Exacerbation of Autoimmune Thyroiditis by CTLA-4 Blockade: A Role for IFNγ-Induced Indoleamine 2, 3-Dioxygenase

Thyroid

Volumn 26, Issue 8, 2016, Pages 1117-1124

  Sharma, Rajni ^a   Di Dalmazi, Giulia ^a,b   Caturegli, Patrizio ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHIETI   (Italy)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DRINKING WATER; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; IODINE; IPILIMUMAB; PHOSPHATE BUFFERED SALINE; THYROGLOBULIN ANTIBODY; TICILIMUMAB; CYTOKINE; MONOCLONAL ANTIBODY; THYROGLOBULIN;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE THYROIDITIS; AUTOPSY; BLOOD; CELL INFILTRATION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; HASHIMOTO DISEASE; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; INCIDENCE; MALE; METASTATIC MELANOMA; MIDDLE AGED; MONONUCLEAR CELL; MORBIDITY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SPLEEN; T LYMPHOCYTE; THYROID GLAND; ANIMAL; IMMUNOLOGY; METABOLISM; NONOBESE DIABETIC MOUSE; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; CTLA-4 ANTIGEN; CYTOKINES; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MICE; MICE, INBRED NOD; T-LYMPHOCYTES, REGULATORY; THYROGLOBULIN; THYROIDITIS, AUTOIMMUNE;

EID: 84982957879     PISSN: 10507256     EISSN: 15579077     Source Type: Journal    
DOI: 10.1089/thy.2016.0092     Document Type: Article

References (42)

