Possible Role of Interleukin-1β in Type 2 Diabetes Onset and Implications for Anti-inflammatory Therapy Strategies

PLoS Computational Biology

Volumn 10, Issue 8, 2014, Pages

  Zhao, Gang ^a   Dharmadhikari, Gitanjali ^b   Maedler, Kathrin ^b   Meyer Hermann, Michael ^a,c  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b UNIVERSITY OF BREMEN   (Germany)

^c TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASE CONTROL; HOSPITAL DATA PROCESSING;

ANTI-INFLAMMATORIES; CHRONIC INFLAMMATION; EXPERIMENT DATA; IL-1Β; IN-VITRO; INTERLEUKIN 1Β; PATIENT DATA; THERAPY STRATEGIES; TYPE-2 DIABETES; VITRO EXPERIMENTS;

GLUCOSE;

GLUCOSE; INSULIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; ANTIDIABETIC AGENT; ANTIINFLAMMATORY AGENT; GLUCOSE BLOOD LEVEL;

ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; GLUCOSE HOMEOSTASIS; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; NON INSULIN DEPENDENT DIABETES MELLITUS; ONSET AGE; PROTEIN FUNCTION; STEADY STATE; TREATMENT DURATION; TREATMENT PLANNING; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; DIABETES MELLITUS, TYPE 2; GLUCOSE BLOOD LEVEL; HUMAN; IMMUNOLOGY; INFLAMMATION; METABOLISM;

ANTI-INFLAMMATORY AGENTS; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; HUMANS; HYPOGLYCEMIC AGENTS; INFLAMMATION; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1BETA; MODELS, IMMUNOLOGICAL;

EID: 84919707452     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003798     Document Type: Article

References (63)

