IFN-γ regulates survival and function of tumor-induced CD11b+Gr-1high myeloid derived suppressor cells by modulating the anti-apoptotic molecule Bcl2a1

European Journal of Immunology

Volumn 44, Issue 8, 2014, Pages 2457-2467

  Medina Echeverz, José ^a   Haile, Lydia A ^a   Zhao, Fei ^a   Gamrekelashvili, Jaba ^a   Ma, Chi ^a   Métais, Jean Yves ^b   Dunbar, Cynthia E ^b   Kapoor, Veena ^c   Manns, Michael P ^d   Korangy, Firouzeh ^a   Greten, Tim F ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

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

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Bcl2a1; G MDSC; GM CSF; IFN ; Immunotherapy; Vaccine

Indexed keywords

BCL2 RELATED PROTEIN A1; CD11B ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; STAT1 PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CD11B GR 1 HIGH MYELOID DERIVED SUPPRESSOR CELL; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL SURVIVAL; COCULTURE; FEMALE; GENE EXPRESSION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SUPPRESSOR CELL; UPREGULATION;

BCL2A1; G-MDSC; GM-CSF; IFN-Γ; IMMUNOTHERAPY; VACCINE;

ANIMALS; ANTIGENS, CD11B; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID CELLS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, CHEMOKINE; STAT1 TRANSCRIPTION FACTOR; UP-REGULATION;

EID: 84906092091     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444497     Document Type: Article

References (42)

