The significance of Treg cells in defective tumor immunity

Archivum Immunologiae et Therapiae Experimentalis

Volumn 56, Issue 3, 2008, Pages 181-191

  Kosmaczewska, Agata ^a   Ciszak, Lidia ^a   Potoczek, Stanisław ^b   Frydecka, Irena ^a,b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b WROCLAW MEDICAL UNIVERSITY   (Poland)

Author keywords

FoxP3; Immunosuppression; Treg cells; Tumor immunity

Indexed keywords

CD45RB ANTIGEN; CYCLOOXYGENASE 2 INHIBITOR; CYCLOPHOSPHAMIDE; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FLUDARABINE; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TUMOR ANTIGEN;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL INTERACTION; CELL PROLIFERATION; CYTOKINE RELEASE; CYTOTOXICITY; EFFECTOR CELL; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; LOW DRUG DOSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; REVIEW; T CELL DEPLETION; T CELL LEUKEMIA; T CELL LYMPHOMA; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR IMMUNITY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYTOKINES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNE TOLERANCE; LIGANDS; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 45849099077     PISSN: 0004069X     EISSN: 16614917     Source Type: Journal    
DOI: 10.1007/s00005-008-0018-1     Document Type: Review

References (115)

1. Aharma S., Yang S. C., Zhu L., Reckamp K., Gardner B., Baratelli F., Huang M., Batra R. K. and Dubinett S. M. (2005): Tumor cyclooxygenase-2/ prostaglandin E2-dependent promotion of FOXP3 expression and CD4+CD25+ T regulatory cell activities in lung cancer. Cancer Res., 65, 5211-5220.
2. Albers A. E., Ferris R. L., Kim G. G., Chikamatsu K., Deleo A. B. and Whiteside T. L. (2005): Immune responses to p53 in patients with cancer: enrichment in tetramer+ p53 peptide-specific T cells and regulatory T cells at tumor sites. Cancer Immunol. Immunother., 54, 1072-1081.
3. Annacker O., Burlen-Defranoux O., Pimenta-Araujo R., Cumano A. and Bandeira A. (2000): Regulatory CD4 T cells control the size of the peripheral activated/memory CD4 T cell compartment. J. Immunol., 164, 3573-3580.
4. Annacker O., Pimenta-Araujo R., Burlen-Defranoux O., Barbosa T. C., Cumano A. and Bandeira A. (2001): CD25+CD4+ T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J. Immunol., 166, 3008-3018.
5. Annunziato F., Cosmi L., Liotta F., Lazzer E., Manetti R., Vanini V., Romagnani P., Maggi E. and Romagnani S. (2002): Phenotype, localization, and mechanism of suppression of CD4+CD25+ human thymocytes. J. Exp. Med., 196, 379-387.
6. Anthony P. A., Piccirillo C. A., Akpinarli A., Finkelstein S. E., Speiss P. J., Surman D. R., Palmer D. C., Chan C. C., Klebanoff C. A., Overwijk W. W., Rosenberg S. A. and Restifo N. P. (2005): CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol., 174, 2591-2601.
7. Asano M., Toda M., Sakaguchi N. and Sakaguchi S. (1996): Autoimmune disease as a consequence of developmental abnormality of a T cell population. J. Exp. Med., 184, 387-396.
8. Asseman C., Mauze S., Leach M. W., Coffman R. L. and Powrie F. (1999): An essential role for interleukin 10 in the function of regulatory T cells that inhibits intestinal inflammation. J. Exp. Med., 190, 995-1004.
9. Azuma T., Takahashi T., Kunisato A., Kitamura T. and Hirai H. (2003): Human CD4+CD25+ regulatory T cells suppress NKT cell functions. Cancer Res., 63, 4516-4520.
10. Baecher-Allan C., Brown J. A., Freeman G. J. and Hafler D. A. (2001): CD4+CD25high regulatory cells in human peripheral blood. J. Immunol., 167, 1245-1253.
11. Bennet C. L., Christi J., Ramsdell F., Brunkow M. E., Ferguson P. J., Whitesell L., Kelly T. E., Sausbury F. T., Chance P. F. and Ochs H. D. (2001): The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet., 27, 20-21.
