Animal models of type 2 diabetes with reduced pancreatic β-cell mass

International Journal of Biochemistry and Cell Biology

Volumn 38, Issue 5-6, 2006, Pages 873-893

  Masiello, Pellegrino ^a  

^a UNIVERSITY OF PISA   (Italy)

Author keywords

cell apoptosis; cell growth; cell mass; Animal models; Type 2 diabetes

Indexed keywords

CYCLIN D2; CYCLIN DEPENDENT KINASE 4; EXENDIN 4;

APOPTOSIS; CELL DEATH; CELL GROWTH; CELL SURVIVAL; ENDOPLASMIC RETICULUM; HUMAN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PSAMMOMYS OBESUS; RAT STRAIN; REVIEW; TRANSGENIC MOUSE;

ANIMALS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIN-DEPENDENT KINASE 4; CYCLINS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; EIF-2 KINASE; FETAL GROWTH RETARDATION; HOMEODOMAIN PROTEINS; INSULIN-SECRETING CELLS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, TRANSGENIC; PEPTIDES; PHOSPHOPROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTOR, INSULIN; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; TRANS-ACTIVATORS; VENOMS;

ANIMALIA; MUS MUSCULUS; PSAMMOMYS OBESUS;

EID: 33644833635     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2005.09.007     Document Type: Review

References (202)

1. J.H. Adler, R. Kalman, G. Lazarovici, H. Bar-On, and E. Ziv Achieving predictable model of type 2 diabetes in the sand rat E. Shafrir Frontiers in diabetic research: Lessons from animal diabetes III 1991 Smith-Gordon London 212 214
2. U. Ahlgren, J. Jonsson, L. Jonsson, K. Simu, and H. Edlund Beta-cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes Genes Dev. 12 1998 1763 1768
3. E. Araki, S. Oyadomari, and M. Mori Impact of endoplasmic reticulum stress pathway on pancreatic β-cells and diabetes mellitus Exp. Biol. Med. 228 2003 1213 1217
4. V.C. Arantes, V.P.A. Teixeira, M.A.B. Reis, M.Q. Latorraca, A.R. Leite, and E.M. Carneiro Expression of PDX-1 is reduced in pancreatic islets from pups of rat dams fed a low protein diet during gestation and lactation J. Nutr. 132 2002 3030 3035
5. J.A. Armitage, I.Y. Khan, P.D. Taylor, P.W. Nathanielsz, and L. Poston Developmental programming of the metabolic syndrome by maternal nutritional imbalance: How strong is the evidence from experimental models in mammals? J. Physiol. 561 2004 355 377
6. D.J. Barker, C.N. Hales, C.H. Fall, C. Osmond, K. Phipps, and P.M. Clark Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidemia (syndrome X): Relation to reduced fetal growth Diabetologia 36 1993 62 67
7. E.B. Becker, and A. Bonni Cell cycle regulation of neuronal apoptosis in development and disease Prog. Neurobiol. 72 2004 1 25
8. C. Bernard-Kargar, and A. Ktorza Endocrine pancreas plasticity under physiological and pathological conditions Diabetes 50 Suppl. 1 2001 S30 S35
9. E. Bertin, M.N. Gangnerau, G. Bellon, D. Bailbe, A. Arbelot De Vacquer, and B. Portha Development of beta-cell mass in fetuses of rats deprived of protein and/or energy in last trimester of pregnancy Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 2002 R623 R630
10. S. Bonner-Weir Islet growth and development in the adult J. Mol. Endocrinol. 24 2000 297 302
11. S. Bonner-Weir Life and death of the pancreatic beta cells Trends Endocrinol. Metab. 11 2000 375 378
12. S. Bonner-Weir Perspective: Postnatal pancreatic beta cell growth Endocrinology 141 2000 1926 1929
13. S. Bonner-Weir β-Cell turnover. Its assessment and implications Diabetes 50 2001 S20 S24
14. S. Bonner-Weir, L.A. Baxter, G.T. Schuppin, and F.E. Smith A second pathway for regeneration of adult exocrine and endocrine pancreas. A possible recapitulation of embryonic development Diabetes 42 1993 1715 1720
15. S. Bonner-Weir, D.F. Trent, C.J. Zmachinski, E.T. Clore, and G.C. Weir Limited β-cell regeneration in a β-cell deficient model: Studies with dexamethasone Metabolism 30 1981 914 918
16. S. Boujendar, B. Reusens, S. Merezak, M.-T. Ahn, A. Arany, and D. Hill Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets Diabetologia 45 2002 856 866
17. D.P. Brazil, and B.A. Hemmings Ten years of protein kinase B signalling: A hard Akt to follow Trends Biochem. Sci. 26 2001 657 664
18. I. Briaud, C.L. Kelpe, L.M. Johnson, P.O.T. Tran, and V. Poitout Differential effects of hyperlipidemia on insulin secretion in islet of Langerhans from hyperglycemic versus normoglycemic rats Diabetes 51 2002 662 668
19. C. Broca, R. Gross, P. Petit, Y. Sauvaire, M. Manteghetti, and M. Tournier 4-Hydroxyisoleucine: Experimental evidence of its insulinotropic and antidiabetic properties Am. J. Physiol. 277 1999 E617 E623
20. J.P. Burke, K. Williams, S.P. Gaskill, H.P. Hazuda, S.M. Haffner, and M.P. Stern Rapid rise in the incidence of type 2 diabetes from 1987 to 1996: Results from the San Antonio Heart Study Arch. Int. Med. 159 1999 1450 1456
