IL-11 induces differentiation of myeloid-derived suppressor cells through activation of STAT3 signalling pathway

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Sumida, Kentaro ^a   Ohno, Yosuke ^a,b   Ohtake, Junya ^a   Kaneumi, Shun ^a   Kishikawa, Takuto ^a   Takahashi, Norihiko ^b   Taketomi, Akinobu ^b   Kitamura, Hidemitsu ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84940702488     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13650     Document Type: Article

References (77)

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2. Yu, H., Kortylewski, M., Pardoll, D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol 7, 41-51, doi: 10.1038/nri1995 (2007).
3. Yu, H., Pardoll, D., Jove, R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9, 798-809, doi: 10.1038/nrc2734 (2009).
4. Narita, Y. et al. The key role of IL-6-arginase cascade for inducing dendritic cell-dependent CD4(+ ) T cell dysfunction in tumour-bearing mice. J Immunol 190, 812-820, doi: 10.4049/jimmunol.1103797 (2013).
5. Hodi, F. S. et al. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci USA 100, 4712-4717, doi: 10.1073/pnas.0830997100 (2003).
6. Zhang, Y. et al. Th1 cell adjuvant therapy combined with tumour vaccination: a novel strategy for promoting CTL responses while avoiding the accumulation of Tregs. Int Immunol 19, 151-161, doi: 10.1093/intimm/dxl132 (2007).
7. Chamoto, K. et al. 3-Methylcholanthrene-induced transforming growth factor-beta-producing carcinomas, but not sarcomas, are refractory to regulatory T cell-depletion therapy. Cancer Sci 101, 855-861, doi: 10.1111/j.1349-7006.2009.01469.x (2010).
8. Youn, J. I., Nagaraj, S., Collazo, M., Gabrilovich, D. I. Subsets of myeloid-derived suppressor cells in tumour-bearing mice. J Immunol 181, 5791-5802, doi: 10.4049/jimmunol.181.8.5791 (2008).
9. Gabrilovich, D. I., Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9, 162-174, doi: 10.1038/nri2506 (2009).
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11. Peranzoni, E. et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 22, 238-244, doi: 10.1016/j.coi.2010.01.021 (2010).
12. Dolcetti, L. et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 40, 22-35, doi: 10.1002/eji.200939903 (2010).
13. Sumida, K. et al. Anti-IL-6 receptor mAb eliminates myeloid-derived suppressor cells and inhibits tumour growth by enhancing T-cell responses. Eur J Immunol 42, 2060-2072, doi: 10.1002/eji.201142335 (2012).
14. Kusmartsev, S. et al. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin Cancer Res 14, 8270-8278, doi: 10.1158/1078-0432.CCR-08-0165 (2008).
15. Diaz-Montero, C. M. et al. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumour burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 58, 49-59, doi: 10.1007/s00262-008-0523-4 (2009).
16. Solito, S. et al. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood 118, 2254-2265, doi: 10.1182/blood-2010-12-325753 (2011).
17. Gros, A. et al. Myeloid cells obtained from the blood but not from the tumour can suppress T-cell proliferation in patients with melanoma. Clin Cancer Res 18, 5212-5223, doi: 10.1158/1078-0432.CCR-12-1108 (2012).
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20. Sinha, P. et al. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol 181, 4666-4675, doi: 10.4049/jimmunol.181.7.4666 (2008).
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23. Lu, T., Gabrilovich, D. I. Molecular pathways: tumour-infiltrating myeloid cells and reactive oxygen species in regulation of tumour microenvironment. Clin Cancer Res 18, 4877-4882, doi: 10.1158/1078-0432.CCR-11-2939 (2012).
24. Li, H., Han, Y., Guo, Q., Zhang, M., Cao, X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol 182, 240-249, doi: 10.4049/jimmunol.182.1.240 (2009).
25. Hirano, T. Interleukin 6 in autoimmune and inflammatory diseases: a personal memoir. Proc Jpn Acad Ser B Phys Biol Sci 86, 717-730, doi: 10.2183/pjab.86.717 (2010).
26. Teramura, M., Kobayashi, S., Hoshino, S., Oshimi, K., Mizoguchi, H. Interleukin-11 enhances human megakaryocytopoiesis in vitro. Blood 79, 327-331 (1992).
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28. Gao, Y. B. et al. Enhanced production of CTGF and IL-11 from highly metastatic hepatoma cells under hypoxic conditions: an implication of hepatocellular carcinoma metastasis to bone. J Cancer Res Clin Oncol 139, 669-679, doi: 10.1007/s00432-012-1370-4 (2013).
