Myeloid-derived suppressor cells in cancer: Therapeutic, predictive, and prognostic implications

Seminars in Oncology

Volumn 41, Issue 2, 2014, Pages 174-184

  Diaz Montero, C Marcela ^a   Finke, Jim ^a   Montero, Alberto J ^b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b TAUSSIG CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CANCER THERAPY; DISEASE MARKER; GENETIC TRANSCRIPTION; GRANULOCYTE; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; METASTASIS; MONOCYTE; MYELOID DERIVED SUPPRESSOR CELL; PHENOTYPE; PRIORITY JOURNAL; PROMYELOCYTE; SUPPRESSOR CELL; TUMOR IMMUNITY;

ANIMALS; BONE MARROW CELLS; DISEASE PROGRESSION; GRANULOCYTES; HUMANS; IMMUNE SYSTEM; IMMUNOSUPPRESSION; IMMUNOTHERAPY; MICE; MONOCYTES; MYELOID CELLS; NEOPLASM METASTASIS; NEOPLASMS; PHENOTYPE; PROGNOSIS; STEM CELLS; TUMOR ESCAPE; TUMOR MICROENVIRONMENT;

EID: 84899709874     PISSN: 00937754     EISSN: 15328708     Source Type: Journal    
DOI: 10.1053/j.seminoncol.2014.02.003     Document Type: Article

References (72)

