Nature versus nurture in T cell cytokine production

Journal of Leukocyte Biology

Volumn 66, Issue 6, 1999, Pages 869-875

  Fitzpatrick, David R ^a   Kelso, Anne ^b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b NONE

Author keywords

Differentiation; Epigenetic; Interferon; Interleukin; T lymphocyte

Indexed keywords

CYTOKINE; INTERFERON;

CELL ACTIVATION; CELL CONTACT; CELL DIFFERENTIATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; IMMUNE RESPONSE; IMMUNOSTIMULATION; LYMPHOCYTE FUNCTION; MEMORY CELL; POLARIZATION; PRIORITY JOURNAL; REVIEW; STOCHASTIC MODEL; T LYMPHOCYTE;

EID: 0033404774     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1002/jlb.66.6.869     Document Type: Review

References (113)

1. Kupiec, J. J. (1997) A Darwinian theory for the origin of cellular differentiation. Mol. Gen. Genet. 255, 201-208.
2. Ko, M. S. (1992) Induction mechanism of a single gene molecule: stochastic or deterministic? Bioessays 14, 341-346.
3. Abbas, A. K., Murphy, K. M., Sher, A. (1996) Functional diversity of helper T lymphocytes. Nature 383, 787-793.
4. Mosmann, T. R., Sad, S. (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol. Today 17, 138-146.
5. + T cells and clones activated in vivo and in vitro. Immunol. Rev. 123, 85-114.
6. Kelso, A. (1995) Th1 and Th2 subsets: paradigms lost? Immunol. Today 16, 374-379.
7. Assenmacher, M., Schmitz, J., Radbruch, A. (1994) Flow cytometric determination of cytokines in activated murine T helper lymphocytes: expression of interleukin-10 in interferon-γ and in interleukin-4-expressing cells. Eur. J. Immunol. 24, 1097-1101.
8. Bucy, R. P., Panoskaltsis-Mortari, A., Huang, G., Li, J., Karr, L., Ross, M., Russell, J. H., Murphy, K. M., Weaver, C. T. (1994) Heterogeneity of single cell cytokine gene expression in clonal T cell populations. J. Exp. Med. 180, 1251-1262.
9. + T cells activated in a T helper type 2-like response in vivo. Eur. J. Immunol. 25, 1168-1175.
10. Openshaw, P., Murphy, E. E., Hosken, N. A., Maino, V., Davis, K., Murphy, K., O'Garra, A. (1995) Heterogeneity of intracellular cytokine synthesis at the single-cell level in polarized T helper 1 and T helper 2 populations. J. Exp. Med. 182, 1357-1367.
11. + T cell populations. Int. Immunol. 11, 617-621.
12. Weiner, H. L. (1997) Oral tolerance: immune mechanisms and treatment of autoimmune diseases. Immunol. Today 18, 335-343.
13. O'Garra, A. (1998) Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8, 275-283.
14. Thomson, A. W. (1998) The Cytokine Handbook. London: Academic Press.
15. Berzofsky, J. (1988) Immunodominance in T lymphocyte recognition. Immunol. Lett. 18, 83-92.
16. Janeway, C. A., Bottomly, K. (1994) Signals and signs for lymphocyte responses. Cell 76, 275-285.
17. Garside, P., Mowat, A. M. (1995) Polarization of Th-cell responses: a phylogenetic consequence of nonspecific immune defence? Immunol. Today 16, 220-223.
18. Fearon, D. T., Locksley, R. M. (1996) The instructive role of innate immunity in the acquired immune response. Science 272, 50-54.
19. Zinkernagel, R. M., Ehl, S., Aichele, P., Oehen, S., Kundig, T., Hengartner, H. (1997) Antigen localisation regulates immune responses in a dose-and time-dependent fashion: a geographical view of immune reactivity. Immunol. Rev. 156, 199-209.
