Tumor cells convert immature myeloid dendritic cells into TGF-β-secreting cells inducing CD4 +CD25 + regulatory T cell proliferation

Journal of Experimental Medicine

Volumn 202, Issue 7, 2005, Pages 919-929

  Ghiringhelli, François ^a   Puig, Pierre E ^a   Roux, Stephan ^b   Parcellier, Arnaud ^a   Schmitt, Elise ^a   Solary, Eric ^a   Kroemer, Guido ^c   Martin, François ^a   Chauffert, Bruno ^a   Zitvogel, Laurence ^b  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b INSERM   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DENDRITIC CELL; EXPERIMENTAL MOUSE; EXPERIMENTAL RAT; HEMATOPOIETIC STEM CELL; IMMUNOGENETICS; IMMUNOSURVEILLANCE; LYMPH NODE; LYMPH NODE CELL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SECRETORY CELL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TUMOR CELL; TUMOR GROWTH; TUMOR IMMUNITY;

ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; DENDRITIC CELLS; DNA PRIMERS; FORKHEAD TRANSCRIPTION FACTORS; IMMUNOHISTOCHEMISTRY; MICE; NEOPLASMS; RATS; RATS, INBRED STRAINS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 25844504654     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20050463     Document Type: Article

References (37)

1. Sakaguchi, S. 2000. Regulatory T cells: key controllers of immunologic self-tolerance. Cell. 101:455-458.
2. Shevach, E.M. 2002. CD4+ CD25+ suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2:389-400.
3. Brunkow, M.E., E.W. Jeffery, K.A. Hjerrild, B. Paeper, L.B. Clark, S.A. Yasayko, J.E. Wilkinson, D. Galas, S.F. Ziegler, and F. Ramsdell. 2001. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27:68-73.
4. Sakaguchi, S. 2004. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22:531-562.
5. Takahashi, T., Y. Kuniyasu, M. Toda, N. Sakaguchi, M. Itoh, M. Iwata, J. Shimizu, and S. Sakaguchi. 1998. Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int. Immunol. 10:1969-1980.
6. Thornton, A.M., and E.M. Shevach. 1998. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin-2 production. J. Exp. Med. 188:287-296.
7. Thornton, C.A., J.W. Upham, M.E. Wikstrom, B.J. Holt, G.P. White, M.J. Sharp, P.D. Sly, and P.G. Holt. 2004. Functional maturation of CD4+CD25+CTLA4+CD45RA+ T regulatory cells in human neonatal T cell responses to environmental antigens/allergens. J. Immunol. 173:3084-3092.
8. Takahashi, T., T. Tagami, S. Yamazaki, T. Uede, J. Shimizu, N. Sakaguchi, T.W. Mak, and S. Sakaguchi. 2000. Immunologic self-tolerance maintained by CD25+CD4+ regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J. Exp. Med. 192:303-310.
9. Yamazaki, S., T. Iyoda, K. Tarbell, K. Olson, K. Velinzon, K. Inaba, and R.M. Steinman. 2003. Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198:235-247.
10. Pasare, C., and R. Medzhitov. 2003. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science. 299:1033-1036.
11. Almeida, A.R., N. Legrand, M. Papiernik, and A.A. Freitas. 2002. Homeostasis of peripheral CD4+ T cells: IL-2R alpha and IL-2 shape a population of regulatory cells that controls CD4+ T cell numbers. J. Immunol. 169:4850-4860.
12. Gavin, M.A., S.R. Clarke, E. Negrou, A. Gallegos, and A. Rudensky. 2001. Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat. Immunol. 3:33-41.
13. Liyanage, U.K., T.T. Moore, H.G. Joo, Y. Tanaka, V. Herrmann, G. Doherty, J.A. Drebin, S.M. Strasberg, T.J. Eberlein, P.S. Goedegebuure, and D.C. Linehan. 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.
14. Wolf, A.M., D. Wolf, M. Steurer, G. Gastl, E. Gunsilius, and B. Grubeck-Loebenstein. 2003. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin. Cancer Res. 9:606-612.
15. Sasada, T., M. Kimura, Y. Yoshida, M. Kanai, and A. Takabayashi. 2003. CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer. 98:1089-1099.
16. Woo, E.Y., C.S. Chu, T.J. Goletz, K. Schlienger, H. Yeh, G. Coukos, S.C. Rubin, L.R. Kaiser, and C.H. June. 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.
