Alterations in growth and apoptosis of insulin receptor substrate-1-deficient β-cells

American Journal of Physiology - Endocrinology and Metabolism

Volumn 289, Issue 2 52-2, 2005, Pages

  Hennige, Anita M ^a   Ozcan, Umut ^a   Okada, Terumasa ^a   Jhala, Ulupi S ^c   Schubert, Markus ^a   White, Morris F ^b   Kulkarni, Rohit N ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d JOSLIN DIABETES CENTER   (United States)

Author keywords

cell growth; Insulin receptor substrate proteins; Insulin resistance; Islets; Transplantation

Indexed keywords

INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; PROTEIN; PROTEIN KINASE B; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXPERIMENTAL MODEL; GROWTH RETARDATION; HORMONE ACTION; HYPERINSULINEMIA; IMMUNOHISTOCHEMISTRY; INSULIN RESISTANCE; KNOCKOUT MOUSE; MALE; MITOSIS RATE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL HYPERPLASIA; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WILD TYPE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; APOPTOSIS; CELL PROLIFERATION; INSULIN; INSULIN RESISTANCE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; KIDNEY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION;

EID: 23044446704     PISSN: 01931849     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpendo.00032.2004     Document Type: Article

References (52)

1. Araki E, Lipes MA, Patti ME, Bruning JC, Haag B III, Johnson RS, and Kahn CR. Alternative pathway of insulin signaling in mice with targeted disruption of the IRS-I gene. Nature 372: 186-190, 1994.
2. 1a. Aspinwall CA, Qian WJ, Roper MG, Kulkarni RN, Kahn CR, and Kennedy RT. Roles of insulin receptor substrate-1, phosphatidylinositol 3-kinase, and release of intracellular Ca2+ stores in insulin-stimulated insulin secretion in beta-cells. J Biol Chem 275: 22331-22338, 2000.
3. Bonner-Weir S, Baxter L, Schuppin GT, and Smith FE. A second pathway for regeneration of adult exocrine and enocringe pancrease. A possible recapitulation of embryonic development. Diabetes 42: 1715-1720, 1993.
4. Bonner-Weir S, Deery D, Leahy JL, and Weir GC. Compensatory growth of pancreatic β-cells in adult rats after short-term glucose infusion. Diabetes 38: 49-53, 1989.
5. Bruning JC, Gautam D, Burks DJ, Gillette J, Schubert M, Orban PC, Klein R, Krone W, Muller-Wieland D, and Kahn CR. Role of brain insulin receptor in control of body weight and reproduction. Science 289: 2122-2125, 2000.
6. Budihardjo I, Oliver H, Lutter M, Luo X, and Wang X. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15: 269-290, 1999.
7. Cheatham B and Kahn CR. Insulin action and the insulin signaling network. Endocr Rev 16: 117-142, 1995.
8. Davalli AM, Scaglia L, Zangen DH, Hollister J, Bonner-Weir S, and Weir GC. Vulnerability of islets in the immediate posttransplantation period. Dynamic changes in structure and function. Diabetes 45: 1161-1167, 1996.
9. D'Ercole AJ and Calikoglu AS. Editorial review: the case of local versus endocrine IGF-I actions: the jury is still out. Growth Horm IGF Res 11: 261-265, 2001.
10. Dor Y, Brown J, Martinez OI, and Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429: 41-46, 2004.
11. Flier SN, Kulkarni RN, and Kahn CR. Evidence for a circulating islet cell growth factor in insulin-resistant states. Proc Natl Acad Sci USA 98: 7475-7480, 2001.
12. Garcia-Ocana A, Takane KK, Syed MA, Philbrick WM, Vasavada RC, and Stewart AF. Hepatocyte growth factor overexpression in the islet of transgenic mice increases beta cell proliferation, enhances islet mass, and induces mild hypoglycemia. J Biol Chem 275: 1226-1232, 2000.
13. Han X, Sun Y, Scott S, and Bleich D. Tissue inhibitor of metalloproteinase-1 prevents cytokine-mediated dysfunction and cytotoxicity in pancreatic islets and beta-cells. Diabetes 50: 1047-1055, 2001.
14. Hennige AM, Burks DJ, Ozcan U, Kulkarni RN, Ye J, Park S, Schubert M, Fisher TL, Dow MA, Leshan R, Zakaria M, Mossa-Basha M, and White MF. Upregulation of insulin receptor substrate-2 in pancreatic beta cells prevents diabetes. J Clin Invest 112: 1521-1532, 2003.