12. Berger C. L., Tigelaar R., Cohen J., Mariwalla K., Trinh J. and Edelson R. L. (2005): Cutaneous T cell lymphoma: malignant proliferation of T regulatory cells. Blood, 105, 1640-1647.
13. Beyer M., Kochanek M., Darbi K., Popov A., Jensen M., Endl E., Knolle P. A., Thomas R. K., Von Bergwellt--Baildon M., Debey S., Hallek M. and Schultze J. L. (2005): Reduced frequencies and suppressive function of CD4+CD25high regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood, 106, 2018-2025.
14. Boitard C., Yasunami R., Dardenne M. and Bach J. F. (1989): T cell-mediated inhibition of the transfer of autoimmune diabetes in NOD mice. J. Exp. Med., 169, 1669-1680.
15. Brusko T. and Atkinson M. (2007): Treg in type 1 diabetes. Cell. Biochem. Biophys., 48, 165-175.
16. Chakraborty N. G., Chattopadhyay S., Mehrotra S., Chhabra A. and Mukherji B. (2004): Regulatory T cell response and tumor vaccine-induced cytotoxic T lymphocytes in human melanoma. Hum. Immunol., 65, 794-802.
17. Chang H.W., Chow Y.H., Chong P. and Sia C. (2007): The cross-regulatory relationship between human dendritic and regulatory T cells and its role in type 1 diabetes mellitus. Rev. Diabet. Stud., 4, 68-76.
18. Chattopadhyay S., Chakraborty N. G. and Mukherji B. (2005): Regulatory T cells and tumor immunity. Cancer Immunol. Immunother., 54, 1153-1161.
19. Chen M. L., Pittet M. J., Gorelik L., Flavell R. A., Weissleder R., Von Boehmer H. and Khazaie K. (2005): Regulatory T cells suppress tumor-specific CD8 T cell cytotoxity through TGF-beta signals in vivo. Proc. Natl. Acad. Sci. USA, 102, 419-424.
20. Chen W., Jin W., Herdegen N., Lei K. J., Li L., Morinos N., McGrady G. and Wahl S. M. (2003): Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med., 198, 1875-1886.
21. Chen W. and Wahl S. M. (2003): TGF-beta: the missing link in CD4+CD25+ regulatory T cell-mediated immunosuppression. Cytokine Growth Factor Rev., 14, 85-89.
22. Chen Y., Kuchroo V. K., Inobe J., Hafler D. A. and Weiner H. (1994): Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalitis. Science, 265, 1237-1240.
23. Cozzo C., Larkin J. III and Caton A. J. (2003): Cutting edge: self-peptides drive the peripheral expansion of CD4+CD25+ regulatory T cells. J. Immunol., 171, 5678-5682.
24. Curiel T. J., Coukos G., Zou L., Alvarez X., Cheng P., Mottram P., Evdemon-Hogan M., Conejo-Garcia J. R., Zhang L., Burow M., Zhu Y., Wei S., Kryczek I., Daniel B., Gordon A., Myers L., Lackner A., Disis M. L., Knutson K. L., Chen L. and Zou W. (2004): Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med., 10, 942-949.
25. Delong P., Carroll R. G., Henry A. C., Tanaka T., Ahmad S., Leibowitz M. S., Sterman D. H., June C. H., Albelda S. M. and Vonderheide R. H. (2005): Regulatory T cells and cytokines in malignant pleural effusions secondary to mesothelioma and carcinoma. Cancer Biol. Ther., 4, 342-346.
26. Den Haan J. M., Kraal G. and Bevan M. J. (2007): Lipopolysaccharide induces IL-10-producing regulatory CD4+ T cells that suppress the CD8+ T cell response. J. Immunol., 178, 5429-5433.
27. Dieckmann D., Plottner H., Berchtold S., Berger T. and Schuler G. (2001): Ex vivo isolation and characterization of CD4+CD25+ T cells with regulatory properties from human blood. J. Exp. Med., 193, 1303-1310.
28. Fontenot J. D., Gavin M. A. and Rudensky A. Y. (2003): Foxp3 programs the development and function of CD4+Cd25+ regulatory T cells. Nat. Immunol., 4, 330-336.
