IFN-α mediates the development of autoimmunity both by direct tissue toxicity and through immune cell recruitment mechanisms

Journal of Immunology

Volumn 186, Issue 8, 2011, Pages 4693-4706

  Akeno, Nagako ^a   Smith, Eric P ^a   Stefan, Mihaela ^b   Huber, Amanda K ^b   Zhang, Weijia ^b   Keddache, Mehdi ^c   Tomer, Yaron ^b,d  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANZYME B; PATTERN RECOGNITION RECEPTOR; SODIUM IODIDE SYMPORTER; THYROGLOBULIN; THYROID PEROXIDASE; THYROTROPIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; AUTOIMMUNE THYROIDITIS; AUTOIMMUNITY; CELL DEATH; CELL INFILTRATION; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; RNA SEQUENCE; UPREGULATION;

ANIMALS; AUTOIMMUNITY; CELL LINE; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; IMMUNE SYSTEM; INTERFERON-ALPHA; LEUKOCYTES, MONONUCLEAR; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; RATS; RECEPTOR, INTERFERON ALPHA-BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYROID GLAND; THYROIDITIS; TIME FACTORS;

EID: 79954992665     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002631     Document Type: Article

References (73)

1. Golomb, H. M. 2008. Hairy cell leukemia: treatment successes in the past 25 years. J. Clin. Oncol. 26:2607-2609.
2. Palumbo, E. 2009. PEG-interferon in acute and chronic hepatitis C: a review. Am. J. Ther. 16:573-578.
3. Edwards, M. R., L. Slater, and S. L. Johnston. 2007. Signalling pathways mediating type I interferon gene expression. Microbes Infect. 9:1245-1251. (Pubitemid 47554534)
4. Russo, M. W., and M. W. Fried. 2003. Side effects of therapy for chronic hepatitis C. Gastroenterology 124:1711-1719. (Pubitemid 36617688)
5. Roti, E., R. Minelli, T. Giuberti, S. Marchelli, C. Schianchi, E. Gardini, M. Salvi, F. Fiaccadori, G. Ugolotti, T. M. Neri, and L. E. Braverman. 1996. Multiple changes in thyroid function in patients with chronic active HCV hepatitis treated with recombinant interferon-alpha. Am. J. Med. 101:482-487. (Pubitemid 126335968)
6. Mazziotti, G., F. Sorvillo, A. Carbone, M. Cioffi, F. Morisco, and C. Carella. 2002. Is the IFN-alpha-related thyroid autoimmunity an immunologically heterogeneous disease? J. Intern. Med. 252:377-378, author reply 379. (Pubitemid 35253706)
7. Villanueva, R. B., and N. Brau. 2002. Graves' ophthalmopathy associated with interferon-alpha treatment for hepatitis C. Thyroid 12:737-738. (Pubitemid 34913248)
8. Crow, M. K., K. A. Kirou, and J. Wohlgemuth. 2003. Microarray analysis of interferon-regulated genes in SLE. Autoimmunity 36:481-490. (Pubitemid 37498244)
9. Tomer, Y., J. T. Blackard, and N. Akeno. 2007. Interferon alpha treatment and thyroid dysfunction. Endocrinol. Metab. Clin. North Am. 36:1051-1066, x-xi. (Pubitemid 350026253)
10. Mandac, J. C., S. Chaudhry, K. E. Sherman, and Y. Tomer. 2006. The clinical and physiological spectrum of interferon-alpha induced thyroiditis: toward a new classification. Hepatology 43:661-672.
11. Akeno, N., and Y. Tomer. 2007. Dissecting the mechanisms of interferon induced thyroiditis (IIT): direct effects of interferon alpha on thyroid epithelial cells. In The 89th Meeting of the Endocrine Society, June 2-7. The Endocrine Society, Chevy Chase, MD.
12. Jacobson, E. M., S. Chaudhry, J. C. Mandac, E. Concepcion, and Y. Tomer. 2006. Immune-regulatory gene involvement in the etiology of interferon induced thyroiditis (IIT). Thyroid 16:926 (Abstr.).