1. Rose NR, Witebsky E 1956 Studies on organ specificity. V. Changes in the thyroid glands of rabbits following active immunization with rabbit thyroid extracts. J Immunol 76: 417-421.
2. Jones HE, Roitt IM 1961 Experimental auto-immune thyroiditis in the rat. Brit J Exp Pathol 42:546-557.
3. Podolin PL, Pressey A, DeLarato NH, Fischer PA, Peterson LB, Wicker LS 1993 I-E+ nonobese diabetic mice develop insulitis and diabetes. Exp Med 178:793-803.
4. Braley-Mullen H, Yu S 2015 NOD.H-2h4 mice: an important and underutilized animal model of autoimmune thyroiditis and Sjogren's syndrome. Adv Immunol 126:1-43.
5. Kolypetri P, King J, Larijani M, Carayanniotis G 2015 Genes and environment as predisposing factors in autoimmunity: acceleration of spontaneous thyroiditis by dietary iodide in NOD.H2 mice. Int Rev Immunol 34:542-56.
6. Chen CR, Hamidi S, Braley-Mullen H, Nagayama Y, Bresee C, Aliesky HA, Rapoport B, McLachlan SM 2010 Antibodies to thyroid peroxidase arise spontaneously with age in NOD.H-2h4 mice and appear after thyroglobulin antibodies. Endocrinology 151:4583-4593.
7. Teng X, Shan Z, Teng W, Fan C, Wang H, Guo R 2009 Experimental study on the effects of chronic iodine excess on thyroid function, structure, and autoimmunity in autoimmuneprone NOD.H-2h4 mice. Clin Exp Med 9:51-59.
8. Wicker LS, Todd JA, Peterson LB 1995 Genetic control of autoimmune diabetes in the NOD mouse. Annu Rev Immunol 13:179-200.
9. Rasooly L, Burek CL, Rose NR 1996 Iodine-induced autoimmune thyroiditis in NOD-H-2h4 mice. Clin Immunol Immunopathol 81:287-292.
10. Braley-Mullen H, Sharp GC, Medling B, Tang H 1999 Spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J Autoimmun 12:157-165.
11. Sharma RB, Alegria JD, Talor MV, Rose NR, Caturegli P, Burek CL 2005 Iodine and IFN-gamma synergistically enhance intercellular adhesion molecule 1 expression on NOD.H2h4 mouse thyrocytes. J Immunol 174:7740-7745.
12. Shi L, Bi M, Yang R, Zhou J, Zhao S, Fan C, Shan Z, Li Y, Teng W 2014 Defective expression of regulatory B cells in iodine-induced autoimmune thyroiditis in non-obese diabetic H-2(h4) mice. J Endocrinol Invest 37:43-50.
13. Xue H, Wang W, Shan Z, Li Y, Li Y, Teng X, Gao Y, Fan C, TengW2011 Dynamic changes of CD4+CD25 + regulatory T cells in NOD.H-2h4 mice with iodine-induced autoimmune thyroiditis. Biol Trace Elem Res 143:292-301.
14. Yang X, Gao T, Shi R, Zhou X, Qu J, Xu J, Shan Z, Teng W 2014 Effect of iodine excess on Th1, Th2, Th17, and Treg cell subpopulations in the thyroid of NOD.H-2h4 mice. Biol Trace Elem Res 159:288-296.
15. Ellis JS, Hong SH, Zaghouani H, Braley-Mullen H 2013 Reduced effectiveness of CD4+Foxp3+ regulatory T cells in CD28-deficient NOD.H-2h4 mice leads to increased severity of spontaneous autoimmune thyroiditis. J Immunol 191:4940-4949.
16. Nagayama Y, Horie I, Saitoh O, Nakahara M, Abiru N 2007 CD4+CD25+ naturally occurring regulatory T cells and not lymphopenia play a role in the pathogenesis of iodide-induced autoimmune thyroiditis in NOD-H2h4 mice. J Autoimmun 29:195-202.
17. Bour-Jordan H, Bluestone JA 2009 Regulating the regulators: costimulatory signals control the homeostasis and function of regulatory T cells. Immunol Rev 229:41-66.
18. Couzin-Frankel J 2013 Breakthrough of the year 2013. Cancer immunotherapy. Science 342:1432-1433.
19. Voskens CJ, Goldinger SM, Loquai C, Robert C, Kaehler KC, Berking C, Bergmann T, Bockmeyer CL, Eigentler T, Fluck M, Garbe C, Gutzmer R, Grabbe S, Hauschild A, Hein R, Hundorfean G, Justich A, Keller U, Klein C, Mateus C, Mohr P, Paetzold S, Satzger I, Schadendorf D, Schlaeppi M, Schuler G, Schuler-Thurner B, Trefzer U, Ulrich J, Vaubel J, von Moos R, Weder P, Wilhelm T, Goppner D, Dummer R, Heinzerling LM 2013 The price of tumor control: an analysis of rare side effects of anti-CTLA-4 therapy in metastatic melanoma from the ipilimumab network. PloS One 8:e53745.
20. Corsello SM, Barnabei A, Marchetti P, De Vecchis L, Salvatori R, Torino F 2013 Endocrine side effects induced by immune checkpoint inhibitors. J Clin Endocrinol Metab 98:1361-1375.
21. Ryder M, Callahan M, Postow MA, Wolchok J, Fagin JA 2014 Endocrine-related adverse events following ipilimumab in patients with advanced melanoma: a comprehensive retrospective review from a single institution. Endocr Relat Cancer 21:371-381.
22. Kimura H, Kimura M, Tzou SC, Chen YC, Suzuki K, Rose NR, Caturegli P 2005 Expression of class II major histocompatibility complex molecules on thyrocytes does not cause spontaneous thyroiditis but mildly increases its severity after immunization. Endocrinology 146:1154-1162.
