Signatures of human regulatory T cells: An encounter with old friends and new players

Genome Biology

Volumn 7, Issue 7, 2006, Pages

  Pfoertner, Susanne ^a   Jeron, Andreas ^a   Probst Kepper, Michael ^b   Guzman, Carlos A ^a   Hansen, Wiebke ^a   Westendorf, Astrid M ^a   Toepfer, Tanja ^a   Schrader, Andres J ^c   Franzke, Anke ^b   Buer, Jan ^a,b   Geffers, Robert ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c Fachbereich Medizin der Universitat Marburg   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR7; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; INTERLEUKIN 2 RECEPTOR ALPHA; PRIMER DNA;

ANIMAL CELL; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DONOR; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN GENOME; LYMPHOCYTE FUNCTION; MICROARRAY ANALYSIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; STATISTICAL ANALYSIS; UNINDEXED SEQUENCE; VALIDATION PROCESS; ADULT; APOPTOSIS; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL SEPARATION; CELL SURVIVAL; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; MALE; MIDDLE AGED; VALIDATION STUDY;

MURINAE;

ADULT; APOPTOSIS; AUTOIMMUNITY; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CELL SURVIVAL; DNA PRIMERS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNOPHENOTYPING; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MALE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 33747303831     PISSN: 1474760X     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2006-7-7-r54     Document Type: Article

References (103)

1. Sakaguchi S: Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005, 6:345-352.
2. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M: Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995, 155:1151-1164.
3. Fontenot JD, Gavin MA, Rudensky AY: Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003, 4:330-336.
4. Hori S, Nomura T, Sakaguchi S: Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
5. Khattri R, Cox T, Yasayko SA, Ramsdell F: An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 2003, 4:337-342.
6. Vigouroux S, Yvon E, Biagi E, Brenner MK: Antigen-induced regulatory T cells. Blood 2004, 104:26-33.
7. Bluestone JA, Abbas AK: Natural versus adaptive regulatory T cells. Nat Rev Immunol 2003, 3:253-257.
8. Shao L, Jacobs AR, Johnson VV, Mayer L: Activation of CD8+ regulatory T cells by human placental trophoblasts. J Immunol 2005, 174:7539-7547.
9. Wei S, Kryczek I, Zou L, Daniel B, Cheng P, Mottram P, Curiell T, Lange A, Zou W: Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res 2005, 65:5020-5026.
10. Barrat FJ, Cua DJ, Boonstra A, Richards DF, Crain C, Savelkoul HF, de Waal-Malefyt R, Coffman RL, Hawrylowicz CM, O'Garra A: In vitro generation of interleukin 10-producing regulatory CD4(+) T cells is induced by immunosuppressive drugs and inhibited by T helper type I (Th1)- and Th2-inducing cytokines. J Exp Med 2002, 195:603-616.
11. Thorstenson KM, Khoruts A: Generation of anergic and potentially immunoregulatory CD25+CD4 T cells in vivo after induction of peripheral tolerance with intravenous or oral antigen. J Immunol 2001, 167:188-195.
12. Read S, Malmstrom V, Powrie F: Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J Exp Med 2000, 192:295-302.
13. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S: Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002, 3:135-142.
14. Szanya V, Ermann J, Taylor C, Holness C, Fathman CG: The subpopulation of CD4+CD25+ splenocytes that delays adoptive transfer of diabetes expresses L-selectin and high levels of CCR7. J Immunol 2002, 169:2461-2465.
15. Roncador G, Brown PJ, Maestre L, Hue S, Martinez-Torrecuadrada JL, Ling KL, Pratap S, Toms C, Fox BC, Cerundolo V, et al.: Analysis of FOXP3 protein expression in human CD4(+)CD25(+) regulatory T cells at the single-cell level. Eur J Immunol 2005, 35:1681-1691.
16. Bruder D, Probst-Kepper M, Westendorf AM, Geffers R, Beissert S, Loser K, von Boehmer H, Buer J, Hansen W: Neuropilin-1: a surface marker of regulatory T cells. Eur J Immunol 2004, 34:623-630.
