Transcription factor abnormalities as a cause of beta cell dysfunction in diabetes: A hypothesis

Acta Diabetologica

Volumn 34, Issue 3, 1997, Pages 177-184

  Weir, G C ^a,b   Sharma, A ^a   Zangen, D H ^a   Bonner Weir, S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b JOSLIN DIABETES CENTER   (United States)

Author keywords

Beta cell; Diabetes; Glucotoxicity; Insulin secretion; PDX 1

Indexed keywords

GLUCOKINASE; GLUCOSE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GLYCOGEN; HEXOKINASE; INSULIN; ION CHANNEL; TRANSCRIPTION FACTOR;

CELL DIFFERENTIATION; DEGRANULATION; DIABETES MELLITUS; ENZYME ACTIVITY; ENZYME DEFECT; INSULIN RELEASE; INSULIN RESISTANCE; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RECYCLING; REVIEW;

ANIMALS; CELL DIFFERENTIATION; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INSULIN; ISLETS OF LANGERHANS; TRANSCRIPTION FACTORS;

EID: 0030656344     PISSN: 09405429     EISSN: None     Source Type: Journal    
DOI: 10.1007/s005920050071     Document Type: Review

References (92)

1. Weir GC, Leahy JL, Pathogenesis of non-insulin-dependent (type II) diabetes mellitus. In: Joslin's Diabetes Mellitus, 13th edn. Lea and Febiger, Philadelphia, pp 240-264, 1994
2. Leahy JL, Bonner-Weir S, Weir GC, Beta cell dysfunction induced by chronic hyperglycemia: current ideas on mechanism of impaired glucose-induced insulin secretion. Diabetes Care 15: 442, 1992
3. Portha B, Giroix MH, Serradas P, Morin L, Saulnier C, Bailbe D, Glucose refractoriness of pancreatic beta-cells in rat models of non-insulin dependent diabetes. Diabetes Metab 20: 108-115, 1994
4. Ogawa A, Johnson JH, Ohneda M, McAllister CT, Inman L, Alam T, Unger RH, Roles of insulin resistance and beta-cell dysfunction in dexamethasone-induced diabetes. J Clin Invest 90: 497-504, 1992
5. O'Rahilly S, Turner RC, Matthews DR, Impaired pulsatile secretion of insulin in relatives of patients with non-insulin-dependent diabetes mellitus. N Engl J Med 318: 1225-1230, 1988
6. Laedtke T, Schmitz O, Porksen N, Velhuis J, Butler P, Mechanism of impaired pulsatile insulin secretion in NIDDM. Diabetes 45: 40A, 1996
7. Matschinsky FM, A lesson in metabolic regulation inspired by the glucokinase glucose sensor paradigm. Diabetes 45: 223-241, 1996
8. De Vos A, Heimberg H, Quartier E, Huypens P, Bouwens L, Pipeleers D, Schuit F, Human and rat beta cells differ in glucose transporter but not in glucokinase gene expression. J Clin Invest 96: 2489-2495, 1995
9. MacDonald MJ, Elusive proximal signals of beta cells for insulin secretion. Diabetes 39: 1461-1466, 1990
10. MacDonald MJ, High content of mitochondrial glycerol-3-phosphate dehydrogenase in pancreatic islets and its inhibition by diazoxide. J Biol Chem 256: 8287-8290, 1981
11. Prentki M, Corkey BE, 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: 273-283, 1996
12. MacDonald MJ, Feasibility of a mitochondrial pyruvate malate shuttle in pancreatic islets. J Biol Chem 270: 20051-20058, 1995
13. MacDonald MJ, McKenzie DI, Walker TM, Kaysen JH, Lack of glyconeogenesis in pancreatic islets: expression of gluconeogenic enzyme genes in islets. Horm Metab Res 24: 158-160, 1992
14. Sekine N, Cirulli V, Regazzi R, Brown LJ, Gine E, Tamarit-Rodriguez J, Girotti M, Marie S, MacDonald MJ, Wollheim CB, Rutter GA, Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic beta cells. J Biol Chem 269: 4895-4902, 1994
15. Stein DT, Esser V, Stevenson BE, Lane KE, Whiteside JH, Daniels MB, Chen S, McGarry JD, Essentiality of circulating fatty acids for glucose-stimulated insulin secretion in the fasted rat. J Clin Invest 97: 2728-2735, 1996
