The differential expression of IL-4 and IL-13 and its impact on type-2 immunity

Cytokine

Volumn 75, Issue 1, 2015, Pages 25-37

  Bao, Katherine ^a   Reinhardt, R Lee ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Follicular T helper cell; Interleukin 13; Interleukin 4; Th2 cell; Type 2 immunity

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 4; MAMMALIAN TARGET OF RAPAMYCIN; NOTCH RECEPTOR; TRANSCRIPTION FACTOR C MAF; CYTOKINE; IL4 PROTEIN, HUMAN; INTERLEUKIN-13, HUMAN; STAT3 PROTEIN; STAT6 PROTEIN;

ALLERGIC DISEASE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FATE; CYTOKINE PRODUCTION; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; INTRACELLULAR SIGNALING; NATURAL KILLER T CELL; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; TH2 CELL; TYPE 2 IMMUNITY; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; HYPERSENSITIVITY; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; HYPERSENSITIVITY; IMMUNE SYSTEM; IMMUNITY, INNATE; INFLAMMATION; INTERLEUKIN-13; INTERLEUKIN-4; STAT3 TRANSCRIPTION FACTOR; STAT6 TRANSCRIPTION FACTOR; TH2 CELLS;

EID: 84938750464     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2015.05.008     Document Type: Review

References (230)

1. Pulendran B., Artis D. New paradigms in type 2 immunity. Science 2012, 337:431-435.
2. Masoli M., Fabian D., Holt S., Beasley R. The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 2004, 59:469-478.
3. WHO fact sheet on soil-transmitted helminth infections.
4. Rook G.A. Hygiene hypothesis and autoimmune diseases. Clin Rev Allergy Immunol 2012, 42:5-15.
5. Wills-Karp M., Santeliz J., Karp C.L. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol 2001, 1:69-75.
6. Strachan D.P. Hay fever, hygiene, and household size. BMJ 1989, 299:1259-1260.
7. Catley M.C., Coote J., Bari M., Tomlinson K.L. Monoclonal antibodies for the treatment of asthma. Pharmacol Ther 2011, 132:333-351.
8. Grunig G., Warnock M., Wakil A.E., Venkayya R., Brombacher F., Rennick D.M., et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 1998, 282:2261-2263.
9. Rankin J.A., Picarella D.E., Geba G.P., Temann U.A., Prasad B., DiCosmo B., et al. Phenotypic and physiologic characterization of transgenic mice expressing interleukin 4 in the lung: lymphocytic and eosinophilic inflammation without airway hyperreactivity. Proc Natl Acad Sci USA 1996, 93:7821-7825.
10. Wills-Karp M., Luyimbazi J., Xu X., Schofield B., Neben T.Y., Karp C.L., et al. Interleukin-13: central mediator of allergic asthma. Science 1998, 282:2258-2261.
11. McKenzie A.N., Li X., Largaespada D.A., Sato A., Kaneda A., Zurawski S.M., et al. Structural comparison and chromosomal localization of the human and mouse IL-13 genes. J Immunol 1993, 150:5436-5444.
12. Dolganov G., Bort S., Lovett M., Burr J., Schubert L., Short D., et al. Coexpression of the interleukin-13 and interleukin-4 genes correlates with their physical linkage in the cytokine gene cluster on human chromosome 5q23-31. Blood 1996, 87:3316-3326.
13. Loots G.G., Locksley R.M., Blankespoor C.M., Wang Z.E., Miller W., Rubin E.M., et al. Identification of a coordinate regulator of interleukins 4, 13, and 5 by cross-species sequence comparisons. Science 2000, 288:136-140.
14. Kelly B.L., Locksley R.M. Coordinate regulation of the IL-4, IL-13, and IL-5 cytokine cluster in Th2 clones revealed by allelic expression patterns. J Immunol 2000, 165:2982-2986.
15. Bucy R.P., Karr L., Huang G.Q., Li J., Carter D., Honjo K., et al. Single cell analysis of cytokine gene coexpression during CD4+ T-cell phenotype development. Proc Natl Acad Sci USA 1995, 92:7565-7569.
16. Bucy R.P., Panoskaltsis-Mortari A., Huang G.Q., Li J., Karr L., Ross M., et al. Heterogeneity of single cell cytokine gene expression in clonal T cell populations. J Exp Med 1994, 180:1251-1262.
17. Guo L., Hu-Li J., Paul W.E. Probabilistic regulation in TH2 cells accounts for monoallelic expression of IL-4 and IL-13. Immunity 2005, 23:89-99.
18. Assenmacher M., Schmitz J., Radbruch A. Flow cytometric determination of cytokines in activated murine T helper lymphocytes: expression of interleukin-10 in interferon-gamma and in interleukin-4-expressing cells. Eur J Immunol 1994, 24:1097-1101.
19. Kelso A., Groves P., Ramm L., Doyle A.G. Single-cell analysis by RT-PCR reveals differential expression of multiple type 1 and 2 cytokine genes among cells within polarized CD4+ T cell populations. Int Immunol 1999, 11:617-621.
20. Liang H.E., Reinhardt R.L., Bando J.K., Sullivan B.M., Ho I.C., Locksley R.M. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat Immunol 2012, 13:58-66.
21. Lee D.U., Rao A. Molecular analysis of a locus control region in the T helper 2 cytokine gene cluster: a target for STAT6 but not GATA3. Proc Natl Acad Sci USA 2004, 101:16010-16015.
22. Lee G.R., Fields P.E., Griffin T.J., Flavell R.A. Regulation of the Th2 cytokine locus by a locus control region. Immunity 2003, 19:145-153.
23. Ansel K.M., Djuretic I., Tanasa B., Rao A. Regulation of Th2 differentiation and Il4 locus accessibility. Annu Rev Immunol 2006, 24:607-656.
24. Lee G.R., Kim S.T., Spilianakis C.G., Fields P.E., Flavell R.A. T helper cell differentiation: regulation by cis elements and epigenetics. Immunity 2006, 24:369-379.
25. Lee G.R., Spilianakis C.G., Flavell R.A. Hypersensitive site 7 of the TH2 locus control region is essential for expressing TH2 cytokine genes and for long-range intrachromosomal interactions. Nat Immunol 2005, 6:42-48.
