Immunomodulatory effects of myeloid-derived suppressor cells in diseases: Role in cancer and infections

Immunobiology

Volumn 223, Issue 4-5, 2018, Pages 432-442

  Tamadaho, Ruth S E ^a   Hoerauf, Achim ^a,b   Layland, Laura E ^a,b  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b German Centre for Infection Research (DZIF)   (Germany)

Author keywords

Cytokine; Immune mechanism; Immune regulation; Infection; Inflammation; MDSC

Indexed keywords

NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; STAT PROTEIN; CYTOKINE;

ALLERGY; AUTOIMMUNITY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CELL ACTIVATION; CELL ACTIVITY; CELL EXPANSION; CELL FATE; CELL MATURATION; HUMAN; IMMUNOMODULATION; INFECTION; MALIGNANT NEOPLASM; MAST CELL; MYELOID-DERIVED SUPPRESSOR CELL; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SEPSIS; TLR SIGNALING; TREATMENT PLANNING; ANIMAL; CELLULAR IMMUNITY; IMMUNOLOGY; METABOLISM; MONOCYTE; NEOPLASM;

ANIMALS; CYTOKINES; HUMANS; IMMUNITY, CELLULAR; IMMUNOMODULATION; INFECTION; MONOCYTES; MYELOID-DERIVED SUPPRESSOR CELLS; NEOPLASMS; T-LYMPHOCYTES, REGULATORY;

EID: 85037720481     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2017.07.001     Document Type: Review

References (133)

1. Albeituni, S.H., Ding, C., Yan, J., Hampering immune suppressors: therapeutic targeting of myeloid-derived suppressor cells in cancer. Cancer J. 19 (2013), 490–501.
2. Almand, B., Resser, J.R., Lindman, B., Nadaf, S., Clark, J.I., Kwon, E.D., Carbone, D.P., Gabrilovich, D.I., Clinical significance of defective dendritic cell differentiation in cancer. Clin. Cancer Res. 6 (2000), 1755–1766.
3. Almand, B., Clark, J.I., Nikitina, E., van Beynen, J., English, N.R., Knight, S.C., Carbone, D.P., Gabrilovich, D.I., Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 166 (2001), 678–689.
4. −/low myeloid-derived suppressor cells in hepatocellular carcinoma patients and its impact on prognosis. Cancer Immunol. Immunother. 62 (2013), 1421–1430.
5. + non-migratory myeloid cells suppress Th2 effector function in the lung. Mucosal Immunol. 3 (2010), 578–593.
6. Ba, H., Li, B., Li, X., Li, C., Feng, A., Zhu, Y., Wang, J., Li, Z., Yin, B., Transmembrane tumor necrosis factor-alpha promotes the recruitment of MDSCs to tumor tissue by upregulating CXCR4 expression via TNFR2. Int. Immunopharmacol. 44 (2017), 143–152.
7. Bobé P., Benihoud, K., Grandjon, D., Opolon, P., Pritchard, L.L., Huchet, R., Nitric oxide mediation of active immunosuppression associated with graft-Versus-Host reaction. Blood 94 (1999), 1028–1037.
8. Brandau, S., Trellakis, S., Bruderek, K., Schmaltz, D., Steller, G., Elian, M., Suttmann, H., Schenck, M., Welling, J., Zabel, P., Lang, S., Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J. Leukoc. Biol. 89 (2011), 311–317.
9. Bronte, V., Chappell, D.B., Apolloni, E., Cabrelle, A., Wang, M., Hwu, P., Restifo, N.P., Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation. J. Immunol. 162 (1999), 5728–5737.
10. Bronte, V., Brandau, S., Chen, S.H., Colombo, M.P., Frey, A.B., Greten, T.F., Mandruzzato, S., Murray, P.J., Ochoa, A., Ostrand-Rosenberg, S., Rodriguez, P.C., Sica, A., Umansky, V., Vonderheide, R.H., Gabrilovich, D.I., Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat. Commun., 7, 2016, 12150.
11. Bunt, S.K., Sinha, P., Clements, V.K., Leips, J., Ostrand-Rosenberg, S., Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 176 (2006), 284–290.
12. Bunt, S.K., Yang, L., Sinha, P., Clements, V.K., Leips, J., 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.
13. Bunt, S.K., Clements, V.K., Hanson, E.M., Sinha, P., Ostrand-Rosenberg, S., Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J. Leukoc. Biol. 85 (2009), 996–1004.
14. Cardillo, F., de Pinho, R.T., Antas, P.R.Z., Mengel, J., Immunity and immune modulation in Trypanosoma cruzi infection. FEMS Pathog. Dis., 73, 2015.
15. Cauley, L.S., Miller, E.E., Yen, M., Swain, S.L., Superantigen-induced CD4T cell tolerance mediated by myeloid cells and IFN-γ. J. Immunol. 165 (2000), 6056–6066.
16. Chalmin, F., Ladoire, S., Mignot, G., Vincent, J., Bruchard, M., Remy-Martin, J.P., Boireau, W., Rouleau, A., Simon, B., Lanneau, D., De Thonel, A., Multhoff, G., Hamman, A., Martin, F., Chauffert, B., Solary, E., Zitvogel, L., Garrido, C., Ryffel, B., Borg, C., Apetoh, L., Rébé C., Ghiringhelli, F., Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 120 (2010), 457–471.