21. A.E. Butler, J. Jang, T. Gurlo, M.D. Carty, W.C. Soeller, and P.C. Butler Diabetes due to a progressive defect in β-cell mass in rats transgenic for human islet amyloid polypeptide (HIP rat). A new model for type 2 diabetes Diabetes 53 2004 1509 1516
22. A.E. Butler, J. Janson, S. Bonner-Weir, R. Ritzel, R.A. Rizza, and P.C. Butler Cell deficit and increased cell apoptosis in humans with type 2 diabetes Diabetes 52 2003 102 110
23. A.E. Butler, J. Janson, W.C. Soeller, and P.C. Butler Increased beta cell apoptosis prevents adaptive increase in beta cell mass in a mouse model of type-2 diabetes; evidence for a role of islet amyloid formation rather than a direct action of amyloid Diabetes 52 2003 2304 2314
24. Center for Disease Control and Prevention Trends in the prevalence and incidence of self reported diabetes mellitus: United States, 1980-1994 MMWR 46 1997 1014 1018
25. T.O. Chan, S.E. Rittenhouse, and P.N. Tsichlis AKT/PKB and other D3 phosphoinositide-regulated kinases: Kinase activation by phosphoinositide- dependent phosphorylation Annu. Rev. Biochem. 68 1999 965 1014
26. H. Cho, J. Mu, J.K. Kim, J.L. Thorvaldsen, Q. Chu, and E.B. Crenshaw III Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta) Science 292 2001 1728 1731
27. M.A. Ciemerych, A.M. Kenney, E. Sicinska, I. Kalaszczynska, R.T. Bronson, and D.H. Rowitch Development of mice expressing a single D-type cyclin Genes Dev. 6 2002 3277 3289
28. A. Clark, C.A. Wells, I.D. Buley, J.K. Cruickshank, R.I. Vanhegan, and D.R. Matthews Islet amyloid, increased A-cells, reduced B-cells and exocrine fibrosis: Quantitative changes in the pancreas in type-2 diabetes Diabetes Res. 9 1988 151 159
29. P. Cohen, and S. Frame The renaissance of GSK3 Nat. Rev. Mol. Cell Biol. 2 2001 769 776
30. S. Dahri, B. Reusens, C. Remacle, and J.J. Hoet Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes Proc. Nutr. Soc. 54 1995 345 356
31. S. Dahri, A. Snoeck, B. Reusens, C. Remacle, and J.J. Hoet Islet function in offspring of mothers on low protein diet during gestation Diabetes 40 1991 115 120
32. D.A. D'Alessio, C.B. Verchere, S.E. Kahn, V. Hoagland, D.G. Baskin, and R.D. Palmiter Pancreatic expression and secretion of human islet amyloid polypeptide in a transgenic mouse Diabetes 43 1994 1457 1461
33. H.C. Dan, M. Sun, S. Kaneko, R.I. Feldman, S.V. Nicosia, and H.G. Wang Akt phosphorylation and stabilization of X-linked inhibitor of apoptosis protein (XIAP) J. Biol. Chem. 279 2004 5405 5412
34. E.J.P. de Koning, N.L. Bodkin, B.C. Hansen, and A. Clark Diabetes-mellitus in Macaca-mulatta monkeys is characterized by islet amyloidosis and reduction in b-cell population Diabetologia 36 1993 378 384
35. M. Delepine, M. Nicolino, T. Barrett, M. Golamaully, G.M. Lathrop, and C. Julier EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome Nat. Genet. 25 2000 406 409
36. L.M. Dickson, and C.J. Rhodes Pancreatic β-cell growth and survival in the onset of type 2 diabetes: A role for protein kinase B in the Akt? Am. J. Physiol. Endocrinol. Metab. 287 2004 E192 E198
37. J.A. Diehl, M. Cheng, M.F. Roussel, and C.J. Sherr Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization Genes Dev. 12 1998 3499 3511
38. M.Y. Donath, and P.A. Halban Decreased beta-cell mass in diabetes: Significance, mechanisms and therapeutic implications Diabetologia 47 2004 581 589
39. M.Y. Donath, D.J. Gross, E. Cerasi, and N. Kaiser Hyperglycemia-induced β-cell apoptosis in pancreatic islets of Psammomys obesus during development of diabetes Diabetes 48 1999 738 744
40. Y. Dor, J. Brown, O.I. Martinez, and D.A. Melton Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation Nature 429 2004 41 46
41. E. Dumonteil, and J. Philippe Insulin gene: Organisation, expression and regulation Diabetes Metab. 22 1996 164 173
42. M.C. Dutrillaux, B. Portha, C. Rozé, and E. Hollande Ultrastructural study of pancreatic β-cell regeneration in newborn rats after destruction by streptozotocin Virch. Arch. B: Cell Pathol. Incl. Mol. Pathol. 39 1982 173 185
43. H. Edlund Transcribing pancreas Diabetes 47 1998 1817 1823
44. H. Edlund Developmental biology of the pancreas Diabetes 50 Suppl. 1 2001 S5 S9
45. H. Edlund Factors controlling pancreatic cell differentiation and function Diabetologia 44 2001 1071 1079
46. W. El-Assaad, J. Buteau, M.L. Peyot, C. Nolan, R. Roduit, and S. Hardy Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death Endocrinology 144 2003 4154 4163
47. S.S. Fajans, G.I. Bell, and K.S. Polonsky Molecular mechanisms and clinical pathophysiology of maturity-onset diabetes of the young N. Engl. J. Med. 345 2001 971 980
48. D.T. Finegood, M.D. McArthur, D. Kojwangt, M.J. Thomas, B.G. Topp, and T. Leonard β-Cell mass dynamics in Zucker diabetic fatty rats: Rosiglitazone prevents the rise in net cell death Diabetes 50 2001 1021 1029
