Myeloid-derived suppressor cell development is regulated by a STAT/IRF-8 axis

Journal of Clinical Investigation

Volumn 123, Issue 10, 2013, Pages 4464-4478

  Waight, Jeremy D ^a   Netherby, Colleen ^a   Hensen, Mary L ^a   Miller, Austin ^b   Hu, Qiang ^b   Liu, Song ^b   Bogner, Paul N ^a   Farren, Matthew R ^a   Lee, Kelvin P ^a   Liu, Kebin ^c   Abrams, Scott I ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b Department of Biostatistics and Bioinformatics ^*  (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; INTERFERON REGULATORY FACTOR; STAT3 PROTEIN, MOUSE; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL POPULATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; MYELOPOIESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SUPPRESSOR CELL; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; BREAST TUMOR; C57BL MOUSE; CANCER TRANSPLANTATION; DISEASE FREE SURVIVAL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KAPLAN MEIER METHOD; KNOCKOUT MOUSE; LUNG TUMOR; METABOLISM; MORTALITY; PATHOLOGY; PHYSIOLOGY; SECONDARY; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE-FREE SURVIVAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERFERON REGULATORY FACTORS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; NEOPLASM TRANSPLANTATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; TRANSCRIPTOME; TUMOR BURDEN;

EID: 84885029080     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI68189     Document Type: Article

References (54)

1. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol. 2012;12(4):253-268.
2. Ostrand-Rosenberg S, Sinha P, Beury DW, Clements VK. Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin Cancer Biol. 2012;22(4):275-281.
3. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumorbearing mice. J Immunol. 2008;181(8):5791-5802.
4. Sawanobori Y, et al. Chemokine-mediated rapid turnover of myeloid-derived suppressor cells in tumor-bearing mice. Blood. 2008;111(12):5457-5466.
5. Sinha P, Chornoguz O, Clements VK, Artemenko KA, Zubarev RA, Ostrand-Rosenberg S. Myeloidderived suppressor cells express the death receptor Fas and apoptose in response to T cell-expressed FasL. Blood. 2011;117(20):5381-5390.
6. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin- cyclophosphamide chemotherapy. Cancer Immunol Immunother. 2009;58(1):49-59.
7. Mandruzzato S, et al. IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J Immunol. 2009;182(10):6562-6568.
8. Rodriguez PC, et al. Arginase I-producing myeloidderived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 2009;69(4):1553-1560.
9. Gabitass RF, Annels NE, Stocken DD, Pandha HA, Middleton GW. 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. 2011;60(10):1419-1430.
10. Raychaudhuri B, et al. Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma. Neuro Oncol. 2011;13(6):591-599.
11. Yu J, et al. Myeloid-derived suppressor cells suppress antitumor immune responses through IDO expression and correlate with lymph node metastasis in patients with breast cancer. J Immunol. 2013;190(7):3783-3797.
12. Tu S, et al. Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell. 2008;14(5):408-419.
13. Yang L, et al. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell. 2008;13(1):23-35.
14. Kujawski M, Kortylewski M, Lee H, Herrmann A, Kay H, Yu H. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J Clin Invest. 2008;118(10):3367-3377.
15. Ko JS, et al. Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained. Cancer Res. 2010;70(9):3526-3536.
16. Chalmin F, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest. 2010;120(2):457-471.
17. Bayne LJ, et al. Tumor-derived granulocyte-macrophage colony-stimulating factor regulates myeloid inflammation and T cell immunity in pancreatic cancer. Cancer Cell. 2012;21(6):822-835.
18. Zhao X, et al. TNF signaling drives myeloid-derived suppressor cell accumulation. J Clin Invest. 2012;122(11):4094-4104.
19. Vasquez-Dunddel D, et al. STAT3 regulates arginase-I in myeloid-derived suppressor cells from cancer patients. J Clin Invest. 2013;123(4):1580-1589.
20. Holtschke T, et al. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell. 1996;87(2):307-317.
21. Gabriele L, et al. Regulation of apoptosis in myeloid cells by interferon consensus sequencebinding protein. J Exp Med. 1999;190(3):411-421.
22. Tamura T, Nagamura-Inoue T, Shmeltzer Z, Kuwata T, Ozato K. ICSBP directs bipotential myeloid progenitor cells to differentiate into mature macrophages. Immunity. 2000;13(2):155-165.
23. Tamura T, Yanai H, Savitsky D, Taniguchi T. The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol. 2008;26:535-584.
24. Hambleton S, et al. IRF8 mut ations and human den - dritic-cell immunodeficiency. N Engl J Med. 2011;365(2):127-138.
25. Becker AM, Michael DG, Satpathy AT, Sciammas R Singh H, Bhattacharya D. IRF-8 extinguishes neutrophil production and promotes dendritic cell lineage commitment in both myeloid and lymphoid mouse progenitors. Blood. 2012;119(9):2003-2012.
26. Stewart TJ, Liewehr DJ, Steinberg SM, Greeneltch KM, Abrams SI. Modulating the expression of IFN regulatory factor 8 alters the pro tumorigenic behavior of CD11b+Gr-1+ myeloid cells. J Immunol. 2009;183(1):117-128.
27. Sinha P, Parker KH, Horn L, Ostrand-Rosenberg S. Tumor-induced myeloid-derived suppressor cell function is independent of IFNy IL-4Ra. Eur J Immunol. 2012;42(8):2052-2059.
28. Waight JD, Hu Q, Miller A, Liu S, Abrams SI. Tumor-derived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism. PLoS One. 2011;6(11):e27690.
29. Tsujimura H, Nagamura-Inoue T, Tamura T, Ozato K. IFN consensus sequence binding protein/IFN regulatory factor-8 guides bone marrow progenitor cells toward the macrophage lineage. J Immunol. 2002;169(3):1261-1269.
30. Li Z, et al. Gr-1+CD11b+ cells are responsible for tumor promoting effect of TGF-p in breast cancer progression. Int J Cancer. 2012;131(11):2584-2595.
31. Meyer C, et al. Chronic inflammation promotes myeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mouse melanoma model. Proc Natl Acad Sci U S A. 2011;108(41):17111-17116.
32. Fridlender ZG, et al. Polarization of tumor-associated neutrophil phenotype by TGF-p: "N1" versus "N2" TAN. Cancer Cell. 2009;16(3):183-194.
33. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252-264.
34. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol. 1992;12(3):954-961.
35. Bill MA, et al. Structurally modified curcumin analogs inhibit STAT3 phosphorylation and promote apoptosis of human renal cell carcinoma and melanoma cell lines. PLoS One. 2012;7(8):e40724.
36. Nelson EA, et al. The STAT5 inhibitor pimozide decreases survival of chronic myelogenous leukemia cells resistant to kinase inhibitors. Blood. 2011;117(12):3421-3429.
37. Esashi E, Wang YH, Perng O, Qin XF, Liu YJ, Watowich SS. The signal transducer STAT5 inhibits plasmacytoid dendritic cell development by suppressing transcription factor IRF8. Immunity. 2008;28(4):509-520.
38. Lehtonen A, Matikainen S, Miettinen M, Julkunen I. Granulocyte-macrophage colony-stimulating factor (GM-CSF)-induced STAT5 activation and target-gene expression during human monocyte/macrophage differentiation. J Leukoc Biol. 2002;71(3):511-519.
39. Panopoulos AD, et al. STAT3 governs distinct pathways in emergency granulopoiesis and mature neutrophils. Blood. 2006;108(12):3682-3690.
40. Kanno Y, et al. Ozato K. The genomic structure of the murine ICSBP gene reveals the presence of the gamma interferon-responsive element, to which an ISGF3 alpha subunit (or similar) molecule binds. Mol Cell Biol. 1993;13(7):3951-3963.
41. Seidel HM, Milocco LH, Lamb P, Darnell JE Jr, Stein RB, Rosen J. Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. Proc Natl Acad Sci U S A. 1995;92(7):3041-3045.
42. DeNardo DG, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 2011;1(1):54-67.
43. Tosolini M, et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 2011;71(4):1263-1271.
44. Suzuki E, Kapoor V, Jassar AS, Kaiser LR, Albelda SM. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumorbearing animals and enhances antitumor immune activity. Clin Cancer Res. 2005;11(18):6713-6721.
45. Shojaei F, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat Biotechnol. 2007;25(8):911-920.
46. Ozao-Choy J, et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 2009;69(6):2514-2522.
47. Nagaraj S, et al. Anti-inflammatory triterpenoid blocks immune suppressive function of MDSCs and improves immune response in cancer. Clin Cancer Res. 2010;16(6):1812-1823.
48. Cheng P, et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med. 2008;205(10):2235-2249.
49. Marigo I, et al. Tumor-induced tolerance and immune suppression depend on the C/EBPβ transcription factor. Immunity. 2010;32(6):790-802.
50. Gade P, Roy SK, Li H, Nallar SC, Kalvakolanu DV. Critical role for transcription factor C/EBP-β in regulating the expression of death-associated protein kinase 1. Mol Cell Biol. 2008;28(8):2528-2548.
51. Ambrosone CB, Nesline MK, Davis W. Establishing a cancer center data bank and biorepository for multidisciplinary research. Cancer Epidemiol Biomarkers Prev. 2006;15(9):1575-1577.
52. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 1992;52(6):1399-1405.
53. Yamamoto M, et al. Shared and distinct functions of the transcription factors IRF4 and IRF8 in myeloid cell development. PLoS One. 2011;6(10):e25812.
54. Bharadwaj U, Li M, Zhang R, Chen C, Yao Q. Elevated interleukin-6 and G-CSF in human pancreatic cancer cell conditioned medium suppress dendritic cell differentiation and activation. Cancer Res. 2007;67(11):5479-5488.