17. Chen, X., Churchill, M.J., Nagar, K.K., Tailor, Y.H., Chu, T., Rush, B.S., Jiang, Z., Wang, E.B., Renz, B.W., Wang, H., Fung, M.C., Worthley, D.L., Mukherjee, S., Wang, T.C., IL-17 producing mast cells promote the expansion of myeloid-derived suppressor cells in a mouse allergy model of colorectal cancer. Oncotarget 6 (2015), 32966–32979.
18. Cherfils-Vicini, J., Platonova, S., Gillard, M., Laurans, L., Validire, P., Caliandro, R., Magdeleinat, P., Mami-Chouaib, F., Dieu-Nosjean, M.C., Fridman, W.H., Damotte, D., Sautès-Fridman, C., Cremer, I., Triggering of TLR7 and TLR8 expressed by human lung cancer cells induces cell survival and chemoresistance. J. Clin. Invest. 120 (2010), 1285–1297.
19. Condamine, T., Gabrilovich, D.I., Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 32 (2011), 19–25.
20. Corzo, C.A., Cotter, M.J., Cheng, P., Cheng, F., Kusmartsev, S., Sotomayor, T., McCaffrey, T.V., McCaffrey, J.C., Gabrilovich, D.I., Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J. Immunol. 182 (2009), 5693–5701.
21. Cripps, J.G., Wang, J., Maria, A., Blumenthal, I., Gorham, J.D., Type 1T helper cells induce the accumulation of myeloid-derived suppressor cells in the inflamed Tgfb1knockout mouse liver. Hepatology 52 (2010), 1350–1359.
22. Crook, K.R., Jin, M., Weeks, M.F., Rampersad, R.R., Baldi, R.M., Glekas, A.S., Shen, Y., Esserman, D.A., Little, P., Schwartz, T.A., Liu, P., Myeloid-derived suppressor cells regulate T cell and B cell responses during autoimmune disease. J. Leukoc. Biol. 97 (2015), 573–582.
23. Cui, T.X., Kryczek, I., Zhao, L., Zhao, E., Kuick, R., Roh, M.H., Vatan, L., Szeliga, W., Mao, Y., Thomas, D.G., Kotarski, J., Tarkowski, R., Wicha, M., Cho, K., Giordano, T., Liu, R., Zou, W., Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing MicroRNA101 and suppressing the corepressor CtBP2. Immunity 39 (2013), 611–621.
24. Dai, J., El Gazzar, M., Li, G.Y., Moorman, J.P., Yao, Z.Q., Myeloid-derived suppressor cells: paradoxical roles in infection and immunity. J. Innate. Immun. 7 (2015), 116–126.
25. Dajon, M., Iribarren, K., Cremer, I., Dual roles of TLR7 in the lung cancer microenvironment. Oncoimmunology, 4, 2015.
26. De Santo, C., Salio, M., Masri, S.H., Lee, L.Y.-H., Dong, T., Speak, A.O., Porubsky, S., Booth, S., Veerapen, N., Besra, G.S., Gröne, H.-J., Platt, F.M., Zambon, M., Cerundolo, V., Invariant NKT cells reduce the immunosuppressive activity of influenza A virus–induced myeloid-derived suppressor cells in mice and humans. J. Clin. Invest. 118 (2008), 4036–4048.
27. Dilek, N., de Silly, V.R., Blancho, G., Vanhove, B., Myeloid-derived suppressor cells: mechanisms of action and recent advances in their role in transplant tolerance. Front. Immunol. 3 (2012), 1–9.
28. Dolcetti, L., Peranzoni, E., Ugel, S., Marigo, I., Gomez, A.F., Mesa, C., Geilich, M., Winkels, G., Traggiai, E., Casati, A., Grassi, F., Bronte, V., Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur. J. Immunol. 40 (2010), 22–35.
29. Douguet, L., Bod, L., Lengagne, R., Labarthe, L., Kato, M., Avril, M.F., Prevost-Blondel, A., Nitric oxide synthase 2 is involved in the pro-tumorigenic potential of gamma delta 17 T cells in melanoma. Oncoimmunology, 5, 2016.
30. Dross, S.E., Munson, P.V., Kim, S.E., Bratt, D.L., Tunggal, H.C., Gervassi, A.L., Fuller, D.H., Horton, H., Kinetics of myeloid-derived suppressor cell frequency and function during simian immunodeficiency virus infection, combination antiretroviral therapy, and treatment interruption. J. Immunol. 198 (2017), 757–766.
31. Egelston, C., Kurkó J., Besenyei, T., Tryniszewska, B., Rauch, T.A., Glant, T.T., Mikecz, K., Suppression of dendritic cell maturation and T cell proliferation by synovial fluid myeloid cells from mice with autoimmune arthritis. Arthritis Rheumatol. 64 (2012), 3179–3188.