1. Bagust A, Beale S, (2003) Deteriorating beta-cell function in type 2 diabetes: a long-term model. QJM 96: 281–288.
2. Ferrannini E, Nannipieri M, Williams K, Gonzales C, Haffner SM, et al. (2004) Mode of Onset of Type 2 Diabetes from Normal or Impaired Glucose Tolerance. Diabetes 53: 160–165 doi:10.2337/diabetes.53.1.160
3. Weir GC, Bonner-Weir S, (2004) Five Stages of Evolving Beta-Cell Dysfunction During Progression to Diabetes. Diabetes 53: S16–S21 doi:10.2337/diabetes.53.suppl_3.S16
4. Mason CC, Hanson RL, Knowler WC, (2007) Progression to Type 2 Diabetes Characterized by Moderate Then Rapid Glucose Increases. Diabetes 56: 2054–2061 doi:10.2337/db07-0053
5. Tabák AG, Jokela M, Akbaraly TN, Brunner EJ, Kivimäki M, et al. (2009) Trajectories of glycaemia, insulin sensitivity, and insulin secretion before diagnosis of type 2 diabetes: an analysis from the Whitehall II study. The Lancet 373: 2215–2221 doi:10.1016/S0140-6736(09)60619-X
6. DeFronzo RA, (2009) From the Triumvirate to the Ominous Octet: A New Paradigm for the Treatment of Type 2 Diabetes Mellitus. Diabetes 58: 773–795 doi:10.2337/db09-9028
7. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC, (2008) Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 10 Suppl 4: 32–42 doi:10.1111/j.1463-1326.2008.00969.x
8. Ferrannini E, (2010) The stunned beta cell: a brief history. Cell Metab 11: 349–352 doi:10.1016/j.cmet.2010.04.009
9. Levy J, Atkinson AB, Bell PM, McCance DR, Hadden DR, (1998) Beta-cell deterioration determines the onset and rate of progression of secondary dietary failure in Type 2 diabetes mellitus: the 10-year follow-up of the Belfast Diet Study. Diabetic Medicine 15: 290–296 doi:;10.1002/(SICI)1096-9136(199804)15:4<290::AID-DIA570>3.0.CO;2-M
10. Muoio DM, Newgard CB, (2008) Molecular and metabolic mechanisms of insulin resistance and [beta]-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9: 193–205 doi:10.1038/nrm2327
11. U.K. prospective diabetes study 16. Overview of 6 years' therapy of type II diabetes: a progressive disease. U.K. Prospective Diabetes Study Group (1995) Diabetes 44: 1249–1258.
12. Turner RCCC, (1999) Glycemic control with diet, sulfonylurea, metformin, or insulin in patients with type 2 diabetes mellitus: Progressive requirement for multiple therapies (ukpds 49). JAMA 281: 2005–2012 doi:10.1001/jama.281.21.2005
13. Lencioni C, Lupi R, Del Prato S, (2008) Beta-cell failure in type 2 diabetes mellitus. Curr Diab Rep 8: 179–184.
14. Maedler K, Sergeev P, Ris F, Oberholzer J, Joller-Jemelka HI, et al. (2002) Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. J Clin Invest 110: 851–860 doi:10.1172/JCI15318
15. Donath MY, Størling J, Berchtold LA, Billestrup N, Mandrup-Poulsen T, (2008) Cytokines and beta-cell biology: from concept to clinical translation. Endocr Rev 29: 334–350 doi:10.1210/er.2007-0033
16. Donath MY, Shoelson SE, (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98–107 doi:10.1038/nri2925
17. Böni-Schnetzler M, Thorne J, Parnaud G, Marselli L, Ehses JA, et al. (2008) Increased interleukin (IL)-1beta messenger ribonucleic acid expression in beta -cells of individuals with type 2 diabetes and regulation of IL-1beta in human islets by glucose and autostimulation. J Clin Endocrinol Metab 93: 4065–4074 doi:10.1210/jc.2008-0396
18. Ehses JA, Perren A, Eppler E, Ribaux P, Pospisilik JA, et al. (2007) Increased Number of Islet-Associated Macrophages in Type 2 Diabetes. Diabetes 56: 2356–2370 doi:10.2337/db06-1650
19. Larsen CM, Faulenbach M, Vaag A, Vølund A, Ehses JA, et al. (2007) Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 356: 1517–1526 doi:10.1056/NEJMoa065213
20. Larsen CM, Faulenbach M, Vaag A, Ehses JA, Donath MY, et al. (2009) Sustained Effects of Interleukin-1 Receptor Antagonist Treatment in Type 2 Diabetes. Dia Care 32: 1663–1668 doi:10.2337/dc09-0533
21. Ramos-Zavala MG, González-Ortiz M, Martínez-Abundis E, Robles-Cervantes JA, González-López R, et al. (2011) Effect of Diacerein on Insulin Secretion and Metabolic Control in Drug-Naïve Patients With Type 2 Diabetes A randomized clinical trial. Dia Care 34: 1591–1594 doi:10.2337/dc11-0357
22. Van Asseldonk EJP, Stienstra R, Koenen TB, Joosten LAB, Netea MG, et al. (2011) Treatment with Anakinra improves disposition index but not insulin sensitivity in nondiabetic subjects with the metabolic syndrome: a randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab 96: 2119–2126 doi:10.1210/jc.2010-2992