17. Curiel, T.J., G. Coukos, L. Zou, X. Alvarez, P. Cheng, P. Mottram, M. Evdemon-Hogan, J.R. Conejo-Garcia, L. Zhang, M. Burow, et al. 2004. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10: 942-949.
18. Ghiringhelli, F., N. Larmonier, E. Schmitt, A. Parcellier, D. Cathelin, C. Garrido, B. Chauffert, E. Solary, B. Bonnotte, and F. Martin. 2004. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of estab-lished tumors to be curative. Eur. J. Immunol. 34:336-344.
19. Turk, M.J., J.A. Guevara-Patino, G.A. Rizzuto, M.E. Engelhorn, S. Sakaguchi, and A.N. Houghton. 2004. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J. Exp. Med. 200:771-782.
20. Peng, Y., Y. Laouar, M.O. Li, E.A. Green, and R.A. Flavell. 2004. TGF-beta regulates in vivo expansion of Foxp3-expressing CD4+ CD25+ regulatory T cells responsible for protection against diabetes. Proc. Natl. Acad. Sci. USA. 101:4572-4577.
21. Huber, S., C. Schramm, H.A. Lehr, A. Mann, S. Schmitt, C. Becker, M. Protschka, P.R. Galle, M.F. Neurath, and M. Blessing. 2004. Cutting edge: TGF-beta signaling is required for the in vivo expansion and immunosuppressive capacity of regulatory CD4+CD25+ T cells. J. Immunol. 173:6526-6531.
22. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198:1875-1886.
23. Walker, M.R., D.J. Kasprowicz, V.H. Gersuk, A. Benard, M. Van Landeghen, J.H. Buckner, and S.F. Ziegler. 2003. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J. Clin. Invest. 112:1437-1443.
24. Fantini, M.C., C. Becker, G. Monteleone, F. Pallone, P.R. Galle, and M.F. Neurath. 2004. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+CD25- T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172:5149-5153.
25. Curotto de Lafaille, M.A., A.C. Lino, N. Kutchukhidze, and J.J. Lafaille. 2004. CD25 T cells generate CD25+Foxp3+ regulatory T cells by peripheral expansion. J. Immunol. 173:7259-7268.
26. North, R.J., and M. Awwad. 1990. Elimination of cycling CD4+ suppressor T cells with an anti-mitotic drug releases non cycling CD8+ T cells to cause regression of an advanced lymphoma. Immunology. 71:90-95.
27. Granucci, F., I. Zanoni, S. Feau, and P. Ricciardi-Castagnoli. 2003. Dendritic cell regulation of immune responses: a new role for interleukin 2 at the intersection of innate and adaptive immunity. EMBO J. 22:2546-2551.
28. + regulatory T cells in vivo. J. Exp. Med. 198:249-258.
29. + T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J. Exp. Med. 199:1467-1477.
30. Gorelik, L., and R.A. Flavell. 2001. Immune-mediated eradication of tumors through the blockade of transforming growth factor-β signaling in T cells. Nat. Med. 7:1118-1121.
31. Mahnke, K., Y. Qian, J. Knop, and A.H. Enk. 2003. Induction of CD4+/CD25+ regulatory T cells by targeting of antigens to immature dendritic cells. Blood. 101:4862-4869.
32. Morelli, A.E., A.F. Zahorchak, A.T. Larregina, B.L. Colvin, A.J. Logar, T. Takayama, L.D. Falo, and A.W. Thomson. 2001. Cytokine production by mouse myeloid dendritic cells in relation to differentiation and terminal maturation induced by lipopolysaccharide or CD40 ligation. Blood. 98:1512-1523.
33. Munn, D.H., M.D. Sharma, D. Hou, B. Baban, J.R. Lee, S.J. Antonia, J.L. Messina, P. Chandler, P.A. Koni, and A.L. Mellor. 2004. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest. 114:280-290.
34. Gabrilovich, D. 2004. Mechanisms and functional significance of tumour-induced dendritic cell defects. Nat. Rev. Immunol. 4:941-952.
35. Wang, T., G. Niu, M. Kortylewski, L. Burdelya, K. Shain, S. Zhang, R. Bhattacharya, D. Gabrilovich, R. Heller, D. Coppola, et al. 2004. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat. Med. 10:48-54.
36. Caignard, A., H. Pelletier, and F. Martin. 1988. Specificity of the immune response leading to protection or enhancement by regressive and progressive variants of a rat colon carcinoma. Int. J. Cancer. 42:883-886.
37. Lucas, P.J., S.J. Kim, S.J. Melby, and R.E. Gress. 2000. Disruption of T cell homeostasis in mice expressing a T cell-specific dominant negative transforming growth factor II receptor. J. Exp. Med. 191:1187-1199.