Differential role of MyD88 and TRIF signaling in myeloid cells in the pathogenesis of autoimmune diabetes

PLoS ONE

Volumn 13, Issue 3, 2018, Pages

  Androulidaki, Ariadne ^a   Wachsmuth, Laurens ^a   Polykratis, Apostolos ^a   Pasparakis, Manolis ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD8ALPHA ANTIGEN; GLUCOSE; GLYCOPROTEIN P 15095; INDOLEAMINE 2,3 DIOXYGENASE; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTION FACTOR FOXP3; GAMMA INTERFERON; MYD88 PROTEIN, MOUSE; STREPTOZOCIN; TICAM-1 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; BONE MARROW CELL; BONE MARROW DERIVED DENDRITIC CELL; CELL EXPANSION; CELL INFILTRATION; CELL ISOLATION; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INCIDENCE; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MOUSE; NONHUMAN; PANCREAS ISLET; PATHOGENESIS; PERCENTAGE OF APOPTOTIC CELLS; PERITONEUM CELL; PHAGOCYTE; PHAGOCYTOSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; RNA ISOLATION; SIGNAL TRANSDUCTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TISSUE SECTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; COMPARATIVE STUDY; DEFICIENCY; DENDRITIC CELL; ENZYME INDUCTION; EXPERIMENTAL DIABETES MELLITUS; FEMALE; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; KNOCKOUT MOUSE; NONOBESE DIABETIC MOUSE; PATHOLOGY; PERITONEUM MACROPHAGE; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; APOPTOSIS; DENDRITIC CELLS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; ENZYME INDUCTION; FEMALE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-GAMMA; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MYELOID CELLS; MYELOID DIFFERENTIATION FACTOR 88; PHAGOCYTOSIS; SPECIFIC PATHOGEN-FREE ORGANISMS; STREPTOZOCIN; T-LYMPHOCYTE SUBSETS;

EID: 85043755522     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0194048     Document Type: Article

References (46)

1. Lehuen A, Diana J, Zaccone P, Cooke A. Immune cell crosstalk in type 1 diabetes. Nat Rev Immunol. 2010; 10(7):501–13. Epub 2010/06/26. doi: 10.1038/nri2787. PMID: 20577267.
2. Anderson MS, Bluestone JA. The NOD mouse: a model of immune dysregulation. Annu Rev Immunol. 2005; 23:447–85. Epub 2005/03/18. doi: 10.1146/annurev.immunol.23.021704.115643. PMID: 15771578.
3. Pearson JA, Wong FS, Wen L. The importance of the Non Obese Diabetic (NOD) mouse model in autoimmune diabetes. J Autoimmun. 2016; 66:76–88. Epub 2015/09/26. doi: 10.1016/j.jaut.2015.08.019. PMID: 26403950; PubMed Central PMCID: PMCPMC4765310.
4. Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia. 2008; 51 (2):216–26. Epub 2007/12/19. doi: 10.1007/s00125-007-0886-7. PMID: 18087688.
5. Paik SG, Fleischer N, Shin SI. Insulin-dependent diabetes mellitus induced by subdiabetogenic doses of streptozotocin: obligatory role of cell-mediated autoimmune processes. Proc Natl Acad Sci U S A. 1980; 77(10):6129–33. Epub 1980/10/01. PMID: 6449703; PubMed Central PMCID: PMCPMC350227.
6. Tai N, Wong FS, Wen L. The role of the innate immune system in destruction of pancreatic beta cells in NOD mice and humans with type I diabetes. J Autoimmun. 2016; 71:26–34. Epub 2016/03/30. doi: 10.1016/j.jaut.2016.03.006. PMID: 27021275; PubMed Central PMCID: PMCPMC4903935.
7. Mathis D, Vence L, Benoist C. beta-Cell death during progression to diabetes. Nature. 2001; 414 (6865):792–8. Epub 2001/12/14. doi: 10.1038/414792a. PMID: 11742411.
8. Trudeau JD, Dutz JP, Arany E, Hill DJ, Fieldus WE, Finegood DT. Neonatal beta-cell apoptosis: a trigger for autoimmune diabetes? Diabetes. 2000; 49(1):1–7. Epub 2000/01/01. PMID: 10615942.
