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The Journal of Immunology, 2004, 173: 1444-1453.
Copyright © 2004 by The American Association of Immunologists

Foxp3 Expressing CD4+CD25high Regulatory T Cells Are Overrepresented in Human Metastatic Melanoma Lymph Nodes and Inhibit the Function of Infiltrating T Cells1

Manuelle Viguier2,*,{dagger}, Fabrice Lemaître*, Olivier Verola{ddagger}, Min-Sun Cho*, Guy Gorochov§, Louis Dubertret{dagger}, Hervé Bachelez{dagger}, Philippe Kourilsky* and Laurent Ferradini2,*

* Unité de Biologie Moléculaire du Gène, Institut National de la Santé et de la Recherche Médicale (INSERM) U277, Institut Pasteur, {dagger} Department of Dermatology and INSERM U532, Skin Research Institute, Hôpital Saint-Louis, Assistance Publique-Hôpitaux de Paris, {ddagger} Department of Pathology, Hôpital Saint-Louis, and § Immunology A, Centre d’Étude et de la Recherche en Virologie et en Immunologie, Institut National de Science et Recherche Medicale, Unité 543, Hôpital Pitié-Salpetrière, Paris, France

Dominant tolerance is mediated by regulatory T cells (Treg) that control harmful autoimmune T cells in the periphery. In this study, we investigate the implication of Treg in modulating infiltrating T lymphocytes in human metastatic melanoma. We found that CD4+CD25high T cells are overrepresented in metastatic lymph nodes (LNs) with a 2-fold increased frequency compared with both tumor-free LNs and autologous PBMCs. These cells express the Foxp3 transcription factor, display an activated phenotype, and display a polyclonal TCR V{beta} chain repertoire. They inhibit in vitro the proliferation and cytokine production of infiltrating CD4+CD25– and CD8+ T cells (IL-2, IFN-{gamma}) through a cell-contact-dependent mechanism, thus behaving as Treg. In some cases, the presence of Treg type 1/Th3-like lymphocytes could also be demonstrated. Thus, Treg are a major component of the immunosuppressive microenvironment of metastatic melanoma LNs. This could explain the poor clinical response of cancer patients under immunotherapeutic protocols, and provides a new basis for future immunotherapeutic strategies counteracting in vivo Treg to reinforce local antitumor immune responses.


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G. Zheng, S. Liu, P. Wang, Y. Xu, and A. Chen
Arming Tumor-Reactive T Cells with Costimulator B7-1 Enhances Therapeutic Efficacy of the T Cells.
Cancer Res., July 1, 2006; 66(13): 6793 - 6799.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. Kasprzycka, M. Marzec, X. Liu, Q. Zhang, and M. A. Wasik
From the Cover: Nucleophosmin/anaplastic lymphoma kinase (NPM/ALK) oncoprotein induces the T regulatory cell phenotype by activating STAT3
PNAS, June 27, 2006; 103(26): 9964 - 9969.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
L. Sfondrini, A. Rossini, D. Besusso, A. Merlo, E. Tagliabue, S. Menard, and A. Balsari
Antitumor Activity of the TLR-5 Ligand Flagellin in Mouse Models of Cancer.
J. Immunol., June 1, 2006; 176(11): 6624 - 6630.
[Abstract] [Full Text] [PDF]

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 BloodHome page
Z.-Z. Yang, A. J. Novak, M. J. Stenson, T. E. Witzig, and S. M. Ansell
Intratumoral CD4+CD25+ regulatory T-cell-mediated suppression of infiltrating CD4+ T cells in B-cell non-Hodgkin lymphoma
Blood, May 1, 2006; 107(9): 3639 - 3646.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
S. Danson and P. Lorigan
Melanoma vaccines - they should work
Ann. Onc., April 1, 2006; 17(4): 539 - 541.
[Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. F. Gajewski
Identifying and overcoming immune resistance mechanisms in the melanoma tumor microenvironment.
Clin. Cancer Res., April 1, 2006; 12(7): 2326s - 2330s.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
V. K. Sondak, M. S. Sabel, and J. J. Mule
Allogeneic and autologous melanoma vaccines: where have we been and where are we going?
Clin. Cancer Res., April 1, 2006; 12(7 Pt 2): 2337s - 2341s.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
G. Lizee, L. G. Radvanyi, W. W. Overwijk, and P. Hwu
Immunosuppression in melanoma immunotherapy: potential opportunities for intervention.
Clin. Cancer Res., April 1, 2006; 12(7): 2359s - 2365s.
[Abstract] [Full Text] [PDF]

