Monocyte-derived dendritic cells from breast cancer patients are biased to induce CD4+CD25+Foxp3+ regulatory T cells

Journal of Leukocyte Biology

Volumn 92, Issue 3, 2012, Pages 673-682

  Ramos, Rodrigo Nalio ^a   Chin, Lilian Sally ^a   dos Santos, Ana Paula S A ^a,b   Bergami Santos, Patrícia Cruz ^a   Laginha, Fábio ^c   Barbuto, José Alexandre M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF MARANHÃO   (Brazil)

^c Hospital Pérola Byngton   (Brazil)

Author keywords

Cancer; Tolerance; Tumor immunology

Indexed keywords

B7 ANTIGEN; CD123 ANTIGEN; CD4 ANTIGEN; CD40 LIGAND; CD83 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; T6 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BREAST CANCER; CANCER PATIENT; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MONOCYTE; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

BREAST NEOPLASMS; COCULTURE TECHNIQUES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE ACTIVATION; MONOCYTES; T-LYMPHOCYTES, REGULATORY; TUMOR ESCAPE;

EID: 84865519693     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0112048     Document Type: Article

References (53)

1. Banchereau, J., Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252.
2. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y. J., Pulendran, B., Palucka, K (2000) Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811.
3. Pulendran, B., Smith, J. L., Caspary, G., Brasel, K., Pettit, D., Marask-ovsky, E., Maliszewski, C. R. (1999) Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 96, 1036-1041.
4. Soumelis, V., Reche, P. A., Kanzler, H., Yuan, W., Edward, G., Homey, B., Gilliet, M., Ho, S., Antonenko, S., Lauerma, A., Smith, K., Gorman, D., Zurawski, S., Abrams, J., Menon, S., McClanahan, T., de Waal-Male-fyt, R. R., Bazan, F., Kastelein, R. A., Liu, Y. J. (2002) Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat. Immunol. 3, 673-680.
5. Bailey, S. L., Schreiner, B., McMahon, E.J., Miller, S. D. (2007) CNS myeloid DCs presenting endogenous myelin peptides "preferentially" polarize CD4+ T(H)-17 cells in relapsing EAE. Nat. Immunol. 8, 172180.
6. Levings, M. K., Gregori, S., Tresoldi, E., Cazzaniga, S., Bonini, C., Ron-carolo, M. G. (2005) Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25 + CD4+ Tr cells. Blood 105, 1162-1169.
7. Ilarregui, J. M., Croci, D. O., Bianco, G. A., Toscano, M. A., Salatino, M., Vermeulen, M. E., Geffner, J. R., Rabinovich, G. A. (2009) Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat. Immunol. 10, 981-991.
8. Baleeiro, R. B., Anselmo, L. B., Soares, F. A., Pinto, C. A., Ramos, O., Gross, J. L., Haddad, F., Younes, R. N., Tomiyoshi, M. Y., Bergami-San-tos, P. C., Barbuto, J. A. (2008) High frequency of immature dendritic cells and altered in situ production of interleukin-4 and tumor necrosis factor-α in lung cancer. Cancer Immunol. Immunother. 57, 1335-1345.
9. Neves, A. R., Ensina, L. F., Anselmo, L. B., Leite, K R., Buzaid, A. C., Camara-Lopes, L. H., Barbuto, J. A. (2005) Dendritic cells derived from metastatic cancer patients vaccinated with allogeneic dendritic cell-autologous tumor cell hybrids express more CD86 and induce higher levels of interferon-γ in mixed lymphocyte reactions. Cancer Immunol. Immunother. 54, 61-66.
10. Hsu, F. J., Benike, C., Fagnoni, F., Liles, T. M., Czerwinski, D., Taidi, B., Engleman, E. G., Levy, R. (1996) Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat. Med. 2, 52-58.
11. Nestle, F. O., Alijagic, S., Gilliet, M., Sun, Y., Grabbe, S., Dummer, R., Burg, G., Schadendorf, D. (1998) Vaccination of melanoma patients with peptide-or tumor lysate-pulsed dendritic cells. Nat. Med. 4, 328332.
