Immune surveillance: a balance between protumor and antitumor immunity

Current Opinion in Genetics and Development

Volumn 18, Issue 1, 2008, Pages 11-18

  Ostrand Rosenberg, Suzanne ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGENESIS; CHRONIC INFLAMMATION; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; INNATE IMMUNITY; PRIORITY JOURNAL; REVIEW; TUMOR GROWTH; TUMOR IMMUNITY;

B-LYMPHOCYTES; HUMANS; IMMUNOLOGIC SURVEILLANCE; KILLER CELLS, NATURAL; MACROPHAGES; MYELOID CELLS; NEOPLASMS; T-LYMPHOCYTES;

EID: 43749102276     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2007.12.007     Document Type: Review

References (57)

1. Swann J.B., and Smyth M.J. Immune surveillance of tumors. J Clin Invest 117 (2007) 1137-1146
2. Reiman J.M., Kmieciak M., Manjili M.H., and Knutson K.L. Tumor immunoediting and immunosculpting pathways to cancer progression. Semin Cancer Biol 17 (2007) 275-287
3. Dunn G.P., Koebel C.M., and Schreiber R.D. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 6 (2006) 836-848
4. Smyth M.J., Dunn G.P., and Schreiber R.D. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol 90 (2006) 1-50. This is a comprehensive review of the concepts of cancer immunosurveillance and immunoediting by the investigators who resurrected the immunosurveillance hypothesis.
5. Galon J., Costes A., Sanchez-Cabo F., Kirilovsky A., Mlecnik B., Lagorce-Pages C., Tosolini M., Camus M., Berger A., Wind P., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313 (2006) 1960-1964
6. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6 (2006) 295-307
7. Baratelli F., Lin Y., Zhu L., Yang S.C., Heuze-Vourc'h N., Zeng G., Reckamp K., Dohadwala M., Sharma S., and Dubinett S.M. Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4+ T cells. J Immunol 175 (2005) 1483-1490. This paper demonstrates that immune-suppressive T regulatory cells are induced and activated by PGE2, demonstrating another mechanism by which inflammation suppresses adaptive antitumor immunity and promotes tumor progression.
8. Sharma S., Zhu L., Yang S.C., Zhang L., Lin J., Hillinger S., Gardner B., Reckamp K., Strieter R.M., Huang M., et al. Cyclooxygenase 2 inhibition promotes IFN-gamma-dependent enhancement of antitumor responses. J Immunol 175 (2005) 813-819
9. Ralainirina N., Poli A., Michel T., Poos L., Andres E., Hentges F., and Zimmer J. Control of NK cell functions by CD4+CD25+ regulatory T cells. J Leukoc Biol 81 (2007) 144-153
10. Wei S., Kryczek I., Zou L., Daniel B., Cheng P., Mottram P., Curiel T., Lange A., and Zou W. Plasmacytoid dendritic cells induce CD8+ regulatory T cells in human ovarian carcinoma. Cancer Res 65 (2005) 5020-5026
11. Castellino F., and Germain R.N. Cooperation between CD4+ and CD8+ T cells: when, where, and how. Annu Rev Immunol 24 (2006) 519-540
12. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med 13 (2007) 139-145
13. + Th17 cells (see reviews [12,15]), this report identifies a novel cytokine pathway that polarizes immunity towards a tumor-promoting phenotoype in response to inflammation.
14. Bi Y., Liu G., and Yang R. Th17 cell induction and immune regulatory effects. J Cell Physiol 211 (2007) 273-278
15. Langowski J.L., Kastelein R.A., and Oft M. Swords into plowshares: IL-23 repurposes tumor immune surveillance. Trends Immunol 28 (2007) 207-212
16. Numasaki M., Fukushi J., Ono M., Narula S.K., Zavodny P.J., Kudo T., Robbins P.D., Tahara H., and Lotze M.T. Interleukin-17 promotes angiogenesis and tumor growth. Blood 101 (2003) 2620-2627
17. Benchetrit F., Ciree A., Vives V., Warnier G., Gey A., Sautes-Fridman C., Fossiez F., Haicheur N., Fridman W.H., and Tartour E. Interleukin-17 inhibits tumor cell growth by means of a T-cell-dependent mechanism. Blood 99 (2002) 2114-2121
18. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., and Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006) 235-238