1. Gabrilovich, D. I. and Nagaraj, S., Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009. 9: 162-174.
2. Peranzoni, E., Zilio, S., Marigo, I., Dolcetti, L., Zanovello, P., Mandruzzato, S. and Bronte, V., Myeloid-derived suppressor cell heterogeneity and subset definition. Curr. Opin. Immunol. 2010. 22: 238-244.
3. Haile, L. A., Gamrekelashvili, J., Manns, M. P., Korangy, F. and Greten, T. F., CD49d is a new marker for distinct myeloid-derived suppressor cell subpopulations in mice. J. Immunol. 2010. 185: 203-210.
4. Movahedi, K., Guilliams, M., Van den Bossche, J., Van den Bergh, R., Gysemans, C., Beschin, A., De Baetselier, P. and Van Ginderachter, J. A., Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 2008. 111: 4233-4244.
5. Youn, J. I., Nagaraj, S., Collazo, M. and Gabrilovich, D. I., Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 2008. 181: 5791-5802.
6. Corzo, C. A., Condamine, T., Lu, L., Cotter, M. J., Youn, J. I., Cheng, P., Cho, H. I. et al., HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 2010. 207: 2439-2453.
7. Marigo, I., Bosio, E., Solito, S., Mesa, C., Fernandez, A., Dolcetti, L., Ugel, S. et al., Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 2010. 32: 790-802.
8. Serafini, P., Carbley, R., Noonan, K. A., Tan, G., Bronte, V. and Borrello, I., High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells. Cancer Res. 2004. 64: 6337-6343.
9. Steding, C. E., Wu, S. T., Zhang, Y., Jeng, M. H., Elzey, B. D. and Kao, C., The role of interleukin-12 on modulating myeloid-derived suppressor cells, increasing overall survival and reducing metastasis. Immunology 2011. 133: 221-238.
10. Talmadge, J. E., Pathways mediating the expansion and immunosuppressive activity of myeloid-derived suppressor cells and their relevance to cancer therapy. Clin. Cancer Res. 2007. 13: 5243-5248.
11. Sonda, N., Chioda, M., Zilio, S., Simonato, F. and Bronte, V., Transcription factors in myeloid-derived suppressor cell recruitment and function. Curr. Opin. Immunol. 2011. 23: 279-285.
12. Condamine, T. and Gabrilovich, D. I., Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 2011. 32: 19-25.
13. Gallina, G., Dolcetti, L., Serafini, P., De Santo, C., Marigo, I., Colombo, M. P., Basso, G. et al., Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 2006. 116: 2777-2790.
14. Ribechini, E., Greifenberg, V., Sandwick, S. and Lutz, M. B., Subsets, expansion and activation of myeloid-derived suppressor cells. Med. Microbiol. Immunol. 2010. 199: 273-281.
15. Schouppe, E., Mommer, C., Movahedi, K., Laoui, D., Morias, Y., Gysemans, C., Luyckx, A. et al., Tumor-induced myeloid-derived suppressor cell subsets exert either inhibitory or stimulatory effects on distinct CD8+ T-cell activation events. Eur. J. Immunol. 2013. 43: 2930-2942.
16. Mazzoni, A., Bronte, V., Visintin, A., Spitzer, J. H., Apolloni, E., Serafini, P., Zanovello, P. and Segal, D. M., Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 2002. 168: 689-695.
17. Bronte, V., Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions. Eur. J. Immunol. 2009. 39: 2670-2672.
18. Greifenberg, V., Ribechini, E., Rossner, S. and Lutz, M. B., Myeloid-derived suppressor cell activation by combined LPS and IFN-gamma treatment impairs DC development. Eur. J. Immunol. 2009. 39: 2865-2876.
19. Vogler, M., BCL2A1: the underdog in the BCL2 family. Cell Death Differ. 2012. 19: 67-74.
20. Sade-Feldman, M., Kanterman, J., Ish-Shalom, E., Elnekave, M., Horwitz, E. and Baniyash, M., Tumor necrosis factor-alpha blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity 2013. 38: 541-554.
21. Elkabets, M., Ribeiro, V. S., Dinarello, C. A., Ostrand-Rosenberg, S., Di Santo, J. P., Apte, R. N. and Vosshenrich, C. A., IL-1beta regulates a novel myeloid-derived suppressor cell subset that impairs NK cell development and function. Eur. J. Immunol. 2010. 40: 3347-3357.
22. Schroder, K., Hertzog, P. J., Ravasi, T. and Hume, D. A., Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 2004. 75: 163-189.
23. Ostrand-Rosenberg, S. and Sinha, P., Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 2009. 182: 4499-4506.
24. Cross, A., Moots, R. J. and Edwards, S. W., The dual effects of TNFalpha on neutrophil apoptosis are mediated via differential effects on expression of Mcl-1 and Bfl-1. Blood 2008. 111: 878-884.
25. Verschelde, C., Walzer, T., Galia, P., Biemont, M. C., Quemeneur, L., Revillard, J. P., Marvel, J. and Bonnefoy-Berard, N., A1/Bfl-1 expression is restricted to TCR engagement in T lymphocytes. Cell Death Differ. 2003. 10: 1059-1067.
26. Lin, E. Y., Orlofsky, A., Berger, M. S. and Prystowsky, M. B., Characterization of A1, a novel hemopoietic-specific early-response gene with sequence similarity to bcl-2. J. Immunol. 1993. 151: 1979-1988.
27. Orlofsky, A., Berger, M. S. and Prystowsky, M. B., Novel expression pattern of a new member of the MIP-1 family of cytokine-like genes. Cell Regul. 1991. 2: 403-412.
28. Karsan, A., Yee, E. and Harlan, J. M., Endothelial cell death induced by tumor necrosis factor-alpha is inhibited by the Bcl-2 family member, A1. J. Biol. Chem. 1996. 271: 27201-27204.
29. Nopora, A. and Brocker, T., Bcl-2 controls dendritic cell longevity in vivo. J. Immunol. 2002. 169: 3006-3014.
30. Hamasaki, A., Sendo, F., Nakayama, K., Ishida, N., Negishi, I., Nakayama, K. and Hatakeyama, S., Accelerated neutrophil apoptosis in mice lacking A1-a, a subtype of the bcl-2-related A1 gene. J. Exp. Med. 1998. 188: 1985-1992.
31. Gollob, J. A., Sciambi, C. J., Huang, Z. and Dressman, H. K., Gene expression changes and signaling events associated with the direct antimelanoma effect of IFN-gamma. Cancer Res. 2005. 65: 8869-8877.
32. de Kleijn, S., Langereis, J. D., Leentjens, J., Kox, M., Netea, M. G., Koenderman, L., Ferwerda, G. et al., IFN-gamma-stimulated neutrophils suppress lymphocyte proliferation through expression of PD-L1. PLoS One 2013. 8: e72249.
33. Fridlender, Z. G., Sun, J., Kim, S., Kapoor, V., Cheng, G., Ling, L., Worthen, G. S. and Albelda, S. M., Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 2009. 16: 183-194.
34. Fridlender, Z. G., Sun, J., Mishalian, I., Singhal, S., Cheng, G., Kapoor, V., Horng, W. et al., Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS One 2012. 7: e31524.
35. Pedra, J. H., Sukumaran, B., Carlyon, J. A., Berliner, N. and Fikrig, E., Modulation of NB4 promyelocytic leukemic cell machinery by Anaplasma phagocytophilum. Genomics 2005. 86: 365-377.
36. Feldman, G. M., Rosenthal, L. A., Liu, X., Hayes, M. P., Wynshaw-Boris, A., Leonard, W. J., Hennighausen, L. and Finbloom, D. S., STAT5A-deficient mice demonstrate a defect in granulocyte-macrophage colony-stimulating factor-induced proliferation and gene expression. Blood 1997. 90: 1768-1776.
37. Sinha, P., Parker, K. H., Horn, L. and Ostrand-Rosenberg, S., Tumor-induced myeloid-derived suppressor cell function is independent of IFN-gamma and IL-4Ralpha. Eur. J. Immunol. 2012. 42: 2052-2059.
38. Sinha, P., Chornoguz, O., Clements, V. K., Artemenko, K. A., Zubarev, R. A. and Ostrand-Rosenberg, S., Myeloid-derived suppressor cells express the death receptor Fas and apoptose in response to T cell-expressed FasL. Blood 2011. 117: 5381-5390.
39. Leber, B., Geng, F., Kale, J. and Andrews, D. W., Drugs targeting Bcl-2 family members as an emerging strategy in cancer. Expert. Rev. Mol. Med. 2010. 12: e28.
40. Vogler, M., Dinsdale, D., Dyer, M. J. and Cohen, G. M., Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ. 2009. 16: 360-367.
41. Sinha, B., Eigler, A., Baumann, K. H., Greten, T. F., Moeller, J. and Endres, S., Nitric oxide downregulates tumour necrosis factor in mRNA in RAW 264.7 cells. Res. Immunol. 1998. 149: 139-150.
42. Metais, J. Y., Winkler, T., Geyer, J. T., Calado, R. T., Aplan, P. D., Eckhaus, M. A. and Dunbar, C. E., BCL2A1a over-expression in murine hematopoietic stem and progenitor cells decreases apoptosis and results in hematopoietic transformation. PLoS One 2012. 7: e48267.