Cellular constituents of immune escape within the tumor microenvironment

Cancer Research

Volumn 72, Issue 13, 2012, Pages 3125-3130

  Kerkar, Sid P ^a,b   Restifo, Nicholas P ^a,b  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; IPILIMUMAB; PROGRAMMED DEATH 1 RECEPTOR; SIPULEUCEL T; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CLONAL ANERGY; CYTOKINE RELEASE; DENDRITIC CELL; DRUG MEGADOSE; HUMAN; IMMUNE EVASION; IMMUNOGENICITY; KIDNEY METASTASIS; MACROPHAGE; METASTATIC MELANOMA; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROSTATE CANCER; REGULATORY T LYMPHOCYTE; REVIEW; SUPPRESSOR CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

HUMANS; IMMUNOTHERAPY; INTERLEUKIN-12; MACROPHAGE ACTIVATION; NEOPLASMS; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 84863594742     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-4094     Document Type: Review

References (71)

1. Li N, Grivennikov SI, Karin M. The unholy trinity: inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell 2011;19:429-31.
2. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 2010;22:231-7.
3. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
4. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-7. (Pubitemid 36019639)
5. Talmadge JE, Fidler IJ. AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res 2010;70:5649-69.
6. van Kempen LC, Ruiter DJ, van Muijen GN, Coussens LM. The tumor microenvironment: a critical determinant of neoplastic evolution. Eur J Cell Biol 2003;82:539-48. (Pubitemid 38008835)
7. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
8. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009;9:798-809.
9. Demaria S, Pikarsky E, Karin M, Coussens LM, Chen YC, El-Omar EM, et al. Cancer and inflammation: promise for biologic therapy. J Immunother 2010;33:335-51.
10. Dougan M, Li D, Neuberg D, Mihm M, Googe P, Wong KK, et al. A dual role for the immune response in a mouse model of inflammation-associated lung cancer. J Clin Invest 2011;121:2436-46.
11. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008;8:618-31.
12. Shojaei F, Zhong C, Wu X, Yu L, Ferrara N. Role of myeloid cells in tumor angiogenesis and growth. Trends Cell Biol 2008;18:372-8.
13. Yu P, Rowley DA, Fu YX, Schreiber H. The role of stroma in immune recognition and destruction of well-established solid tumors. Curr Opin Immunol 2006;18:226-31. (Pubitemid 43327307)
14. Bronte V. Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions. Eur J Immunol 2009;39:2670-2.
15. Fricke I, Gabrilovich DI. Dendritic cells and tumor microenvironment: a dangerous liaison. Immunol Invest 2006;35:459-83. (Pubitemid 44266783)
16. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
17. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004;6:409-21. (Pubitemid 39361441)
18. Balachandran VP, Cavnar MJ, Zeng S, Bamboat ZM, Ocuin LM, Obaid H, et al. Imatinib potentiates antitumor T cell responses in gastrointestinal stromal tumor through the inhibition of Ido. Nat Med 2011;17:1094-100.
19. Zitvogel L, Kepp O, Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 2011;8:151-60.
20. Gershon RK, Kondo K. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 1970;18:723-37.
21. North RJ. Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. J Exp Med 1982;155:1063-74. (Pubitemid 12142723)
22. Antony PA, Restifo NP. CD4+CD25+ T regulatory cells, immunotherapy of cancer, and interleukin-2. J Immunother 2005;28:120-8. (Pubitemid 40328198)
23. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999;59:3128-33. (Pubitemid 29316012)
24. Shimizu J, Yamazaki S, Sakaguchi S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J Immunol 1999;163:5211-8.
25. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003;4:330-6. (Pubitemid 36432314)
26. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-61. (Pubitemid 36222930)
27. Shevach EM. Fatal attraction: tumors beckon regulatory T cells. Nat Med 2004;10:900-1. (Pubitemid 39273725)
28. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 2006;6:295-307.
29. Bluestone JA, Abbas AK. Natural versus adaptive regulatory T cells. Nat Rev Immunol 2003;3:253-7. (Pubitemid 37323210)
30. Fehérvari Z, Sakaguchi S. CD4+ Tregs and immune control. J Clin Invest 2004;114:1209-17.
31. Matsui S, Ahlers JD, Vortmeyer AO, Terabe M, Tsukui T, Carbone DP, et al. A model for CD8+CTL tumor immunosurveillance and regulation of tumor escape by CD4 T cells through an effect on quality of CTL. J Immunol 1999;163:184-93. (Pubitemid 29295840)
32. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, et al. Removal of homeostatic cytokine sinks by lympho-depletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 2005;202:907-12. (Pubitemid 41396891)
33. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
34. Topalian SL, Weiner GJ, Pardoll DM. Cancer immunotherapy comes of age. J Clin Oncol 2011;29:4828-36.
35. Bronte V, Wang M, Overwijk WW, Surman DR, Pericle F, Rosenberg SA, et al. Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells. J Immunol 1998;161:5313-20. (Pubitemid 28519091)
36. Gabrilovich DI, Chen HL, Girgis KR, Cunningham HT, Meny GM, Nadaf S, et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med 1996;2:1096-103. (Pubitemid 26338628)
