Androgen signaling negatively controls group 2 innate lymphoid cells

Journal of Experimental Medicine

Volumn 214, Issue 6, 2017, Pages 1581-1592

  Laffont, Sophie ^a   Blanquart, Eve ^a   Savignac, Magali ^a   Cénac, Claire ^a   Laverny, Gilles ^b   Metzger, Daniel ^b   Girard, Jean Philippe ^c   Belz, Gabrielle T ^d   Pelletier, Lucette ^a   Seillet, Cyril ^d   Guéry, Jean Charles ^a  

^a University of Toulouse III   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; ANDROGEN; ANDROGEN RECEPTOR; CD11B ANTIGEN; CD3 ANTIGEN; GLYCOPROTEIN P 15095; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 33; INTERLEUKIN 5; THY 1 ANTIGEN; TRANSCRIPTION FACTOR GATA 3;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; FEMALE; HOMEOSTASIS; IMMUNE RESPONSE; INTRACELLULAR SIGNALING; LYMPHOID CELL; MALE; MOUSE; NONHUMAN; ORCHIECTOMY; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; ANIMAL; ASTHMA; C57BL MOUSE; CASTRATION; CELL PROLIFERATION; COMPLICATION; DRUG EFFECTS; HYPERSENSITIVITY; IMMUNOLOGY; INNATE IMMUNITY; LUNG; LYMPHOCYTE; LYMPHOCYTE COUNT; METABOLISM; PATHOLOGY; PNEUMONIA; PYROGLYPHIDAE; SEXISM; SIGNAL TRANSDUCTION;

ANDROGENS; ANIMALS; ASTHMA; CASTRATION; CELL PROLIFERATION; DISEASE SUSCEPTIBILITY; FEMALE; HYPERSENSITIVITY; IMMUNITY, INNATE; INTERLEUKIN-33; LUNG; LYMPHOCYTE COUNT; LYMPHOCYTES; MALE; MICE, INBRED C57BL; PNEUMONIA; PYROGLYPHIDAE; RECEPTORS, ANDROGEN; SEXISM; SIGNAL TRANSDUCTION;

EID: 85021855365     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20161807     Document Type: Article

References (39)