19. Nanni P., Nicoletti G., De Giovanni C., Landuzzi L., Di Carlo E., Cavallo F., Pupa S.M., Rossi I., Colombo M.P., Ricci C., et al. Combined allogeneic tumor cell vaccination and systemic interleukin 12 prevents mammary carcinogenesis in HER-2/neu transgenic mice. J Exp Med 194 (2001) 1195-1205
20. de Visser K.E., Korets L.V., and Coussens L.M. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7 (2005) 411-423. Using an in vivo skin carcinogenesis mouse system, this article demonstrates that B lymphocytes produce soluble factors that support an inflammatory environment that leads to de novo carcinogenesis. In addition to identifying a protumor role for B cells, this report directly links tumor induction to inflammation.
21. Tan T.T., and Coussens L.M. Humoral immunity, inflammation and cancer. Curr Opin Immunol 19 (2007) 209-216
22. Ostrand-Rosenberg S, Sinha P: Macrophages and tumor development. In Tumor-induced Immune Suppression: Mechanisms and Therapeutic Reversal. Edited by Gabrilovich D, Hurwitz A. Springer; 2008, pp. 131-155.
23. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 3 (2003) 23-35
24. Mills C.D., Kincaid K., Alt J.M., Heilman M.J., and Hill A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 164 (2000) 6166-6173
25. Mantovani A., Sica A., and Locati M. New vistas on macrophage differentiation and activation. Eur J Immunol 37 (2007) 14-16
26. Mantovani A., Schioppa T., Porta C., Allavena P., and Sica A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev 25 (2006) 315-322
27. Lin E.Y., Li J.F., Gnatovskiy L., Deng Y., Zhu L., Grzesik D.A., Qian H., Xue X.N., and Pollard J.W. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 66 (2006) 11238-11246
28. Wyckoff J.B., Wang Y., Lin E.Y., Li J.F., Goswami S., Stanley E.R., Segall J.E., Pollard J.W., and Condeelis J. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 67 (2007) 2649-2656
29. Kryczek I., Zou L., Rodriguez P., Zhu G., Wei S., Mottram P., Brumlik M., Cheng P., Curiel T., Myers L., et al. B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 203 (2006) 871-881
30. Biswas S.K., Gangi L., Paul S., Schioppa T., Saccani A., Sironi M., Bottazzi B., Doni A., Vincenzo B., Pasqualini F., et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood 107 (2006) 2112-2122
31. Ghassabeh G.H., De Baetselier P., Brys L., Noel W., Van Ginderachter J.A., Meerschaut S., Beschin A., Brombacher F., and Raes G. Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions. Blood 108 (2006) 575-583
32. Rabinovich B.A., Li J., Shannon J., Hurren R., Chalupny J., Cosman D., and Miller R.G. Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J Immunol 170 (2003) 3572-3576
33. Ferlazzo G., Morandi B., D'Agostino A., Meazza R., Melioli G., Moretta A., and Moretta L. The interaction between NK cells and dendritic cells in bacterial infections results in rapid induction of NK cell activation and in the lysis of uninfected dendritic cells. Eur J Immunol 33 (2003) 306-313
34. Barber M.A., Zhang T., Gagne B.A., and Sentman C.L. NK cells negatively regulate antigen presentation and tumor-specific CTLs in a syngeneic lymphoma model. J Immunol 178 (2007) 6140-6147
35. Hayakawa Y., Screpanti V., Yagita H., Grandien A., Ljunggren H.G., Smyth M.J., and Chambers B.J. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol 172 (2004) 123-129
36. Terabe M., Swann J., Ambrosino E., Sinha P., Takaku S., Hayakawa Y., Godfrey D.I., Ostrand-Rosenberg S., Smyth M.J., and Berzofsky J.A. A nonclassical non-Valpha14Jalpha18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J Exp Med 202 (2005) 1627-1633
37. Gabrilovich D.I., Bronte V., Chen S.H., Colombo M.P., Ochoa A., Ostrand-Rosenberg S., and Schreiber H. The terminology issue for myeloid-derived suppressor cells. Cancer Res 67 (2007) 425 [author reply 426]
38. Serafini P., Borrello I., and Bronte V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol 16 (2006) 53-65