15. Hugl SR, White MF, and Rhodes CJ. Insulin-like growth factor I (IGF-I)-stimulated pancreatic beta-cell growth is glucose-dependent. Synergistic activation of insulin receptor substrate-mediated signal transduction pathways by glucose and IGF-I in INS-1 cells. J Biol Chem 273: 17771-17779, 1998.
16. Kahn CR. Banting Lecture. Insulin action, diabetogenes, and the cause of type II diabetes. Diabetes 43: 1066-1084, 1994.
17. Kitamura T, Nakae J, Kitamura Y, Kido Y, Biggs WH III, Wright CV, White MF, Arden KC, and Accili D. The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J Clin Invest 110: 1839-1847, 2002.
18. Kloppel G, Lohr M, Habich K, Oberholzer M, and Heitz PU. Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv Synth Pathol Res 4: 110-125, 1985.
19. Kondo T, Vicent D, Suzuma K, Yanagisawa M, King GL, Holzenberger M, and Kahn CR. Knockout of insulin and IGF-I receptors on vascular endothelial cells protects against retinal neovascularization. J Clin Invest 111: 1835-1842, 2003.
20. Kubota N, Tobe K, Terauchi Y, Eto K, Yamauchi T, Suzuki R, Tsubamoto Y, Komeda K, Nakano R, Miki H, Satoh S, Sekihara H, Sciacchitano S, Lesniak M, Aizawa S, Nagai R, Kimura S, Akanuma Y, Taylor SI, and Kadowaki T. Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory β-cell hyperplasia. Diabetes 49: 1880-1889, 2000.
21. Kulkarni RN. Receptors for insulin and insulin-like growth factor-1 and insulin receptor substrate-1 mediate pathways that regulate islet function. Biochem Soc Trans 30: 317-322, 2002.
22. Kulkarni RN, Bruning JC, Winnay JN, Postic C, Magnuson MA, and Kahn CR. Tissue-specific knockout of the insulin receptor in pancreatic β cells creates an insulin secretory defect similar to that in Type 2 diabetes. Cell 96: 329-339, 1999.
23. Kulkarni RN, Holzenberger M, Shih DQ, Ozcan U, Stoffel M, Magnuson MA, and Kahn CR. Beta-cell-specific deletion of the Igf1 receptor leads to hyperinsulinemia and glucose intolerance but does not alter beta-cell mass. Nat Genet 31: 111-115, 2002.
24. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, and Kahn CR. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest 114: 828-836, 2004.
25. Kulkarni RN and Kahn CR. Genetic models of insulin resistance: alterations in β-cell biology. In: Molecular Basis of Pancreas Development and Function, edited by Habener JF and Hussain M. New York: Kluwer Academic, 2001, p. 299-323.
26. Kulkarni RN and Kahn CR. Molecular biology. HNFs-linking the liver and pancreatic islets in diabetes. Science 303: 1311-1312, 2004.
27. 26a. Kulkarni RN, Roper MG, Dahlgren G, Shih DQ, Kauri LM, Peters JL, Stoffel M, and Kennedy RT. Islet secretory defect in insulin receptor substrate 1 null mice is linked with reduced calcium signaling and expression of sarco(endo)plasmic reticulum Ca2+-ATPase (SERCA)-2b and -3. Diabetes 53: 1517-1525, 2004.
28. Kulkarni RN, Winnay JN, Daniels M, Bruning JC, Flier SN, Hanahan D, and Kahn CR. Altered function of insulin receptor substrate-1-deficient mouse islets and cultured beta-cell lines. J Clin Invest 104: R69-R75, 1999.
29. Lammert E, Cleaver O, and Melton D. Induction of pancreatic differentiation by signals from blood vessels. Science 294: 1-10, 2001.
30. Lammert E, Cleaver O, and Melton D. Role of endothelial cells in early pancreas and liver development. Mech Dev 120: 59-64, 2003.
31. Lammert E, Gu G, McLaughlin M, Brown D, Brekken R, Murtaugh LC, Gerber HP, Ferrara N, and Melton DA. Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 13: 1070-1074, 2003.
32. Lillioja S, Mott DM, Spraul M, Ferraro R, Foley JE, Ravussin E, Knowler WC, Bennett PH, and Bogardus C. Insulin resistance and insulin secretory dysfunction as precursors of non-insulin-dependent diabetes mellitus: prospective studies of Pima Indians. N Engl J Med 329: 1992, 1993.
33. Martin BC, Warram J, Krolewski AS, Bergman RN, Soeldner JS, and Kahn CR. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study+. Lancet 340: 925-929, 1992.
34. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, and Kahn CR. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 6: 87-97, 2000.