49. D.T. Finegood, L. Scaglia, and S. Bonner-Weir Dynamics of β cell mass in the growing rat pancreas Diabetes 44 1995 249 256
50. N. Fox, J. Schrementi, M. Nishi, S. Ohagi, S.J. Chan, and J.A. Heisserman Human islet amyloid polypeptide transgenic mice as a model of non-insulin-dependent diabetes-mellitus (NIDDM) FEBS Lett. 323 1993 40 44
51. R.S. Garofalo, S.J. Orena, K. Rafidi, A.J. Torchia, J.L. Stock, and A.L. Hildebrandt Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKBβ J. Clin. Invest. 112 2003 197 208
52. B.R. Gedulin, S.E. Nikoulina, P.A. Smith, G. Gedulin, L.L. Nielsen, and A.D. Baron Exenatide (exendin-4) improves insulin sensitivity and β-cell mass in insulin-resistant obese fa/fa Zucker rats independent of glycemia and body weight Endocrinology 146 2005 2069 2076
53. S. Georgia, and A. Bhushan Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass J. Clin. Invest. 114 2004 963 968
54. W. Gepts, and P.M. Lecompte The pancreatic islets in diabetes Am. J. Med. 70 1981 105 115
55. M.H. Giroix, B. Portha, M. Kergoat, D. Bailbe, and L. Picon Glucose insensitivity and aminoacid hypersensitivity of insulin release in rats with non-insulin dependent diabetes: A study with the perfused pancreas Diabetes 32 1983 445 451
56. Y. Goto, K.I. Suzuki, M. Sasaki, T. Ono, and S. Abe GK rat as a model of non-obese, non-insulin dependent diabetes: Selective breeding over 35 generations E. Shafrir A.E. Renold Lessons from animal studies II 1998 Libbey London 301 303
57. V. Grill, and A. Bjorklund Overstimulation and β-cell function Diabetes 50 Suppl. 1 2001 S122 S124
58. C.N. Hales, and D.J. Barker The thrifty phenotype hypothesis Br. Med. Bull. 60 2001 5 20
59. E.H. Hani, D.A. Stoffers, J.C. Chevre, E. Durand, V. Stanojevic, and C. Dina Defective mutations in the insulin promoter factor-1 (IPF-1) gene in late-onset type 2 diabetes mellitus J. Clin. Invest. 104 1999 R41 R48
60. J. Hanke Apoptosis and occurrence of Bcl-2, Bak, Bax, Fas and FasL in the developing and adult rat endocrine pancreas Anat. Embryol. (Berl.) 202 2000 303 312
61. H.P. Harding, and D. Ron Endoplasmic reticulum stress and the development of diabetes Diabetes 51 2002 S455 S461
62. H.P. Harding, H. Zeng, Y. Zhang, R. Jungries, P. Chung, and H. Plesken Diabetes mellitus and exocrine pancreatic dysfunction in perk -/- mice reveals a role for translational control in survival of secretory cells Mol. Cell 7 2001 1153 1163
63. J.S. Harmon, C.E. Gleason, Y. Tanaka, E.A. Oseid, K.K. Hunter-Berger, and R. Paul Robertson In vivo prevention of hyperglycemia also prevents glucotoxic effects on PDX-1 and insulin gene expression Diabetes 48 1999 1995 2000
64. A. Hart, N. Baeza, A. Apelqvist, and H. Edlund Attenuation of FGF-signalling in mouse β-cells leads to diabetes Nature 408 2000 864 868
65. C. Hellerstrom, and I. Swenne Growth patterns of pancreatic islets in animals B.W. Volk M.D. Arquilla The diabetic pancreas 1985 Plenum Press New York 53 59
66. A.M. Hennige, D.J. Burks, U. Ozcan, R.N. Kulkarni, J. Ye, and S. Park Upregulation of insulin receptor substrate-2 in pancreatic beta cells prevents diabetes J. Clin. Invest. 112 2003 1521 1532
67. D.J. Hill, B. Strutt, E. Arany, S. Zaina, S. Coukell, and C.F. Graham Persistent circulating insulin-like growth factor II in neonatal transgenic mice suppresses developmental apoptosis in the pancreatic islets Endocrinology 141 2000 1151 1157
68. M. Hollingdal, C.B. Juhl, S.M. Pincus, J. Sturis, J.D. Veldhuis, and K.S. Polonsky Failure of physiological plasma glucose excursions to entrain high-frequency pulsatile insulin secretion in type 2 diabetes Diabetes 49 2000 1334 1340
69. J.W.M. Höppener, C. Oosterwijk, M.G. Nieuwenhuis, G. Posthuma, J.H.H. Thijssen, and T.M. Vroom Extensive islet amyloid formation is induced by development of type II diabetes mellitus and contributes to its progression: Pathogenesis of diabetes in a mouse model Diabetologia 42 1999 427 434
70. H. Hosokawa, B.E. Corkey, and J.L. Leahy Beta-cell hypersensitivity to glucose following 24-h exposure of rat islets to fatty acids Diabetologia 40 1997 392 397
71. C.F. Howard Jr. Longitudinal studies on the development of diabetes in individual Macaca nigra Diabetologia 29 1986 301 306
72. R.L. Hull, G.T. Westermark, P. Westermark, and S.E. Kahn Islet amyloid: A critical entity in the pathogenesis of type 2 diabetes J. Clin. Endocrinol. Metab. 89 2004 3629 3643
73. Y. Ihara, S. Toyokuni, K. Uchida, H. Odaka, T. Tanaka, and H. Ikeda Hyperglycaemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes Diabetes 48 1999 927 932
74. H. Inoue, Y. Tanizawa, J. Wasson, P. Behn, K. Kalidas, and E. Bernal-Mizrachi A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome) Nat. Genet. 20 1998 143 148