32. Fiorucci, S., Santucci, L., Antonelli, E., Distrutti, E., Del Sero, G., Morelli, O., Romani, L., Federici, B., Del Soldato, P., Morelli, A., NO-aspirin protects from T cell-mediated liver injury by inhibiting caspase-dependent processing of Th1-like cytokines. Gastroenterology 118 (2000), 404–421.
33. Gabitass, R.F., Annels, N.E., Stocken, D.D., Pandha, H.A., Middleton, G.W., 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.
34. Gabrilovich, D.I., Nagaraj, S., Myeloid-derived-suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9 (2009), 162–174.
35. Gabrilovich, D.I., Bronte, V., Chen, S.-H., Colombo, M.P., Ochoa, A., Ostrand-Rosenberg, S., Schreiber, H., The terminology issue for myeloid-derived suppressor cells. Cancer Res. 67 (2007), 425–426.
36. + T cells. J. Clin. Invest. 116 (2006), 2777–2790.
37. Gebhardt, C., Németh, J., Angel, P., Hess, J., S100A8 and S100A9 in inflammation and cancer. Biochem. Pharmacol. 72 (2006), 1622–1631.
38. Gebremeskel, S., Clattenburg, D.R., Slauenwhite, D., Lobert, L., Johnston, B., Natural killer T cell activation overcomes immunosuppression to enhance clearance of postsurgical breast cancer metastasis in mice. Oncoimmunology, 4, 2015.
39. Gehad, A.E., Lichtman, M.K., Schmults, C.D., Teague, J.E., Calarese, A.W., Jiang, Y., Watanabe, R., Clark, R.A., Nitric oxide-producing myeloid-derived suppressor cells inhibit vascular E-selectin expression in human squamous cell carcinomas. J. Invest. Dermatol. 132 (2012), 2642–2651.
40. Goedegebuure, P., Mitchem, J.B., Porembka, M.R., Tan, M.C., Belt, B.A., Wang-Gillam, A., Gillanders, W.E., Hawkins, W.G., Linehan, D.C., Myeloid-derived suppressor cells: general characteristics and relevance to clinical management of pancreatic cancer. Curr. Cancer Drug Targets 11 (2011), 734–751.
41. Gorden, K.B., Gorski, K.S., Gibson, S.J., Kedl, R.M., Kieper, W.C., Qiu, X., Tomai, M.A., Alkan, S.S., Vasilakos, J.P., Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol. 174 (2005), 1259–1268.
42. Green, K.A., Cook, W.J., Green, W.R., Myeloid-derived suppressor cells in murine retrovirus-induced AIDS inhibit T- and B-cell responses in vitro that are used to define the immunodeficiency. J. Virol. 87 (2013), 2058–2071.
43. Greenhough, A., Smartt, H.J.M., Moore, A.E., Roberts, H.R., Williams, A.C., Paraskeva, C., Kaidi, A., The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis 30 (2009), 377–386.
44. Grela, F., Aumeunier, A., Bardel, E., Van, L.P., Bourgeois, E., Vanoirbeek, J., Leite-de-Moraes, M., Schneider, E., Dy, M., Herbelin, A., Thieblemont, N., The TLR7 agonist R848 alleviates allergic inflammation by targeting invariant NKT cells to produce IFN-gamma. J. Immunol. 186 (2011), 284–290.
45. Groemping, Y., Rittinger, K., Activation and assembly of the NADPH oxidase: a structural perspective. Biochem. J. 386 (2005), 401–416.
46. Guilliams, M., Movahedi, K., Bosschaerts, T., VandenDriessche, T., Chuah, M.K., Hérin, M., Acosta-Sanchez, A., Ma, L., Moser, M., VanGinderachter, J.A., Brys, L., DeBaetselier, P., Beschin, A., IL-10 dampens TNF/inducible nitric oxide synthase-producing dendritic cells-mediated pathogenicity during parasite infection. J. Immunol. 182 (2009), 1107–1118.
47. Höchst, B., Mikulec, J., Baccega, T., Metzger, C., Welz, M., Peusquens, J., Tacke, F., Knolle, P., Kurts, C., Diehl, L., Ludwig-Portugall, I., Differential induction of Ly6G and Ly6C positive myeloid derived suppressor cells in chronic kidney and liver inflammation and fibrosis. PLoS One, 10, 2015.
48. Haile, L.A., Gamrekelashvili, J., Manns, M.P., Korangy, F., Greten, T.F., CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice. J. Immunol. 185 (2010), 203–210.
49. Ham, B., Wang, N., D'Costa, Z., Fernandez, M.C., Bourdeau, F., Auguste, P., Illemann, M., Eefsen, R.L., Hoyer-Hansen, G., Vainer, B., Evrard, M., Gao, Z.H., Brodt, P., TNF receptor-2 facilitates an immunosuppressive microenvironment in the liver to promote the colonization and growth of hepatic metastases. Cancer Res. 75 (2015), 5235–5247.
50. + T cells. J. Immunol. 183 (2009), 937–944.
51. Hegde, V.L., Tomar, S., Jackson, A., Rao, R., Yang, X., Singh, U.P., Singh, N.P., Nagarkatti, P.S., Nagarkatti, M., Distinct microRNA expression profile and targeted biological pathways in functional myeloid-derived suppressor cells induced by Δ9-tetrahydrocannabinol in vivo: regulation of CCAAT/enhancer-binding protein α by microRNA-690. J. Biol. Chem. 288 (2013), 36810–36826.