35. Myers MG Jr and White MF. Insulin signal transduction and the IRS proteins. Annu Rev Pharmacol Toxicol 36: 615-658, 1996.
36. Nakae J, Kido Y, and Accili D. Distinct and overlapping functions of insulin and IGF-I receptors. Endocr Rev 22: 818-835, 2001.
37. 36a. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, Hogan BL, and Wright CV. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 122: 983-995, 1996.
38. 36b. Otani K, Kulkarni RN, Baldwin AC, Krutzfeldt J, Ueki K, Stoffel M, Kahn CR, and Polonsky KS. Reduced β-cell mass and altered glucose sensing impair insulin-secretory function in βIRKO mice. Am J Physiol Endocrinol Metab 286: E41-E49, 2004.
39. Shepherd PR, Withers DJ, and Siddle K. Phosphoinositide 3-kinase: the key switch mechanism in insulin signalling. Biochem J 333: 471-490, 1998.
40. Shirakami A, Toyonaga T, Tsuruzoe K, Shirotani T, Matsumoto K, Yoshizato K, Kawashima J, Hirashima Y, Miyamura N, Kahn CR, and Araki E. Heterozygous knockout of the IRS-1 gene in mice enhances obesity-linked insulin resistance: a possible model for the development of type 2 diabetes. J Endocrinol 174: 309-319, 2002.
41. Smith FE, Rosen KM, Villa-Komaroff L, Weir GC, and Bonner-Weir S. Enhanced insulin-like growth factor I gene expression in regenerating rat pancreas. Proc Natl Acad Sci USA 88: 6152-6156, 1991.
42. Stoffers DA, Zinkin NT, Stanojevic V, Clarke WL, and Habener JF. Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence. Nat Genet 1: 106-110, 1997.
43. Tamemoto H, Kadowaki T, Tobe K, Yagi T, Sakura H, Hayakawa T, Terauchi Y, Ueki K, Kaburagi Y, Satoh S, Sekihara H, Yoshioka S, Horikoshi H, Furuta Y, Ikawa Y, Kasuga M, Yazaki Y, and Aizawa S. Insulin resistance and growth retardation in mice lacking insulin receptor substrate-1. Nature 372: 182-186, 1994.
44. Terauchi Y, Matsui J, Suzuki R, Kubota N, Komeda K, Aizawa S, Eto K, Kimura S, Nagai R, Tobe K, Lienhard GE, and Kadowaki T. Impact of genetic background and ablation of insulin receptor substrate (IRS)-3 on IRS-2 knock-out mice. J Biol Chem 278: 14284-14290, 2003.
45. Trivedi N, Steil GM, Colton CK, Bonner-Weir S, and Weir GC. Improved vascularization of planar membrane diffusion devices following continuous infusion of vascular endothelial growth factor. Cell Transplant 9: 115-124, 2000.
46. Tseng YH, Ueki K, Kriauciunas KM, and Kahn CR. Differential roles of insulin receptor substrates in the anti-apoptotic function of insulin-like growth factor-1 and insulin. J Biol Chem 111: 31601-31611, 2002.
47. Ueki K, Fruman DA, Brachmann SM, Tseng YH, Cantley LC, and Kahn CR. Molecular balance between the regulatory and catalytic subunits of phosphoinositide 3-kinase regulates cell signaling and survival. Mol Cell Biol 22: 965-977, 2002.
48. Vasavada RC, Cavaliere C, D'Ercole AJ, Dann P, Burtis WJ, Madlener AL, Zawalich K, Zawalich W, Philbrick W, and Stewart AF. Overexpression of parathyroid hormone-related protein in the pancreatic islets of transgenic mice causes islet hyperplasia, hyperinsulinemia, and hypoglycemia. J Biol Chem 271: 1200-1208, 1996.
49. Vasavada RC, Garcia-Ocana A, Zawalich WS, Sorenson RL, Dann P, Syed M, Ogren L, Talamantes F, and Stewart AF. Targeted expression of placental lactogen in the beta cells of transgenic mice results in beta cell proliferation, islet mass augmentation, and hypoglycemia. J Biol Chem 275: 15399-15406, 2000.
50. Warram JH, Martin BC, Krolewski AS, Soeldner JS, and Kahn CR. Slow glucose removal rate and hyperinsulinemia are predictors of the risk of Type II diabetes in offspring of diabetic parents. Ann Intern Med 113: 909-915, 1990.
51. Withers DJ, Gutierrez JS, Towery H, Burks DJ, Ren JM, Previs S, Zhang Y, Bernal D, Pons S, Shulman GI, Bonner-Weir S, and White MF. Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391: 900-904, 1998.
52. Xuan S, Kitamura T, Nakae J, Politi K, Kido Y, Fisher PE, Morroni M, Cinti S, White MF, Herrera PL, Accili D, and Efstratiadis A. Defective insulin secretion in pancreatic beta cells lacking type 1 IGF receptor. J Clin Invest 110: 1011-1019, 2002.