Myeloid-Derived Cells in Tumors: Effects of Radiation

Seminars in Radiation Oncology

Volumn 25, Issue 1, 2015, Pages 18-27

  Vatner, Ralph E ^a   Formenti, Silvia C ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MARROW CELL; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL STRESS; DENDRITIC CELL; HUMAN; IONIZING RADIATION; MACROPHAGE; NEUTROPHIL; NONHUMAN; PHENOTYPE; RADIATION RESPONSE; REVIEW; SUPPRESSOR CELL; TUMOR MICROENVIRONMENT; NEOPLASMS; PATHOLOGY;

HUMANS; MYELOID CELLS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84919489041     PISSN: 10534296     EISSN: 15329461     Source Type: Journal    
DOI: 10.1016/j.semradonc.2014.07.008     Document Type: Review

References (108)

1. Balkwill F.R., Capasso M., Hagemann T. The tumor microenvironment at a glance. J Cell Sci 2012, 125:5591-5596.
2. Pietras K., Ostman A. Hallmarks of cancer: Interactions with the tumor stroma. Exp Cell Res 2010, 316:1324-1331.
3. Gajewski T.F., Schreiber H., Fu Y.-X. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013, 14:1014-1022.
4. Hanahan D., Coussens L.M. Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
5. Gajewski T.F., Meng Y., Blank C., et al. Immune resistance orchestrated by the tumor microenvironment. Immunol Rev 2006, 213:131-145.
6. Geissmann F., Gordon S., Hume D.A., et al. Unravelling mononuclear phagocyte heterogeneity. Nat Rev Immunol 2010, 10:453-460.
7. Solito S., Pinton L., Damuzzo V., et al. Highlights on molecular mechanisms of MDSC-mediated immune suppression: Paving the way for new working hypotheses. Immunol Invest 2014, 41:722-737.
8. Sica A., Porta C., Morlacchi S., et al. Origin and functions of tumor-associated myeloid cells (TAMCs). Cancer Microenviron 2012, 5:133-149.
9. Becker J.C. Tumor-educated myeloid cells: Impact the micro- and macroenvironment. Exp Dermatol 2014, 23:157-158.
10. Ostrand-Rosenberg S., Sinha P., Beury D.W., et al. Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin Cancer Biol 2012, 22:275-281.
11. + T-cell activation events. Eur J Immunol 2013, 43:2930-2942.
12. McDonnell A.M., Robinson B.W.S., Currie A.J. Tumor antigen cross-presentation and the dendritic cell: Where it all begins?. Clin Dev Immunol 2010, 2010:539519.
13. Huang A.Y., Golumbek P., Ahmadzadeh M., et al. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science 1994, 264:961-965.
14. + T cells by exogenous cell-associated antigens. Immunity 2002, 17:211-220.
15. Gabrilovich D. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 2004, 4:941-952.
16. Cuenca A., Cheng F., Wang H., et al. Extra-lymphatic solid tumor growth is not immunologically ignored and results in early induction of antigen-specific T-cell anergy: Dominant role of cross-tolerance to tumor antigens. Cancer Res 2003, 63:9007-9015.
17. Staveley-O'Carroll K., Sotomayor E., Montgomery J., et al. Induction of antigen-specific T cell anergy: An early event in the course of tumor progression. Proc Natl Acad Sci U S A 1998, 95:1178-1183.
18. Chaput N., Conforti R., Viaud S., et al. The Janus face of dendritic cells in cancer. Oncogene 2008, 27:5920-5931.
19. Qian B.-Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
20. Condeelis J., Pollard J.W. Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006, 124:263-266.
21. Pollard J.W. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 2004, 4:71-78.
22. Mantovani A., Sica A. Macrophages, innate immunity and cancer: Balance, tolerance, and diversity. Curr Opin Immunol 2010, 22:231-237.
23. Smyth M.J., Godfrey D.I., Trapani J.A. A fresh look at tumor immunosurveillance and immunotherapy. Nat Immunol 2001, 2:293-299.
24. Dunn G.P., Koebel C.M., Schreiber R.D. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006, 6:836-848.
25. Prestwich R.J., Errington F., Hatfield P., et al. The immune system-Is it relevant to cancer development, progression and treatment?. Clin Oncol (R Coll Radiol) 2008, 20:101-112.
26. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011, 11:723-737.
27. Allavena P., Mantovani A. Immunology in the clinic review series; focus on cancer: Tumour-associated macrophages: Undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 2012, 167:195-205.
28. Sica A., Mantovani A. Macrophage plasticity and polarization: In vivo veritas. J Clin Invest 2012, 122:787-795.
29. Van Overmeire E., Laoui D., Keirsse J., et al. Mechanisms driving macrophage diversity and specialization in distinct tumor microenvironments and parallelisms with other tissues. Front Immunol 2014, 5:127.
30. Gabrilovich D.I., Ostrand-Rosenberg S., Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012, 12:253-268.
31. Rodríguez P.C., Quiceno D.G., Zabaleta J., et al. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res 2004, 64:5839-5849.
32. Rodríguez P.C., Quiceno D.G., Ochoa A.C. l-Arginine availability regulates T-lymphocyte cell-cycle progression. Blood 2007, 109:1568-1573.
33. Doedens A.L., Stockmann C., Rubinstein M.P., et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res 2010, 70:7465-7475.
34. Movahedi K., Laoui D., Gysemans C., et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Re 2010, 70:5728-5739.
35. Aoe T., Okamoto Y., Saito T. Activated macrophages induce structural abnormalities of the T cell receptor-CD3 complex. J Exp Med 1995, 181:1881-1886.
36. Fridlender Z.G., Albelda S.M. Tumor-associated neutrophils: Friend or foe?. Carcinogenesis 2012, 33:949-955.
37. Otsuji M., Kimura Y., Aoe T., et al. Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 zeta chain of T-cell receptor complex and antigen-specific T-cell responses. Proc Natl Acad Sci U S A 1996, 93:13119-13124.
38. Mishalian I., Bayuh R., Levy L., et al. Tumor-associated neutrophils (TAN) develop pro-tumorigenic properties during tumor progression. Cancer Immunol Immunother 2013, 62:1745-1756.
39. Fridlender Z.G., Sun J., Kim S., et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 2009, 16:183-194.
40. Lu T., Ramakrishnan R., Altiok S., et al. Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J Clin Invest 2011, 121:4015-4029.
41. Molon B., Ugel S., Del Pozzo F., et al. Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. J Exp Med 2011, 208:1949-1962.
42. Bingisser R.M., Tilbrook P.A., Holt P.G., et al. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J Immunol 1998, 160:5729-5734.
43. Curiel T.J., Coukos G., Zou L., et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004, 10:942-949.
44. Fidler I.J., Schroit A.J. Recognition and destruction of neoplastic cells by activated macrophages: Discrimination of altered self. Biochim Biophys Acta 1988, 948:151-173.
45. Mantovani A., Caprioli V., Gritti P., et al. Human mature macrophages mediate antibody-dependent cellular cytotoxicity on tumour cells. Transplantation 1977, 24:291-293.
46. Mills C.D., Shearer J., Evans R., et al. Macrophage arginine metabolism and the inhibition or stimulation of cancer. J Immunol 1992, 149:2709-2714.
47. Mills C.D., Kincaid K., Alt J.M., et al. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol 2000, 164:6166-6173.
48. Edin S., Wikberg M.L., Dahlin A.M., et al. The distribution of macrophages with a M1 or M2 phenotype in relation to prognosis and the molecular characteristics of colorectal cancer. PLoS One 2012, 7:e47045.
49. Zhang M., He Y., Sun X., et al. A high M1/M2 ratio of tumor-associated macrophages is associated with extended survival in ovarian cancer patients. J Ovarian Res 2014, 7:19.
50. Ma J., Liu L., Che G., et al. The M1 form of tumor-associated macrophages in non-small cell lung cancer is positively associated with survival time. BMC Cancer 2010, 10:112.
51. Thomsen L.L., Miles D.W. Role of nitric oxide in tumour progression: Lessons from human tumours. Cancer Metastasis Rev 1998, 17:107-118.
52. Lala P.K., Orucevic A. Role of nitric oxide in tumor progression: Lessons from experimental tumors. Cancer Metastasis Rev 1998, 17:91-106.
53. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009, 9:162-174. (Available at:). http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=19197294&retmode=ref&cmd=prlinks.
54. Dudziak D., Kamphorst A.O., Heidkamp G.F., et al. Differential antigen processing by dendritic cell subsets in vivo. Science 2007, 315:107-111.
55. Villadangos J.A., Schnorrer P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 2007, 7:543-555.
56. Shortman K., Liu Y.-J. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2002, 2:151-161.
57. Gresser I., Belardelli F., Maury C., et al. Injection of mice with antibody to interferon enhances the growth of transplantable murine tumors. J Exp Med 1983, 158:2095-2107.
58. Picaud S., Bardot B., De Maeyer E., et al. Enhanced tumor development in mice lacking a functional type I interferon receptor. J Interferon Cytokine Res 2002, 22:457-462.
59. Dunn G.P., Bruce A.T., Sheehan K.C.F., et al. A critical function for type I interferons in cancer immunoediting. Nat Immunol 2005, 6:722-729.
60. Diamond M.S., Kinder M., Matsushita H., et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011, 208:1989-2003.
61. + T cell responses through CD8{alpha}+ dendritic cells. J Exp Med 2011, 208:2005-2016.
62. Honda K., Yanai H., Negishi H., et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777.
63. Takagi H., Fukaya T., Eizumi K., et al. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 2011, 35:958-971.
64. Seliger B., Massa C. The dark side of dendritic cells: Development and exploitation of tolerogenic activity that favor tumor outgrowth and immune escape. Front Immunol 2013, 4:419.
65. Zhong H., Gutkin D.W., Han B., et al. Origin and pharmacological modulation of tumor-associated regulatory dendritic cells. Int J Cancer 2014, 134:2633-2645.
66. Brandau S., Moses K., Lang S. The kinship of neutrophils and granulocytic myeloid-derived suppressor cells in cancer: Cousins, siblings or twins?. Semin Cancer Biol 2013, 23:171-182.
67. Fridlender Z.G., Sun J., Mishalian I., et al. Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS One 2012, 7:e31524.
68. Ohno Y., Nakashima J., Ohori M., et al. Pretreatment neutrophil-to-lymphocyte ratio as an independent predictor of recurrence in patients with nonmetastatic renal cell carcinoma. J Urol 2010, 184:873-878.
69. Sharaiha R.Z., Halazun K.J., Mirza F., et al. Elevated preoperative neutrophil:lymphocyte ratio as a predictor of postoperative disease recurrence in esophageal cancer. Ann Surg Oncol 2011, 18:3362-3369.
70. Perisanidis C., Kornek G., Pöschl P.W., et al. High neutrophil-to-lymphocyte ratio is an independent marker of poor disease-specific survival in patients with oral cancer. Med Oncol 2013, 30:334.
71. Jiang N., Deng J.-Y., Liu Y., et al. The role of preoperative neutrophil-lymphocyte and platelet-lymphocyte ratio in patients after radical resection for gastric cancer. Biomarkers 2014, 19(6):444-451.
72. Schmielau J., Finn O.J. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res 2001, 61:4756-4760.
73. Peranzoni E., Zilio S., Marigo I., et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 2010, 22:238-244.
74. Montero A.J., Diaz-Montero C.M., Kyriakopoulos C.E., et al. Myeloid-derived suppressor cells in cancer patients: A clinical perspective. J Immunother 2012, 35:107-115.
75. Nagaraj S., Gabrilovich D.I. Myeloid-derived suppressor cells in human cancer. Cancer J 2010, 16:348-353.
76. Dolcetti L., Peranzoni E., Ugel S., et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 2010, 40:22-35.
77. Youn J.-I., Nagaraj S., Collazo M., et al. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008, 181:5791-5802.
78. Ochoa A.C., Zea A.H., Hernandez C., et al. Arginase, prostaglandins, and myeloid-derived suppressor cells in renal cell carcinoma. Clin Cancer Res 2007, 13:721s-726s.
79. Meyer C., Cagnon L., Costa-Nunes C.M., et al. Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab. Cancer Immunol Immunother 2014, 63:247-257.
80. Bronte V., Serafini P., De Santo C., et al. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J Immunol 2003, 170:270-278.
