Heterogeneity in the CD4 T cell compartment and the variability of neonatal immune responsiveness

Current Immunology Reviews

Volumn 3, Issue 3, 2007, Pages 151-159

  Adkins, Becky ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Animals; Comparative immunology; Cytokines; Immune plasticity; Newborn; Ontogeny; Th1 Th2 cells; Vaccination

Indexed keywords

CD4 ANTIGEN; CD45RA ANTIGEN; CD8 ANTIGEN; CYTOKINE; DNA NUCLEOTIDYLEXOTRANSFERASE; T LYMPHOCYTE RECEPTOR;

CD4+ T LYMPHOCYTE; CELL HETEROGENEITY; CELL TYPE; CELLULAR IMMUNITY; DEVELOPMENTAL STAGE; EPIGENETICS; FETUS; FETUS CELL; GENE LOCUS; GENETIC VARIABILITY; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IMMUNE RESPONSE; INFLAMMATION; LYMPHOCYTE PROLIFERATION; MOUSE; NEWBORN; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL; THYMOCYTE;

EID: 41649099526     PISSN: 15733955     EISSN: None     Source Type: Journal    
DOI: 10.2174/157339507781483496     Document Type: Review

References (97)

1. Siegrist CA. Vaccination in the neonatal period and early infancy. Int Rev Immunol 2000; 19: 195-219.
2. Fadel S, Sarzotti M. Cellular immune responses in neonates. Int Rev Immunol. 2000; 19: 173-93.
3. Adkins B. Development of neonatal Th1/Th2 function. Int Rev Immunol 2000; 19: 157-171.
4. Ribeiro-do-Couto LM, Boeije LC, Kroon JS, et al. High IL-13 production by human neonatal T cells: neonate immune system regulator? Eur J Immunol 2001; 31: 3394-402.
5. Webster RB, Rodriguez Y, Klimecki WT and Vercelli D. The human IL-13 locus in neonatal CD4+ T cells is refractory to the acquisition of a repressive chromatin architecture. J Biol Chem 2007; 282: 700-9.
6. Upham JW, Rate A, Rowe J, Kusel M, Sly PD and Holt PG. Dendritic cell immaturity during infancy restricts the capacity to express vaccine-specific T-cell memory. Infect Immun 2006; 74: 1106-12.
7. Prescott SL, Macaubas C, Holt BJ, et al. Transplacental priming of the human immune system to environmental allergens: universal skewing of initial T cell responses toward the Th2 cytokine profile. J Immunol 1998; 160: 4730-7.
8. Adkins B, Marshall-Clarke S and Leclerc C. Neonatal adaptive immunity comes of age. Nat Rev Immunol 2004; 4: 553-564.
9. Levy O. Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol 2007; 7: 379-90.
10. Agarwal S, Rao A. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 1998; 9: 765-75.
11. Fields PE, Lee GR, Kim ST, Bartsevich VV and Flavell RA. Th2-specific chromatin remodeling and enhancer activity in the Th2 cytokine locus control region. Immunity 2004; 21: 865-76.
12. Lee DU, 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 U S A 2004; 101: 16010-5.
13. Takemoto N, Koyano-Nakagawa N, Yokota T, Arai N, Miyatake S and Arai K. Th2-specific DNase I-hypersensitive sites in the murine IL-13 and IL-4 intergenic region. Int Immunol 1998; 10: 1981-5.
14. Avni O, Lee D, Macian F, Szabo SJ, Glimcher LH and Rao A. T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat Immunol 2002; 3: 643-51.
15. Fields PE, Kim ST and Flavell RA. Cutting edge: changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation. J Immunol. 2002; 169:647-50.
16. Guo L, Hu-Li J, Zhu J, et al. In TH2 cells the Il4 gene has a series of accessibility states associated with distinctive probabilities of IL-4 production. Proc Natl Acad Sci U S A 2002; 99: 10623-8.
