Oral-resident natural Th17 cells and γδ T cells control opportunistic Candida albicans infections

Journal of Experimental Medicine

Volumn 211, Issue 10, 2014, Pages 2075-2084

  Conti, Heather R ^a   Peterson, Alanna C ^a   Brane, Lucas ^a   Huppler, Anna R ^c   Herna´ndez Santos, Nydiaris ^a   Whibley, Natasha ^a   Garg, Abhishek V ^a   Simpson Abelson, Michelle R ^a   Gibson, Gregory A ^b   Mamo, Anna J ^a   Osborne, Lisa C ^d   Bishu, Shrinivas ^a   Ghilardi, Nico ^e   Siebenlist, Ulrich ^f   Watkins, Simon C ^b   Artis, David ^d   McGeachy, Mandy J ^a   Gaffen, Sarah L ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e GENENTECH INC   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CYCLOSPORIN; HERMES ANTIGEN; INTERLEUKIN 17; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; IL17R PROTEIN, MOUSE; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 23; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANDIDA ALBICANS; CELLS; GAMMA DELTA T LYMPHOCYTE; INNATE IMMUNITY; INNATE LYMPHOID CELL; LABORATORY; LYMPHOID CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; OPPORTUNISTIC INFECTION; OROPHARYNX CANDIDIASIS; TH17 CELL; ANIMAL; CANDIDIASIS; CONFOCAL MICROSCOPY; CYTOLOGY; FLOW CYTOMETRY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MOUTH; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; FLOW CYTOMETRY; IMMUNITY, INNATE; INTERLEUKIN-23; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MOUTH; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, INTERLEUKIN-17; TH17 CELLS;

EID: 84907202739     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130877     Document Type: Article

References (55)

1. Acosta-Rodriguez, E.V., L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, and G. Napolitani. 2007. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8:639-646. http://dx.doi.org/10.1038/ ni1467
2. Ba¨r, E., A. Gladiator, S. Bastidas, B. Roschitzki, H. Acha-Orbea, A. Oxenius, and S. LeibundGut-Landmann. 2012. A novel Th cell epitope of Candida albicans mediates protection from fungal infection. J. Immunol. 188:5636-5643. http://dx.doi.org/10.4049/jimmunol.1200594
3. Bishu, S., N. Herna´ndez-Santos, M.R. Simpson-Abelson, A.R. Huppler, H.R. Conti, N. Ghilardi, A.J. Mamo, and S.L. Gaffen. 2014. The adaptor CARD9 is required for adaptive but not innate immunity to oral mucosal Candida albicans infections. Infect. Immun. 82:1173-1180. http://dx.doi.org/10.1128/IAI.01335-13
4. Boisson, B., C. Wang, V. Pedergnana, L. Wu, S. Cypowyj, M. Rybojad, A. Belkadi, C. Picard, L. Abel, C. Fieschi, et al. 2013. An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis. Immunity. 39:676-686. http://dx.doi.org/10.1016/j.immuni.2013.09.002
5. Brown, G.D., and M.G. Netea. 2012. Exciting developments in the immunology of fungal infections. Cell Host Microbe. 11:422-424. http:// dx.doi.org/10.1016/j.chom.2012.04.010
6. Browne, S.K., and S.M. Holland. 2010. Anti-cytokine autoantibodies explain some chronic mucocutaneous candidiasis. Immunol. Cell Biol. 88: 614-615. http://dx.doi.org/10.1038/icb.2010.72