52. Hongo, D., Tang, X., Baker, J., Englemanand, E.G., Strober, S., Requirement for interactions of natural killer T cells and myeloid-derived suppressor cells for transplantation tolerance. Am. J. Transplant. 14 (2014), 2467–2477.
53. Horinaka, A., Sakurai, D., Ihara, F., Makita, Y., Kunii, N., Motohashi, S., Nakayama, T., Okamoto, Y., Invariant NKT cells are resistant to circulating CD15(+) myeloid-derived suppressor cells in patients with head and neck cancer. Cancer Sci. 107 (2016), 207–216.
54. Hossain, D.M., Pal, S.K., Moreira, D.F., Duttagupta, P., Zhang, Q., Won, H., Jones, J.O., D'Apuzzo, M., Forman, S.J., Kortylewski, M., TLR9-Targeted STAT3 silencing abrogates immunosuppressive activity of myeloid-derived suppressor cells from prostate cancer patients. Clin. Cancer Res. 21 (2015), 3771–3782.
55. Hu, X., Li, B., Xiaoyan, L., Zhao, X., Wan, L., Lin, G., Yu, M., Wang, J., Jiang, X., Feng, W., Zhihai, Q., Yin, B., Li, Z., Transmembrane TNF-a promotes suppressive activities of myeloid-derived suppressor cells via TNFR2. J. Immunol. 192 (2014), 1320–1331.
56. + 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.
57. Huang, A., Zhang, B., Wang, B., Zhang, F., Fan, K.X., Guo, Y.J., 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.
58. Ignarro, L.J., Napoli, C., Loscalzo, J., Nitric oxide donors and cardiovascular agents modulating the bioactivity of nitric oxide. Circ. Res. 90 (2002), 21–28.
59. Jeisy-Scott, V., Davis, W.G., Patel, J.R., Bowzard, J.B., Shieh, W.-J., Zaki, S.R., Katz, J.M., Sambhara, S., Increased MDSC accumulation and Th2 biased response to influenza A virus infection in the absence of TLR7 in mice. PLoS One, 6, 2011.
60. Jiang, J., Guo, W., Liang, X., Phenotypes, accumulation, and functions of myeloid-derived suppressor cells and associated treatment strategies in cancer patients. Hum. Immunol. 75 (2014), 1128–1137.
61. Kapanadze, T., Gamrekelashvili, J., Ma, C., Chan, C., Zhao, F., Hewitt, S., Zender, L., Kapoor, V., Felsher, D.W., Manns, M.P., Korangy, F., Greten, T.F., Regulation of accumulation and function of myeloid derived suppressor cells in different murine models of hepatocellular carcinoma. J. Hepatol. 59 (2013), 1007–1013.
62. Kawarada, Y., Ganss, R., Garbi, N., Sacher, T., Arnold, B., Hammerling, G.J., NK- and CD8 (+) T cell-mediated eradication of established tumors by peritumoral injection of CpG-containing oligodeoxynucleotides. J. Immunol. 167 (2001), 5247–5253.
63. Keskinov, A.A., Shurin, M.R., Myeloid regulatory cells in tumor spreading and metastasis. Immunobiology 220 (2015), 236–242.
64. Knaul, J.K., Jörg, S., Oberbeck-Mueller, D., Heinemann, E., Scheuermann, L., Brinkmann, V., Mollenkopf, H.J., Yeremeev, V., Kaufmann, S.H., Dorhoi, A., Lung-residing myeloid-derived suppressors display dual functionality in murine pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 190 (2014), 1053–1066.
65. Kohanbash, G., McKaveney, K., Sakaki, M., Ueda, R., Mintz, A.H., Amankulor, N., Fujita, M., Ohlfest, J.R., Okada, H., GM-CSF promotes the immunosuppressive activity of glioma-infiltrating myeloid cells through interleukin-4 receptor-alpha. Cancer Res. 73 (2013), 6413–6423.
66. Ku, A.W., Muhitch, J.B., Powers, C.A., Diehl, M., Kim, M., Fisher, D.T., Sharda, A.P., Clements, V.K., O'Loughlin, K., Minderman, H., Messmer, M.N., Ma, J., Skitzki, J.J., Steeber, D.A., Walcheck, B., Ostrand-Rosenberg, S., Abrams, S.I., Evans, S.S., Tumor-induced MDSC act via remote control to inhibit L-selectin-dependent adaptive immunity in lymph nodes. Elife, 5, 2016.
67. Kurkó J., Vida, A., Glant, T.T., Scanzello, C.R., Katz, R.S., Nair, A., Mikecz, K., Szekanecz, Z., Identification of myeloid-derived suppressor cells in the synovial fluid of patients with rheumatoid arthritis: a pilot study. BMC Musculoskelet Disord., 15, 2014.
68. Lei, G.-S., Zhang, C., Lee, C.-H., Myeloid-derived suppressor cells impair alveolar macrophages through PD-1 receptor ligation during Pneumocystis pneumonia. Infect. Immun. 83 (2015), 572–582.
