Publication Cover
Immunological Investigations
A Journal of Molecular and Cellular Immunology
Volume 41, 2012 - Issue 6-7
969
Views
56
CrossRef citations to date
0
Altmetric
Research Article

Immune Suppression: The Hallmark of Myeloid Derived Suppressor Cells

, &
Pages 581-594 | Published online: 27 Sep 2012

REFERENCES

  • Apolloni, E., Bronte, V., Mazzoni, A., Serafini, P., Cabrelle, A., Segal, D. M., Young, H. A., Zanovello, P. (2000). Immortalized myeloid suppressor cells trigger apoptosis in antigen-activated T lymphocytes. J. Immunol. 165 (12):6723–6730.
  • Bronte, V., Serafini, P., Apolloni, E., Zanovello, P. (2001). Tumor-induced immune dysfunctions caused by myeloid suppressor cells. J Immunother 24 (6):431–446.
  • Bronte, V., Serafini, P., De Santo, C., Marigo, I., Tosello, V., Mazzoni, A., Segal, D.M., Staib, C., Lowel, M., Sutter, G., Colombo, M. P., Zanovello, P. (2003). IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J Immunol 170 (1):270–278.
  • Bronte, V., Wang, M., Overwijk, W.W., Surman, D. R., Pericle, F., Rosenberg, S. A., Restifo, N. F. (1998). Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells. J. Immunol. 161 (10):5313–5320.
  • Bronte, V., Zanovello, P. (2005). Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5 (8):641–654.
  • Cheng, P., Corzo, C. A., Luetteke, N., Yu, B., Nagaraj, S., Bui, M. M., Ortiz, M., Nacken, W., Sorg, C., Vogl, T., Roth, J., Gabrilovich, D. I. (2008). Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J. Exp. Med. 205(10):2235–2249.
  • Corzo, C. A., Condamine, T., Lu, L., Cotter M. J., Youn, J. I., Cheng, P., Cho, H. I., Celis, E., Quiceno, D.G., Padhya, T., McCaffrey, T. V., McCaffrey, J. C., Gabrilovich. D. J. (2010). HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207(11):2439–2453.
  • Corzo, C. A., Cotter, M. J., Cheng, P., Cheng, F., Kusmartsev, S., Sotomayor, E., Padhya, T., McCaffrey, T. V., McCaffrey, J. C., Gabrilovich, D. I. (2009). Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J. Immunol. 182(9):5693–5701.
  • Cripps, J. G., and Gorham, J. D. (2011). MDSC in autoimmunity. Int. Immunopharmacol. 11 (7):789–793.
  • De Wilde, V., Van Rompaey, N., Hill, M., Lebrun, J.F., Lemaitre, P., Lhomme, F., Kubjak, C., Vokaer, B., Oldenhove, G., Charbonnier, L. M., Cuturi, M. C., Goldman, M., Le Moine, A. (2009). Endotoxin-induced myeloid-derived suppressor cells inhibit alloimmune responses via heme oxygenase-1. Am. J. Transplant 9 (9):2034–2047.
  • Delano, M. J., Scumpia, P. O., Weinstein, J. S., Coco, D., Nagaraj, S., Kelly-Scumpia, K. M., O’Malley, K. A., Wynn, J. L., Antonenko, S., Al-Quran, S. Z., Swan, R., Chung, C. S., Atkinson, M. A., Ramphal, R., Gabrilovich, D. I., Reeves, W. H., Ayala, A., Phillips, J., Laface, D., Heyworth, P. G., Clare-Salzler, M., Moldawer, L. L. (2007). MyD88-dependent expansion of an immature GR-1(+)CD11b(+) population induces T cell suppression and Th2 polarization in sepsis. J. Exp. Med. 204 (6):1463–1474.
  • Dolcetti, L., Peranzoni, E., Bronte, V. (2010). Measurement of myeloid cell immune suppressive activity. Curr. Protoc. Immunol. Chapter 14:Unit 14–17.
  • Dolcetti, L., Peranzoni, E., Ugel, S., Marigo, I., Fernandez Gomez, A., Mesa, C., Geilich, M., Winkels, G., Traggiai, E., Casati, A., Grassi, F., Bronte, V. (2010). Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur. J. Immunol. 40(1):22–35.
  • Dugast, A. S., Haudebourg, T., Coulon, F., Heslan, M., Haspot, F., Poirier, N., Vuillefroy de Silly, R., Usal, C., Smit, H., Martinet, B., Thebault, P., Renaudin, K., Vanhove, B. (2008). Myeloid-derived suppressor cells accumulate in kidney allograft tolerance and specifically suppress effector T cell expansion. J. Immunol. 180 (12): 7898–7906.
  • Fernandez, A., Mesa, C., Marigo, I., Dolcetti, L., Clavell, M., Oliver, L., Fernandez, L. E., Bronte, V. (2011). Inhibition of tumor-induced myeloid-derived suppressor cell function by a nanoparticulated adjuvant. J. Immunol. 186: (1):264–274.
