Regulation of humoral immunity by FoxP3+ regulatory T cells

Expert Review of Clinical Immunology

Volumn 2, Issue 6, 2006, Pages 859-868

  Kim, Chang H ^a  

^a Purdue University   (United States)

Author keywords

Antibodies; B cells; Chemokine; FoxP3; Migration; Regulatory cells

Indexed keywords

EID: 34250749016     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2.6.859     Document Type: Review

References (120)

1. regs for immunologic self-tolerance and negative control of immune responses. Ann. Rev. Immunol. 22, 531-562 (2004). (Pubitemid 38680433)
2. regs. Semin. Immunol. 16, 89-98 (2004).
3. regs under scrutiny. Nat. Rev. Immunol. 3, 189-198 (2003).
4. regs. Nat. Rev. Immunol. 3, 253-257 (2003).
5. + suppressor T cells. Novartis Found. Symp. 252, 24-36; discussion 36-44, 106-114 (2003).
6. Rudensky A. Foxp3 and dominant tolerance. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360, 1645-1646 (2005). (Pubitemid 43997812)
7. regs. Curr. Opin. Pharmacol. 4, 408-414 (2004).
8. regs in transplantation tolerance. Nat. Rev. Immunol. 3, 199-210. (2003).
9. +CD25- T cells by in vitro Foxp3 gene transfer, can induce transplantation tolerance. Transplantation 79, 1310-1316(2005). (Pubitemid 40734792)
10. Jaeckel E, von Boehmer H, Manns MP. Antigen-specific FoxP3-transduced T-cells can control established type 1 diabetes. Diabetes 54, 306-310 (2005).
11. + T cells: a common basis between tumor immunity and autoimmunity. J. Immunol. 163, 5211-5218. (1999).
12. + T cells. Immunology 107, 5-9 (2002).
13. + T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficienrmice. Eur. J. Immunol. 32, 1282-1291 (2002). (Pubitemid 34546255)
14. rgs: friend or foe in immunity to infection? Nat. Rev. Immunol. 4, 841-855 (2004). (Pubitemid 39490760)
15. Baum J, Liebermann G. Frenkel EP. The effect of immunologically induced lymphopenia on antibody formation. J. Immunol. 102, 187-193 (1969).
16. Baker PJ, Barth RF, Stashak PW, Amsbaugh DF. Enhancement of the antibody response to type 3 pneumococcal polysaccharide in mice treated with antilymphocyte serum. J. Immunol. 104, 1313-1315 (1970).
17. Kerbel RS, Eidinger D. Variable effects of anti-lymphocyte serum on humoral antibody formation: role of thymus dependency of antigen. J. Immunol. 106, 917-926 (1971).
18. Katz DH. The allogeneic effect on immune responses: model for regulatory influences of T lymphocytes on the immune system. Transplant. Rev. 12, 141-179(1972).
19. Gershon, RK, Kondo K. Infectious immunological tolerance. Immunology 21, 903-914 (1971).
20. Katz DH, Benacerraf B. The regulatory influence of activated T cells on B cell responses to antigen. Adv. Immunol. 15, 1-94 (1972).
21. Okumura K, Herzenberg LA, Murphy DB, McDevitt HO. Selective expression of H-2 (i-region) loci controlling determinants on helper and suppressor T lymphocytes. J. Exp. Med. 144, 685-698 (1976).
22. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164. (1995).
23. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat. Immunol. 6, 338-344 (2005). (Pubitemid 41716770)
24. regs in immunological tolerance to self and non-self. Nat. Immunol. 6, 345-352 (2005). (Pubitemid 41716771)
25. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Sciencc 299, 1057-1061. (2003). (Pubitemid 36222930)
26. + T cell effector function. J. Immunol. 171, 1216-1223 (2003). (Pubitemid 36900050)
27. regs. Nat. Immunol. 4, 330-336 (2003). (Pubitemid 36432314)
28. Schubert LA, Jeffery E, Zhang Y, Ramsdell F, Ziegler SF. Scurfin (FOXP3) acts as a repressor of transcription and regulates T cell activation. J. Biol Chem. 276, 37672-37679 (2001).
29. Bettelli E, Dastrange M, Oukka M. Foxp3 interacts with nuclear factor of activated T cells and NF-κ B to repress cytokine gene expression and effector functions of T helper cells. Proc. Natl Acad. Sci. USA 102, 5138-5143 (2005).
30. Szabo SJ, Sullivan BM, Peng SL, Glimcher LH. Molecular mechanisms regulating Th1 immune responses. Ann. Rev. Immunol. 21, 713-758 (2003). (Pubitemid 37174546)
