Serum amyloid A3 exacerbates cancer by enhancing the suppressive capacity of myeloid-derived suppressor cells via TLR2-dependent STAT3 activation

European Journal of Immunology

Volumn 44, Issue 6, 2014, Pages 1672-1684

  Lee, Jung Mi ^a   Kim, Eun Kyung ^a   Seo, Hyungseok ^b   Jeon, Insu ^b   Chae, Min Ji ^a   Park, Young Jun ^a   Song, Boyeong ^b   Kim, Yun Sun ^a   Kim, Yeon Jeong ^c   Ko, Hyun Jeong ^d   Kang, Chang Yuil ^a,b  

^a Seoul National University   (South Korea)

^b Seoul National University   (South Korea)

^c Inje University   (South Korea)

^d Kangwon National University   (South Korea)

Author keywords

Myeloid derived suppressor cell; Serum amyloid A3; STAT3; TLR2; Tumor microenvironment

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; SERUM AMYLOID A; SERUM AMYLOID A3; STAT3 PROTEIN; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; BONE MARROW CELL; CANCER GROWTH; CANCER SURVIVAL; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE EXACERBATION; GENE EXPRESSION; IN VIVO STUDY; MOLECULAR MECHANICS; MONOCYTE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

MYELOID-DERIVED SUPPRESSOR CELL; SERUM AMYLOID A3; STAT3; TLR2; TUMOR MICROENVIRONMENT;

ANIMALS; CELL LINE, TUMOR; INFLAMMATION; MICE; MICE, INBRED BALB C; MYELOID CELLS; NEOPLASMS, EXPERIMENTAL; SERUM AMYLOID A PROTEIN; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 2; TUMOR MICROENVIRONMENT;

EID: 84901818801     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343867     Document Type: Article

References (42)

