Insights into the role of STAT3 in human lymphocyte differentiation as revealed by the hyper-IgE syndrome

Journal of Immunology

Volumn 182, Issue 1, 2009, Pages 21-28

  Tangye, Stuart G ^a   Cook, Matthew C ^b,c   Fulcher, David A ^d  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b Biology and Environment   (Australia)

^c CANBERRA HOSPITAL   (Australia)

^d WESTMEAD HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 9; JANUS KINASE 3; PROTEIN KINASE TYK2; STAT1 PROTEIN; STAT3 PROTEIN; STAT5B PROTEIN; CYTOKINE; STAT3 PROTEIN, HUMAN; UNCLASSIFIED DRUG;

B LYMPHOCYTE; BONE DEVELOPMENT; CD4+ T LYMPHOCYTE; CLINICAL FEATURE; GENE MUTATION; HUMAN; HYPER IGE SYNDROME; IMMUNE RESPONSE; INFECTION SENSITIVITY; LYMPHOCYTE DIFFERENTIATION; MICROBIAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHORT SURVEY; SIGNAL TRANSDUCTION; ANIMAL; ANTIBODY PRODUCTION; CELL DIFFERENTIATION; CELLULAR IMMUNITY; COMPARATIVE STUDY; DISEASE MODEL; EPITHELIUM CELL; GENETICS; IMMUNOLOGY; LYMPHOCYTE; METABOLISM; MICROBIOLOGY; MOUSE; PATHOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; ANTIBODY FORMATION; CELL DIFFERENTIATION; CYTOKINES; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; HUMANS; IMMUNITY, CELLULAR; JOB'S SYNDROME; LYMPHOCYTES; MICE; STAT3 TRANSCRIPTION FACTOR;

EID: 59849121375     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.1.21     Document Type: Short Survey

References (86)