75. T.L. Jetton, J. Lausier, K. LaRock, W.E. Trotman, B. Larmie, A. Habibovic, M. Peshavaria, and J.L. Leahy Mechanisms of compensatory β-cell growth in insulin-resistant rats. Roles of Akt kinase Diabetes 54 2005 2294 2304
76. U.S. Jhala, G. Canettieri, R.A. Screaton, R.N. Kulkarni, S. Krajewski, and J. Reed cAMP promotes pancreatic β-cell survival via CREB-mediated induction of IRS2 Genes Dev. 17 2003 1575 1580
77. J.D. Johnson, N.T. Ahmed, D.S. Luciani, Z. Han, H. Tran, and J. Fujita Increased islet apoptosis in Pdx1+/- mice J. Clin. Invest. 111 2003 1147 1160
78. J.C. Jonas, A. Sharma, W. Hasenkamp, H. Ilkova, G. Patane, and R. Laybutt Chronic hyperglycemia triggers loss of pancreatic beta cell differentiation in an animal model of diabetes J. Biol. Chem. 274 1999 14112 14121
79. J. Jonsson, L. Carlsson, T. Edlund, and H. Edlund Insulin-promoter-factor 1 is required for pancreas development in mice Nature 371 1994 606 609
80. S.E. Kahn The importance of β-cell failure in the development and progression of type 2 diabetes J. Clin. Endocrinol. Metab. 86 2001 4047 4058
81. S.E. Kahn The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of type 2 diabetes Diabetologia 46 2003 3 19
82. B. Kalderon, A. Gutman, E. Levy, E. Shafrir, and J.H. Adler Characterization of stages in development of obesity-diabetes syndrome in the sand rat (Psammomys obesus) Diabetes 35 1986 717 723
83. D.M. Kendall, D.E. Sutherland, J.S. Najarian, F.C. Goetz, and R.P. Robertson Effects of hemipancreatectomy on insulin secretion and glucose tolerance in healthy humans N. Engl. J. Med. 322 1990 898 903
84. T. Kitamura, J. Nakae, Y. Kitamura, Y. Kido, W.H. Biggs III, and C.V. Wright The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth J. Clin. Invest. 110 2002 1839 1847
85. G. Klöppel, M. Löhr, K. Habich, M. Oberholzer, and P.U. Heitz Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited Surv. Synth. Pathol. Res. 4 1985 110 125
86. N. Kubota, K. Tobe, Y. Terauchi, and K. Eto Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory β-cell hyperplasia Diabetes 49 2000 1880 1889
87. R.N. Kulkarni, U.S. Jhala, J.N. Winnay, S. Krajewski, M. Montminy, and C.R. Kahn PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance J. Clin. Invest. 114 2004 828 836
88. J.A. Kushner, J. Ye, M. Schubert, D.J. Burks, M.A. Dow, and C.L. Flint Pdx1 restores beta cell function in Irs2 knockout mice J. Clin. Invest. 109 2002 1193 1201
89. M.O. Larsen, C.F. Gotfredsen, M. Wilken, R.D. Carr, N. Porksen, and B. Rolin Loss of beta-cell mass leads to a reduction of pulse mass with normal periodicity, regularity and entrainment of pulsatile insulin secretion in Göttingen minipigs Diabetologia 46 2003 195 202
90. M.O. Larsen, B. Rolin, C.F. Gotfredsen, R.D. Carr, and J.J. Holst Reduction of beta cell mass: Partial insulin secretory compensation from the residual beta cell population in the nicotinamide-streptozotocin Göttingen minipig after oral glucose in vivo and in the perfused pancreas Diabetologia 47 2004 1873 1878
91. M.O. Larsen, B. Rolin, M. Wilken, R.D. Carr, and C.F. Gotfredsen Measurements of insulin secretory capacity and glucose tolerance to predict pancreatic beta-cell mass in vivo in the nicotinamide-streptozotocin Göttingen minipig, a model of moderate insulin deficiency and diabetes Diabetes 52 2003 118 123
92. M.O. Larsen, M. Wilken, C.F. Gotfredsen, R.D. Carr, O. Svendsen, and B. Rolin Mild streptozotocin diabetes in the Göttingen minipig. A novel model of moderate insulin deficiency and diabetes Am. J. Physiol. Endocrinol. Metab. 282 2002 E1342 E1351
93. D.R. Laybutt, M. Glandt, G. Xu, Y.B. Ahn, N. Trivedi, and S. Bonner-Weir Critical reduction in β-cell mass results in two distinct outcomes over time. Adaptation with impaired glucose tolerance or decompensated diabetes J. Biol. Chem. 278 2003 2997 3005
94. D.R. Laybutt, H. Kaneto, W. Hasenkamp, S. Grey, J.C. Jonas, and D.C. Sgroi Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to beta-cell survival during chronic hyperglycaemia Diabetes 51 2002 413 423
95. J.L. Leahy, S. Bonner-Weir, and G.C. Weir Abnormal glucose regulation of insulin secretion in model of reduced B-cell mass Diabetes 33 1984 667 673
96. J.L. Leahy, S. Bonner-Weir, and G.C. Weir Minimal chronic hyperglycemia is a critical determinant of impaired insulin secretion after an incomplete pancreatectomy J. Clin. Invest. 81 1988 1407 1414
97. J.L. Leahy, L.M. Bumbalo, and C. Chen Beta-cell hypersensitivity for glucose precedes loss of glucose induced insulin secretion in 90% pancreatectomized rats Diabetologia 36 1993 1238 1244
98. G. Leibowitz, S. Ferber, A. Apelqvist, H. Edlund, D.J. Gross, and E. Cerasi IPF1/PDX1 deficiency and β-cell dysfunction in Psammomys obesus, an animal with type 2 diabetes Diabetes 50 2001 1799 1806