31. Kretschmer K, Apostolou I, Hawiger D, Khazaie K, Nussenzweig MC, von Boehmer H. Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. (2005).
32. +CD25-cells to develop suppressive activity: the role of IL-2, TGF-β, and IL-10. J. Immunol. 172, 5213-5221 (2004). (Pubitemid 38542018)
33. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192, 1213-1222 (2000).
34. reg by targeting of antigens to immature dendritic cells. Blood 101, 4862-4869 (2003). (Pubitemid 36857748)
35. reg in transplant tolerance. J. Immunol. 170, 1304-1312 (2003). (Pubitemid 36139497)
36. Verhasselt V, Vosters O, Beuneu C, Nicaise C, Stordeur P, Goldman M. Induction of FOXP3-expressing regulatory CD4pos T cells by human mature autologous dendritic cells. Eur. J. Immunol. 34, 762-772 (2004). (Pubitemid 39255924)
37. regs from human peripheral blood. J. Immunol. 166, 7282-7289 (2001). (Pubitemid 32525603)
38. +CD25-precursors. J. Immunol. 169, 4183-4189 (2002). (Pubitemid 35178188)
39. + precursors. Am. J. Transplant. 4, 1614-1627 (2004). (Pubitemid 39312295)
40. + precursors. J. Immunol. 175, 6107-6116 (2005). (Pubitemid 41508098)
41. + regulatory T cell compartment. J. Immunol. 173, 2227-2230 (2004). (Pubitemid 39063075)
42. reg induced by 1 α,25-dihydroxyvitamin D3 and mycophenolate mofetil treatment mediate transplantation tolerance. J. Immunol. 167, 1945-1953 (2001). (Pubitemid 32747499)
43. + T cells. J. Immunol. 175, 1483-1490 (2005). (Pubitemid 41023048)
44. regs. J. Immunol. 172, 5986-5993 (2004). (Pubitemid 38621199)
45. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor Foxp3. Immunity 22, 329-341 (2005). (Pubitemid 40387475)
46. regs. J. Immunol. 175, 4180-4183 (2005). (Pubitemid 41361949)
47. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 6, 331-337 (2005). (Pubitemid 41716769)
48. regs at the single-cell level. Eur. J. Immunol. 35, 1681-1691 (2005). (Pubitemid 40862316)
49. O'Garra A. Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8, 275-283 (1998). (Pubitemid 28188888)
50. regs is mediated by cell surface-bound transforming growth factor β. J. Exp. Med. 194, 629-644 (2001). (Pubitemid 32844773)
51. regs by oral. antigen administration. J. Immunol. 167, 4245-4253 (2001). (Pubitemid 32954298)
52. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389, 737-742 (1997). (Pubitemid 27458961)
53. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265, 1237-1240 (1994). (Pubitemid 24291983)
54. + Tr cells. Blood 105, 1162-1169 (2005). (Pubitemid 40170889)
55. Gray D, Bergthorsdottir S, van Essen D, Wykes M, Poudrier J, Siepmann K. Observations on memory B-cell development. Semin. Immunol. 9, 249-254. (1997). (Pubitemid 27331994)
56. Parker DC. T cell-dependent B cell activation. Ann. Rev. Immunol. 11, 331-360 (1993). (Pubitemid 23115011)
57. McHeyzer-Williams MG, McHeyzer-Williams LJ, Fanelli Panus J. Antigen-specific immunity. Th cell-dependent B cell responses. Immunol. Res. 22, 223-236 (2000). (Pubitemid 32382236)
58. Noelle RJ, Ledbetter JA, Aruffo A. CD40 and its ligand, an essential ligand-receptor pair for thymus-dependent B-cell activation. Immunol. Today 13, 431-433 (1992).
59. Lipsky PE, Attrep JF, Grammer AC, McIlraith MJ, Nishioka Y. Analysis of CD40-CD40 ligand interactions in the regulation of human B cell function. Ann. NY Acad. Sci. 815, 372-383 (1997). (Pubitemid 27309532)
60. Sharon R, McMaster PR, Kask AM, Owens JD, Paul WE. DNP-Lys-ficoll: a T-independent antigen which elicits both IgM and IgG anti-DNP antibody-secreting cells. J. Immunol. 114, 1585-1589 (1975).
61. McHeyzer-Williams LJ, Driver DJ, McHeyzer-Williams MG. Germinal center reaction. Curr. Opin. Hematol. 8, 52-59 (2001). (Pubitemid 32047663)
62. Wolniak KL, Shinall SM, Waldschmidt TJ The germinal center response. Crit. Rev. Immunol. 24, 39-65 (2004). (Pubitemid 39655011)
63. + germinal center-T cells are the major helpers for GC-B cells and induce class switch recombination. BMC Immunol 6, 3 (2005).
64. Kim C. Chemokines and their receptors in hematopoietic cell development and function. In: Chemokines, Chemokine Receptors, and Disease. Schwiebert L (Ed.), 115-142 (2005).
