Islet inflammation impairs the pancreatic B-ceII in type 2 diabetes

Physiology

Volumn 24, Issue 6, 2009, Pages 325-331

  Donath, Marc Y ^a   Böni Schnetzler, Marianne ^a   Ellingsgaard, Helga ^a   Ehses, Jan A ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ANIMAL; HUMAN; IMMUNOLOGY; INFLAMMATION; INSULIN RESISTANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PATHOLOGY; REVIEW;

ANIMALS; CYTOKINES; DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN RESISTANCE; INSULIN-SECRETING CELLS;

EID: 73949126369     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00032.2009     Document Type: Review

References (71)

1. Boni-Schnetzler M, Boller S, Debray S, Bouzakri K, Meier DT, Prazak R, Kerr-Conte J, Pattou F, Ehses JA, Schuit FC, Donath MY. Free fatty acids induce a pro-inflammatory response in islets via the abundantly expressed interleukin-1 receptor I. Endocrinology. In press.
2. Boni-Schnetzler M, Thorne J, Parnaud G, Marselli L, Ehses JA, Kerr-Conte J, Pattou F, Halban PA, Weir GC, Donath MY. Increased interleukin (IL)-I beta messenger ribonucleic acid expression in beta-cells of individuals with Type 2 diabetes and regulation of IL-1 beta in human islets by glucose and autostimulation. J Clin Endocrinol Metab 93: 4065-4074, 2008.
3. Bonner-Weir S. Islet growth and development in the adult. J Mol Endocrinol 24: 297-302, 2000.
4. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferreres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772, 2007.
5. Cerasi E, Luft R. Insulin response to glucose infusion in diabetic and non-diabetic monozygotic twin pairs. Genetic control of insulin response? Acta Endocrinol 55: 330-345, 1967.
6. Cheng N, He R, Tian J, Ye PP, Ye RD. Cutting edge: TLR2 is a functional receptor for acute-phase serum amyloid A. J Immunol 181: 22-26, 2008.
7. Creely SJ, McTernan PG, Kusminski CM, Fisher M, Da Silva NF, Khanolkar M, Evans M, Harte AL, Kumar S. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and Type 2 diabetes. Am J Physiol Endocrinol Metab 292: E740-E747, 2007.
8. Dasu MR, Devaraj S, Jialal I. High glucose induces IL-1 beta expression in human monocytes: mechanistic insights. Am J Physiol Endocrinol Metab 293: E337-E346, 2007.
9. Dayer-Metroz MD, Wollheim CB, Seckinger P, Dayer JM. A natural interleukin 1 (IL-1) inhibitor counteracts the inhibitory effect of IL-1 on insulin production in cultured rat pancreatic islets. J Autoimmun 2: 163-171, 1989.
10. Deng S, Vatamaniuk M, Huang X, Doliba N, Lian MM, Frank A, Velidedeoglu E, Desai NM, Koeberlein B, Wolf B, Barker CF, Naji A, Matschinsky FM, Markmann JF. Structural and functional abnormalities in the islets isolated from Type 2 diabetic subjects. Diabetes 53: 624-632, 2004.
11. Di Gregorio GB, Hensley L, Lu T, Ranganathan G, Kern PA. Lipid and carbohydrate metabolism in mice with a targeted mutation in the IL-6 gene: absence of development of agerelated obesity. Am J Physiol Endocrinol Metab 287: E182-E187, 2004.
12. Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 27: 519-550, 2009.
13. Donath MY, Ehses JA, Maedler K, Schumann DM, Ellingsgaard H, Eppler E, Reinecke M. Mechanisms of betacell death in Type 2 diabetes. Diabetes 54, Suppl 2: S108-S113, 2005.
14. Donath MY, Gross DJ, Cerasi E, Kaiser N. Hyperglycemiainduced beta-cell apoptosis in pancreatic islets of Psammomys obesus during development of diabetes. Diabetes 48: 738-744, 1999.
15. Donath MY, Mandrup-Poulsen T. The use of interleukin-1receptor antagonists in the treatment of diabetes mellitus. Nat Clin Pract Endocrinol Metab 4: 240-241, 2008.
16. Donath MY, Schumann DM, Faulenbach M, Ellingsgaard H, Rütti S, Perren A, Böni-Schnetzler M, Ehses JA. Islet inflammation in Type 2 diabetes: from metabolic stress to therapy. Diabetes Care31:S161-S164, 2008.
