Glucose regulation of islet stress responses and β-cell failure in type 2 diabetes

Diabetes, Obesity and Metabolism

Volumn 11, Issue SUPPL. 4, 2009, Pages 65-81

  Jonas, J C ^a   Bensellam, M ^a   Duprez, J ^a   Elouil, H ^a   Guiot, Y ^a   Pascal, S M A ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Apoptosis; Endoplasmic reticulum stress; Gene expression; Glucose deprivation; Glucotoxicity; Hyperglycaemia; Hypoglycaemia; Hypoxia; Insulin secretion; Integrated stress response; Oxidative stress; Phenotypic plasticity; Type 2 diabetes; Unfolded protein response

Indexed keywords

CYTOKINE; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

APOPTOSIS; ARTICLE; CELL GROWTH; CELL SURVIVAL; CYTOKINE PRODUCTION; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GLUCOSE INTOLERANCE; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PHENOTYPE;

ANIMALS; APOPTOSIS; CELL HYPOXIA; DIABETES MELLITUS, TYPE 2; DISEASE PROGRESSION; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GLUCOSE; HUMANS; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN-SECRETING CELLS; OXIDATIVE STRESS; RATS;

EID: 70350310991     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/j.1463-1326.2009.01112.x     Document Type: Article

References (97)

1. Kahn SE. The relative contributions of insulin resistance and β-cell dysfunction to the pathophysiology of Type 2 diabetes. Diabetologia 2003, 46:3-19.
2. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52:102-110.
3. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC. Pancreatic β-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 2008, 10(Suppl. 4):32-42.
4. Ahren B. Type 2 diabetes, insulin secretion and β-cell mass. Curr Mol Med 2005, 5:275-286.
5. Overview of 6 years' therapy of type II diabetes: a progressive disease. Diabetes 1995, 44:1249-1258. U.K. Prospective Diabetes Study 16.
6. Ferrannini E, Gastaldelli A, Miyazaki Y, Matsuda M, Mari A, DeFronzo RA. β-cell function in subjects spanning the range from normal glucose tolerance to overt diabetes: a new analysis. J Clin Endocrinol Metab 2005, 90:493-500.
7. Doria A, Patti ME, Kahn CR. The emerging genetic architecture of type 2 diabetes. Cell Metab 2008, 8:186-200.
8. Prentki M, Nolan CJ. Islet beta cell failure in type 2 diabetes. J Clin Invest 2006, 116:1802-1812.
9. Grill V, Bjorklund A. Impact of metabolic abnormalities for beta cell function: clinical significance and underlying mechanisms. Mol Cell Endocrinol 2009, 297:86-92.
10. Portha B, Lacraz G, Kergoat M. The GK rat beta-cell: a prototype for the diseased human beta-cell in type 2 diabetes?. Mol Cell Endocrinol 2009, 297:73-85.
11. Poitout V, Robertson RP. Glucolipotoxicity: fuel excess and β-cell dysfunction. Endocr Rev 2008, 29:351-366.
12. Donath MY, Ehses JA, Maedler K. Mechanisms of β-cell death in type 2 diabetes. Diabetes 2005, 54(Suppl. 2):S108-S113.
13. Cnop M, Welsh N, Jonas JC, Jorns A, Lenzen S, Eizirik DL. Mechanisms of pancreatic β-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 2005, 54(Suppl. 2):S97-S107.
14. Chang-Chen KJ, Mullur R, Bernal-Mizrachi E. β-cell failure as a complication of diabetes. Rev Endocr Metab Disord 2008, 9:329-343.
15. MacDonald PE, Joseph JW, Rorsman P. Glucose-sensing mechanisms in pancreatic β-cells. Philos Trans R Soc Lond B Biol Sci 2005, 360:2211-2225.
16. Henquin JC, Dufrane D, Nenquin M. Nutrient control of insulin secretion in isolated normal human islets. Diabetes 2006, 55:3470-3477.
