The myeloid immune signature of enterotoxigenic Bacteroides fragilis-induced murine colon tumorigenesis

Mucosal Immunology

Volumn 10, Issue 2, 2017, Pages 421-433

  Thiele Orberg, E ^a,b   Fan, H ^a,b   Tam, A J ^a,b   Dejea, C M ^b,c   Destefano Shields, C E ^b,c   Wu, S ^b,c   Chung, L ^a,b,d   Finard, B B ^a,b   Wu, X ^b,c   Fathi, P ^b,c   Ganguly, S ^b,c   Fu, J ^a,b   Pardoll, D M ^a,b   Sears, C L ^a,b,c   Housseau, F ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; NITRIC OXIDE SYNTHASE; ARG1 PROTEIN, MOUSE; ARGINASE; BACTERIAL TOXIN; FRAGILYSIN; INDUCIBLE NITRIC OXIDE SYNTHASE; METALLOPROTEINASE; NOS2 PROTEIN, MOUSE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARG1 GENE; ARTICLE; BACTEROIDES FRAGILIS; BONE MARROW CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL INFILTRATION; CELL POPULATION; COLON CANCER; COLON TUMOR; CONTROLLED STUDY; ENTEROTOXIGENIC BACTEROIDES FRAGILIS; EPITHELIUM CELL; ESCHERICHIA COLI; FLOW CYTOMETRY; FUSOBACTERIUM NUCLEATUM; GENE; GENE EXPRESSION; HUMAN; INTERMETHOD COMPARISON; LYMPHOCYTE PROLIFERATION; MOUSE; MYELOID-DERIVED SUPPRESSOR CELL; MYELOPOIESIS; NONHUMAN; NOS1 GENE; PATHOGENESIS; RISK FACTOR; STEADY STATE; TUMOR ASSOCIATED LEUKOCYTE; UPREGULATION; ANIMAL; BACTEROIDES INFECTION; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; COLON; COLORECTAL TUMOR; DISEASE MODEL; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MUTANT MOUSE STRAIN; PATHOLOGY; T LYMPHOCYTE; TUMOR SUPPRESSOR GENE;

ANIMALS; ARGINASE; BACTERIAL TOXINS; BACTEROIDES FRAGILIS; BACTEROIDES INFECTIONS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COLON; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GENES, APC; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-17; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MYELOID-DERIVED SUPPRESSOR CELLS; NITRIC OXIDE SYNTHASE TYPE II; T-LYMPHOCYTES; TRANSCRIPTOME;

EID: 85014554479     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2016.53     Document Type: Article

References (34)

