Cross-talk among Myeloid-derived suppressor cells, Macrophages, and Tumor cells impacts the inflammatory milieu of solid tumors

Journal of Leukocyte Biology

Volumn 96, Issue 6, 2014, Pages 1109-1118

  Beury, Daniel W ^a   Parker, Katherine H ^a   Nyandjo, Maeva ^a   Sinha, Pratima ^a   Carter, Kayla A ^a   Ostrand Rosenberg, Suzanne ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Cancer; Cytokines; IL 10; IL 6; Nitric oxide; Tumor microenvironment

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 27; INTERLEUKIN 4; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; NITRIC OXIDE; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; IL10 PROTEIN, MOUSE; INTERLEUKIN-6, MOUSE; STAT3 PROTEIN; STAT3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INFLAMMATORY MILIEU; MACROPHAGE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PROTEIN INTERACTION; SOLID TUMOR; STROMA CELL; SUPPRESSOR CELL; TUMOR CELL LINE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CANCER TRANSPLANTATION; CELL COMMUNICATION; COLON TUMOR; DISEASE COURSE; EXPERIMENTAL MAMMARY NEOPLASM; EXPERIMENTAL NEOPLASM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; ISOGRAFT; METABOLISM; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

ANIMALS; CELL COMMUNICATION; CELL LINE, TUMOR; COLONIC NEOPLASMS; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-6; MACROPHAGES; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID CELLS; NEOPLASM TRANSPLANTATION; NEOPLASMS, EXPERIMENTAL; NITRIC OXIDE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STROMAL CELLS; TRANSPLANTATION, ISOGENEIC; TUMOR MICROENVIRONMENT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84914096079     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0414-210R     Document Type: Article

References (39)

