IL-12 drives functional plasticity of human group 2 innate lymphoid cells

Journal of Experimental Medicine

Volumn 213, Issue 4, 2016, Pages 569-583

  Lim, Ai Ing ^a,b   Menegatti, Silvia ^a   Bustamante, Jacinta ^c,d,e,f   Le Bourhis, Lionel ^g   Allez, Matthieu ^g,h   Rogge, Lars ^a   Casanova, Jean Laurent ^c,d,e,f   Yssel, Hans ⁱ   Di Santo, James P ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c IMAGINE INSTITUTE   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f ROCKEFELLER UNIVERSITY   (United States)

^g UNIVERSITÉ PARIS DIDEROT   (France)

^h SAINT LOUIS HOSPITAL   (France)

ⁱ Assistance publique Hôpitaux de Paris   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 13; TRANSCRIPTION FACTOR T BET; IFNG PROTEIN, HUMAN; IL5 PROTEIN, HUMAN; INTERLEUKIN 5; INTERLEUKIN-13, HUMAN;

ARTICLE; CELL PLASTICITY; CLONE; CONTROLLED STUDY; CROHN DISEASE; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; LYMPHOID CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CELL CULTURE; FEMALE; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE; LYMPHOCYTE; MALE; MOUSE; PATHOLOGY;

ANIMALS; CELLS, CULTURED; CROHN DISEASE; FEMALE; HUMANS; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-12; INTERLEUKIN-13; INTERLEUKIN-5; INTESTINES; LYMPHOCYTES; MALE; MICE;

EID: 84994879643     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20151750     Document Type: Article

References (41)