  • Filipazzi, P., V. Huber, L. Rivoltini. 2012. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients. Cancer Immunol. Immunother. 61 (2):255–263.
  • Gabrilovich, D. I., Nagaraj, S. (2009). Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9(3):162–174.
  • Gabrilovich, D. I., Velders, M. P., Sotomayor, E. M., Kast, W. M. (2001). Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J. Immunol. 166 (9):5398–5406.
  • Gallina, G., Dolcetti, L., Serafini, P., De Santo, C., Marigo, I., Colombo, M. P., Basso, G., Brombacher, F., Borrello, I., Zanovello, P., Bicciato, S., Bronte, V. (2006). Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 116 (10):2777–2790.
  • Greten, T. F., Manns, M. P., Korangy, F. (2011). Myeloid derived suppressor cells in human diseases. Int. Immunopharmacol. 11 (7):802–807.
  • Haile, L. A., Gamrekelashvili, J., M., Manns, M. P., Korangy, F., Greten, T. F. (2010). CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice. J. Immunol. 185 (1):203–210.
  • Haile, L. A., von Wasielewski, R., Gamrekelashvili, J., Kruger, C., Bachmann, O., Westendorf, A. M., Buer, J., Liblau, R., Manns, M. P., Korangy, F., Greten, T. F. (2008). Myeloid-derived suppressor cells in inflammatory bowel disease: a new immunoregulatory pathway. Gastroenterology 135 (3):871–881, 881 e1–5.
  • Hanson, E. M., Clements, V. K., Sinha, P., Ilkovitch, D., and Ostrand-Rosenberg, S. (2009). Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells. J. Immunol. 183 (2):937–944.
  • Hoechst, B., Gamrekelashvili, J., Manns, M. P., Greten, T. F., Korangy, F. (2011). Plasticity of human Th17 cells and iTregs is orchestrated by different subsets of myeloid cells. Blood 117 (24):6532–6541.
  • Hoechst, B., Ormandy, L. A., Ballmaier, M., Lehner, F., Kruger, C., Manns, M. P., Greten, T. F., Korangy, F. (2008). A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 135(1):234–243.
  • Hoechst, B., Voigtlaender, T., Ormandy, L., Gamrekelashvili, J., Zhao, F., Wedemeyer, H., Lehner, F., Manns, M. P., Greten, T. F., Korangy, F. (2009). Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 50(3):799–807.
  • Huang, B., Pan, P. Y., Li, Q., Sato, A. I., Levy, D. E., Bromberg, J., Divino, C. M., Chen, S. H. (2006). 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 (2):1123–1131.
  • Kusmartsev, S. A., Li, Y., Chen, S. H. (2000). Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation. J. Immunol. 165 (2):779–785.
  • Kusmartsev, S., Gabrilovich, D. I. (2002). Immature myeloid cells and cancer-associated immune suppression. Cancer Immunol. Immunother. 51(6):293–298.
  • Kusmartsev, S., Nefedova, Y., Yoder, D., Gabrilovich, D. I. (2004). Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172 (2):989–999.
  • Le, H. K., Graham, L., Cha, E., Morales, J. K., Manjili, M. H., Bear, H. D. (2009). Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int. Immunopharmacol. 9 (7–8):900–909.
  • Liu, C., Yu, S., Kappes, J., Wang, J., Grizzle, W. E., Zinn, K. R., Zhang, H. G. (2007). Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood 109 (10):4336–4342.
  • Lu, T., Ramakrishnan, R., Altiok, S., Youn, J. I., Cheng, P., Celis, E., Pisarev, V., Sherman, S., Sporn, M. B., and Gabrilovich, D. (2011). Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J. Clin. Invest.
  • Makarenkova, V. P., Bansal, V., Matta, B. M., Perez, L. A., Ochoa, J. B. (2006). CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J. Immunol. 176 (4):2085–2094.
  • Mandruzzato, S., Solito, S., Falisi, E., Francescato, S., Chiarion-Sileni, V., Mocellin, S., Zanon, A., Rossi, C. R., Nitti, D., Bronte, V., Zanovello, P. (2009). IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 182 (10):6562–6528.
  • Marigo, I., Bosio, E., Solito, S., Mesa, C., Fernandez, A., Dolcetti, L., Ugel, S., Sonda, N., Bicciato, S., Falisi, E., Calabrese, F., Basso, G., Zanovello, P., Cozzi, E., Mandruzzato, S., Bronte, V. (2010). Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 32 (6):790–802.
  • Marigo, I., Dolcetti, L., Serafini, P., Zanovello, P., and Bronte, V. (2008). Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev. 222:162–179.
  • Movahedi, K., Guilliams, M., Van den Bossche, J., Van den Bergh, R., Gysemans, C., Beschin, A., De Baetselier, P., Van Ginderachter, J. A. (2008). Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111(8):4233–4244.