17. Ruprecht CR, Gattorno M, Ferlito F, Gregorio A, Martini A, Lanzavecchia A, Sallusto F: Coexpression of CD25 and CD27 identifies FoxP3+ regulatory T cells in inflamed synovia. J Exp Med 2005, 201:1793-1803.
18. Allan SE, Passerini L, Bacchetta R, Crellin N, Dai M, Orban PC, Ziegler SF, Roncarolo MG, Levings MK: The role of 2 FOXP3 isoforms in the generation of human CD4+ Tregs. J Clin Invest 2005, 115:3276-3284.
19. Lechner O, Lauber J, Franzke A, Sarukhan A, von BH, Buer J: Fingerprints of anergic T cells. Curr Biol 2001, 11:587-595.
20. Gavin MA, Clarke SR, Negrou E, Gallegos A, Rudensky A: Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat Immunol 2002, 3:33-41.
21. Ziegler SF: FOXP3: of mice and men. Annu Rev Immunol 2006, 24:209-26.
22. Bakay M, Chen YW, Borup R, Zhao P, Nagaraju K, Hoffman EP: Sources of variability and effect of experimental approach on expression profiling data interpretation. BMC Bioinformatics 2002, 3:4.
23. Unger MA, Rishi M, Clemmer VB, Hartman JL, Keiper EA, Greshock JD, Chodosh LA, Liebman MN, Weber BL: Characterization of adjacent breast tumors using oligonucleotide microarrays. Breast Cancer Res 2001, 3:336-341.
24. Park PJ, Cao YA, Lee SY, Kim J, Chang MS, Hart R, Choi S: Current issues for DNA microarrays: platform comparison, double linear amplification, and universal RNA reference. J Biotechnol 2004, 112:225-245.
25. Yuen T, Wurmbach E, Pfeffer RL, Ebersole BJ, Sealfon SC: Accuracy and calibration of commercial oligonucleotide and custom cDNA microarrays. Nucleic Acids Res 2002, 30:e48.
26. Hehlgans T, Pfeffer K: The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: players, rules and the games. Immunology 2005, 115:1-20.
27. Karin M, Greten FR: NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005, 5:749-759.
28. Haupt S, Berger M, Goldberg Z, Haupt Y: Apoptosis: the p53 network. J Cell Sci 2003, 116:4077-4085.
29. Schultz L, Khera S, Sleve D, Heath J, Chang NS: TIAF1 and p53 functionally interact in mediating apoptosis and silencing of TIAF1 abolishes nuclear translocation of serine 15-phosphorylated p53. DNA Cell Biol 2004, 23:67-74.
30. Tomasini R, Samir AA, Carrier A, Isnardon D, Cecchinelli B, Soddu S, Malissen B, Dagorn JC, Iovanna JL, Dusetti NJ: TP53INPIs and homeodomain-interacting protein kinase-2 (HIPK2) are partners in regulating p53 activity. J Biol Chem 2003, 278:37722-37729.
31. van der Leij J, van den Berg A, Albrecht EW, Blokzijl T, Roozendaall R, Gouw AS, de Jong KP, Stegeman CA, van Goor H, Chang NS, et al.: High expression of TIAF-1 in chronic kidney and liver allograft rejection and in activated T-helper cells. Transplantation 2003, 75:2076-2082.
32. Fernandez-Fernandez MR, Veprintsev DB, Fersht AR: Proteins of the S100 family regulate the oligomerization of p53 tumor suppressor. Proc Natl Acad Sci USA 2005, 102:4735-4740.
33. Daoud SS, Munson PJ, Reinhold W, Young L, Prabhu W, Yu Q, LaRose J, Kohn KW, Weinstein JN, Pommier Y: Impact of p53 knockout and topotecan treatment on gene expression profiles in human colon carcinoma cells: a pharmacogenomic study. Cancer Res 2003, 63:2782-2793.
