Two FOXP3 + CD4 + T cell subpopulations distinctly control the prognosis of colorectal cancers

Nature Medicine

Volumn 22, Issue 6, 2016, Pages 679-684

  Saito, Takuro ^a   Nishikawa, Hiroyoshi ^a,f   Wada, Hisashi ^a   Nagano, Yuji ^b   Sugiyama, Daisuke ^a   Atarashi, Koji ^b   Maeda, Yuka ^a   Hamaguchi, Masahide ^a   Ohkura, Naganari ^a   Sato, Eiichi ^c   Nagase, Hirotsugu ^a   Nishimura, Junichi ^a   Yamamoto, Hirofumi ^a   Takiguchi, Shuji ^a   Tanoue, Takeshi ^b   Suda, Wataru ^d   Morita, Hidetoshi ^e   Hattori, Masahira ^d   Honda, Kenya ^b   Mori, Masaki ^a   Doki, Yuichiro ^a   Sakaguchi, Shimon ^a   more..

^a OSAKA UNIVERSITY   (Japan)

^b Institute of Physical and Chemical Research   (Japan)

^c TOKYO MEDICAL UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e AZABU UNIVERSITY   (Japan)

^f NATIONAL CANCER CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD45RA ANTIGEN; INTERLEUKIN 12; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; IL12A PROTEIN, HUMAN; INTERLEUKIN 12P35; TGFB1 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CANCER PROGNOSIS; CD4+ T LYMPHOCYTE; CELL INFILTRATION; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINE RELEASE; FUSOBACTERIUM NUCLEATUM; HUMAN; HUMAN TISSUE; INTESTINE FLORA; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR INVASION; ABDOMINAL SURGERY; ADULT; AGED; CANCER STAGING; COLORECTAL NEOPLASMS; FEMALE; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; SURVIVAL RATE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CD4-POSITIVE T-LYMPHOCYTES; COLORECTAL NEOPLASMS; DIGESTIVE SYSTEM SURGICAL PROCEDURES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-12 SUBUNIT P35; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; NEOPLASM STAGING; PROGNOSIS; SURVIVAL RATE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84964311408     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4086     Document Type: Article

References (34)

1. Sakaguchi, S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6, 345-352 (2005).
2. Zou, W. Regulatory T cells, tumor immunity and immunotherapy. Nat. Rev. Immunol. 6, 295-307 (2006).
3. Nishikawa, H. & Sakaguchi, S. Regulatory T cells in cancer immunotherapy. Curr. Opin. Immunol. 27, 1-7 (2014).
4. Curiel, T.J. et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10, 942-949 (2004).
5. Sato, E. et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci. USA 102, 18538-18543 (2005).
6. deLeeuw, R.J., Kost, S.E., Kakal, J.A. & Nelson, B.H. The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: A critical review of the literature. Clin. Cancer Res. 18, 3022-3029 (2012).
7. Sinicrope, F.A. et al. Intraepithelial effector (CD3+)/regulatory (FoxP3+) T cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 137, 1270-1279 (2009).
8. Salama, P. et al. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J. Clin. Oncol. 27, 186-192 (2009).
9. Frey, D.M. et al. High frequency of tumor-infiltrating FOXP3+ regulatory T cells predicts improved survival in mismatch-repair-proficient colorectal cancer patients. Int. J. Cancer 126, 2635-2643 (2010).
10. Miyara, M. et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 30, 899-911 (2009).
11. Josefowicz, S.Z., Lu, L.F. & Rudensky, A.Y. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564 (2012).
12. Sakaguchi, S., Miyara, M., Costantino, C.M. & Hafler, D.A. FOXP3+ regulatory T cells in the human immune system. Nat. Rev. Immunol. 10, 490-500 (2010).
13. Sugiyama, D. et al. Anti-CCR4 mAb selectively depletes effector-Type FoxP3+CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc. Natl. Acad. Sci. USA 110, 17945-17950 (2013).
14. Yamaguchi, T. et al. Construction of self-recognizing regulatory T cells from conventional T cells by controlling CTLA-4 and IL-2 expression. Proc. Natl. Acad. Sci. USA 110, E2116-E2125 (2013).
15. Joller, N. et al. Treg cells expressing the co-inhibitory molecule TIGIT selectively inhibit pro-inflammatory TH1 and TH17 cell responses. Immunity 40, 569-581 (2014).
16. Blatner, N.R. et al. Expression of ROR-γt marks a pathogenic regulatory T cell subset in human colon cancer. Sci. Transl. Med. 4, 164ra159 (2012).
17. Ohkura, N. et al. T cell-receptor-stimulation-induced epigenetic changes and Foxp3 expression are independent and complementary events required for Treg cell development. Immunity 37, 785-799 (2012).
18. Dejea, C.M. et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc. Natl. Acad. Sci. USA 111, 18321-18326 (2014).
19. Tosolini, M. et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (TH1, TH2, Treg, TH17) in patients with colorectal cancer. Cancer Res. 71, 1263-1271 (2011).
20. Galon, J. et al. Type, density and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960-1964 (2006).
21. Pagès, F. et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J. Clin. Oncol. 27, 5944-5951 (2009).
22. Schreiber, R.D., Old, L.J. & Smyth, M.J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331, 1565-1570 (2011).
23. Rubinstein, M.R. et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin-β-catenin signaling via its FadA adhesin. Cell Host Microbe 14, 195-206 (2013).
24. Kostic, A.D. et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14, 207-215 (2013).
25. Atarashi, K. et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500, 232-236 (2013).
26. Grivennikov, S.I. et al. Adenoma-linked barrier defects and microbial products drive IL-23-And IL-17-mediated tumor growth. Nature 491, 254-258 (2012).
27. Wu, P. et al. γδ T17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity 40, 785-800 (2014).
28. Gur, C. et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42, 344-355 (2015).
29. Mima, K. et al. Fusobacterium nucleatum and T cells in colorectal carcinoma. JAMA Oncol. 1, 653-661 (2015).
30. Mima, K. et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut http://dx.doi.org/10.1136/gutjnl-2015-310101 (2015).
31. Rech, A.J. et al. CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients. Sci. Transl. Med. 4, 134ra62 (2012).
32. Vom Berg, J. et al. Intratumoral IL-12 combined with CTLA-4 blockade elicits T cell-mediated glioma rejection. J. Exp. Med. 210, 2803-2811 (2013).
33. Kim, S.W. et al. Robustness of gut microbiota of healthy adults in response to probiotic intervention revealed by high-Throughput pyrosequencing. DNA Res. 20, 241-253 (2013).
34. Said, H.S. et al. Dysbiosis of salivary microbiota in inflammatory bowel disease and its association with oral immunological biomarkers. DNA Res. 21, 15-25 (2014).