akt markedly improves human islet transplant outcomes in diabetic severe combined immunodeficient mice. Diabetes 54: 1664-1675.
113. Guthalu Kondegowda, N. et al. 2010. Parathyroid hormone-related protein enhances human ss-cell proliferation and function with associated induction of cyclin-dependent kinase 2 and cyclin E expression. Diabetes 59: 3131-3138.
114. Fiaschi-Taesch, N. M. et al. 2010. Induction of human beta-cell proliferation and engraftment using a single G1/S regulatory molecule, cdk6. Diabetes 59: 1926-1936.
115. Davis, D. B. et al. 2010. FoxM1 is up-regulated by obesity and stimulates beta-cell proliferation. Mol. Endocrinol. 24: 1822-1834.
116. Schisler, J. C. et al. 2008. Stimulation of human and rat islet beta-cell proliferation with retention of function by the homeodomain transcription factor Nkx6.1. Mol. Cell. Biol. 28: 3465-3476.
117. Ravassard, P. et al. 2011. A genetically engineered human pancreatic beta cell line exhibiting glucose-inducible insulin secretion. J. Clin. Invest. 121: 3589-3597.
118. Hering, B. J. et al. 2006. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat. Med. 12: 301-303.
119. Veld, P. I. et al. 2006. Xenotransplantation of purified pre-natal porcine beta cells in mice normalizes diabetes when a short anti-CD4-CD8 antibody treatment is combined with transient insulin injections. Xenotransplantation 13: 415-422.
120. O'Sullivan, E. S. et al. 2011. Islets transplanted in immunoisolation devices: a review of the progress and the challenges that remain. Endocr. Rev. 32: 827-844.
121. Cruise, G. M. et al. 1999. In vitro and in vivo performance of porcine islets encapsulated in interfacially photopolymerized poly(ethylene glycol) diacrylate membranes. Cell Transplant. 8: 293-306.
122. Halban, P. A. et al. 2010. Current status of islet cell replacement and regeneration therapy. J. Clin. Endocrinol. Metab. 95: 1034-1043.
123. Ferber, S. et al. 2000. Pancreatic and duodenal homeobox gene 1 induces expression of insulin genes in liver and ameliorates streptozotocin-induced hyperglycemia. Nat. Med. 6: 505-506.
124. Zhou, Q. et al. 2008. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455: 627-632.