39. Bunt S.K., Hanson E.M., Sinha P., Srivastava M.K., Clements V.K., and Ostrand-Rosenberg S. Tumor-associated myeloid-derived suppressor cells. In: Prendergast G.C., and Jaffee E. (Eds). Cancer Immunotherapy: Immune Suppression and Tumor Growth (2007), Elsevier 309-331. This article comprehensively reviews the development, function, activation, and mechanisms of suppression of MDSC.
40. Sinha P., Clements V.K., and Ostrand-Rosenberg S. Interleukin-13-regulated M2 macrophages in combination with myeloid suppressor cells block immune surveillance against metastasis. Cancer Res 65 (2005) 11743-11751
41. Yanagisawa K., Exley M.A., Jiang X., Ohkochi N., Taniguchi M., and Seino K. Hyporesponsiveness to natural killer T-cell ligand alpha-galactosylceramide in cancer-bearing state mediated by CD11b+ Gr-1+ cells producing nitric oxide. Cancer Res 66 (2006) 11441-11446
42. Rodriguez P.C., and Ochoa A.C. T cell dysfunction in cancer: role of myeloid cells and tumor cells regulating amino acid availability and oxidative stress. Semin Cancer Biol 16 (2006) 66-72
43. Kusmartsev S., and Gabrilovich D.I. Role of immature myeloid cells in mechanisms of immune evasion in cancer. Cancer Immunol Immunother 55 (2006) 237-245
44. Yang R., Cai Z., Zhang Y., Yutzy W.Ht., Roby K.F., and Roden R.B. CD80 in immune suppression by mouse ovarian carcinoma-associated Gr-1+CD11b+ myeloid cells. Cancer Res 66 (2006) 6807-6815
45. Sinha P., Clements V.K., and Ostrand-Rosenberg S. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J Immunol 174 (2005) 636-645
46. •] demonstrate that inflammation, in these cases induced by IL-1β, regulate the accumulation and retention of MDSC. This report is the first to propose that inflammation promotes tumor progression by inducing MDSC which block immune surveillance.
47. Gallina G., Dolcetti L., Serafini P., De Santo C., Marigo I., Colombo M.P., Basso G., Brombacher F., Borrello I., Zanovello P., et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 116 (2006) 2777-2790
48. + T cell from receiving activating peptide-MHC I signals from normal antigen presenting cells.
49. Huang B., Pan P.Y., Li Q., Sato A.I., Levy D.E., Bromberg J., Divino C.M., and Chen S.H. 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 (2006) 1123-1131
50. Sinha P., Clements V.K., Bunt S.K., Albelda S.M., and Ostrand-Rosenberg S. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 179 (2007) 977-983
51. •])
52. Bunt S.K., Yang L., Sinha P., Clements V.K., Leips J., and Ostrand-Rosenberg S. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res 67 (2007) 10019-10026
53. •], provide direct evidence that induction of this important population of suppressor cells that is found in most cancer patients and experimental animals with tumors, is directly regulated by inflammation.
54. Rodriguez P.C., Hernandez C.P., Quiceno D., Dubinett S.M., Zabaleta J., Ochoa J.B., Gilbert J., and Ochoa A.C. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med 202 (2005) 931-939. This paper demonstrated that a mouse lung tumor produces COX-2 which upregulates the immunosuppressive enzyme arginase I in myeloid-derived suppressor cells via the E-prostanoid receptor 4, thereby promoting immune suppression.
55. Karin M., and Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5 (2005) 749-759. This comprehensive review article describes the studies demonstrating a linkage between infection, inflammation, and cancer, and proposed that NF-κB is a key regulatory molecule in inflammation-induced tumor progression. It also reviews the various immune mediators that are activated by inflammation.
56. Balkwill F., Charles K.A., and Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7 (2005) 211-217
57. de Visser K.E., Eichten A., and Coussens L.M. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 6 (2006) 24-37