Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells

Journal of Experimental Medicine

Volumn 205, Issue 7, 2008, Pages 1543-1550

  De Beaucoudtey, Ludovic ^a,b   Puel, Anne ^a,b   Filipe Santos, Orchidée ^a,b   Cobat, Aurélie ^a,b   Ghandil, Pegah ^a,b   Chrabieh, Maya ^a,b   Felnberg, Jacqueline ^a,b   Von Bernuth, Horst ^a,b   Samarina, Arina ^a,b   Jannière, Lucile ^a,b   Fieschi, Claire ^c   Stéphan, Jean Louis ^d   Boileau, Catherine ^e   Lyonnet, Stanislas ^b,f   Jondeau, Guillaume ^b,j   Cormier Daire, Valérie ^b,f   Le Merrer, Martine ^b,f   Hoarau, Cyrille ^k   Lebranchu, Yvon ^k   Lortholary, Olivier ^g   Chandesris, Marie Olivia ^g   Tron, François ^f,l   Gambineri, Eleonora ^m   Bianchi, Lucia ^m   Rodriguez Gallego, Carlos ⁿ   Zitnik, Simona E ^o   Vasconcelos, Julia ^p   Guedes, Margarida ^q   Vitor, Artur Bonito ^r   Marodi, Laszlo ^s   Chapel, Helen ^t   Reid, Brenda ^u   Roifman, Chaim ^u   Nadal, David ^v   Reichenbach, Janine ^v   Caragol, Isabel ^w   Garty, Ben Zion ^x   Dogu, Figen ^y   Camcioglu, Yildiz ^z   Gülle, Sanyie ^aa   Sanal, Ozden ^ab   Fischer, Alain ^b,f,h   Abel, Laurent ^a,b   Stockinger, Birgitta ^ac   Picard, Capucine ^a,b,i   Casanova, Jean Laurent ^a,b,h   more..

^a IMAGINE INSTITUTE   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c SAINT LOUIS HOSPITAL   (France)

^d UNIVERSITÉ JEAN MONNET   (France)

^e LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^f INSERM   (France)

^g Necker Pasteur Infectiology Center   (France)

^h Pediatric Hematology Immunology Unit   (France)

ⁱ HÔPITAL NECKER ENFANTS MALADES   (France)

^j BICHAT HOSPITAL   (France)

^k UNIVERSITÉ DE TOURS   (France)

^l ROUEN UNIVERSITY HOSPITAL   (France)

^m UNIVERSITY OF FLORENCE   (Italy)

ⁿ HOSPITAL UNIVERSITARIO DE GRAN CANARIA DR NEGRÍN   (Spain)

^o UNIVERSITY CHILDREN S HOSPITAL   (Slovenia)

^p University Children's Hospital ^*  (Portugal)

^q HOSPITAL DE SANTO ANTÓNIO   (Portugal)

^r HOSPITAL DE SÃO JOÃO   (Portugal)

^s UNIVERSITY OF DEBRECEN   (Hungary)

^t UNIVERSITY OF OXFORD   (United Kingdom)

^u HOSPITAL FOR SICK CHILDREN   (Canada)

^v UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^w Vail d'Hebron University Hospital   (Spain)

^x SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^y ANKARA UNIVERSITY   (Turkey)

^z ISTANBUL UNIVERSITY   (Turkey)

^aa Dr Behcet Uz Childrens Public Hospital   (Turkey)

^ab HACETTEPE UNIVERSITY   (Turkey)

^ac NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2;

ARTICLE; BLAST CELL; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EX VIVO STUDY; GENE MUTATION; GENETIC TRAIT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; T LYMPHOCYTE;

CELL DIFFERENTIATION; CYTOKINES; FEMALE; GENETIC DISEASES, INBORN; HUMANS; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-17; MALE; MUTATION; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN-SERINE-THREONINE KINASES; QUANTITATIVE TRAIT LOCI; RECEPTORS, INTERLEUKIN-12; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 46949086109     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20080321     Document Type: Article

References (40)