17. Hinke SA, Hellemans K, Schuit FC. Plasticity of the β cell insulin secretory competence: preparing the pancreatic β cell for the next meal. J Physiol 2004, 558:369-380.
18. Schuit F, Flamez D, De Vos A, Pipeleers D. Glucose-regulated gene expression maintaining the glucose-responsive state of β-cells. Diabetes 2002, 51(Suppl. 3):S326-S332.
19. Blume N, Skouv J, Larsson LI, Holst JJ, Madsen OD. Potent inhibitory effects of transplantable rat glucagonomas and insulinomas on the respective endogenous islet cells are associated with pancreatic apoptosis. J Clin Invest 1995, 96:2227-2235.
20. Sempoux C, Guiot Y, Lefevre A. Neonatal hyperinsulinemic hypoglycemia: heterogeneity of the syndrome and keys for differential diagnosis. J Clin Endocrinol Metab 1998, 83:1455-1461.
21. Hoorens A, Van de Casteele M, Kl öppel G, Pipeleers DG. Glucose promotes survival of rat pancreatic β cells by activating synthesis of proteins which suppress a constitutive apoptotic program. J Clin Invest 1996, 98:1568-1574.
22. Efanova IB, Zaitsev SV, Zhivotovsky B. Glucose and tolbutamide induce apoptosis in pancreatic β-cells. A process dependent on intracellular Ca2+ concentration. J Biol Chem 1998, 273:33501-33507.
23. Srinivasan S, Bernal-Mizrachi E, Ohsugi M, Permutt MA. Glucose promotes pancreatic islet β-cell survival through a PI 3-kinase/Akt-signaling pathway. Am J Physiol Endocrinol Metab 2002, 283:E784-E793.
24. Van de Casteele M, Kefas BA, Cai Y. Prolonged culture in low glucose induces apoptosis of rat pancreatic β-cells through induction of c-myc. Biochem Biophys Res Commun 2003, 312:937-944.
25. Weir GC, Laybutt DR, Kaneto H, Bonner-Weir S, Sharma A. β-cell adaptation and decompensation during the progression of diabetes. Diabetes 2001, 50(Suppl. 1):S154-S159.
26. Jonas JC, Sharma A, Hasenkamp W. Chronic hyperglycemia triggers loss of pancreatic β cell differentiation in an animal model of diabetes. J Biol Chem 1999, 274:14112-14121.
27. Laybutt DR, Glandt M, Xu G. Critical reduction in β-cell mass results in two distinct outcomes over time. Adaptation with impaired glucose tolerance or decompensated diabetes. J Biol Chem 2003, 278:2997-3005.
28. Kjorholt C, Akerfeldt MC, Biden TJ, Laybutt DR. Chronic hyperglycemia, independent of plasma lipid levels, is sufficient for the loss of β-cell differentiation and secretory function in the db/db mouse model of diabetes. Diabetes 2005, 54:2755-2763.
29. Zraika S, Aston-Mourney K, Laybutt DR. The influence of genetic background on the induction of oxidative stress and impaired insulin secretion in mouse islets. Diabetologia 2006, 49:1254-1263.
30. Bensellam M, Van Lommel L, Overbergh L, Schuit FC, Jonas JC. Cluster analysis of rat pancreatic islet gene mRNA levels after culture in low-, intermediate- and high-glucose concentrations. Diabetologia 2009, 52:463-476.
31. Bolea S, Pertusa JA, Martin F, Sanchez-Andres JV, Soria B. Regulation of pancreatic β-cell electrical activity and insulin release by physiological amino acid concentrations. Pflugers Arch 1997, 433:699-704.
32. Ehses JA, Calderari S, Irminger JC. Islet Inflammation in type 2 diabetes (T2D): from endothelial to β-cell dysfunction. Curr Immunol Rev 2007, 3:216-232.
33. Alarcon C, Leahy JL, Schuppin GT, Rhodes CJ. 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 1995, 95:1032-1039.
34. Khaldi MZ, Guiot Y, Gilon P, Henquin JC, Jonas JC. Increased glucose sensitivity of both triggering and amplifying pathways of insulin secretion in rat islets cultured for one week in high glucose. Am J Physiol Endocrinol Metab 2004, 287:E207-E217.
