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Conversion of Peripheral CD4⁺CD25^- Naive T Cells to CD4⁺CD25⁺ Regulatory T Cells by TGF-ß Induction of Transcription Factor Foxp3

WanJun Chen, Wenwen Jin, Neil Hardegen, Ke-jian Lei, Li Li, Nancy Marinos, George McGrady and Sharon M. Wahl

Cellular Immunology Section, Oral Infection and Immunity Branch, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892

Address correspondence to WanJun Chen, Cellular Immunology Section, Oral Infection and Immunity Branch, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, MD 20892. Phone: (301) 435-7168; Fax: (301) 402-1064; email: wchen{at}dir.nidcr.nih.gov; or Sharon M. Wahl. Phone: (301) 496-4178; email: smwahl{at}dir.nidcr.nih.gov

CD4⁺CD25⁺ regulatory T cells (T_reg) are instrumental in the maintenance of immunological tolerance. One critical question is whether T_reg can only be generated in the thymus or can differentiate from peripheral CD4⁺CD25^- naive T cells. In this paper, we present novel evidence that conversion of naive peripheral CD4⁺CD25^- T cells into anergic/suppressor cells that are CD25⁺, CD45RB^-/low and intracellular CTLA-4⁺ can be achieved through costimulation with T cell receptors (TCRs) and transforming growth factor ß (TGF-ß). Although transcription factor Foxp3 has been shown recently to be associated with the development of T_reg, the physiological inducers for Foxp3 gene expression remain a mystery. TGF-ß induced Foxp3 gene expression in TCR-challenged CD4⁺CD25^- naive T cells, which mediated their transition toward a regulatory T cell phenotype with potent immunosuppressive potential. These converted anergic/suppressor cells are not only unresponsive to TCR stimulation and produce neither T helper cell 1 nor T helper cell 2 cytokines but they also express TGF-ß and inhibit normal T cell proliferation in vitro. More importantly, in an ovalbumin peptide TCR transgenic adoptive transfer model, TGF-ß–converted transgenic CD4⁺CD25⁺ suppressor cells proliferated in response to immunization and inhibited antigen-specific naive CD4⁺ T cell expansion in vivo. Finally, in a murine asthma model, coadministration of these TGF-ß–induced suppressor T cells prevented house dust mite–induced allergic pathogenesis in lungs.

Key Words: anergy • IL-10 • OVA TCR transgenic • house dust mite • asthma

Abbreviations used in this paper: 7-AAD, 7-amino-actinomycin D; CFSE, carboxy-fluorescein diacetate succinimidyl ester; HDM, house dust mite; HPRT, hypoxanthineguanine phosphoribosyl transferase; PAS, periodic acid schiff; P-Smad2/3, phosphorylated Smad2/3; T_reg, CD4⁺CD25⁺ regulatory T cells.