26. Koh B.H., Hwang S.S., Kim J.Y., Lee W., Kang M.J., Lee C.G., et al. Th2 LCR is essential for regulation of Th2 cytokine genes and for pathogenesis of allergic asthma. Proc Natl Acad Sci USA 2010, 107:10614-10619.
27. Williams A., Lee G.R., Spilianakis C.G., Hwang S.S., Eisenbarth S.C., Flavell R.A. Hypersensitive site 6 of the Th2 locus control region is essential for Th2 cytokine expression. Proc Natl Acad Sci USA 2013, 110:6955-6960.
28. Spilianakis C.G., Flavell R.A. Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat Immunol 2004, 5:1017-1027.
29. Fields P.E., Lee G.R., Kim S.T., Bartsevich V.V., Flavell R.A. Th2-specific chromatin remodeling and enhancer activity in the Th2 cytokine locus control region. Immunity 2004, 21:865-876.
30. Hwang S.S., Kim Y.U., Lee S., Jang S.W., Kim M.K., Koh B.H., et al. Transcription factor YY1 is essential for regulation of the Th2 cytokine locus and for Th2 cell differentiation. Proc Natl Acad Sci USA 2013, 110:276-281.
31. Cai S., Lee C.C., Kohwi-Shigematsu T. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat Genet 2006, 38:1278-1288.
32. Seder R.A., Paul W.E., Ben-Sasson S.Z., LeGros G.S., Kagey-Sobotka A., Finkelman F.D., et al. Production of interleukin-4 and other cytokines following stimulation of mast cell lines and in vivo mast cells/basophils. Int Arch Allergy Appl Immunol 1991, 94:137-140.
33. Ouyang W., Lohning M., Gao Z., Assenmacher M., Ranganath S., Radbruch A., et al. Stat6-independent GATA-3 autoactivation directs IL-4-independent Th2 development and commitment. Immunity 2000, 12:27-37.
34. Kaplan M.H., Schindler U., Smiley S.T., Grusby M.J. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 1996, 4:313-319.
35. Takeda K., Tanaka T., Shi W., Matsumoto M., Minami M., Kashiwamura S., et al. Essential role of Stat6 in IL-4 signalling. Nature 1996, 380:627-630.
36. Shimoda K., van Deursen J., Sangster M.Y., Sarawar S.R., Carson R.T., Tripp R.A., et al. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 1996, 380:630-633.
37. Kurata H., Lee H.J., O'Garra A., Arai N. Ectopic expression of activated Stat6 induces the expression of Th2-specific cytokines and transcription factors in developing Th1 cells. Immunity 1999, 11:677-688.
38. Tamauchi H., Terashima M., Ito M., Maruyama H., Ikewaki N., Inoue M., et al. Evidence of GATA-3-dependent Th2 commitment during the in vivo immune response. Int Immunol 2004, 16:179-187.
39. Pai S.Y., Truitt M.L., Ho I.C. GATA-3 deficiency abrogates the development and maintenance of T helper type 2 cells. Proc Natl Acad Sci USA 2004, 101:1993-1998.
40. Lee H.J., Takemoto N., Kurata H., Kamogawa Y., Miyatake S., O'Garra A., et al. GATA-3 induces T helper cell type 2 (Th2) cytokine expression and chromatin remodeling in committed Th1 cells. J Exp Med 2000, 192:105-115.
41. Zheng W., Flavell R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 1997, 89:587-596.
42. Zhang D.H., Cohn L., Ray P., Bottomly K., Ray A. Transcription factor GATA-3 is differentially expressed in murine Th1 and Th2 cells and controls Th2-specific expression of the interleukin-5 gene. J Biol Chem 1997, 272:21597-21603.
43. Ouyang W., Ranganath S.H., Weindel K., Bhattacharya D., Murphy T.L., Sha W.C., et al. Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism. Immunity 1998, 9:745-755.
44. Avni O., Lee D., Macian F., Szabo S.J., Glimcher L.H., Rao A. T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat Immunol 2002, 3:643-651.
45. Yamashita M., Ukai-Tadenuma M., Miyamoto T., Sugaya K., Hosokawa H., Hasegawa A., et al. Essential role of GATA3 for the maintenance of type 2 helper T (Th2) cytokine production and chromatin remodeling at the Th2 cytokine gene loci. J Biol Chem 2004, 279:26983-26990.
46. Wilson C.B., Rowell E., Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat Rev Immunol 2009, 9:91-105.
47. Mohrs M., Shinkai K., Mohrs K., Locksley R.M. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 2001, 15:303-311.
48. Jankovic D., Kullberg M.C., Noben-Trauth N., Caspar P., Paul W.E., Sher A. Single cell analysis reveals that IL-4 receptor/Stat6 signaling is not required for the in vivo or in vitro development of CD4+ lymphocytes with a Th2 cytokine profile. J Immunol 2000, 164:3047-3055.
49. van Panhuys N., Tang S.C., Prout M., Camberis M., Scarlett D., Roberts J., et al. In vivo studies fail to reveal a role for IL-4 or STAT6 signaling in Th2 lymphocyte differentiation. Proc Natl Acad Sci USA 2008, 105:12423-12428.
50. Cunningham A.F., Serre K., Toellner K.M., Khan M., Alexander J., Brombacher F., et al. Pinpointing IL-4-independent acquisition and IL-4-influenced maintenance of Th2 activity by CD4 T cells. Eur J Immunol 2004, 34:686-694.
51. Noben-Trauth N., Shultz L.D., Brombacher F., Urban J.F., Gu H., Paul W.E. An interleukin 4 (IL-4)-independent pathway for CD4+ T cell IL-4 production is revealed in IL-4 receptor-deficient mice. Proc Natl Acad Sci USA 1997, 94:10838-10843.
52. Cunningham A.F., Fallon P.G., Khan M., Vacheron S., Acha-Orbea H., MacLennan I.C., et al. Th2 activities induced during virgin T cell priming in the absence of IL-4, IL-13, and B cells. J Immunol 2002, 169:2900-2906.
53. McKenzie G.J., Fallon P.G., Emson C.L., Grencis R.K., McKenzie A.N. Simultaneous disruption of interleukin (IL)-4 and IL-13 defines individual roles in T helper cell type 2-mediated responses. J Exp Med 1999, 189:1565-1572.
54. Le Gros G., Ben-Sasson S.Z., Seder R., Finkelman F.D., Paul W.E. Generation of interleukin 4 (IL-4)-producing cells in vivo and in vitro: IL-2 and IL-4 are required for in vitro generation of IL-4-producing cells. J Exp Med 1990, 172:921-929.