29. Fritzsching B., Oberle N., Eberhardt N., Quick S., Haas J., Willdemann B., Krammer P. H. and Suri-Payer E. (2005): Cutting edge: 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., 175, 32-36.
30. Fujimoto S., Greene M. and Dehon A. A. (1975): Immunosuppressor T cells in tumor bearing host. Immunol. Commun., 4, 201-217.
31. Furtado G. C., Curotto de Lafaille M. A., Kutchukhidze N. and Lafaille J. J. (2002): Interleukin 2 signalling is required for CD4+ regulatory T cell function. J. Exp. Med., 196, 851-857.
32. Gavin M. and Rudensky A. (2003): Control of immune homeostasis by naturally arising regulatory CD4+ T cells. Curr. Opin. Immunol., 15, 690-696.
33. Glimcher L. H., Longo D. L., Green I. and Schwartz R. H. (1981): Murine syngeneic mixed lymphocyte response. I. Target antigens are self Ia molecules. J. Exp. Med., 154, 1652-1670.
34. Gorelik L. and Flavell R. A. (2001): Immune-mediated eradication of tumors through the blockade of transforming growth factor-beta signalling in T cells. Nat. Med., 7, 1118-1122.
35. Gregori S., Bacchetta R., Passerini L., Levings M. K. and Roncarolo M. G. (2007): Isolation, expansion, and characterization of human natural and adaptive regulatory cells. Methods Mol. Biol., 380, 83-106.
36. Groux H., O'Garra A., Bigler M., Roueau M., Antonenko S., De Vries J. E. and Roncarolo M. G. (1997): A CD4+ T cell subset inhibits antigen-specific T cell responses and prevents colitis. Nature, 389, 737-742.
37. Ho W. Y., Yee C. and Greenberg P. D. (2002): Adoptive therapy with CD8+ T cells: it may get by with a little help from its friends. J. Clin. Invest., 110, 1415-1417.
38. Hori S., Nomura T. and Sakaguchi S. (2003): Control of regulatory T cell development by the transcription factor Foxp3. Science, 299, 1057-1061.
39. Houghton A. (1994): Cancer antigens: immune recognition of self and altered self. J. Exp. Med., 180, 14.
40. Ichihara F., Kono K., Takahashi A., Kawaida H., Sugai H. and Fuji H. (2003): Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers. Clin. Cancer Res., 9, 4404-4408.
41. Itoh M., Takahashi T., Sakaguchi N., Kuniyasu Y., Shimizu J., Otsuka F. and Sakaguchi S. (1999): Thymus and autoimmunity: production of CD25+CD4+ anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J. Immunol. 162, 5317-5326.
42. Jonuleit H., Schmitt E., Schuler G., Knop J. and Enk A. H. (2000): 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.
43. Jonuleit H., Schmitt E., Stassen M., Tuettenberg A., Knop J. and Enk A. H. (2001): Identification and functional characterization of human CD4+CD25+ T cells with regulatory properties isolated from peripheral blood. J. Exp. Med., 193, 1285-1294.
44. Jordan M. S., Boesreanu A., Red A. J., Petrone A. L., Holenbeck A. E., Lerman M. A., Naji A. and Caton A. J. (2001): Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol., 2, 301-306.
45. Karube K., Ohshima K., Tsuchiya T., Yamaguchi R. K., Suzumiya J., Utsunomiya A., Harada M. and Kikuchi M. (2004): Expression of FoxP3, a key molecule in CD4+CD25+ regulatory T cells, in adult T cell leukaemia/lymphoma cells. Br. J. Haematol., 126, 81-84.
46. Kawaida H., Kono K., Takahashi A., Sugai H., Mimura K., Miyagawa N., Omata H., Ooi A. and Fujii H. (2005): Distribution of CD4+CD25high regulatory T cells in tumor-draining lymph nodes in patients with gastric cancer. J. Surg. Res., 124, 151-157.
47. Khatri R., Cox T., Yasayko S. A. and Ramsdell F. (2003): An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol., 4, 337-342.
