Glucolipotoxicity age-dependently impairs beta cell function in rats despite a marked increase in beta cell mass

Diabetologia

Volumn 53, Issue 11, 2010, Pages 2369-2379

  Fontes G ^a,b   Zarrouki, B ^a,b   Hagman, D K ^a,b,f   Latour, M G ^a,b   Semache, M ^a,b   Roskens, V ^d   Moore, P C ^e   Prentki, M ^a,b,c   Rhodes, C J ^e   Jetton, T L ^d   Poitout, V ^a,b,c  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY OF MONTREAL   (Canada)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^e Fred Hutchinson Cancer Research Center ^*  (United States)

^f Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Ageing; Biosynthesis; Gene expression; Glucose clamp; Hyperglycaemia; Hyperlipidaemia; Insulin; Islets of Langerhans

Indexed keywords

C PEPTIDE; GLUCOSE; LIPID EMULSION; PROINSULIN;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION; HYPERINSULINEMIA; INSULIN RELEASE; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN SYNTHESIS; MALE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; FATTY ACIDS; GLUCOSE; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN-SECRETING CELLS; MALE; PROINSULIN; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77957655499     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-1850-5     Document Type: Article

References (50)

1. M Prentki CJ Nolan 2006 Islet beta cell failure in type 2 diabetes J Clin Invest 116 1802 1812 1:CAS:528:DC%2BD28XmvV2ltLs%3D 10.1172/JCI29103 16823478 (Pubitemid 44033300)
2. RP Robertson 2004 Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes J Biol Chem 279 42351 42354 1:CAS:528:DC%2BD2cXotVOhurw%3D 10.1074/jbc.R400019200 15258147 (Pubitemid 39372114)
3. RH Unger 1995 Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications Diabetes 44 863 870 1:CAS:528:DyaK2MXnsVSnsbo%3D 10.2337/diabetes.44.8.863 7621989
4. M Prentki BE Corkey 1996 Are the -cell signaling molecules malonyl-CoA and cytosolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45 273 283 1:CAS:528:DyaK28XjslSnu74%3D 10.2337/diabetes.45.3.273 8593930
5. V Poitout RP Robertson 2002 Minireview: secondary beta-cell failure in type 2 diabetes-a convergence of glucotoxicity and lipotoxicity Endocrinology 143 339 342 1:CAS:528:DC%2BD38XosFWltg%3D%3D 10.1210/en.143.2.339 11796484 (Pubitemid 34107184)
6. TM Mason T Goh V Tchipashvili, et al. 1999 Prolonged elevation of plasma free fatty acids desensitizes the insulin secretory response to glucose in vivo in rats Diabetes 48 524 530 1:CAS:528:DyaK1MXhsFymtr8%3D 10.2337/diabetes.48.3. 524 10078552
7. TT Goh TM Mason N Gupta, et al. 2007 Lipid-induced beta-cell dysfunction in vivo in models of progressive beta-cell failure Am J Physiol Endocrinol Metab 292 E549 E560 1:CAS:528:DC%2BD2sXjt1GlsLs%3D 10.1152/ajpendo.00255.2006 17003242 (Pubitemid 46220580)
8. AI Oprescu G Bikopoulos A Naassan, et al. 2007 Free fatty acid-induced reduction in glucose-stimulated insulin secretion: evidence for a role of oxidative stress in vitro and in vivo Diabetes 56 2927 2937 1:CAS:528: DC%2BD2sXhsValurrJ 10.2337/db07-0075 17717282 (Pubitemid 350223627)
9. Y Sako VE Grill 1990 A 48-hour lipid infusion in the rat time-dependently inhibits glucose-induced insulin secretion and -cell oxidation through a process likely coupled to fatty acid oxidation Endocrinology 127 1580 1589 1:CAS:528:DyaK3cXlvVGisrs%3D 10.1210/endo-127-4-1580 1698143