16. Weir GC, Non-insulin-dependent diabetes mellitus: interplay between beta cell inadequacy and insulin resistance. Am J Med 73: 461-464, 1982
17. McGarry JD, What if Minkowski had been ageusic? An alternative angle on diabetes. Science 258: 766-770, 1992
18. Zhou Y-P, Grill VE, Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J Clin Invest 93: 870-876, 1994
19. Zhou Y-P, Grill VE, Palmitate-induced beta cell insensitivity to glucose is coupled to decreased pyruvate dehydrogenase activity and enhanced kinase activity in rat pancreatic islets. Diabetes 44: 394-399, 1995
20. Zhou YP, Berggren PO, Grill V, A fatty acid-induced decrease in pyruvate dehydrogenase activity is an important determinant of beta-cell dysfunction in the obese diabetic db/db mouse. Diabetes 45: 580-586, 1996
21. Brunzell JD, Robertson RP, Lerner RL, Hazzard WR, Ensinck JW, Bierman EL, Porte D Jr, Relationships between fasting plasma glucose levels and insulin secretion during intravenous glucose tolerance tests. J Clin Endocrinol Metab 42: 222-229, 1976
22. Weir GC, The relationship of diabetes, loss of glucose-induced insulin secretion, and GLUT2. J Diabetes Complications 7: 124-129, 1993
23. Unger RH, Diabetic hyperglycemia: link to impaired glucose transport in pancreatic B cells. Science 251: 1200-1205, 1991
24. Johnson JH, Ogawa A, Chen L, Orci L, Newgard CB, Alam T, Unger RH, Underexpression of beta cell high Km glucose transporters in non-insulin-dependent diabetes. Science 250: 546-549, 1990
25. Valera A, Solanes G, Fernandez-Alvarez J, Pujol A, Ferrer J, Asins G, Gomis R, Bosch F, Expression of GLUT-2 antisense RNA in beta cells of transgenic mice leads to diabetes. J Biol Chem 269: 28543-28546, 1994
26. Tal M, Wu YJ, Leiser M, Surana M, Lodish H, Fleischer N, Weir GC, Efrat S, HRAS downregulates GLUT2 in beta cells of transgenic mice without affecting glucose homeostasis. Proc Natl Acad Sci USA 89: 5744-5748, 1992
27. Ferber S, Beltrandel Rio H, Johnson JH, Noel RJ, Cassidy LE, Clark S, Becker TC, GLUT-2 gene transfer into insulinoma cells confers both low and high affinity glucose-stimulated insulin release. J Biol Chem 269: 11523-11529, 1994
28. Lachall M, Spangler RA, Jung CY, High Km of GLUT-2 glucose transporter does not explain its role in insulin secretion. Am J Physiol 265: E914-E919, 1993
29. Marynissen G, Leclerg-Meyer V, Sener A, Malaisse WJ, Perturbation of pancreatic islet function in glucose-infused rats. Metabolism 39: 87-95, 1990
30. Malaisse WJ, Maggetto JC, Leclercq-Meyer V, Sener A, Interference of glycogenolysis with glycolysis in pancreatic islets from glucose-infused rats. J Clin Invest 91: 432-436, 1993
31. Khan A, Ostenson CG, Berggren S, Glucocorticoid increases glucose cycling and inhibits insulin release in pancreatic islets of ob/ob mice. Am J Physiol 263: E663-E666, 1992
32. Efrat S, Leiser M, Jian Y, Fusco-DeMane D, Emran OA, Surana M, Jetton TL, Magnuson MA, Weir G, Fleischer N, Ribozyme-mediated attenuation of pancreatic B-cell glucokinase expression in transgenic mice results in impaired glucose-induced insulin secretion. Proc Natl Acad Sci USA 91: 2051-2055, 1994
33. Chen C, Hosokawa H, Bumbalo LM, Leahy JL, Regulatory effects of glucose on the catalytic activity and cellular content of glucokinase in the pancreatic B cell. J Clin Invest 94: 1616-1620, 1994
34. Hosokawa H, Hosokawa YA, Leahy JL, Upregulated hexokinase activity in isolated islets from diabetic 90% pancreatectomized rats. Diabetes 44: 1328-1333, 1995
35. Ostenson CG, Abdel-Halim SM, Rasschaert J, Malaisse-Lagae F, Meuris S, Sener A, Deficient activity of FAD-linked glycerophosphate dehydrogenase in islets of GK rats. Diabetologia 36: 722-726, 1993