69. Lesokhin, A.M., Hohl, T.M., Kitano, S., Cortez, C., Hirschhorn-Cymerman, D., Avogadri, F., Rizzuto, G.A., Lazarus, J.J., Pamer, E.G., Houghton, A.N., Merghoub, T., Wolchok, J.D., Monocytic CCR2(+) myeloid-derived suppressor cells promote immune escape by limiting activated CD8 T-cell infiltration into the tumor microenvironment. Cancer Res. 72 (2012), 876–886.
70. Liu, J., Wang, H., Yu, Q., Zheng, S., Jiang, Y., Liu, Y., Yuan, G., Qiu, L., Aberrant frequency of IL-10-producing B cells and its association with Treg and MDSC cells in Non Small Cell Lung Carcinoma patients. Hum. Immunol. 77 (2016), 84–89.
71. Mandruzzato, S., Solito, S., Falisi, E., Francescato, S., Chiarion-Sileni, V., Mocellin, S., Zanon, A., Rossi, C.R., Nitti, D., Bronte, V., Zanovello, P., IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 182 (2009), 6562–6568.
72. Mao, Y., Poschke, I., Wennerberg, E., Pico, D.C.Y., Egyhazi, B.S., Schultz, I., Hansson, J., Masucci, G., Lundqvist, A., Kiessling, R., Melanoma-educated CD14+ cells acquire a myeloid-derived suppressor cell phenotype through COX-2-dependent mechanisms. Cancer Res. 73 (2013), 3877–3887.
73. Markiewski, M.M., DeAngelis, R.A., Benencia, F., Ricklin-Lichtsteiner, S.K., Koutoulaki, A., Gerard, C., Coukos, G., Lambris, J.D., Modulation of the antitumor immune response by complement. Nat. Immunol. 9 (2008), 1225–1235.
74. Marshall, M.A., Jankovic, D., Maher, V.E., Sher, A., Berzofsky, J.A., Mice infected with Schistosoma mansoni develop a novel non-T-lymphocyte suppressor population which inhibits virus-specific CTL induction via a soluble factor. Microbes Infect. 3 (2001), 1051–1061.
75. Marvel, D., Gabrilovich, D.I., Myeloid-derived suppressor cells in the tumor microenvironment: expect the unexpected. J. Clin. Invest. 125 (2015), 3356–3364.
76. + myeloid cells inhibit development of antifungal Th1 immunity in mice with candidiasis. J. Immunol. 169 (2002), 3180–3190.
77. Movahedi, K., Guilliams, M., Van den Bossche, J., Van den Bergh R. l. Gysemans, C., Beschin, A., De Baetselier, P., Van Ginderachter, J.A., Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111 (2008), 4233–4244.
78. Nagaraj, S., Gupta, K., Pisarev, V., Kinarsky, L., Sherman, S., Kang, L., Herber, D., Schneck, J., Gabrilovich, D.I., Altered recognition of antigen is a novel mechanism of CD8-T cell tolerance in cancer. Nat. Med. 13 (2007), 828–835.
79. Nam, S., Kang, K., Cha, J.S., Kim, J.W., Lee, H.G., Kim, Y., Yang, Y., Lee, M.S., Lim, J.S., Interferon regulatory factor 4 (IRF4) controls myeloid-derived suppressor cell (MDSC) differentiation and function. J. Leukoc. Biol. 100 (2016), 1273–1284.
80. Obermajer, N., Muthuswamy, R., Lesnock, J., Edwards, R.P., Kalinski, P., Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells towards stable myeloid-derived suppressor cells. Blood 118 (2011), 5498–5505.
81. Ostrand-Rosenberg, S., Sinha, P., Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 182 (2009), 4499–4506.
82. Pak, A.S., Wright, M.A., Matthews, J.P., Collins, S.L., Petruzzelli, G.J., Young, M.R., 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.
83. Pan, P.Y., Wang, G.X., Yin, B., Ozao, J., Ku, T., Divino, C.M., Chen, S.H., Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood 111 (2008), 219–228.
84. Pan, W., Zhou, H.-J., Shen, Y.-J., Wang, Y., Xu, Y.-X., Hu, Y., Jiang, Y.-Y., Yuan, Z.-Y., Ugwu, C., Cao, E., J-, P., Surveillance on the status of immune cells after Echinnococcus granulosus protoscoleces infection in BALB/c mice. PLoS One, 8, 2013.
85. Pan, W., Shen, Y.J., Liu, H., Hu, Y., Jiang, Y.Y., Zhou, H.J., Xu, Y.X., Yuan, Z.Y., Wang, Y.J., Cao, J.P., Accumulation of myeloid-derived suppressor cells in the spleen and peripheral blood of Schistosoma japonicum-infected mice. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 32 (2014), 6–11.
86. Panni, R.Z., Dominic, E., Sanford, D.E., Belt, B.A., Mitchem, J.B., Worley, L.A., Goetz, B.D., Mukherjee, P., Wang-Gillam, A., Link, D.C., DeNardo, D.G., Goedegebuure, S.P., Linehan, D.C., Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer. Cancer Immunol. Immunother. 63 (2014), 513–528.