17. Lee DU, Agarwal S and Rao A. Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 2002; 16: 649-60.
18. Wilson CB, Merkenschlager M. Chromatin structure and gene regulation in T cell development and function. Curr Opin Immunol 2006; 18: 143-51.
19. Wilson CB, Makar KW, Shnyreva M and Fitzpatrick DR. DNA methylation and the expanding epigenetics of T cell lineage commitment. Semin Immunol 2005; 17: 105-19.
20. Lee GR, Kim ST, Spilianakis CG, Fields PE and Flavell RA. T helper cell differentiation: regulation by cis elements and epigenetics. Immunity 2006; 24:369-79.
21. Ansel KM, Djuretic I, Tanasa B and Rao A. Regulation of Th2 differentiation and I14 locus accessibility. Annu Rev Immunol 2006; 24: 607-56.
22. Adkins B, Ghanei A and Hamilton K. Developmental regulation of IL-4, IL-2, and IFN-gamma production by murine peripheral T lymphocytes. J Immunol 1993; 151: 6117-6126.
23. Adkins B, Hamilton K and Ghanei A. Upregulation of murine neonatal T helper cell function by accessory cell factors. J Immunol 1994; 153: 3378-3385.
24. Rose S, Lichtenheld M, Foote M and Adkins B. Murine neonatal CD4+ cells are poised for rapid Th2 effector-like function. J Immunol 2007; 178: 2667-2678.
25. Loots GG, Locksley RM, Blankespoor CK et al. Identification of a coordinate regulator of interleukins 4, 13, and 5 by crois-species sequence comparisons. Science 2000; 288: 136-40.
26. Adkins B, Guevara P and Rose S. Thymic and extrathymic contributions to T helper cell function in murine neonates. Heamatologica reports 2006; 2: 9-13.
27. White GP, Watt PM, Holt BJ and Holt PG. Differential patterns of methylation of the IFN-gamma promoter at CpG and non-CpG sites underlie differences in IFN-gamma gene expression between human neonatal and adult CD45RO- T cells. J Immunol 2002; 168: 2820-7.
28. Surh CD, Sprent J. Regulation of mature T cell homeostasis. Semin Immunol 2005; 17: 183-91.
29. Min B, Paul WE. Endogenous proliferation: burst-like CD4 T cell proliferation in lymphopenic settings. Semin Immunol 2005; 17: 201-7.
30. Min B, McHugh R, Sempowski GD, Mackall C, Foucras G and Paul WE. Neonates support lymphopenia-induced proliferation. Immunity 2003; 18: 131-40.
31. Schuler, T, Hammerling GJ and Arnold B. Cutting Edge: IL-7-dependent homeostatic proliferation of CD8+ T cells in neonatal mice allows the generation of long-lived natural memory T cells. J Immunol 2004; 172: 15-9.
32. Le Campion A, Bourgeois C, Lambolez F, et al. Naive T cells proliferate strongly in neonatal mice in response to self- peptide/ self-MHC complexes. Proc Natl Acad Sci USA 2002; 99: 4538-43.
33. Schonland SO, Zimmer JK, Lopez-Benitez CM, et al. Homeostatic control of T-cell generation in neonates. Blood 2003; 102: 1428-34.
34. Hassan J, Reen DJ. Human recent thymic emigrants-identification, expansion, and survival characteristics. J Immunol 2001; 167: 1970-6.
35. Hassan J, Reen DJ. IL-7 promotes the survival and maturation but not differentiation of human post-thymic CD4+ T cells. Eur J Immunol 1998; 28: 3057-65.
36. Fukui T, Katamura K, Abe N, et al. IL-7 induces proliferation, variable cytokine-producing ability and IL-2 responsiveness in naive CD4+ T-cells from human cord blood. Immunol Lett 1997; 59: 21-8.
37. Dardalhon V, Jaleco S, Kinet S, et al. IL-7 differentially regulates cell cycle progression and HIV- 1 -based vector infection in neonatal and adult CD4+ T cells. Proc Natl Acad Sci USA 2001; 98: 9277-82.