1. Dong, C. 2008. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8:337-348.
2. Acosta-Rodriguez, E.V., L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, and G. Napolitani. 2007. Surface phenotype and antigenic specif city of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8:639-646.
3. Sato, W., T. Aranami, and T. Yamamura. 2007. Cutting edge: Human Th17 cells are identif ed as bearing CCR2+CCR5- phenotype. J. Immunol. 178:7525-7529.
4. Annunziato, F., L. Cosmi, V. Santarlasci, L. Maggi, F. Liotta, B. Mazzinghi, E. Parente, L. Fili, S. Ferri, F. Frosali, et al. 2007. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204:1849-1861.
5. Acosta-Rodriguez, E.V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8:942-949.
6. Wilson, N.J., K. Boniface, J.R. Chan, B.S. McKenzie, W.M. Blumenschein, J.D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, et al. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8:950-957.
7. Chen, Z., C.M. Tato, L. Muul, A. Laurence, and J.J. O ' Shea. 2007. Distinct regulation of interleukin-17 in human T helper lymphocytes. Arthritis Rheum. 56:2936-2946.
8. Evans, H.G., T. Suddason, I. Jackson, L.S. Taams, and G.M. Lord. 2007. Optimal induction of T helper 17 cells in humans requires T cell receptor ligation in the context of Toll-like receptor-activated monocytes. Proc. Natl. Acad. Sci. USA. 104:17034-17039.
9. Lim, H.W., J. Lee, P. Hillsamer, and C.H. Kim. 2008. Human Th17 cells share major traf cking receptors with both polarized effector T cells and FOXP3+ regulatory T cells. J. Immunol. 180:122-129.
10. Singh, S.P., H.H. Zhang, J.F. Foley, M.N. Hedrick, and J.M. Farber. 2008. Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J. Immunol. 180:214-221.
11. Manel, N., D. Unutmaz, and D.R. Littman. 2008. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat. Immunol. 9:641-649.
12. Volpe, E., N. Servant, R. Zollinger, S.I. Bogiatzi, P. Hupe, E. Barillot, and V. Soumelis. 2008. A critical function for transforming growth factor-beta, interleukin 23 and proinf ammatory cytokines in driving and modulating human T(H)-17 responses. Nat. Immunol. 9:650-657.
13. Yang, L., D.E. Anderson, C. Baecher-Allan, W.D. Hastings, E. Bettelli, M. Oukka, V.K. Kuchroo, and D.A. Hafler. 2008. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature. DOI:10.1038/nature07021.
14. Janssens, K., F. Vanhoenacker, M. Bonduelle, L. Verbruggen, L. Van Maldergem, S. Ralston, N. Guanabens, N. Migone, S. Wientroub, M.T. Divizia, et al. 2006. Camurati-Engelmann disease: review of the clinical, radiological, and molecular data of 24 families and implications for diagnosis and treatment. J. Med. Genet. 43:1-11.
15. Ramirez, F., and H.C. Dietz. 2007. Marfan syndrome: from molecular pathogenesis to clinical treatment. Curr. Opin. Genet. Dev. 17:252-258.
16. Ku, C.L., H. von Bernuth, C. Picard, S.Y. Zhang, H.H. Chang, K. Yang, M. Chrabieh, A.C. Issekutz, C.K. Cunningham, J. Gallin, et al. 2007. Selective predisposition to bacterial infections in IRAK-4-deficient children: IRAK-4-dependent TLRs are otherwise redundant in protective immunity. J. Exp. Med. 204:2407-2422.
17. Minegishi, Y., M. Saito, S. Tsuchiya, I. Tsuge, H. Takada, T. Hara, N. Kawamura, T. Ariga, S. Pasic, O. Stojkovic, et al. 2007. Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyperIgE syndrome. Nature. 448:1058-1062.
18. 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.
19. Filipe-Santos, O., J. Bustamante, A. Chapgier, G. Vogt, L. de Beaucoudrey, J. Feinberg, E. Jouanguy, S. Boisson-Dupuis, C. Fieschi, C. Picard, and J.L. Casanova. 2006. Inborn errors of IL-12/23- and IFN-gamma-mediated immunity: molecular, cellular, and clinical features. Semin. Immunol. 18:347-361.