36. Sener A, Malaisse-Lagae F, Ostenson CG, Malaisse WJ, Metabolism of endogenous nutrients in islets of GK rats. Biochem J 296: 329-334, 1993
37. MacDonald MJ, Efendic S, Ostenson CG, Normalization by insulin treatment of low mitochondrial glycerol phosphate dehydrogenase and pyruvate carboxylase in pancreatic islets of the GK rat. Diabetes 45: 886-890, 1996
38. Purrello F, Vetri M, Vinci C, Gatta C, Buscema M, Vigneri R, Chronic exposure to high glucose and impairment of K (+)-channel function in perifused rat pancreatic islets. Diabetes 39: 397-399, 1990
39. Iwashima Y, Pugh W, Depaoli AM, Takeda J, Seino S, Bell GI, Polonsky KS, Expression of calcium channel mRNAs in rat pancreatic islets and downregulation after glucose infusion Diabetes 42: 948-955, 1993
40. Hosokawa YA, Leahy JL, Granule insulin content is a critical regulatory factor in insulin secretory responses. Diabetes 45: 159A, 1996
41. Chen L, Alam T, Johnson JH, Hughes S, Newgard CB, Unger RH, Regulation of beta cell glucose transporter gene expression. Proc Natl Acad Sci USA 87: 4088-4092, 1990
42. Tokuyama Y, Sturis J, Depaoli AM, Takeda J, Stoffel M, Tang J, Sun X, Polonsky KS, Bell GL, Evoluation of beta cell dysfunction in the male Zucker diabetic fatty rat. Diabetes 44: 1447-1457, 1995
43. Tal M, Liang Y, Najafi H, Lodish HF, Matschinsky FM, Expression and function of GLUT-1 and GLUT-2 glucose transporter isoforms in cells of cultured rat pancreatic islets. J Biol Chem 267: 17241-17247, 1992
44. Yasuda K, Yamada Y, Inagaki N, Yano H, Okamoto Y, Tsuji K, Fukumoto H, Imura H, Seino S, Seino Y, Expression of GLUT1 and GLUT2 glucose transporter isoforms in rat islets of Langerhans and their regulation by glucose. Diabetes 41: 76-81, 1992
45. Ferrer J, Gomis R, Fernandez Alvarez J, Casamitjana R, Vilardell E, Signals derived from glucose metabolism are required for glucose regulation of pancreatic islet GLUT2 mRNA and protein. Diabetes 42: 1273-1280, 1993
46. Zangen DH, Bonner-Weir S, Lee CH, Latimer JB, Miller CP, Habener JF, Weir GC, Reduced insulin, GLUT2, and IDX-1 in beta cells after partial pancreatectomy. Diabetes 46: 258-264, 1997
47. Bonner-Weir S, Trent DF, Weir GC, Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. J Clin Invest 71: 1544-1553, 1983
48. Sharma A, Stein R, Glucose-induced transcription of the insulin gene is mediated by factors required for beta cell-type-specific expression. Mol Cell Biol 14: 871-879, 1994
49. German MS, Moss LG, Wang J, Rutter WJ, The insulin and islet amyloid polypeptide genes contain similar cell-specific promoter elements that bind identical beta cell nuclear complexes. Mol Cell Biol 12: 1777-1788, 1992
50. Shieh S-Y, Tsai M-J, Cell-specific and ubiquitous factors are responsible for the enhancer activity of the rat insulin II gene. J Biol Chem 266: 16708-16714, 1991
51. Peshavaria M, Gamer L, Henderson E, Teitelman G, Wright CVE, Stein R, XIHbox 8, an endoderm-specific Xenopus homeodomain protein, is closely related to a mammalian insulin gene transcription factor. Mol Endocrinol 8: 806-816, 1994
52. Petersen HV, Serup P, Leonard J, Michelsen BK, Madsen OD, Transcriptional regulation of the human insulin gene is dependent on the homeodomain protein STF1/IPF1 acting through the CT boxes. Proc Natl Acad Sci USA 91: 10465-10469, 1994
53. Karlsson O, Edlund T, Barnett Moss J, Rutter WJ, Walker MD, A mutational analysis of the insulin gene transcriptional control region: expression in beta cells is dependent on two related sequences within the enhancer. Proc Natl Acad Sci USA 84: 8819, 1987