1. Altare, F., A. Durandy, D. Lammas, J.F. Emile, S. Lamhamedi, F. Le Deist, P. Drysdale, E. Jouanguy, R. Döffinger, F. Bernaudin, et al. 1998. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science. 280:1432-1435. http://dx.doi.org/10.1126/science.280.5368.1432
2. Artis, D., and H. Spits. 2015. The biology of innate lymphoid cells. Nature. 517:293-301. http://dx.doi.org/10.1038/nature14189
3. Ashkar, A.A., J.P. Di Santo, and B.A. Croy. 2000. Interferon γ contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J. Exp. Med. 192:259-270. http://dx.doi.org/10.1084/jem.192.2.259
4. Barlow, J.L., and A.N. McKenzie. 2014. Type-2 innate lymphoid cells in human allergic disease. Curr. Opin. Allergy Clin. Immunol. 14:397-403. http://dx.doi.org/10.1097/ACI.0000000000000090
5. Barnig, C., M. Cernadas, S. Dutile, X. Liu, M.A. Perrella, S. Kazani, M.E. Wechsler, E. Israel, and B.D. Levy. 2013. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci. Transl. Med. 5:174ra26. http://dx.doi.org/10.1126/scitranslmed.3004812
6. Bartemes, K.R., G.M. Kephart, S.J. Fox, and H. Kita. 2014. Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J. Allergy Clin. Immunol. 134:671-678. http://dx.doi.org/10.1016/j.jaci.2014.06.024
7. Bernink, J.H., C.P. Peters, M. Munneke, A.A. te Velde, S.L. Meijer, K. Weijer, H.S. Hreggvidsdottir, S.E. Heinsbroek, N. Legrand, C.J. Buskens, et al. 2013. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 14:221-229. http://dx.doi.org/10.1038/ni.2534
8. + group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity. 43:146-160. http://dx.doi.org/10.1016/j.immuni.2015.06.019
9. Brestoff, J.R., B.S. Kim, S.A. Saenz, R.R. Stine, L.A. Monticelli, G.F. Sonnenberg, J.J. Thome, D.L. Farber, K. Lutfy, P. Seale, and D. Artis. 2015. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature. 519:242-246. http://dx.doi.org/10.1038/nature14115
10. Bustamante, J., S. Boisson-Dupuis, L. Abel, and J.L. Casanova. 2014. Mendelian susceptibility to mycobacterial disease: genetic, immunological, and clinical features of inborn errors of IFN-γ immunity. Semin. Immunol. 26:454-470. http://dx.doi.org/10.1016/j.smim.2014.09.008
11. de Beaucoudrey, L., A. Puel, O. Filipe-Santos, A. Cobat, P. Ghandil, M. Chrabieh, J. Feinberg, H. von Bernuth, A. Samarina, L. Jannière, et al. 2008. Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J. Exp. Med. 205:1543-1550. http://dx.doi.org/10.1084/jem.20080321
12. de Beaucoudrey, L., A. Samarina, J. Bustamante, A. Cobat, S. Boisson-Dupuis, J. Feinberg, S. Al-Muhsen, L. Jannière, Y. Rose, M. de Suremain, et al. 2010. Revisiting human IL-12Rβ1 deficiency: a survey of 141 patients from 30 countries. Medicine. 89:381-402. http://dx.doi.org/10.1097/MD.0b013e3181fdd832
13. 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
14. Fuchs, A., W. Vermi, J.S. Lee, S. Lonardi, S. Gilfillan, R.D. Newberry, M. Cella, and M. Colonna. 2013. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12-and IL-15-responsive IFN-γ-producing cells. Immunity. 38:769-781. http://dx.doi.org/10.1016/j.immuni.2013.02.010
15. Geremia, A., C.V. Arancibia-Cárcamo, M.P. Fleming, N. Rust, B. Singh, N.J. Mortensen, S.P. Travis, and F. Powrie. 2011. IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J. Exp. Med. 208:1127-1133. http://dx.doi.org/10.1084/jem.20101712
16. + T cells in vivo. Blood. 111:5008-5016. http://dx.doi.org/10.1182/blood-2007-11-122259
17. Guillot-Delost, M., S. Le Gouvello, M. Mesel-Lemoine, M. Cheraï, C. Baillou, A. Simon, Y. Levy, L. Weiss, S. Louafi, N. Chaput, et al. 2012. Human CD90 identifies Th17/Tc17 T cell subsets that are depleted in HIV-infected patients. J. Immunol. 188:981-991. http://dx.doi.org/10.4049/jimmunol.1101592
18. Hazenberg, M.D., and H. Spits. 2014. Human innate lymphoid cells. Blood. 124:700-709. http://dx.doi.org/10.1182/blood-2013-11-427781
19. Huang, Y., L. Guo, J. Qiu, X. Chen, J. Hu-Li, U. Siebenlist, P.R. Williamson, J.F. Urban Jr., and W.E. Paul. 2015. IL-25-responsive, lineage-negative KLRG1(hi) cells are multipotential 'inflammatory' type 2 innate lymphoid cells. Nat. Immunol. 16:161-169. http://dx.doi.org/10.1038./ni.3078