48. Kim J. D., Choi B. K., Bae J. S., Lee U. H., Han I. S., Lee H. W., Youn B. S., Vinay D. S. and Kwon B. S. (2003): Cloning and characterization of GITR ligand. Genes Immun., 4, 564-569.
49. Kono K., Kawaida H., Takahashi A., Sugai H., Mimura K., Miyagawa N., Omata H. and Fujii H. (2006): CD4+CD25high regulatory T cells increase with tumor stage in patients with gastric and esophageal cancers. Cancer Immunol. Immunother., 55, 1064-1071.
50. Kudo-Saito C., Schlom J., Camphausen K., Coleman C. N. and Hodge J. W. (2005): The requirement of multimodal therapy (vaccine, local tumor radiation, and reduction of suppressor cells) to eliminate established tumors. Clin. Cancer Res., 11, 4533-4544.
51. Kuniyasu Y., Takahashi T., Itoh M., Shimizu J., Toda G. and Sakaguchi S. (2000): Naturally anergic and suppressive CD25+CD4+ T cells as a functionally and phenotypically distinct immunoregulatory T cell subpopulation. Int. Immunol., 12, 1145-1155.
52. loCD4+ T cells. J. Immunol., 144, 3288-3295.
53. Lethe B., Lucas S., Michaux L., De Smet C., Godeline D., Serrano A., De Plaen E. and Boon T. (1998): LAGE-1, a new gene with tumor specificity. Int. J. Cancer, 76, 903-908.
54. Levings M. K., Sangregorio R. and Roncarolo M. G. (2001): Human CD25+CD4+ T regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J. Ex. Med., 193, 1295-1301.
55. Levings M. K., Sangregorio R., Sartirana C., Moschin A. L., Battaglia M., Orban P. C. and Roncarolo M. G. (2002): Human CD25+CD4+ T suppressor cell clones produce transforming growth factor beta, but not interleukin 10, and are distinct from type 1 T regulatory cells. J. Exp. Med., 196, 1335-1346.
56. Li B., Samanta A., Song X., Iacono K. T., Brennan P., Chatila T. A., Roncador G., Banham A. H., Riley J. L., Wang Q., Shen Y., Saouaf S. J. and Greene M. I. (2007): FOXP3 is a homo-oligomer and a component of a supramolecular regulatory complex disabled in the human XLAAD/IPEX autoimmune disease. Int. Immunol., 19, 825-835.
57. Li Z., Mahesh S. P., Kim B. J., Buggage R. R. and Nussenblat R. B. (2003): Expression of glucocorticoid-induced TNF receptor family related protein (GITR) on peripheral T cells from normal human donors and patients with non-infectious uveitis. J. Autoimmunol., 21, 83-92.
58. Liyanage U. D., Moore T. T., Joo H-G., Tanaka Y., Herrmann V., Doherty G., Drebin J. A., Strasberg S. M., Eberlein T. J., Goedegebuure P. S. and Linehan D. C. (2002): Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol., 169, 2756-2761.
59. Loeffler M., Kruger J. A. and Reisfeld R. A. (2005): Immunostimulatory effect of low-dose cyclophosphamide are controlled by inducible nitric oxide synthase. Cancer Res., 65, 5027-5030.
60. Lutisiak C., Semnani R. T., De Pascalis R., Kashmiri S. V., Scholm J. and Sabzevari H. (2005): Inhibition of CD4+CD25+ T regulatory cell function implicated in enhanced immune response by low dose cyclophosphamide. Blood, 105, 2862-2868.
61. Mc Hugh R. S., Whitters M. J., Piccirillo C. A., Young D. A., Shevach E. M., Collins M. and Byrne M. C. (2002): CD4+CD25+ immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity, 16, 311-323.
62. Mohamood A. S., Trujillo C. J., Zheng D., Jie C., Murillo F. M., Schneck J. P. and Hamad A. R. (2006): Gld mutation of Fas ligand increases the frequency and up-regulates cell survival genes in CD25+CD4+ TR cells. Int. Immunol., 18, 1265-1277.
63. Murakami M., Sakamoto A., Bender J., Kappler J. and Marrack P. (2002): CD25+CD4+ T cells contribute to the control of memory CD8+ T cells. Proc. Natl. Acad. Sci. USA, 99, 8832-8837.
