How regulatory CD25+CD4+T cells impinge on tumor immunobiology? On the existence of two alternative dynamical classes of tumors

Journal of Theoretical Biology

Volumn 247, Issue 1, 2007, Pages 122-137

  Leon, Kalet ^a,b   Garcia, Karina ^a   Carneiro, Jorge ^b   Lage, Agustin ^a  

^a CENTER OF MOLECULAR IMMUNOLOGY   (Cuba)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Mathematical modelling; Regulatory T cells; Tumor growth dynamics; Tumor immune system interaction; Tumor immunology

Indexed keywords

TUMOR ANTIGEN;

ANTIBODY; ANTIGEN; GROWTH RATE; IMMUNE SYSTEM; NUMERICAL MODEL; TUMOR;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL GROWTH; CELL INTERACTION; CELL MIGRATION; CELL STIMULATION; DYNAMICS; EFFECTOR CELL; GROWTH RATE; IMMUNOBIOLOGY; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; LYMPH NODE; MATHEMATICAL MODEL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STIMULATION; TUMOR CELL DESTRUCTION; TUMOR GROWTH; TUMOR IMMUNOLOGY;

ANIMALS; ANTIGEN-PRESENTING CELLS; CELL DIVISION; HUMANS; IMMUNITY, CELLULAR; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPH NODES; LYMPHOCYTES, TUMOR-INFILTRATING; MODELS, IMMUNOLOGICAL; NEOPLASM TRANSPLANTATION; NEOPLASMS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TUMOR CELLS, CULTURED;

EID: 34249024527     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2007.01.029     Document Type: Article

References (43)