20. Kim, B.S., and D. Artis. 2015. Group 2 innate lymphoid cells in health and disease. Cold Spring Harb. Perspect. Biol. 7:11-20. http://dx.doi.org/10.1101/cshperspect.a016337
21. 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
22. Mjösberg, J.M., S. Trifari, N.K. Crellin, C.P. Peters, C.M. van Drunen, B. Piet, W.J. Fokkens, T. Cupedo, and H. Spits. 2011. Human IL-25-and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat. Immunol. 12:1055-1062. http://dx.doi.org/10.1038/ni.2104
23. Monticelli, L.A., G.F. Sonnenberg, M.C. Abt, T. Alenghat, C.G. Ziegler, T.A. Doering, J.M. Angelosanto, B.J. Laidlaw, C.Y. Yang, T. Sathaliyawala, et al. 2011. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12:1045-1054. http://dx.doi.org/10.1038/ni.2131
24. 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 T(H)2 cytokines by adipose tissue-associated c-Kit+Scα-1+ lymphoid cells. Nature. 463:540-544. http://dx.doi.org/10.1038/nature08636
25. Munneke, J.M., A.T. Björklund, J.M. Mjösberg, K. Garming-Legert, J.H. Bernink, B. Blom, C. Huisman, M.H. van Oers, H. Spits, K.J. Malmberg, and M.D. Hazenberg. 2014. Activated innate lymphoid cells are associated with a reduced susceptibility to graft-versus-host disease. Blood. 124:812-821. http://dx.doi.org/10.1182/blood-2013-11-536888
26. Neill, D.R., S.H. Wong, A. Bellosi, R.J. Flynn, M. Daly, T.K. 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
27. Okada, S., J.G. Markle, E.K. Deenick, F. Mele, D. Averbuch, M. Lagos, M. Alzahrani, S. Al-Muhsen, R. Halwani, C.S. Ma, et al. 2015. Impairment of immunity to Candida and Mycobacterium in humans with bi-allelic RORC mutations. Science. 349:606-613. http://dx.doi.org/10.1126/science.aaa4282
28. Ouederni, M., O. Sanal, A. Ikinciogullari, I. Tezcan, F. Dogu, I. Sologuren, S. Pedraza-Sánchez, 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
29. Price, A.E., H.E. Liang, B.M. Sullivan, R.L. Reinhardt, C.J. Eisley, D.J. Erle, and R.M. Locksley. 2010. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. USA. 107:11489-11494. http://dx.doi.org/10.1073/pnas.1003988107
30. Roediger, B., and W. Weninger. 2015. Group 2 innate lymphoid cells in the regulation of immune responses. Adv. Immunol. 125:111-154. http://dx.doi.org/10.1016/bs.ai.2014.09.004
31. Rutz, S., X. Wang, and W. Ouyang. 2014. The IL-20 subfamily of cytokines-from host defence to tissue homeostasis. Nat. Rev. Immunol. 14:783-795. http://dx.doi.org/10.1038/nri3766
32. 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. 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
33. Schroder, K., P.J. Hertzog, T. Ravasi, and D.A. Hume. 2004. Interferon-γ: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75:163-189. http://dx.doi.org/10.1189/jlb.0603252
34. + group 3 innate lymphoid cells. J. Exp. Med. 211:199-208. http://dx.doi.org/10.1084/jem.20131038
35. Serafini, N., C.A. Vosshenrich, and J.P. Di Santo. 2015. Transcriptional regulation of innate lymphoid cell fate. Nat. Rev. Immunol. 15:415-428. http://dx.doi.org/10.1038/nri3855
36. 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
37. Teng, M.W., E.P. Bowman, J.J. McElwee, M.J. Smyth, J.L. Casanova, A.M. Cooper, and D.J. Cua. 2015. IL-12 and IL-23 cytokines: from discovery to targeted therapies for immune-mediated inflammatory diseases. Nat. Med. 21:719-729. http://dx.doi.org/10.1038/nm.3895
38. + innate lymphocytes. Immunity. 33:736-751. http://dx.doi.org/10.1016/j.immuni.2010.10.017
39. Xue, L., M. Salimi, I. Panse, J.M. Mjösberg, A.N. McKenzie, H. Spits, P. Klenerman, and G. Ogg. 2014. Prostaglandin D2 activates group 2 innate lymphoid cells through chemoattractant receptor-homologous molecule expressed on TH2 cells. J. Allergy Clin. Immunol. 133:1184-1194. http://dx.doi.org/10.1016/j.jaci.2013.10.056
40. Yssel, H., and H. Spits. 2002. Generation and maintenance of cloned human T cell lines. Current Protocols in Immunology. Chapter 7:Unit 7.19
41. Yu, X., R. Pappu, V. Ramirez-Carrozzi, N. Ota, P. Caplazi, J. Zhang, D. Yan, M. Xu, W.P. Lee, and J.L. Grogan. 2014. TNF superfamily member TL1A elicits type 2 innate lymphoid cells at mucosal barriers. Mucosal Immunol. 7:730-740. http://dx.doi.org/10.1038/mi.2013.92