54. German MS, Blanar MA, Nelson C, Moss LG, Rutter WJ, Two related helix-loop-helix proteins participate in separate cell-specific complexes that bind the insulin enhancer. Mol Endocrinol 5: 292-299, 1991
55. Hwung Y-P, Gu Y-Z, Tsai M-J, Cooperativity of sequence elements mediates tissue specificity of the rat insulin II gene. Mol Cell Biol 10: 1784-1788, 1990
56. Ohlsson H, Karlsson K, Edlund T, IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12: 4251-4259, 1993
57. Leonard J, Peers B, Johnson T, Ferreri K, Lee S, Montminy MR, Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells. Mol Endocrinol 1275-1283, 1993
58. Miller CP, McGehee RE, Habener JF, IDX-I: a new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostating gene. EMBO J 13: 1145-1156, 1994
59. Jonsson J, Carlsson L, Edlund T, Edlund H, Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371: 606-609, 1994
60. Peyton M, Moss L, Tsai MJ, Two distinct class A helix-loop-helix transcription factors, E2A and BETA1, form separate DNA-binding complexes on the insulin E-box. J Biol Chem 269: 25936-25941, 1994
61. Naya FJ, Stellrecht CMM, Tsai M-J, Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 9: 1009-1019, 1995
62. Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H, Conversion of Xenopus ectoderm into neurons by neuroD, a basic helix-loop-helix, protein. Science 268: 836, 1995
63. Sharma A, Fusco-DeMaine D, Henderson E, Efrat S, Stein R, The role of the insulin control element and RIPE3b1 activators in glucose-stimulated transcription of the insulin gene. Mol Endocrinol 9: 1468-1476, 1995
64. Poitout V, Olson LK, Robertson RP, Chronic exposure of betaTC-6 cells to supraphysiologic concentrations of glucose decreases binding of the RIPESb1 insulin gene transcription activator. J Clin Invest 97: 1041-1046, 1996
65. Robinson GLWG, Peshavaria M, Henderson E, Shieh S-Y, Tsais M-J, Teitelman G, Stein R, Expression of the trans-active factors that simulate insulin control element-mediated activity appear to precede insulin gene transcription. J Biol Chem 269: 2452-2460, 1994
66. Watada H, Kajimoto Y, Umayahara Y, Matsuoka T, Kaneto H, Fujitani Y, Kamada T, Kawamori R, Yamasaki Y, The human glucokinase gene beta cell-type promoter. Diabetes 45: 1478-1488, 1996
67. Waeber G, Thompson N, Nicod P, Bonny C, Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol Endocrinol 10: 1327-1334, 1996
68. Watada H, Kajimoto Y, Miyagawa J, Hanafusa T, Hamaguchi K, Matsuoka T, Yamamoto K, Matsuzawa Y, Kawamori R, Yamasaki Y, PDX-1 induces insulin and glucokinase gene expressions in alpha TC1 clone 6 cells in the presence of betacellulin. Diabetes 45: 1826-1831, 1996
69. Serup P, Jensen J, Andersen FG, Jorgensen MC, Blume N, Holst JJ, Madsen OD, Induction of insulin and islet amyloid polypeptide production in pancreatic islet glucagonoma cells by insulin promoter factor I. Proc Natl Acad Sci USA 93: 9015-9020, 1996
70. Wheeler MB, Nishitani J, Buchan AMJ, Kopin AS, Chey WY, Chang T, Leiter AB, Identification of a transcriptional enhancer important for enteroendocrine and pancreatic islet cell-specific expression of the secretin gene Mol Cell Biol 12: 3531-3539, 1992
71. German MS, Wang J, The insulin gene contains multiple transcriptional elements that respond to glucose. Mol Cell Biol 14: 4067-4075, 1994
72. MacFarlane WM, Read ML, Gilligan M, Bujalska I, Docherty K, Glucose modulates the binding activity of the beta cell transcription factor IUF1 in a phosphorylation-dependent manner. Biochem J 303: 625-631, 1994