1. Almeida A.R., Rocha B., Freitas A.A., and Tanchot C. Homeostasis of T cell numbers: from thymus production to peripheral compartmentalization and the indexation of regulatory T cells. Semin. Immunol. 17 (2005) 239-249
2. Baecher-Allan C., and Anderson D.E. Regulatory cells and human cancer. Semin. Cancer Biol. 16 (2006) 98-105
3. Baecher-Allan C., and Hafler D.A. Human regulatory T cells and their role in autoimmune disease. Immunol. Rev. 212 (2006) 203-216
4. Bharat A., Fields R.C., and Mohanakumar T. Regulatory T cell-mediated transplantation tolerance. Immunol. Res. 33 (2005) 195-212
5. Carneiro J., Leon K., Caramalho I., Van den Dool C., Gardner R., Oliveira V., Bergman M., Sepúlveda N., Paixão T., Faro J., et al. When three is not a crowd: a crossregulation model of the dynamics and repertoire selection of regulatory CD4T cells. Immunol. Rev. 216 (2007) 48-68
6. Cederbom L., Hall H., and Ivars F. CD4+CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur. J. Immunol. 30 (2000) 1538-1543
7. Coombes J.L., Robinson N.J., Maloy K.J., Uhlig H.H., and Powrie F. Regulatory T cells and intestinal homeostasis. Immunol. Rev. 204 (2005) 184-194
8. Curiel T.J., Coukos G., Zou L., Alvarez X., Cheng P., Mottram P., Evdemon-Hogan M., Conejo-Garcia J.R., Zhang L., and Burow M.etal. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10 (2004) 942-949
9. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., xTopalian S.L., Sherry R., Restifo N.P., and Hubicki A.M.etal. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298 (2002) 850-854
10. Edinger M., Hoffmann P., Ermann J., Drago K., Fathman C.G., Strober S., and Negrin R.S. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat. Med. 9 (2003) 1144-1150
11. Engelhorn M.E., Guevara-Patino J.A., Noffz G., Hooper A.T., Lou O., Gold J.S., Kappel B.J., and Houghton A.N. Autoimmunity and tumor immunity induced by immune responses to mutations in self. Nat. Med. 12 (2006) 198-206
12. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4 (2003) 330-336
13. Gogas H., Ioannovich J., Dafni U., Stavropoulou-Giokas C., Frangia K., Tsoutsos D., Panagiotou P., Polyzos A., Papadopoulos O., Stratigos A., Markopoulos C., Bafaloukos D., Pectasides D., Fountzilas G., and Kirkwood J.M. Prognostic significance of autoimmunity during treatment of melanoma with interferon. N. Engl. J. Med. 354 7 (2006) 709-718
14. Graca L., Thompson S., Lin C.Y., Adams E., Cobbold S.P., and Waldmann H. Both CD4(+)CD25(+) and CD4(+)CD25(-) regulatory cells mediate dominant transplantation tolerance. J. Immunol. 168 (2002) 5558-5565
15. Hontsu S., Yoneyama H., Ueha S., Terashima Y., Kitabatake M., Nakano A., Ito T., Kimura H., and Matsushima K. Visualization of naturally occurring Foxp3+ regulatory T cells in normal and tumor-bearing mice. Int. Immunopharmacol. 4 (2004) 1785-1793
16. Hori S., Carvalho T.L., and Demengeot J. CD25+CD4+ regulatory T cells suppress CD4+ T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur. J. Immunol. 32 (2002) 1282-1291
17. Hori S., Nomura T., and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 299 (2003) 1057-1061
18. Jones E., Dahm-Vicker M., Simon A.K., Green A., Powrie F., Cerundolo V., and Gallimore A. Depletion of CD25+ regulatory cells results in suppression of melanoma growth and induction of autoreactivity in mice. Cancer Immunol. 2 (2002) 1
19. Khattri R., Cox T., Yasayko S.A., and Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4 (2003) 337-342
20. Kono K., Kawaida H., Takahashi A., Sugai H., Mimura K., Miyagawa N., Omata H., and Fujii H. CD4(+)CD25high regulatory T cells increase with tumor stage in patients with gastric and esophageal cancers. Cancer Immunol. Immunother. 55 (2006) 1064-1071
21. Leon K. A Quantitative Approach to Dominant Tolerance (2002), PhD Thesis, University of Porto, Porto, Portugal
22. Leon K., Perez R., Lage A., and Carneiro J. Modelling T-cell-mediated suppression dependent on interactions in multicellular conjugates. J. Theor. Biol. 207 (2000) 231-254
23. Leon K., Perez R., Lage A., and Carneiro J. Three-cell interactions in T cell-mediated suppression? A mathematical analysis of its quantitative implications. J. Immunol. 166 (2001) 5356-5365
24. Leon K., Lage A., and Carneiro J. Tolerance and immunity in a mathematical model of T-cell mediated suppression. J. Theor. Biol. 225 (2003) 107-126
25. Li X., Ye D.F., Xie X., Chen H.Z., and Lu W.G. Proportion of CD4+CD25+ regulatory T cell is increased in the patients with ovarian carcinoma. Cancer Invest. 23 (2005) 399-403
26. Nair R.E., Kilinc M.O., Jones S.A., and Egilmez N.K. Chronic immune therapy induces a progressive increase in intratumoral T suppressor activity and a concurrent loss of tumor-specific CD8+ T effectors in her-2/neu transgenic mice bearing advanced spontaneous tumors. J. Immunol. 176 (2006) 7325-7334
27. Nishikawa H., Kato T., Tanida K., Hiasa A., Tawara I., Ikeda H., Ikarashi Y., Wakasugi H., Kronenberg M., Nakayama T., et al. CD4+ CD25+ T cells responding to serologically defined autoantigens suppress antitumor immune responses. Proc. Natl. Acad. Sci. USA 100 (2003) 10902-10906
28. Nishikawa H., Kato T., Tawara I., Saito K., Ikeda H., Kuribayashi K., Allen P.M., Schreiber R.D., Sakaguchi S., and Old L.J.etal. Definition of target antigens for naturally occurring CD4(+) CD25(+) regulatory T cells. J. Exp. Med. 201 (2005) 681-686
29. Nishikawa H., Kato T., Tawara I., Takemitsu T., Saito K., Wang L., Ikarashi Y., Wakasugi H., Nakayama T., Taniguchi M., et al. Accelerated chemically induced tumor development mediated by CD4+CD25+ regulatory T cells in wild-type hosts. Proc. Natl. Acad. Sci. USA 102 (2005) 9253-9257
30. Onizuka S., Tawara I., Shimizu J., Sakaguchi S., Fujita T., and Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res. 59 (1999) 3128-3133
31. Overwijk W.W., Lee D.S., Surman D.R., Irvine K.R., Touloukian C.E., Chan C.C., Carroll M.W., Moss B., Rosenberg S.A., and Restifo N.P. Vaccination with a recombinant vaccinia virus encoding a "self" antigen induces autoimmune vitiligo and tumor cell destruction in mice: requirement for CD4(+) T lymphocytes. Proc. Natl. Acad. Sci. USA 96 (1999) 2982-2987
32. Sakaguchi S., and Sakaguchi N. Regulatory T cells in immunologic self-tolerance and autoimmune disease. Int. Rev. Immunol. 24 (2005) 211-226
33. Shimizu J., Yamazaki S., and Sakaguchi S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J. Immunol. 163 (1999) 5211-5218
34. Suvas S., Azkur A.K., Kim B.S., Kumaraguru U., and Rouse B.T. CD4+CD25+ regulatory T cells control the severity of viral immunoinflammatory lesions. J. Immunol. 172 (2004) 4123-4132
35. Taams L.S., Boot E.P., van Eden W., and Wauben M.H. 'Anergic' T cells modulate the T-cell activating capacity of antigen-presenting cells. J. Autoimmun. 14 (2000) 335-341
36. Thornton A.M., and Shevach E.M. Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific. J. Immunol. 164 (2000) 183-190
37. Vendetti S., Chai J.G., Dyson J., Simpson E., Lombardi G., and Lechler R. Anergic T cells inhibit the antigen-presenting function of dendritic cells. J. Immunol. 165 (2000) 1175-1181
38. Wei W.Z., Jacob J.B., Zielinski J.F., Flynn J.C., Shim K.D., Alsharabi G., Giraldo A.A., and Kong Y.C. Concurrent induction of antitumor immunity and autoimmune thyroiditis in CD4+ CD25+ regulatory T cell-depleted mice. Cancer Res. 65 (2005) 8471-8478
39. Wolf D., Wolf A.M., Rumpold H., Fiegl H., Zeimet A.G., Muller-Holzner E., Deibl M., Gastl G., Gunsilius E., and Marth C. The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin. Cancer Res. 11 (2005) 8326-8331
40. Wolf D., Rumpold H., and Wolf A.M. Regulatory T cells in cancer biology: a possible new target for biochemical therapies. Mini Rev. Med. Chem. 6 (2006) 509-513
41. Woo E.Y., Yeh H., Chu C.S., Schlienger K., Carroll R.G., Riley J.L., Kaiser L.R., and June C.H. Cutting edge: regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J. Immunol. 168 (2002) 4272-4276
42. Yamaguchi T., and Sakaguchi S. Regulatory T cells in immune surveillance and treatment of cancer. Semin. Cancer Biol. 16 (2006) 115-123
43. Zhou G., Drake C.G., and Levitsky H.I. Amplification of tumor-specific regulatory T cells following therapeutic cancer vaccines. Blood 107 (2006) 628-636