55. Ben-Sasson S.Z., Le Gros G., Conrad D.H., Finkelman F.D., Paul W.E. IL-4 production by T cells from naive donors. IL-2 is required for IL-4 production. J Immunol 1990, 145:1127-1136.
56. Zhu J., Cote-Sierra J., Guo L., Paul W.E. Stat5 activation plays a critical role in Th2 differentiation. Immunity 2003, 19:739-748.
57. Kagami S., Nakajima H., Suto A., Hirose K., Suzuki K., Morita S., et al. Stat5a regulates T helper cell differentiation by several distinct mechanisms. Blood 2001, 97:2358-2365.
58. Kagami S., Nakajima H., Kumano K., Suzuki K., Suto A., Imada K., et al. Both stat5a and stat5b are required for antigen-induced eosinophil and T-cell recruitment into the tissue. Blood 2000, 95:1370-1377.
59. Moriggl R., Topham D.J., Teglund S., Sexl V., McKay C., Wang D., et al. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 1999, 10:249-259.
60. Takatori H., Nakajima H., Hirose K., Kagami S., Tamachi T., Suto A., et al. Indispensable role of Stat5a in Stat6-independent Th2 cell differentiation and allergic airway inflammation. J Immunol 2005, 174:3734-3740.
61. Yamane H., Zhu J., Paul W.E. Independent roles for IL-2 and GATA-3 in stimulating naive CD4+ T cells to generate a Th2-inducing cytokine environment. J Exp Med 2005, 202:793-804.
62. Cote-Sierra J., Foucras G., Guo L., Chiodetti L., Young H.A., Hu-Li J., et al. Interleukin 2 plays a central role in Th2 differentiation. Proc Natl Acad Sci USA 2004, 101:3880-3885.
63. Radtke F., Fasnacht N., Macdonald H.R. Notch signaling in the immune system. Immunity 2010, 32:14-27.
64. Minter L.M., Turley D.M., Das P., Shin H.M., Joshi I., Lawlor R.G., et al. Inhibitors of gamma-secretase block in vivo and in vitro T helper type 1 polarization by preventing Notch upregulation of Tbx21. Nat Immunol 2005, 6:680-688.
65. Amsen D., Antov A., Jankovic D., Sher A., Radtke F., Souabni A., et al. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity 2007, 27:89-99.
66. Fang T.C., Yashiro-Ohtani Y., Del Bianco C., Knoblock D.M., Blacklow S.C., Pear W.S. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 2007, 27:100-110.
67. Tu L., Fang T.C., Artis D., Shestova O., Pross S.E., Maillard I., et al. Notch signaling is an important regulator of type 2 immunity. J Exp Med 2005, 202:1037-1042.
68. Skokos D., Nussenzweig M.C. CD8-DCs induce IL-12-independent Th1 differentiation through Delta 4 Notch-like ligand in response to bacterial LPS. J Exp Med 2007, 204:1525-1531.
69. Mukherjee S., Schaller M.A., Neupane R., Kunkel S.L., Lukacs N.W. Regulation of T cell activation by Notch ligand, DLL4, promotes IL-17 production and Rorc activation. J Immunol 2009, 182:7381-7388.
70. Keerthivasan S., Suleiman R., Lawlor R., Roderick J., Bates T., Minter L., et al. Notch signaling regulates mouse and human Th17 differentiation. J Immunol 2011, 187:692-701.
71. Tanigaki K., Tsuji M., Yamamoto N., Han H., Tsukada J., Inoue H., et al. Regulation of alphabeta/gammadelta T cell lineage commitment and peripheral T cell responses by Notch/RBP-J signaling. Immunity 2004, 20:611-622.
72. Amsen D., Blander J.M., Lee G.R., Tanigaki K., Honjo T., Flavell R.A. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 2004, 117:515-526.
73. Maekawa Y., Tsukumo S., Chiba S., Hirai H., Hayashi Y., Okada H., et al. Delta1-Notch3 interactions bias the functional differentiation of activated CD4+ T cells. Immunity 2003, 19:549-559.
74. Ong C.T., Sedy J.R., Murphy K.M., Kopan R. Notch and presenilin regulate cellular expansion and cytokine secretion but cannot instruct Th1/Th2 fate acquisition. PLoS ONE 2008, 3:e2823.
75. Bailis W., Yashiro-Ohtani Y., Fang T.C., Hatton R.D., Weaver C.T., Artis D., et al. Notch simultaneously orchestrates multiple helper T cell programs independently of cytokine signals. Immunity 2013, 39:148-159.
76. Delgoffe G.M., Pollizzi K.N., Waickman A.T., Heikamp E., Meyers D.J., Horton M.R., et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol 2011, 12:295-303.
77. Lee K., Gudapati P., Dragovic S., Spencer C., Joyce S., Killeen N., et al. Mammalian target of rapamycin protein complex 2 regulates differentiation of Th1 and Th2 cell subsets via distinct signaling pathways. Immunity 2010, 32:743-753.
78. Ho I.C., Lo D., Glimcher L.H. C-maf promotes T helper cell type 2 (Th2) and attenuates Th1 differentiation by both interleukin 4-dependent and -independent mechanisms. J Exp Med 1998, 188:1859-1866.
79. Ho I.C., Hodge M.R., Rooney J.W., Glimcher L.H. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 1996, 85:973-983.
80. Kim J.I., Ho I.C., Grusby M.J., Glimcher L.H. The transcription factor c-Maf controls the production of interleukin-4 but not other Th2 cytokines. Immunity 1999, 10:745-751.
81. Rengarajan J., Mowen K.A., McBride K.D., Smith E.D., Singh H., Glimcher L.H. Interferon regulatory factor 4 (IRF4) interacts with NFATc2 to modulate interleukin 4 gene expression. J Exp Med 2002, 195:1003-1012.
82. Li B., Tournier C., Davis R.J., Flavell R.A. Regulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J 1999, 18:420-432.
83. Yang Y., Ochando J., Yopp A., Bromberg J.S., Ding Y. IL-6 plays a unique role in initiating c-Maf expression during early stage of CD4 T cell activation. J Immunol 2005, 174:2720-2729.
84. Nurieva R.I., Duong J., Kishikawa H., Dianzani U., Rojo J.M., Ho I., et al. Transcriptional regulation of th2 differentiation by inducible costimulator. Immunity 2003, 18:801-811.