73. Melloul D, Ben-Neriah Y, Cerasi E, Glucose modulates the binding of an islet-specific factor to a conserved sequence within the rat I and the human insulin promoters. Proc Natl Acad Sci USA 90: 3865-3869, 1993
74. Olson LK, Redmon JB, Towle HC, Robertson RP, Chronic exposure of HIT cells to high glucose concentrations paradoxically decreases insulin gene transcription and alters binding of insulin gene regulatory protein. J Clin Invest 92: 514-519 1993
75. Olson LK, Sharma A, Peshavaria M, Wright CVE, Towle HC, Robertson RP, Stein R, Reduction of insulin gene transcription in HIT-T15 beta cells chronically exposed to a supraphysiologic glucose concentration is associated with loss of STF-1 transcription factor expression. Proc Natl Acad Sci USA 92: 9127-9131, 16401
76. Sharma A, Olson LK, Robertson RP, Stein R, The reduction of insulin gene transcription in HIT-T15b cells chronically exposed to high glucose concentration is associated with the loss of RIPE3b1 and STF-1 transcription factor expression. Mol Endocrinol 9: 1127-1134, 1995
77. Yamato E, Ikegami H, Miyazaki J-I, Ogihara T, Identification of genes regulated by glucose in a pancreatic beta-cell line by a new method for substraction of mRNA. Diabetologia 39: 1293-1298, 1996
78. Goodison S, Kenna S, Ashcroft SJH, Control of insulin gene expression by glucose. Biochem J 285: 563-568, 1992
79. Brun T, Roche E, Kim K-H, Prentki M, Glucose regulated acetyl-CoA carboxylase gene expression in a pancreatic B-cell line (INS-1). J Biol Chem 268: 18905-18911, 1993
80. Efrat S, Surana M, Fleischer N, Glucose induces insulin gene transcription in a murine pancreatic B-cell line. J Biol Chem 266: 11141-11143, 1991
81. Guest PC, Bailyes EM, Rutherford NG, Hutton JC, Insulin secretory granule biogenesis. Biochem J 274: 73-78, 1991
82. Schuit FC, In't Veld PA, Pipeleers DG, Glucose stimulates proinsulin biosynthesis by a dose-dependent recruitment of pancreatic beta cells. Proc Natl Acad Sci USA 85: 3865-3869, 1988
83. Rudnick A, Ling TY, Odagiri H, Rutter WJ, German MS, Pancreatic beta cells express a diverse set of homeobox genes. Proc Natl Acad Sci USA 91: 12203-12207, 1994
84. Jensen J, Serup P, Karlsen C, Nielsen TF, Madsen OD, mRNA profiling of rat islet tumors reveals Nkx 6.1 as a B-cell-specific homeodomain transcription factor. J Biol Chem 271: 18749-18758, 1996
85. Emens LA, Landers DW, Moss LG, Hepatocyte nuclear factor 1 alpha is expressed in a hamster insulinoma line and transactivates the rat insulin I gene. Proc Natl Acad Sci USA 89: 7300-7304, 1992
86. Wang M, Drucker DJ, Activation of amylin gene transcription by the LIM domain homeobox gene isl-1. Mol Endocrinol 10: 243-251, 1996
87. Ahlgren U, Paff SL, Jessell TM, Edlund T, Edlund H, Independent requirement for Isl-1 in formation of pancreatic mesenchyme and islet cells. Nature 385: 257-260, 1997
88. Laser B, Meda P, Constant I, Philipps J, The caudal-related homeodomain protein Cdx-2/3 regulates glucagon gene expression in islet cells. J Biol Chem 271: 28984-28994, 1996
89. Umek RM, Friedman AD, McKnight SL, CCAAT-enhancer binding protein: a component of a differentiation switch. Science 251: 288-291, 1991
90. Zhang H-J, Walseth TF, Robertson RP, Insulin secretion and cAMP metabolism in HIT cells. Reciprocal and serial passage-dependent relationships. Diabetes 38: 44-48, 1989
91. Robertson RP, Zhang H-J, Pyzdrowski KL, Walseth TF, Preservation of insulin mRNA levels and insulin secretion in HIT cell by avoidance of chronic exposure to high glucose concentrations. J Clin Invest 90: 320-325, 1992
92. Bonner-Weir S, Baxter LA, Schuppin GT, Smith FE, A second pathway for regeneration of adult exocrine and endocrine pancreas. Diabetes 42: 1715-1720, 1993