35. Malaisse WJ. The beta cell in NIDDM: giving light to the blind. Diabetologia 1994, 37(Suppl. 2):S36-S42.
36. Leahy JL, Bumbalo LM, Chen C. β-cell hypersensitivity for glucose precedes loss of glucose-induced insulin secretion in 90% pancreatectomized rats. Diabetologia 1993, 36:1238-1244.
37. Laybutt DR, Sharma A, Sgroi DC, Gaudet J, Bonner-Weir S, Weir GC. Genetic regulation of metabolic pathways in β-cells disrupted by hyperglycemia. J Biol Chem 2002, 277:10912-10921.
38. Gunton JE, Kulkarni RN, Yim S. Loss of ARNT/HIF1β mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 2005, 122:337-349.
39. Dubois M, Vacher P, Roger B. Glucotoxicity inhibits late steps of insulin exocytosis. Endocrinology 2007, 148:1605-1614.
40. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ. Chop deletion reduces oxidative stress, improves β cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008, 118:3378-3389.
41. Chen J, Saxena G, Mungrue IN, Lusis AJ, Shalev A. Thioredoxin-interacting protein: a critical link between glucose toxicity and β-cell apoptosis. Diabetes 2008, 57:938-944.
42. Cardozo AK, Heimberg H, Heremans Y. A comprehensive analysis of cytokine-induced and nuclear factor- κB- dependent genes in primary rat pancreatic β-cells. J Biol Chem 2001, 276:48879-48886.
43. Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet β cells in diabetes. J Biol Chem 2004, 279:42351-42354.
44. Pirot P, Naamane N, Libert F. Global profiling of genes modified by endoplasmic reticulum stress in pancreatic beta cells reveals the early degradation of insulin mRNAs. Diabetologia 2007, 50:1006-1014.
45. Ainscow EK, Zhao C, Rutter GA. Acute overexpression of lactate dehydrogenase-A perturbs β-cell mitochondrial metabolism and insulin secretion. Diabetes 2000, 49:1149-1155.
46. Laybutt DR, Weir GC, Kaneto H. Overexpression of c-Myc in β-cells of transgenic mice causes proliferation and apoptosis, downregulation of insulin gene expression, and diabetes. Diabetes 2002, 51:1793-1804.
47. Kaneto H, Sharma A, Suzuma K. Induction of c-Myc expression suppresses insulin gene transcription by inhibiting NeuroD/BETA2-mediated transcriptional activation. J Biol Chem 2002, 277:12998-13006.
48. Pascal SM, Guiot Y, Pelengaris S, Khan M, Jonas JC. Effects of c-MYC activation on glucose stimulus-secretion coupling events in mouse pancreatic islets. Am J Physiol Endocrinol Metab 2008, 295:E92-102.
49. Shalev A. Lack of TXNIP protects β-cells against glucotoxicity. Biochem Soc Trans 2008, 36:963-965.
50. Tobiasch E, Gunther L, Bach FH. Heme oxygenase-1 protects pancreatic β cells from apoptosis caused by various stimuli. J Investig Med 2001, 49:566-571.
51. Tanaka Y, Tran PO, Harmon J, Robertson RP. A role for glutathione peroxidase in protecting pancreatic β cells against oxidative stress in a model of glucose toxicity. Proc Natl Acad Sci U S A 2002, 99:12363-12368.
52. Laybutt DR, Kaneto H, Hasenkamp W. Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to β-cell survival during chronic hyperglycemia. Diabetes 2002, 51:413-423.
53. Jonas JC, Laybutt DR, Steil GM. High glucose stimulates early response gene c-Myc expression in rat pancreatic β cells. J Biol Chem 2001, 276:35375-35381.
54. Hartman MG, Lu D, Kim ML. Role for activating transcription factor 3 in stress-induced β-cell apoptosis. Mol Cell Biol 2004, 24:5721-5732.
55. Laybutt DR, Preston AM, Akerfeldt MC. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 2007, 50:752-763.