87. Peranzoni, E., Zilio, S., Marigo, I., Dolcetti, L., Zanovello, P., Mandruzzato, S., Bronte, V., Myeloid-derived suppressor cell heterogeneity and subset definition. Curr. Opin. Immunol. 22 (2010), 238–244.
88. Pico de Coaña, Y., Poschke, I., Gentilcore, G., Mao, Y., Nyström, M., Hansson, J., Masucci, G.V., Kiessling, R., Ipilimumab treatment results in an early decrease in the frequency of circulating granulocytic myeloid-derived suppressor cells as well as their arginase 1 production. Cancer. Immunol. Res. 1 (2013), 158–162.
89. Poe, S.L., Arora, M., Oriss, T.B., Yarlagadda, M., Isse, K., Khare, A., Levy, D.E., Lee, J.S., Mallampalli, R.K., Chan, Y.R., Ray, A., Ray, P., STAT1-regulated lung MDSC-like cells produce IL-10 and efferocytose apoptotic neutrophils with relevance in resolution of bacterial pneumonia. Mucosal Immunol. 6 (2013), 189–199.
90. Polz, J., Remke, A., Weber, S., Schmidt, D., Weber-Steffens, D., Pietryga-Krieger, A., Müller, N., Ritter, U., Mostböck, S., Männel, D.N., Myeloid suppressor cells require membrane TNFR2 expression for suppressive activity. Immun. Inflamm. Dis. 2 (2014), 121–130.
91. Raber, P.L., Thevenot, P., Sierra, R., Wyczechowska, D., Halle, D., Ramirez, M.E., Ochoa, A.C., Fletcher, M., Velasco, C., Wilk, A., Reiss, K., Rodriguez, P.C., Subpopulations of myeloid-derived suppressor cells impair T cell responses through independent nitric oxide-related pathways. Int. J. Cancer 134 (2014), 2853–2864.
92. Ray, A., Chakraborty, K., Ray, P., Immunosuppressive MDSCs induced by TLR signaling during infection and role in resolution of inflammation. Front Cell Infect. Microbiol. 3 (2013), 1–8.
93. Rieber, N., Brand, A., Hector, A., Graepler-Mainka, U., Ost, M., Schäfer, I., Wecker, I., Neri, D., Wirth, A., Mays, L., Zundel, S., Fuchs, J., Handgretinger, R., Stern, M., Hogardt, M., Döring, G., Riethmüller, J., Kormann, M., Hartl, D., Flagellin induces myeloid-derived suppressor cells: implications for Pseudomonas aeruginosa infection in cystic fibrosis lung disease. J. Immunol. 190 (2013), 1276–1284.
94. Rieber, N., Singh, A., Hasan, Öz., Carevic, M., Bouzani, B., Amich, J., Ost, M., Ye, Z., Ballbach, M., Schäfer, I., Mezger, M., Klimosch, S.N., Weber, A.N.R., Handgretinger, R., Krappmann, S., Liese, J., Engeholm, M., Schuüle, R., Salih, H.R., Marodi, L., Speckmann, C., Grimbacher, B., Ruland, J., Brown, G.D., Beilhack, A., Loeffler, J., Hartl, D., Pathogenic fungi regulate immunity by inducing neutrophilic myeloid-derived suppressor cells. Cell Host Microbe 17 (2015), 507–514.
95. Robinson, M.W., Harmon, C., O'Farrelly, C., Liver immunology and its role in inflammation and homeostasis. Cell. Mol. Immunol. 13 (2016), 267–276.
96. Rose, S., Misharin, A., Perlman, H., A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A 81A (2012), 343–350.
97. Rudolph, B.M., Loquai, C., Gerwe, A., Bacher, N., Steinbrink, K., Grabbe, S., Tuettenberg, A., Increased frequencies of CD11b(+) CD33(+) CD14(+) HLA-DR(low) myeloid derived suppressor cells are an early event in melanoma patients. Exp. Dermatol. 23 (2014), 202–204.
98. Saleem, S.J., Martin, R.K., Morales, J.K., Sturgill, J.L., Gibb, D.R., Graham, L., Bear, H.D., Manjili, M.H., Ryan, J.J., Conrad, D.H., Cutting edge: mast cells critically augment myeloid-derived suppressor cell activity. J. Immunol. 18 (2012), 511–515.
99. Sander, L.E., Sackett, S.D., Dierssen, U., Beraza, N., Linke, R.P., Müller, M., Blander, J.M., Tacke, F., Trautwein, C., Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J. Med. 207 (2010), 1453–1464.
100. Sauer, H., Wartenberg, M., Hescheler, J., Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell. Physiol. Biochem. 11 (2001), 173–186.
101. Schilling, B., Sucker, A., Griewank, K., Zhao, F., Weide, B., Goergens, A., Giebel, B., Schadendorf, D., Paschen, A., Vemurafenib reverses immunosuppression by myeloid derived suppressor cells. Int. J. Cancer 133 (2013), 1653–1663.
102. Schmid, M., Zimara, N., Wege, A.K., Ritter, U., Myeloid-derived suppressor cell functionality and interaction with Leishmania major parasites differ in C57BL/6 and BALB/c mice. Eur. J. Immunol. 00 (2014), 1–12.