7. Buonocore, S., P.P. Ahern, H.H. Uhlig, I.I. Ivanov, D.R. Littman, K.J. Maloy, and F. Powrie. 2010. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature. 464:1371-1375. http://dx.doi.org/10.1038/nature08949
8. Butler, G., M.D. Rasmussen, M.F. Lin, M.A. Santos, S. Sakthikumar, C.A. Munro, E. Rheinbay, M. Grabherr, A. Forche, J.L. Reedy, et al. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature. 459:657-662. http://dx.doi.org/10.1038/nature08064
9. Chen, Z., A. Laurence, Y. Kanno, M. Pacher-Zavisin, B.M. Zhu, C. Tato, A. Yoshimura, L. Hennighausen, and J.J. O'Shea. 2006. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc. Natl. Acad. Sci. USA. 103:8137-8142. http://dx.doi.org/10.1073/ pnas.0600666103
10. Conti, H.R., F. Shen, N. Nayyar, E. Stocum, J.N. Sun, M.J. Lindemann, A.W. Ho, J.H. Hai, J.J. Yu, J.W. Jung, et al. 2009. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 206:299-311. http://dx.doi.org/10.1084/jem.20081463
11. Cua, D.J., and C.M. Tato. 2010. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10:479-489. http://dx.doi.org/10.1038/nri2800
12. de Beaucoudrey, L., A. Samarina, J. Bustamante, A. Cobat, S. Boisson- Dupuis, J. Feinberg, S. Al-Muhsen, L. Jannie`re, Y. Rose, M. de Suremain, et al. 2010. Revisiting human IL-12Rβ1 deficiency: a survey of 141 patients from 30 countries. Medicine (Baltimore). 89:381-402. http://dx.doi.org/10.1097/MD.0b013e3181fdd832
13. Farah, C.S., S. Elahi, K. Drysdale, G. Pang, T. Gotjamanos, G.J. Seymour, R.L. Clancy, and R.B. Ashman. 2002. Primary role for CD4+ T lymphocytes in recovery from oropharyngeal candidiasis. Infect. Immun. 70:724-731. http://dx.doi.org/10.1128/IAI.70.2.724-731.2002
14. Farah, C.S., Y. Hu, S. Riminton, and R.B. Ashman. 2006. Distinct roles for interleukin-12p40 and tumour necrosis factor in resistance to oral candidiasis defined by gene-targeting. Oral Microbiol. Immunol. 21:252-255. http://dx.doi.org/10.1111/j.1399-302X.2006.00288.x
15. Ferreira, M.C., N. Whibley, A.J. Mamo, U. Siebenlist, Y.R. Chan, and S.L. Gaffen. 2014. Interleukin-17-induced protein lipocalin 2 is dispensable for immunity to oral candidiasis. Infect. Immun. 82:1030-1035. http:// dx.doi.org/10.1128/IAI.01389-13
16. Fidel, P.L. Jr. 2011. Candida-host interactions in HIV disease: implications for oropharyngeal candidiasis. Adv. Dent. Res. 23:45-49. http://dx.doi.org/10.1177/0022034511399284
17. Gladiator, A., N. Wangler, K. Trautwein-Weidner, and S. LeibundGut- Landmann. 2013. Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J. Immunol. 190:521-525. http://dx.doi.org/10.4049/jimmunol.1202924
18. Haines, C.J., Y. Chen, W.M. Blumenschein, R. Jain, C. Chang, B. Joyce- Shaikh, K. Porth, K. Boniface, J. Mattson, B. Basham, et al. 2013. Autoimmune memory T helper 17 cell function and expansion are dependent on interleukin-23. Cell Reports. 3:1378-1388. http://dx.doi.org/ 10.1016/j.celrep.2013.03.035