1. Almqvist, C., M. Worm, and B. Leynaert. Working group of GA2LEN WP 2.5 Gender. 2008. Impact of gender on asthma in childhood and adolescence: A GA2LEN review. Allergy. 63:47-57. http ://dx .doi .org/10 .1111/j .1398-9995 .2007 .01524 .x
2. Barlow, J.L., S. Peel, J. Fox, V. Panova, C.S. Hardman, A. Camelo, C. Bucks, X. Wu, C.M. Kane, D.R. Neill, et al. 2013. IL-33 is more potent than IL-25 in provoking IL-13-producing nuocytes (type 2 innate lymphoid cells) and airway contraction. J. Allergy Clin. Immunol. 132:933-941. http ://dx .doi .org/10 .1016/j .jaci .2013 .05 .012
3. + CD44hi lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J. Immunol. 188:1503-1513. http ://dx .doi .org/10 .4049/jimmunol .1102832
4. Carey, M.A., J.W. Card, J.W. Voltz, S.J. Arbes Jr., D.R. Germolec, K.S. Korach, and D.C. Zeldin. 2007. It's all about sex: Gender, lung development and lung disease. Trends Endocrinol. Metab. 18:308-313. http ://dx .doi .org/10 .1016/j .tem .2007 .08 .003
5. Doherty, T.A., N. Khorram, S. Lund, A.K. Mehta, M. Croft, and D.H. Broide. 2013. Lung type 2 innate lymphoid cells express cysteinyl leukotriene receptor 1, which regulates TH2 cytokine production. J. Allergy Clin. Immunol. 132:205-213. http ://dx .doi .org/10 .1016/j .jaci .2013 .03 .048
6. Eberl, G., M. Colonna, J.P. Di Santo, and A.N. McKenzie. 2015. Innate lymphoid cells: A new paradigm in immunology. Science. 348:aaa6566. http ://dx .doi .org/10 .1126/science .aaa6566
7. Gasteiger, G., X. Fan, S. Dikiy, S.Y. Lee, and A.Y. Rudensky. 2015. Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science. 350:981-985. http ://dx .doi .org/10 .1126/science .aac9593
8. Gold, M.J., F. Antignano, T.Y. Halim, J.A. Hirota, M.R. Blanchet, C. Zaph, F. Takei, and K.M. McNagny. 2014. Group 2 innate lymphoid cells facilitate sensitization to local, but not systemic, TH2-inducing allergen exposures. J. Allergy Clin. Immunol. 133:1142-1148.e5. http ://dx .doi .org/10 .1016/j .jaci .2014 .02 .033
9. Halim, T.Y.F., R.H. Krauss, A.C. Sun, and F. Takei. 2012. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergeninduced airway inflammation. Immunity. 36:451-463. http ://dx .doi .org/10 .1016/j .immuni .2011 .12 .020
10. Halim, T.Y.F., C.A. Steer, L. Mathä, M.J. Gold, I. Martinez-Gonzalez, K.M. McNagny, A.N.J. McKenzie, and F. Takei. 2014. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity. 40:425-435. http ://dx .doi .org/10 .1016/j .immuni .2014 .01 .011
11. Hoyler, T., C.S. Klose, A. Souabni, A. Turqueti-Neves, D. Pfeifer, E.L. Rawlins, D. Voehringer, M. Busslinger, and A. Diefenbach. 2012. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity. 37:634-648. http ://dx .doi .org/10 .1016/j .immuni .2012 .06 .020
12. hi cells are multipotential 'inflammatory' type 2 innate lymphoid cells. Nat. Immunol. 16:161-169. http ://dx .doi .org/10 .1038/ni .3078
13. Hwang, L.L., C.H. Wang, T.L. Li, S.D. Chang, L.C. Lin, C.P. Chen, C.T. Chen, K.C. Liang, I.K. Ho, W.S. Yang, and L.C. Chiou. 2010. Sex differences in high-fat diet-induced obesity, metabolic alterations and learning, and synaptic plasticity deficits in mice. Obesity (Silver Spring). 18:463-469. http ://dx .doi .org/10 .1038/oby .2009 .273
14. Imai, Y., K. Yasuda, Y. Sakaguchi, T. Haneda, H. Mizutani, T. Yoshimoto, K. Nakanishi, and K. Yamanishi. 2013. Skin-specific expression of IL-33 activates group 2 innate lymphoid cells and elicits atopic dermatitis-like inflammation in mice. Proc. Natl. Acad. Sci. USA. 110:13921-13926. http ://dx .doi .org/10 .1073/pnas .1307321110
15. Keselman, A., and N. Heller. 2015. Estrogen signaling modulates allergic inflammation and contributes to sex differences in asthma. Front. Immunol. 6:568. http ://dx .doi .org/10 .3389/fimmu .2015 .00568
16. Kim, B.S., M.C. Siracusa, S.A. Saenz, M. Noti, L.A. Monticelli, G.F. Sonnenberg, M.R. Hepworth, A.S. Van Voorhees, M.R. Comeau, and D. Artis. 2013. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci. Transl. Med. 5:170ra16. http ://dx .doi .org/10 .1126/scitranslmed .3005374
17. Kissick, H.T., M.G. Sanda, L.K. Dunn, K.L. Pellegrini, S.T. On, J.K. Noel, and M.S. Arredouani. 2014. Androgens alter T-cell immunity by inhibiting T-helper 1 differentiation. Proc. Natl. Acad. Sci. USA. 111:9887-9892. http ://dx .doi .org/10 .1073/pnas .1402468111
18. Lambrecht, B.N., and H. Hammad. 2015. The immunology of asthma. Nat. Immunol. 16:45-56. http ://dx .doi .org/10 .1038/ni .3049
19. Lefrançais, E., A. Duval, E. Mirey, S. Roga, E. Espinosa, C. Cayrol, and J.P. Girard. 2014. Central domain of IL-33 is cleaved by mast cell proteases for potent activation of group-2 innate lymphoid cells. Proc. Natl. Acad. Sci. USA. 111:15502-15507. http ://dx .doi .org/10 .1073/pnas .1410700111