99. G. Leibowitz, M. Yuli, M.Y. Donath, R. Nesher, D. Melloul, and E. Cerasi β-Cell glucotoxicity in the Psammomys obesus model of type 2 diabetes Diabetes 50 Suppl. 1 2001 S113 S117
100. Y. Lee, H. Hirose, M. Ohneda, J.H. Johnson, J.D. McGarry, and R.H. Unger Beta-cell lipotoxicity in the pathogenesis of non-insulin dependent diabetes mellitus of obese rats: Impairment in adipocyte-beta-cell relationships Proc. Natl. Acad. Sci. U.S.A. 91 1994 10878 10882
101. Y. Lee, H. Hirose, Y.-T. Zhou, V. Esser, J.D. McGarry, and R.H. Unger Increased lipogenic capacity of the islets of obese rats: A role in the pathogenesis of NIDDM Diabetes 46 1997 408 413
102. Y. Li, X. Cao, L.X. Li, P.L. Brubaker, H. Edlund, and D.J. Drucker β-Cell Pdx1 expression is essential for the glucoregulatory, proliferative, and cytoprotective actions of glucagon-like peptide-1 Diabetes 54 2005 482 491
103. M.K. Lingohr, R. Buettner, and C.J. Rhodes Pancreatic beta-cell growth and survival: A role in obesity-linked type 2 diabetes? Trends Mol. Med. 8 2002 375 384
104. M.K. Lingohr, L.M. Dickson, C.E. Wrede, I. Briaud, J.F. McCuaig, and M.G. Myers Jr. Decreasing IRS-2 expression in pancreatic β-cells (INS-1) promotes apoptosis, which can be compensated for by introduction of IRS-4 expression Mol. Cell. Endocrinol. 209 2003 17 31
105. Y.Q. Liu, P.W. Nevin, and J.L. Leahy β-Cell adaptation in 60% pancreatectomy rats that preserves normoinsulinemia and normoglycemia Am. J. Physiol. Endocrinol. Metab. 279 2000 E68 E73
106. M. Lohr, J. Lubbersmeyer, B. Otremba, R. Klapdor, D. Grossner, and G. Klöppel Increase in B-cells in the pancreatic remnant after partial pancreatectomy in pigs: An immunocytochemical and functional study Virch. Arch. B: Cell Pathol. Incl. Mol. Pathol. 56 1989 277 286
107. Z. Ma, G.T. Westermark, K.H. Johnson, T.D. O'Brien, and P. Westermark Quantitative immunohistochemical analysis of islet amyloid polypeptide (IAPP) in normal, impaired glucose tolerant, and diabetic cats Amyloid 5 1998 255 261
108. W.M. Macfarlane, T.M. Frayling, S. Ellard, J.C. Evans, L.I. Allen, and M.P. Bulman Missense mutations in the insulin promoter factor-1 gene predispose to type 2 diabetes J. Clin. Invest. 104 1999 R33 R39
109. K. Maedler, P. Sergeev, F. Ris, J. Oberholzer, H.I. Joller-Jemelka, and G.A. Spinas Glucose-induced beta cell production of IL-1 beta contributes to glucose toxicity in human pancreatic islets J. Clin. Invest. 110 2002 851 860
110. W.J. Malaisse On the track to the beta-cell Diabetologia 44 2001 393 406
111. W.J. Malaisse Non-invasive imaging of the endocrine pancreas Int. J. Mol. Med. 15 2005 243 246
112. S. Marshak, H. Totary, E. Cerasi, and D. Melloul Purification of the β-cell glucose-sensitive factor that transactivates the insulin gene differentially in normal and transformed islet cells Proc. Natl. Acad. Sci. U.S.A. 93 1996 15057 15062
113. F. Martín, E. Andreu, J.M. Rovira, J.A.G. Pertusa, M. Raurell, and C. Ripoll Mechanisms of glucose hypersensitivity in β-cells from normoglycemic, partially pancreatectomized mice Diabetes 48 1999 1954 1961
114. J. Martin, S.L. Hunt, P. Dubus, R. Sotillo, F. Nehme-Pelluard, and M.A. Magnuson Genetic rescue of Cdk4 null mice restores pancreatic beta-cell proliferation but not homeostatic cell number Oncogene 22 2003 5261 5269
115. P. Masiello, C. Broca, R. Gross, M. Roye, M. Manteghetti, and D. Hillaire-Buys Experimental NIDDM: Development of a new model in adult rats administered streptozotocin and nicotinamide Diabetes 47 1998 224 229
116. D. Mathis, L. Vence, and C. Benoist β-Cell death during progression to diabetes Nature 414 2001 792 798
117. F. Matschinsky, Y. Liang, P. Kesavan, L. Wang, P. Froguel, and G. Velho Glucokinase as β-cell glucose sensor and diabetes gene J. Clin. Invest. 92 1993 2092 2098
118. D.R. Matthews, C.A. Cull, I.M. Stratton, R.R. Holman, and R.C. Turner UKPDS 26: Sulphonylurea failure in non-insulin-dependent diabetic patients over six years. UK Prospective Diabetes Study (UKPDS) Group Diabetes Med. 15 1998 297 303
119. L.D. Mayo, and D.B. Donner A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus Proc. Natl. Acad. Sci. U.S.A. 98 2001 11598 11603
120. D.K. McCulloch, D.J. Koerker, S.E. Kahn, S. Bonner-Weir, and J.P. Palmer Correlations of in vivo β-cell function tests with β-cell mass and pancreatic insulin content in streptozotocin-administered baboons Diabetes 40 1991 673 679
121. M.L. McDaniel, C.A. Marshall, K.L. Pappan, and G. Kwon Metabolic and autocrine regulation of the mammalian target of rapamycin by pancreatic beta-cells Diabetes 51 2002 2877 2885
122. J.D. McGarry, and R.L. Dobbins Fatty acids, lipotoxicity and insulin secretion Diabetologia 42 1999 128 138
123. F. Miralles, and B. Portha Early development of beta-cells is impaired in the GK rat model of type 2 diabetes Diabetes 50 Suppl. 1 2001 S84 S88