10. C Magnan S Collins MF Berthault, et al. 1999 Lipid infusion lowers sympathetic nervous activity and leads to increased beta-cell responsiveness to glucose J Clin Invest 103 413 419 1:CAS:528:DyaK1MXovVKmug%3D%3D 10.1172/JCI3883 9927503
11. GM Steil N Trivedi JC Jonas, et al. 2001 Adaptation of beta-cell mass to substrate oversupply: enhanced function with normal gene expression Am J Physiol Endocrinol Metab 280 E788 E796 1:CAS:528:DC%2BD3MXjsVahsL4%3D 11287362
12. DK Hagman MG Latour SK Chakrabarti, et al. 2008 Cyclical and alternating infusions of glucose and intralipid in rats inhibit insulin gene expression and Pdx-1 binding in islets Diabetes 57 424 431 1:CAS:528:DC%2BD1cXhvVOkt7g%3D 10.2337/db07-1285 17991758
13. KM Utzschneider DB Carr RL Hull, et al. 2004 Impact of intra-abdominal fat and age on insulin sensitivity and -cell function Diabetes 53 2867 2872 1:CAS:528:DC%2BD2cXpvV2itL8%3D 10.2337/diabetes.53.11.2867 15504967 (Pubitemid 39425912)
14. CL Kelpe LM Johnson V Poitout 2002 Increasing triglyceride synthesis inhibits glucose-induced insulin secretion in isolated rat islets of Langerhans. A study using adenoviral expression of diacylglycerol acyltransferase Endocrinology 143 3326 3332 1:CAS:528:DC%2BD38XmsVSgtL0%3D 10.1210/en.2002- 220402 12193544
15. LC Bollheimer RH Skelly MW Chester JD McGarry CJ Rhodes 1998 Chronic exposure to free fatty acid reduces pancreatic beta cell insulin content by increasing basal insulin secretion that is not compensated for by a corresponding increase in proinsulin biosynthesis translation J Clin Invest 101 1094 1101 1:CAS:528:DyaK1cXhs1yqsLY%3D 10.1172/JCI420 9486980
16. TL Jetton J Lausier K LaRock, et al. 2005 Mechanisms of compensatory beta-cell growth in insulin-resistant rats: roles of Akt kinase Diabetes 54 2294 2304 1:CAS:528:DC%2BD2MXnt1ynsbg%3D 10.2337/diabetes.54.8.2294 16046294 (Pubitemid 41134255)
17. WS Zawalich H Yamazaki KC Zawalich 2008 Biphasic insulin secretion from freshly isolated or cultured, perifused rodent islets: comparative studies with rats and mice Metabolism 57 30 39 1:CAS:528:DC%2BD2sXhsVeqtb3F 10.1016/j.metabol.2007.07.020 18078856 (Pubitemid 350234971)
18. H Lottmann J Vanselow B Hessabi R Walther 2001 The Tet-On system in transgenic mice: inhibition of the mouse pdx-1 gene activity by antisense RNA expression in pancreatic beta-cells J Mol Med 79 321 328 1:CAS:528: DC%2BD3MXlslWgtLw%3D 10.1007/s001090100229 11485027 (Pubitemid 32646390)
19. G Fontes M Semache DK Hagman, et al. 2009 Involvement of Per-Arnt-Sim kinase and extracellular-regulated kinases-1/2 in palmitate inhibition of insulin gene expression in pancreatic beta-cells Diabetes 58 2048 2058 1:CAS:528:DC%2BD1MXhtFChsbbM 10.2337/db08-0579 19502418
20. MC Lawrence K McGlynn BH Park MH Cobb 2005 ERK1/2-dependent activation of transcription factors required for acute and chronic effects of glucose on the insulin gene promoter J Biol Chem 280 26751 26759 1:CAS:528:DC%2BD2MXmt1Ggs7s%3D 10.1074/jbc.M503158200 15899886 (Pubitemid 41040708)
21. Y Sako VE Grill 1990 Coupling of -cell desensitization by hyperglycemia to excessive stimulation and circulating insulin in glucose-infused rats Diabetes 39 1580 1583 1:CAS:528:DyaK3MXitVSjtr0%3D 10.2337/diabetes.39.12.1580 2245882
22. C Bernard C Thibault MF Berthault, et al. 1998 Pancreatic beta-cell regeneration after 48-h glucose infusion in mildly diabetic rats is not correlated with functional improvement Diabetes 47 1058 1065 1:CAS:528:DyaK1cXkt1ajtbc%3D 10.2337/diabetes.47.7.1058 9648829 (Pubitemid 28294548)