56. Elouil H, Cardozo AK, Eizirik DL, Henquin JC, Jonas JC. High glucose and hydrogen peroxide increase c-Myc and haeme-oxygenase 1 mRNA levels in rat pancreatic islets without activating NFκB. Diabetologia 2005, 48:496-505.
57. Khaldi MZ, Elouil H, Guiot Y, Henquin JC, Jonas JC. The antioxidants N-acetyl-L-cysteine and manganese(III)tetrakis (4-benzoic acid)porphyrin do not prevent β-cell dysfunction in rat islets cultured in high glucose for 1 wk. Am J Physiol Endocrinol Metab 2006, 291:E137-E146.
58. Elouil H, Bensellam M, Guiot Y. Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia 2007, 50:1442-1452.
59. Li X, Zhang L, Meshinchi S. Islet microvasculature in islet hyperplasia and failure in a model of type 2 diabetes. Diabetes 2006, 55:2965-2973.
60. Scheuner D, Kaufman RJ. The unfolded protein response: a pathway that links insulin demand with β-cell failure and diabetes. Endocr Rev 2008, 29:317-333.
61. Jonas JC, Guiot Y, Rahier J, Henquin JC. Haeme-oxygenase 1 expression in rat pancreatic beta-cells is stimulated by supraphysiological glucose concentrations and by cyclic AMP. Diabetologia 2003, 46:1234-1244.
62. Paraskevas S, Aikin R, Maysinger D. Activation and expression of ERK, JNK, and p38 MAP-kinases in isolated islets of Langerhans: implications for cultured islet survival. FEBS Lett 1999, 455:203-208.
63. Ling Z, Kiekens R, Mahler T. Effects of chronically elevated glucose levels on the functional properties of rat pancreatic β-cells. Diabetes 1996, 45:1774-1782.
64. Bensellam M, Jonas JC. High glucose activates hypoxia inducible factors 1 and 2 in cultured rat islets and INS1-E cell monolayers. Diabetologia 2008, 51(Suppl. 1):S94.
65. Tiedge M, Lortz S, Drinkgern J, Lenzen S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 1997, 46:1733-1742.
66. Bindokas VP, Kuznetsov A, Sreenan S, Polonsky KS, Roe MW, Philipson LH. Visualizing superoxide production in normal and diabetic rat islets of Langerhans. J Biol Chem 2003, 278:9796-9801.
67. Hou ZQ, Li HL, Gao L, Pan L, Zhao JJ, Li GW. Involvement of chronic stresses in rat islet and INS-1 cell glucotoxicity induced by intermittent high glucose. Mol Cell Endocrinol 2008, 291:71-78.
68. Ihara Y, Toyokuni S, Uchida K. Hyperglycemia causes oxidative stress in pancreatic β-cells of GK rats, a model of type 2 diabetes. Diabetes 1999, 48:927-932.
69. Sakuraba H, Mizukami H, Yagihashi N, Wada R, Hanyu C, Yagihashi S. Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese Type II diabetic patients. Diabetologia 2002, 45:85-96.
70. Martens GA, Cai Y, Hinke S, Stange G, Van de Casteele M, Pipeleers D. Glucose suppresses superoxide generation in metabolically responsive pancreatic β cells. J Biol Chem 2005, 280:20389-20396.
71. Alam J, Cook JL. How many transcription factors does it take to turn on the heme oxygenase-1 gene?. Am J Respir Cell Mol Biol 2007, 36:166-174.
72. Hou N, Torii S, Saito N, Hosaka M, Takeuchi T. Reactive oxygen species-mediated pancreatic β-cell death is regulated by interactions between stress-activated protein kinases, p38 and c-Jun N-terminal kinase, and mitogen-activated protein kinase phosphatases. Endocrinology 2008, 149:1654-1665.
73. Kaneto H, Kawamori D, Nakatani Y, Gorogawa S, Matsuoka TA. Oxidative stress and the JNK pathway as a potential therapeutic target for diabetes. Drug News Perspect 2004, 17:447-453.
74. Robertson RP, Harmon JS. Pancreatic islet β-cell and oxidative stress: the importance of glutathione peroxidase. FEBS Lett 2007, 581:3743-3748.
75. Tang C, Han P, Oprescu AI. Evidence for a role of superoxide generation in glucose-induced β-cell dysfunction in vivo. Diabetes 2007, 56:2722-2731.