19. Herna´ndez-Santos, N., A.R. Huppler, A.C. Peterson, S.A. Khader, K.C. McKenna, and S.L. Gaffen. 2013. Th17 cells confer long-term adaptive immunity to oral mucosal Candida albicans infections. Mucosal Immunol. 6:900-910. http://dx.doi.org/10.1038/mi.2012.128
20. Hirota, K., J.H. Duarte, M. Veldhoen, E. Hornsby, Y. Li, D.J. Cua, H. Ahlfors, C. Wilhelm, M. Tolaini, U. Menzel, et al. 2011. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12:255-263. http://dx.doi.org/10.1038/ni.1993
21. Ho, A.W., F. Shen, H.R. Conti, N. Patel, E.E. Childs, A.C. Peterson, N. Herna´ndez-Santos, J.K. Kolls, L.P. Kane, W. Ouyang, and S.L. Gaffen. 2010. IL-17RC is required for immune signaling via an extended SEF/IL-17R signaling domain in the cytoplasmic tail. J. Immunol. 185:1063- 1070. http://dx.doi.org/10.4049/jimmunol.0903739
22. Holland, S.M., F.R. DeLeo, H.Z. Elloumi, A.P. Hsu, G. Uzel, N. Brodsky, A.F. Freeman, A. Demidowich, J. Davis, M.L. Turner, et al. 2007. STAT3 mutations in the hyper-IgE syndrome. N. Engl. J. Med. 357:1608-1619. http://dx.doi.org/10.1056/NEJMoa073687
23. Huppler, A.R., S. Bishu, and S.L. Gaffen. 2012. Mucocutaneous candidiasis: the IL-17 pathway and implications for targeted immunotherapy. Arthritis Res. Ther. 14:217. http://dx.doi.org/10.1186/ar3893
24. Huppler, A.R., H.R. Conti, N. Herna´ndez-Santos, T. Darville, P.S. Biswas, and S.L. Gaffen. 2014. Role of neutrophils in IL-17-dependent immunity to mucosal candidiasis. J. Immunol. 192:1745-1752. http://dx.doi.org/10.4049/jimmunol.1302265
25. Igya´rto´, B.Z., K. Haley, D. Ortner, A. Bobr, M. Gerami-Nejad, B.T. Edelson, S.M. Zurawski, B. Malissen, G. Zurawski, J. Berman, and D.H. Kaplan. 2011. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity. 35:260-272. http://dx.doi.org/10.1016/j.immuni.2011.06.005
26. Iliev, I.D., V.A. Funari, K.D. Taylor, Q. Nguyen, C.N. Reyes, S.P. Strom, J. Brown, C.A. Becker, P.R. Fleshner, M. Dubinsky, et al. 2012. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 336:1314-1317. http://dx.doi.org/ 10.1126/science.1221789
27. Itohara, S., A.G. Farr, J.J. Lafaille, M. Bonneville, Y. Takagaki, W. Haas, and S. Tonegawa. 1990. Homing of a γδ thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature. 343:754-757. http://dx.doi.org/10.1038/343754a0
28. Kagami, S., H.L. Rizzo, S.E. Kurtz, L.S. Miller, and A. Blauvelt. 2010. IL-23 and IL-17A, but not IL-12 and IL-22, are required for optimal skin host defense against Candida albicans. J. Immunol. 185:5453-5462. http://dx.doi.org/10.4049/jimmunol.1001153
29. Kamai, Y., M. Kubota, Y. Kamai, T. Hosokawa, T. Fukuoka, and S.G. Filler. 2001. New model of oropharyngeal candidiasis in mice. Antimicrob. Agents Chemother. 45:3195-3197. http://dx.doi.org/10.1128/AAC.45.11.3195-3197.2001
30. Kaplan, M.H., U. Schindler, S.T. Smiley, and M.J. Grusby. 1996. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity. 4:313-319. http://dx.doi.org/10.1016/S1074-7613 (00)80439-2
31. Lee, P.P., D.R. Fitzpatrick, C. Beard, H.K. Jessup, S. Lehar, K.W. Makar, M. Pe´rez-Melgosa, M.T. Sweetser, M.S. Schlissel, S. Nguyen, et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity. 15:763-774. http://dx.doi.org/10.1016/S1074-7613(01)00227-8
