IL-1 receptor antagonist-deficient mice develop autoimmune arthritis due to intrinsic activation of IL-17-producing CCR2 + Vγ6 + γδT cells

Nature Communications

Volumn 6, Issue , 2015, Pages

  Akitsu, Aoi ^a,b,c,d   Ishigame, Harumichi ^a,g   Kakuta, Shigeru ^a,h   Chung, Soo Hyun ^a,d   Ikeda, Satoshi ^a   Shimizu, Kenji ^a,d   Kubo, Sachiko ^a,d   Liu, Yang ^a,i   Umemura, Masayuki ^e   Matsuzaki, Goro ^e   Yoshikai, Yasunobu ^f   Saijo, Shinobu ^a,j   Iwakura, Yoichiro ^a,c,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d TOKYO UNIVERSITY OF SCIENCE   (Japan)

^e UNIVERSITY OF THE RYUKYUS   (Japan)

^f KYUSHU UNIVERSITY   (Japan)

^g Institute of Physical and Chemical Research   (Japan)

^h UNIVERSITY OF TOKYO   (Japan)

ⁱ SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^j CHIBA UNIVERSITY   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR2; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 17; MONOCYTE CHEMOTACTIC PROTEIN 1; CCL2 PROTEIN, MOUSE; IL1R1 PROTEIN, MOUSE; IL1RN PROTEIN, MOUSE; INTERLEUKIN 1 RECEPTOR TYPE I; LYMPHOCYTE ANTIGEN RECEPTOR;

CYTOLOGY; GENE EXPRESSION; IMMUNE RESPONSE; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; GAMMA DELTA T LYMPHOCYTE; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; JOINT; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION;

MUS;

ANIMALS; ARTHRITIS; AUTOIMMUNE DISEASES; CHEMOKINE CCL2; GENE EXPRESSION REGULATION; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-17; JOINTS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, INTERLEUKIN-1 TYPE I; T-LYMPHOCYTE SUBSETS;

EID: 84933074064     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8464     Document Type: Article

References (54)