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• Wilde, B., Dolff, S., Cai, X., Specker, C., Becker, J., Totsch, M., Costabel, U., Durig, J., Kribben, A., Tervaert, J. W. C., Schmid, K. W., Witzke, O. (2009). CD4+CD25+ T-cell populations expressing CD134 and GITR are associated with disease activity in patients with Wegener's granulomatosis. Nephrol Dial Transplant 24: 161-171 [Abstract] [Full Text]  
• Lal, G., Zhang, N., van der Touw, W., Ding, Y., Ju, W., Bottinger, E. P., Reid, St. P., Levy, D. E., Bromberg, J. S. (2009). Epigenetic Regulation of Foxp3 Expression in Regulatory T Cells by DNA Methylation. J. Immunol. 182: 259-273 [Abstract] [Full Text]  
• Di Nicola, M., Zappasodi, R., Carlo-Stella, C., Mortarini, R., Pupa, S. M., Magni, M., Devizzi, L., Matteucci, P., Baldassari, P., Ravagnani, F., Cabras, A., Anichini, A., Gianni, A. M. (2009). Vaccination with autologous tumor-loaded dendritic cells induces clinical and immunologic responses in indolent B-cell lymphoma patients with relapsed and measurable disease: a pilot study. Blood 113: 18-27 [Abstract] [Full Text]  
• Zhang, B., Liu, R., Shi, D., Liu, X., Chen, Y., Dou, X., Zhu, X., Lu, C., Liang, W., Liao, L., Zenke, M., Zhao, R. C. H. (2009). Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2-dependent regulatory dendritic cell population. Blood 113: 46-57 [Abstract] [Full Text]  
• Huber, M., Brustle, A., Reinhard, K., Guralnik, A., Walter, G., Mahiny, A., von Low, E., Lohoff, M. (2008). IRF4 is essential for IL-21-mediated induction, amplification, and stabilization of the Th17 phenotype. Proc. Natl. Acad. Sci. USA 105: 20846-20851 [Abstract] [Full Text]  
• Huter, E. N., Stummvoll, G. H., DiPaolo, R. J., Glass, D. D., Shevach, E. M. (2008). Cutting Edge: Antigen-Specific TGF{beta}-Induced Regulatory T Cells Suppress Th17-Mediated Autoimmune Disease. J. Immunol. 181: 8209-8213 [Abstract] [Full Text]  
• Duan, W., So, T., Croft, M. (2008). Antagonism of Airway Tolerance by Endotoxin/Lipopolysaccharide through Promoting OX40L and Suppressing Antigen-Specific Foxp3+ T Regulatory Cells. J. Immunol. 181: 8650-8659 [Abstract] [Full Text]  
• Ahmadzadeh, M., Felipe-Silva, A., Heemskerk, B., Powell, D. J. Jr, Wunderlich, J. R., Merino, M. J., Rosenberg, S. A. (2008). FOXP3 expression accurately defines the population of intratumoral regulatory T cells that selectively accumulate in metastatic melanoma lesions. Blood 112: 4953-4960 [Abstract] [Full Text]  
• Imarai, M., Candia, E., Rodriguez-Tirado, C., Tognarelli, J., Pardo, M., Perez, T., Valdes, D., Reyes-Cerpa, S., Nelson, P., Acuna-Castillo, C., Maisey, K. (2008). Regulatory T Cells Are Locally Induced during Intravaginal Infection of Mice with Neisseria gonorrhoeae. Infect. Immun. 76: 5456-5465 [Abstract] [Full Text]  
• Sarangi, P. P., Kim, B., Rouse, B. T. (2008). Non-mitogenic Anti-CD3F(ab')2 Monoclonal Antibody: A Novel Approach to Control Herpetic Stromal Keratitis. IOVS 49: 5425-5433 [Abstract] [Full Text]  
• Zang, W., Lin, M., Kalache, S., Zhang, N., Kruger, B., Waaga-Gasser, A. M., Grimm, M., Hancock, W., Heeger, P., Schroppel, B., Murphy, B. (2008). Inhibition of the Alloimmune Response through the Generation of Regulatory T Cells by a MHC Class II-Derived Peptide. J. Immunol. 181: 7499-7506 [Abstract] [Full Text]  
• Sugita, S., Horie, S., Nakamura, O., Futagami, Y., Takase, H., Keino, H., Aburatani, H., Katunuma, N., Ishidoh, K., Yamamoto, Y., Mochizuki, M. (2008). Retinal Pigment Epithelium-Derived CTLA-2{alpha} Induces TGF{beta}-Producing T Regulatory Cells. J. Immunol. 181: 7525-7536 [Abstract] [Full Text]  
• Yamazaki, S., Dudziak, D., Heidkamp, G. F., Fiorese, C., Bonito, A. J., Inaba, K., Nussenzweig, M. C., Steinman, R. M. (2008). CD8+CD205+ Splenic Dendritic Cells Are Specialized to Induce Foxp3+ Regulatory T Cells. J. Immunol. 181: 6923-6933 [Abstract] [Full Text]  

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