9. 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. 2003; 198(10):1527–37. Epub 2003/11/19. doi: 10.1084/jem.20030966. PMID: 14623908; PubMed Central PMCID: PMCPMC2194112.
10. Kim HS, Han MS, Chung KW, Kim S, Kim E, Kim MJ, et al. Toll-like receptor 2 senses beta-cell death and contributes to the initiation of autoimmune diabetes. Immunity. 2007; 27(2):321–33. Epub 2007/08/ 21. doi: 10.1016/j.immuni.2007.06.010. PMID: 17707128.
11. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010; 11(5):373–84. doi: 10.1038/ni.1863. PMID: 20404851.
12. Marty RR, Dirnhofer S, Mauermann N, Schweikert S, Akira S, Hunziker L, et al. MyD88 signaling controls autoimmune myocarditis induction. Circulation. 2006; 113(2):258–65. Epub 2006/01/13. doi: 10.1161/CIRCULATIONAHA.105.564294. PMID: 16401773.
13. Su SB, Silver PB, Grajewski RS, Agarwal RK, Tang J, Chan CC, et al. Essential role of the MyD88 pathway, but nonessential roles of TLRs 2, 4, and 9, in the adjuvant effect promoting Th1-mediated autoimmunity. J Immunol. 2005; 175(10):6303–10. Epub 2005/11/08. doi: 175/10/6303 [pii]. PMID: 16272281.
14. Isnardi I, Ng YS, Srdanovic I, Motaghedi R, Rudchenko S, von Bernuth H, et al. IRAK-4- and MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans. Immunity. 2008; 29(5):746–57. Epub 2008/11/14. doi: 10.1016/j.immuni.2008.09.015. PMID: 19006693; PubMed Central PMCID: PMCPMC2666307.
15. Woods A, Soulas-Sprauel P, Jaulhac B, Arditi B, Knapp AM, Pasquali JL, et al. MyD88 negatively controls hypergammaglobulinemia with autoantibody production during bacterial infection. Infect Immun. 2008; 76(4):1657–67. Epub 2008/01/30. doi: 10.1128/IAI.00951-07. PMID: 18227170; PubMed Central PMCID: PMCPMC2292895.
16. Guo B, Chang EY, Cheng G. The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J Clin Invest. 2008; 118(5):1680–90. Epub 2008/04/03. doi: 10.1172/JCI33342. PMID: 18382764; PubMed Central PMCID: PMCPMC2276397.
17. Touil T, Fitzgerald D, Zhang GX, Rostami A, Gran B. Cutting Edge: TLR3 stimulation suppresses experimental autoimmune encephalomyelitis by inducing endogenous IFN-beta. J Immunol. 2006; 177 (11):7505–9. Epub 2006/11/23. doi: 177/11/7505 [pii]. PMID: 17114417.
18. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008; 455(7216):1109–13. Epub 2008/09/23. doi: 10.1038/nature07336. PMID: 18806780; PubMed Central PMCID: PMCPMC2574766.
19. Burrows MP, Volchkov P, Kobayashi KS, Chervonsky AV. Microbiota regulates type 1 diabetes through Toll-like receptors. Proc Natl Acad Sci U S A. 2015; 112(32):9973–7. doi: 10.1073/pnas.1508740112. PMID: 26216961; PubMed Central PMCID: PMCPMC4538618.
20. Bollyky PL, Bice JB, Sweet IR, Falk BA, Gebe JA, Clark AE, et al. The toll-like receptor signaling molecule Myd88 contributes to pancreatic beta-cell homeostasis in response to injury. PLoS One. 2009; 4 (4):e5063. Epub 2009/04/10. doi: 10.1371/journal.pone.0005063. PMID: 19357791; PubMed Central PMCID: PMCPMC2666970.
21. Hutton MJ, Soukhatcheva G, Johnson JD, Verchere CB. Role of the TLR signaling molecule TRIF in beta-cell function and glucose homeostasis. Islets. 2010; 2(2):104–11. Epub 2010/11/26. doi: 10.4161/isl.2.2.11209. PMID: 21099302.
