Foxp3+IL-17+ T cells promote development of cancer-initiating cells in colorectal cancer

Journal of Leukocyte Biology

Volumn 89, Issue 1, 2011, Pages 85-91

  Yang, Shaobo ^a   Wang, Binquan ^d   Guan, Chunying ^b   Wu, Benyan ^a   Cai, Changhao ^a   Wang, Mengwei ^a   Zhang, Binsheng ^b   Liu, Tao ^d   Yang, Pingchang ^b,c  

^a CHINESE PLA GENERAL HOSPITAL   (China)

^b CHANGZHOU UNIVERSITY   (China)

^c MCMASTER UNIVERSITY   (Canada)

^d SHANXI MEDICAL UNIVERSITY   (China)

Author keywords

Hypoxia; T lymphocyte; Tumor

Indexed keywords

CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR3; CXCL11 CHEMOKINE; INTERLEUKIN 17; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADULT; AGED; ARTICLE; CD68 CELL; CELL; CHEMOTAXIS; CLINICAL ARTICLE; COLON CARCINOGENESIS; COLONY FORMATION; COLORECTAL CANCER; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; WESTERN BLOTTING;

ADULT; AGED; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CELL HYPOXIA; CHEMOKINE CXCL11; CHEMOTAXIS; COLORECTAL NEOPLASMS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-17; MACROPHAGES; MALE; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASTIC STEM CELLS; PROTO-ONCOGENE PROTEINS C-AKT; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TUMOR MARKERS, BIOLOGICAL;

EID: 79251557498     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0910506     Document Type: Article

References (30)