23. Caturegli P, Rose NR, Kimura M, Kimura H, Tzou SC 2003 Studies on murine thyroiditis: new insights from organ flow cytometry. Thyroid 13:419-426.
24. Holmgaard RB, Zamarin D, Munn DH, Wolchok JD, Allison JP 2013 Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J Exp Med 210:1389-1402.
25. Yuan J, Ginsberg B, Page D, Li Y, RasalanT,GallardoHF, Xu Y, Adams S, Bhardwaj N, Busam K, Old LJ, Allison JP, Jungbluth A, Wolchok JD 2011 CTLA-4 blockade increases antigen-specific CD8(+) T cells in prevaccinated patientswith melanoma: three cases. Cancer Immunol Immunother 60: 1137-1146.
26. Kohlhapp FJ, Broucek JR, Hughes T, Huelsmann EJ, Lusciks J, Zayas JP, Dolubizno H, Fleetwood VA, Grin A, Hill GE, Poshepny JL, Nabatiyan A, Ruby CE, Snook JD, Rudra JS, Schenkel JM, Masopust D, Zloza A, Kaufman HL 2015 NK cells and CD8+ T cells cooperate to improve therapeutic responses in melanoma treated with interleukin-2 (IL-2) and CTLA-4 blockade. J Immunother Cancer 3:18.
27. Mbongue JC, Nicholas DA, Torrez TW, Kim NS, Firek AF, LangridgeWH2015 The role of indoleamine 2, 3-dioxygenase in immune suppression and autoimmunity. Vaccines 3:703-729.
28. Nouel A, Pochard P, Simon Q, Segalen I, Le Meur Y, Pers JO, Hillion S 2015 B-Cells induce regulatory T cells through TGF-beta/IDO production in A CTLA-4 dependent manner. J Autoimmun 59:53-60.
29. PlattenM, von Knebel DoeberitzN,Oezen I, Wick W, OchsK 2014 Cancer immunotherapy by targeting IDO1/TDO and their downstream effectors. Front Immunol 5:673.
30. Moretti S, Menicali E, Voce P, Morelli S, Cantarelli S, Sponziello M, Colella R, Fallarino F, Orabona C, Alunno A, de Biase D, Bini V, Mameli MG, Filetti S, Gerli R, Macchiarulo A, Melillo RM, Tallini G, Santoro M, Puccetti P, Avenia N, Puxeddu E 2014 Indoleamine 2,3-dioxygenase 1 (IDO1) is up-regulated in thyroid carcinoma and drives the development of an immunosuppressant tumor microenvironment. J Clin Endocrinol Metab 99:E832-840.
31. Ryu HS, Park YS, Park HJ, Chung YR, Yom CK, Ahn SH, Park YJ, Park SH, Park SY 2014 Expression of indoleamine 2,3-dioxygenase and infiltration of FOXP3+ regulatory T cells are associated with aggressive features of papillary thyroid microcarcinoma. Thyroid 24:1232-1240.
32. Dailey ME, Lindsay S, Skahen R 1955 Relation of thyroid neoplasms to Hashimoto disease of the thyroid gland. AMA Arch Surg 70:291-297.
33. Sheridan C 2015 IDO inhibitors move center stage in immuno-oncology. Nature Biotechnol 33:321-322.
34. Opitz CA, Wick W, Steinman L, Platten M 2007 Tryptophan degradation in autoimmune diseases. Cellular Mol Life Sci 64:2542-2563.
35. Bischoff L, Alvarez S, Dai DL, Soukhatcheva G, Orban PC, Verchere CB 2015 Cellular mechanisms of CCL22-mediated attenuation of autoimmune diabetes. J Immunol 194:3054-3064.
36. Zoso A, Mazza EM, Bicciato S, Mandruzzato S, Bronte V, Serafini P, Inverardi L 2014 Human fibrocytic myeloidderived suppressor cells express IDO and promote tolerance via Treg-cell expansion. Eur J Immunol 44:3307-3319.
37. Nakahara M, Nagayama Y, SaitohO, Sogawa R, Tone S, Abiru N 2009 Expression of immunoregulatory molecules by thyrocytes protects nonobese diabetic-H2h4 mice from developing autoimmune thyroiditis. Endocrinology 150:1545-1551.
38. Pigott E, DuHadaway JB, Muller AJ, Gilmour S, Prendergast GC, Mandik-Nayak L 2014 1-Methyl-tryptophan synergizes with methotrexate to alleviate arthritis in a mouse model of arthritis. Autoimmunity 47:409-418.
39. Mancuso R, Hernis A, Agostini S, Rovaris M, Caputo D, Fuchs D, Clerici M 2015 Indoleamine 2,3 Dioxygenase (IDO) Expression and Activity in Relapsing-Remitting Multiple Sclerosis. PloS One 10:e0130715.
40. Lood C, Tyden H, Gullstrand B, Klint C, Wenglen C, Nielsen CT, Heegaard NH, Jonsen A, Kahn R, Bengtsson AA 2015 Type I interferon-mediated skewing of the serotonin synthesis is associated with severe disease in systemic lupus erythematosus. PloS One 10:e0125109.
41. Wolf AM, Wolf D, Rumpold H, Moschen AR, Kaser A, Obrist P, Fuchs D, Brandacher G, Winkler C, Geboes K, Rutgeerts P, Tilg H 2004 Overexpression of indoleamine 2,3-dioxygenase in human inflammatory bowel disease. Clin Immunol 113:47-55.
42. Leskela S, Rodriguez-Munoz A, de la Fuente H, Figueroa-Vega N, Bonay P, Martin P, Serrano A, Sanchez-Madrid F, Gonzalez-Amaro R, Marazuela M 2013 Plasmacytoid dendritic cells in patients with autoimmune thyroid disease. JClin Endocrinol Metab 98:2822-2833.