22. Vlantis K, Polykratis A, Welz PS, van Loo G, Pasparakis M, Wullaert A. TLR-independent anti-inflammatory function of intestinal epithelial TRAF6 signalling prevents DSS-induced colitis in mice. Gut. 2016; 65(6):935–43. doi: 10.1136/gutjnl-2014-308323. PMID: 25761602; PubMed Central PMCID: PMCPMC4893119.
23. Dannappel M, Vlantis K, Kumari S, Polykratis A, Kim C, Wachsmuth L, et al. RIPK1 maintains epithelial homeostasis by inhibiting apoptosis and necroptosis. Nature. 2014; 513(7516):90–4. doi: 10.1038/nature13608. PMID: 25132550.
24. Caton ML, Smith-Raska MR, Reizis B. Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J Exp Med. 2007; 204(7):1653–64. doi: 10.1084/jem.20062648. PMID: 17591855; PubMed Central PMCID: PMCPMC2118632.
25. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999; 8(4):265–77. PMID: 10621974.
26. Schwenk F, Baron U, Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 1995; 23(24):5080–1. Epub 1995/12/25. doi: l50367 [pii]. PMID: 8559668; PubMed Central PMCID: PMCPMC307516.
27. Li DS, Yuan YH, Tu HJ, Liang QL, Dai LJ. A protocol for islet isolation from mouse pancreas. Nat Protoc. 2009; 4(11):1649–52. Epub 2009/10/31. doi: 10.1038/nprot.2009.150. PMID: 19876025.
28. Huynh ML, Fadok VA, Henson PM. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J Clin Invest. 2002; 109(1):41–50. Epub 2002/01/10. doi: 10.1172/JCI11638. PMID: 11781349; PubMed Central PMCID: PMCPMC150814.
29. Clayton AR, Prue RL, Harper L, Drayson MT, Savage CO. Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: relevance to systemic vasculitis. Arthritis Rheum. 2003; 48(8):2362–74. Epub 2003/08/09. doi: 10.1002/art.11130. PMID: 12905492.
30. Takahashi M, Kobayashi Y. Cytokine production in association with phagocytosis of apoptotic cells by immature dendritic cells. Cell Immunol. 2003; 226(2):105–15. Epub 2004/02/14. doi: 10.1016/j.cellimm.2003.11.008. PMID: 14962498.
31. Manches O, Fernandez MV, Plumas J, Chaperot L, Bhardwaj N. Activation of the noncanonical NF-kappaB pathway by HIV controls a dendritic cell immunoregulatory phenotype. Proc Natl Acad Sci U S A. 2012; 109(35):14122–7. Epub 2012/08/11. doi: 10.1073/pnas.1204032109. PMID: 22879398; PubMed Central PMCID: PMCPMC3435221.
32. Tas SW, Vervoordeldonk MJ, Hajji N, Schuitemaker JH, van der Sluijs KF, May MJ, et al. Noncanonical NF-kappaB signaling in dendritic cells is required for indoleamine 2,3-dioxygenase (IDO) induction and immune regulation. Blood. 2007; 110(5):1540–9. Epub 2007/05/08. doi: 10.1182/blood-2006-11-056010. PMID: 17483297.
33. Hosseini-Tabatabaei A, Jalili RB, Li Y, Kilani RT, Moeen Rezakhanlou A, Ghahary A. Mechanism underlying defective interferon gamma-induced IDO expression in non-obese diabetic mouse fibroblasts. PLoS One. 2012; 7(5):e37747. Epub 2012/06/05. doi: 10.1371/journal.pone.0037747. PMID: 22662207; PubMed Central PMCID: PMCPMC3360620.
34. Jeong YI, Kim SW, Jung ID, Lee JS, Chang JH, Lee CM, et al. Curcumin suppresses the induction of indoleamine 2,3-dioxygenase by blocking the Janus-activated kinase-protein kinase Cdelta-STAT1 signaling pathway in interferon-gamma-stimulated murine dendritic cells. J Biol Chem. 2009; 284(6):3700–8. Epub 2008/12/17. doi: 10.1074/jbc.M807328200. PMID: 19075017.
35. Sarkar SA, Wong R, Hackl SI, Moua O, Gill RG, Wiseman A, et al. Induction of indoleamine 2,3-dioxy-genase by interferon-gamma in human islets. Diabetes. 2007; 56(1):72–9. Epub 2006/12/29. doi: 10.2337/db06-0617. PMID: 17192467.