38. Swainson L, Kinet S, Mongellaz C, Sourisseau M, Henriques T and Taylor N. IL-7-induced proliferation of recent thymic emigrants requires activation of die PI3K pathway. Blood 2007; 109: 1034-42.
39. Jaleco S, Swainson L, Dardalhon V, Burjanadze M, Kinet S and Taylor N. Homeostasis of naive and memory CD4+ T cells: IL-2 and IL-7 differentially regulate the balance between proliferation and Fas-mediated apoptosis. J Immunol 2003; 171: 61-8.
40. Soares MV, Borthwick NJ, Maini MK, Janossy G, Salmon M and Akbar AN. IL-7-dependent extrathymic expansion of CD45RA+ T cells enables preservation of a naive repertoire. J Immunol 1998; 161: 5909-17.
41. Hassan J, Reen DJ. Human Recent Thymic Emigrants-Identification, Expansion, And Survival Characteristics. J Immunol 2001; 167: 1970-1976.
42. Mazmanian SK, Liu CH, Tzianabos AO and Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the bost immune system. Cell 2005; 122: 107-18.
43. Jotereau F, Heuze F, Salomon-Vie V and Gascan H. Cell kinetics in the fetal mouse thymus: precursor cell input, proliferation, and emigration. J Immunol 1987; 138: 1026-30.
44. Owen JJ, Ritter MA. Tissue interaction in the development of thymus lymphocytes. J Exp Med 1969; 129: 431-42.
45. Douagi II, Andre II, Ferraz JC and Cumano A. Characterization of T cell precursor activity in the murine fetal thymus: evidence for an input of T cell precursors between days 12 and 14 of gestation. Eur J Immunol 2000; 30: 2201-2210.
46. Foss DL, Donskoy E and Goldschneider I. The importation of hematogenous precursors by the thymus is a gated phenomenon in normal adult mice. J Exp Med 2001; 193: 365-74.
47. Porritt HE, Gordon K and Petrie HT. Kinetics of steady-state differentiation and mapping of intrathymic-signaling environments by stem cell transplantation in nonirradiated mice. J Exp Med 2003; 198: 957-62.
48. David-Fung ES, Yui MA, Morales M, et al. Progression of regulatory gene expression states in fetal and adult pro-T-cell development. Immunol Rev 2006; 209: 212-36.
49. + dendritic epidermal cells of adult mice from fetal thymic precursors. Nature 1990;, 344: 68-70.
50. Havran WL, Allison JP. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 1988; 335: 443-5.
51. Wang JH, Nichogiannopoulou A, Wu L, et al. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 1996; 5: 537-49.
52. Crompton T, Outram SV, Buckland J and Owen MJ. Distinct roles of the interleukin-7 receptor alpha chain in fetal and adult thymocyte development revealed by analysis of interleukin-7 receptor alpha-deficient mice. Eur J Immunol 1998; 28: 1859-66.
53. Schilham MW, Wilson A, Moerer P, Benaissa-Trouw BJ, Cumano A and Clevers HC. Critical involvement of Tef-1 in expansion of thymocytes. J Immunol 1998; 161: 3984-91.
54. Sano S, Takahama Y, Sugawara, T, et al. Stat3 in thymic epithelial cells is essential for postnatal maintenance of thymic architecture and thymocyte survival. Immunity 2001; 15: 261-73.
55. Arroyo AG, Yang JT, Rayburn H and Hynes RO. Differential requirements for alpha4 integrins during fetal and adult hematopoiesis. Cell 1996; 85: 997-1008.
56. Adkins B. Peripheral CD4(+) Lymphocytes Derived from Fetal versus Adult Thymic Precursors Differ Phenotypically and Functionally. J Immunol 2003; 171: 5157-64.
57. Malhotra I, Mungai P, Muchiri E, et al. Distinct Th1- and Th2- Type prenatal cytokine responses to Plasmodium falciparum erythrocyte invasion ligands. Infect Immun 2005; 73: 3462-70.