32. Lin, L., A.S. Ibrahim, X. Xu, J.M. Farber, V. Avanesian, B. Baquir, Y. Fu, S.W. French, J.E. Edwards Jr., and B. Spellberg. 2009. Th1-Th17 cells mediate protective adaptive immunity against Staphylococcus aureus and Candida albicans infection in mice. PLoS Pathog. 5:e1000703. http:// dx.doi.org/10.1371/journal.ppat.1000703
33. Liu, L., S. Okada, X.F. Kong, A.Y. Kreins, S. Cypowyj, A. Abhyankar, J. Toubiana, Y. Itan, M. Audry, P. Nitschke, et al. 2011. Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J. Exp. Med. 208:1635-1648. http://dx.doi.org/10.1084/jem.20110958
34. Marks, B.R., H.N. Nowyhed, J.Y. Choi, A.C. Poholek, J.M. Odegard, R.A. Flavell, and J. Craft. 2009. Thymic self-reactivity selects natural interleukin 17-producing T cells that can regulate peripheral inflammation. Nat. Immunol. 10:1125-1132. http://dx.doi.org/10.1038/ni.1783
35. Martin, B., K. Hirota, D.J. Cua, B. Stockinger, and M. Veldhoen. 2009. Interleukin-17-producing γδ T cells selectively expand in response to pathogen products and environmental signals. Immunity. 31:321-330. http://dx.doi.org/10.1016/j.immuni.2009.06.020
36. Massot, B., M.L. Michel, S. Diem, C. Ohnmacht, S. Latour, M. Dy, G. Eberl, and M.C. Leite-de-Moraes. 2014. TLR-induced cytokines promote effective proinflammatory natural Th17 cell responses. J. Immunol. 192:5635-5642. http://dx.doi.org/10.4049/jimmunol.1302089
37. McGeachy, M.J., Y. Chen, C.M. Tato, A. Laurence, B. Joyce-Shaikh, W.M. Blumenschein, T.K. McClanahan, J.J. O'Shea, and D.J. Cua. 2009. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10:314-324. http://dx.doi.org/10.1038/ni.1698
38. Milner, J.D., and S.M. Holland. 2013. The cup runneth over: lessons from the ever-expanding pool of primary immunodeficiency diseases. Nat. Rev. Immunol. 13:635-648.
39. Ouederni, M., O. Sanal, A. Ikinciogullari, I. Tezcan, F. Dogu, I. Sologuren, S. Pedraza-Sa´nchez, M. Keser, G. Tanir, C. Nieuwhof, et al. 2014. Clinical features of Candidiasis in patients with inherited interleukin 12 receptor β1 deficiency. Clin. Infect. Dis. 58:204-213. http://dx.doi.org/10.1093/cid/cit722
40. Pandiyan, P., H.R. Conti, L. Zheng, A.C. Peterson, D.R. Mathern, N. Herna´ndez-Santos, M. Edgerton, S.L. Gaffen, and M.J. Lenardo. 2011. CD4+CD25+Foxp3+ regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity. 34:422-434. http://dx.doi.org/10.1016/j.immuni.2011.03.002
41. Prinz, I. 2011. Dynamics of the interaction of γδ T cells with their neighbors in vivo. Cell. Mol. Life Sci. 68:2391-2398. http://dx.doi.org/10.1007/s00018-011-0701-y
42. Puel, A., C. Picard, S. Cypowyj, D. Lilic, L. Abel, and J.L. Casanova. 2010. Inborn errors of mucocutaneous immunity to Candida albicans in humans: a role for IL-17 cytokines? Curr. Opin. Immunol. 22:467-474. http://dx.doi.org/10.1016/j.coi.2010.06.009
43. Puel, A., S. Cypowyj, J. Bustamante, J.F. Wright, L. Liu, H.K. Lim, M. Migaud, L. Israel, M. Chrabieh, M. Audry, et al. 2011. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science. 332:65-68. http://dx.doi.org/10.1126/science.1200439