20. Banchereau, J., Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252.
21. Whitton, J. L. (1998) An overview of antigen presentation and its central role in the immune response. Curr. Top. Microbiol. Immunol. 232, 1-13.
22. Chambers, C. A., Allison, J. P. (1999) Costimulatory regulation of T cell function. Curr. Opin. Cell Biol. 11, 203-210.
23. Daynes, R. A., Araneo, B. A., Dowell, T. A., Huang, K., Dudley, D. (1990) Regulation of murine lymphokine production in vivo. III. The lymphoid tissue microenvironment exerts regulatory influences over T helper cell function. J. Exp. Med. 171, 979-996.
24. Everson, M. P., McDuffie, D. S., Lemak, D. G., Koopman, W. J., McGhee, J. R., Beagley, K. W. (1996) Dendritic cells from different tissues induce production of different T cell cytokine profiles. J. Leukoc. Biol. 59, 494-498.
25. Stumbles, P. A., Thomas, J. A., Pimm, C. L., Lee, P. T., Venaille, T. J., Proksch, S., Holt, P. G. (1998) Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J. Exp. Med. 188, 2019-2031.
26. Pulendran, B., Smith, J. L., Caspary, G., Brasel, K., Pettit, D., Maraskovsky, E., Maliszewski, C. R. (1999) Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 96, 1036-1041.
27. Rissoan, A., Soumelis, V., Kadowaki, N., Grouard, G., Briere, F., de Waal Malefyt, R., Liu, Y. (1999) Reciprocal control of T helper cell and dendritic cell differentiation. Science 283, 1183-1186.
28. + T cells. J. Exp. Med. 182, 1591-1596.
29. + T helper cell phenotype development in a T cell receptor-alpha-beta-transgenic model. J. Exp. Med. 182, 1579-1584.
30. Murray, J. S. (1998) How the MHC selects Th1/Th2 immunity. Immunol. Today 19, 157-163.
31. Lanzavecchia, A., Iezzi, G., Viola, A. (1999) From TCR engagement to T cell activation: a kinetic view of T cell behavior. Cell 96, 1-4.
32. Hsieh, C., Macatonia, S. E., O'Garra, A., Murphy, K. M. (1995) T cell genetic background determines default T helper phenotype development in vitro. J. Exp. Med. 181, 713-721.
33. Lipoldova, M., Kosarova, M., Zajicova, A., Holan, V., Hart, A. M., Krulova, M., Demant, P. (1995) Separation of multiple genes controlling the T-cell proliferative response to IL-2 and anti-CD3 using recombinant congenic strains. Immunogenet. 132, 301-311.
34. Gorham, J. D., Guler, M. L., Steen, R. G., Mackey, A. J., Daly, M. J., Frederick, K., Dietrich, W. F., Murphy, K. M. (1996) Genetic mapping of a murine locus controlling development of T helper 1/T helper 2 type responses. Proc. Natl. Acad. Sci. USA 93, 12467-12472.
35. Guler, M. L., Gorham, J. D., Hsieh, C., Mackey, A. J., Steen, R. G., Dietrich, W. F., Murphy, K. M. (1996) Genetic susceptibility to leishmania: IL-12 responsiveness in Th1 cell development. Science 271, 984-987.
36. Havelkova, H., Krulova, M., Kosarova, M., Holan, V., Hart, A. A., Demant, P., Lipoldova, M. (1996) Genetic control of T-cell proliferative response in mice linked to chromosomes 11 and 15. Immunogenet. 44, 475-477.
37. Conboy, I. M., DeKruyff, R. H., Tate, K. M., Cao, Z. A., Moore, T. A., Umetsu, D. T., Jones, P. P. (1997) Novel genetic regulation of T helper 1 (Th1)/Th2 cytokine production and encephalitogenicity in inbred mouse strains. J. Exp. Med. 185, 439-451.