29. Ren, L., Wang, X., Dong, Z., Liu, J., Zhang, S. Bone metastasis from breast cancer involves elevated IL-11 expression and the gp130/STAT3 pathway. Med Oncol 30, 634, doi: 10.1007/s12032-013-0634-4 (2013).
30. Nakayama, T. et al. Expression of interleukin-11 (IL-11) and IL-11 receptor alpha in human gastric carcinoma and IL-11 upregulates the invasive activity of human gastric carcinoma cells. Int J Oncol 30, 825-833, doi: 10.3892/ijo.30.4.825 (2007).
31. Necula, L. G. et al. IL-6 and IL-11 as markers for tumour aggressiveness and prognosis in gastric adenocarcinoma patients without mutations in Gp130 subunits. J Gastrointestin Liver Dis 21, 23-29 (2012).
32. Xiang, Z. L., Zeng, Z. C., Fan, J., Tang, Z. Y., Zeng, H. Y. Expression of connective tissue growth factor and interleukin-11 in intratumoral tissue is associated with poor survival after curative resection of hepatocellular carcinoma. Mol Biol Rep 39, 6001-6006, doi: 10.1007/s11033-011-1413-y (2012).
33. Bellone, G. et al. Cytokine expression profile in human pancreatic carcinoma cells and in surgical specimens: implications for survival. Cancer Immunol Immunother 55, 684-698, doi: 10.1007/s00262-005-0047-0 (2006).
34. Putoczki, T. L. et al. Interleukin-11 is the dominant IL-6 family cytokine during gastrointestinal tumourigenesis and can be targeted therapeutically. Cancer Cell 24, 257-271, doi: 10.1016/j.ccr.2013.06.017 (2013).
35. Campbell, C. L. et al. Interleukin-11 receptor expression in primary ovarian carcinomas. Gynecol Oncol 80, 121-127, doi: 10.1006/gyno.2000.6064 (2001).
36. Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 5, 263-274, doi: 10.1038/nrc1586 (2005).
37. Yu, H., Kortylewski, M., Pardoll, D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol 7, 41-51, doi: 10.1038/nri1995 (2007).
38. Yu, H., Pardoll, D., Jove, R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9, 798-809, doi: 10.1038/nrc2734 (2009).
39. Narita, Y. et al. The key role of IL-6-arginase cascade for inducing dendritic cell-dependent CD4(+ ) T cell dysfunction in tumour-bearing mice. J Immunol 190, 812-820, doi: 10.4049/jimmunol.1103797 (2013).
40. Hodi, F. S. et al. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci USA 100, 4712-4717, doi: 10.1073/pnas.0830997100 (2003).
41. Zhang, Y. et al. Th1 cell adjuvant therapy combined with tumour vaccination: a novel strategy for promoting CTL responses while avoiding the accumulation of Tregs. Int Immunol 19, 151-161, doi: 10.1093/intimm/dxl132 (2007).
42. Chamoto, K. et al. 3-Methylcholanthrene-induced transforming growth factor-beta-producing carcinomas, but not sarcomas, are refractory to regulatory T cell-depletion therapy. Cancer Sci 101, 855-861, doi: 10.1111/j.1349-7006.2009.01469.x (2010).
43. Youn, J. I., Nagaraj, S., Collazo, M., Gabrilovich, D. I. Subsets of myeloid-derived suppressor cells in tumour-bearing mice. J Immunol 181, 5791-5802, doi: 10.4049/jimmunol.181.8.5791 (2008).
44. Gabrilovich, D. I., Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9, 162-174, doi: 10.1038/nri2506 (2009).
45. Ostrand-Rosenberg, S., Sinha, P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182, 4499-4506, doi: 10.4049/jimmunol.0802740 (2009).
46. Peranzoni, E. et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 22, 238-244, doi: 10.1016/j.coi.2010.01.021 (2010).
47. Dolcetti, L. et al. Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol 40, 22-35, doi: 10.1002/eji.200939903 (2010).
48. Sumida, K. et al. Anti-IL-6 receptor mAb eliminates myeloid-derived suppressor cells and inhibits tumour growth by enhancing T-cell responses. Eur J Immunol 42, 2060-2072, doi: 10.1002/eji.201142335 (2012).
49. Kusmartsev, S. et al. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin Cancer Res 14, 8270-8278, doi: 10.1158/1078-0432.CCR-08-0165 (2008).
50. Diaz-Montero, C. M. et al. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumour burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 58, 49-59, doi: 10.1007/s00262-008-0523-4 (2009).
51. Solito, S. et al. A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood 118, 2254-2265, doi: 10.1182/blood-2010-12-325753 (2011).