85. Tanaka Y., So T., Lebedeva S., Croft M., Altman A. Impaired IL-4 and c-Maf expression and enhanced Th1-cell development in Vav1-deficient mice. Blood 2005, 106:1286-1295.
86. Gessner A., Mohrs K., Mohrs M. Mast cells, basophils, and eosinophils acquire constitutive IL-4 and IL-13 transcripts during lineage differentiation that are sufficient for rapid cytokine production. J Immunol 2005, 174:1063-1072.
87. Ying S., Humbert M., Barkans J., Corrigan C.J., Pfister R., Menz G., et al. Expression of IL-4 and IL-5 mRNA and protein product by CD4+ and CD8+ T cells, eosinophils, and mast cells in bronchial biopsies obtained from atopic and nonatopic (intrinsic) asthmatics. J Immunol 1997, 158:3539-3544.
88. Sullivan B.M., Liang H.E., Bando J.K., Wu D., Cheng L.E., McKerrow J.K., et al. Genetic analysis of basophil function in vivo. Nat Immunol 2011, 12:527-535.
89. Gibbs B.F., Haas H., Falcone F.H., Albrecht C., Vollrath I.B., Noll T., et al. Purified human peripheral blood basophils release interleukin-13 and preformed interleukin-4 following immunological activation. Eur J Immunol 1996, 26:2493-2498.
90. van Panhuys N, Prout M, Forbes E, Min B, Paul WE, Le Gros G. Basophils are the major producers of IL-4 during primary helminth infection. J Immunol 186:2719-28.
91. Li H., Sim T.C., Alam R. IL-13 released by and localized in human basophils. J Immunol 1996, 156:4833-4838.
92. Phillips C., Coward W.R., Pritchard D.I., Hewitt C.R. Basophils express a type 2 cytokine profile on exposure to proteases from helminths and house dust mites. J Leukoc Biol 2003, 73:165-171.
93. Wu D., Molofsky A.B., Liang H.E., Ricardo-Gonzalez R.R., Jouihan H.A., Bando J.K., et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 2011, 332:243-247.
94. Voehringer D., Shinkai K., Locksley R.M. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity 2004, 20:267-277.
95. Shinkai K., Mohrs M., Locksley R.M. Helper T cells regulate type-2 innate immunity in vivo. Nature 2002, 420:825-829.
96. Qiu Y., Nguyen K.D., Odegaard J.I., Cui X., Tian X., Locksley R.M., et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 2014, 157:1292-1308.
97. Spencer L.A., Melo R.C., Perez S.A., Bafford S.P., Dvorak A.M., Weller P.F. Cytokine receptor-mediated trafficking of preformed IL-4 in eosinophils identifies an innate immune mechanism of cytokine secretion. Proc Natl Acad Sci USA 2006, 103:3333-3338.
98. Spencer L.A., Szela C.T., Perez S.A., Kirchhoffer C.L., Neves J.S., Radke A.L., et al. Human eosinophils constitutively express multiple Th1, Th2, and immunoregulatory cytokines that are secreted rapidly and differentially. J Leukoc Biol 2009, 85:117-123.
99. Junttila I.S., Watson C., Kummola L., Chen X., Hu-Li J., Guo L., et al. Efficient cytokine-induced IL-13 production by mast cells requires both IL-33 and IL-3. J Allergy Clin Immunol 2013, 132(704-712):e10.
100. Toru H., Pawankar R., Ra C., Yata J., Nakahata T. Human mast cells produce IL-13 by high-affinity IgE receptor cross-linking: enhanced IL-13 production by IL-4-primed human mast cells. J Allergy Clin Immunol 1998, 102:491-502.
101. Stassen M., Muller C., Arnold M., Hultner L., Klein-Hessling S., Neudorfl C., et al. IL-9 and IL-13 production by activated mast cells is strongly enhanced in the presence of lipopolysaccharide: NF-kappa B is decisively involved in the expression of IL-9. J Immunol 2001, 166:4391-4398.
102. Wilson S.J., Shute J.K., Holgate S.T., Howarth P.H., Bradding P. Localization of interleukin (IL)-4 but not IL-5 to human mast cell secretory granules by immunoelectron microscopy. Clin Exp Allergy 2000, 30:493-500.
103. Iwamura C., Nakayama T. Role of NKT cells in allergic asthma. Curr Opin Immunol 2010, 22:807-813.
104. Thomas S.Y., Chyung Y.H., Luster A.D. Natural killer T cells are not the predominant T cell in asthma and likely modulate, not cause, asthma. J Allergy Clin Immunol 2010, 125:980-984.
105. Lisbonne M., Diem S., de Castro Keller A., Lefort J., Araujo L.M., Hachem P., et al. Cutting edge: invariant V alpha 14 NKT cells are required for allergen-induced airway inflammation and hyperreactivity in an experimental asthma model. J Immunol 2003, 171:1637-1641.
106. Meyer E.H., Goya S., Akbari O., Berry G.J., Savage P.B., Kronenberg M., et al. Glycolipid activation of invariant T cell receptor+ NK T cells is sufficient to induce airway hyperreactivity independent of conventional CD4+ T cells. Proc Natl Acad Sci USA 2006, 103:2782-2787.
107. Akbari O., Faul J.L., Hoyte E.G., Berry G.J., Wahlstrom J., Kronenberg M., et al. CD4+ invariant T-cell-receptor+ natural killer T cells in bronchial asthma. N Engl J Med 2006, 354:1117-1129.
108. Akbari O., Stock P., Meyer E., Kronenberg M., Sidobre S., Nakayama T., et al. Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat Med 2003, 9:582-588.
109. Scanlon S.T., Thomas S.Y., Ferreira C.M., Bai L., Krausz T., Savage P.B., et al. Airborne lipid antigens mobilize resident intravascular NKT cells to induce allergic airway inflammation. J Exp Med 2011, 208:2113-2124.
110. Matsuda J.L., Gapin L., Baron J.L., Sidobre S., Stetson D.B., Mohrs M., et al. Mouse V alpha 14i natural killer T cells are resistant to cytokine polarization in vivo. Proc Natl Acad Sci USA 2003, 100:8395-8400.
111. Stetson D.B., Mohrs M., Reinhardt R.L., Baron J.L., Wang Z.E., Gapin L., et al. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J Exp Med 2003, 198:1069-1076.