38. + T cell-intrinsic mechanism. J. Exp. Med. 188. 2289-2299.
39. Guler, M. L., Gorham, J. D., Dietrich, W. F., Murphy, T. L., Steen, R. G., Parvin, C. A., Fenoglio, D., Grupe, A., Peltz, G., Murphy, K. M. (1999) Tpml, a locus controlling IL-12 responsiveness, acts by a cell-autonomous mechanism. J. Immunol. 162, 1339-1347.
40. McKenzie, A. N., Li, X., Largaespada, D. A., Sato, A., Kaneda, A., Zurawski, S. M., Doyle, E. L., Milatovich, A., Francke, U., Copeland, N. G., Jenkins, N. A., Zurawski, G. (1993) Structural comparison and chromosomal localization of the human and mouse IL-13 genes. J. Immunol. 150, 5436-5444.
41. Kelso, A., Metcalf, D., Gough, N. M. (1986) Independent regulation of granulocyte-macrophage colony-stimulating factor and multi-lineage colony-stimulating factor production in T lymphocyte clones. J. Immunol. 136, 1718-1725.
42. Kelso, A., Gough, N. M. (1988) Coexpression of granulocyte-macrophage colony-stimulating factor, gamma interferon, and interleukins 3 and 4 is random in murine alloreactive T-lymphocyte clones. Proc. Natl. Acad. Sci. USA 85, 9189-9193.
43. Kelso, A., Owens, T. (1988) Production of two hemopoietic growth factors is differentially regulated in single T lymphocytes activated with an anti-T-cell receptor antibody. J. Immunol. 140, 1159-1167.
44. + Th0, Th1 and Th2 cell clones and EBV-transformed B cells. Int. Immunol. 7, 1405-1416.
45. Fitzpatrick, D. R., Kelso, A. (1995) Dissociated expression of granulocyte-macrophage CSF and IL-3 in short-term T cell clones from normal mice. J. Immunol. 155, 5140-5150.
46. Egerton, M., Fitzpatrick, D. R., Catling, A. D., Kelso, A. (1996) Differential activation of T cell cytokine production by the extracellular signal-regulated kinase (ERK) signaling pathway. Eur. J. Immunol. 26, 2279-2285.
47. + T cells. J. Exp. Med. 186, 757-766.
48. Egerton, M., Fitzpatrick, D. R., Kelso, A. (1998) Activation of the extracellular signal-regulated kinase pathway is differentially required for TCR-stimulated production of six cytokines in primary T lymphocytes. Int. Immunol. 10, 223-229.
49. Fitzpatrick, D. R., Kelso, A. (1998) Independent regulation of cytokine genes in T cells: the paradox in the paradigm. Transplantation 65, 1-5.
50. Weaver, C. T., Saparov, A., Kraus, L. A., Rogers, W. O., Hockett, R. D., Bucy, R. P. (1998) Heterogeneity in the clonal T cell response. Immunol. Res. 17, 279-302.
51. Bird, J. J., Brown, D. R., Mullen, A. C., Moskowitz, N. H., Mahowald, M. A., Sider, J. R., Gajewski, T. F., Wang, C., Reiner, S. L. (1998) Helper T cell differentiation is controlled by the cell cycle. Immunity 9, 229-237.
52. Gett, A. V., Hodgkin, P. D. (1998) Cell division regulates the T cell cytokine repertoire, revealing a mechanism underlying immune class regulation. Proc. Natl. Acad. Sci. USA 95, 9488-9493.
53. Young, H. A., Ghosh, P., Ye, J., Lederer, J., Lichtman, A., Gerard, J., Penix, L., Wilson, C. B., Melvin, A. J., McGurn, M., Lewis, D. B., Taub, D. (1994) Differentiation of the T helper phenotypes by analysis of the methylation state of the IFN-γ gene. J. Immunol. 153, 3603-3610.
54. Melvin, A. J., McGurn, M. E., Bort, S. J., Gibson, C., Lewis, D. B. (1995) Hypomethylation of the interferon-γ gene correlates with its expression by primary T-lineage cells. Eur. J. Immunol. 25, 426-430.