1. C.U. Blank The perspective of immunotherapy: new molecules and new mechanisms of action in immune modulation Curr Opin Oncol 26 2 2014 204 214
2. C. Kyi, and M.A. Postow Checkpoint blocking antibodies in cancer immunotherapy FEBS Lett 588 2014 368 376
3. O. Hamid, C. Robert, A. Daud, F.S. Hodi, W.J. Hwu, and R. Kefford et al. Safety and tumor responses with lambrolizumab (anti-pd-1) in melanoma N Engl J Med 369 2013 134 144
4. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
5. Y.G. Najjar, and J.H. Finke Clinical perspectives on targeting of myeloid derived suppressor cells in the treatment of cancer Front Oncol 3 2013 49
6. D.I. Gabrilovich, V. Bronte, S.H. Chen, M.P. Colombo, A. Ochoa, and S. Ostrand-Rosenberg et al. The terminology issue for myeloid-derived suppressor cells Cancer Res 67 2007 425
7. D.I. Gabrilovich, and S. Nagaraj Myeloid-derived suppressor cells as regulators of the immune system Nat Rev Immunol 9 2009 162 174
8. A.J. Montero, C.M. Diaz-Montero, C.E. Kyriakopoulos, V. Bronte, and S. Mandruzzato Myeloid-derived suppressor cells in cancer patients: a clinical perspective J Immunother 35 2012 107 115
9. S. Ostrand-Rosenberg Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity Cancer Immunol Immunother 59 2010 1593 1600
10. D.I. Gabrilovich, S. Ostrand-Rosenberg, and V. Bronte Coordinated regulation of myeloid cells by tumours Nat Rev Immunol 12 2012 253 268
11. F. Balkwill, and A. Mantovani Inflammation and cancer: back to Virchow? Lancet 357 2001 539 545
12. J. Finke, J. Ko, B. Rini, P. Rayman, J. Ireland, and P. Cohen Mdsc as a mechanism of tumor escape from sunitinib mediated anti-angiogenic therapy Int Immunopharmacol 11 2011 856 861
13. C.A. Corzo, M.J. Cotter, P. Cheng, F. Cheng, S. Kusmartsev, and E. Sotomayor et al. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells J Immunol 182 2009 5693 5701
14. P. Serafini, S. Mgebroff, K. Noonan, and I. Borrello Myeloid-derived suppressor cells promote cross-tolerance in b-cell lymphoma by expanding regulatory t cells Cancer Res 68 2008 5439 5449
15. P.C. Rodriguez, D.G. Quiceno, and A.C. Ochoa L-arginine availability regulates t-lymphocyte cell-cycle progression Blood 109 2007 1568 1573
16. P.C. Rodriguez, A.H. Zea, K.S. Culotta, J. Zabaleta, J.B. Ochoa, and A.C. Ochoa Regulation of t cell receptor cd3zeta chain expression by l-arginine J Biol Chem 277 2002 21123 21129
17. P.C. Rodriguez, and A.C. Ochoa Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives Immunol Rev 222 2008 180 191
18. E. Eruslanov, M. Neuberger, I. Daurkin, G.Q. Perrin, C. Algood, and P. Dahm et al. Circulating and tumor-infiltrating myeloid cell subsets in patients with bladder cancer Int J Cancer 130 2012 1109 1119
19. R.F. Gabitass, N.E. Annels, D.D. Stocken, H.A. Pandha, and G.W. Middleton Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the th2 cytokine interleukin-13 Cancer Immunol Immunother 60 2011 1419 1430
20. S. Solito, E. Falisi, C.M. Diaz-Montero, A. Doni, L. Pinton, and A. Rosato et al. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells Blood 118 2011 2254 2265
21. A.J. Montero, C.M. Diaz-Montero, Y.E. Deutsch, J. Hurley, L.G. Koniaris, and T. Rumboldt et al. Phase 2 study of neoadjuvant treatment with nov-002 in combination with doxorubicin and cyclophosphamide followed by docetaxel in patients with her-2 negative clinical stage ii-iiic breast cancer Breast Cancer Res Treat 132 2012 215 223
22. C.M. Diaz-Montero, M.L. Salem, M.I. Nishimura, E. Garrett-Mayer, D.J. Cole, and A.J. Montero Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy Cancer Immunol Immunother 58 2009 49 59
23. J.A. Joyce, and J.W. Pollard Microenvironmental regulation of metastasis Nat Rev Cancer 9 2009 239 252
24. J.P. Sleeman The metastatic niche and stromal progression Cancer Metastasis Rev 31 2012 429 440
25. V. Umansky, and A. Sevko Tumor microenvironment and myeloid-derived suppressor cells Cancer Microenvironment 6 2013 169 177
26. S. Ugel, F. Delpozzo, G. Desantis, F. Papalini, F. Simonato, and N. Sonda et al. Therapeutic targeting of myeloid-derived suppressor cells Curr Opin Pharmacol 9 2009 470 481
27. V. Bronte Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions Eur J Immunol 39 2009 2670 2672
28. S. Nagaraj, K. Gupta, V. Pisarev, L. Kinarsky, S. Sherman, and L. Kang et al. Altered recognition of antigen is a mechanism of cd8+ t cell tolerance in cancer Nat Med 13 2007 828 835