13. Farrar, J. D., and K. M. Murphy. 2000. Type I interferons and T helper development. Immunol. Today 21:484-489.
14. Mazziotti, G., F. Sorvillo, M. Piscopo, F. Morisco, M. Cioffi, G. Stornaiuolo, G. B. Gaeta, A. M. Molinari, J. H. Lazarus, G. Amato, and C. Carella. 2005. Innate and acquired immune system in patients developing interferon-alpharelated autoimmune thyroiditis: a prospective study. J. Clin. Endocrinol. Metab. 90:4138-4144. (Pubitemid 41058188)
15. Tilg, H. 1997. New insights into the mechanisms of interferon alfa: an immunoregulatory and anti-inflammatory cytokine. Gastroenterology 112:1017-1021. (Pubitemid 27113829)
16. Ajjan, R. A., P. F. Watson, R. S. McIntosh, and A. P. Weetman. 1996. Intrathyroidal cytokine gene expression in Hashimoto's thyroiditis. Clin. Exp. Immunol. 105:523-528. (Pubitemid 26297900)
17. Oberg, K., K. Funa, and G. Alm. 1983. Effects of leukocyte interferon on clinical symptoms and hormone levels in patients with mid-gut carcinoid tumors and carcinoid syndrome. N. Engl. J. Med. 309:129-133. (Pubitemid 13069520)
18. Burman, P., T. H. Tötterman, K. Oberg, and F. A. Karlsson. 1986. Thyroid autoimmunity in patients on long term therapy with leukocyte-derived interferon. J. Clin. Endocrinol. Metab. 63:1086-1090. (Pubitemid 17173042)
19. Fentiman, I. S., B. S. Thomas, F. R. Balkwill, R. D. Rubens, and J. L. Hayward. 1985. Primary hypothyroidism associated with interferon therapy of breast cancer. Lancet 325:1166. (Pubitemid 15080733)
20. Koh, L. K., F. S. Greenspan, and P. P. Yeo. 1997. Interferon-alpha induced thyroid dysfunction: three clinical presentations and a review of the literature. Thyroid 7:891-896. (Pubitemid 28041664)
21. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159. (Pubitemid 17064313)
22. Roberts, R. M., L. Liu, Q. Guo, D. Leaman, and J. Bixby. 1998. The evolution of the type I interferons. J. Interferon Cytokine Res. 18:805-816. (Pubitemid 28489658)
23. Muller, P. Y., H. Janovjak, A. R. Miserez, and Z. Dobbie. 2002. Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 32:1372-1374, 1376, 1378-1379.
24. Knauf, J. A., R. Elisei, D. Mochly-Rosen, T. Liron, X. N. Chen, R. Gonsky, J. R. Korenberg, and J. A. Fagin. 1999. Involvement of protein kinase Cepsilon (PKCepsilon) in thyroid cell death: a truncated chimeric PKCepsilon cloned from a thyroid cancer cell line protects thyroid cells from apoptosis. J. Biol. Chem. 274:23414-23425.
25. Pohlenz, J., A. Maqueem, K. Cua, R. E. Weiss, J. Van Sande, and S. Refetoff. 1999. Improved radioimmunoassay for measurement of mouse thyrotropin in serum: strain differences in thyrotropin concentration and thyrotroph sensitivity to thyroid hormone. Thyroid 9:1265-1271. (Pubitemid 30038940)
26. de Weerd, N. A., S. A. Samarajiwa, and P. J. Hertzog. 2007. Type I interferon receptors: biochemistry and biological functions. J. Biol. Chem. 282:20053-20057. (Pubitemid 47099976)
27. Tsujimoto, Y., and S. Shimizu. 2005. Another way to die: autophagic programmed cell death. Cell Death Differ. 12 (Suppl. 2):1528-1534. (Pubitemid 41553989)
28. Shimizu, S., T. Kanaseki, N. Mizushima, T. Mizuta, S. Arakawa-Kobayashi, C. B. Thompson, and Y. Tsujimoto. 2004. Role of Bcl-2 family proteins in a nonapoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6:1221-1228. (Pubitemid 39625121)
29. Rubinsztein, D. C., J. E. Gestwicki, L. O. Murphy, and D. J. Klionsky. 2007. Potential therapeutic applications of autophagy. Nat. Rev. Drug Discov. 6:304-312. (Pubitemid 46505881)
30. Negro, R., G. Formoso, T. Mangieri, A. Pezzarossa, D. Dazzi, and H. Hassan. 2006. Levothyroxine treatment in euthyroid pregnant women with autoimmune thyroid disease: effects on obstetrical complications. J. Clin. Endocrinol. Metab. 91:2587-2591. (Pubitemid 44024622)
31. Vladutiu, A. O., and N. R. Rose. 1971. Autoimmune murine thyroiditis relation to histocompatibility (H-2) type. Science 174:1137-1139.