1. Shiao, S. L., Ganesan, A. P., Rugo, H. S., Coussens, L. M. (2011) Immune microenvironments in solid tumors: new targets for therapy. Genes Dev. 25, 2559-2572.
2. Yang, L., Pang, Y., Moses, H. L. (2010) TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol. 31, 220-227.
3. Gabrilovich, D. I., Ostrand-Rosenberg, S., Bronte, V. (2012) Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12, 253-268.
4. Viola, A., Sarukhan, A., Bronte, V., Molon, B. (2012) The pros and cons of chemokines in tumor immunology. Trends Immunol. 33, 496-504.
5. Sica, A., Larghi, P., Mancino, A., Rubino, L., Porta, C., Totaro, M. G., Rimoldi, M., Biswas, S. K., Allavena, P., Mantovani, A. (2008) Macrophage polarization in tumour progression. Semin. Cancer Biol. 18, 349-355.
6. Ostrand-Rosenberg, S., Sinha, P. (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 182, 4499-4506.
7. Bunt, S. K., Clements, V. K., Hanson, E. M., Sinha, P., Ostrand-Rosenberg, S. (2009) Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J. Leukoc. Biol. 85, 996-1004.
8. 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, 977-983.
9. Becker, C., Fantini, M. C., Wirtz, S., Nikolaev, A., Lehr, H. A., Galle, P. R., Rose-John, S., Neurath, M. F. (2005) IL-6 signaling promotes tumor growth in colorectal cancer. Cell Cycle 4, 217-220.
10. Su, Y. W., Xie, T. X., Sano, D., Myers, J. N. (2011) IL-6 stabilizes Twist and enhances tumor cell motility in head and neck cancer cells through activation of casein kinase 2. PLoS One 6, e19412.
11. Santer, F. R., Malinowska, K., Culig, Z., Cavarretta, I. T. (2010) Interleukin-6 trans-signalling differentially regulates proliferation, migration, adhesion and maspin expression in human prostate cancer cells. Endocr. Relat. Cancer 17, 241-253.
12. Balkwill, F. (2006) TNF-alpha in promotion and progression of cancer. Cancer Metastasis Rev. 25, 409-416.
13. Hussain, S. P., Trivers, G. E., Hofseth, L. J., He, P., Shaikh, I., Mechanic, L. E., Doja, S., Jiang, W., Subleski, J., Shorts, L., Haines, D., Laubach, V. E., Wiltrout, R. H., Djurickovic, D., Harris, C. C. (2004) Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res. 64, 6849-6853.
14. Bronte, V., Zanovello, P. (2005) Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5, 641-654.
15. Mocellin, S., Marincola, F. M., Young, H. A. (2005) Interleukin-10 and the immune response against cancer: a counterpoint. J. Leukoc. Biol. 78, 1043-1051.
16. Sinha, P., Parker, K. H., Horn, L., Ostrand-Rosenberg, S. (2012) Tumorinduced myeloid-derived suppressor cell function is independent of IFNgamma and IL-4Ralpha. Eur. J. Immunol. 42, 2052-2059.
17. Bunt, S. K., Sinha, P., Clements, V. K., Leips, J., Ostrand-Rosenberg, S. (2006) Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 176, 284-290.
18. Sinha, P., Clements, V. K., Ostrand-Rosenberg, S. (2005) Reduction of myeloidderived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J. Immunol. 174, 636-645.
19. Lippitz, B. E. (2013) Cytokine patterns in patients with cancer: a systematic review. Lancet Oncol. 14, e218-28.
20. Tsukamoto, H., Nishikata, R., Senju, S., Nishimura, Y. (2013) Myeloidderived suppressor cells attenuate TH1 development through IL-6 production to promote tumor progression. Cancer Immunol. Res. 1, 64-76.
21. Berg, D. J., Davidson, N., Kuhn, R., Muller, W., Menon, S., Holland, G., Thompson-Snipes, L., Leach, M. W., Rennick, D. (1996) Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J. Clin. Invest. 98, 1010-1020.
22. Neven, B., Mamessier, E., Bruneau, J., Kaltenbach, S., Kotlarz, D., Suarez, F., Masliah-Planchon, J., Billot, K., Canioni, D., Frange, P., Radford-Weiss, I., Asnafi, V., Murugan, D., Bole, C., Nitschke, P., Goulet, O., Casanova, J. L., Blanche, S., Picard, C., Hermine, O., Rieux-Laucat, F., Brousse, N., Davi, F., Baud, V., Klein, C., Nadel, B., Ruemmele, F., Fischer, A. (2013) A Mendelian predisposition to B-cell lymphoma caused by IL-10R deficiency. Blood 122, 3713-3722.
23. Emmerich, J., Mumm, J. B., Chan, I. H., LaFace, D., Truong, H., McClanahan, T., Gorman, D. M., Oft, M. (2012) IL-10 directly activates and expands tumor-resident CD8(+) T cells without de novo infiltration from secondary lymphoid organs. Cancer Res. 72, 3570-3581.