55. Penix, L. A., Sweetser, M. T., Weaver, W. M., Hoeffler, J. P., Kerppola, T. K., Wilson, C. B. (1996) The proximal regulatory element of the interferon-γ promoter mediates selective expression in T cells. J. Biol. Chem. 271, 31964-31972.
56. + T cells. J. Exp. Med. 188, 103-117.
57. Agarwal, S., Rao, A. (1998) Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 9, 765-775.
58. Ward, S. B., Hernandez-Hoyos, G., Chen, F., Waterman, M., Reeves, R., Rothenberg, E. V. (1998) Chromatin remodeling of the interleukin-2 gene: distinct alterations in the proximal versus distal enhancer regions. Nucleic Acids Res. 26, 2923-2934.
59. + T lymphocytes. J. Immunol. 162, 5053-5057.
60. + T cells. Science 281, 1352-1354.
61. Hollander, G. A., Zuklys, S., Morel, C., Mizoguchi, E., Mobisson, K., Simpson, S., Terhorst, C., Wishart, W., Golan, D. E., Bhan, A. K., Burakoff, S. J. (1998) Monoallelic expression of the interleukin-2 locus. Science 279, 2118-2121.
62. Naramura, M., Hu, R., Gu, H. (1998) Mice with a fluorescent marker for interleukin-2 gene activation. Immunity 9, 209-216.
63. Riviere, I., Sunshine, M. J., Littman, D. R. (1998) Regulation of IL-4 expression by activation of individual alleles. Immunity 9, 217-228.
64. Mosmann, T. R., Moore, K. W. (1991) The role of IL-10 in crossregulation of Th1 and Th2 responses. Immunol. Today 12, A49-A53.
65. Muraille, E., Leo, O. (1998) Revisiting the Th1/Th2 paradigm. Scand. J. Immunol. 47, 1-9.
66. Murphy, K. M. (1998) T lymphocyte development in the periphery. Curr. Opin. Immunol. 10, 226-232.
67. Szabo, S. J., Jacobsen, N. G., Dighe, A. S., Gubler, U., Murphy, K. M. (1995) Developmental commitment to the Th2 lineage by extinction of IL-12 signaling. Immunity 2, 665-675.
68. Rogge, L., Barberis-Maino, L., Biffi, M., Passini, N., Presky, D. H., Gubler, U., Sinigaglia, F. (1997) Selective expression of an interleukin-12 receptor component by human T helper 1 cells. J. Exp. Med. 185, 825-831.
69. Szabo, S. J., Dighe, A., Gubler, U., Murphy, K. M. (1997) Regulation of the interleukin (IL)-12R beta 2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J. Exp. Med. 185, 817-824.
70. Xu, D., Chan, W. L., Leung, B. P., Hunter, D., Schulz, K., Carter, R. W., McInnes, I. B., Robinson, J. H., Liew, F. Y. (1998) Selective expression and functions of interleukin-18 receptor on T helper (Th) type 1 but not Th2 cells. J. Exp. Med. 188, 1485-1492.
71. + T cells, interleukin 4 production is cytokine-autonomous, whereas interferon γ production is cytokine-dependent. Proc. Natl. Acad. Sci. USA 94, 3189-3194.
72. Huang, H., Paul, W. E. (1998) Impaired interleukin-4 signaling in T helper type 1 cells. J. Exp. Med. 187, 1305-1313.
73. Ho, I., Hodge, M. R., Rooney, J. W., Glimcher, L. H. (1996) The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85, 973-983.
74. Hodge, M. R., Chun, H. J., Rengarajan, J., Alt, A., Lieberson, R., Glimcher, L. H. (1996) NF-AT-driven interleukin-4 transcription potentiated by NIP45. Science 274, 1903-1905.
75. Kubo, M., Ransom, J., Webb, D., Hashimoto, Y., Tada, T., Nakayama, T. (1997) T-cell subset-specific expression of the IL-4 gene is regulated by a silencer element and STAT6. EMBO J. 16, 4007-4020.
