Depletion of regulatory T cells facilitates growth of established tumors: A mechanism involving the regulation of myeloid-derived suppressor cells by lipoxin A4

Journal of Immunology

Volumn 185, Issue 12, 2010, Pages 7199-7206

  Zhang, Biao ^a   Jia, Haibo ^b   Liu, Jing ^a   Yang, Zhuoshun ^a   Jiang, Tao ^b   Tang, Ke ^a   Li, Dapeng ^a   Huang, Chunmei ^b   Ma, Jingwei ^b   Shen, Guan Xin ^b   Ye, Duyun ^a   Huang, Bo ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 5 LIPOXYGENASE; CD11B ANTIGEN; CYCLOPHOSPHAMIDE; GAMMA INTERFERON; INTERLEUKIN 10; LIPOXIN A; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE MARROW CELL; CANCER MODEL; CANCER STAGING; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME SYNTHESIS; FLOW CYTOMETRY; IMMUNE RESPONSE; INFLAMMATION; LIVER CANCER; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, MONOCLONAL; CYCLOPHOSPHAMIDE; INFLAMMATION; LIPOXINS; LIPOXYGENASES; LIVER NEOPLASMS; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED BALB C; MICE, NUDE; MUTAGENS; MYELOID CELLS; NEOPLASMS, EXPERIMENTAL; RECEPTORS, CELL SURFACE; T-LYMPHOCYTES, REGULATORY;

EID: 78650642294     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001876     Document Type: Article

References (54)