32. Keeble, A. H., Z. Khan, A. Forster, and L. C. James. 2008. TRIM21 is an IgG receptor that is structurally, thermodynamically, and kinetically conserved. Proc. Natl. Acad. Sci. USA 105:6045-6050. (Pubitemid 351758396)
33. Espinosa, A., W. Zhou, M. Ek, M. Hedlund, S. Brauner, K. Popovic, L. Horvath, T. Wallerskog, M. Oukka, F. Nyberg, et al. 2006. The Sjogren's syndromeassociated autoantigen Ro52 is an E3 ligase that regulates proliferation and cell death. J. Immunol. 176:6277-6285.
34. Strandberg, L., A. Ambrosi, A. Espinosa, L. Ottosson, M. L. Eloranta, W. Zhou, A. Elfving, E. Greenfield, V. K. Kuchroo, and M. Wahren-Herlenius. 2008. Interferon-alpha induces up-regulation and nuclear translocation of the Ro52 autoantigen as detected by a panel of novel Ro52-specific monoclonal antibodies. J. Clin. Immunol. 28:220-231.
35. Devadas, S., J. Das, C. Liu, L. Zhang, A. I. Roberts, Z. Pan, P. A. Moore, G. Das, and Y. Shi. 2006. Granzyme B is critical for T cell receptor-induced cell death of type 2 helper T cells. Immunity 25:237-247. (Pubitemid 44224145)
36. Zocco, M. A., E. Carloni, M. Pescatori, N. Saulnier, A. Lupascu, E. C. Nista, M. Novi, M. Candelli, V. Cimica, S. Mihm, et al. 2006. Characterization of gene expression profile in rat Kupffer cells stimulated with IFN-alpha or IFN-gamma. Dig. Liver Dis. 38:563-577. (Pubitemid 44356255)
37. Yang, K., H. X. Shi, X. Y. Liu, Y. F. Shan, B. Wei, S. Chen, and C. Wang. 2009. TRIM21 is essential to sustain IFN regulatory factor 3 activation during antiviral response. J. Immunol. 182:3782-3792.
38. Corona, G., C. Biagini, M. Rotondi, A. Bonamano, N. Cremonini, L. Petrone, B. Conforti, G. Forti, and M. Serio. 2008. Correlation between, clinical, biochemical, color Doppler ultrasound thyroid parameters, and CXCL-10 in autoimmune thyroid diseases. Endocr. J. 55:345-350. (Pubitemid 351670961)
39. Rotondi, M., R. Minelli, F. Magri, P. Leporati, P. Romagnani, M. C. Baroni, R. Delsignore, M. Serio, and L. Chiovato. 2007. Serum CXCL10 levels and occurrence of thyroid dysfunction in patients treated with interferon-alpha therapy for hepatitis C virus-related hepatitis. Eur. J. Endocrinol. 156:409-414. (Pubitemid 46679458)
40. Rotondi, M., L. Chiovato, S. Romagnani, M. Serio, and P. Romagnani. 2007. Role of chemokines in endocrine autoimmune diseases. Endocr. Rev. 28:492-520. (Pubitemid 47236335)
41. Antonelli, A., C. Ferri, P. Fallahi, S. M. Ferrari, A. Ghinoi, M. Rotondi, and E. Ferrannini. 2006. Thyroid disorders in chronic hepatitis C virus infection. Thyroid 16:563-572. (Pubitemid 44066263)
42. Antonelli, A., M. Rotondi, P. Fallahi, P. Romagnani, S. M. Ferrari, A. Buonamano, E. Ferrannini, and M. Serio. 2004. High levels of circulating CXC chemokine ligand 10 are associated with chronic autoimmune thyroiditis and hypothyroidism. J. Clin. Endocrinol. Metab. 89:5496-5499. (Pubitemid 39518431)
43. Akwa, Y., D. E. Hassett, M. L. Eloranta, K. Sandberg, E. Masliah, H. Powell, J. L. Whitton, F. E. Bloom, and I. L. Campbell. 1998. Transgenic expression of IFN-alpha in the central nervous system of mice protects against lethal neurotropic viral infection but induces inflammation and neurodegeneration. J. Immunol. 161:5016-5026. (Pubitemid 28492084)
44. Li, Q., B. Xu, S. A. Michie, K. H. Rubins, R. D. Schreriber, and H. O. McDevitt. 2008. Interferon-alpha initiates type 1 diabetes in nonobese diabetic mice. Proc. Natl. Acad. Sci. USA 105:12439-12444.