24. Mumm, J. B., Emmerich, J., Zhang, X., Chan, I., Wu, L., Mauze, S., Blaisdell, S., Basham, B., Dai, J., Grein, J., Sheppard, C., Hong, K., Cutler, C., Turner, S., LaFace, D., Kleinschek, M., Judo, M., Ayanoglu, G., Langowski, J., Gu, D., Paporello, B., Murphy, E., Sriram, V., Naravula, S., Desai, B., Medicherla, S., Seghezzi, W., McClanahan, T., Cannon-Carlson, S., Beebe, A. M., Oft, M. (2011) IL-10 elicits IFNgamma-dependent tumor immune surveillance. Cancer Cell 20, 781-796.
25. Sato, T., Terai, M., Tamura, Y., Alexeev, V., Mastrangelo, M. J., Selvan, S. R. (2011) Interleukin 10 in the tumor microenvironment: a target for anticancer immunotherapy. Immunol. Res. 51, 170-182.
26. Jacobs, F., Chaussabel, D., Truyens, C., Leclerq, V., Carlier, Y., Goldman, M., Vray, B. (1998) IL-10 up-regulates nitric oxide (NO) synthesis by lipopolysaccharide (LPS)-activated macrophages: improved control of Trypanosoma cruzi infection. Clin. Exp. Immunol. 113, 59-64.
27. Qasimi, P., Ming-Lum, A., Ghanipour, A., Ong, C. J., Cox, M. E., Ihle, J., Cacalano, N., Yoshimura, A., Mui, A. L. (2006) Divergent mechanisms utilized by SOCS3 to mediate interleukin-10 inhibition of tumor necrosis factor alpha and nitric oxide production by macrophages. J. Biol. Chem. 281, 6316-6324.
28. Smith, C., Chang, M. Y., Parker, K. H., Beury, D. W., DuHadaway, J. B., Flick, H. E., Boulden, J., Sutanto-Ward, E., Soler, A. P., Laury-Kleintop, L. D., Mandik-Nayak, L., Metz, R., Ostrand-Rosenberg, S., Prendergast, G. C., Muller, A. J. (2012) IDO is a nodal pathogenic driver of lung cancer and metastasis development. Cancer Discov. 2, 722-735.
29. 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, 790-802.
30. Bunt, S. K., Yang, L., Sinha, P., Clements, V. K., Leips, J., Ostrand-Rosenberg, S. (2007) Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res. 67, 10019-10026.
31. Ouyang, W., Rutz, S., Crellin, N. K., Valdez, P. A., Hymowitz, S. G. (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 29, 71-109.
32. Lee, J. H., Lee, G. T., Woo, S. H., Ha, Y. S., Kwon, S. J., Kim, W. J., Kim, I. Y. (2013) BMP-6 in renal cell carcinoma promotes tumor proliferation through IL-10-dependent M2 polarization of tumor-associated macrophages. Cancer Res. 73, 3604-3614.
33. Dennis, K. L., Wang, Y., Blatner, N. R., Wang, S., Saadalla, A., Trudeau, E., Roers, A., Weaver, C. T., Lee, J. J., Gilbert, J. A., Chang, E. B., Khazaie, K. (2013) Adenomatous polyps are driven by microbe-instigated focal inflammation and are controlled by IL-10-producing T cells. Cancer Res. 73, 5905-5913.
34. Tanikawa, T., Wilke, C. M., Kryczek, I., Chen, G. Y., Kao, J., Nunez, G., Zou, W. (2012) Interleukin-10 ablation promotes tumor development, growth, and metastasis. Cancer Res. 72, 420-429.
35. Niemand, C., Nimmesgern, A., Haan, S., Fischer, P., Schaper, F., Rossaint, R., Heinrich, P. C., Muller-Newen, G. (2003) Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J. Immunol. 170, 3263-3272.
36. Vallania, F., Schiavone, D., Dewilde, S., Pupo, E., Garbay, S., Calogero, R., Pontoglio, M., Provero, P., Poli, V. (2009) Genome-wide discovery of functional transcription factor binding sites by comparative genomics: the case of Stat3. Proc. Natl. Acad. Sci. USA 106, 5117-5122.
37. Hutchins, A. P., Diez, D., Miranda-Saavedra, D. (2013) The IL-10/STAT3-mediated anti-inflammatory response: recent developments and future challenges. Brief Funct. Genomics 12, 489-498.
38. Morales, J. K., Saleem, S. J., Martin, R. K., Saunders, B. L., Barnstein, B. O., Faber, T. W., Pullen, N. A., Kolawole, E. M., Brooks, K. B., Norton, S. K., Sturgill, J., Graham, L., Bear, H. D., Urban J. F., Jr., Lantz, C. S., Conrad, D. H., Ryan, J. J. (2014) Myeloid-derived suppressor cells enhance IgE-mediated mast cell responses. J. Leukoc. Biol. 95, 643-650.
39. 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. (2012) Cutting edge: mast cells critically augment myeloid-derived suppressor cell activity. J. Immunol. 189, 511-515.