1. Shuai, K., and B. Liu. 2003. Regulation of JAK-STAT signalling in the immune system. Nat Rev Immunol 3: 900-911.
2. Levy, D. E., and J. E. Darnell, Jr. 2002. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3: 651-662.
3. Murray, P. J. 2007. The JAK-STAT signaling pathway: input and output integration. J. Immunol. 178: 2623-2629.
4. O'Shea, J. J., and P. J. Murray. 2008. Cytokine signaling modules in inflammatory responses. Immunity 28: 477-487.
5. Fischer, A. 2007. Human primary immunodeficiency diseases. Immunity 27: 835-845.
6. Macchi, P., A. Villa, S. Giliani, M. G. Sacco, A. Frattini, F. Porta, A. G. Ugazio, J. A. Johnston, F. Candotti, J. J. O'Shea, et al. 1995. Mutations of Jak-3 gene in patients with autosomal severe combined immune deficiency (SCID). Nature 377: 65-68.
7. Minegishi, Y., M. Saito, T. Morio, K. Watanabe, K. Agematsu, S. Tsuchiya, H. Takada, T. Hara, N. Kawamura, T. Ariga, et al. 2006. Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity 25: 745-755.
8. Bernasconi, A., R. Marino, A. Ribas, J. Rossi, M. Ciaccio, M. Oleastro, A. Ornani, R. Paz, M. A. Rivarola, M. Zelazko, and A. Belgorosky. 2006. Characterization of immunodeficiency in a patient with growth hormone insensitivity secondary to a novel STAT5b gene mutation. Pediatrics 118: e1584-e1592.
9. 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 hyper-IgE syndrome. Nature 448: 1058-1062.
10. 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.
11. Akira, S. 2000. Roles of STAT3 defined by tissue-specific gene targeting. Oncogene 19: 2607-2611.
12. Takeda, K., B. E. Clausen, T. Kaisho, T. Tsujimura, N. Terada, I. Forster, and S. Akira. 1999. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10: 39-49.
13. Laouar, Y., T. Welte, X. Y. Fu, and R. A. Flavell. 2003. STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity 19: 903-912.
14. Renauld, J. C. 2003. Class II cytokine receptors and their ligands: key antiviral and inflammatory modulators. Nat Rev Immunol 3: 667-676.
15. Stumhofer, J. S., J. S. Silver, A. Laurence, P. M. Porrett, T. H. Harris, L. A. Turka, M. Ernst, C. J. Saris, J. J. O'Shea, and C. A. Hunter. 2007. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat Immunol. 8: 1363-1371.
16. Fitzgerald, J. S., T. G. Poehlmann, E. Schleussner, and U. R. Markert. 2008. Trophoblast invasion: the role of intracellular cytokine signalling via signal transducer and activator of transcription 3 (STAT3). Hum Reprod Update 14: 335-344.
17. Takeda, K., K. Noguchi, W. Shi, T. Tanaka, M. Matsumoto, N. Yoshida, T. Kishimoto, and S. Akira. 1997. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. USA 94: 3801-3804.
18. Dong, C. 2008. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8: 337-348.
19. 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.
20. Pene, J., S. Chevalier, L. Preisser, E. Venereau, M. H. Guilleux, S. Ghannam, J. P. Moles, Y. Danger, E. Ravon, S. Lesaux, et al. 2008. Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes. J. Immunol. 180: 7423-7430.
21. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189.
22. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
23. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-β induces development of theTH17 lineage. Nature 441: 231-234.
24. Nurieva, R., X. O. Yang, G. Martinez, Y. Zhang, A. D. Panopoulos, L. Ma, K. Schluns, Q. Tian, S. S. Watowich, A. M. Jetten, and C. Dong. 2007. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448: 480-483.
25. H17 cells. Nature 448: 484-487.
26. Zhou, L., Ivanov, II, R. Spolski, R. Min, K. Shenderov, T. Egawa, D. E. Levy, W. J. Leonard, and D. R. Littman. 2007. IL-6 programs TH-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8: 967-974.
27. 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.
28. Coquet, J. M., S. Chakravarti, M. J. Smyth, and D. I. Godfrey. 2008. Cutting edge: IL-21 is not essential for Th17 differentiation or experimental autoimmune encephalomyelitis. J. Immunol. 180: 7097-7101.
29. 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.
30. 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.
31. Laurence, A., C. M. Tato, T. S. Davidson, Y. Kanno, Z. Chen, Z. Yao, R. B. Blank, F. Meylan, R. Siegel, L. Hennighausen, et al. 2007. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26: 371-381.
32. 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.
33. + T helper cells. Cell 126: 1121-1133.
34. Yang, X. O., B. P. Pappu, R. Nurieva, A. Akimzhanov, H. S. Kang, Y. Chung, L. Ma, B. Shah, A. D. Panopoulos, K. S. Schluns, et al. 2008. T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORα and RORγ. Immunity 28: 29-39.