37. Fu YX, Watson G, Jimenez JJ, Wang Y, Lopez DM. Expansion of immunoregulatory macrophages by granulocyte-macrophage colony-stimulating factor derived from a murine mammary tumor. Cancer Res 1990;50:227-34. (Pubitemid 20041218)
38. Young MR, Young ME, Wright MA. Stimulation of immune-suppressive bone marrow cells by colony-stimulating factors. Exp Hematol 1990;18:806-11. (Pubitemid 20269449)
39. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science 2010;327:656-61.
40. Ostrand-Rosenberg S, Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009;182:4499-506.
41. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007;117:1155-66. (Pubitemid 46718400)
42. Seung LP, Rowley DA, Dubey P, Schreiber H. Synergy between T-cell immunity and inhibition of paracrine stimulation causes tumor rejection. Proc Natl Acad Sci U S A 1995;92:6254-8.
43. Bronte V, Chappell DB, Apolloni E, Cabrelle A, Wang M, Hwu P, et al. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation. J Immunol 1999;162:5728-37. (Pubitemid 29314923)
44. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
45. Gallina G, Dolcetti L, Serafini P, De Santo C, Marigo I, Colombo MP, et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 2006;116:2777-90. (Pubitemid 44511641)
46. Bronte V, Serafini P, Apolloni E, Zanovello P. Tumor-induced immune dysfunctions caused by myeloid suppressor cells. J Immunother 2001;24:431-46. (Pubitemid 33104863)
47. Highfill SL, Rodriguez PC, Zhou Q, Goetz CA, Koehn BH, Veenstra R, et al. Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13. Blood 2010;116:5738-47.
48. Srivastava MK, Sinha P, Clements VK, Rodriguez P, Ostrand-Rosenberg S. Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res 2010;70:68-77.
49. Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, et al. 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 2006;66:1123-31. (Pubitemid 43165981)
50. Guiducci C, Vicari AP, Sangaletti S, Trinchieri G, Colombo MP. Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res 2005;65:3437-46. (Pubitemid 40524630)
51. Chmielewski M, Kopecky C, Hombach AA, Abken H. IL-12 release by engineered T cells expressing chimeric antigen receptors can effectively muster an antigen-independent macrophage response on tumor cells that have shut down tumor antigen expression. Cancer Res 2011;71:5697-706.
52. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-52. (Pubitemid 28155090)
53. Dhodapkar MV, Steinman RM, Krasovsky J, Munz C, Bhardwaj N. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J Exp Med 2001;193:233-8. (Pubitemid 32524454)
54. Gabrilovich D. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 2004;4:941-52. (Pubitemid 39620069)
55. Munn DH, Sharma MD, Lee JR, Jhaver KG, Johnson TS, Keskin DB, et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 2002;297:1867-70. (Pubitemid 35024345)
56. Rosenberg SA. The development of new immunotherapies for the treatment of cancer using interleukin-2. A review. Ann Surg 1988;208:121-35.
57. Sharma P, Wagner K, Wolchok JD, Allison JP. Novel cancer immunotherapy agents with survival benefit: recent successes and next steps. Nat Rev Cancer 2011;11:805-12.
58. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A 2010;107:4275-80.
59. Brenner MK, Heslop HE. Adoptive T cell therapy of cancer. Curr Opin Immunol 2010;22:251-7.
60. Hwu P, Rosenberg SA. The use of gene-modified tumor-infiltrating lymphocytes for cancer therapy. Ann N Y Acad Sci 1994;716:188-97, discussion 197-203.
61. June CH. Principles of adoptive T cell cancer therapy. J Clin Invest 2007;117:1204-12. (Pubitemid 46718405)
62. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008;8:299-308. (Pubitemid 351430867)
63. Sadelain M. T-cell engineering for cancer immunotherapy. Cancer J 2009;15:451-5.
64. Kerkar SP, Muranski P, Kaiser A, Boni A, Sanchez-Perez L, Yu Z, et al. Tumor-specific CD8+ T cells expressing interleukin-12 eradicate established cancers in lymphodepleted hosts. Cancer Res 2010;70:6725-34.
65. Zhang L, Kerkar SP, Yu Z, Zheng Z, Yang S, Restifo NP, et al. Improving adoptive T cell therapy by targeting and controlling IL-12 expression to the tumor environment. Mol Ther 2011;19:751-9.
66. Kerkar SP, Goldszmid RS, Muranski P, Chinnasamy D, Yu Z, Reger RN, et al. IL-12 triggers a programmatic change in dysfunctional myeloid-derived cells within mouse tumors. J Clin Invest 2011;121:4746-57.
67. Matzinger P. The danger model: a renewed sense of self. Science 2002;296:301-5. (Pubitemid 34303674)
68. Pegram HJ, Lee JC, Hayman EG, Imperato GH, Tedder TF, Sadelain M, et al. Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning. Blood 2012;119:4133-41.
69. Chinnasamy D, Yu Z, Kerkar SP, Zhang L, Morgan RA, Restifo NP, et al. Local delivery of interleukin-12 using T cells targeting VEGF receptor-2 eradicates multiple vascularized tumors in mice. Clin Cancer Res 2012;18:1672-83.
70. Chinnasamy D, Yu Z, Theoret MR, Zhao Y, Shrimali RK, Morgan RA, et al. Gene therapy using genetically modified lymphocytes targeting VEGFR-2 inhibits the growth of vascularized syngenic tumors in mice. J Clin Invest 2010;120:3953-68.
71. Kraman M, Bambrough PJ, Arnold JN, Roberts EW, Magiera L, Jones JO, et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 2010;330:827-30.