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 JEMHome page
M. Miyara, Z. Amoura, C. Parizot, C. Badoual, K. Dorgham, S. Trad, M. Kambouchner, D. Valeyre, C. Chapelon-Abric, P. Debre, et al.
The immune paradox of sarcoidosis and regulatory T cells
J. Exp. Med., February 21, 2006; 203(2): 359 - 370.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
A. Comes, O. Rosso, A. M. Orengo, E. Di Carlo, C. Sorrentino, R. Meazza, T. Piazza, B. Valzasina, P. Nanni, M. P. Colombo, et al.
CD25+ Regulatory T Cell Depletion Augments Immunotherapy of Micrometastases by an IL-21-Secreting Cellular Vaccine
J. Immunol., February 1, 2006; 176(3): 1750 - 1758.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
S. Chattopadhyay, S. Mehrotra, A. Chhabra, U. Hegde, B. Mukherji, and N. G. Chakraborty
Effect of CD4+CD25+ and CD4+CD25- T Regulatory Cells on the Generation of Cytolytic T Cell Response to a Self but Human Tumor-Associated Epitope In Vitro
J. Immunol., January 15, 2006; 176(2): 984 - 990.
[Abstract] [Full Text] [PDF]

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 BloodHome page
R. H. Prabhala, P. Neri, J. E. Bae, P. Tassone, M. A. Shammas, C. K. Allam, J. F. Daley, D. Chauhan, E. Blanchard, H. S. Thatte, et al.
Dysfunctional T regulatory cells in multiple myeloma
Blood, January 1, 2006; 107(1): 301 - 304.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
D. Wolf, A. M. Wolf, H. Rumpold, H. Fiegl, A. G. Zeimet, E. Muller-Holzner, M. Deibl, G. Gastl, E. Gunsilius, and C. Marth
The Expression of the Regulatory T Cell-Specific Forkhead Box Transcription Factor FoxP3 Is Associated with Poor Prognosis in Ovarian Cancer
Clin. Cancer Res., December 1, 2005; 11(23): 8326 - 8331.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
Y.-Q. Chen, H.-Z. Shi, X.-J. Qin, W.-N. Mo, X.-D. Liang, Z.-X. Huang, H.-B. Yang, and C. Wu
CD4+CD25+ Regulatory T Lymphocytes in Malignant Pleural Effusion
Am. J. Respir. Crit. Care Med., December 1, 2005; 172(11): 1434 - 1439.
[Abstract] [Full Text] [PDF]

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 JEMHome page
F. Ghiringhelli, C. Menard, M. Terme, C. Flament, J. Taieb, N. Chaput, P. E. Puig, S. Novault, B. Escudier, E. Vivier, et al.
CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-{beta}-dependent manner
J. Exp. Med., October 17, 2005; 202(8): 1075 - 1085.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
L.-X. Wang, S. Shu, and G. E. Plautz
Host Lymphodepletion Augments T Cell Adoptive Immunotherapy through Enhanced Intratumoral Proliferation of Effector Cells
Cancer Res., October 15, 2005; 65(20): 9547 - 9554.
[Abstract] [Full Text] [PDF]

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 Phil Trans R Soc BHome page
Z. Fehervari and S. Sakaguchi
CD4+ regulatory cells as a potential immunotherapy
Phil Trans R Soc B, September 29, 2005; 360(1461): 1647 - 1661.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
W.-Z. Wei, J. B. Jacob, J. F. Zielinski, J. C. Flynn, K. D. Shim, G. Alsharabi, A. A. Giraldo, and Y.-c. M. Kong
Concurrent Induction of Antitumor Immunity and Autoimmune Thyroiditis in CD4+CD25+ Regulatory T Cell-Depleted Mice
Cancer Res., September 15, 2005; 65(18): 8471 - 8478.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
F. Baratelli, Y. Lin, L. Zhu, S.-C. Yang, N. Heuze-Vourc'h, G. Zeng, K. Reckamp, M. Dohadwala, S. Sharma, and S. M. Dubinett
Prostaglandin E2 Induces FOXP3 Gene Expression and T Regulatory Cell Function in Human CD4+ T Cells
J. Immunol., August 1, 2005; 175(3): 1483 - 1490.
[Abstract] [Full Text] [PDF]

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 BloodHome page
H. Nishikawa, E. Jager, G. Ritter, L. J. Old, and S. Gnjatic
CD4+ CD25+ regulatory T cells control the induction of antigen-specific CD4+ helper T cell responses in cancer patients
Blood, August 1, 2005; 106(3): 1008 - 1011.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
J. Andersson, A. Boasso, J. Nilsson, R. Zhang, N. J. Shire, S. Lindback, G. M. Shearer, and C. A. Chougnet
Cutting Edge: The Prevalence of Regulatory T Cells in Lymphoid Tissue Is Correlated with Viral Load in HIV-Infected Patients
J. Immunol., March 15, 2005; 174(6): 3143 - 3147.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
H. Y. Wang, G. Peng, Z. Guo, E. M. Shevach, and R.-F. Wang
Recognition of a New ARTC1 Peptide Ligand Uniquely Expressed in Tumor Cells by Antigen-Specific CD4+ Regulatory T Cells
J. Immunol., March 1, 2005; 174(5): 2661 - 2670.
[Abstract] [Full Text] [PDF]


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