112. Lee P.T., Benlagha K., Teyton L., Bendelac A. Distinct functional lineages of human V(alpha)24 natural killer T cells. J Exp Med 2002, 195:637-641.
113. Wang Z.Y., Kusam S., Munugalavadla V., Kapur R., Brutkiewicz R.R., Dent A.L. Regulation of Th2 cytokine expression in NKT cells: unconventional use of Stat6, GATA-3, and NFAT2. J Immunol 2006, 176:880-888.
114. Lee Y.J., Holzapfel K.L., Zhu J., Jameson S.C., Hogquist K.A. Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 2013, 14:1146-1154.
115. Neill D.R., Wong S.H., Bellosi A., Flynn R.J., Daly M., Langford T.K., et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010, 464:1367-1370.
116. Price A.E., Liang H.E., Sullivan B.M., Reinhardt R.L., Eisley C.J., Erle D.J., et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc Natl Acad Sci USA 2010, 107:11489-11494.
117. Moro K., Yamada T., Tanabe M., Takeuchi T., Ikawa T., Kawamoto H., et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010, 463:540-544.
118. Fort M.M., Cheung J., Yen D., Li J., Zurawski S.M., Lo S., et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 2001, 15:985-995.
119. Fallon P.G., Ballantyne S.J., Mangan N.E., Barlow J.L., Dasvarma A., Hewett D.R., et al. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med 2006, 203:1105-1116.
120. Klein Wolterink R.G., Kleinjan A., van Nimwegen M., Bergen I., de Bruijn M., Levani Y., et al. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur J Immunol 2012, 42:1106-1116.
121. Nussbaum J.C., Van Dyken S.J., von Moltke J., Cheng L.E., Mohapatra A., Molofsky A.B., et al. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 2013, 502:245-248.
122. Barlow J.L., Bellosi A., Hardman C.S., Drynan L.F., Wong S.H., Cruickshank J.P., et al. Innate IL-13-producing nuocytes arise during allergic lung inflammation and contribute to airways hyperreactivity. J Allergy Clin Immunol 2012, 129(191-198):e1-e4.
123. Salimi M., Barlow J.L., Saunders S.P., Xue L., Gutowska-Owsiak D., Wang X., et al. A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J Exp Med 2013, 210:2939-2950.
124. Barlow J.L., Peel S., Fox J., Panova V., Hardman C.S., Camelo A., et al. 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 2013, 132:933-941.
125. Camelo A., Barlow J.L., Drynan L.F., Neill D.R., Ballantyne S.J., Wong S.H., et al. Blocking IL-25 signalling protects against gut inflammation in a type-2 model of colitis by suppressing nuocyte and NKT derived IL-13. J Gastroenterol 2012.
126. Chu D.K., Llop-Guevara A., Walker T.D., Flader K., Goncharova S., Boudreau J.E., et al. IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol 2013, 131(187-200):e1-e8.
127. Kim B.S., Siracusa M.C., Saenz S.A., Noti M., Monticelli L.A., Sonnenberg G.F., et al. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med 2013, 5:170ra16.
128. Mjosberg J., Bernink J., Golebski K., Karrich J.J., Peters C.P., Blom B., et al. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 2012, 37:649-659.
129. Bartemes K.R., Iijima K., Kobayashi T., Kephart G.M., McKenzie A.N., Kita H. IL-33-responsive lineage-CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol 2012, 188:1503-1513.
130. Halim T.Y., Krauss R.H., Sun A.C., Takei F. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 2012, 36:451-463.
131. Halim T.Y., Steer C.A., Matha L., Gold M.J., Martinez-Gonzalez I., McNagny K.M., et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 2014, 40:425-435.
132. Finkelman F.D., Shea-Donohue T., Morris S.C., Gildea L., Strait R., Madden K.B., et al. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol Rev 2004, 201:139-155.
133. Finkelman F.D., Shea-Donohue T., Goldhill J., Sullivan C.A., Morris S.C., Madden K.B., et al. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu Rev Immunol 1997, 15:505-533.
134. Urban J.F., Noben-Trauth N., Donaldson D.D., Madden K.B., Morris S.C., Collins M., et al. IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 1998, 8:255-264.
135. Urban J.F., Katona I.M., Paul W.E., Finkelman F.D. Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc Natl Acad Sci USA 1991, 88:5513-5517.
136. Zurawski S.M., Vega F., Huyghe B., Zurawski G. Receptors for interleukin-13 and interleukin-4 are complex and share a novel component that functions in signal transduction. EMBO J 1993, 12:2663-2670.
137. Mandel T.E., Phipps R.P., Abbot A.P., Tew J.G. Long-term antigen retention by dendritic cells in the popliteal lymph node of immunized mice. Immunology 1981, 43:353-362.
138. Urban J.F., Maliszewski C.R., Madden K.B., Katona I.M., Finkelman F.D. IL-4 treatment can cure established gastrointestinal nematode infections in immunocompetent and immunodeficient mice. J Immunol 1995, 154:4675-4684.
139. Bancroft A.J., McKenzie A.N., Grencis R.K. A critical role for IL-13 in resistance to intestinal nematode infection. J Immunol 1998, 160:3453-3461.
140. McKenzie G.J., Bancroft A., Grencis R.K., McKenzie A.N. A distinct role for interleukin-13 in Th2-cell-mediated immune responses. Curr Biol 1998, 8:339-342.
141. Lawrence R.A., Gray C.A., Osborne J., Maizels R.M. Nippostrongylus brasiliensis: cytokine responses and nematode expulsion in normal and IL-4-deficient mice. Exp Parasitol 1996, 84:65-73.
142. Fallon P.G., Jolin H.E., Smith P., Emson C.L., Townsend M.J., Fallon R., et al. IL-4 induces characteristic Th2 responses even in the combined absence of IL-5, IL-9, and IL-13. Immunity 2002, 17:7-17.
143. Madden K.B., Whitman L., Sullivan C., Gause W.C., Urban J.F., Katona I.M., et al. Role of STAT6 and mast cells in IL-4- and IL-13-induced alterations in murine intestinal epithelial cell function. J Immunol 2002, 169:4417-4422.
144. Brusselle G.G., Kips J.C., Tavernier J.H., van der Heyden J.G., Cuvelier C.A., Pauwels R.A., et al. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin Exp Allergy 1994, 24:73-80.