17. Donath MY, Starling J, Maedler K, MandrupPoulsen T. Inflammatory mediators and islet betacell failure: a link between Type 1 and Type 2 diabetes. J Mol Med 81: 455-470, 2003.
18. Donath MY, Weder C, Whitmore J, Bauer RJ, Der K, Scannon PJ, Dinarello C, Solinger AM. XOMA 052, an anti-IL-1 beta antibody, in a double-blind, placebo-controlled, dose escalation study of the safety and pharmacokinetics in patients with Type 2 diabets mellitus: a new approach to therapy. Diabetologia 51 : S7, 2008.
19. Ehses JA, Ellingsgaard H, Boni-Schnetzler M, Donath MY. Pancreatic islet inflammation in Type 2 diabetes: from alpha and beta cell compensation to dysfunction. Arch Physiol Biochem 115: 240-247, 2009.
20. Ehses JA, lacraz G, Giroix MH, Schmidlin F, Coulaud J, Kassis N, lrminger JC, Kergoat M, Portha B, Homo-Delarche F, Donath MY. IL1 antagonism reduces hyperglycemia and tissue inflammation in the Type 2 diabetic GK rat. Proc Natl Acad Sci USA 106: 13998-14003, 2009.
21. Ehses JA, Perren A, Eppler E, Ribaux P, Pospisilik JA, Maor-Cahn R, Gueripel X, Ellingsgaard H, Schneider MK, Biollaz G, Fontana A, Reinecke M, Homo-Delarche F, Donath MY. Increased number of islet-associated macrophages in Type 2 diabetes. Diabetes 56: 2356-2370, 2007.
22. Ellingsgaard H, Ehses JA, Hammar EB, Van Lommel L, Quintens R, Martens G, Kerr-Conte J, Pattou F, Berney T, Pipeleers D, Halban PA, Schuit FC, Donath MY. lnterleukin-6 regulates pancreatic alpha-cell mass expansion. Proc Natl Acad Sci USA 105: 13163-13168,2008.
23. Febbraio MA, Pedersen BK. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 16: 1335-1347, 2002.
24. Fei H, Zhao B, Zhao S, Wang Q. Requirements of calcium fluxes and ERK kinase activation for glucose- and interleukin-1 beta-induced beta-cell apoptosis. Mol Cell Biochem 315: 75-84, 2008.
25. Gelling RW, Vuguin PM, Du XQ, Cui L, Romer J, Pederson RA, Leiser M, Sorensen H, Holst JJ, Fledelius C, Johansen PB, Fleischer N, Mcintosh CH, Nishimura E, Charron MJ. Pancreatic beta-cell overexpression of the glucagon receptor gene results in enhanced beta-cell function and mass. Am J Physiol Endocrinol Metab 297: E695-E707, 2009.
26. Guardado-Mendoza R, Davalli AM, Chavez AO, Hubbard GB, Dick EJ, Majluf-Cruz A, Tene-Perez CE, Goldschmidt L, Hart J, Perego C, Comuzzie AG, Tejero ME, Finzi G, Placidi C, La Rosa S, Capella C, HaIfF G, Gastaldelli A, DeFronzo RA, Folli F. Pancreatic islet amyloidosis, beta-cell apoptosis, and alpha-cell proliferation are determinants of islet remodeling in Type-2 diabetic baboons. Proc Natl Acad Sci USA 106: 13992-13997,2009.
27. Hammar EB, lrminger JC, Rickenbach K, Parnaud G, Ribaux P, Bosco D, Rouiller DG, Halban PA. Activation of NF-kappaB by extracellular matrix is involved in spreading and glucose-stimulated insulin secretion of pancreatic beta cells. J Biol Chem 280: 30630-30637, 2005.
28. Harding HP, Ron D. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51, Suppl 3: S455-S461, 2002.
29. Haversen L, Danielsson KN, Fogelstrand L, Wiklund O. Induction of proinflammatory cytokines by longchain saturated fatty acids in human macrophages. Atherosclerosis 202: 382-393, 2009.
30. Herder C, Haastert B, Muller-Scholze S, Koenig W, Thorand B, Holle R, Wichmann HE, Scherbaum WA, Martin S, Kolb H. Association of systemic chemokine concentrations with impaired glucose tolerance and Type 2 diabetes: results from the Cooperative Health Research in the Region of Augsburg Survey S4 (KORA S4). Diabetes 54, Suppl 2: S11-S17, 2005.
31. Hotamisligil GS, Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 8: 923-934, 2008.
32. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factoralpha: direct role in obesity-linked insulin resistance. Science 259: 87-91, 1993.