1. Iwakura, Y., Ishigame, H., Saijo, S. & Nakae, S. Functional specialization of interleukin-17 family members. Immunity. 34, 149-162 (2011
2. Kellner, H. Targeting interleukin-17 in patients with active rheumatoid arthritis: rationale and clinical potential. Ther. Adv. Musculoskelet. Dis. 5, 141-152 (2013
3. Cua, D. J. & Tato, C. M. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10, 479-489 (2010
4. Akitsu, A., Kakuta, S., Saijo, S. & Iwakura, Y. Rag2-deficient IL-1 receptor antagonist-deficient mice are a novel colitis model in which innate lymphoid cell-derived IL-17 is involved in the pathogenesis. Exp. Anim. 63, 235-246 (2014
5. Sutton, C. E, et al. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity. 31, 331-341 (2009
6. Petermann, F, et al. gd T cells enhance autoimmunity by restraining regulatory T cell responses via an interleukin-23-dependent mechanism. Immunity. 33, 351-363 (2010
7. Roark, C. L, et al. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J. Immunol. 179, 5576-5583 (2007
8. Park, S.-G, et al. T regulatory cells maintain intestinal homeostasis by suppressing gd T cells. Immunity. 33, 791-803 (2010
9. Gray, E. E., Suzuki, K. & Cyster, J. G. Cutting edge: identification of a motile IL-17-producing T cell population in the dermis. J. Immunol. 186, 6091-6095 (2011
10. Sumaria, N, et al. Cutaneous immunosurveillance by self-renewing dermal gammadelta T cells. J. Exp. Med. 208, 505-518 (2011
11. Cai, Y, et al. Pivotal role of dermal IL-17-producing gd T cells in skin inflammation. Immunity. 35, 596-610 (2011
12. Gray, E. E, et al. Deficiency in IL-17-committed Vg4(+) gd T cells in a spontaneous Sox13-mutant CD45.1(+) congenic mouse substrain provides protection from dermatitis. Nat. Immunol. 14, 584-592 (2013
13. Ito, Y, et al. Gamma/delta T cells are the predominant source of interleukin-17 in affected joints in collagen-induced arthritis, but not in rheumatoid arthritis. Arthritis Rheum. 60, 2294-2303 (2009
14. Roark, C. L, et al. A canonical Vg4Vd4+ gd T cell population with distinct stimulation requirements which promotes the Th17 response. Immunol. Res. 55, 217-230 (2012
15. Shibata, K, et al. Identification of CD25+ gamma delta T cells as fetal thymusderived naturally occurring IL-17 producers. J. Immunol. 181, 5940-5947 (2008
16. Ribot, J. C, et al. CD27 is a thymic determinant of the balance between interferon-gamma- And interleukin. 17-producing gammadelta T cell subsets. Nat. Immunol. 10, 427-436 (2009
17. Haas, J. D, et al. CCR6 and NK1.1 distinguish between IL-17A and IFNgamma-producing gammadelta effector T cells. Eur. J. Immunol. 39, 3488-3497 (2009
18. Narayan, K, et al. Intrathymic programming of effector fates in three molecularly distinct gd T cell subtypes. Nat. Immunol. 13, 511-518 (2012
19. Prinz, I., Silva-Santos, B. & Pennington, D. J. Functional development of gd T cells. Eur. J. Immunol. 43, 1988-1994 (2013
20. Duan, J., Chung, H., Troy, E. & Kasper, D. L. Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells. Cell Host Microbe 7, 140-150 (2010
21. Laird, R. M., Laky, K. & Hayes, S. M. Unexpected role for the B cell-specific Src family kinase B lymphoid kinase in the development of IL-17-producing T cells. J. Immunol. 185, 6518-6527 (2010
22. Shibata, K, et al. Notch-Hes1 pathway is required for the development of IL-17-producing gd T cells. Blood. 118, 586-593 (2011
23. Powolny-Budnicka, I, et al. RelA and RelB transcription factors in distinct thymocyte populations control lymphotoxin-dependent interleukin-17 production in gd T cells. Immunity. 34, 364-374 (2011
24. Malhotra, N, et al. A network of high-mobility group box transcription factors programs innate interleukin-17 production. Immunity. 38, 681-693 (2013
25. Pereira, P, et al. Rearrangement and expression of V g1, V g2 and V g3 TCR g genes in C57BL/6 mice. Int. Immunol. 8, 83-90 (1996
26. O'Brien, R. L. & Born, W. K. gammadelta T cell subsets: a link between TCR and function?. Semin. Immunol. 22, 193-198 (2010
27. Heilig, J. S. & Tonegawa, S. Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature. 322, 836-840 (1986
28. Cai, Y, et al. Differential developmental requirement and peripheral regulation for dermal Vg4 and Vg6T17 cells in health and inflammation. Nat. Commun. 5, 3986 (2014
29. Itohara, S, et al. Homing of a gamma delta thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature. 343, 754-757 (1990
30. Bonneville, M., O'Brien, R. L. & Born, W. K. Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10, 467-478 (2010
31. Horai, R, et al. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J. Exp. Med. 191, 313-320 (2000
32. Nakae, S, et al. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc. Natl Acad. Sci. USA. 100, 5986-5990 (2003
33. Horai, R, et al. TNF-Alpha is crucial for the development of autoimmune arthritis in IL-1 receptor antagonist-deficient mice. J. Clin. Invest. 114, 1603-1611 (2004
34. Fujikado, N., Saijo, S. & Iwakura, Y. Identification of arthritis-related gene clusters by microarray analysis of two independent mouse models for rheumatoid arthritis. Arthritis Res. Ther. 8, R100 (2006
35. Lalor, S. J, et al. Caspase-1-processed cytokines IL-1beta and IL-18 promote IL-17 production by gammadelta and CD4 T cells that mediate autoimmunity. J. Immunol. 186, 5738-5748 (2011
36. Nakamura, R, et al. Tyk2-signaling plays an important role in host defense against Escherichia coli through IL-23-induced IL-17 production by gammadelta T cells. J. Immunol. 181, 2071-2075 (2008
37. Hayes, S. M. & Laird, R. M. Genetic requirements for the development and differentiation of interleukin-17-producing gd T cells. Crit. Rev. Immunol. 32, 81-95 (2012
38. Lafaille, J. J., DeCloux, A., Bonneville, M., Takagaki, Y. & Tonegawa, S. Junctional sequences of T cell receptor gamma delta genes: implications for gamma delta T cell lineages and for a novel intermediate of V-(D)-J joining. Cell. 59, 859-870 (1989).
39. Koenecke, C, et al. In vivo application of mAb directed against the gd TCR does not deplete but generates 'invisible' gd T cells. Eur. J. Immunol. 39, 372-379 (2009
40. Shibata, K., Yamada, H., Hara, H., Kishihara, K. & Yoshikai, Y. Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 178, 4466-4472 (2007
41. Lanc'a, T, et al. Protective role of the inflammatory CCR2/CCL2 chemokine pathway through recruitment of type 1 cytotoxic gd T lymphocytes to tumor beds. J. Immunol. 190, 6673-6680 (2013
42. Hirota, K, et al. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J. Exp. Med. 204, 2803-2812 (2007
43. Reboldi, A, et al. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10, 514-523 (2009
44. Arima, Y, et al. Regional neural activation defines a gateway for autoreactive T cells to cross the blood-brain barrier. Cell. 148, 447-457 (2012
45. Reddy, S, et al. An autoinflammatory disease due to homozygous deletion of the IL1RN locus. N. Engl. J. Med. 360, 2438-2444 (2009
46. Aksentijevich, I, et al. An autoinflammatory disease with deficiency of the interleukin-1-receptor antagonist. N. Engl. J. Med. 360, 2426-2437 (2009
47. Haas, J. D, et al. Development of interleukin-17-producing gd T cells is restricted to a functional embryonic wave. Immunity. 37, 48-59 (2012
48. Kenna, T. J, et al. Enrichment of circulating interleukin-17-secreting interleukin-23 receptor-positive g/d T cells in patients with active ankylosing spondylitis. Arthritis Rheum. 64, 1420-1429 (2012
49. Caccamo, N, et al. Differentiation, phenotype, and function of interleukin-17-producing human Vg9Vd2 T cells. Blood. 118, 129-138 (2011
50. Hueber, A. J, et al. Mast cells express IL-17A in rheumatoid arthritis synovium. J. Immunol. 184, 3336-3340 (2010
51. Horai, R, et al. Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 187, 1463-1475 (1998
52. Itohara, S, et al. T cell receptor delta gene mutant mice: independent generation of alpha beta T cells and programmed rearrangements of gamma delta TCR genes. Cell. 72, 337-348 (1993
53. Houlden, B. A, et al. A TCR gamma delta cell recognizing a novel TL-encoded gene product. Cold Spring Harb. Symp. Quant. Biol. 54(Pt 1): 45-55 (1989
54. Komiyama, Y, et al. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177, 566-573 (2006