103. Schumak, B., Klocke, K., Kuepper, J.M., Biswas, A., Djie-Maletz, A., Limmer, A., van Rooijen, N., Mack, M., Hoerauf, A., Dunay, I.R., Specific depletion of Ly6C(hi) inflammatory monocytes prevents immunopathology in experimental cerebral malaria. PLoS One, 17, 2015.
104. Shirota, Y., Shirota, H., Klinman, D.M., Intratumoral injection of CpG oligonucleotides induces the differentiation and reduces the immunosuppressive activity of myeloid-derived suppressor cells. J. Immunol. 188 (2012), 1592–1599.
105. Sinha, P., Chornoguz, O., Clements, V.K., Artemenko, K.A., Zubarev, R.A., Ostrand-Rosenberg, S., Myeloid-derived suppressor cells express the death receptor Fas and apoptose in response to T cell-expressed FasL. Blood 117 (2011), 5381–5390.
106. Sinha, P., Parker, K.H., Horn, L., Ostrand-Rosenberg, S., Tumor-induced myeloid-derived suppressor cell function is independent of IFNγ and IL-4Rα. Eur. J. Immunol. 42 (2012), 2052–2059.
107. Skabytska, Y., Wölbing, F., Günther, C., Köberle, M., Kaesler, S., Chen, K.M., Guenova, E., Demircioglu, D., Kempf, W.E., Volz, T., Rammensee, H.G., Schaller, M., Röcken, M., Götz, F., Biedermann, T., Cutaneous innate immune sensing of Toll-like receptor 2-6 ligands suppresses T cell immunity by inducing myeloid-derived suppressor cells. Immunity 41 (2014), 762–775.
108. Song, J., Lee, J., Kim, J., Jo, S., Kim, Y.J., Baek, J.E., Kwon, E.S., Lee, K.P., Yang, S., Kwon, K.S., Kim, D.U., Kang, T.H., Park, Y.Y., Chang, S., Cho, H.J., Kim, S.C., Koh, S.S., Kim, S., Pancreatic adenocarcinoma up-regulated factor (PAUF) enhances the accumulation and functional activity of myeloid-derived suppressor cells (MDSCs) in pancreatic cancer. Oncotarget 7:32 (2016), 51840–51853.
109. Srivastava, M., Sinha, P., Ostrand-Rosenberg, M., Myeloid-derived suppressor cells inhibit T cell activation by sequestering cystine and cysteine. Cancer Res. 70 (2010), 68–77.
110. Talmadge, J.E., Pathways mediating the expansion and immunosuppressive activity of myeloid-derived suppressor cells and their relevance to cancer therapy. Clin. Cancer Res. 13 (2007), 5243–5248.
111. Tarhini, A.A., Edington, H., Butterfield, L.H., Lin, Y., Shuai, Y.L., Tawbi, H., Sander, C., Yin, Y., Holtzman, M., Johnson, J., Rao, U.N.M., Kirkwood, J.M., Immune monitoring of the circulation and the tumor microenvironment in patients with regionally advanced melanoma receiving neoadjuvant ipilimumab. PLoS One, 9, 2014.
112. Tebartz, C., Horst, S.A., Sparwasser, T., Huehn, J., Beineke, A., Peters, G., Medina, E., A major role for myeloid-derived suppressor cells and a minor role for regulatory T cells in immunosuppression during Staphylococcus aureus infection. J. Immunol. 194 (2015), 1100–1111.
113. Trellakis, S., Bruderek, K., Hutte, J., Elian, M., Hoffmann, T.K., Lang, S., Brandau, S., Granulocytic myeloid-derived suppressor cells are cryosensitive and their frequency does not correlate with serum concentrations of colony-stimulating factors in head and neck cancer. Innate Immun. 19 (2013), 328–336.
114. Tu, S., Bhagat, G., Cui, G., Takaishi, S., Kurt-Jones, E.A., Rickman, B., Betz, K.S., Penz-Oesterreicher, M., Bjorkdahl, O., Fox, J.G., Wang, T.C., Overexpression of interleukin-1β induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 14 (2008), 408–419.
115. Tumino, N., Bilotta, M.T., Pinnetti, C., Ammassari, A., Antinori, A., Turchi, F., Agrati, C., Casetti, R., Bordoni, V., Cimini, E., Abbate, I., Capobianchi, M.R., Martini, F., Sacchi, A., Granulocytic Myeloid-Derived Suppressor Cells increased in early phases of primary HIV infection depending on TRAIL plasma level. J. Acquir. Immune Defic. Syndr. 74 (2017), 575–582.
116. Uhel, F., Azzaoui, I., Gregoire, M., Pangault, C., Dulong, J., Tadie, J.M., Gacouin, A., Camus, C., Cynober, L., Fest, T., Le Tulzo, Y., Roussel, M., Tarte, K., Early expansion of circulating granulocytic myeloid-derived suppressor cells predicts development of nosocomial infections in Patients with Sepsis. Am. J. Respir. Crit. Care Med 196 (2017), 315–327.