1. Blatner, N. R., Bonertz, A., Beckhove, P., Cheon, E. C., Krantz, S. B., Strouch, M., Weitz, J., Koch, M., Halverson, A. L., Bentrem, D. J., Khazaie, K. (2010) In colorectal cancer mast cells contribute to systemic regulatory T-cell dysfunction. Proc. Natl. Acad. Sci. USA 107, 6430-6435.
2. Jarnicki, A. G., Lysaght, J., Todryk, S., Mills, K. H. (2006) Suppression of antitumor immunity by IL-10 and TGF-β-producing T cells infiltrating the growing tumor: influence of tumor environment on the induction of CD4+ and CD8+ regulatory T cells. J. Immunol. 177, 896-904.
3. Zou, W. (2006) Regulatory T cells, tumor immunity and immunotherapy. Nat. Rev. Immunol. 6, 295-307.
4. Zou, W., Restifo, N. P. (2010) T(H)17 cells in tumor immunity and immunotherapy. Nat. Rev. Immunol. 10, 248-256.
5. Ahern, P. P., Izcue, A., Maloy, K. J., Powrie, F. (2008) The interleukin-23 axis in intestinal inflammation. Immunol. Rev. 226, 147-159.
6. Wägsäter, D., Löfgren, S., Hugander, A., Dimberg, J. (2006) Expression of interleukin-17 in human colorectal cancer. Anticancer Res. 26, 4213-4216.
7. Wu, S., Rhee, K.J., Albesiano, E., Rabizadeh, S., Wu, X., Yen, H.R., Huso, D.L., Brancati, F.L., Wick, E., McAllister, F., Housseau, F., Pardoll, D. M., Sears, C. L. (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat. Med. 15, 1016-1022.
8. Su, X., Ye, J., Hsueh, E. C., Zhang, Y., Hoft, D. F., Peng, G. (2010) Tumor microenvironments direct the recruitment and expansion of human Th17 cells. J. Immunol. 184, 1630-1641.
9. Voo, K. S., Wang, Y. H., Santori, F. R., Boggiano, C., Wang, Y. H., Arima, K., Bover, L., Hanabuchi, S., Khalili, J., Marinova, E., Zheng, B., Littman, D. R., Liu, Y. J. (2009) Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc. Natl. Acad. Sci. USA 106, 4793-4798.
10. Zheng, J., Sun, X., Wang, W., Lu, S. (2010) Hypoxia-inducible factor-1α modulates the down-regulation of the homeodomain protein CDX2 in colorectal cancer. Oncol. Rep. 24, 97-104.
11. Zeng, M., Kikuchi, H., Pino, M. S., Chung, D. C. (2010) Hypoxia activates the K-ras proto-oncogene to stimulate angiogenesis and inhibit apoptosis in colon cancer cells. PLoS ONE 5, e10966.
12. Salama, P., Phillips, M., Grieu, F., Morris, M., Zeps, N., Joseph, D., Platell, C., Iacopetta, B. (2009) Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J. Clin. Oncol. 27, 186-192.
13. Lugli, A., Iezzi, G., Hostettler, I., Muraro, M. G., Mele, V., Tornillo, L., Carafa, V., Spagnoli, G., Terracciano, L., Zlobec, I. (2010) Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br. J. Cancer 103, 382-390.
14. Vivanco, I., Sawyers, C. L. (2002) The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2, 489-501.
15. Fang, J. Y., Richardson, B. C. (2005) The MAPK signaling pathways and colorectal cancer. Lancet Oncol. 6, 322-327.
16. Yang, L., Pang, Y., Moses, H. L. (2010) TGF-β and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol. 31, 220-227.
17. Le Gouvello, S., Bastuji-Garin, S., Aloulou, N., Mansour, H., Chaumette, M. T., Berrehar, F., Seikour, A., Charachon, A., Karoui, M., Leroy, K., Farcet, J. P., Sobhani, I. (2008) High prevalence of Foxp3 and IL17 in MMR-proficient colorectal carcinomas. Gut 57, 772-779.
18. Berencsi, K., Meropol, N. J., Hoffman, J. P., Sigurdson, E., Giles, L., Rani, P., Somasundaram, R., Zhang, T., Kalabis, J., Caputo, L., Furth, E., Swoboda, R., Marincola, F., Herlyn, D. (2007) Colon carcinoma cells induce CXCL11-dependent migration of CXCR3-expressing cytotoxic T lymphocytes in organotypic culture. Cancer Immunol. Immunother. 56, 359-370.
19. Ma, X., Norsworthy, K., Kundu, N., Rodgers, W. H., Gimotty, P. A., Goloubeva, O., Lipsky, M., Li, Y., Holt, D., Fulton, A. (2009) CXCR3 expression is associated with poor survival in breast cancer and promotes metastasis in a murine model. Mol. Cancer Ther. 8, 490-498.
20. Oo, Y. H., Weston, C. J., Lalor, P. F. (2010) Distinct roles for CCR4 and CXCR3 in the recruitment and positioning of regulatory T cells in the inflamed human liver. J. Immunol. 184, 2886-2898.
21. Ji, Y., Zhang, W. (2010) Th17 cells: positive or negative role in tumor? Cancer Immunol. Immunother. 59, 979-987.
22. Lin, Q., Yun, Z. (2010) Impact of the hypoxic tumor microenvironment on the regulation of cancer stem cell characteristics. Cancer Biol. Ther. 9, 949-956.
23. Afzali, B., Mitchell, P., Lechler, R. I., John, S., Lombardi, G. (2010) Translational mini-review series on Th17 cells: induction of interleukin-17 production by regulatory T cells. Clin. Exp. Immunol. 159, 120-130.
24. Yin, Y., Wen, S., Li, G., Wang, D. (2009) Hypoxia enhances stimulating effect of amyloid β peptide (25-35) for interleukin 17 and T helper lymphocyte subtype 17 upregulation in cultured peripheral blood mononuclear cells. Microbiol. Immunol. 53, 281-286.
25. Khaleghpour, K., Li, Y., Banville, D., Yu, Z., Shen, S. H. (2004) Involvement of the PI 3-kinase signaling pathway in progression of colon adenocarcinoma. Carcinogenesis 25, 241-248.
26. Ding, Q., Wang, Q., Evers, B. M. (2001) Alterations of MAPK activities associated with intestinal cell differentiation. Biochem. Biophys. Res. Commun. 284, 282-288.
27. Kehrl, J. H., Wakefield, L. M., Roberts, A. B., Jakowlew, S., Alvarez-Mon, M., Derynck, R., Sporn, M. B., Fauci, A. S. (1986) Production of transforming growth factor β by human T lymphocytes and its potential role in the regulation of T cell growth. J. Exp. Med. 163, 1037-1050.
28. Bierie, B., Moses, H. L. (2006) Tumor microenvironment: TGFβ: the molecular Jekyll and Hyde of cancer. Nat. Rev. Cancer 6, 506-520.
29. Wrzesinski, S. H., Wan, Y. Y., Flavell, R. A. (2007) Transforming growth factor-β and the immune response: implications for anticancer therapy. Clin. Cancer Res. 13, 5262-5270.
30. Kryczek, I., Wei, S., Zou, L., Altuwaijri, S., Szeliga, W., Kolls, J., Chang, A., Zou, W. (2007) Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J. Immunol. 178, 6730-6733. (Pubitemid 46847396)