64. Nagai H., Horikawa T., Hara I., Fukunaga A., Oniki S., Oka M., Nishigori C. and Ichhashi M. (2004): In vivo elimination of CD25+ regulatory T cells leads to tumor rejection of B16F10 melanoma, when combined with interleukin-12 gene transfer. Exp. Dermatol., 13, 613-620.
65. Nakamura K., Kitani A. and Strober W. (2001): Cell contact-dependent immunosuppression by CD4+CD25+ regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J. Exp. Med., 194, 629-644.
66. Ng W. F., Duggan P. J., Ponchel F., Matarese G., Lombardi G., Edwards A. D., Isaacs J., D. and Lechler R. I. (2001): Human CD4+CD25+ cells: a naturally occurring population of regulatory T cells. Blood, 98, 2736-2744.
67. Nishikawa H., Jager E., Ritter G., Old L. J. and Gnajatic S. (2005): CD4+CD25+ regulatory T cells control the induction of antigen-specific CD4+ helper T cell responses in cancer patients. Blood, 106, 1008-1011.
68. Nishikawa H., Kato T., Tanida K., Hiasa A., Tawara I., Ikeda H., Ikarashi Y., Wakasugi H., Kronenberg M., Nakayama T., Taniguchi M., Kuribayashi K., Old L. J. and Shiku H. (2003): CD4+CD25+ T cells responding to serologically defined autoantigens suppress antitumor immune response. Proc. Natl. Acad. Sci. USA, 100, 10902-10906.
69. Oldenhove G., De Heusch M., Urbain-Vansanten G., CD4+CD25+ regulatory T cells control T helper cell type 1 responses to foreign antigens induced by mature dendritic cells in vivo. J. Exp. Med., 198, 259-266.
70. Ormandy L. A., Hillemann T., Wedemeyer H., Manns M. P., Graten T. F. and Korangy F. (2005): Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma. Cancer Res., 65, 2457-2464.
71. Piccirillo C. A., Letterio J. J., Thornton A. M., Mc Hugh R. S., Mamura M., Mizuhara H. and Shevach E. M. (2002): CD4+CD25+ regulatory T cells can mediate suppressor function in the absence of transforming growth factor beta1 production and responsiveness. J. Exp. Med., 196, 237-245.
72. Piccirillo C. A. and Shevach E. M. (2001): Control of CD8+ T cell activation by CD4+CD25+ immunoregulatory cells. J. Immunol., 167, 1137-1140.
73. Read S., Malmstrom V and Powrie F. (2000): 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., 192, 295-302.
74. Ronchetti S., Nocentini G., Riccardi C. and Pandolfi P. P. (2002): Role of GITR in activation response of T lymphocytes. Blood, 100, 350-352.
75. Rook A. H. and Heald P. (1995): The immunopathogenesis of cutaneous T cell lymphoma. Hematol. Oncol. Clin. North Am., 9, 997-1010.
76. Rosenberg S. A. and White D. E. (1996): Vitiligo in patients with melanoma: normal tissue antigens can be targets for cancer immunotherapy. J. Immunother., 19, 81-84.
77. Sakaguchi S., Sakaguchi N., Asano M., Itoh M. and Toda M. (1995): Immunologic 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., 155, 1151-1164.
78. Sasada T., Kimura M., Yoshida Y., Kanai M. and Takabahashi A. (2003): CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer, 98, 1089-1099.
79. Schaeffer C., Kim G. G., Albers A., Hoermann K., Myers E. N. and Whiteside T. L. (2005): Characteristics of CD4+CD25+ regulatory T cells in the peripheral circulation of patients with head and neck cancer. Br. J. Cancer, 92, 913-920.
80. Schubert L. A., Jeffery E., Zhang Y., Ramsdell F. and Ziegler S. F. (2001): Scurfin (FOXP3) acts as a repressor of transcription and regulates T cell activation. J. Biol. Chem., 276, 37672-37679.