76. Zheng, W., Flavell, R. A. (1997) The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89, 587-596.
77. Ho, I., Lo, D., Glimcher, L. H. (1998) c-maf promotes T helper cell type 2 (Th2) and attenuates Th1 differentiation by both interleukin-4-dependent and -independent mechanisms. J. Exp. Med. 188, 1859-1866.
78. Yoshida, H., Nishina, H., Takimoto, H., Marengere, L. E., Wakeham, A. C., Bouchard, D., Kong, Y., Ohteki, T., Shahinian, A., Bachmann, M., Ohashi, P. S., Penninger, J. M., Crabtree, G. R., Mak, T. W. (1998) The transcription factor NF-ATc1 regulates lymphocyte proliferation and Th2 cytokine production. Immunity 8, 115-124.
79. Li, B., Tournier, C., Davis, R. J., Flavell, R. A. (1999) Regulation of IL-4 expression by the transcription factor junB during T helper cell differentiation. EMBO J. 18, 420-432.
80. Penix, L., Weaver, W. M., Pang, Y., Young, H. A., Wilson, C. B. (1993) Two essential regulatory elements in the human interferon-γ promoter confer activation specific expression in T cells. J. Exp. Med. 178, 1483-1496.
81. Young, H. A., Ghosh, P. (1997) Molecular regulation of cytokine gene expression: interferon-γ as a model system. Prog. Nucleic Acid Res. Mol. Biol. 56, 109-127.
82. Ouyang, W., Ranganath, S. H., Weindel, K., Bhattacharya, D., Murphy, T. L., Sha, W. C., Murphy, K. M. (1998) Inhibition of Th1 development mediated by GATA-3 through an IL-4-imlependent mechanism. Immunity 9, 745-755.
83. Sweetser, M. T., Hoey, T., Sun, Y., Weaver, W. M., Price, G. A., Wilson, C. B. (1998) The roles of nuclear factor of activated T cells and ying-yang 1 in activation-induced expression of the interferon-γ promoter in T cells. J. Biol. Chem. 273, 34775-34783.
84. Ouyang, W., Jacobsen, N. G., Bhattacharya, D., Gorham, J. D., Fenoglio, D., Sha, W. C., Murphy, T. L., Murphy, K. M. (1999) The Ets transcription factor ERM is Th1-specific and induced by IL-12 through a STAT4-dependent pathway. Proc. Natl. Acad. Sci. USA 96, 3888-3893.
85. Glimcher, L. H., Singh, H. (1999) Transcription factors in lymphocyte development - T and B cells get together. Cell 96, 13-23.
86. Mocci, S., Coffman, R. L. (1995) Induction of a Th2 population from a polarized Leishmania-specific Th1 population by in vitro culture with IL-4. J. Immunol. 154, 3779-3787.
87. Perez, V. L., Lederer, J. A., Lichtman, A. H., Abbas, A. K. (1995) Stability of Th1 and Th2 populations. Int. Immunol. 7, 869-875.
88. Lederer, J. A., Perez, V. L., Desroches, L., Kim, S. M., Abbas, A. K., Lichtman, A. H. (1996) Cytokine transcriptional events during helper T cell subset differentiation. J. Exp. Med. 184, 397-406.
89. Murphy, E., Shibuya, K., Hosken, N., Openshaw, P., Maino, V., Davis, K., Murphy, K., O'Garra, A. (1996) Reversibility of T helper 1 and 2 populations is lost after long-term stimulation. J. Exp. Med. 183, 901-913.
90. + T cells, analyzed at the single-cell level. J. Exp. Med. 184, 473-483.
91. Assenmacher, M., Lohning, M., Scheffold, A., Richter, A., Miltenyi, S., Schmitz, J., Radbruch, A. (1998) Commitment of individual Th1-like lymphocytes to expression of IFN-γ versus IL-4 and IL-10: selective induction of IL-10 by sequential stimulation of naive Th cells with IL-12 and IL-4. J. Immunol. 161, 2825-2832.