1. Zou, W. 2005. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer 5:263-274.
2. Rabinovich, G. A., D. Gabrilovich, and E. M. Sotomayor. 2007. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol. 25:267-296.
3. Gabrilovich, D. I., and S. Nagaraj. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9:162-174.
4. Talmadge, J. E. 2007. Pathways mediating the expansion and immunosuppressive activity of myeloid-derived suppressor cells and their relevance to cancer therapy. Clin. Cancer Res. 13:5243-5248.
5. Marigo, I., L. Dolcetti, P. Serafini, P. Zanovello, and V. Bronte. 2008. Tumorinduced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev. 222:162-179.
6. Serafini, P., I. Borrello, and V. Bronte. 2006. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin. Cancer Biol. 16:53-65.
7. Colombo, M. P., and S. Piconese. 2007. Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat. Rev. Cancer 7:880-887.
8. Curiel, T. J. 2007. Tregs and rethinking cancer immunotherapy. J. Clin. Invest. 117:1167-1174.
9. Orentas, R. J., M. E. Kohler, and B. D. Johnson. 2006. Suppression of anti-cancer immunity by regulatory T cells: back to the future. Semin. Cancer Biol. 16:137-149.
10. Huang, B., P. Y. Pan, Q. Li, A. I. Sato, D. E. Levy, J. Bromberg, C. M. Divino, and S. H. Chen. 2006. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 66:1123-1131.
11. 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.
12. Campbell, D. J., and S. F. Ziegler. 2007. FOXP3 modifies the phenotypic and functional properties of regulatory T cells. Nat. Rev. Immunol. 7:305-310.
13. Balkwill, F., K. A. Charles, and A. Mantovani. 2005. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7:211-217.
14. Mantovani, A., P. Allavena, A. Sica, and F. Balkwill. 2008. Cancer-related inflammation. Nature 454:436-444.
15. Coussens, L. M., and Z. Werb. 2002. Inflammation and cancer. Nature 420:860-867.
16. Erdman, S. E., J. J. Sohn, V. P. Rao, P. R. Nambiar, Z. Ge, J. G. Fox, and D. B. Schauer. 2005. CD4+CD25+ regulatory lymphocytes induce regression of intestinal tumors in ApcMin/+ mice. Cancer Res. 65:3998-4004.
17. Maderna, P., and C. Godson. 2009. Lipoxins: resolutionary road. Br. J. Pharmacol. 158:947-959.
18. Serhan, C. N., S. Yacoubian, and R. Yang. 2008. Anti-inflammatory and proresolving lipid mediators. Annu. Rev. Pathol. 3:279-312.
19. Folco, G., and R. C. Murphy. 2006. Eicosanoid transcellular biosynthesis: from cell-cell interactions to in vivo tissue responses. Pharmacol. Rev. 58:375-388.
20. Ghiringhelli, F., C. Menard, P. E. Puig, S. Ladoire, S. Roux, F. Martin, E. Solary, A. Le Cesne, L. Zitvogel, and B. Chauffert. 2007. Metronomic cyclophosphamideCY regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol. Immunother. 56:641-648.
21. Daenen, L. G., Y. Shaked, S. Man, P. Xu, E. E. Voest, R. M. Hoffman, D. J. Chaplin, and R. S. Kerbel. 2009. Low-dose metronomic cyclophosphamide combined with vascular disrupting therapy induces potent antitumor activity in preclinical human tumor xenograft models. Mol. Cancer Ther. 8:2872-2881.
22. Castano, A. P., P. Mroz, M. X. Wu, and M. R. Hamblin. 2008. Photodynamic therapy plus low-dose cyclophosphamide generates antitumor immunity in a mouse model. Proc. Natl. Acad. Sci. USA 105:5495-5500.
23. Lutsiak, M. E., R. T. Semnani, R. De Pascalis, S. V. Kashmiri, J. Schlom, and H. Sabzevari. 2005. Inhibition of CD4 (+) 25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 105:2862-2868.
24. Yu, P., Y. Lee, W. Liu, T. Krausz, A. Chong, H. Schreiber, and Y. X. Fu. 2005. Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J. Exp. Med. 201:779-791.
25. Lin, W. W., and M. Karin. 2007. A cytokine-mediated link between innate immunity, inflammation, and cancer. J. Clin. Invest. 117:1175-1183.
26. Huang, B., Z. Lei, J. Zhao, W. Gong, J. Liu, Z. Chen, Y. Liu, D. Li, Y. Yuan, G. M. Zhang, and Z. H. Feng. 2007. CCL2/CCR2 pathway mediates recruitment of myeloid suppressor cells to cancers. Cancer Lett. 252:86-92.
27. Serafini, P., K. Meckel, M. Kelso, K. Noonan, J. Califano, W. Koch, L. Dolcetti, V. Bronte, and I. Borrello. 2006. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J. Exp. Med. 203:2691-2702.
28. Yang, Z., B. Zhang, D. Li, M. Lv, C. Huang, G. X. Shen, and B. Huang. 2010. Mast cells mobilize myeloid-derived suppressor cells and Treg cells in tumor microenvironment via IL-17 pathway in murine hepatocarcinoma model. PLoS ONE 5: e8922.
29. Huang, B., J. Zhao, S. Shen, H. Li, K. L. He, G. X. Shen, L. Mayer, J. Unkeless, D. Li, Y. Yuan, et al. 2007. Listeria monocytogenes promotes tumor growth via tumor cell toll-like receptor 2 signaling. Cancer Res. 67:4346-4352.
30. Pan, P. Y., G. X. Wang, B. Yin, J. Ozao, T. Ku, C. M. Divino, and S. H. Chen. 2008. Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood 111:219-228.
31. Sinha, P., V. K. Clements, A. M. Fulton, and S. Ostrand-Rosenberg. 2007. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res. 67:4507-4513.