  • Nagaraj, S., Gupta, K., Pisarev, V., Kinarsky, L., Sherman, S., Kang, L., Herber, D. L., Schneck, J., Gabrilovich, D. I. (2007). Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 13(7):828–835.
  • Nagaraj, S., Nelson, A., Youn, J. L., Cheng, P., Quiceno, D., Gabrilovich, D. I. (2012). Antigen-specific CD4+ T cells regulate function of myeloid-derived suppressor cells in cancer via retrograde MHC Class II signaling. Cancer Res. 72 (4):928–938.
  • Nagaraj, S., Schrum, A. G., Cho, H. I., Celis, E., Gabrilovich, D. I. (2010). Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J. Immunol. 184 (6):3106–3116.
  • Ostrand-Rosenberg, S. (2010). Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol. Immunother 59 (10):1593–1600.
  • Ribechini, E., Leenen, P. J., Lutz, M. B. (2009). Gr-1 antibody induces STAT signaling, macrophage marker expression and abrogation of myeloid-derived suppressor cell activity in BM cells. Eur. J. Immunol. 39(12):3538–3551.
  • Serafini, P., Borrello, I., Bronte, V. (2006). Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin. Cancer Biol. 16 (1):53–65.
  • Serafini, P., Mgebroff, S., Noonan, K., Borrello, I. (2008). Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res. 68 (13):5439–5449.
  • Sinha, P., Chornoguz, O., Clements, V. K., Artemenko, K. A., Zubarev, R. A., Ostrand-Rosenberg, S. (2011). Myeloid-derived suppressor cells express the death receptor Fas and apoptose in response to T cell-expressed FasL. Blood 117(20):5381–5390.
  • Sinha, P., Clements, V. K., Bunt, S. K., Albelda, S. M., Ostrand-Rosenberg, S. (2007). Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol. 179(2):977–983.
  • Solito, S., Bronte, V., Mandruzzato, S. (2011). Antigen specificity of immune suppression by myeloid-derived suppressor cells. J. Leukoc. Biol. 90(1):31–36.
  • Stewart, T. J., Smyth, M. J. (2011). Improving cancer immunotherapy by targeting tumor-induced immune suppression. Cancer Metastasis Rev. 30 (1):125–140.
  • Suzuki, E., Kapoor, V., Jassar, A. S., Kaiser, L. R., Albelda, S. M. (2005). Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res. 11 (18):6713–6721.
  • Terabe, M., Matsui, S., Park, J. M., Mamura, M., Noben-Trauth, N., Donaldson, D. D., Chen, W., Wahl, S. M., Ledbetter, S., Pratt, B., Letterio, J. J., Paul, W. E., Berzofsky, J. A. (2003). Transforming growth factor-beta production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance: abrogation prevents tumor recurrence. J. Exp. Med. 198 (11):1741–1752.
  • Ugel, S., Delpozzo, F., Desantis, G., Papalini, F., Simonato, F., Sonda, N., Zilio, S., and Bronte, V. (2009). Therapeutic targeting of myeloid-derived suppressor cells. Curr. Opin. Pharmacol. 9(4):470–481.
  • Vincent, J., Mignot, G., Chalmin, F., Ladoire, S., Bruchard, M., Chevriaux, A., Martin, F., Apetoh, L., Rebe, C., Ghiringhelli, F. (2010). 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 70 (8):3052–3061.
  • Watanabe, S., Deguchi, K., Zheng, R., Tamai, H., Wang, L. H., Cohen, P. A., Shu, S. (2008). Tumor-induced CD11b+Gr-1+ myeloid cells suppress T cell sensitization in tumor-draining lymph nodes. J. Immunol. 181(5):3291–3300.
  • Yang, L., DeBusk, L. M., Fukuda, K., Fingleton, B., Green-Jarvis, B., Shyr, Y., Matrisian, L. M., Carbone, D. P., Lin, P. C. (2004). Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6 (4):409–421.
  • Youn, J. I., Nagaraj, S., Collazo, M., Gabrilovich, D. I. (2008). Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181(8):5791–5802.
  • Zea, A. H., Rodriguez, P. C., Atkins, M. B., Hernandez, C., Signoretti, S., Zabaleta, J., McDermott, D., Quiceno, D., Youmans, A., O’Neill, A., Mier, J., Ochoa, A. O.. (2005). Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 65 (8):3044–3048.
  • Zhao, F., Hoechst, B., Duffy, A., Gamrekelashvili, J., Fioravanti, S., Manns, M. P., Greten, T. P., Korangy, F. (2012). S100A9 a new marker for monocytic human myeloid derived suppressor cells. Immunology.
  • Zhou, R., He, P. L., Ren, Y. X., Wang, W. H., Zhou, R. Y., Wan, H., Ono, S., Fujiwara, H., Zuo, J. P. (2007). Myeloid suppressor cell-associated immune dysfunction in CSA1M fibrosarcoma tumor-bearing mice. Cancer Sci. 98 (6):882–889.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.