45. Stewart, T. A., B. Hultgren, X. Huang, S. Pitts-Meek, J. Hully, and N. J. MacLachlan. 1993. Induction of type I diabetes by interferon-alpha in transgenic mice. Science 260:1942-1946. (Pubitemid 23258275)
46. Caturegli, P., M. Hejazi, K. Suzuki, O. Dohan, N. Carrasco, L. D. Kohn, and N. R. Rose. 2000. Hypothyroidism in transgenic mice expressing IFN-gamma in the thyroid. Proc. Natl. Acad. Sci. USA 97:1719-1724. (Pubitemid 30118509)
47. Caturegli, P., and H. Kimura. 2010. A nonclassical model of autoimmune hypothyroidism. Thyroid 20:3-5.
48. Marinkovic, T., A. Garin, Y. Yokota, Y. X. Fu, N. H. Ruddle, G. C. Furtado, and S. A. Lira. 2006. Interaction of mature CD3+CD4+ T cells with dendritic cells triggers the development of tertiary lymphoid structures in the thyroid. J. Clin. Invest. 116:2622-2632. (Pubitemid 44511626)
49. Kuang, M., S. Wang, M. Wu, G. Ning, Z. Yao, and L. Li. 2010. Expression of IFNalpha-inducible genes and modulation of HLA-DR and thyroid stimulating hormone receptors in Graves' disease. Mol. Cell. Endocrinol. 319:23-29.
50. Akeno, N., J. T. Blackard, and Y. Tomer. 2008. HCV E2 protein binds directly to thyroid cells and induces IL-8 production: a new mechanism for HCV induced thyroid autoimmunity. J. Autoimmun. 31:339-344.
51. Tsan, M. F., and B. Gao. 2009. Heat shock proteins and immune system. J. Leukoc. Biol. 85:905-910.
52. Caraccio, N., R. Giannini, S. Cuccato, P. Faviana, P. Berti, D. Galleri, A. Dardano, F. Basolo, E. Ferrannini, and F. Monzani. 2005. Type I interferons modulate the expression of thyroid peroxidase, sodium/iodide symporter, and thyroglobulin genes in primary human thyrocyte cultures. J. Clin. Endocrinol. Metab. 90:1156-1162. (Pubitemid 40279248)
53. Antonelli, A., S. M. Ferrari, P. Fallahi, E. Ghiri, C. Crescioli, P. Romagnani, P. Vitti, M. Serio, and E. Ferrannini. 2010. Interferon-alpha,-beta and-gamma induce CXCL9 and CXCL10 secretion by human thyrocytes: modulation by peroxisome proliferator-activated receptor-gamma agonists. Cytokine 50:260-267.
54. Wenzel, J., S. Zahn, T. Bieber, and T. Tüting. 2009. Type I interferon-associated cytotoxic inflammation in cutaneous lupus erythematosus. Arch. Dermatol. Res. 301:83-86.
55. Wenzel, J., B. Bekisch, M. Uerlich, O. Haller, T. Bieber, and T. Tüting. 2005. Type I interferon-associated recruitment of cytotoxic lymphocytes: a common mechanism in regressive melanocytic lesions. Am. J. Clin. Pathol. 124:37-48. (Pubitemid 40944372)
56. Figueroa-Vega, N., M. Alfonso-Pérez, I. Benedicto, F. Sánchez-Madrid, R. González-Amaro, and M. Marazuela. 2010. Increased circulating proinflammatory cytokines and Th17 lymphocytes in Hashimoto's thyroiditis. J. Clin. Endocrinol. Metab. 95:953-962.