117. Valanparambil, R.M., Tam, M., Jardim, A., Geary, T.G., Stevenson, M.M., Primary Heligmosomoides polygyrus bakeri infection induces myeloid-derived suppressor cells that suppress CD4+ Th2 responses and promote chronic infection. Mucos. Immunol. 10 (2017), 238–249.
118. + myeloid cells and anergy of T lymphocytes participate in hyporesponsiveness of the lung-associated immune system during acute toxoplasmosis. Infect. Immun. 72 (2004), 5487–5492.
119. Vollbrecht, T., Stirner, R., Tufman, A., Roider, J., Huber, R.M., Bogner, J.R., Lechner, A., Bourquin, C., Draenert, R., Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS, 26, 2012 000–000.
120. Vollmer, J., Krieg, A.M., Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv. Drug Deliv. Rev. 61 (2009), 195–204.
121. Wang, L., Chang, E.W., Wong, S.C., Ong, S.M., Chong, D.Q., Ling, K.L., Increased myeloid-derived suppressor cells in gastric cancer correlate with cancer stage and plasma S100A8/A9 proinflammatory proteins. J. Immunol. 190 (2013), 794–804.
122. Wright, A.K., Newby, C., Hartley, R.A., Mistry, V., Gupta, S., Berair, R., Roach, K.M., Saunders, R., Thornton, T., Shelley, M., Edwards, K., Barker, B., Brightling, C.E., Myeloid-derived suppressor cell-like fibrocytes are increased and associated with preserved lung function in chronic obstructive pulmonary disease. Allergy 72 (2017), 645–655.
123. Wu, L., Yan, C., Czader, M., Foreman, O., Blum, J.S., Kapur, R., Du, H., Inhibition of PPARγ in myeloid-lineage cells induces systemic inflammation, immunosuppression, and tumorigenesis. Blood 119 (2012), 115–126.
124. Xu, X., Meng, Q., Erben, U., Wang, P., Glauben, R., Kuhl, A.A., Wu, H., Ma, C.W., Hu, M., Wang, Y., Sun, W., Jia, J., Wu, X., Chen, W., Siegmund, B., Qin, Z., Myeloid-derived suppressor cells promote B-cell production of IgA in a TNFR2-dependent manner. Cell. Mol. Immunol. 14 (2017), 597–606.
125. Youn, J.-I., Nagaraj, S., Collazo, M., Gabrilovich, D.I., Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181 (2008), 5791–5802.
126. Youn, J.-I., Kumar, V., Collazo, M., Nefedova, Y., Condamine, T., Cheng, P., Villagra, A., Antonia, S., McCaffrey, J.C., Fishman, M., Sarnaik, A., Horna, P., Sotomayor, E., Gabrilovich, D.I., Epigenetic silencing of retinoblastoma gene regulates pathologic differentiation of myeloid cells in cancer. Nat. Immunol. 14 (2013), 211–220.
127. Young, M.R.I., Wright, M.A., Lozano, Y., Prechel, M.M., Benefield, J., Leonetti, J.P., Collins, S.L., Petruzzelli, G.J., Increased recurrence and metastasis in patients whose primary head and neck squamous cell carcinomas secreted granulocyte–macrophage colony stimulating factor and contained CD34+ natural suppressor cells. Int. J. Cancer 74 (1997), 69–74.
128. Young, M.R.I., Petruzzelli, G.J., Kolesiak, K., Achille, N., Lathers, D.M., Gabrilovich DI: Human squamous cell carcinomas of the head and neck chemoattract immune suppressive CD34(+) progenitor cells. Hum. Immunol. 62 (2001), 332–341.
129. Zhai, N., Li, H., Song, H., Yang, Y., Cui, A., Li, T., Niu, J., Crispe, I.N., Su, L., Tu, Z., Hepatitis C virus induces MDSCs-Like monocytes through TLR2/PI3K/AKT/STAT3 signaling. PLoS One, 12, 2017, e0170516.
130. Zhang, Y.-L., Luan, B., Wang, X.-F., Qiao, J.-Y., Song, L., Lei, R.-R., Gao, W.-X., Liu, Y., Peripheral blood MDSCs, IL-10 and IL-12 in children with asthma and their importance in asthma development. PLoS One, 8, 2013.
131. Zhao, F., Hoechst, B., Duffy, A., Gamrekelashvili, J., Fioravanti, S., Manns, M.P., Greten, T.F., Korangy, F., S100A9 a new marker for monocytic human myeloid derived suppressor cells. Immunology 136 (2012), 176–183.
132. Zhao, G., Vasilakos, J.P., Tross, D., Smirnov, D., Klinman, D.M., Combination therapy targeting toll like receptors 7, 8 and 9 eliminates large established tumors. J. Immunother. Cancer, 2, 2014.
133. Zhu, K., Zhang, N., Guo, N., Yang, J., Wang, J., Yang, C., Yang, C., Zhu, L., Xu, C., Deng, Q., Zhu, R., Wang, H., Chen, X., Shi, Y., Li, Y., Leng, Q., SSChighCD11bhighLy-6ChighLy-6Glow myeloid cells curtail CD4 T cell response by inducible nitric oxide synthase in murine hepatitis. Int. J. Biochem. Cell Biol. 54 (2014), 89–97.