32. Chang, X., P. Zheng, and Y. Liu. 2008. Homeostatic proliferation in the mice with germline FoxP3 mutation and its contribution to fatal autoimmunity. J. Immunol. 181:2399-2406.
33. Setiady, Y. Y., J. A. Coccia, and P. U. Park. 2010. In vivo depletion of CD4+ FOXP3+ Treg cells by the PC61 anti-CD25 monoclonal antibody is mediated by FcgammaRIII+ phagocytes. Eur. J. Immunol. 40:780-786.
34. Ko, K., S. Yamazaki, K. Nakamura, T. Nishioka, K. Hirota, T. Yamaguchi, J. Shimizu, T. Nomura, T. Chiba, and S. Sakaguchi. 2005. Treatment of advanced tumors with agonistic anti-GITR mAb and its effects on tumor-infiltrating Foxp3+CD25+CD4+ regulatory T cells. J. Exp. Med. 202:885-891.
35. Read, S., R. Greenwald, A. Izcue, N. Robinson, D. Mandelbrot, L. Francisco, A. H. Sharpe, and F. Powrie. 2006. Blockade of CTLA-4 on CD4+CD25+ regulatory T cells abrogates their function in vivo. J. Immunol. 177:4376-4383.
36. Zhou, Q., C. Bucher, M. E. Munger, S. L. Highfill, J. Tolar, D. H. Munn, B. L. Levine, M. Riddle, C. H. June, D. A. Vallera, et al. 2009. Depletion of endogenous tumor-associated regulatory T cells improves the efficacy of adoptive cytotoxic T-cell immunotherapy in murine acute myeloid leukemia. Blood 114:3793-3802.
37. Steitz, J., J. Brück, J. Lenz, J. Knop, and T. Tüting. 2001. Depletion of CD25 (+) CD4 (+) T cells and treatment with tyrosinase-related protein 2-transduced dendritic cells enhance the interferon alpha-induced, CD8 (+) T-cell-dependent immune defense of B16 melanoma. Cancer Res. 61:8643-8646.
38. Tanaka, H., J. Tanaka, J. Kjaergaard, and S. Shu. 2002. Depletion of CD4+ CD25+ regulatory cells augments the generation of specific immune T cells in tumor-draining lymph nodes. J. Immunother. 25:207-217.
39. Zhou, J., T. Ding, W. Pan, L. Y. Zhu, L. Li, and L. Zheng. 2009. Increased intratumoral regulatory T cells are related to intratumoral macrophages and poor prognosis in hepatocellular carcinoma patients. Int. J. Cancer 125:1640-1648.
40. 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.
41. Kobayashi, N., N. Hiraoka, W. Yamagami, H. Ojima, Y. Kanai, T. Kosuge, A. Nakajima, and S. Hirohashi. 2007. FOXP3+ regulatory T cells affect the development and progression of hepatocarcinogenesis. Clin. Cancer Res. 13:902-911.
42. Salama, P., M. Phillips, F. Grieu, M. Morris, N. Zeps, D. Joseph, C. Platell, and B. Iacopetta. 2009. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J. Clin. Oncol. 27:186-192.
43. Tzankov, A., C. Meier, P. Hirschmann, P. Went, S. A. Pileri, and S. Dirnhofer. 2008. Correlation of high numbers of intratumoral FOXP3+ regulatory T cells with improved survival in germinal center-like diffuse large B-cell lymphoma, follicular lymphoma and classical Hodgkin's lymphoma. Haematologica 93:193-200.
44. Haas, M., A. Dimmler, W. Hohenberger, G. G. Grabenbauer, G. Niedobitek, and L. V. Distel. 2009. Stromal regulatory T-cells are associated with a favourable prognosis in gastric cancer of the cardia. BMC Gastroenterol. 9:65.
45. Curtin, J. F., M. Candolfi, T. M. Fakhouri, C. Liu, A. Alden, M. Edwards, P. R. Lowenstein, and M. G. Castro. 2008. Treg depletion inhibits efficacy of cancer immunotherapy: implications for clinical trials. PLoS One 3: e1983.
46. Young, M. R., M. Newby, and H. T. Wepsic. 1987. Hematopoiesis and suppressor bone marrow cells in mice bearing large metastatic Lewis lung carcinoma tumors. Cancer Res. 47:100-105.
47. Young, M. R., M. A. Wright, and R. Pandit. 1997. Myeloid differentiation treatment to diminish the presence of immune-suppressive CD34+ cells within human head and neck squamous cell carcinomas. J. Immunol. 159:990-996.
48. Maier, T., J. H. Holda, and H. N. Claman. 1989. Natural suppressor cells. Prog. Clin. Biol. Res. 288:235-244.
49. Marx, J. 2008. Cancer immunology. Cancer's bulwark against immune attack: MDS cells. Science 319:154-156.
50. Yang, L., L. M. DeBusk, K. Fukuda, B. Fingleton, B. Green-Jarvis, Y. Shyr, L. M. Matrisian, D. P. Carbone, and P. C. Lin. 2004. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6:409-421.
51. Kim, J. M., J. P. Rasmussen, and A. Y. Rudensky. 2007. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8:191-197.
52. Porro, M., M. Saletti, L. Nencioni, L. Tagliaferri, and I. Marsili. 1980. Immunogenic correlation between cross-reacting material (CRM197) produced by a mutant of Corynebacterium diphtheriae and diphtheria toxoid. J. Infect. Dis. 142:716-724.
53. Naglich, J. G., J. E. Metherall, D. W. Russell, and L. Eidels. 1992. Expression cloning of a diphtheria toxin receptor: identity with a heparin-binding EGF-like growth factor precursor. Cell 69:1051-1061.
54. Kiso, S., S. Kawata, S. Tamura, J. Miyagawa, N. Ito, H. Tsushima, A. Yamada, S. Umeki, S. Higashiyama, N. Taniguchi, and Y. Matsuzawa. 1999. Expression of heparin-binding epidermal growth factor-like growth factor in the hepatocytes of fibrotic rat liver during hepatocarcinogenesis. J. Gastroenterol. Hepatol. 14:1203-1209. (Pubitemid 30032960)