29. J.I. Youn, S. Nagaraj, M. Collazo, and D.I. Gabrilovich Subsets of myeloid-derived suppressor cells in tumor-bearing mice J Immunol 181 2008 5791 5802
30. A. Kotsakis, M. Harasymczuk, B. Schilling, V. Georgoulias, A. Argiris, and T.L. Whiteside Myeloid-derived suppressor cell measurements in fresh and cryopreserved blood samples J Immunol Methods 381 2012 14 22
31. T.L. Whiteside Disarming suppressor cells to improve immunotherapy Cancer Immunol Immunother 61 2012 283 288
32. S. Kusmartsev, Y. Nefedova, D. Yoder, and D.I. Gabrilovich Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species J Immunol 172 2004 989 999
33. Dolcetti L, Peranzoni E, Bronte V. Measurement of myeloid cell immune suppressive activity. Curr Protoc Immunol. 2010;Chapter 14 Unit 14:17
34. G. Gallina, L. Dolcetti, P. Serafini, C. De Santo, I. Marigo, and M.P. Colombo et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells J Clin Invest 116 2006 2777 2790
35. L. Dolcetti, E. Peranzoni, S. Ugel, I. Marigo, A. Fernandez Gomez, and C. Mesa et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by gm-csf Eur J Immunol 40 2010 22 35
36. I. Marigo, E. Bosio, S. Solito, C. Mesa, A. Fernandez, and L. Dolcetti et al. Tumor-induced tolerance and immune suppression depend on the c/ebpbeta transcription factor Immunity 32 2010 790 802
37. P. Cheng, A. Zlobin, V. Volgina, S. Gottipati, B. Osborne, and E.J. Simel et al. Notch-1 regulates nf-kappab activity in hemopoietic progenitor cells J Immunol 167 2001 4458 4467
38. D.R. Gibb, S.J. Saleem, D.J. Kang, M.A. Subler, and D.H. Conrad Adam10 overexpression shifts lympho- and myelopoiesis by dysregulating site 2/site 3 cleavage products of notch J Immunol 186 2011 4244 4252
39. P. Cheng, V. Kumar, H. Liu, J.I. Youn, M. Fishman, S. Sherman, and D. Gabrilovich Effects of notch signaling on regulation of myeloid cell differentiation in cancer Cancer Res 74 2014 141 152
40. H. Yu, D. Pardoll, and R. Jove Stats in cancer inflammation and immunity: a leading role for stat3 Nat Rev Cancer 9 2009 798 809
41. I. Poschke, D. Mougiakakos, J. Hansson, G.V. Masucci, and R. Kiessling Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are STAT3hi and overexpress CD80, CD83, and DC-sign Cancer Res 70 2010 4335 4345
42. P. Cheng, C.A. Corzo, N. Luetteke, B. Yu, S. Nagaraj, and M.M. Bui et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by s100a9 protein J Exp Med 205 2008 2235 2249
43. P. Sinha, C. Okoro, D. Foell, H.H. Freeze, S. Ostrand-Rosenberg, and G. Srikrishna Proinflammatory s100 proteins regulate the accumulation of myeloid-derived suppressor cells J Immunol 181 2008 4666 4675
44. S. Kusmartsev, and D.I. Gabrilovich Stat1 signaling regulates tumor-associated macrophage-mediated T cell deletion J Immunol 174 2005 4880 4891
45. K. Movahedi, M. Guilliams, J. Van den Bossche, R. Van den Bergh, C. Gysemans, and A. Beschin et al. Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity Blood 111 2008 4233 4244
46. V. Bronte, P. Serafini, C. De Santo, I. Marigo, V. Tosello, and A. Mazzoni et al. Il-4-induced arginase 1 suppresses alloreactive t cells in tumor-bearing mice J Immunol 170 2003 270 278
47. A.S. Pak, M.A. Wright, J.P. Matthews, S.L. Collins, G.J. Petruzzelli, and M.R. Young Mechanisms of immune suppression in patients with head and neck cancer: presence of CD34(+) cells which suppress immune functions within cancers that secrete granulocyte-macrophage colony-stimulating factor Clin Cancer Res 1 1995 95 103
48. B. Almand, J.I. Clark, E. Nikitina, J. van Beynen, N.R. English, and S.C. Knight et al. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer J Immunol 166 2001 678 689
49. B. Zhang, Z. Wang, L. Wu, M. Zhang, W. Li, J. Ding, J. Zhu, H. Wei, and K. Zhao Circulating and tumor-infiltrating myeloid-derived suppressor cells in patients with colorectal carcinoma PLoS One 8 2013 e57114
50. B. Raychaudhuri, P. Rayman, J. Ireland, J. Ko, B. Rini, and E.C. Borden et al. Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma Neurooncology 13 2011 591 599
51. S. Walter, T. Weinschenk, A. Stenzl, R. Zdrojowy, A. Pluzanska, and C. Szczylik et al. Multipeptide immune response to cancer vaccine ima901 after single-dose cyclophosphamide associates with longer patient survival Nat Med 18 2012 1254 1261
