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Role of Innate Immunity in Diabetes and Metabolism: Recent Progress in the Study of Inflammasomes

  • Lee, Myung-Shik (Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine)
  • Received : 2011.03.03
  • Accepted : 2011.03.07
  • Published : 2011.04.30

Abstract

Type 1 diabetes is one of the classical examples of organ-specific autoimmune diseases characterized by lymphocytic infiltration or inflammation in pancreatic islets called 'insulitis'. In contrast, type 2 diabetes has been traditionally regarded as a metabolic disorder with a pathogenesis that is totally different from that of type 1 diabetes. However, recent investigation has revealed contribution of chronic inflammation in the pathogenesis of type 2 diabetes. In addition to type 2 diabetes, the role of chronic inflammation is being appreciated in a wide variety of metabolic disorders such as obesity, metabolic syndrome, and atherosclerosis. In this review, we will cover the role of innate immunity in the pathogenesis of metabolic disorders with an emphasis on NLRP3.

Keywords

References

  1. Michelsen KS, Wong MH, Shah PK, Zhang W, Yano J, Doherty TM, Akira S, Rajavashisth TB, Arditi M: Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc Natl Acad Sci U S A 101;10679-10684, 2004 https://doi.org/10.1073/pnas.0403249101
  2. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS: TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116;3015-3025, 2006 https://doi.org/10.1172/JCI28898
  3. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Lee J, Goldfine AB, Benoist C, Shoelson S, Mathis D: Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15;930-939, 2009 https://doi.org/10.1038/nm.2002
  4. Hotamisligil GS, Shargill NS, Spiegelman BM: Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259;87-91, 1993 https://doi.org/10.1126/science.7678183
  5. Kufer TA, Sansonetti PJ: NLR functions beyond pathogen recognition. Nat Immunol 12;121-128, 2011 https://doi.org/10.1038/ni.1985
  6. Kim S, Kim HS, Chung KW, Oh SH, Yun JW, Im SH, Lee MK, Kim KW, Lee MS: Essential role for signal transducer and activator of transcription-1 in pancreatic beta-cell death and autoimmune type 1 diabetes of nonobese diabetic mice. Diabetes 56;2561-2568, 2007 https://doi.org/10.2337/db06-1372
  7. Kim S, Millet I, Kim HS, Kim JY, Han MS, Lee MK, Kim KW, Sherwin RS, Karin M, Lee MS: NF-kappa B prevents beta cell death and autoimmune diabetes in NOD mice. Proc Natl Acad Sci U S A 104;1913-1918, 2007 https://doi.org/10.1073/pnas.0610690104
  8. 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 https://doi.org/10.1056/NEJMoa065213
  9. Gallucci S, Lolkema M, Matzinger P: Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5;1249-1255, 1999 https://doi.org/10.1038/15200
  10. Schroder K, Tschopp J: The inflammasomes. Cell 140;821-832, 2010 https://doi.org/10.1016/j.cell.2010.01.040
  11. Kanneganti TD, Lamkanfi M, Kim YG, Chen G, Park JH, Franchi L, Vandenabeele P, Nunez G: Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 26;433-443, 2007 https://doi.org/10.1016/j.immuni.2007.03.008
  12. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM: Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 12;222-230, 2011
  13. Zhou R, Yazdi AS, Menu P, Tschopp J: A role for mitochondria in NLRP3 inflammasome activation. Nature 469;221-225, 2011 https://doi.org/10.1038/nature09663
  14. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J: Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11;136-140, 2010 https://doi.org/10.1038/ni.1831
  15. Lamkanfi M, Mueller JL, Vitari AC, Misaghi S, Fedorova A, Deshayes K, Lee WP, Hoffman HM, Dixit VM: Glyburide inhibits the Cryopyrin/Nalp3 inflammasome. J Cell Biol 187;61-70, 2009 https://doi.org/10.1083/jcb.200903124
  16. Zaki MH, Boyd KL, Vogel P, Kastan MB, Lamkanfi M, Kanneganti TD: The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32;379-391, 2010 https://doi.org/10.1016/j.immuni.2010.03.003
  17. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R: Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118;229-241, 2004 https://doi.org/10.1016/j.cell.2004.07.002
  18. Liu J, Divoux A, Sun J, Zhang J, Clement K, Glickman JN, Sukhova GK, Wolters PJ, Du J, Gorgun CZ, Doria A, Libby P, Blumberg RS, Kahn BB, Hotamisligil GS, Shi GP: Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 15;940-945, 2009 https://doi.org/10.1038/nm.1994
  19. Wu D, Molofsky AB, Liang HE, Ricardo-Gonzalez RR, Jouihan HA, Bando JK, Chawla A, Locksley RM: Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332;243-247, 2011 https://doi.org/10.1126/science.1201475
  20. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD: The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 17;179-188, 2011 https://doi.org/10.1038/nm.2279
  21. Oka S, Yoshihara E, Bizen-Abe A, Liu W, Watanabe M, Yodoi J, Masutani H: Thioredoxin binding protein-2/thioredoxin-interacting protein is a critical regulator of insulin secretion and peroxisome proliferator-activated receptor function. Endocrinology 150;1225-1234, 2009 https://doi.org/10.1210/en.2008-0646
  22. Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, Sharp FA, Becker C, Franchi L, Yoshihara E, Chen Z, Mullooly N, Mielke LA, Harris J, Coll RC, Mills KH, Mok KH, Newsholme P, Nunez G, Yodoi J, Kahn SE, Lavelle EC, O'Neill LA: Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1$\beta$ in type 2 diabetes. Nat Immunol 11;897-904, 2010 https://doi.org/10.1038/ni.1935
  23. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, Fitzgerald KA, Latz E, Moore KJ, Golenbock DT: The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 9;857-865, 2008 https://doi.org/10.1038/ni.1636
  24. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nunez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E: NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464;1357-1361, 2010 https://doi.org/10.1038/nature08938
  25. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J: Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440;237-241, 2006 https://doi.org/10.1038/nature04516
  26. Jun HS, Santamaria P, Lim HW, Zhang ML, Yoon JW: Absolute requirement of macrophages for the development and activation of beta-cell cytotoxic CD8+ T-cells in T-cell receptor transgenic NOD mice. Diabetes 48;34-42, 1999 https://doi.org/10.2337/diabetes.48.1.34
  27. Turley S, Poirot L, Hattori M, Benoist C, Mathis D: Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J Exp Med 198;1527-1537, 2003 https://doi.org/10.1084/jem.20030966
  28. Kim HS, Han MS, Chung KW, Kim S, Kim E, Kim MJ, Jang E, Lee HA, Youn J, Akira S, Lee MS: Toll-like receptor 2 senses beta-cell death and contributes to the initiation of autoimmune diabetes. Immunity 27;321-333, 2007 https://doi.org/10.1016/j.immuni.2007.06.010
  29. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV: Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455;1109-1113, 2008 https://doi.org/10.1038/nature07336

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