Inflammation induces dermal Vγ4+ γδT17 memory-like cells that travel to distant skin and accelerate secondary IL-17-driven responses

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 26, 2015, Pages 8046-8051

  Ramírez Valle, Francisco ^a   Gray, Elizabeth E ^a,c   Cyster, Jason G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Immunological memory; Inflammation; T cells

Indexed keywords

BETA DEFENSIN 3; BETA DEFENSIN 4; CHEMOKINE RECEPTOR CCR2; CXCL2 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FINGOLIMOD; IMIQUIMOD; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 1BETA; INTERLEUKIN 23; MESSENGER RNA; PADGEM PROTEIN; AMINOQUINOLINE DERIVATIVE; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL EXPANSION; CELL PROLIFERATION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DERMATITIS; GAMMA DELTA T LYMPHOCYTE; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MEMORY T LYMPHOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN SENSITIZATION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VGAMMA4+ GAMMA DELTA T17 MEMORY LIKE CELL; ANIMAL; DRUG EFFECTS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLAMMATION; METABOLISM; SKIN;

MUS;

AMINOQUINOLINES; ANIMALS; IMMUNOLOGIC MEMORY; INFLAMMATION; INTERLEUKIN-17; MICE; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SKIN; T-LYMPHOCYTES;

EID: 84937945349     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1508990112     Document Type: Article

References (39)