124. A.H. Mokdad, B.A. Bowman, E.S. Ford, F. Vinicor, J.S. Marks, and J.P. Koplan The continuing epidemics of obesity and diabetes in the United States JAMA 286 2001 1195 1200
125. A. Moore, S. Bonner-Weir, and R. Weissleder Noninvasive in vivo measurement of beta-cell mass in mouse model of diabetes Diabetes 50 2001 2231 2236
126. J. Movassat, C. Saulnier, and B. Portha Beta-cell mass depletion precedes the onset of hyperglycemia in the GK rat, a genetic model of non-insulindependent diabetes mellitus Diabetes Metab. 21 1995 365 370
127. J. Movassat, C. Saulnier, P. Serradas, and B. Portha Impaired development of pancreatic beta-cell mass is a primary event during the progression to diabetes in the GK rat Diabetologia 40 1997 916 925
128. T. Nakagawa, H. Zhu, N. Morishima, E. Li, J. Xu, and B.A. Yankner Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta Nature 403 2000 98 103
129. R. Nesher, D.J. Gross, M.Y. Donath, E. Cerasi, and N. Kaiser Interaction between genetic and dietary factors determines β-cell function in Psammomys obesus, an animal model of type 2 diabetes Diabetes 48 1999 731 737
130. L.L. Nielsen, A.A. Young, and D.G. Parkes Pharmacology of exenatide (synthetic exendin-4): A potential therapeutic for improved glycemic control of type 2 diabetes Regul. Pept. 117 2004 77 88
131. M. Novelli, M.E. Fabregat, J. Fernandez-Alvarez, R. Gomis, and P. Masiello Metabolic and functional studies on isolated islets in a new rat model of type 2 diabetes Mol. Cell. Endocrinol. 175 2001 57 66
132. T.D. O'Brien, P.C. Butler, P. Westermark, and K.H. Johnson Islet amyloid polypeptide: A review of its biology and potential roles in the pathogenesis of NIDDM Vet. Pathol. 30 1993 317 332
133. M.F. Offield, T.L. Jetton, P.A. Labosky, M. Ray, R.W. Stein, and M.A. Magnuson PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum Development 122 1996 983 995
134. K. Owen, and A.T. Hattersley Maturity-onset diabetes of the young: From clinical description to molecular genetic characterization Best Pract. Res. Clin. Endocrinol. Metab. 15 2001 309 323
135. S. Oyadomari, A. Koizumi, K. Takeda, T. Gotoh, S. Akira, and E. Araki Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes J. Clin. Invest. 109 2002 525 532
136. S. Ozyazgan, N. Kutluata, S. Af, S.B. Ozda, and A.G. Akkan Effect of glucagon-like peptide-1(7-36) and exendin-4 on the vascular reactivity in streptozotocin-nicotinamide-induced diabetic rats Pharmacology 3 2005 119 126
137. M. Pende, S.C. Kozma, M. Jaquet, V. Oorschot, R. Burcelin, and Y. Le Marchand-Brustel Hypoinsulinaemia, glucose intolerance and diminished beta-cell size in S6K1-deficient mice Nature 408 2000 994 997
138. R. Perfetti, J. Zhou, M.E. Doyle, and J.M. Egan Glucagon-like peptide-1 induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats Endocrinology 141 2000 4600 4605
139. J. Petrik, E. Arany, T.J. McDonald, and D.J. Hill Apoptosis in the pancreatic islet cells of the neonatal rat is associated with a reduced expression of insulin-like growth factor II that may act as a survival factor Endocrinology 139 1998 2994 3004
140. J. Petrik, B. Reusens, E. Arany, C. Remacle, J.J. Hoet, and D.J. Hill A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat, and is associated with a reduced pancreatic expression of insulin-like growth factor-II Endocrinology 140 1999 4861 4873
141. C.J. Petry, M.W. Dorling, D.B. Pawlak, S.E. Ozanne, and C.N. Hales Diabetes in old male offsprings of rats dams fed a reduced protein diet Int. J. Exp. Diabetes Res. 2 2001 139 143
142. M.S. Phillips, Q. Liu, H.A. Hammond, V. Dugan, P.J. Hey, and C.T. Caskey Leptin receptor missense mutation in the fatty Zucker rat Nat. Genet. 13 1996 18 19
143. A. Pick, J. Clark, C. Kubstrup, M. Levisetti, W. Pugh, and S. Bonner-Weir Role of apoptosis in failure of β-cell mass compensation for insulin resistance and β-cell defects in the male Zucker diabetic fatty rat Diabetes 47 1998 358 364
144. C. Plachot, J. Movassat, and B. Portha Impaired beta cell regeneration after partial pancreatectomy in the adult Goto Kakizaki rat, a spontaneous model of type II diabetes Histochem. Cell. Biol. 116 2001 131 139
145. V. Poitout, and R.P. Robertson Minireview: Secondary β-cell failure in type 2 diabetes - A convergence of glucotoxicity and lipotoxicity Endocrinology 143 2002 339 342
146. M. Pontoglio, S. Sreenan, M. Roe, W. Pugh, D. Ostrega, and A. Doyen Defective insulin secretion in hepatocyte nuclear factor 1a-deficient mice J. Clin. Invest. 101 1998 2215 2222
147. D. Porte Banting Lecture 1990: β-Cells in type II diabetes mellitus Diabetes 40 1991 166 180
148. B. Portha Transmitted beta-cell dysfunction as a cause for type 2-diabetes Med. Sci. (Paris) 19 2003 847 853