34. Kho PS, Wang Z, Zhuang L, Li Y, Chew JL, Ng HH, Liu ET, Yu Q: p53-regulated transcriptional program associated with genotoxic stress-induced apoptosis. J Biol Chem 2004, 279:21183-21192.
35. Hamid T, Kakar SS: PTTG/securin activates expression of p53 and modulates its function. Mol Cancer 2004, 3:18.
36. Pei L: Identification of c-myc as a down-stream target for pituitary tumor-transforming gene. J Biol Chem 2001, 276:8484-8491.
37. Nishizaki M, Sasaki J, Fang B, Atkinson EN, Minna JD, Roth JA, Ji L: Synergistic tumor suppression by coexpression of FHIT and p53 coincides with FHIT-mediated MDM2 inactivation and p53 stabilization in human non-small cell lung cancer cells. Cancer Res 2004, 64:5745-5752.
38. Banz A, Pontoux C, Papiernik M: Modulation of Fas-dependent apoptosis: a dynamic process controlling both the persistence and death of CD4 regulatory T cells and effector T cells. J Immunol 2002, 169:750-757.
39. Chen X, Murakami T, Oppenheim JJ, Howard OM: Differential response of murine CD4+CD25+ and CD4+. Eur J Immunol 2004, 34:859-869.
40. Fritzsching B, Oberle N, Eberhardt N, Quick S, Haas J, Wildemann B, Krammer PH, Suri-Payer E: In contrast to effector T cells, CD4+CD25+FoxP3+ regulatory T cells are highly susceptible to CD95 ligand- but not to TCR-mediated cell death. J Immunol 2005, 175:32-36.
41. Wang X, Zheng J, Liu J, Yao J, He Y, Li X, Yu J, Yang J, Liu Z, Huang S: Increased population of CD4(+)CD25(high), regulatory T cells with their higher apoptotic and proliferating status in peripheral blood of acute myeloid leukemia patients. Eur J Haematol 2005, 75:468-476.
42. Demetriou M, Granovsky M, Quaggin S, Dennis JW: Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature 2001, 409:733-739.
43. Nakahara S, Oka N, Raz A: On the role of galectin-3 in cancer apoptosis. Apoptosis 2005, 10:267-275.
44. Akahani S, Nangia-Makker P, Inohara, H, Kim HR, Raz A: Galectin-3: a novel antiapoptotic molecule with a functional BHI (NWGR) domain of Bcl-2 family. Cancer Res 1997, 57:5272-5276.
45. Kim HR, Lin HM, Biliran H, Raz A: Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. Cancer Res 1999, 59:4148-4154.
46. Chung CD, Patel VP, Moran M, Lewis LA, Miceli MC: Galectin-1 induces partial TCR zeta-chain phosphorylation and antagonizes processive TCR signal transduction. J Immunol 2000, 165:3722-3729.
47. Rabinovich GA, Gruppi A: Galectins as immunoregulators during infectious processes: from microbial invasion to the resolution of the disease. Parasite Immunol 2005, 27:103-114.
48. Rabinovich GA, Ariel A, Hershkoviz R, Hirabayashi J, Kasai KI, Lider O: Specific inhibition of T-cell adhesion to extracellular matrix and proinflammatory cytokine secretion by human recombinant galectin-1. Immunology 1999, 97:100-106.
49. van der LJ, van den BA, Blokzijl T, Harms G, van GH, Zwiers P, van Weeghel R, Poppema S, Visser L: Dimeric galectin-1 induces IL-10 production in T-lymphocytes: an important tool in the regulation of the immune response. J Pathol 2004, 204:511-518.
50. Birebent B, Lorho R, Lechartier H, de Guibert S, Alizadeh M, Vu N, Vu N, Beauplet A, Robillard N, Semana G: Suppressive properties of human CD4+CD25+ regulatory T cells are dependent on CTLA-4 expression. Eur J Immunol 2004, 34:3485-3496.
51. Aspalter RM, Eibl MM, Wolf HM: Regulation of TCR-mediated T cell activation by TNF-R11. J Leukoc Biol 2003, 74:572-582.