145. Corry D.B., Folkesson H.G., Warnock M.L., Erle D.J., Matthay M.A., Wiener-Kronish J.P., et al. Interleukin 4, but not interleukin 5 or eosinophils, is required in a murine model of acute airway hyperreactivity. J Exp Med 1996, 183:109-117.
146. Castilow E.M., Meyerholz D.K., Varga S.M. IL-13 is required for eosinophil entry into the lung during respiratory syncytial virus vaccine-enhanced disease. J Immunol 2008, 180:2376-2384.
147. Heller N.M., Gwinn W.M., Donnelly R.P., Constant S.L., Keegan A.D. IL-4 engagement of the type I IL-4 receptor complex enhances mouse eosinophil migration to eotaxin-1 in vitro. PLoS ONE 2012, 7:e39673.
148. Voehringer D., Reese T.A., Huang X., Shinkai K., Locksley R.M. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J Exp Med 2006, 203:1435-1446.
149. Min B., Prout M., Hu-Li J., Zhu J., Jankovic D., Morgan E.S., et al. Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 2004, 200:507-517.
150. Munitz A., Brandt E.B., Mingler M., Finkelman F.D., Rothenberg M.E. Distinct roles for IL-13 and IL-4 via IL-13 receptor alpha1 and the type II IL-4 receptor in asthma pathogenesis. Proc Natl Acad Sci USA 2008, 105:7240-7245.
151. Junttila I.S., Mizukami K., Dickensheets H., Meier-Schellersheim M., Yamane H., Donnelly R.P., et al. Tuning sensitivity to IL-4 and IL-13: differential expression of IL-4Ralpha, IL-13Ralpha1, and gammac regulates relative cytokine sensitivity. J Exp Med 2008, 205:2595-2608.
152. Ramalingam T.R., Pesce J.T., Sheikh F., Cheever A.W., Mentink-Kane M.M., Wilson M.S., et al. Unique functions of the type II interleukin 4 receptor identified in mice lacking the interleukin 13 receptor alpha1 chain. Nat Immunol 2008, 9:25-33.
153. Murata T., Obiri N.I., Puri R.K. Structure of and signal transduction through interleukin-4 and interleukin-13 receptors (review). Int J Mol Med 1998, 1:551-557.
154. Heller N.M., Qi X., Junttila I.S., Shirey K.A., Vogel S.N., Paul W.E., et al. Type I IL-4Rs selectively activate IRS-2 to induce target gene expression in macrophages. Sci Signal 2008, 1:ra17.
155. LaPorte S.L., Juo Z.S., Vaclavikova J., Colf L.A., Qi X., Heller N.M., et al. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 2008, 132:259-272.
156. Rothenberg M.E., Wen T., Shik D., Cole E.T., Mingler M.M., Munitz A. IL-13 receptor alpha1 differentially regulates aeroallergen-induced lung responses. J Immunol 2011, 187:4873-4880.
157. Keegan A.D., Nelms K., White M., Wang L.M., Pierce J.H., Paul W.E. An IL-4 receptor region containing an insulin receptor motif is important for IL-4-mediated IRS-1 phosphorylation and cell growth. Cell 1994, 76:811-820.
158. Wang H.Y., Zamorano J., Yoerkie J.L., Paul W.E., Keegan A.D. The IL-4-induced tyrosine phosphorylation of the insulin receptor substrate is dependent on JAK1 expression in human fibrosarcoma cells. J Immunol 1997, 158:1037-1040.
159. Heller N.M., Qi X., Gesbert F., Keegan A.D. The extracellular and transmembrane domains of the gammaC and interleukin (IL)-13 receptor alpha1 chains, not their cytoplasmic domains, dictate the nature of signaling responses to IL-4 and IL-13. J Biol Chem 2012, 287:31948-31961.
160. Hu-Li J., Pannetier C., Guo L., Lohning M., Gu H., Watson C., et al. Regulation of expression of IL-4 alleles: analysis using a chimeric GFP/IL-4 gene. Immunity 2001, 14:1-11.
161. Mohrs K., Wakil A.E., Killeen N., Locksley R.M., Mohrs M. A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity 2005, 23:419-429.
162. Reinhardt R.L., Liang H.E., Locksley R.M. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat Immunol 2009, 10:385-393.
163. Yusuf I., Kageyama R., Monticelli L., Johnston R.J., Ditoro D., Hansen K., et al. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J Immunol 2010, 185:190-202.
164. Zaretsky A.G., Taylor J.J., King I.L., Marshall F.A., Mohrs M., Pearce E.J. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J Exp Med 2009, 206:991-999.
165. King I.L., Mohrs M. IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J Exp Med 2009, 206:1001-1007.
166. Johnston R.J., Poholek A.C., DiToro D., Yusuf I., Eto D., Barnett B., et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 2009, 325:1006-1010.
167. Yu D., Rao S., Tsai L.M., Lee S.K., He Y., Sutcliffe E.L., et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 2009, 31:457-468.
168. Nurieva R.I., Chung Y., Martinez G.J., Yang X.O., Tanaka S., Matskevitch T.D., et al. Bcl6 mediates the development of T follicular helper cells. Science 2009, 325:1001-1005.
169. Kitano M., Moriyama S., Ando Y., Hikida M., Mori Y., Kurosaki T., et al. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 2011, 34:961-972.
170. Baumjohann D., Okada T., Ansel K.M. Cutting edge: distinct waves of BCL6 expression during T follicular helper cell development. J Immunol 2011, 187:2089-2092.
171. Poholek A.C., Hansen K., Hernandez S.G., Eto D., Chandele A., Weinstein J.S., et al. In vivo regulation of Bcl6 and T follicular helper cell development. J Immunol 2010, 185:313-326.
172. Zhu J., Min B., Hu-Li J., Watson C.J., Grinberg A., Wang Q., et al. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat Immunol 2004, 5:1157-1165.
173. Kishikawa H., Sun J., Choi A., Miaw S.C., Ho I.C. The cell type-specific expression of the murine IL-13 gene is regulated by GATA-3. J Immunol 2001, 167:4414-4420.
174. Zhang D.H., Yang L., Ray A. Differential responsiveness of the IL-5 and IL-4 genes to transcription factor GATA-3. J Immunol 1998, 161:3817-3821.