65. Kim CH. The greater chemotactic network for lymphocyte trafficking: chemokines and beyond. Curr. Opin. Hematol. 12, 298-304 (2005). (Pubitemid 41058394)
66. regs. J. Immunol. 177(2), 840-851 (2006). (Pubitemid 44036584)
67. +) human thymocytes. J. Exp. Med. 196, 379-387. (2002). (Pubitemid 34879113)
68. regs. J. Exp. Med. 194, 847-853. (2001). (Pubitemid 32983019)
69. + suppressor T cells. Eur. J. Immunol. 33, 1488-1496 (2003). (Pubitemid 36790409)
70. regs are numerically deficient in acute and chronic GvHD. Blood (2005).
71. regs can migrate to follicles upon T cell activation and suppress GC-Th cells and GC-Th cell-driven B cell responses. J. Clin. Invest. 114, 1640-1649 (2004). (Pubitemid 40385555)
72. Benner R, Meima F, van der Meulen GM, van Muiswinkel WB. Antibody formation in mouse bone marrow. I. Evidence for the development of plaque-forming cells in situ. Immunology 26, 247-255 (1974).
73. Chaperon EA, Seiner JC, Claman HN. Migration of antibody-forming cells and antigen-sensitive precursors between spleen, thymus and bone marrow. Immunology 14, 553-561 (1968).
74. O'Connor BP, Gleeson MW, Noelle RJ, Erickson LD. The rise and fall of long-lived humoral immunity: terminal differentiation of plasma cells in health and disease. Immunol. Rev. 194, 61-76 (2003). (Pubitemid 36886429)
75. Cyster JG. Homing of antibody secreting cells. Immunol. Rev. 194, 48-60 (2003). (Pubitemid 36886428)
76. Kunkel EJ, Butcher EC. Plasma-cell homing. Nat. Rev. Immunol. 3, 822-829 (2003). (Pubitemid 37328660)
77. Hargreaves DC, Hyman PL, Lu TT et al. A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194, 45-56 (2001). (Pubitemid 32660436)
78. Kunkel EJ, Campbell JJ, Haraldsen G et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J. Exp. Med 192, 761-768 (2000).
79. Bowman EP, Kuklin NA, Youngman KR et al. The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J. Exp. Med 195, 269-275 (2002). (Pubitemid 34461270)
80. Pan J, Kunkel EJ, Gosslar U et al. A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J. Immunol. 165, 2943-2949 (2000).
81. Kunkel EJ, Kim CH, Lazarus NH et al. CCR10 expression is a common feature of circulating and mucosal epithelial tissue IgA Ab-secreting cells. J. Clin. Invest. 111, 1001-1010 (2003). (Pubitemid 36397476)
82. regs that traffic through CXCL12/CXCR4 signals. Cancer Res. 64, 8451-8455 (2004). (Pubitemid 39491786)
83. Lee JH, Kang SG, Kim CH. FoxP3+ T cells undergo conventional first switch to lymphoid tissue homing receptors in thymus but accelerated second switch to non-lymphoid tissue homing receptors in secondary lymphoid tissues. J. Immunol. 178 (2007) (In Press).
84. Kim CH, Johnson R. Trafficking potentials of unconventional T cell subsets. Curr. Med. Chem. Anti Inflamm. Anti Allergy Agents, 321-330(2004). (Pubitemid 39549439)
85. regs control the magnitude of T-dependenc humoral immune responses to exogenous antigens. Eur. J. Immunol. 36, 855-863 (2006).
86. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4, 762-774 (2004). (Pubitemid 39336293)
87. regs. Eur. J. Immunol. 32, 2888-2896 (2002). (Pubitemid 35238182)
88. Grohmann, U, Orabona, C, Fallarino F et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3, 1097-1101 (2002). (Pubitemid 35363664)
89. Otterbein LE, Soares, MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trrends Immunol. 24, 449-455 (2003). (Pubitemid 36928103)
90. Sato K, Balla J, Otterbein L et al. Carbon mononoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J. Immunol. 166, 4185-4194 (2001). (Pubitemid 32224952)
91. Pae HO, Oh GS, Choi BM et al. Carbon monoxide produced by heme oxygenase-1 suppresses T cell proliferation via inhibition of 1L-2 production. J. Immunol. 172, 4744-4751 (2004).
92. Choi BM, Pae HO, Jeong YR, Kim YM, Chung HT. Critical role of heme tygenase-1 in Foxp3-mediated immune suppression. Biochem. Biophys. Res. Commun. 327, 1066-1071 (2005).
93. Grossman WJ, Verbsky JW, Barchet W, Colonna M, Atkinson JP, Ley TJ. Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity 21, 589-601 (2004). (Pubitemid 39370513)
94. + regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J. Immunol. 174, 1783-1786 (2005). (Pubitemid 40223916)
95. + T cells selectively kill B lymphocytes. Blood 107, 3925-3932 (2006). (Pubitemid 43726798)
96. + T cells and dendritic cells in vivo. J. Exp. Med. 203, 505-511 (2006).
97. Tang Q, Adams JY, Tooley AJ et al. Bluestone JA. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 7, 83-92 (2006). (Pubitemid 41823872)
98. Bystry RS, Aluvihare V, Welch KA, Kallikourdis M, Betz AG. B cells and professional APCs recruit T via CCL4. Nat. Immunol. 2, 1126-1132. (2001). (Pubitemid 33130146)
99. + naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int. Immunol. 10, 1969-1980. (1998). (Pubitemid 28566059)
100. Seo SJ, Fields ML, Buckler JL et al. The impact of T helper and T regulatory cells on the regulation of anti-double-stranded DNA B cells. Immunity 16, 535-546 (2002). (Pubitemid 34442578)
101. + regulatory T-cell population and autoantibody levels in paediatric patients with systemic lupus erythematosus. Immunology 117, 280-286 (2006).
102. + cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum 48, 1452-1460 (2003). (Pubitemid 36554546)
103. Russel W, Russel L, Gower J. Exceptional Inheritiance of a sex-linked gene in the mouse explained on the basis that the X/O sex-chromosome constitution is female. Proc. Natl Acad Sri. USA 45, 554-560 (1959).
104. Brunkow ME, Jeffery EW, Hjerrild KA et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27, 68-73 (2001). (Pubitemid 32044521)
105. Shull MM, Ormsby I, Kier AB et al. Targeted disruption of the mouse transforming growth factor-β 1 gene results in multifocal inflammatory disease. Nature 359, 693-699 (1992).
106. Waterhouse P, Penninger JM, Timms E et al. Lymphoproliferative disorders with early lethality in mice deficient in Cda-4. Science 270, 985-988 (1995).
107. Clark LB, Appleby MW, Brunkow ME, Wilkinson JE, Ziegler SF, Ramsdell F. Cellular and molecular characterization of the scurfy mouse mutant. J. Immunol. 162, 2546-2554 (1999). (Pubitemid 29309272)
108. Smyk-Pearson SK, Bakke AC, Held PK, Wildin RS. Rescue of the autoimmune scurry mouse by partial bone marrow transplantation or by injection with T-enriched splenocytes. Can. Exp. Immunol. 133, 193-199 (2003). (Pubitemid 36926288)
109. Schmidt-Weber CB, Blaser K. The role of the FOXP3 transcription factor in the immune regulation of allergic asthma. Curr. Allergy Asthma Rep. 5, 356-361 (2005). (Pubitemid 41683978)
110. regs inhibit the maturation but not the initiation of an autoantibody response. J. Immunol. 175, 4255-4264 (2005). (Pubitemid 41361959)
111. Oldstone MB. Molecular mimicry, microbial infection, and autoimmune disease: evolution of the concept. Curr. Top. Microbiol Immunol 296, 1-17 (2005). (Pubitemid 41667258)
112. Penninger JM, Bachmaier K. Review of microbial infections and the immune response to cardiac antigens. J. Infect. Dis. 181 (Suppl. 3), S498-S504 (2000). (Pubitemid 30416128)
113. Taylor MD, LcGoff L, Harris A, Malone E, Allen JE, Maizels RM. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 174, 4924-4933 (2005).
114. regs play no apparent role in the acute humoral response to intact Streptococcus pneumoniae. Infect. Immun. 73, 4427-4431 (2005). (Pubitemid 40923194)
115. regs selectively express Toll-like receptors and are activated by lipopoiysaccharide. J. Exp. Med. 197, 403-411(2003). (Pubitemid 36278597)
116. Netea MG, Sutmuller R, Hermann C et al. Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and T. J. Immunol. 172, 3712-3718 (2004). (Pubitemid 38337955)
117. + T regulatory cells. J. Immunol. 175, 8051-8059 (2005). (Pubitemid 41798367)
118. Yang Y, Huang CT, Huang X, Pardoll DM. Persistent Toll-like receptor signals are required for reversal of regulatory T cell-mediated CD8 tolerance. Nat. Immunol. 5, 508-515 (2004). (Pubitemid 38660463)
119. regs. J. Immunol. 172, 2778-2784 (2004). (Pubitemid 38263661)
120. regs through GITR breaks immunological self-tolerance. Nat. Immunol. 3, 135-142 (2002). (Pubitemid 34141443)