20. Buckley, R.H. 2004. Molecular defects in human severe combined immunodeficiency and approaches to immune reconstitution. Annu. Rev. Immunol. 22:625-655.
21. Harris, T.J., J.F. Grosso, H.R. Yen, H. Xin, M. Kortylewski, E. Albesiano, E.L. Hipkiss, D. Getnet, M.V. Goldberg, C.H. Maris, et al. 2007. Cutting edge: An in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J. Immunol. 179:4313-4317.
22. Wei, L., A. Laurence, K.M. Elias, and J.J. O ' Shea. 2007. IL-21 is produced by Th17 cells and drives IL-17 production in a STAT3-dependent manner. J. Biol. Chem. 282:34605-34610.
23. 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 inf ammatory helper T cells. J. Biol. Chem. 282:9358-9363.
24. Mathur, A.N., H.C. Chang, D.G. Zisoulis, G.L. Stritesky, Q. Yu, J.T. O ' Malley, R. Kapur, D.E. Levy, G.S. Kansas, and M.H. Kaplan. 2007. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J. Immunol. 178:4901-4907.
25. Milner, J.D., J.M. Brenchley, A. Laurence, A.F. Freeman, B.J. Hill, K.M. Elias, Y. Kanno, C. Spalding, H.Z. Elloumi, M.L. Paulson, et al. 2008. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature. 452:773-776.
26. Kimura, A., T. Naka, and T. Kishimoto. 2007. IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc. Natl. Acad. Sci. USA. 104:12099-12104.
27. Chen, X., O.M. Howard, and J.J. Oppenheim. 2007. Pertussis toxin by inducing IL-6 promotes the generation of IL-17-producing CD4 cells. J. Immunol. 178:6123-6129.
28. Langrish, C.L., Y. Chen, W.M. Blumenschein, J. Mattson, B. Basham, J.D. Sedgwick, T. McClanahan, R.A. Kastelein, and D.J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inf ammation. J. Exp. Med. 201:233-240.
29. Thakker, P., M.W. Leach, W. Kuang, S.E. Benoit, J.P. Leonard, and S. Marusic. 2007. IL-23 is critical in the induction but not in the ef ector phase of experimental autoimmune encephalomyelitis. J. Immunol. 178:2589-2598.
30. Matsuzaki, G., and M. Umemura. 2007. Interleukin-17 as an effector molecule of innate and acquired immunity against infections. Microbiol. Immunol. 51:1139-1147.
31. Happel, K.I., P.J. Dubin, M. Zheng, N. Ghilardi, C. Lockhart, L.J. Quinton, A.R. Odden, J.E. Shellito, G.J. Bagby, S. Nelson, and J.K. Kolls. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202:761-769.
32. Ye, P., F.H. Rodriguez, S. Kanaly, K.L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194:519-527.
33. Huang, W., L. Na, P.L. Fidel, and P. Schwarzenberger. 2004. Requirement of interleukin-17A for systemic anti- Candida albicans host defense in mice. J. Infect. Dis. 190:624-631.
34. LeibundGut-Landmann, S., O. Gross, M.J. Robinson, F. Osorio, E.C. Slack, S.V. Tsoni, E. Schweighoffer, V. Tybulewicz, G.D. Brown, J. Ruland, and C. Reis e Sousa. 2007. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8:630-638.
35. Ouyang, W., J.K. Kolls, and Y. Zheng. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity. 28:454-467.
36. Umemura, M., A. Yahagi, S. Hamada, M.D. Begum, H. Watanabe, K. Kawakami, T. Suda, K. Sudo, S. Nakae, Y. Iwakura, and G. Matsuzaki. 2007. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178:3786-3796.
37. Khader, S.A., G.K. Bell, J.E. Pearl, J.J. Fountain, J. Rangel-Moreno, G.E. Cilley, F. Shen, S.M. Eaton, S.L. Gaffen, S.L. Swain, et al. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8:369-377.
38. Schwarzenberger, P., and J.K. Kolls. 2002. Interleukin 17: an example for gene therapy as a tool to study cytokine mediated regulation of hematopoiesis. J. Cell. Biochem. Suppl. 38:88-95.
39. Casanova, J.L., and L. Abel. 2007. Primary immunodef ciencies: a field in its infancy. Science. 317:617-619.
40. Quintana-Murci, L., A. Alcais, L. Abel, and J.L. Casanova. 2007. Immunology in natura: clinical, epidemiological and evolutionary genetics of infectious diseases. Nat. Immunol. 8:1165-1171.