92. Miner, K. T., Croft, M. (1998) Generation, persistence, and modulation of Th0 effector cells: role of autocrine IL-4 and IFN-γ. J. Immunol. 160, 5280-5287.
93. + T cells producing IL-2 or IL-4. J. Immunol. 148, 1031-1036.
94. Manetti, R., Gerosa, F., Giudizi, M. G., Biagiotti, R., Parronchi, P., Piccinni, M., Sampognaro, S., Maggi, E., Romagnani, S., Trinchieri, G. (1994) Interleukin-12 induces stable priming for interferon-γ (IFN-γ) production during differentiation of human T helper (Th) cells and transient IFN-γ production in established Th2 clones. J. Exp. Med. 179, 1273-1283.
95. + T cells secreting Th1 or Th2 cytokines. Immunity 2, 271-279.
96. + T cell can give rise to progeny expressing type 1 and/or type 2 cytokine genes and can retain its multipotentiality through many cell divisions. Proc. Natl. Acad. Sci. USA 94, 8070-8075.
97. Sprent, J., Tough, D. F. (1994) Lymphocyte life-span and memory. Science 265, 1395-1400.
98. Ahmed, R., Gray, D. (1996) Immunological memory and protective immunity: understanding their relation. Science 272, 54-60.
99. Swain, S. L., Croft, M., Dubey, C., Haynes, L., Rogers, P., Zhang, X., Bradley, L. M. (1996) From naive to memory T cells. Immunol. Rev. 150, 143-167.
100. Dutton, R. W., Bradley, L. M., Swain, S. (1998) T cell memory. Annu. Rev. Immunol. 16, 201-223.
101. Swain, S. L. (1994) Generation and in vivo persistence of polarized Th1 and Th2 memory cells. Immunity 1, 543-552.
102. Cerwenka, A., Carter, L. L., Reome, J. B., Swain, S. L., Dutton, R. W. (1998) In vivo persistence of CD8 polarized T cell subsets producing type 1 or type 2 cytokines. J. Immunol. 161, 97-105.
103. Murali-Krishna, K., Altman, J. D., Suresh, M., Sourdive, D. J., Zajac, A. J., Miller, J. D., Slansky, J., Ahmed, R. (1998) Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8, 177-187.
104. + T cell function during in vivo memory in tolerance induction. Immunity 8, 581-590.
105. Farber, D. L. (1998) Differential TCR signaling and the generation of memory T cells. J. Immunol. 160, 535-539.
106. Antia, R., Pilyugin, S. S., Ahmed, R. (1998) Models of immune memory: on the role of cross-reactive stimulation, competition, and homeostasis in maintaining immune memory. Proc. Natl. Acad. Sci. USA 95, 14926-14931.
107. Cross, M. A., Enver, T. (1997) The lineage commitment of haemopoietic progenitor cells. Curr. Opin. Genet. Dev. 7, 609-613.
108. Socolovsky, M., Lodish, H. F., Daley, G. Q. (1998) Control of hematopoietic differentiation: lack of specificity in signaling by cytokine receptors. Proc. Natl. Acad. Sci. USA 95, 6573-6575.
109. Wilkinson, H. A., Fitzgerald, K., Greenwald, I. (1994) Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior to commitment in a C. elegans cell fate decision. Cell 79, 1187-1198.
110. Jan, Y. N., Jan, L. Y. (1998) Asymmetric cell division. Nature 392, 775-778.
111. Cook, D. L., Gerber, A. N., Tapscott, S. J. (1998) Modeling stochastic gene expression: implications for haploinsufficiency. Proc. Natl. Acad. Sci. USA 95, 15641-15646.
112. Nowak, M. A., et al. (1997) Evolution of genetic redundancy. Nature 388, 167-171.
113. McAdams, H. H., Arkin, A. (1999) It's a noisy business! Genetic regulation at the nanomolar scale. Trends Genet. 15, 65-69.