81. Schwartz R. H. (1990): A cell culture model for T lymphocyte clonal anergy. Science, 248, 1349-1356.
82. Seddon B. and Mason D. (1999): Peripheral autoantigen induces regulatory T cells that prevent autoimmunity. J. Exp. Med., 189, 877-882.
83. Shafer-Weaver K., Anderson M., Malyguine A. and Hurwitz A. A. (2007): T cell tolerance to tumors and cancer immunotherapy. Adv. Exp. Med. Biol., 601, 357-368.
84. Shimizu J., Yamazaki S. and Sakaguchi S. (1999): Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J. Immunol., 163, 5211-5218.
85. Shimizu J., Yamazaki S., Takahashi T., Ishida Y. and Sakaguchi S. (2002): Stimulation of CD25+CD4+ regula-tory T cells through GITR breaks immunological self-tolerance. Nat. Immunol., 3, 135-142.
86. Silvia S. C., Togbe D., Couillin I., Mercier I., Brombacher F., Quesniaux V., Fossiez F., Ryffel B. and Schnyder B. (2006): Interleukin 17 is a negative regulator of established allergic asthma. J. Ex. Med., 203, 2715-2725.
87. Somasundaram R., Jacob L., Swoboda R., Caputo L., Song H., Basak S., Monos D., Peritt D., Marincola F., Cai D., Birebent B., Bloome E., Kim J., Berencsi K, Mastrangelo M. and Herlyn D. (2002): Inhibition of cytolytic T lymphocyte proliferation by autologous CD4+/CD25+ regulatory T cells in a colorectal carcinoma patient is mediated by transforming growth factor-beta1. Cancer Res., 62, 5267-5272.
88. Suri-Payer E., Amar A. Z., Thornton A. M. and Shevach E. M. (1998): CD4+CD25+ T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J. Immunol., 160, 1212-1218.
89. Sutmuller R. P., Van Duivenvoorde L. M., Van Elsas A., Schumacher T. N., Wildenberg M. E., Allison J. P., Toes R. E., Offringa R. and Melief C. J. (2001): Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25+ regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J. Exp. Med., 194, 823-832.
90. Taams L. S., Vukmanovic-Stejic M., Smith J., Dunne P. J., Fletcher J. M., Plunkett F. J., Ebelings S. B., Lombardi G., Rustin M. H., Bijlsma J. W., Lafeber F. P., Salmon M. and Akbar A. N. (2002): Antigen-specific T cell suppression by human CD4+CD25+ regulatory T cells. Eur. J. Immunol., 32, 1621-1630.
91. Takahashi T., Tagami T., Yamazaki S., Uede T., Shimizu J., Sakaguchi N., Mak T. W. and Sakaguchi S. (2000): Immunologic self-tolerance maintained by CD25+CD4+ regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med., 192, 303-309.
92. Tanchot C., Lemonnier F. A., Perarnau B., Freitas A. A. and Rocha B. (1997): Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science, 276, 2057-2062.
93. Thornton A. M. and Shevach E. M. (1998): CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med., 188, 287-296.
94. Thornton A. M. and Shevach E. M. (2000): Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific. J. Immunol., 164, 183-190.
95. Tommasini A., Ferrari S., Moratto D., Badolato R., Boniotto M., Pirulli D., Notarangelo L. D. and Andolina M. (2002): X-chromosome inactivation analysis in a female carrier of FOXP3 mutation. Clin. Exp. Immunol., 130, 127-130.
96. Tone M., Tone Y., Adams E., Yates S. F., Frewin M. R., Cobbold S. P. and Waldmann H. (2003): Mouse glucocorticoid-induced tumor necrosis factor receptor ligand is costimulatory for T cells. Proc. Natl. Acad. Sci. USA, 100, 15292-15293.
97. Uruashihawa K., Kanai T., Ko K., Totsuka T., Makita S., Iiyama R., Nakamura T. and Watanabe M. (2003): Regulation of murine inflammatory bowel disease by CD25+ and CD25- CD4+ glucocorticoid-induced TNF receptor family-related gene+ regulatory T cells. J. Immunol., 171, 708-716.
98. Van Belle P., Rodeck U., Nuamah I., Halpern A. C. and Elder D. E. (1996): Melanoma-associated expression of transforming growth factor-beta isoforms. Am. J. Pathol., 148, 1887-1894.