1. Belkaid Y, Segre JA (2014) Dialogue between skin microbiota and immunity. Science 346(6212):954-959.
2. Sumaria N, et al. (2011) Cutaneous immunosurveillance by self-renewing dermal gammadelta T cells. J Exp Med 208(3):505-518.
3. Cai Y, et al. (2011) Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity 35(4):596-610.
4. Gray EE, Suzuki K, Cyster JG (2011) Cutting edge: Identification of a motile IL-17-producing gammadelta T cell population in the dermis. J Immunol 186(11):6091-6095.
5. Pantelyushin S, et al. (2012) Rorγt+ innate lymphocytes and γδ T cells initiate psoriasiform plaque formation in mice. J Clin Invest 122(6):2252-2256.
6. Heilig JS, Tonegawa S (1986) Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature 322(6082):836-840.
7. Gray EE, et al. (2013) Deficiency in IL-17-committed Vγ4(+) γδ T cells in a spontaneous Sox13-mutant CD45.1(+) congenic mouse substrain provides protection from dermatitis. Nat Immunol 14(6):584-592.
8. Cai Y, et al. (2014) Differential developmental requirement and peripheral regulation for dermal Vγ4 and Vγ6T17 cells in health and inflammation. Nat Commun 5:3986.
9. O'Brien RL, Born WK (2015) Dermal γδ T cells: What have we learned? Cell Immunol, 10.1016/j.cellimm.2015.01.011.
10. Roark CL, et al. (2007) Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J Immunol 179(8):5576-5583.
11. Nakamizo S, et al. (2015) Dermal Vγ4(+) γδ T cells possess a migratory potency to the draining lymph nodes and modulate CD8(+) T-cell activity through TNF-α production. J Invest Dermatol 135(4):1007-1015.
12. Haas JD, et al. (2012) Development of interleukin-17-producing γδ T cells is restricted to a functional embryonic wave. Immunity 37(1):48-59.
13. Woodward Davis AS, Bergsbaken T, Delaney MA, Bevan MJ (2015) Dermal-resident versus recruited γδ T cell response to cutaneous vaccinia virus infection. J Immunol 194(5):2260-2267.
14. Puel A, et al. (2012) Inborn errors of human IL-17 immunity underlie chronic mucocutaneous candidiasis. Curr Opin Allergy Clin Immunol 12(6):616-622.
15. Laggner U, et al. (2011) Identification of a novel proinflammatory human skin-homing Vγ9Vδ2 T cell subset with a potential role in psoriasis. J Immunol 187(5):2783-2793.
16. Gatzka M, et al. (2013) Reduction of CD18 promotes expansion of inflammatory γδ T cells collaborating with CD4+ T cells in chronic murine psoriasiform dermatitis. J Immunol 191(11):5477-5488.
17. van der Fits L, et al. (2009) Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol 182(9):5836-5845.
18. Malhotra N, et al.; Immunological Genome Project Consortium (2013) A network of high-mobility group box transcription factors programs innate interleukin-17 production. Immunity 38(4):681-693.
19. Sutton CE, et al. (2009) Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31(2):331-341.
20. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M (2009) Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31(2):321-330.
21. Sheridan BS, et al. (2013) γδ T cells exhibit multifunctional and protective memory in intestinal tissues. Immunity 39(1):184-195.
22. Murphy AG, et al. (2014) Staphylococcus aureus infection of mice expands a population of memory γδ T cells that are protective against subsequent infection. J Immunol 192(8):3697-3708.
23. Matloubian M, et al. (2004) Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427(6972):355-360.
24. Fuhlbrigge RC, Kieffer JD, Armerding D, Kupper TS (1997) Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature 389(6654):978-981.
25. Mabuchi T, et al. (2013) CCR6 is required for epidermal trafficking of γδ-T cells in an IL-23-induced model of psoriasiform dermatitis. J Invest Dermatol 133(1):164-171.
26. Vestergaard C, Just H, Baumgartner Nielsen J, Thestrup-Pedersen K, Deleuran M (2004) Expression of CCR2 on monocytes and macrophages in chronically inflamed skin in atopic dermatitis and psoriasis. Acta Derm Venereol 84(5):353-358.
27. Willenborg S, et al. (2012) CCR2 recruits an inflammatory macrophage subpopulation critical for angiogenesis in tissue repair. Blood 120(3):613-625.
28. Gillitzer R, et al. (1993) MCP-1 mRNA expression in basal keratinocytes of psoriatic lesions. J Invest Dermatol 101(2):127-131.
29. Khmaladze Ia, et al. (2014) Mannan induces ROS-regulated, IL-17A-dependent psoriasis arthritis-like disease in mice. Proc Natl Acad Sci USA 111(35):E3669-E3678.
30. Moran AE, et al. (2011) T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J Exp Med 208(6):1279-1289.
31. Patel U, Mark NM, Machler BC, Levine VJ (2011) Imiquimod 5% cream induced psoriasis: A case report, summary of the literature and mechanism. Br J Dermatol 164(3):670-672.
32. Michel M-L, et al. (2012) Interleukin 7 (IL-7) selectively promotes mouse and human IL-17-producing γδ cells. Proc Natl Acad Sci USA 109(43):17549-17554.
33. Chong BF, Murphy J-E, Kupper TS, Fuhlbrigge RC (2004) E-selectin, thymus- and activation-regulated chemokine/CCL17, and intercellular adhesion molecule-1 are constitutively coexpressed in dermal microvessels: A foundation for a cutaneous immunosurveillance system. J Immunol 172(3):1575-1581.
34. Penido C, Vieira-de-Abreu A, Bozza MT, Castro-Faria-Neto HC, Bozza PT (2003) Role of monocyte chemotactic protein-1/CC chemokine ligand 2 on gamma delta T lymphocyte trafficking during inflammation induced by lipopolysaccharide or Mycobacterium bovis bacille Calmette-Guérin. J Immunol 171(12):6788-6794.
35. Fütterer A, Mink K, Luz A, Kosco-Vilbois MH, Pfeffer K (1998) The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 9(1):59-70.
36. Naik S, et al. (2012) Compartmentalized control of skin immunity by resident commensals. Science 337(6098):1115-1119.
37. Hwang J, et al. (2011) Epidermal ablation of Dlx3 is linked to IL-17-associated skin inflammation. Proc Natl Acad Sci USA 108(28):11566-11571.
38. Kobayashi T, et al. (2015) Dysbiosis and Staphyloccus aureus colonization drives inflammation in atopic dermatitis. Immunity 42(4):756-766.
39. Wu W, Debbaneh M, Moslehi H, Koo J, Liao W (2014) Tonsillectomy as a treatment for psoriasis: A review. J Dermatolog Treat 25(6):482-486.