23. Cavelti-Weder C, Babians-Brunner A, Keller C, Stahel MA, Kurz-Levin M, et al. (2012) Effects of Gevokizumab on Glycemia and Inflammatory Markers in Type 2 Diabetes. Dia Care 35: 1654–1662 doi:10.2337/dc11-2219
24. Rissanen A, Howard CP, Botha J, Thuren T, Investigators for the G (2012) (2012) Effect of anti-IL-1β antibody (canakinumab) on insulin secretion rates in impaired glucose tolerance or type 2 diabetes: results of a randomized, placebo-controlled trial. Diabetes, Obesity and Metabolism 14: 1088–1096 doi:10.1111/j.1463-1326.2012.01637.x
25. Sloan-Lancaster J, Abu-Raddad E, Polzer J, Miller JW, Scherer JC, et al. (2013) Double-Blind, Randomized Study Evaluating the Glycemic and Anti-inflammatory Effects of Subcutaneous LY2189102, a Neutralizing IL-1β Antibody, in Patients With Type 2 Diabetes. Diabetes Care 36: 2239–46 doi:10.2337/dc12-1835
26. Mandrup-Poulsen T, (2012) Perspective: Testing failures. Nature 485: S17–S17 doi:10.1038/485S17a
27. Maedler K, Sergeev P, Ehses JA, Mathe Z, Bosco D, et al. (2004) Leptin modulates beta cell expression of IL-1 receptor antagonist and release of IL-1beta in human islets. Proc Natl Acad Sci USA 101: 8138–8143 doi:10.1073/pnas.0305683101
28. Glas R, Sauter N, Schulthess F, Shu L, Oberholzer J, et al. (2009) Purinergic P2X7 receptors regulate secretion of interleukin-1 receptor antagonist and beta cell function and survival. Diabetologia 52: 1579–1588 doi:10.1007/s00125-009-1349-0
29. Dinarello C, (1996) Biologic basis for interleukin-1 in disease. Blood 87: 2095–2147.
30. Carstensen M, Herder C, Kivimäki M, Jokela M, Roden M, et al. (2010) Accelerated Increase in Serum Interleukin-1 Receptor Antagonist Starts 6 Years Before Diagnosis of Type 2 Diabetes. Diabetes 59: 1222–1227 doi:10.2337/db09-1199
31. Retnakaran R, Drucker DJ, (2008) Intensive insulin therapy in newly diagnosed type 2 diabetes. The Lancet 371: 1725–1726 doi:10.1016/S0140-6736(08)60736-9
32. Maedler K, Schumann DM, Sauter N, Ellingsgaard H, Bosco D, et al. (2006) Low concentration of interleukin-1beta induces FLICE-inhibitory protein-mediated beta-cell proliferation in human pancreatic islets. Diabetes 55: 2713–2722 doi:10.2337/db05-1430
33. Topp B, Promislow K, deVries G, Miura RM, Finegood DT, (2000) A model of beta-cell mass, insulin, and glucose kinetics: pathways to diabetes. J Theor Biol 206: 605–619 doi:10.1006/jtbi.2000.2150
34. Blasio BFD, Bak P, Pociot F, Karlsen AE, Nerup J, (1999) Onset of type 1 diabetes: a dynamical instability. Diabetes 48: 1677–1685 doi:10.2337/diabetes.48.9.1677
35. Gaetano AD, Hardy T, Beck B, Abu-Raddad E, Palumbo P, et al. (2008) Mathematical models of diabetes progression. Am J Physiol Endocrinol Metab 295: E1462–E1479 doi:10.1152/ajpendo.90444.2008
36. Perreault L, Pan Q, Mather KJ, Watson KE, Hamman RF, et al. (2012) Effect of regression from prediabetes to normal glucose regulation on long-term reduction in diabetes risk: results from the Diabetes Prevention Program Outcomes Study. Lancet 379: 2243–2251 doi:10.1016/S0140-6736(12)60525-X
37. Bergman RN, Lovejoy JC (1997) The Minimal Model Approach and Determinants of Glucose Tolerance. Louisiana State University Press. 406 p.
38. García-Estévez DA, Araújo-Vilar D, Fiestras-Janeiro G, Saavedra-González A, Cabezas-Cerrato J, (2003) Comparison of several insulin sensitivity indices derived from basal plasma insulin and glucose levels with minimal model indices. Horm Metab Res 35: 13–17 doi:10.1055/s-2003-38385
39. Spranger J, Kroke A, Möhlig M, Hoffmann K, Bergmann MM, et al. (2003) 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 doi:10.2337/diabetes.52.3.812
40. Schmidt H, Jirstrand M, (2006) Systems Biology Toolbox for MATLAB: a computational platform for research in systems biology. Bioinformatics 22: 514–515 doi:10.1093/bioinformatics/bti799
41. Laybutt DR, Glandt M, Xu G, Ahn YB, Trivedi N, et al. (2003) Critical reduction in beta-cell mass results in two distinct outcomes over time. Adaptation with impaired glucose tolerance or decompensated diabetes. J Biol Chem 278: 2997–3005 doi:10.1074/jbc.M210581200
42. Alejandro R, Cutfield RG, Shienvold FL, Polonsky KS, Noel J, et al. (1986) Natural history of intrahepatic canine islet cell autografts. J Clin Invest 78: 1339–1348 doi:10.1172/JCI112720