175. Choi Y.S., Yang J.A., Yusuf I., Johnston R.J., Greenbaum J., Peters B., et al. Bcl6 expressing follicular helper CD4 T cells are fate committed early and have the capacity to form memory. J Immunol 2013, 190:4014-4026.
176. Liu X., Yan X., Zhong B., Nurieva R.I., Wang A., Wang X., et al. Bcl6 expression specifies the T follicular helper cell program in vivo. J Exp Med 2012, 209:1841-1852.
177. Tubo N.J., Pagan A.J., Taylor J.J., Nelson R.W., Linehan J.L., Ertelt J.M., et al. Single naive CD4(+) T cells from a diverse repertoire produce different effector cell types during infection. Cell 2013, 153:785-796.
178. Hale J.S., Youngblood B., Latner D.R., Mohammed A.U., Ye L., Akondy R.S., et al. Distinct memory CD4(+) T cells with commitment to T follicular helper- and T helper 1-cell lineages are generated after acute viral infection. Immunity 2013, 38:805-817.
179. Fazilleau N., McHeyzer-Williams L.J., Rosen H., McHeyzer-Williams M.G. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat Immunol 2009, 10:375-384.
180. Fairfax K.C., Everts B., Amiel E., Smith A.M., Schramm G., Haas H., et al. IL-4-secreting secondary T follicular helper (Tfh) cells arise from memory T cells, not persisting Tfh cells, through a B cell-dependent mechanism. J Immunol 2015, 194:2999-3010.
181. Dent A.L., Doherty T.M., Paul W.E., Sher A., Staudt L.M. BCL-6-deficient mice reveal an IL-4-independent, STAT6-dependent pathway that controls susceptibility to infection by Leishmania major. J Immunol 1999, 163:2098-2103.
182. Dent A.L., Shaffer A.L., Yu X., Allman D., Staudt L.M. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 1997, 276:589-592.
183. Dent A.L., Hu-Li J., Paul W.E., Staudt L.M. T helper type 2 inflammatory disease in the absence of interleukin 4 and transcription factor STAT6. Proc Natl Acad Sci USA 1998, 95:13823-13828.
184. Ye B.H., Cattoretti G., Shen Q., Zhang J., Hawe N., de Waard R., et al. The BCL-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat Genet 1997, 16:161-170.
185. Kusam S., Toney L.M., Sato H., Dent A.L. Inhibition of Th2 differentiation and GATA-3 expression by BCL-6. J Immunol 2003, 170:2435-2441.
186. Sawant D.V., Sehra S., Nguyen E.T., Jadhav R., Englert K., Shinnakasu R., et al. Bcl6 controls the Th2 inflammatory activity of regulatory T cells by repressing Gata3 function. J Immunol 2012, 189:4759-4769.
187. Pepper M., Pagan A.J., Igyarto B.Z., Taylor J.J., Jenkins M.K. Opposing signals from the bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 2011, 35:583-595.
188. Nurieva R.I., Podd A., Chen Y., Alekseev A.M., Yu M., Qi X., et al. STAT5 protein negatively regulates T follicular helper (Tfh) cell generation and function. J Biol Chem 2012, 287:11234-11239.
189. Johnston R.J., Choi Y.S., Diamond J.A., Yang J.A., Crotty S. STAT5 is a potent negative regulator of TFH cell differentiation. J Exp Med 2012, 209:243-250.
190. Cannons J.L., Yu L.J., Jankovic D., Crotty S., Horai R., Kirby M., et al. SAP regulates T cell-mediated help for humoral immunity by a mechanism distinct from cytokine regulation. J Exp Med 2006, 203:1551-1565.
191. Crotty S., Kersh E.N., Cannons J., Schwartzberg P.L., Ahmed R. SAP is required for generating long-term humoral immunity. Nature 2003, 421:282-287.
192. Cannons J.L., Qi H., Lu K.T., Dutta M., Gomez-Rodriguez J., Cheng J., et al. Optimal germinal center responses require a multistage T cell: B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2010, 32:253-265.
193. Qi H., Cannons J.L., Klauschen F., Schwartzberg P.L., Germain R.N. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008, 455:764-769.
194. Cannons J.L., Yu L.J., Hill B., Mijares L.A., Dombroski D., Nichols K.E., et al. SAP regulates T(H)2 differentiation and PKC-theta-mediated activation of NF-kappaB1. Immunity 2004, 21:693-706.
195. Haynes N.M., Allen C.D., Lesley R., Ansel K.M., Killeen N., Cyster J.G. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1 high germinal center-associated subpopulation. J Immunol 2007, 179:5099-5108.
196. Liu X., Chen X., Zhong B., Wang A., Wang X., Chu F., et al. Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development. Nature 2014, 507:513-518.
197. Greenwald R.J., McAdam A.J., Van der Woude D., Satoskar A.R., Sharpe A.H. Cutting edge: inducible costimulator protein regulates both Th1 and Th2 responses to cutaneous leishmaniasis. J Immunol 2002, 168:991-995.
198. Tesciuba A.G., Subudhi S., Rother R.P., Faas S.J., Frantz A.M., Elliot D., et al. Inducible costimulator regulates Th2-mediated inflammation, but not Th2 differentiation, in a model of allergic airway disease. J Immunol 2001, 167:1996-2003.
199. Tafuri A., Shahinian A., Bladt F., Yoshinaga S.K., Jordana M., Wakeham A., et al. ICOS is essential for effective T-helper-cell responses. Nature 2001, 409:105-109.
200. Dong C., Temann U.A., Flavell R.A. Cutting edge: critical role of inducible costimulator in germinal center reactions. J Immunol 2001, 166:3659-3662.
201. Loke P., Zang X., Hsuan L., Waitz R., Locksley R.M., Allen J.E., et al. Inducible costimulator is required for type 2 antibody isotype switching but not T helper cell type 2 responses in chronic nematode infection. Proc Natl Acad Sci USA 2005, 102:9872-9877.
202. Scales H.E., Ierna M.X., Gutierrez-Ramos J.C., Coyle A.J., Garside P., Lawrence C.E. Effect of inducible costimulator blockade on the pathological and protective immune responses induced by the gastrointestinal helminth Trichinella spiralis. Eur J Immunol 2004, 34:2854-2862.
203. Xu H., Li X., Liu D., Li J., Zhang X., Chen X., et al. Follicular T-helper cell recruitment governed by bystander B cells and ICOS-driven motility. Nature 2013, 496:523-527.