57. Chowdhury, D., and J. Lieberman. 2008. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu. Rev. Immunol. 26:389-420. (Pubitemid 351611623)
58. Voskoboinik, I., M. J. Smyth, and J. A. Trapani. 2006. Perforin-mediated targetcell death and immune homeostasis. Nat. Rev. Immunol. 6:940-952. (Pubitemid 44851736)
59. Niland, B., G. Miklossy, K. Banki, W. E. Biddison, L. Casciola-Rosen, A. Rosen, D. Martinvalet, J. Lieberman, and A. Perl. 2010. Cleavage of transaldolase by granzyme B causes the loss of enzymatic activity with retention of antigenicity for multiple sclerosis patients. J. Immunol. 184:4025-4032.
60. Thomas, H. E., J. A. Trapani, and T. W. Kay. 2010. The role of perforin and granzymes in diabetes. Cell Death Differ. 17:577-585.
61. Blanco, P., V. Pitard, J. F. Viallard, J. L. Taupin, J. L. Pellegrin, and J. F. Moreau. 2005. Increase in activated CD8+ T lymphocytes expressing perforin and granzyme B correlates with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum. 52:201-211. (Pubitemid 40129249)
62. Kroemer, G., L. Galluzzi, P. Vandenabeele, J. Abrams, E. S. Alnemri, E. H. Baehrecke, M. V. Blagosklonny, W. S. El-Deiry, P. Golstein, D. R. Green, et al; Nomenclature Committee on Cell Death. 2009. 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 16:3-11.
63. Lin, J. D. 2001. The role of apoptosis in autoimmune thyroid disorders and thyroid cancer. BMJ 322:1525-1527.
64. Golstein, P., and G. Kroemer. 2007. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 32:37-43. (Pubitemid 46043552)
65. Vieland, V. J., Y. Huang, C. Bartlett, T. F. Davies, and Y. Tomer. 2008. A multilocus model of the genetic architecture of autoimmune thyroid disorder, with clinical implications. Am. J. Hum. Genet. 82:1349-1356.
66. Oppenheim, Y., G. Kim, Y. Ban, P. Unger, E. Concepcion, T. Ando, and Y. Tomer. 2003. The effects of alpha interferon on the development of autoimmune thyroiditis in the NOD H2h4 mouse. Clin. Dev. Immunol. 10:161-165. (Pubitemid 38089407)
67. Ozato, K., D. M. Shin, T. H. Chang, and H. C. Morse, III. 2008. TRIM family proteins and their emerging roles ininnate immunity. Nat. Rev. Immunol. 8:849-860.
68. Carthagena, L., A. Bergamaschi, J. M. Luna, A. David, P. D. Uchil, F. Margottin-Goguet, W. Mothes, U. Hazan, C. Transy, G. Pancino, and S. Nisole. 2009. Human TRIM gene expression in response to interferons. PLoS One 4: e4894.
69. Ben-Chetrit, E., E. K. Chan, K. F. Sullivan, and E. M. Tan. 1988. A 52-kD protein is a novel component of the SS-A/Ro antigenic particle. J. Exp. Med. 167:1560-1571.
70. Nakken, B., R. Jonsson, and A. I. Bolstad. 2001. Polymorphisms of the Ro52 gene associated with anti-Ro 52-kd autoantibodies in patients with primary Sjögren's syndrome. Arthritis Rheum. 44:638-646.
71. Frank, M. B., K. Itoh, A. Fujisaku, P. Pontarotti, M. G. Mattei, and B. R. Neas. 1993. The mapping of the human 52-kD Ro/SSA autoantigen gene to human chromosome 11, and its polymorphisms. Am. J. Hum. Genet. 52:183-191. (Pubitemid 23059062)
72. Manoharan, A., and M. P. Madaio. 2010. Biomarkers in lupus nephritis. Rheum. Dis. Clin. North Am. 36:131-143, ix.
73. Tomer, Y., and T. F. Davies. 1993. Infection, thyroid disease, and autoimmunity. Endocr. Rev. 14:107-120. (Pubitemid 23066535)