35. Fornek, J. L., L. T. Tygrett, T. J. Waldschmidt, V. Poli, R. C. Rickert, and G. S. Kansas. 2006. Critical role for Stat3 in T-dependent terminal differentiation of IgG B cells. Blood 107: 1085-1091.
36. Calame, K. L., K. I. Lin, and C. Tunyaplin. 2003. Regulatory mechanisms that determine the development and function of plasma cells. Annu. Rev. Immunol. 21: 205-230.
37. Suematsu, S., T. Matsuda, K. Aozasa, S. Akira, N. Nakano, S. Ohno, J. Miyazaki, K. Yamamura, T. Hirano, and T. Kishimoto. 1989. IgG1 plasmacytosis in interleukin 6 transgenic mice. Proc. Natl. Acad. Sci. USA 86: 7547-7551.
38. Ettinger, R., S. Kuchen, and P. E. Lipsky. 2008. The role of IL-21 in regulating B-cell function in health and disease. Immunol. Rev. 223: 60-86.
39. de Waal Malefyt, R., J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1220.
40. El Kasmi, K. C., J. Holst, M. Coffre, L. Mielke, A. de Pauw, N. Lhocine, A. M. Smith, R. Rutschman, D. Kaushal, Y. Shen, et al. 2006. General nature of the STAT3-activated anti-inflammatory response. J. Immunol. 177: 7880-7888.
41. Matsukawa, A., S. Kudo, T. Maeda, K. Numata, H. Watanabe, K. Takeda, S. Akira, and T. Ito. 2005. Stat3 in resident macrophages as a repressor protein of inflammatory response. J. Immunol. 175: 3354-3359.
42. -/- mice: an overview. J. Leukocyte Biol. 61: 389-396.
43. Wu, L., and Y. J. Liu. 2007. Development of dendritic-cell lineages. Immunity 26: 741-750.
44. Davis, S. D., J. Schaller, and R. J. Wedgwood. 1966. Job's syndrome. Recurrent, "cold", staphylococcal abscesses. Lancet 1: 1013-1015.
45. Buckley, R. H., B. B. Wray, and E. Z. Belmaker. 1972. Extreme hyperimmunoglobulinemia E and undue susceptibility to infection. Pediatrics 49: 59-70.
46. Grimbacher, B., S. M. Holland, J. I. Gallin, F. Greenberg, S. C. Hill, H. L. Malech, J. A. Miller, A. C. O'Connell, and J. M. Puck. 1999. Hyper-IgE syndrome with recurrent infections-an autosomal dominant multisystem disorder. N. Engl. J. Med. 340: 692-702.
47. Buckley, R. H. 2001. The hyper-IgE syndrome. Clin. Rev. Allergy Immunol. 20: 139-154.
48. Freeman, A. F., and S. M. Holland. 2008. The hyper-IgE syndromes. Immunol Allergy Clin. North Am. 28: 277-291, viii.
49. Dreskin, S. C., P. K. Goldsmith, and J. I. Gallin. 1985. Immunoglobulins in the hyperimmunoglobulin E and recurrent infection (Job's) syndrome. Deficiency of anti-Staphylococcus aureus immunoglobulin A. J. Clin. Invest. 75: 26-34.
50. Leung, D. Y., D. M. Ambrosino, R. D. Arbeit, J. L. Newton, and R. S. Geha. 1988. Impaired antibody responses in the hyperimmunoglobulin E syndrome. J. Allergy Clin. Immunol. 81: 1082-1087.
51. Sheerin, K. A., and R. H. Buckley. 1991. Antibody responses to protein, polysaccharide, and phi X174 antigens in the hyperimmunoglobulinemia E (hyper-IgE) syndrome. J. Allergy Clin. Immunol. 87: 803-811.
52. Renner, E. D., J. M. Puck, S. M. Holland, M. Schmitt, M. Weiss, M. Frosch, M. Bergmann, J. Davis, B. H. Belohradsky, and B. Grimbacher. 2004. Autosomal recessive hyperimmunoglobulin E syndrome: a distinct disease entity. J. Pediatr. 144: 93-99.
53. Woellner, C., A. A. Schaffer, J. M. Puck, E. D. Renner, C. Knebel, S. M. Holland, A. Plebani, and B. Grimbacher. 2007. The hyper IgE syndrome and mutations in TYK2. Immunity 26: 535; author reply: 536.
54. Milner, J. D., J. M. Brenchley, A. Laurence, A. F. Freeman, B. J. Hill, K. M. Elias, Y. Kanno, C. Spalding, H. Z. Elloumi, and M. L. Paulson. 2008. Impaired TH17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452: 773-776.
55. Ma, C. S., G. Y. Chew, N. Simpson, A. Priyadarshi, M. Wong, B. Grimbacher, D. A. Fulcher, S. G. Tangye, and M. C. Cook. 2008. Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 205: 1551-1557.
56. de Beaucoudrey, L., A. Puel, O. Filipe-Santos, A. Cobat, P. Ghandil, M. Chrabieh, J. Feinberg, H. von Bernuth, A. Samarina, L. Janniere, et al. 2008. Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J. Exp. Med. 205: 1543-1550.
57. H17 cell numbers, and variably defective STAT3 phosphorylation in hyper-IgE syndrome. J. Allergy Clin. Immunol. 122: 181-187.
58. 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.
59. 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.
60. 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.
61. Boniface, K., C. Diveu, F. Morel, N. Pedretti, J. Froger, E. Ravon, M. Garcia, E. Venereau, L. Preisser, E. Guignouard, et al. 2007. Oncostatin M secreted by skin infiltrating T lymphocytes is a potent keratinocyte activator involved in skin inflammation. J. Immunol. 178: 4615-4622.