204. Choi Y.S., Kageyama R., Eto D., Escobar T.C., Johnston R.J., Monticelli L., et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 2011, 34:932-946.
205. Gigoux M., Shang J., Pak Y., Xu M., Choe J., Mak T.W., et al. Inducible costimulator promotes helper T-cell differentiation through phosphoinositide 3-kinase. Proc Natl Acad Sci USA 2009, 106:20371-20376.
206. Nurieva R.I., Chung Y., Hwang D., Yang X.O., Kang H.S., Ma L., et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 2008, 29:138-149.
207. Bauquet A.T., Jin H., Paterson A.M., Mitsdoerffer M., Ho I.C., Sharpe A.H., et al. The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat Immunol 2009, 10:167-175.
208. Ise W., Kohyama M., Schraml B.U., Zhang T., Schwer B., Basu U., et al. The transcription factor BATF controls the global regulators of class-switch recombination in both B cells and T cells. Nat Immunol 2011, 12:536-543.
209. Kroenke M.A., Eto D., Locci M., Cho M., Davidson T., Haddad E.K., et al. Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation. J Immunol 2012, 188:3734-3744.
210. Ubel C., Sopel N., Graser A., Hildner K., Reinhardt C., Zimmermann T., et al. The activating protein 1 transcription factor basic leucine zipper transcription factor, ATF-like (BATF), regulates lymphocyte- and mast cell-driven immune responses in the setting of allergic asthma. J Allergy Clin Immunol 2014, 133(198-206):e1-e9.
211. Jabeen R., Goswami R., Awe O., Kulkarni A., Nguyen E.T., Attenasio A., et al. Th9 cell development requires a BATF-regulated transcriptional network. J Clin Invest 2013, 123:4641-4653.
212. van den Ham H.J., de Waal L., Zaaraoui-Boutahar F., Bijl M., van Ijcken W.F., Osterhaus A.D., et al. Early divergence of Th1 and Th2 transcriptomes involves a small core response and sets of transiently expressed genes. Eur J Immunol 2013, 43:1074-1084.
213. Vijayanand P., Seumois G., Simpson L.J., Abdul-Wajid S., Baumjohann D., Panduro M., et al. Interleukin-4 production by follicular helper T cells requires the conserved Il4 enhancer hypersensitivity site V. Immunity 2012, 36:175-187.
214. Harada Y., Tanaka S., Motomura Y., Ohno S., Yanagi Y., Inoue H., et al. The 3' enhancer CNS2 is a critical regulator of interleukin-4-mediated humoral immunity in follicular helper T cells. Immunity 2012, 36:188-200.
215. Tanaka S., Tsukada J., Suzuki W., Hayashi K., Tanigaki K., Tsuji M., et al. The interleukin-4 enhancer CNS-2 is regulated by Notch signals and controls initial expression in NKT cells and memory-type CD4 T cells. Immunity 2006, 24:689-701.
216. Auderset F., Schuster S., Fasnacht N., Coutaz M., Charmoy M., Koch U., et al. Notch signaling regulates follicular helper T cell differentiation. J Immunol 2013, 191:2344-2350.
217. Serafini N., Klein Wolterink R.G., Satoh-Takayama N., Xu W., Vosshenrich C.A., Hendriks R.W., et al. Gata3 drives development of RORgammat+ group 3 innate lymphoid cells. J Exp Med 2014, 211:199-208.
218. Hoyler T., Klose C.S., Souabni A., Turqueti-Neves A., Pfeifer D., Rawlins E.L., et al. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012, 37:634-648.
219. Parker W., Ollerton J. Evolutionary biology and anthropology suggest biome reconstitution as a necessary approach toward dealing with immune disorders. Evol Med Publ Health 2013, 2013:89-103.
220. Manconi R., Poletti A., Volpe R., Sulfaro S., Carbone A. Dendritic reticulum cell pattern as a microenvironmental indicator for a distinct origin of lymphoma of follicular mantle cells. Br J Haematol 1988, 68:213-218.
221. Carbone A., Gloghini A., Gruss H.J., Pinto A. CD40 ligand is constitutively expressed in a subset of T cell lymphomas and on the microenvironmental reactive T cells of follicular lymphomas and Hodgkin's disease. Am J Pathol 1995, 147:912-922.
222. Ame-Thomas P., Le Priol J., Yssel H., Caron G., Pangault C., Jean R., et al. Characterization of intratumoral follicular helper T cells in follicular lymphoma: role in the survival of malignant B cells. Leukemia 2011.
223. Calvo K.R., Dabir B., Kovach A., Devor C., Bandle R., Bond A., et al. IL-4 protein expression and basal activation of Erk in vivo in follicular lymphoma. Blood 2008, 112:3818-3826.
224. Pangault C., Ame-Thomas P., Ruminy P., Rossille D., Caron G., Baia M., et al. Follicular lymphoma cell niche: identification of a preeminent IL-4-dependent T(FH)-B cell axis. Leukemia 2010, 24:2080-2089.
225. Fabbri G., Rasi S., Rossi D., Trifonov V., Khiabanian H., Ma J., et al. Analysis of the chronic lymphocytic leukemia coding genome: role of NOTCH1 mutational activation. J Exp Med 2011, 208:1389-1401.
226. Puente X.S., Pinyol M., Quesada V., Conde L., Ordonez G.R., Villamor N., et al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia. Nature 2011, 475:101-105.
227. Lee S.Y., Kumano K., Nakazaki K., Sanada M., Matsumoto A., Yamamoto G., et al. Gain-of-function mutations and copy number increases of Notch2 in diffuse large B-cell lymphoma. Cancer Sci 2009, 100:920-926.
228. Morito N., Yoh K., Fujioka Y., Nakano T., Shimohata H., Hashimoto Y., et al. Overexpression of c-Maf contributes to T-cell lymphoma in both mice and human. Cancer Res 2006, 66:812-819.
229. Murakami Y.I., Yatabe Y., Sakaguchi T., Sasaki E., Yamashita Y., Morito N., et al. C-Maf expression in angioimmunoblastic T-cell lymphoma. Am J Surg Pathol 2007, 31:1695-1702.
230. Bisig B., Thielen C., Herens C., Gofflot S., Travert M., Delfau-Larue M.H., et al. C-Maf expression in angioimmunoblastic T-cell lymphoma reflects follicular helper T-cell derivation rather than oncogenesis. Histopathology 2012, 60:371-376.