12. Yates, S. F., Paterson, A. M., Nolan, K F., Cobbold, S. P., Saunders, N. J., Waldmann, H., Fairchild, P. J. (2007) Induction of regulatory T cells and dominant tolerance by dendritic cells incapable of full activation. J. Immunol. 179, 967-976.
13. Jonuleit, H., Schmitt, E., Schuler, G., Knop, J., 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.
14. Dhodapkar, M. V., Steinman, R. M. (2002) Antigen-bearing immature dendritic cells induce peptide-specific CD8(+) regulatory T cells in vivo in humans. Blood 100, 174-177.
15. Belkaid, Y., Oldenhove, G. (2008) Tuning microenvironments: induction of regulatory T cells by dendritic cells. Immunity 29, 362-371.
16. Banerjee, D. K., Dhodapkar, M. V., Matayeva, E., Steinman, R. M., Dhodapkar, K M. (2006) Expansion of FOXP3high regulatory T cells by human dendritic cells (DCs) in vitro and after injection of cytokine-matured DCs in myeloma patients. Blood 108, 2655-2661.
17. Barbuto, J. A., Ensina, L. F., Neves, A. R., Bergami-Santos, P., Leite, K R., Marques, R., Costa, F., Martins, S. C., Camara-Lopes, L. H., Bu-zaid, A. C. (2004) Dendritic cell-tumor cell hybrid vaccination for metastatic cancer. Cancer Immunol. Immunother. 53, 1111-1118.
18. Sakaguchi, S. (2005) Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6, 345-352.
19. Campanelli, A. P., Roselino, A. M., Cavassani, K A., Pereira, M. S., Mortara, R. A., Brodskyn, C. I., Goncalves, H. S., Belkaid, Y., Barral-Netto, M., Barral, A., Silva, J. S. (2006) CD4 + CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J. Infect. Dis. 193, 1313-1322.
20. Montagnoli, C., Bacci, A., Bozza, S., Gaziano, R., Mosci, P., Sharpe, A. H., Romani, L. (2002) B7/CD28-dependent CD4 + CD25+ regulatory T cells are essential components of the memory-protective immunity to Candida albicans. J. Immunol. 169, 6298-6308.
21. Dunn, G. P., Old, L. J., Schreiber, R. D. (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21, 137-148.
22. Zou, W. (2005) Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer 5, 263-274.
23. Xystrakis, E., Dejean, A. S., Bernard, I., Druet, P., Liblau, R., Gonzalez-Dunia, D., Saoudi, A. (2004) Identification of a novel natural regulatory CD8 T-cell subset and analysis of its mechanism of regulation. Blood 104, 3294-3301.
24. Curotto de Lafaille, M. A., Lafaille, J. J. (2009) Natural and adaptive Foxp3+ regulatory T cells: more of the same or a division of labor? Immunity 30, 626-635.
25. Shevach, E. M. (2009) Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 30, 636-645.
26. Roncarolo, M. G., Gregori, S., Battaglia, M., Bacchetta, R., Fleischhauer, K., Levings, M. K (2006) Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunol. Rev. 212, 28-50.
27. Faria, A. M., Weiner, H. L. (2005) Oral tolerance. Immunol. Rev. 206, 232-259.
28. Chen, W., Jin, W., Hardegen, N., Lei, K J., Li, L., Marinos, N., McGrady, G., Wahl, S. M. (2003) Conversion of peripheral CD4+. J. Exp. Med. 198, 1875-1886.
29. 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., Zou, W. (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10, 942-949.
30. Woo, E. Y., Chu, C. S., Goletz, T. J., Schlienger, K., Yeh, H., Coukos, G., Rubin, S. C., Kaiser, L. R., 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.
31. Liyanage, U. K, Moore, T. T., Joo, H. G., Tanaka, Y., Herrmann, V., Doherty, G., Drebin, J. A., Strasberg, S. M., Eberlein, T. J., Goedege-buure, P. S., 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.
32. Banchereau, J., Palucka, A. K. (2005) Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 5, 296-306.
33. Gabrilovich, D. (2004) Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat. Rev. Immunol. 4, 941-952.
34. Walker, M. R., Carson, B. D., Nepom, G. T., Ziegler, S. F., Buckner, J. H. (2005) De novo generation of antigen-specific CD4 + CD25+ regulatory T cells from human CD4 +. Proc. Natl. Acad. Sci. USA 102, 41034108.