44. Ribot, J.C., A. deBarros, D.J. Pang, J.F. Neves, V. Peperzak, S.J. Roberts, M. Girardi, J. Borst, A.C. Hayday, D.J. Pennington, and B. Silva- Santos. 2009. CD27 is a thymic determinant of the balance between interferon-γ- and interleukin 17-producing γδ T cell subsets. Nat. Immunol. 10:427-436. http://dx.doi.org/10.1038/ni.1717
45. Robins, H. 2013. Immunosequencing: applications of immune repertoire deep sequencing. Curr. Opin. Immunol. 25:646-652. http://dx.doi.org/ 10.1016/j.coi.2013.09.017
46. Sherlock, J.P., B. Joyce-Shaikh, S.P. Turner, C.C. Chao, M. Sathe, J. Grein, D.M. Gorman, E.P. Bowman, T.K. McClanahan, J.H. Yearley, et al. 2012. IL-23 induces spondyloarthropathy by acting on ROR-γt+ CD3+CD4-CD8- entheseal resident T cells. Nat. Med. 18:1069-1076. http://dx.doi.org/10.1038/nm.2817
47. Spellberg, B.J., A.S. Ibrahim, V. Avanesian, Y. Fu, C. Myers, Q.T. Phan, S.G. Filler, M.R. Yeaman, and J.E. Edwards Jr. 2006. Efficacy of the anti-Candida rAls3p-N or rAls1p-N vaccines against disseminated and mucosal candidiasis. J. Infect. Dis. 194:256-260. http://dx.doi.org/10.1086/504691
48. Spits, H., D. Artis, M. Colonna, A. Diefenbach, J.P. Di Santo, G. Eberl, S. Koyasu, R.M. Locksley, A.N. McKenzie, R.E. Mebius, et al. 2013. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:145-149. http://dx.doi.org/10.1038/nri3365
49. Sutton, C.E., S.J. Lalor, C.M. Sweeney, C.F. Brereton, E.C. Lavelle, and K.H. Mills. 2009. Interleukin-1 and IL-23 induce innate IL-17 production from γδ T cells, amplifying Th17 responses and autoimmunity. Immunity. 31:331-341. http://dx.doi.org/10.1016/j.immuni.2009.08.001
50. Sutton, C.E., L.A. Mielke, and K.H. Mills. 2012. IL-17-producing γδ T cells and innate lymphoid cells. Eur. J. Immunol. 42:2221-2231. http:// dx.doi.org/10.1002/eji.201242569
51. Takatori, H., Y. Kanno, W.T. Watford, C.M. Tato, G. Weiss, I.I. Ivanov II, D.R. Littman, and J.J. O'Shea. 2009. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J. Exp. Med. 206:35-41. http://dx.doi.org/10.1084/jem.20072713
52. Tanaka, S., T. Yoshimoto, T. Naka, S. Nakae, Y. Iwakura, D. Cua, and M. Kubo. 2009. Natural occurring IL-17 producing T cells regulate the initial phase of neutrophil mediated airway responses. J. Immunol. 183:7523-7530. http://dx.doi.org/10.4049/jimmunol.0803828
53. Wu¨thrich, M., B. Gern, C.Y. Hung, K. Ersland, N. Rocco, J. Pick-Jacobs, K. Galles, H. Filutowicz, T. Warner, M. Evans, et al. 2011. Vaccine-induced protection against 3 systemic mycoses endemic to North America requires Th17 cells in mice. J. Clin. Invest. 121:554-568. http://dx.doi.org/10.1172/JCI43984
54. Yang, X.O., A.D. Panopoulos, R. Nurieva, S.H. Chang, D. Wang, S.S. Watowich, and C. Dong. 2007. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282:9358- 9363. http://dx.doi.org/10.1074/jbc.C600321200
55. Zu´ñiga, L.A., R. Jain, C. Haines, and D.J. Cua. 2013. Th17 cell development: from the cradle to the grave. Immunol. Rev. 252:78-88. http:// dx.doi.org/10.1111/imr.12036