81. + T cell tolerance in cancer. Nat Med 2007, 13:828-835.
82. + myeloid cells. Cancer Res 2006, 66:6807-6815.
83. Serafini P., Mgebroff S., Noonan K., et al. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res 2008, 68:5439-5449.
84. Movahedi K., Guilliams M., Van den Bossche J., et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008, 111:4233-4244.
85. Gough M.J., Young K., Crittenden M. The impact of the myeloid response to radiation therapy. Clin Dev Immunol 2013, 2013:281958.
86. Toivonen P., Kivelä T. Infiltrating macrophages in extratumoural tissues after brachytherapy of uveal melanoma. Acta Ophthalmol 2012, 90:341-349.
87. Julow J., Szeifert G.T., Bálint K., et al. The role of microglia/macrophage system in the tissue response to I-125 interstitial brachytherapy of cerebral gliomas. Neurol Res 2007, 29:233-238.
88. Crittenden M.R., Cottam B., Savage T., et al. Expression of NF-κB p50 in tumor stroma limits the control of tumors by radiation therapy. PLoS One 2012, 7:e39295.
89. Chiang C.-S., Fu S.Y., Wang S.-C., et al. Irradiation promotes an m2 macrophage phenotype in tumor hypoxia. Front Oncol 2012, 2:89.
90. Ahn G.-O., Tseng D., Liao C.-H., et al. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci U S A 2010, 107:8363-8368.
91. Lugade A.A., Moran J.P., Gerber S.A., et al. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol 2005, 174:7516-7523.
92. Xu J., Escamilla J., Mok S., et al. CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer. Cancer Res 2013, 73:2782-2794.
93. Kioi M., Vogel H., Schultz G., et al. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J Clin Invest 2010, 120:694-705.
94. Ceradini D.J., Kulkarni A.R., Callaghan M.J., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004, 10:858-864.
95. Kozin S.V., Kamoun W.S., Huang Y., et al. Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res 2010, 70:5679-5685.
96. Deng L., Liang H., Burnette B., et al. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest 2014, 124:687-695.
97. Crittenden M.R., Savage T., Cottam B., et al. The peripheral myeloid expansion driven by murine cancer progression is reversed by radiation therapy of the tumor. PLoS One 2013, 8:e69527.
98. Chen F.-H., Chiang C.-S., Wang C.-C., et al. Radiotherapy decreases vascular density and causes hypoxia with macrophage aggregation in TRAMP-C1 prostate tumors. Clin Cancer Res 2009, 15:1721-1729.
99. Cavnar M.J., Zeng S., Kim T.S., et al. KIT oncogene inhibition drives intratumoral macrophage M2 polarization. J Exp Med 2013, 210:2873-2886.
100. Tsai C.-S., Tsai C.-S., Chen F.-H., et al. Macrophages from irradiated tumors express higher levels of iNOS, arginase-I and COX-2, and promote tumor growth. Int J Radiat Oncol Biol Phys 2007, 68:499-507.
101. +/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 2013, 24:589-602.
102. Wunderlich R., Ernst A., Rödel F., et al. Low and moderate dose of ionising radiation up to 2Gy modulates transmigration and chemotaxis of activated macrophages, provokes an anti-inflammatory cytokine milieu, but does not impact on viability and phagocytic function. Clin Exp Immunol 2014, Epub ahead of print.
103. Heath W.R., Belz G.T., Behrens G.M.N., et al. Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev 2004, 199:9-26.
104. + T cells: Changing strategies for cancer treatment. Blood 2009, 114:589-595.
105. Teitz-Tennenbaum S., Li Q., Okuyama R., et al. Mechanisms involved in radiation enhancement of intratumoral dendritic cell therapy. J Immunother 2008, 31:345-358.
106. Zhang B., Bowerman N.A., Salama J.K., et al. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med 2007, 204:49-55.
107. Ahn G.-O., Brown J.M. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: Role of bone marrow-derived myelomonocytic cells. Cancer Cell 2008, 13:193-205.
108. Burnette B.C., Liang H., LEE Y., et al. The efficacy of radiotherapy relies upon induction of type I interferon-dependent innate and adaptive immunity. Cancer Res 2011, 71:2488-2496.