52. Rainio EM, Sandholm J, Koskinen PJ: Cutting edge:Transcriptional activity of NFATcl is enhanced by the Pim-1 kinase. J Immunol 2002, 168:1524-1527.
53. Alvarez JD, Yasui DH, Niida H, Joh T, Loh DY, Kohwi-Shigematsu T: The MAR-binding protein SATBI orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev 2000, 14:521-535.
54. Ting CN, Olson MC, Barton KP, Leiden JM: Transcription factor GATA-3 is required for development of the T-cell lineage. Nature 1996, 384:474-478.
55. Lund R, Ahlfors H, Kainonen E, Lahesmaa AM, Dixon C, Lahesmaa R: Identification of genes involved in the initiation of human Th1 or Th2 cell commitment. Eur J Immunol 2005, 35:3307-3319.
56. Fry TJ, Mackall CL: Interleukin-7: master regulator of peripheral T-cell homeostasis? Trends Immunol 2001, 22:564-571.
57. Cozzo C, Larkin J III, Caton AJ: Cutting edge: self-peptides drive the peripheral expansion of CD4+CD25+ regulatory T cells. J Immunol 2003, 171:5678-5682.
58. Anderson MK, Hernandez-Hoyos G, Dionne CJ, Arias AM, Chen D, Rothenberg EV: Definition of regulatory network elements for T cell development by perturbation analysis with PU.1 and GATA-3. Dev Biol 2002, 246:103-121.
59. Rioux JD, Abbas AK: Paths to understanding the genetic basis of autoimmune disease. Nature 2005, 435:584-589.
60. Ehling R, Gassner C, Lutterotti A, Strasser-Fuchs S, Kollegger H, Kristoferitsch W, Reindl M, Berger T: Genetic variants in the tumor necrosis factor receptor II gene in patients with multiple sclerosis. Tissue Antigens 2004, 63:28-33.
61. Sashio H, Tamura K, Ito R, Yamamoto Y, Bamba H, Kosaka T, Fukui S, Sawada K, Fukuda Y, Tamura K, et al.: Polymorphisms of the TNF gene and the TNF receptor superfamily member 1B gene are associated with susceptibility to ulcerative colitis and Crohn's disease, respectively. Immunogenetics 2002, 53:1020-1027.
62. Morita C, Horiuchi T, Tsukamoto H, Hatta N, Kikuchi Y, Arinobu Y, Otsuka T, Sawabe T, Harashima S, Nagasawa K, et al.: Association of tumor necrosis factor receptor type II polymorphism 196R with systemic lupus erythematosus in the Japanese: molecular and functional analysis. Arthritis Rheum 2001, 44:2819-2827.
63. Held W, MacDonald HR, Weissman IL, Hess MW, Mueller C: Genes encoding tumor necrosis factor alpha and granzyme A are expressed during development of autoimmune diabetes. Proc Natl Acad Sci USA 1990, 87:2239-2243.
64. Jinchuan Y, Zonggui W, Jinming C, Li L, Xiantao K: Upregulation of CD40-CD40 ligand system in patients with diabetes mellitus. Clin Chim Acta 2004, 339:85-90.
65. Xu Y, Song G: The role of CD40-CD154 interaction in cell immunoregulation. J Biomed Sci 2004, 11:426-438.
66. Zalloua PA, Abchee A, Shbaklo H, Zreik TG, Terwedow H, Halaby G, Azar ST: Patients with early onset of type I diabetes have significantly higher GG genotype at position 49 of the CTLA4 gene. Hum Immunol 2004, 65:719-724.
67. Noble JA, White AM, Lazzeroni LC, Valdes AM, Mirel DB, Reynolds R, Grupe A, Aud D, Peltz G, Erlich HA: A polymorphism in the TCF7 gene, C883A, is associated with type I diabetes. Diabetes 2003, 52:1579-1582.
68. Todd JA, Wicker LS: Genetic protection from the inflammatory disease type I diabetes in humans and animal models. Immunity 2001, 15:387-395.