58. Metenou S. Suguitan AL, Jr., Long C, Leke RG and Taylor DW. Fetal Immune Responses to Plasmodium falciparum Antigens in a Malaria-Endemic Region of Cameroon. J Immunol 2007; 178: 2770-7.
59. Scollay RG, Butcher EC and Weissman IL. Thymus cell migration. Quantitative aspects of cellular traffic from the thymus to the periphery in mice. Eur J Immunol 1980; 10: 210.
60. Yu W, Nagaoka H, Jankovic M, et al. Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature 1999; 400: 682-7.
61. Boursalian TE, Golob J, Soper DM, Cooper CJ and Fink PJ. Continued maturation of thymic emigrants in the periphery. Nat Immunol 2004; 5: 418-25.
62. Ridge JP, Fuchs EJ and Matzinger P. Neonatal tolerance revisited: Turning on newborn T cells with dendritic cells. Science 1996; 271: 1723-1726.
63. Adkins B, Hamilton K. Freshly isolated, murine neonatal T cells produce IL-4 in response to anti-CD3 stimulation. J Immunol 1992; 149: 3448-3455.
64. - T helper lymphocytes requires post-thymic development. J Immunol 1991; 147: 851.
65. Bendelac A, Matzinger P, Seder RA, Paul WE and Schwartz RH. Activation events during thymic selection. J Exp Med 1992; 175: 731-742.
66. Clise-Dwyer K, Huston GE, Buck AL, Duso DK and Swain SL. Environmental and Intrinsic Factors Lead to Antigen Unresponsiveness in CD4+ Recent Thymic Emigrants from Aged Mice. J Immunol 2007; 178: 1321-31.
67. a mice. J Exp Med 1989; 169: 2149-2158.
68. Smith H, Chen I-M, Kubo R and Tung KSK. Neonatal thymectomy results in a repertoire enriched in T cells deleted in the adult thymus. Science 1989; 245: 749.
69. Zuklys S, Balciunaite G, Agarwal A, Fasler-Kan E, Palmer E and Hollander CA. Normal thymic architecture and negative selection are associated with Aire expression, the gene defective in the autoimmune-polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED). J Immunol 2000; 165: 1976-83.
70. Holt PG, Jones CA. The development of the immune system during pregnancy and early life. Allergy 2000; 55: 688-97.
71. Jones LA, Chin LT, Merriam GR, Nelson LM and Kruisbeck AM. Failure of clonal deletion in neonatally thymectomized mice: Tolerance is preserved through clonal energy. J Exp Med 1990; 172: 1277.
72. Kojima A, Prehn RT. Genetic susceptibility to post-thymectomy autoimmune diseases in mice. Immunogenetics 1981; 14: 15-27.
73. Andrea-Sanchez JL, Moreno de Alboran IM, Marcos MA, Sanchez-Movilla A, Martinez AC and Kroemer G. Interleukin 2 abrogates the nonresponsive state of T cells expressing a forbidden T cell receptor repertoire and induces autoimmune disease in neonatally thymectomized mice. J Exp Med 1991; 173: 1323.
74. Gallegos AM, Bevan MJ. Central tolerance: good but imperfect. Immunol Rev 2006; 209: 290-6.
75. Asano M, Toda M, Sakaguchi N and Sakaguchi S. Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 1996; 184: 387-96.
76. Hori S, Nomura T and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299: 1057-61.
77. Fontenot JD, Dooley JL, Farr AG and Rudensky AY. Developmental regulation of Foxp3 expression during ontogeny. J Exp Med 2005; 202: 901-6.
78. Jiang Q, Su H, Knudsen G, Helms W and Su L. Delayed functional maturation of natural regulatory T cells in the medulla of postnatal thymus: role of TSLP. BMC Immunol 2006; 7: 6.