76. Harding HP, Zhang Y, Zeng H. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003, 11:619-633.
77. Lipson KL, Fonseca SG, Ishigaki S. Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 2006, 4:245-254.
78. Marchetti P, Bugliani M, Lupi R. The endoplasmic reticulum in pancreatic beta cells of type 2 diabetes patients. Diabetologia 2007, 50:2486-2494.
79. Huang CJ, Lin CY, Haataja L. High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress mediated β-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 2007, 56:2016-2027.
80. Akerfeldt MC, Howes J, Chan JY. Cytokine-induced β-cell death is independent of endoplasmic reticulum stress signaling. Diabetes 2008, 57:3034-3044.
81. Greenman IC, Gomez E, Moore CE, Herbert TP. Distinct glucose-dependent stress responses revealed by translational profiling in pancreatic β-cells. J Endocrinol 2007, 192:179-187.
82. Vander Mierde D, Scheuner D, Quintens R. Glucose activates a protein phosphatase-1-mediated signaling pathway to enhance overall translation in pancreatic β-cells. Endocrinology 2007, 148:609-617.
83. Martens GA, Van de Casteele M. Glycemic control of apoptosis in the pancreatic beta cell: danger of extremes?. Antioxid Redox Signal 2007, 9:309-317.
84. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008, 29:42-61.
85. Boni-Schnetzler M, Thorne J, Parnaud G. Increased interleukin (IL)-1β messenger ribonucleic acid expression in b-cells of individuals with type 2 diabetes and regulation of IL-1β in human islets by glucose and autostimulation. J Clin Endocrinol Metab 2008, 93:4065-4074.
86. Larsen CM, Faulenbach M, Vaag A. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 2007, 356:1517-1526.
87. Taylor CT. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J 2008, 409:19-26.
88. Zehetner J, Danzer C, Collins S. pVHL is a regulator of glucose metabolism and insulin secretion in pancreatic β cells. Genes Dev 2008, 22:3135-3146.
89. Hosokawa H, Hosokawa YA, Leahy JL. Upregulated hexokinase activity in isolated islets from diabetic 90% pancreatectomized rats. Diabetes 1995, 44:1328-1333.
90. Roche E, Assimacopoulos-Jeannet F, Witters LA. Induction by glucose of genes coding for glycolytic enzymes in a pancreatic β-cell line (INS-1). J Biol Chem 1997, 272:3091-3098.
91. Nesher R, Warwar N, Khan A, Efendic S, Cerasi E, Kaiser N. Defective stimulus-secretion coupling in islets of Psammomys obesus, an animal model for type 2 diabetes. Diabetes 2001, 50:308-314.
92. Jung SK, Gorski W, Aspinwall CA, Kauri LM, Kennedy RT. Oxygen microsensor and its application to single cells and mouse pancreatic islets. Anal Chem 1999, 71:3642-3649.
93. Carlsson PO, Liss P, Andersson A, Jansson L. Measurements of oxygen tension in native and transplanted rat pancreatic islets. Diabetes 1998, 47:1027-1032.
94. Carlsson PO, Andersson A, Jansson L. Pancreatic islet blood flow in normal and obese-hyperglycemic (ob/ob) mice. Am J Physiol Endocrinol Metab 1996, 271:E990-E995.
95. Iwase M, Uchizono Y, Tashiro K, Goto D, Iida M. Islet hyperperfusion during prediabetic phase in OLETF rats, a model of type 2 diabetes. Diabetes 2002, 51:2530-2535.
96. Carlsson PO, Andersson A, Jansson L. Influence of age, hyperglycemia, leptin, and NPY on islet blood flow in obese-hyperglycemic mice. Am J Physiol Endocrinol Metab 1998, 275:E594-E601.
97. Leonard MO, Kieran NE, Howell K. Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in isch-emia-reperfusion injury. FASEB J 2006, 20:2624-2626.