69. Harjacek M, az-Cano S, De MM, Wolfe H, Maldonado CA, Rabinovich GA: Expression of galectins-1 and -3 correlates with defective mononuclear cell apoptosis in patients with juvenile idiopathic arthritis. J Rheumatol 2001, 28:1914-1922.
70. Ohshima S, Kuchen S, Seemayer CA, Kyburz D, Hirt A, Klinzing S, Michel BA, Gay RE, Liu FT, Gay S, et al.: Galectin 3 and its binding protein in rheumatoid arthritis. Arthritis Rheum 2003, 48:2788-2795.
71. Tak PP, Spaeny-Dekking L, Kraan MC, Breedveld FC, Froelich CJ, Hack CE: The levels of soluble granzyme A and B are elevated in plasma and synovial fluid of patients with rheumatoid arthritis (RA). Clin Exp Immunol 1999, 116:366-370.
72. Masuda K, Masuda R, Neidhart M, Simmen BR, Michel BA, Muller-Ladner U, Gay RE, Gay S: Molecular profile of synovial fibroblasts in rheumatoid arthritis depends on the stage of proliferation. Arthritis Res 2002, 4:R8.
73. Garred P, Madsen HO, Petersen J, Marquart H, Hansen TM, Freiesleben Sorensen S, Volck B, Svejgaard A, Andersen V: CC chemokine receptor 5 polymorphism in rheumatoid arthritis. J Rheumatol 1998, 25:1462-1465.
74. Jawaheer D, Li W, Graham RR, Chen W, Damle A, Xiao X, Monteiro J, Khalili H, Lee A, Lundsten R, et al.: Dissecting the genetic complexity of the association between human leukocyte antigens and rheumatoid arthritis. Am J Hum Genet 2002, 71:585-594.
75. Finnegan A, Grusby MJ, Kaplan CD, O'Neill SK, Eibel H, Koreny T, Czipri M, Mikecz K, Zhang J: IL-4 and IL-12 regulate proteoglycan-induced arthritis through Stat-dependent mechanisms. J Immunol 2002, 169:3345-3352.
76. Boyton RJ, Davies S, Marden C, Fantino C, Reynolds C, Portugal K, Dewchand H, Altmann DM: Stat4-null non-obese diabetic mice: protection from diabetes and experimental allergic encephalomyelitis, but with concomitant epitope spread. Int Immunol 2005, 17:1157-1165.
77. Chitnis T, Najafian N, Benou C, Salama AD, Grusby MJ, Sayegh MH, Khoury SJ: Effect of targeted disruption of STAT4 and STAT6 on the induction of experimental autoimmune encephalomyelitis. J Clin Invest 2001, 108:739-747.
78. Amersham Biosciences: CodeLink Activated Slides: User Guide Amersham Biosciences, Freiburg, Germany; 2003.
79. Battaglia C, Salani G, Consolandi C, Bernardi LR, De BG: Analysis of DNA microarrays by non-destructive fluorescent staining using SYBR green II. Biotechniques 2000, 29:78-81.
80. Kane MD, Jatkoe TA, Stumpf CR, Lu J, Thomas JD, Madore SJ: Assessment of the sensitivity and specificity of oligonucleotide (50 mer) microarrays. Nucleic Acids Res 2000, 28:4552-4557.
81. GBF array website [http://www.gbf.de/array]
82. Eberwine J, Yeh H, Miyashiro K, Cao Y, Nair S, Finnell R, Zettel M, Coleman P: Analysis of gene expression in single live neurons. Proc Natl Acad Sci USA 1992, 89:3010-3014.
83. Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98:5116-5121.
84. Zelenika D, Adams E, Humm S, Graca L, Thompson S, Cobbold SP, Waldmann H: Regulatory T cells overexpress a subset of Th2 gene transcripts. J Immunol 2002, 168:1069-1079.