33. Hull RL, Westermark GT, Westermark P, Kahn SE. Islet amyloid: a critical entity in the pathogenesis of Type 2 diabetes. J Clin Endocrinol Metab 89: 3629-3643, 2004.
34. Kahn BB. Type 2 diabetes: when insulin secretion fails to compensate for insulin resistance. Cell 92: 593-596, 1998.
35. Kristiansen OP, Mandrup-Poulsen T. lnterleukin-6 and diabetes: the good, the bad, or the indifferent? Diabetes 54, Suppl 2: S114-S124, 2005.
36. Lacraz G, Giroix MH, Kassis N, Coulaud J, Galinier A, Noll C, Cornut M, Schmidlin F, Paul JL, Janel N, lrminger JC, Kergoat M, Portha B, Donath MY, Ehses JA, Homo-Delarche F. Islet endothelial activation and oxidative stress gene expression is reduced by IL-1 Ra treatment in the Type 2 diabetic GK rat. PLoS ONE 4: e6963, 2009.
37. Larsen CM, Faulenbach M, Vaag A, Ehses JA, Donath MY, Mandrup-Poulsen T. Sustained effects of interleukin-1-receptor antagonist treatment in Type 2 diabetes mellitus. Diabetes Care 32: 1663-1668,2009.
38. Larsen CM, Faulenbach M, Vaag A, Volund A, Ehses JA, Seifert B, Mandrup-Poulsen T, Donath MY. Interleukin-1-receptor antagonist in Type 2 diabetes mellitus. N Engl J Med 356: 1517-1526, 2007.
39. Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem 276: 16683-16689,2001.
40. Li X, Zhang L, Meshinchi S, Dias-Leme C, Raffln D, Johnson JD, Treutelaar MK, Burant CF. Islet microvasculature in islet hyperplasia and failure in a model of Type 2 diabetes. Diabetes 55: 2965-2973, 2006.
41. Maedler K, Fontana A, Ris F, Sergeev P, Toso C, Oberholzer J, Lehmann R, Bachmann F, Tasinato A, Spinas GA, Halban PA, Donath MY. FLIP switches Fas-mediated glucose signaling in human pancreatic ß cells from apoptosis to cell replication. Proc Natl Acad Sci USA 99: 8236-8241, 2002.
42. Maedler K, Schumann DM, Sauter N, Ellingsgaard H, Bosco D, Baertschiger R, Iwakura Y, Oberholzer J, Wollheim CB, Gauthier BR, Donath MY. Low concentration of interleukin-1 beta induces FLICEinhibitory protein-mediated beta-cell proliferation in human pancreatic islets. Diabetes 55: 2713-2722,2006.
43. Maedler K, Sergeev P, Ris F, Oberholzer J, JollerJemelka Hl, Spinas GA, Kaiser N, Halban PA, Donath MY. Glucose-induced beta-cell production of interleukin-1 beta contributes to glucotoxicity in human pancreatic islets. J Clin Invest 110: 851-860, 2002.
44. Maedler K, Spinas GA, Lehmann R, Sergeev P, Weber M, Fontana A, Kaiser N, Donath MY. Glucose induces beta-cell apoptosis via upregulation of the Fas-receptor in human islets. Diabetes 50: 1683-1690,2001.
45. Mandrup-Poulsen T. The role of interleukin-1 in the pathogenesis of IDDM. Diabetologia 39: 1005-1029, 1996.
46. Marselli L, Sgroi DC, Thome J, Dahiya S, Torri S, Orner A, Del Prato S, Towia L, Otu HH, Sharma A, Bonner-Weir S, Marchetti P, Weir GC. Evidence of inflammatory markers in beta cells of Type 2 diabetic subjects. Diabetologia 50: S178, 2007.
47. Nguyen MT, Favelyukis S, Nguyen AK, Reichart D, Scott PA, Jenn A, Liu-Bryan R, Glass CK, Neels JG, Olefsky JM. A subpopulation of macrophages infiltrates hypertrophic adipose tissue and is activated by free fatty acids via Toll-like receptors 2 and 4 and JNK-dependent pathways. J Biol Chem 282: 35279-35292, 2007.
48. Norlin S, Ahlgren U, Edlund H. Nuclear factorkappaB activity in beta-cells is required for glucose-stimulated insulin secretion. Diabetes 54: 125-132,2005.
49. O'Neill LA. The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol Rev 226: 10-18, 2008.
50. Pickup JC, Mattock MB, Chusney GD, Burt D. NIDDM as a disease of the innate immune system: association of acute- phase reactants and interleukin-6 with metabolic syndrome X. Diabetologia 40: 1286-1292, 1997.
51. Prentki M, Nolan CJ. Islet beta cell failure in Type 2 diabetes. J Clin Invest 116: 1802-1812, 2006.