79. Dujardin HC, Burlen-Defranoux O, Boucontet L, Vieira P, Cumano A and Bandeira A. Regulatory potential and control of Foxp3 expression in newborn CD4+ T cells. Proc Natl Acad Sci USA 2004; 101: 14473-8.
80. Michaelsson J, Mold JE, McCune JM and Nixon DF. Regulation of T cell responses in the developing human fetus. J Immunol 2006; 176: 5741-8.
81. Cupedo T, Nagasawa M, Weijer K, Blom B and Spits H. Development and activation of regulatory T cells in the human fetus. Eur J Immunol 2005; 35: 383-90.
82. Darrasse-Jeze G, Marodon G, Salomon BL, Catala M and Klatzmann D. Ontogeny of CD4+CD25+ regulatory/suppressor T cells in human fetuses. Blood 2005; 105: 4715-21.
83. Field EH, Matesic D, Rigby S, Fehr T, Rouse T and Gao Q. CD4+CD25+ regulatory cells in acquired MHC tolerance. Immunol Rev 2001; 182: 99-112.
84. Gregoire KE, Goldschneider I, Barton RW and Bollum FJ. Ontogeny of terminal deoxynucleotidyl transferase-positive cells in lymphohemopoietic tissues of rat and mouse. J Immunol 1979; 123: 1347.
85. Bogue M, Gilfillan S, Benoist C and Mathis D. Regulation of N-region diversity in antigen receptors through thymocyte differentiation and thymus ontogeny. Proc Natl Acad Sci USA 1992; 89: 11011-5.
86. Rothenberg E, Triglia D. Clonal proliferation unlinked to terminal deoxynucleotidyl transferase synthesis in thymocytes of young mice. J Immunol 1983; 130: 1627-33.
87. Bogue M, Candeias S, Benoist C and Mathis D. A special repertoire of alpha: beta T cells in neonatal mice. EMBO J 1991; 10: 3647-54.
88. Feeney AJ. Junctional sequences of fetal T cell receptor beta chains have few N regions. J Exp Med 1991; 174: 115-24.
89. Raaphorst FM, Kaijzel EL, van Tol MJ, Vossen JM and van den Elsen PJ. Non-random employment of V beta 6 and J beta gene elements and conserved amino acid usage profiles in CDR3 regions of human fetal and adult TCR beta chain rearrangements. Int Immunol 1994; 6: 1-9.
90. George JF, Jr., Schroeder HW, Jr. Developmental regulation of D beta reading frame and junctional diversity in T cell receptor-beta transcripts from human thymus. J Immunol 1992; 148: 1230-9.
91. Hall MA, Reid JL and Lanchbury JS. The distribution of human TCR junctional region lengths shifts with age in both CD4 and CD8 T cells. Int Immunol 1998; 10: 1407-19.
92. Schelonka RL, Raaphorst FM, Infante D, Kraig E, Teale JM and Infante AJ. T cell receptor repertoire diversity and clonal expansion in human neonates. Pediatr Res 1998; 43: 396-402.
93. Gilfillan S, Bachmann M, Trembleau S, et al. Efficient immune responses in mice lacking N-region diversity. Eur J Immunol 1995; 25: 3115-3122.
94. Gavin MA, Bevan MJ. Ircreased peptide promiscuity provides a rationale for the lack of N regions in the neonatal T cell repertoire. Immunity 1995; 3: 793-800.
95. Conde C, Weller S, Gilfillan S, Marcellin L, Martin T and Pasquali JL, Terminal deoxynucleotidyl transferase deficiency reduces the incidence of autoimmune nephritis in (New Zealand Black x New Zealand White)F1 mice. J Immunol 1998; 161: 7023-30.
96. Feeney AJ, Lawson BR, Kono DH and Theofilopoulos AN. Terminal deoxynucleotidyl transferase deficiency decreases autoimmune disease in MRL-Fas(lpr) mice. J Immunol 2001; 167: 3486-93.
97. Robey IF, Peterson M, Horwitz MS, et al. Terminal deoxynucleotidyltransferase deficiency decreases autoimmune disease in diabetes-prone nonobese diabetic mice and lupus-prone MRL-Fas(lpr) mice. J Immunol 2004; 172: 4624-9.