62. Sano, S., S. Itami, K. Takeda, M. Tarutani, Y. Yamaguchi, H. Miura, K. Yoshikawa, S. Akira, and J. Takeda. 1999. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J. 18: 4657-4668.
63. Boniface, K., F. X. Bernard, M. Garcia, A. L. Gurney, J. C. Lecron, and F. Morel. 2005. IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J. Immunol. 174: 3695-3702.
64. 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.
65. 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.
66. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol 98: 942-949.
67. H-17 cells requires transforming growth factor-β and induction of the nuclear receptor RORγt. Nat. Immunol. 9: 641-649.
68. H-17 responses. Nat. Immunol. 9: 650-657.
69. Schnyder-Candrian, S., D. Togbe, I. Couillin, I. Mercier, F. Brombacher, V. Quesniaux, F. Fossiez, B. Ryffel, and B. Schnyder. 2006. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203: 2715-2725.
70. Avery, D. T., V. L. Bryant, C. S. Ma, R. de Waal Malefyt, and S. G. Tangye. 2008. IL-21-induced isotype switching to IgG and IgA by human naive B cells is differentially regulated by IL-4. J. Immunol. 181: 1767-1779.
71. + T follicular helper cells. J. Immunol. 179: 8180-8190.
72. Rousset, F., E. Garcia, T. Defrance, C. Peronne, N. Vezzio, D. H. Hsu, R. Kastelein, K. W. Moore, and J. Banchereau. 1992. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl. Acad. Sci. USA 89: 1890-1893.
73. Klein, B., K. Tarte, M. Jourdan, K. Mathouk, J. Moreaux, E. Jourdan, E. Legouffe, J. De Vos, and J. F. Rossi. 2003. Survival and proliferation factors of normal and malignant plasma cells. Int. J. Hematol. 78: 106-113.
74. Ramsay, A. J., A. J. Husband, I. A. Ramshaw, S. Bao, K. I. Matthaei, G. Koehler, and M. Kopf. 1994. The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science 264: 561-563.
75. Leung, D. Y., L. Key, J. J. Steinberg, M. C. Young, M. Von Deck, R. Wilkinson, and R. S. Geha. 1988. Increased in vitro bone resorption by monocytes in the hyper-immunoglobulin E syndrome. J. Immunol. 140: 84-88.
76. Tanaka, S., K. Nakamura, N. Takahasi, and T. Suda. 2005. Role of RANKL in physiological and pathological bone resorption and therapeutics targeting the RANKL-RANK signaling system. Immunol. Rev. 208: 30-49.
77. Zhang, Z., T. Welte, N. Troiano, S. E. Maher, X. Y. Fu, and A. L. Bothwell. 2005. Osteoporosis with increased osteoclastogenesis in hematopoietic cell-specific STAT3-deficient mice. Biochem. Biophys. Res. Commun. 328: 800-807.
78. Itoh, S., N. Udagawa, N. Takahashi, F. Yoshitake, H. Narita, S. Ebisu, and K. Ishihara. 2006. A critical role for interleukin-6 family-mediated Stat3 activation in osteoblast differentiation and bone formation. Bone 39: 505-512.
79. Kawasaki, K., Y. H. Gao, S. Yokose, Y. Kaji, T. Nakamura, T. Suda, K. Yoshida, T. Taga, T. Kishimoto, H. Kataoka, et al. 1997. Osteoclasts are present in gp130-deficient mice. Endocrinology 138: 4959-4965.
80. Duplomb, L., M. Baud'huin, C. Charrier, M. Berreur, V. Trichet, F. Blanchard, and D. Heymann. 2008. Interleukin-6 inhibits receptor activator of nuclear factor κB ligand-induced osteoclastogenesis by diverting cells into the macrophage lineage: key role of serine727 phosphorylation of signal transducer and activator of transcription 3. Endocrinology 149: 3688-3697.
81. Lenton, K. A., R. P. Nacamuli, D. C. Wan, J. A. Helms, and M. T. Longaker. 2005. Cranial suture biology. Curr. Top. Dev. Biol. 66: 287-328.
82. Cheng, G. Z., W. Z. Zhang, M. Sun, Q. Wang, D. Coppola, M. Mansour, L. M. Xu, C. Costanzo, J. Q. Cheng, and L. H. Wang. 2008. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J. Biol. Chem. 283: 14665-14673.
83. Avery, D. T., C. S. Ma, V. L. Bryant, B. Santner-Nanan, R. Nanan, M. Wong, D. A. Fulcher, M. C. Cook, and S. G. Tangye. 2008. STAT3 is required for IL-21-induced secretion of IgE from human naive B cells. Blood 112: 1784-1793.
84. Geha, R. S., H. H. Jabara, and S. R. Brodeur. 2003. The regulation of immunoglobulin E class-switch recombination. Nat. Rev. Immunol. 3: 721-732.
85. Wood, P. M., C. Fieschi, C. Picard, T. H. Ottenhoff, J. L. Casanova, and D. S. Kumararatne. 2005. Inherited defects in the interferon-γ receptor or interleukin-12 signalling pathways are not sufficient to cause allergic disease in children. Eur. J. Pediatr. 164: 741-747.
86. Gennery, A. R., T. J. Flood, M. Abinun, and A. J. Cant. 2000. Bone marrow transplantation does not correct the hyper IgE syndrome. Bone Marrow Transplant. 25: 1303-1305.