43. Suzuki K, Bonner-Weir S, Trivedi N, Yoon KH, Hollister-Lock J, et al. (1998) Function and survival of macroencapsulated syngeneic islets transplanted into streptozocin-diabetic mice. Transplantation 66: 21–28.
44. Hardy T, Abu-Raddad E, Porksen N, Gaetano AD, (2012) Evaluation of a mathematical model of diabetes progression against observations in the Diabetes Prevention Program. Am J Physiol Endocrinol Metab 303: E200–E212 doi:10.1152/ajpendo.00421.2011
45. Hyun E, Ramachandran R, Hollenberg MD, Vergnolle N, (2011) Mechanisms behind the anti-inflammatory actions of insulin. Crit Rev Immunol 31: 307–340.
46. Pruski M, Krysiak R, Okopien B, (2009) Pleiotropic action of short-term metformin and fenofibrate treatment, combined with lifestyle intervention, in type 2 diabetic patients with mixed dyslipidemia. Diabetes Care 32: 1421–1424 doi:10.2337/dc08-2335
47. Gómez-García A, Torres GM, Ortega-Pierres LE, Rodríguez-Ayala E, Álvarez-Aguilar C, et al. (2007) Rosuvastatin and Metformin Decrease Inflammation and Oxidative Stress in Patients With Hypertension and Dyslipidemia. Rev Esp Cardiol 60: 1242–1249.
48. Stumvoll M, Goldstein BJ, van Haeften TW, (2005) Type 2 diabetes: principles of pathogenesis and therapy. The Lancet 365: 1333–1346 doi:10.1016/S0140-6736(05)61032-X
49. Kita Y, Takamura T, Misu H, Ota T, Kurita S, et al. (2012) Metformin Prevents and Reverses Inflammation in a Non-Diabetic Mouse Model of Nonalcoholic Steatohepatitis. PLoS ONE 7: e43056 doi:10.1371/journal.pone.0043056
50. Dinarello CA, Donath MY, Mandrup-Poulsen T, (2010) Role of IL-1β in type 2 diabetes. Current Opinion in Endocrinology, Diabetes and Obesity 17: 1 doi:10.1097/MED.0b013e32833bf6dc
51. Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, et al. (2010) Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nature Immunology 11: 897–904 doi:10.1038/ni.1935
52. Butler PC, Meier JJ, Butler AE, Bhushan A, (2007) The replication of beta cells in normal physiology, in disease and for therapy. Nat Clin Pract Endocrinol Metab 3: 758–768 doi:10.1038/ncpendmet0647
53. Talchai C, Xuan S, Lin HV, Sussel L, Accili D, (2012) Pancreatic β Cell Dedifferentiation as a Mechanism of Diabetic β Cell Failure. Cell 150: 1223–1234 doi:10.1016/j.cell.2012.07.029
54. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, et al. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102–110.
55. Böni-Schnetzler M, Boller S, Debray S, Bouzakri K, Meier DT, et al. (2009) Free fatty acids induce a proinflammatory response in islets via the abundantly expressed interleukin-1 receptor I. Endocrinology 150: 5218–5229 doi:10.1210/en.2009-0543
56. Larsson H, Ahrén B, (2000) Glucose intolerance is predicted by low insulin secretion and high glucagon secretion: outcome of a prospective study in postmenopausal Caucasian women. Diabetologia 43: 194–202 doi:10.1007/s001250050029
57. Ahrén B, (2009) β- and α-Cell Dysfunction in Subjects Developing Impaired Glucose Tolerance Outcome of a 12-Year Prospective Study in Postmenopausal Caucasian Women. Diabetes 58: 726–731 doi:10.2337/db08-1158
58. Saunders PT, Koeslag JH, Wessels JA, (1998) Integral Rein Control in Physiology. Journal of Theoretical Biology 194: 163–173 doi:10.1006/jtbi.1998.0746
59. Saunders PT, Koeslag JH, Wessels JA, (2000) Integral Rein Control in Physiology II: a General Model. Journal of Theoretical Biology 206: 211–220 doi:10.1006/jtbi.2000.2118
60. Mari A, Tura A, Natali A, Laville M, Laakso M, et al. (2010) Impaired beta cell glucose sensitivity rather than inadequate compensation for insulin resistance is the dominant defect in glucose intolerance. Diabetologia 53: 749–756 doi:10.1007/s00125-009-1647-6
61. Ferrannini E, Natali A, Muscelli E, Nilsson PM, Golay A, et al. (2011) Natural history and physiological determinants of changes in glucose tolerance in a non-diabetic population: the RISC Study. Diabetologia 54: 1507–1516 doi:10.1007/s00125-011-2112-x
62. Matveyenko AV, Liuwantara D, Gurlo T, Kirakossian D, Dalla Man C, et al. (2012) Pulsatile portal vein insulin delivery enhances hepatic insulin action and signaling. Diabetes 61: 2269–2279 doi:10.2337/db11-1462
63. Kudo S, Mizuno K, Hirai Y, Shimizu T, (1990) Clearance and Tissue Distribution of Recombinant Human Interleukin 1β in Rats. Cancer Res 50: 5751–5755.