85. Sturn A, Quackenbush J, Trajanoski Z: Genesis: cluster analysis of microarray data. Bioinformatics 2002, 18:207-208.
86. Pati N, Schowinsky V, Kokanovic O, Magnuson V, Ghosh S: A comparison between SNaPshot, pyrosequencing, and biplex invader SNP genotyping methods: accuracy, cost, and throughput. J Biochem Biophys Methods 2004, 60:1-12.
87. Browning MB, Woodliff JE, Konkol MC, Pati NT, Ghosh S, Truitt RL, Johnson BD: The T cell activation marker CD150 can be used to identify alloantigen-activated CD4(+)25+ regulatory T cells. Cell Immunol 2004, 227:129-139.
88. Baecher-Allan C, Viglietta V, Hafler DA: Human CD4+CD25+ regulatory T cells. Semin Immunol 2004, 16:89-98.
89. Kohm AP, Williams JS, Miller SD: Cutting edge: ligation of the glucocorticoid-induced TNF receptor enhances autoreactive CD4+ T cell activation and experimental autoimmune encephalomyelitis. J Immunol 2004, 172:4686-4690.
90. Huehn J, Siegmund K, Lehmann JC, Siewert C, Haubold U, Feuerer M, Debes GF, Lauber J, Frey O, Przybylski GK, et al.: Developmental stage, phenotype, and migration distinguish naive- and effector/memory-likeCD4+ regulatory T cells. J Exp Med 2004, 199:303-313.
91. Walker LS: CD4+ CD25+ Treg: divide and rule? Immunology 2004, 111:129-137.
92. Piccirillo CA, Thornton AM: Cornerstone of peripheral tolerance: naturally occurring CD4+CD25+ regulatory T cells. Trends Immunol 2004, 25:374-380.
93. Fantini MC, Becker C, Monteleone G, Pallone F, Galle PR, Neurath MF: Cutting edge: TGF-beta induces a regulatory phenotype in CD4+. J Immunol 2004, 172:5149-5153.
94. Kasow KA, Chen X, Knowles J, Wichlan D, Handgretinger R, Riberdy JM: Human CD4+CD25+ regulatory T cells share equally complex and comparable repertoires with CD4+. J Immunol 2004, 172:6123-6128.
95. Buer J, Lanoue A, Franzke A, Garcia C, von BH, Sarukhan A: Interleukin 10 secretion and impaired effector function of major histocompatibility complex class II-restricted T cells anergized in vivo. J Exp Med 1998, 187:177-183.
96. McHugh RS, Whitters MJ, Piccirillo CA, Young DA, Shevach EM, Collins M, Byrne MC: CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002, 16:311-323.
97. Sakaguchi S: Control of immune responses by naturally arising CD4+ regulatory T cells that express toll-like receptors. J Exp Med 2003, 197:397-401.
98. Sakaguchi S, Sakaguchi N, Shimizu J, Yamazaki S, Sakihama T, Itoh M, Kuniyasu Y, Nomura T, Toda M, Takahashi T: Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 2001, 182:18-32.
99. Shevach EM: CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002, 2:389-400.
100. Stassen M, Fondel S, Bopp T, Richter C, Muller C, Kubach J, Becker C, Knop J, Enk AH, Schmitt S, et al.: Human CD25+ regulatory T cells: two subsets defined by the integrins alpha 4 beta 7 or alpha 4 beta 1 confer distinct suppressive properties upon CD4+ T helper cells. Eur J Immunol 2004, 34:1303-1311.
101. Cobbold SP, Nolan KF, Graca L, Castejon R, Le MA, Frewin M, Humm S, Adams E, Thompson S, Zelenika D, et al.: Regulatory T cells and dendritic cells in transplantation tolerance: molecular markers and mechanisms. Immunol Rev 2003, 196:109-124.
102. Kingsley CI, Karim M, Bushell AR, Wood KJ: CD25+CD4+ regulatory T cells prevent graft rejection: CTLA-4- and IL-10-dependent immunoregulation of alloresponses. J Immunol 2002, 168:1080-1086.
103. Gene Expression Omnibus [http://www.ncbi.nlm.nih.gov/projects/geo/]