149. B. Portha, O. Blondel, P. Serradas, R. McEvoy, M.H. Giroix, and M. Kergoat The rat models of non-insulin dependant diabetes induced by neonatal streptozotocin Diabetes Metab. 15 1989 161 175
150. B. Portha, M.H. Giroix, P. Serradas, L. Morin, M.A. Tormo, and D. Bailbé Cellular basis of pancreatic β-cells in non-insulin dependent diabetes P.R. Flatt S. Lenzen Insulin secretion and pancreatic β-cell research 1994 Smith-Gordon London 461 472
151. B. Portha, C. Levacher, L. Picon, and G. Rosselin Diabetogenic effect of streptozotocin in the rat during the perinatal period Diabetes 23 1974 889 895
152. B. Portha, P. Serradas, D. Bailbe, K. Suzuki, Y. Goto, and M.H. Giroix Beta-cell insensitivity to glucose in the GK rat, a spontaneous nonobese model for type 2 diabetes Diabetes 40 1991 486 491
153. M. Prentki, and B.E. Corkey Are the beta-cell signaling molecules malonyl-CoA and cytosolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45 1996 273 283
154. S.G. Rane, P. Dubus, R.V. Mettus, E.J. Galbreath, G. Boden, and E.P. Reddy Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia Nat. Genet. 22 1999 44 52
155. S.G. Rane, and E.P. Reddy Cell cycle control and pancreatic β-cell proliferation Front. Biosci. 5 2000 1 19
156. B. Reusens, and C. Remacle Effects of maternal nutrition and metabolism on the developing endocrine pancreas D.J.P. Barker Fetal origins of cardiovascular and lung disease 17 2000 Marcel Dekker Inc New York 339 358
157. C.J. Rhodes, and M.F. White Molecular insights into insulin action and secretion Eur. J. Clin. Invest. 32 Suppl. 3 2002 3 13
158. C.J. Rhodes Type 2 diabetes: A matter of β-cell life and death? Science 307 2005 380 384
159. J.W. Rich-Edwards, G.A. Colditz, M.J. Stampfer, W.C. Willett, M.W. Gillman, and C.H. Hennekens Birthweight and the risk for type 2 diabetes mellitus in adult women Ann. Intern. Med. 130 1999 278 284
160. R. Rizza, and P. Butler Insulin resistance in type II diabetes mellitus Adv. Second Messenger Phosphoprotein Res. 24 1990 511 516
161. M.E. Roehrich, V. Mooser, V. Lenain, J. Herz, J. Nimpf, and S. Azhar Insulin-secreting beta-cell dysfunctions induced by human lipoproteins J. Biol. Chem. 278 2003 18368 18375
162. K. Saito, N. Yaginuma, and T. Takahashi Differential volummetry of A, B and D cells in the pancreatic islets of diabetic and nondiabetic subjects Tohoku J. Exp. Med. 129 1979 273 283
163. H. Sakuraba, H. Mizukami, N. Yagihashi, R. Wada, C. Hanyu, and S. Yagihashi Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese type II diabetic patients Diabetologia 45 2002 85 96
164. L. Scaglia, C.J. Cahill, D.T. Finegood, and S. Bonner-Weir Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat Endocrinology 138 1997 1736 1741
165. L. Scaglia, F.E. Smith, and S. Bonner-Weir Apoptosis contributes to the involution of beta cell mass in the post partum rat pancreas Endocrinology 136 1995 5461 5468
166. M. Schuhmacher, M.S. Staege, A. Pajic, A. Polack, U.H. Weidle, and G.W. Bornkamm Control of cell growth by c-Myc in the absence of cell division Curr. Biol. 9 1999 1255 1258
167. P. Serradas, M.N. Gangnerau, M.H. Giroix, C. Saulnier, and B. Portha Impaired pancreatic beta cell function in the fetal GK rat: Impact of diabetic inheritance J. Clin. Invest. 101 1998 899 904
168. P. Serradas, L. Goya, M. Lacorne, M.-N. Gangnerua, S. Ramos, and C. Alvarez Fetal insulin-like growth factor-2 production is impaired in the GK rat model of type 2 diabetes Diabetes 51 2002 392 397
169. M. Shimabukuro, Y.-T. Zhou, M. Levi, and R.H. Unger Fatty acid-induced β-cell apoptosis: A link between obesity and diabetes Proc. Natl. Acad. Sci. U.S.A. 95 1998 2498 2502
170. R.A. Simmons, L.J. Templeton, and S.J. Gertz Intrauterine growth retardation leads to the development of type 2 diabetes in the rat Diabetes 50 2001 2279 2286
171. A. Snoeck, C. Remacle, B. Reusens, and J.J. Hoet Effect of low protein diet during pregnancy on the fetal rat endocrine pancreas Biol. Neonate 57 1990 107 118
172. W.C. Soeller, J. Janson, S.E. Hart, J.C. Parker, M.D. Carty, and R.W. Stevenson Islet amyloid-associated diabetes in obese A(vy)/a mice expressing human islet amyloid polypeptide Diabetes 47 1998 743 750
173. R.L. Sorenson, and T.C. Brelje Adaptation of islets of Langerhans to pregnancy: Beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones Horm. Metab. Res. 29 1997 301 307
174. D.A. Stoffers, B.M. Desai, D.D. DeLeon, and R.A. Simmons Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat Diabetes 52 2003 734 740
175. D.A. Stoffers, J. Ferrer, W.L. Clarke, and J.F. Habener Early-onset type-II diabetes mellitus (MODY4) linked to IPF1 Nat. Genet. 17 1997 138 139
176. D.A. Stoffers, N.T. Zinkin, V. Stanojevic, W.L. Clarke, and J.F. Habener Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence Nat. Genet. 15 1997 106 110