1. Mantovani, A., Allavena, P., Sica, A. and Balkwill, F., Cancer-related inflammation. Nature 2008. 454: 436-444.
2. Coussens, L. M. and Werb, Z., Inflammation and cancer. Nature 2002. 420: 860-867.
3. Mantovani, A., Garlanda, C. and Allavena, P., Molecular pathways and targets in cancer-related inflammation. Ann. Med. 2010. 42: 161-170.
4. Porta, C., Riboldi, E. and Sica, A., Mechanisms linking pathogens-associated inflammation and cancer. Cancer Lett. 2011. 305: 250-262.
5. Vakkila, J. and Lotze, M. T., Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol. 2004. 4: 641-648.
6. Ostrand-Rosenberg, S. and Sinha, P., Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 2009. 182: 4499-4506.
7. Malle, E., Sodin-Semrl, S. and Kovacevic, A., Serum amyloid A: an acute-phase protein involved in tumour pathogenesis. Cell. Mol. Life. Sci. 2009. 66: 9-26.
8. Vlasova, M. A. and Moshkovskii, S. A., Molecular interactions of acute phase serum amyloid A: possible involvement in carcinogenesis. Biochemistry (Mosc.) 2006. 71: 1051-1059.
9. Uhlar, C. M. and Whitehead, A. S., Serum amyloid A, the major vertebrate acute-phase reactant. Eur. J. Biochem. 1999. 265: 501-523.
10. Jensen, L. E. and Whitehead, A. S., Regulation of serum amyloid A protein expression during the acute-phase response. Biochem. J. 1998. 334(Pt 3): 489-503.
11. Kumon, Y., Suehiro, T., Hashimoto, K., Nakatani, K. and Sipe, J. D., Local expression of acute phase serum amyloid A mRNA in rheumatoid arthritis synovial tissue and cells. J. Rheumatol. 1999. 26: 785-790.
12. Cunnane, G., Amyloid precursors and amyloidosis in inflammatory arthritis. Curr. Opin. Rheumatol. 2001. 13: 67-73.
13. Glojnaric, I., Casl, M. T., Simic, D. and Lukac, J., Serum amyloid A protein (SAA) in colorectal carcinoma. Clin. Chem. Lab. Med. 2001. 39: 129-133.
14. Khan, N., Cromer, C. J., Campa, M. and Patz, E. F., Jr., Clinical utility of serum amyloid A and macrophage migration inhibitory factor as serum biomarkers for the detection of nonsmall cell lung carcinoma. Cancer 2004. 101: 379-384.
15. Kimura, M., Tomita, Y., Imai, T., Saito, T., Katagiri, A., Ohara-Mikami, Y., Matsudo, T. et al., Significance of serum amyloid A on the prognosis in patients with renal cell carcinoma. Cancer 2001. 92: 2072-2075.
16. Yokoi, K., Shih, L. C., Kobayashi, R., Koomen, J., Hawke, D., Li, D., Hamilton, S. R. et al., Serum amyloid A as a tumor marker in sera of nude mice with orthotopic human pancreatic cancer and in plasma of patients with pancreatic cancer. Int. J. Oncol. 2005. 27: 1361-1369.
17. Kristiansson, M. H., Bhat, V. B., Babu, I. R., Wishnok, J. S. and Tannenbaum, S. R., Comparative time-dependent analysis of potential inflammation biomarkers in lymphoma-bearing SJL mice. J. Proteome Res. 2007. 6: 1735-1744.
18. Juan, H. F., Chen, J. H., Hsu, W. T., Huang, S. C., Chen, S. T., Yi-Chung Lin, J., Chang, Y. W. et al., Identification of tumor-associated plasma biomarkers using proteomic techniques: from mouse to human. Proteomics 2004. 4: 2766-2775.
19. Liu, D. H., Wang, X. M., Zhang, L. J., Dai, S. W., Liu, L. Y., Liu, J. F., Wu, S. S. et al., Serum amyloid A protein: a potential biomarker correlated with clinical stage of lung cancer. Biomed. Environ. Sci. 2007. 20: 33-40.
20. Cho, W. C., Yip, T. T., Yip, C., Yip, V., Thulasiraman, V., Ngan, R. K., Lau, W. H. et al., Identification of serum amyloid a protein as a potentially useful biomarker to monitor relapse of nasopharyngeal cancer by serum proteomic profiling. Clin. Cancer Res. 2004. 10: 43-52.
21. De Santo, C., Arscott, R., Booth, S., Karydis, I., Jones, M., Asher, R., Salio, M. et al., Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat. Immunol. 2010. 11: 1039-1046.
22. He, R. L., Zhou, J., Hanson, C. Z., Chen, J., Cheng, N. and Ye, R. D., Serum amyloid A induces G-CSF expression and neutrophilia via Toll-like receptor 2. Blood 2009. 113: 429-437.
23. Li, Y., Cai, L., Wang, H., Wu, P., Gu, W., Chen, Y., Hao, H. et al., Pleiotropic regulation of macrophage polarization and tumorigenesis by formyl peptide receptor-2. Oncogene 2011. 30: 3887-3899.
24. Kim, Y. S., Kim, Y. J., Lee, J. M., Kim, E. K., Park, Y. J., Choe, S. K., Ko, H. J. et al., Functional changes in myeloid-derived suppressor cells (MDSCs) during tumor growth: FKBP51 contributes to the regulation of the immunosuppressive function of MDSCs. J. Immunol. 2012. 188: 4226-4234.
25. Ather, J. L., Ckless, K., Martin, R., Foley, K. L., Suratt, B. T., Boyson, J. E., Fitzgerald, K. A. et al., Serum amyloid A activates the NLRP3 inflammasome and promotes Th17 allergic asthma in mice. J. Immunol. 2011. 187: 64-73.
26. Kim, S., Takahashi, H., Lin, W. W., Descargues, P., Grivennikov, S., Kim, Y., Luo, J. L. et al., Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009. 457: 102-106.
27. Chalmin, F., Ladoire, S., Mignot, G., Vincent, J., Bruchard, M., Remy-Martin, J. P., Boireau, W. 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: 457-471.
28. Gabrilovich, D. I. and Nagaraj, S., Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009. 9: 162-174.
29. Sinha, P., Clements, V. K., Fulton, A. M. and Ostrand-Rosenberg, S., Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res. 2007. 67: 4507-4513.
30. Bunt, S. K., Sinha, P., Clements, V. K., Leips, J. and Ostrand-Rosenberg, S., Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 2006. 176: 284-290.
31. Bunt, S. K., Yang, L., Sinha, P., Clements, V. K., Leips, J. and Ostrand-Rosenberg, S., Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res. 2007. 67: 10019-10026.
32. Tu, S., Bhagat, G., Cui, G., Takaishi, S., Kurt-Jones, E. A., Rickman, B., Betz, K. S. et al., Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 2008. 14: 408-419.
33. Cheng, L., Wang, J., Li, X., Xing, Q., Du, P., Su, L. and Wang, S., Interleukin-6 induces Gr-1+CD11b+ myeloid cells to suppress CD8+ T cell-mediated liver injury in mice. PLoS One 2011. 6: e17631.
34. Almand, B., Clark, J. I., Nikitina, E., van Beynen, J., English, N. R., Knight, S. C., Carbone, D. P. et al., Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 2001. 166: 678-689.
35. Sinha, P., Okoro, C., Foell, D., Freeze, H. H., Ostrand-Rosenberg, S. and Srikrishna, G., Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J. Immunol. 2008. 181: 4666-4675.
36. Cheng, P., Corzo, C. A., Luetteke, N., Yu, B., Nagaraj, S., Bui, M. M., Ortiz, M. 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: 2235-2249.
37. Markiewski, M. M., DeAngelis, R. A., Benencia, F., Ricklin-Lichtsteiner, S. K., Koutoulaki, A., Gerard, C., Coukos, G. et al., Modulation of the antitumor immune response by complement. Nat. Immunol. 2008. 9: 1225-1235.
38. Urieli-Shoval, S., Shubinsky, G., Linke, R. P., Fridkin, M., Tabi, I. and Matzner, Y., Adhesion of human platelets to serum amyloid A. Blood 2002. 99: 1224-1229.
39. Preciado-Patt, L., Hershkoviz, R., Fridkin, M. and Lider, O., Serum amyloid A binds specific extracellular matrix glycoproteins and induces the adhesion of resting CD4+ T cells. J. Immunol. 1996. 156: 1189-1195.
40. Sander, L. E., Sackett, S. D., Dierssen, U., Beraza, N., Linke, R. P., Muller, M., Blander, J. M. et al., Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J. Exp. Med. 2010. 207: 1453-1464.
41. Hiratsuka, S., Watanabe, A., Sakurai, Y., Akashi-Takamura, S., Ishibashi, S., Miyake, K., Shibuya, M. et al., The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat. Cell Biol. 2008. 10: 1349-1355.
42. Chang, S. Y., Lee, K. C., Ko, S. Y., Ko, H. J. and Kang, C. Y., Enhanced efficacy of DNA vaccination against Her-2/neu tumor antigen by genetic adjuvants. Int. J. Cancer 2004. 111: 86-95.