20. Lélu, K., S. Laffont, L. Delpy, P.E. Paulet, T. Périnat, S.A. Tschanz, L. Pelletier, B. Engelhardt, and J.C. Guéry. 2011. Estrogen receptor α signaling in T lymphocytes is required for estradiol-mediated inhibition of Th1 and Th17 cell differentiation and protection against experimental autoimmune encephalomyelitis. J. Immunol. 187:2386-2393. http ://dx .doi .org/10 .4049/jimmunol .1101578
21. Liao, Y., G.K. Smyth, and W. Shi. 2013. The Subread aligner: Fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 41:e108. http ://dx .doi .org/10 .1093/nar/gkt214
22. Liao, Y., G.K. Smyth, and W. Shi. 2014. featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 30:923-930. http ://dx .doi .org/10 .1093/bioinformatics/btt656
23. Liou, C.J., and W.C. Huang. 2011. Dehydroepiandrosterone suppresses eosinophil infiltration and airway hyperresponsiveness via modulation of chemokines and Th2 cytokines in ovalbumin-sensitized mice. J. Clin. Immunol. 31:656-665. http ://dx .doi .org/10 .1007/s10875-011-9529-3
24. Markle, J.G., and E.N. Fish. 2014. SeXX matters in immunity. Trends Immunol. 35:97-104. http ://dx .doi .org/10 .1016/j .it .2013 .10 .006
25. Melgert, B.N., D.S. Postma, I. Kuipers, M. Geerlings, M.A. Luinge, B.W. van der Strate, H.A. Kerstjens, W. Timens, and M.N. Hylkema. 2005. Female mice are more susceptible to the development of allergic airway inflammation than male mice. Clin. Exp. Allergy. 35:1496-1503. http ://dx .doi .org/10 .1111/j .1365-2222 .2005 .02362 .x
26. Molofsky, A.B., J.C. Nussbaum, H.-E. Liang, S.J. Van Dyken, L.E. Cheng, A. Mohapatra, A. Chawla, and R.M. Locksley. 2013. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 210:535-549. http ://dx .doi .org/10 .1084/jem .20121964
27. Moro, K., T. Yamada, M. Tanabe, T. Takeuchi, T. Ikawa, H. Kawamoto, J. Furusawa, M. Ohtani, H. Fujii, and S. Koyasu. 2010. Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells. Nature. 463:540-544. http ://dx .doi .org/10 .1038/nature08636
28. Mulligan, T., M.F. Frick, Q.C. Zuraw, A. Stemhagen, and C. McWhirter. 2006. Prevalence of hypogonadism in males aged at least 45 years: The HIM study. Int. J. Clin. Pract. 60:762-769. http ://dx .doi .org/10 .1111/j .1742-1241 .2006 .00992 .x
29. Neill, D.R., S.H. Wong, A. Bellosi, R.J. Flynn, M. Daly, T.K.A. Langford, C. Bucks, C.M. Kane, P.G. Fallon, R. Pannell, et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 464:1367-1370. http ://dx .doi .org/10 .1038/nature08900
30. Robinette, M.L., A. Fuchs, V.S. Cortez, J.S. Lee, Y. Wang, S.K. Durum, S. Gilfillan, M. Colonna, and C. Immunological Genome. Immunological Genome Consortium. 2015. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16:306-317. http ://dx .doi .org/10 .1038/ni .3094
31. Salimi, M., J.L. Barlow, S.P. Saunders, L. Xue, D. Gutowska-Owsiak, X. Wang, L.C. Huang, D. Johnson, S.T. Scanlon, A.N.J. McKenzie, et al. 2013. A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J. Exp. Med. 210:2939-2950. http ://dx .doi .org/10 .1084/jem .20130351
32. Sato, T., T. Matsumoto, H. Kawano, T. Watanabe, Y. Uematsu, K. Sekine, T. Fukuda, K. Aihara, A. Krust, T. Yamada, et al. 2004. Brain masculinization requires androgen receptor function. Proc. Natl. Acad. Sci. USA. 101:1673-1678. http ://dx .doi .org/10 .1073/pnas .0305303101
33. Schmitz, J., A. Owyang, E. Oldham, Y. Song, E. Murphy, T.K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, et al. 2005. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity. 23:479-490. http ://dx .doi .org/10 .1016/j .immuni .2005 .09 .015
34. Shah, S. 2004. European Respiratory Society-14th Annual Congress. Drug highlights. 4-8 September 2004, Glasgow, UK. IDrugs. 7:914-916
35. Tait Wojno, E.D., and D. Artis. 2016. Emerging concepts and future challenges in innate lymphoid cell biology. J. Exp. Med. 213:2229-2248. http ://dx .doi .org/10 .1084/jem .20160525
36. Tait Wojno, E.D., L.A. Monticelli, S.V. Tran, T. Alenghat, L.C. Osborne, J.J. Thome, C. Willis, A. Budelsky, D.L. Farber, and D. Artis. 2015. The prostaglandin D2 receptor CRTH2 regulates accumulation of group 2 innate lymphoid cells in the inflamed lung. Mucosal Immunol. 8:1313-1323. http ://dx .doi .org/10 .1038/mi .2015 .21
37. Townsend, E.A., V.M. Miller, and Y.S. Prakash. 2012. Sex differences and sex steroids in lung health and disease. Endocr. Rev. 33:1-47. http ://dx .doi .org/10 .1210/er .2010-0031
38. Vivier, E., S.A. van de Pavert, M.D. Cooper, and G.T. Belz. 2016. The evolution of innate lymphoid cells. Nat. Immunol. 17:790-794. http ://dx .doi .org/10 .1038/ni .3459
39. Wenzel, S.E., C.B. Robinson, J.M. Leonard, and R.A. Panettieri Jr. 2010. Nebulized dehydroepiandrosterone-3-sulfate improves asthma control in the moderate-to-severe asthma results of a 6-week, randomized, double-blind, placebo-controlled study. Allergy Asthma Proc. 31:461-471. http ://dx .doi .org/10 .2500/aap .2010 .31 .3384