35. Luo, X., Tarbell, K. V., Yang, H., Pothoven, K., Bailey, S. L., Ding, R., Steinman, R. M., Suthanthiran, M. (2007) Dendritic cells with TGF-^1 differentiate naive CD4 +. Proc. Natl. Acad. Sci. USA 104, 2821-2826.
36. Selvaraj, R. K., Geiger, T. L. (2007) A kinetic and dynamic analysis of Foxp3 induced in T cells by TGF-β. J. Immunol. 178, 7667-7677.
37. Sakaguchi, S., Miyara, M., Costantino, C. M., Hafler, D. A. (2010) FOXP3+ regulatory T cells in the human immune system. Nat. Rev. Immunol. 10, 490-500.
38. Sallusto, F., Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and down-regulated by tumor necrosis factor a. J. Exp. Med. 179, 1109-1118.
39. Sharpe, A. H., Freeman, G. J. (2002) The B7-CD28 superfamily. Nat. Rev. Immunol. 2, 116-126.
40. Sansom, D. M., Manzotti, C. N., Zheng, Y. (2003) What's the difference between CD80 and CD86? Trends Immunol. 24, 314-319.
41. Zheng, Y., Manzotti, C. N., Liu, M., Burke, F., Mead, K. I., Sansom, D. M. (2004) CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J. Immunol. 172, 2778-2784.
42. Perez, N., Karumuthil-Melethil, S., Li, R., Prabhakar, B. S., Holterman, M. J., Vasu, C. (2008) Preferential costimulation by CD80 results in IL-10-dependent TGF-^1(+)-adaptive regulatory T cell generation. J. Immunol. 180, 6566-6576.
43. Wang, L., Pino-Lagos, K., de Vries, V. C., Guleria, I., Sayegh, M. H., No-elle, R. J. (2008) Programmed death 1 ligand signaling regulates the generation of adaptive Foxp3+CD4+ regulatory T cells. Proc. Natl. Acad. Sci. USA 105, 9331-9336.
44. Kuang, D. M., Zhao, Q., Peng, C., Xu, J., Zhang, J. P., Wu, C., Zheng, L. (2009) Activated monocytes in peritumoral stroma of hepatocellular carcinoma foster immune privilege and disease progression through PD-L1. J. Exp. Med. 206, 1327-1337.
45. Dong, H., Strome, S. E., Salomao, D. R., Tamura, H., Hirano, F., Flies, D. B., Roche, P. C., Lu, J., Zhu, G., Tamada, K., Lennon, V. A., Celis, E., Chen, L. (2002) Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8, 793-800.
46. Munn, D. H., Sharma, M. D., Lee, J. R., Jhaver, K. G., Johnson, T. S., Keskin, D. B., Marshall, B., Chandler, P., Antonia, S. J., Burgess, R., Slin-gluff C. L. Jr., Mellor, A. L. (2002) Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297, 1867-1870.
47. Nakamura, T., Shima, T., Saeki, A., Hidaka, T., Nakashima, A., Takikawa, O., Saito, S. (2007) Expression of indoleamine 2, 3-dioxygenase and the recruitment of Foxp3-expressing regulatory T cells in the development and progression of uterine cervical cancer. Cancer Sci. 98, 874-881.
48. Zeng, M., Guinet, E., Nouri-Shirazi, M. (2009) B7-1 and B7-2 differentially control peripheral homeostasis of CD4(+)CD25(+)Foxp3(+) regulatory T cells. Transpl. Immunol. 20, 171-179.
49. Zheng, S. G., Wang, J. H., Gray, J. D., Soucier, H., Horwitz, D. A. (2004) Natural and induced CD4 + CD25+ cells educate CD4+. J. Immunol. 172, 5213-5221.
50. Massague, J. (2000) How cells read TGF-β signals. Nat. Rev. Mol. Cell. Biol. 1, 169-178.
51. Gorelik, L., Constant, S., Flavell, R. A. (2002) Mechanism of transforming growth factor β-induced inhibition of T helper type 1 differentiation. J. Exp. Med. 195, 1499-1505.
52. Ghiringhelli, F., Puig, P. E., Roux, S., Parcellier, A., Schmitt, E., Solary, E., Kroemer, G., Martin, F., Chauffert, B., Zitvogel, L. (2005) Tumor cells convert immature myeloid dendritic cells into TGF^-secreting cells inducing CD4 + CD25+ regulatory T cell proliferation. J. Exp. Med. 202, 919-929.
53. Miyara, M., Yoshioka, Y., Kitoh, A., Shima, T., Wing, K., Niwa, A., Par-izot, C., Taflin, C., Heike, T., Valeyre, D., Mathian, A., Nakahata, T., Yamaguchi, T., Nomura, T., Ono, M., Amoura, Z., Gorochov, G., Saka-guchi, S. (2009) Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 30, 899-911.