23. CJ de Souza JV Capotorto S Cornell-Kennon, et al. 2000 Beta-cell dysfunction in 48-hour glucose-infused rats is not a consequence of elevated plasma lipid or islet triglyceride levels Metabolism 49 755 759 10.1053/meta.2000.6240 10877202
24. M Paris C Bernard-Kargar MF Berthault L Bouwens A Ktorza 2003 Specific and combined effects of insulin and glucose on functional pancreatic beta-cell mass in vivo in adult rats Endocrinology 144 2717 2727 1:CAS:528: DC%2BD3sXktFegsLw%3D 10.1210/en.2002-221112 12746336 (Pubitemid 36629925)
25. BG Topp MD McArthur DT Finegood 2004 Metabolic adaptations to chronic glucose infusion in rats Diabetologia 47 1602 1610 1:CAS:528: DC%2BD2cXotVGgu7c%3D 10.1007/s00125-004-1493-5 15349726 (Pubitemid 39371643)
26. G Boden X Chen J Rosner M Barton 1995 Effects of a 48 h fat infusion on insulin secretion and glucose utilization Diabetes 44 1239 1242 1:CAS:528:DyaK2MXotlGgsro%3D 10.2337/diabetes.44.10.1239 7556964
27. CB Jensen H Storgaard JJ Holst F Dela S Madsbad AA Vaag 2003 Insulin secretion and cellular glucose metabolism after prolonged low-grade intralipid infusion in young men J Clin Endocrinol Metab 88 2775 2783 1:CAS:528: DC%2BD3sXkslCrsLs%3D 10.1210/jc.2002-021430 12788887
28. S Kashyap R Belfort A Gastaldelli, et al. 2003 A sustained increase in plasma free fatty acids impairs insulin secretion in nondiabetic subjects genetically predisposed to develop type 2 diabetes Diabetes 52 2461 2474 1:CAS:528:DC%2BD3sXotVWhs7k%3D 10.2337/diabetes.52.10.2461 14514628 (Pubitemid 37210533)
29. A Carpentier SD Mittelman RN Bergman A Giacca GF Lewis 2000 Prolonged elevation of plasma free fatty acids impairs pancreatic beta-cell function in obese nondiabetic humans but not in individuals with type 2 diabetes Diabetes 49 399 408 1:CAS:528:DC%2BD3cXlsFCru7s%3D 10.2337/diabetes.49.3.399 10868961
30. A Carpentier A Giacca GF Lewis 2001 Effect of increased plasma non-esterified fatty acids (NEFAs) on arginine-stimulated insulin secretion in obese humans Diabetologia 44 1989 1997 1:CAS:528:DC%2BD38XisFGmtw%3D%3D 10.1007/s001250100002 11719829 (Pubitemid 33124043)
31. N Leung T Sakaue A Carpentier K Uffelman A Giacca GF Lewis 2004 Prolonged increase of plasma non-esterified fatty acids fully abolishes the stimulatory effect of 24 hours of moderate hyperglycaemia on insulin sensitivity and pancreatic beta-cell function in obese men Diabetologia 47 204 213 1:CAS:528:DC%2BD2cXjtFCktb0%3D 10.1007/s00125-003-1301-7 14712348 (Pubitemid 38315356)
32. AC Carpentier A Bourbonnais F Frisch A Giacca GF Lewis 2010 Plasma nonesterified fatty acid intolerance and hyperglycemia are associated with intravenous lipid-induced impairment of insulin sensitivity and disposition index J Clin Endocrinol Metab 95 1256 1264 1:CAS:528:DC%2BC3cXjs1Kqt7s%3D 10.1210/jc.2009-1932 20097711
33. K Maedler GA Spinas D Dyntar W Moritz N Kaiser MY Donath 2001 Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function Diabetes 50 69 76 1:CAS:528:DC%2BD3MXis1Ontg%3D%3D 10.2337/diabetes.50. 1.69 11147797
34. R Lupi F Dotta L Marselli, et al. 2002 Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated Diabetes 51 1437 1442 1:CAS:528: DC%2BD38XjtlGmtL4%3D 10.2337/diabetes.51.5.1437 11978640
35. S Piro M Anello C Di Pietro, et al. 2002 Chronic exposure to free fatty acids or high glucose induces apoptosis in rat pancreatic islets: possible role of oxidative stress Metabolism 51 1340 1347 1:CAS:528:DC%2BD38XnvFGru78%3D 10.1053/meta.2002.35200 12370856 (Pubitemid 35174157)