99. Viguier M., Lamaitre F., Verola O., Cho M. S., Gorochov G., Dubertret L., Bachelez H., Kourilsky P. and Ferradini L. (2004): FoxP3 expressing CD4+CD25high regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibits the function of infiltrating T cells. J. Immunol., 173, 1444-1453
100. Waldmann T. A. (1991): The interleukin-2 receptor. J. Biol. Chem., 266, 2681-2684.
101. Walker L. S., Chodos A., Eggena M., Dooms H. and Abbas A. K. (2003): Antigen-dependent proliferation of CD4+CD25+ regulatory T cells in vivo. J. Exp. Med., 198, 249-258.
102. Walker M. R., Kasprowicz D. J., Gersuk V. H., Benard A., Van Landeghen M., Buckner J. H. and Ziegler S. F. (2003): Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J. Clin. Invest., 112, 1437-1443.
103. Wallace V. A., Fung-Leung W. P., Timms E., Gray D., Kishihara K., Loh D. Y., Penninger J. and Mak T. W. (1992): CD45RA and CD45Rbhigh expression induced by thymic selection events. J. Exp. Med., 176, 1657-1663.
104. Wang H. Y., Lee D. A., Peng G., Guo Z., Li Y., Kiniwa Y., Shevach E. M. and Wang R. F. (2004): Tumor-specific human CD4+ regulatory T cells and their ligands. Implications for immunotherapy. Immunity, 20, 107-118.
105. Wi W. Z., Morris G. P. and Kong Y. C. (2004): Anti-tumor immunity and autoimmunity: a balancing act of regulatory T cells. Cancer Immunol. Immunother., 53, 73-78.
106. Wolf A. M., Wolf D., Steurer M., Gastl G., Gunsilius E. and Grubeck-Loebenstein B. (2003): Increase of regulatory T cells in the peripheral blood of cancer patients. Clin. Cancer Res., 9, 606-612.
107. Woo E. Y., Chu C. S., Goletz T. J., Schlienger K., Yeh H., Coukos G., Rubin S. C., Kaiser L. R. and June C. H. (2001): Regulatory CD4+CD25+ T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res., 61, 4766-4772.
108. Woo E. Y., Yeh H., Chu C. S., Schlienger K., Carroll R. G., Riley J. L., Kaiser L. R. and June C. H. (2002): Regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J. Immunol., 168, 4272-4276.
109. Xu L., Kitani A., Fuss I. and Strober W. (2007): Regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J. Immunol., 178, 6725-6729.
110. Yamagiwa S., Gray J. D., Hashimoto S. and Horwitz D. A. (2001): A role for TGF-beta in the generation and expansion of CD4+CD25+ regulatory T cells from human peripheral blood. J. Immunol., 166, 7282-7289.
111. Yu K. Y., Kim H. S., Song S. Y., Min S. S., Jeong J. J. and Youn B. S. (2003): Identification of a ligand for glucocorticoid-induced tumor necrosis factor receptor constitutively expressed in dendritic cells. Biochem. Biophys. Res. Commun., 310, 433-438.
112. Yu P., Lee Y., Liu W., Krausz T., Chong A., Schreiber H. and Fu Y-X. (2005): Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J. Exp. Med., 201, 779-791.
113. Zheng S. G., Gray J. D., Ohtsuka K., Yamagiwa S. and Horwitz D. A. (2002): Generation ex vivo of TGF-beta-producing regulatory T cells from CD4+CD25- precursors. J. Immunol., 169, 4183-4189.
114. Zheng S. G., Wang J. H., Stohl W., Kim K. S., Gray J. D. and Horwitz D. A. (2006): TGF-beta requires CTLA-4 early after T cell activation to induce FoxP3 and generate adaptive CD4+CD25+ regulatory cells. J. Immunol., 176, 3321-3329.
115. Zheng S. G., Wang J., Wang P., Gray J. D. and Horwitz D. A. (2007): IL-2 is essential for TGF-beta to convert naive CD4+CD25- cells to CD25+FoxP3+ regulatory T cells and for expansion of these cells. J. Immunol., 178, 2018-2027.