52. Gros, A. et al. Myeloid cells obtained from the blood but not from the tumour can suppress T-cell proliferation in patients with melanoma. Clin Cancer Res 18, 5212-5223, doi: 10.1158/1078-0432.CCR-12-1108 (2012).
53. Bronte, V., Zanovello, P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 5, 641-654, doi: 10.1038/nri1668 (2005).
54. Nagaraj, S. et al. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med 13, 828-835, doi: 10.1038/nm1609 (2007).
55. Sinha, P. et al. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol 181, 4666-4675, doi: 10.4049/jimmunol.181.7.4666 (2008).
56. Lu, T. et al. Tumor-infiltrating myeloid cells induce tumour cell resistance to cytotoxic T cells in mice. J Clin Invest 121, 4015-4029, doi: 10.1172/JCI45862 (2011).
57. Gabrilovich, D. I., Ostrand-Rosenberg, S., Bronte, V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 12, 253-268, doi: 10.1038/nri3175 (2012).
58. Lu, T., Gabrilovich, D. I. Molecular pathways: tumour-infiltrating myeloid cells and reactive oxygen species in regulation of tumour microenvironment. Clin Cancer Res 18, 4877-4882, doi: 10.1158/1078-0432.CCR-11-2939 (2012).
59. Li, H., Han, Y., Guo, Q., Zhang, M., Cao, X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol 182, 240-249, doi: 10.4049/jimmunol.182.1.240 (2009).
60. Hirano, T. Interleukin 6 in autoimmune and inflammatory diseases: a personal memoir. Proc Jpn Acad Ser B Phys Biol Sci 86, 717-730, doi: 10.2183/pjab.86.717 (2010).
61. Teramura, M., Kobayashi, S., Hoshino, S., Oshimi, K., Mizoguchi, H. Interleukin-11 enhances human megakaryocytopoiesis in vitro. Blood 79, 327-331 (1992).
62. Putoczki, T., Ernst, M. More than a sidekick: the IL-6 family cytokine IL-11 links inflammation to cancer. J Leukoc Biol 88, 1109-1117, doi: 10.1189/jlb.0410226 (2010).
63. Gao, Y. B. et al. Enhanced production of CTGF and IL-11 from highly metastatic hepatoma cells under hypoxic conditions: an implication of hepatocellular carcinoma metastasis to bone. J Cancer Res Clin Oncol 139, 669-679, doi: 10.1007/s00432-012-1370-4 (2013).
64. Ren, L., Wang, X., Dong, Z., Liu, J., Zhang, S. Bone metastasis from breast cancer involves elevated IL-11 expression and the gp130/STAT3 pathway. Med Oncol 30, 634, doi: 10.1007/s12032-013-0634-4 (2013).
65. Nakayama, T. et al. Expression of interleukin-11 (IL-11) and IL-11 receptor alpha in human gastric carcinoma and IL-11 upregulates the invasive activity of human gastric carcinoma cells. Int J Oncol 30, 825-833, doi: 10.3892/ijo.30.4.825 (2007).
66. Necula, L. G. et al. IL-6 and IL-11 as markers for tumour aggressiveness and prognosis in gastric adenocarcinoma patients without mutations in Gp130 subunits. J Gastrointestin Liver Dis 21, 23-29 (2012).
67. Xiang, Z. L., Zeng, Z. C., Fan, J., Tang, Z. Y., Zeng, H. Y. Expression of connective tissue growth factor and interleukin-11 in intratumoral tissue is associated with poor survival after curative resection of hepatocellular carcinoma. Mol Biol Rep 39, 6001-6006, doi: 10.1007/s11033-011-1413-y (2012).
68. Bellone, G. et al. Cytokine expression profile in human pancreatic carcinoma cells and in surgical specimens: implications for survival. Cancer Immunol Immunother 55, 684-698, doi: 10.1007/s00262-005-0047-0 (2006).
69. Putoczki, T. L. et al. Interleukin-11 is the dominant IL-6 family cytokine during gastrointestinal tumourigenesis and can be targeted therapeutically. Cancer Cell 24, 257-271, doi: 10.1016/j.ccr.2013.06.017 (2013).
70. Campbell, C. L. et al. Interleukin-11 receptor expression in primary ovarian carcinomas. Gynecol Oncol 80, 121-127, doi: 10.1006/gyno.2000.6064 (2001).
71. Mace, T. A. et al. Pancreatic Cancer-Associated Stellate Cells Promote Differentiation of Myeloid-Derived Suppressor Cells in a STAT3-Dependent Manner. Cancer Res 73, 3007-3018, doi: 10.1158/0008-5472.CAN-12-4601 (2013).
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