36. W El-Assaad J Buteau ML Peyot, et al. 2003 Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death Endocrinology 144 4154 4163 1:CAS:528:DC%2BD3sXmvFWrsb4%3D 10.1210/en.2003-0410 12933690 (Pubitemid 37088771)
37. I Kharroubi L Ladriere AK Cardozo Z Dogusan M Cnop DL Eizirik 2004 Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress Endocrinology 145 5087 5096 1:CAS:528:DC%2BD2cXptVyhurs%3D 10.1210/en.2004-0478 15297438 (Pubitemid 39551129)
38. DR Laybutt AM Preston MC Akerfeldt, et al. 2007 Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes Diabetologia 50 752 763 1:CAS:528:DC%2BD2sXitlOntL0%3D 10.1007/s00125-006-0590-z 17268797 (Pubitemid 46355827)
39. S Jacqueminet I Briaud C Rouault G Reach V Poitout 2000 Inhibition of insulin gene expression by long-term exposure of pancreatic beta-cells to palmitate is dependent upon the presence of a stimulatory glucose concentration Metabolism 49 532 536 1:CAS:528:DC%2BD3cXisVeqsr0%3D 10.1016/S0026-0495(00) 80021-9 10778881
40. I Briaud JS Harmon CL Kelpe VB Segu V Poitout 2001 Lipotoxicity of the pancreatic beta-cell is associated with glucose-dependent esterification of fatty acids into neutral lipids Diabetes 50 315 321 1:CAS:528: DC%2BD3MXhtVOgsrc%3D 10.2337/diabetes.50.2.315 11272142
41. CL Kelpe PC Moore SD Parazzoli B Wicksteed CJ Rhodes V Poitout 2003 Palmitate inhibition of insulin gene expression is mediated at the transcriptional level via ceramide synthesis J Biol Chem 278 30015 30021 1:CAS:528:DC%2BD3sXlvFOnt74%3D 10.1074/jbc.M302548200 12771145 (Pubitemid 36962391)
42. DK Hagman LB Hays SD Parazzoli V Poitout 2005 Palmitate inhibits insulin gene expression by altering PDX-1 nuclear localization and reducing MafA expression in isolated rat islets of Langerhans J Biol Chem 280 32413 32418 1:CAS:528:DC%2BD2MXpvVyqtLs%3D 10.1074/jbc.M506000200 15944145 (Pubitemid 41361852)
43. ER Seaquist RP Robertson 1992 Effects of hemipancreatectomy on pancreatic alpha and beta cell function in healthy human donors J Clin Invest 89 1761 1766 1:CAS:528:DyaK38XksVGrt7k%3D 10.1172/JCI115779 1601986
44. MM Rankin JA Kushner 2009 Adaptive beta-cell proliferation is severely restricted with advanced age Diabetes 58 1365 1372 1:CAS:528: DC%2BD1MXntFanurY%3D 10.2337/db08-1198 19265026
45. SI Tschen S Dhawan T Gurlo A Bhushan 2009 Age-dependent decline in beta-cell proliferation restricts the capacity of beta-cell regeneration in mice Diabetes 58 1312 1320 1:CAS:528:DC%2BD1MXntFanurw%3D 10.2337/db08-1651 19228811
46. ZV Wang J Mu TD Schraw, et al. 2008 PANIC-ATTAC: a mouse model for inducible and reversible beta-cell ablation Diabetes 57 2137 2148 1:CAS:528:DC%2BD1cXps1Ois7c%3D 10.2337/db07-1631 18469203
47. C Kargar A Ktorza 2008 Anatomical versus functional beta-cell mass in experimental diabetes Diabetes Obes Metab 10 Suppl 4 43 53 1:CAS:528: DC%2BD1cXhsVeqsb7O 10.1111/j.1463-1326.2008.00940.x 18834432
48. V Delghingaro-Augusto CJ Nolan D Gupta, 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 1:CAS:528:DC%2BD1MXlt1Gqt7Y%3D 10.1007/s00125-009-1317-8 19294363
49. RN Kulkarni US Jhala JN Winnay S Krajewski M Montminy CR Kahn 2004 PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance J Clin Invest 114 828 836 1:CAS:528: DC%2BD2cXnslWiurc%3D 15372107
50. MM Sachdeva KC Claiborn C Khoo, et al. 2009 Pdx1 (MODY4) regulates pancreatic beta cell susceptibility to ER stress Proc Natl Acad Sci U S A 106 19090 19095 1:CAS:528:DC%2BD1MXhsFGlsbnE 10.1073/pnas.0904849106 19855005