36. Diana J, Simoni Y, Furio L, Beaudoin L, Agerberth B, Barrat F, et al. Crosstalk between neutrophils, B-1a cells and plasmacytoid dendritic cells initiates autoimmune diabetes. Nat Med. 2013; 19(1):65–73. Epub 2012/12/18. doi: 10.1038/nm.3042. PMID: 23242473.
37. Pallotta MT, Orabona C, Volpi C, Vacca C, Belladonna ML, Bianchi R, et al. Indoleamine 2,3-dioxygen-ase is a signaling protein in long-term tolerance by dendritic cells. Nat Immunol. 2011; 12(9):870–8. Epub 2011/08/02. doi: 10.1038/ni.2077. PMID: 21804557.
38. Baban B, Chandler PR, Johnson BA 3rd, Huang L, Li M, Sharpe ML, et al. Physiologic control of IDO competence in splenic dendritic cells. J Immunol. 2011; 187(5):2329–35. Epub 2011/08/05. doi: 10.4049/jimmunol.1100276. PMID: 21813777; PubMed Central PMCID: PMCPMC3556270.
39. Harden JL, Egilmez NK. Indoleamine 2,3-dioxygenase and dendritic cell tolerogenicity. Immunol Invest. 2012; 41(6–7):738–64. Epub 2012/09/29. doi: 10.3109/08820139.2012.676122. PMID: 23017144; PubMed Central PMCID: PMCPMC3645912.
40. Volpi C, Fallarino F, Pallotta MT, Bianchi R, Vacca C, Belladonna ML, et al. High doses of CpG oligo-deoxynucleotides stimulate a tolerogenic TLR9-TRIF pathway. Nat Commun. 2013; 4:1852. Epub 2013/05/16. doi: 10.1038/ncomms2874. PMID: 23673637.
41. Park MK, Oh HJ, Heo YM, Park EM, Cho ML, Kim HY, et al. Myeloid differentiation primary response protein 88 blockade upregulates indoleamine 2,3-dioxygenase expression in rheumatoid synovial fibroblasts. Exp Mol Med. 2011; 43(8):446–54. Epub 2011/06/10. doi: 10.3858/emm.2011.43.8.050. PMID: 21654189; PubMed Central PMCID: PMCPMC3174378.
42. De Luca A, Montagnoli C, Zelante T, Bonifazi P, Bozza S, Moretti S, et al. Functional yet balanced reactivity to Candida albicans requires TRIF, MyD88, and IDO-dependent inhibition of Rorc. J Immunol. 2007; 179(9):5999–6008. Epub 2007/10/20. doi: 179/9/5999 [pii]. PMID: 17947673.
43. Ravishankar B, Liu H, Shinde R, Chandler P, Baban B, Tanaka M, et al. Tolerance to apoptotic cells is regulated by indoleamine 2,3-dioxygenase. Proc Natl Acad Sci U S A. 2012; 109(10):3909–14. Epub 2012/02/23. doi: 10.1073/pnas.1117736109. PMID: 22355111; PubMed Central PMCID: PMCPMC3309765.
44. Fallarino F, Volpi C, Zelante T, Vacca C, Calvitti M, Fioretti MC, et al. IDO mediates TLR9-driven protection from experimental autoimmune diabetes. J Immunol. 2009; 183(10):6303–12. Epub 2009/10/21. doi: 10.4049/jimmunol.0901577. PMID: 19841163.
45. Grohmann U, Fallarino F, Bianchi R, Orabona C, Vacca C, Fioretti MC, et al. A defect in tryptophan catabolism impairs tolerance in nonobese diabetic mice. J Exp Med. 2003; 198(1):153–60. Epub 2003/ 07/02. doi: 10.1084/jem.20030633. PMID: 12835483; PubMed Central PMCID: PMCPMC2196078.
46. Zhang Y, Jalili RB, Kilani RT, Elizei SS, Farrokhi A, Khosravi-Maharlooei M, et al. IDO-Expressing Fibroblasts Protect Islet Beta Cells From Immunological Attack and Reverse Hyperglycemia in Non-Obese Diabetic Mice. J Cell Physiol. 2016; 231(9):1964–73. Epub 2016/01/09. doi: 10.1002/jcp.25301. PMID: 26743772.