52. Rhodes CJ. Type 2 diabetes-a matter of beta-cell life and death? Science 307: 380-384, 2005.
53. Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG. Islet-associated macrophages in Type 2 diabetes. Diabetologia 52: 1686-1688, 2009.
54. Robertson RP, Harmon J, Tran PO, Poitout V. Betacell glucose toxicity, lipotoxicity, and chronic oxidative stress in Type 2 diabetes. Diabetes 53, Suppl 1: S119-S124, 2004.
55. Scarim AL, Arnush M, Hill JR, Marshall CA, Baldwin A, McDaniel ML, Corbett JA. Evidence for the presence of type I IL-1 receptors on betacells of islets of Langerhans. Biochim Biophys Acta 1361:313-320, 1997.
56. Schumann DM, Maedler K, Franklin I, Konrad D, Starling J, Boni-Schnetzler M, Gjinovci A, Kurrer MO, Gauthier BR, Bosco D, Andres A, Berney T, Greter M, Becher B, Chervonsky AV, Halban PA, Mandrup-Poulsen T, Wollheim CB, Donath MY. The Fas pathway is involved in pancreatic beta cell secretory function. Proc Natl Acad Sci USA 104: 2861-2866, 2007.
57. Senn JJ. Toll-like receptor-2 is essential for the development of palmitate-induced insulin resistance in myotubes. J Biol Chem 281: 26865-26875, 2006.
58. Shi H, Kokoeva MV, lnouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acidinduced insulin resistance. J Clin Invest 116: 3015-3025, 2006.
59. Shoelson SE, Goldfine AB. Getting away from glucose: fanning the flames of obesity-induced inflammation. Nat Med 15: 373-374, 2009.
60. Song MJ, Kim KH, Yoon JM, Kim JB. Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes. Siochem Biophys Res Commun 346: 739-745, 2006.
61. Spranger J, Kroke A, Mohlig M, Hoffmann K, Bergmann MM, Ristow M, Boeing H, Pfeiffer AF. Inflammatory cytokines and the risk to develop Type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 52: 812-817, 2003.
62. Staiger H, Staiger K, Stefan N, Wahl HG, Machicao F, Kellerer M, Haring HU. Palmitateinduced interleukin-6 expression in human coronary artery endothelial cells. Diabetes 53: 3209-3216,2004.
63. Unger RH, Orci L. The essential role of glucagon in tne pathogenesis of diabetes mellitus. Lancet 1 : 14-16, 1975.
64. Vives-Pi M, Somoza N, Fernandez-Alvarez J, Vargas F, Caro P, Alba A, Gomis R, Labeta MO, Pujol-Borrell R. Evidence of expression of endotoxin receptors CD14, toll-like receptors TLR4 and TLR2 and associated molecule MD-2 and of sensitivity to endotoxin (LPS) in islet beta cells. Clin Exp Immunol 133: 208-218, 2003.
65. Weir GC, Bonner-Weir S. Five stages of evolving beta-cell dysfunction during progression to diabetes. Diabetes 53, Suppl 3: S16-S21, 2004.
66. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
67. Weksler-Zangen S, Raz I, Lenzen S, Jorns A, Ehrenfeld S, Amir G, Oprescu A, Yagil Y, Yagil C, Zangen DH, Kaiser N. Impaired glucose-stimulated insulin secretion is coupled with exocrine pancreatic lesions in the Cohen diabetic rat. Diabetes 57: 279-287, 2008.
68. Wellen KE, Hotamisligil GS. Inflammation, stress, diabetes. J Clin Invest 115:1111-1119, 2005.
69. Wideman RD, Yu IL, Webber TD, Verchere CB, Johnson JD, Cheung AT, Kieffer TJ. Improving function and survival of pancreatic islets by endogenous production of glucagon-like peptide 1 (GLP-1). Proc Natl Acad Sci USA 103: 13468-13473,2006.
70. Yego EC, Vincent JA, Sarthy V, Busik JV, Mohr S. Differential regulation of high glucose-induced glyceraldehyde-3-phosphate dehydrogenase nuclear accumulation in Muller cells by IL-1 beta and IL-6. Invest Ophthalmol Vis Sci 50: 1920-1928, 2009.
71. Yoon KH, Ko SH, Cho JH, Lee JM, Ahn YB, Song KH, Yoo SJ, Kang Ml, Cha BY, Lee KW, Son HY, Kang SK, Kim HS, Lee IK, Bonner-Weir S. Selective beta-cell loss and alpha-cell expansion in patients with Type 2 diabetes mellitus in Korea. J Clin Endocrinol Metab 88: 2300-2308, 2003.