1. Prindiville, T.P., Sheikh, R.A., Cohen, S.H., Tang, Y.J., Cantrell, M.C. & Silva, J. Jr. Bacteroides fragilis enterotoxin gene sequences in patients with inflammatory bowel disease. Emerg. Infect. Dis. 6, 171-174 (2000).
2. Toprak, N.U. et al. A possible role of Bacteroides fragilis enterotoxin in the aetiology of colorectal cancer. Clin. Microbiol. Infect. 12, 782-786 (2006).
3. Boleij, A. et al. The Bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients. Clin. Infect. Dis. 60, 208-215 (2015).
4. Wu, S. et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17Tcell responses. Nat. Med. 15, 1016-1022 (2009).
5. Tosolini, M. et al. Clinical impact of different classes of infiltrating Tcytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 71, 1263-1271 (2011).
6. Sears, C.L. & Garrett, W.S. Microbes, microbiota, and colon cancer. Cell. Host Microbe 15, 317-328 (2014).
7. Ma, S. et al. IL-17A produced by gammadelta T cells promotes tumor growth in hepatocellular carcinoma. Cancer Res. 74, 1969-1982 (2014).
8. He, D. et al. IL-17 promotes tumor development through the induction of tumor promoting microenvironments at tumor sites and myeloid-derived suppressor cells. J. Immunol. 184, 2281-2288 (2010).
9. Wang, L., Yi, T., Zhang, W., Pardoll, D.M. & Yu, H. IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res. 70, 10112-10120 (2010).
10. Bronte, V. Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions. Eur. J. Immunol. 39, 2670-2672 (2009).
11. Gabrilovich, D.I., Ostrand-Rosenberg, S. & Bronte, V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12, 253-268 (2012).
12. Corzo, C.A. et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207, 2439-2453 (2010).
13. Gabrilovich, D.I. & Nagaraj, S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174 (2009).
14. Ostrand-Rosenberg, S. & Sinha, P. Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 182, 4499-4506 (2009).
15. Gallina, G. et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8 T cells. J. Clin. Invest. 116, 2777-2790 (2006).
16. Sinha, P., Parker, K.H., Horn, L. & Ostrand-Rosenberg, S. Tumor-induced myeloid-derived suppressor cell function is independent of IFN-gamma and IL-4Ralpha. Eur. J. Immunol. 42, 2052-2059 (2012).
17. Chang, S.H. et al. T helper 17 cells play a critical pathogenic role in lung cancer. Proc. Natl. Acad. Sci. USA 111, 5664-5669 (2014).
18. Kostic, A.D. et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell. Host Microbe 14, 207-215 (2013).
19. Arthur, J.C. et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338, 120-123 (2012).
20. Housseau, F. et al. Redundant innate and adaptive sources of IL-17 production drive colon tumorigenesis. Cancer Res. 76, 2115-2124 (2016).
21. Katz, J.B., Muller, A.J. & Prendergast, G.C. Indoleamine 2, 3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol. Rev. 222, 206-221 (2008).
22. Huang, B. et al. Gr-1CD115 immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 66, 1123-1131 (2006).
23. Wu, P. et al. GammadeltaT17 cells promote the accumulation and expansion ofmyeloid-derived suppressor cells in human colorectal cancer. Immunity 40, 785-800 (2014).
24. Wang, L., Yi, T., Kortylewski, M., Pardoll, D.M., Zeng, D. & Yu, H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J. Exp. Med. 206, 1457-1464 (2009).
25. Sinha, P., Okoro, C., Foell, D., Freeze, H.H., Ostrand-Rosenberg, S. & Srikrishna, G. Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J. Immunol. 181, 4666-4675 (2008).
26. Sears, C.L., Geis, A.L. & Housseau, F. Bacteroides fragilis subverts mucosal biology: from symbiont to colon carcinogenesis. J. Clin. Invest. 124, 4166-4172 (2014).
27. Chung, A.S. et al. An interleukin-17-mediated paracrine network promotes tumor resistance to anti-Angiogenic therapy. Nat. Med. 19, 1114-1123 (2013).
28. Wu, S., Morin, P.J., Maouyo, D. & Sears, C.L. Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology 124, 392-400 (2003).
29. Wu, S., Powell, J., Mathioudakis, N., Kane, S., Fernandez, E. & Sears, C.L. Bacteroides fragilis enterotoxin induces intestinal epithelial cell secretion of interleukin-8 through mitogen-Activated protein kinases and a tyrosine kinase-regulated nuclear factor-kappaB pathway. Infect. Immun. 72, 5832-5839 (2004).
30. Highfill, S.L. et al. Disruption of CXCR2-mediated MDSC tumor trafficking enhances anti-PD1 efficacy. Sci. Transl. Med. 6, 237ra-267r (2014).
31. DeStefano Shields, C.E. et al. Reduction of murine colon tumorigenesis driven by enterotoxigenic Bacteroides fragilis using cefoxitin treatment. J. Infect. Dis., pii:jiw069 (e-pub ahead of print) (2016).
32. Geis, A.L. et al. Regulatory Tcell response to enterotoxigenic Bacteroides fragilis colonization triggers IL-17-dependent colon carcinogenesis. Cancer. Discov. 5, 1098-1109 (2015).
33. Ortiz, M.L. et al. Immature myeloid cells directly contribute to skin tumor development by recruiting IL-17-producing CD4 T cells. J. Exp. Med. 212, 351-367 (2015).
34. Kusmartsev, S.A., Li, Y. & Chen, S.H. Gr-1 myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation. J. Immunol. 165, 779-785 (2000).