177. K.C. Stump, M.M. Swindle, C.D. Saudek, and J.D. Strandberg Pancreatectomized swine as a model of diabetes mellitus Lab. Anim. Sci. 38 1988 439 443
178. K. Takaya, Y. Ogawa, N. Isse, T. Okazaki, N. Satoh, and H. Masuzaki Molecular cloning of rat leptin receptor isoform complementary DNAs: Identification of missense mutation in Zucker fatty (fa/fa) rats Biochem. Biophys. Res. Commun. 225 1996 75 83
179. A.U. Teuscher, D.M. Kendall, Y.F.C. Smets, J.P. Leone, D.E.R. Sutherland, and R.P. Robertson Successful islet autotransplantation in humans: Functional insulin secretory reserve as an estimate of surviving islet cell mass Diabetes 47 1998 324 330
180. Y. Tokuyama, J. Sturis, A.M. DePaoli, J. Takeda, M. Stoffel, and J. Tang Evolution of beta cell dysfunction in the male Zucker diabetic fatty rat Diabetes 44 1995 1447 1457
181. l during development of the human fetal and rat neonatal endocrine pancreas: Correlation to programmed cell death Exp. Clin. Endocrinol. Diabetes 105 1997 A27
182. C. Tourrel, D. Bailbe, M. Lacorne, M.J. Meile, M. Kergoat, and B. Portha Persistent improvement of type 2 diabetes in the Goto-Kakizaki rat model by expansion of the β-cell mass during the prediabetic period with glucagon-like peptide-1 or exendin-4 Diabetes 51 2002 1443 1452
183. C. Tourrel, D. Bailbe, M.J. Meile, M. Kergoat, and B. Portha Glucagon-like peptide-1 and exendin-4 stimulate β-cell neogenesis in streptozotocin-treated newborn rats resulting in persistently improved glucose homeostasis at adult age Diabetes 50 2001 1562 1570
184. P. Trayhurn, and I.S. Wood Adipokines: Inflammation and the pleiotropic role of white adipose tissue Br. J. Nutr. 92 2004 347 355
185. R.L. Tuttle, N.S. Gill, W. Pugh, J.P. Lee, B. Koeberlein, and E.E. Furth Regulation of pancreatic beta-cell growth and survival by the serine/threonine protein kinase Akt1/PKBalpha Nat. Med. 7 2001 1133 1137
186. R.H. Unger, and L. Orci Lipoapoptosis: Its mechanism and its diseases Biochim. Biophys. Acta 1585 2002 202 212
187. F. Urano, X. Wang, A. Bertolotti, Y. Zhang, P. Chung, and H.P. Harding Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666
188. C.B. Verchere, D.A. D'Alessio, R.D. Palmiter, and S.E. Kahn Transgenic mice overproducing islet amyloid polypeptide have increased insulin storage and secretion in vitro Diabetologia 37 1994 725 728
189. H. Wang, G. Kouri, and C.B. Wollheim ER stress and SREBP-1 activation are implicated in β-cell glucolipotoxicity J. Cell Sci. 118 2005 3905 3915
190. J. Wang, T. Takeuchi, S. Tanaka, S.K. Kubo, T. Kayo, and D. Lu A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse J. Clin. Invest. 103 1999 27 37
191. Q. Wang, L. Li, E. Xu, V. Wong, C.J. Rhodes, and P.L. Brubaker Glucagon-like peptide-1 regulates proliferation and apoptosis via activation of protein kinase B in pancreatic INS-1 beta cells Diabetologia 47 2004 478 487
192. R.N. Wang, L. Bouwens, and G. Klöppel β-Cell proliferation in normal and streptozotocin-treated newborn rats: Site, dynamics and capacity Diabetologia 37 1994 1088 1096
193. G.C. Weir, E.T. Clore, C.J. Zmachinski, and S. Bonner-Weir Islet secretion in a new experimental model for non-insulin-dependent Diabetes 30 1981 590 595
194. G.C. Weir, J.L. Leahy, and S. Bonner-Weir Experimental reduction of the β-cell mass: Implications for the pathogenesis of diabetes Diabetes Metab. Rev. 2 1986 125 161
195. C. Weyer, C. Bogardus, D.M. Mott, and R.E. Pratley The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus J. Clin. Invest. 104 1999 787 794
196. M.F. White IRS proteins and the common path to diabetes Am. J. Physiol. Endocrinol. Metab. 283 2002 E413 E422
197. D.J. Withers, D.J. Burks, H.H. Towery, S.L. Altamuro, C.L. Flint, and M.F. White Irs-2 coordinates Igf-1 receptor-mediated beta-cell development and peripheral insulin signalling Nat. Genet. 23 1999 32 40
198. D.J. Withers, J.S. Gutierres, H. Towery, J.M. Ren, D.J. Burks, and S. Previs Disruption of IRS-2 causes type-2 diabetes in mice Nature 391 1998 900 904
199. C.E. Wrede, L.M. Dickson, M.K. Lingohr, I. Briaud, J.F. McCuaig, and C.J. Rhodes Protein kinase B/Akt prevents fatty acid induced apoptosis in pancreatic beta-cells (INS-1) J. Biol. Chem. 277 2002 49676 49684
200. G. Xu, D.A. Stoffers, J.F. Habener, and S. Bonner-Weir Exendin-4 stimulates both β-cell replication and neogenesis, resulting in increased β-cell mass and improved glucose tolerance in diabetic rats Diabetes 48 1999 2270 2276
201. K. Yagui, T. Yamaguchi, A. Kanatsuka, F. Shimada, C.I. Huang, and Y. Tokuyama Formation of islet amyloid fibrils in β-secretory granules of transgenic mice expressing human islet amyloid polypeptide (amylin) Eur. J. Endocrinol. 132 1995 487 496
202. K.H. Yoon, S.H. Ko, J.H. Cho, and J.M. Lee Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in Korea J. Clin. Endocrinol. Metab. 88 2003 2300 2308