52. F. Arihara, E. Mizukoshi, M. Kitahara, Y. Takata, K. Arai, and T. Yamashita et al. Increase in CD14+HLA-DR-/low myeloid-derived suppressor cells in hepatocellular carcinoma patients and its impact on prognosis Cancer Immunol Immunother 62 2013 1421 1430
53. A. Huang, B. Zhang, B. Wang, F. Zhang, K.X. Fan, and Y.J. Guo Increased CD14(+)HLA-DR (-/low) myeloid-derived suppressor cells correlate with extrathoracic metastasis and poor response to chemotherapy in non-small cell lung cancer patients Cancer Immunol Immunother 62 2013 1439 1451
54. A.H. Zea, P.C. Rodriguez, M.B. Atkins, C. Hernandez, S. Signoretti, and J. Zabaleta et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion Cancer Res 65 2005 3044 3048
55. L. Wang, E.W. Chang, S.C. Wong, S.M. Ong, D.Q. Chong, and K.L. Ling Increased myeloid-derived suppressor cells in gastric cancer correlate with cancer stage and plasma s100a8/a9 proinflammatory proteins J Immunol 190 2013 794 804
56. B.L. Mundy-Bosse, G.S. Young, T. Bauer, E. Binkley, M. Bloomston, and M.A. Bill et al. Distinct myeloid suppressor cell subsets correlate with plasma IL-6 and IL-10 and reduced interferon-alpha signaling in CD4(+) T cells from patients with GI malignancy Cancer Immunol Immunother 60 2011 1269 1279
57. H.L. Kaufman, D.W. Kim, G. DeRaffele, J. Mitcham, R.S. Coffin, and S. Kim-Schulze Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage IIIC and IV melanoma Ann Surg Oncol 17 2010 718 730
58. M.R. Porembka, J.B. Mitchem, B.A. Belt, C.S. Hsieh, and H.M. Lee et al. Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth Cancer Immunol Immunother 61 2012 1373 1385
59. T.X. Cui, I. Kryczek, L. Zhao, E. Zhao, R. Kuick, and M.H. Roh et al. Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing microrna101 and suppressing the corepressor ctbp2 Immunity 39 2013 611 621
60. S.E. Finkelstein, T. Carey, I. Fricke, D. Yu, D. Goetz, and M. Gratz et al. Changes in dendritic cell phenotype after a new high-dose weekly schedule of interleukin-2 therapy for kidney cancer and melanoma J Immunother 33 2010 817 827
61. T. Kimura, J.R. McKolanis, L.A. Dzubinski, K. Islam, D.M. Potter, and A.M. Salazar et al. Muc1 vaccine for individuals with advanced adenoma of the colon: a cancer immunoprevention feasibility study Cancer Prev Res (Phila) 6 2013 18 26
62. C. Murdoch, M. Muthana, S.B. Coffelt, and C.E. Lewis The role of myeloid cells in the promotion of tumour angiogenesis Nature Rev Cancer 8 2008 618 631
63. B. Toh, X. Wang, J. Keeble, W.J. Sim, K. Khoo, and W.C. Wong et al. Mesenchymal transition and dissemination of cancer cells is driven by myeloid-derived suppressor cells infiltrating the primary tumor PLoS Biol 9 2011 e1001162
64. L. Yang, L.M. DeBusk, K. Fukuda, B. Fingleton, B. Green-Jarvis, and Y. Shyr et al. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis Cancer Cell 6 2004 409 421
65. L. Yang, J. Huang, X. Ren, A.E. Gorska, A. Chytil, and M. Aakre et al. Abrogation of tgf beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis Cancer Cell 13 2008 23 35
66. G.O. Ahn, and J.M. Brown Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells Cancer Cell 13 2008 193 205
67. H. Zhang, I. Maric, M.J. DiPrima, J. Khan, R.J. Orentas, R.N. Kaplan, and C.L. Mackall Fibrocytes represent a novel mdsc subset circulating in patients with metastatic cancer Blood 122 2013 1105 1113
68. C.A. Corzo, T. Condamine, L. Lu, M.J. Cotter, J.I. Youn, and P. Cheng et al. Hif-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment J Exp Med 207 2010 2439 2453
69. A. Sawant, J. Deshane, J. Jules, C.M. Lee, B.A. Harris, and X. Feng et al. Myeloid-derived suppressor cells function as novel osteoclast progenitors enhancing bone loss in breast cancer Cancer Res 73 2013 672 682
70. A. Sawant, and S. Ponnazhagan Myeloid-derived suppressor cells as osteoclast progenitors: a novel target for controlling osteolytic bone metastasis Cancer Res 73 2013 4606 4610
71. H.H. Yan, M. Pickup, Y. Pang, A.E. Gorska, Z. Li, and A. Chytil et al. Gr-1+CD11b+ myeloid cells tip the balance of immune protection to tumor promotion in the premetastatic lung Cancer Res 70 2010 6139 6149
72. I. Daurkin, E. Eruslanov, J. Vieweg, and S. Kusmartsev Generation of antigen-presenting cells from tumor-infiltrated cd11b myeloid cells with DNA demethylating agent 5-aza-2'-deoxycytidine Cancer Immunol Immunother 59 2010 697 706