Apoptosis of tumor infiltrating effector TIM-3+CD8+ T cells in colon cancer

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kang, Chiao Wen ^a   Dutta, Avijit ^b   Chang, Li Yuan ^a   Mahalingam, Jayashri ^a   Lin, Yung Chang ^b   Chiang, Jy Ming ^b   Hsu, Chen Yu ^a   Huang, Ching Tai ^b   Su, Wan Ting ^a   Chu, Yu Yi ^a   Lin, Chun Yen ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GALECTIN; HAVCR2 PROTEIN, HUMAN; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; LGALS9 PROTEIN, HUMAN; MEMBRANE PROTEIN;

ANTAGONISTS AND INHIBITORS; APOPTOSIS; CD8+ T LYMPHOCYTE; COLON TUMOR; HUMAN; IMMUNOLOGY; PATHOLOGY; PHYSIOLOGY;

APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; COLONIC NEOPLASMS; GALECTINS; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; HUMANS; MEMBRANE PROTEINS;

EID: 84944931173     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep15659     Document Type: Article

References (50)

1. Pages, F. et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353, 2654-2666 (2005).
2. Zhang, L. et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 348, 203-213 (2003).
3. Yamada, N. et al. CD8+ tumor-infiltrating lymphocytes predict favorable prognosis in malignant pleural mesothelioma after resection. Cancer Immunol. Immunother. 59, 1543-1549 (2010).
4. Blank, C., Gajewski, T. F. & Mackensen, A. Interaction of PD-L1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: implications for tumor immunotherapy. Cancer Immunol. Immunother. 54, 307-314 (2005).
5. Dong, H. et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8, 793-800 (2002).
6. Sakuishi, K. et al. TIM3+ FOXP3+ regulatory T cells are tissue-specific promoters of T-cell dysfunction in cancer. Oncoimmunology 2, e23849 (2013).
7. Golden-Mason, L. et al. Negative immune regulator Tim-3 is overexpressed on T cells in hepatitis C virus infection and its blockade rescues dysfunctional CD4+ and CD8+ T cells. J. Virol. 83, 9122-9130 (2009).
8. Jones, R. B. et al. Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J. Exp. Med. 205, 2763-2779 (2008).
9. Sakuishi, K. et al. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J. Exp. Med. 207, 2187-2194 (2010).
10. Fourcade, J. et al. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J. Exp. Med. 207, 2175-2186 (2010).
11. Jin, H. T. et al. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 107, 14733-14738 (2010).
12. Zhou, Q. et al. Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia. Blood 117, 4501-4510 (2011).
13. Monney, L. et al. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 415, 536-541 (2002).
14. Qiu, Y. et al. Tim-3-expressing CD4+ and CD8+ T cells in human tuberculosis (TB) exhibit polarized effector memory phenotypes and stronger anti-TB effector functions. PLoS Pathog. 8, e1002984 (2012).
15. Ngiow. S. F. et al. Anti-TIM3 antibody promotes T cell IFN-γ -mediated antitumor immunity and suppresses established tumors. Cancer Res. 71, 3540-3551 (2011).
16. Zhu, C. et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6, 1245-1252 (2005).
17. Kashio, Y. et al. Galectin-9 induces apoptosis through the calcium-calpain-caspase-1 pathway. J. Immunol. 170, 3631-3636 (2003).
18. Sharma, S. et al. T cell immunoglobulin and mucin protein-3 (Tim-3)/Galectin-9 interaction regulates influenza A virus-specific humoral and CD8 T-cell responses. Proc. Natl. Acad. Sci. USA 108, 19001-19006 (2011).
19. World Health Organization. World Cancer Report 2014. Chapter 1.1. ISBN 9283204298 (2014).
20. Yan, J. et al. Tim-3 expression defines regulatory T cells in human tumors. PLoS One 8, e58006 (2013).
21. Arai, Y., Saito, H. & Ikeguchi, M. Upregulation of TIM-3 and PD-1 on CD4+ and CD8+ T Cells Associated with Dysfunction of Cell-Mediated Immunity after Colorectal Cancer Operation. Yonago Acta Med. 55, 1-9 (2012).
22. Galon, J. et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960-1964 (2006).
23. 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).
24. Salama, P. et al. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J. Clin. Oncol. 27, 186-192 (2009).
25. Lin, Y. C. et al. Effector/memory but not naive regulatory T cells are responsible for the loss of concomitant tumor immunity. J. Immunol. 182, 6095-6104 (2009).
26. Chang, L. Y. et al. The indispensable role of CCR5 for in vivo suppressor function of tumor-derived CD103+ effector/memory regulatory T cells. J. Immunol. 189, 567-574 (2012).
27. Chang, L. Y. et al. Tumor-derived chemokine CCL5 enhances TGF-β -mediated killing of CD8(+) T cells in colon cancer by T-regulatory cells. Cancer Res. 72, 1092-1102 (2012).
28. Paley, M. A. et al. Progenitor and Terminal Subsets of CD8+ T Cells Cooperate to Contain Chronic Viral Infection. Science 338, 1220-1225 (2012).
29. Radojcic, V. et al. Cyclophosphamide resets dendritic cell homeostasis and enhances antitumor immunity through effects that extend beyond regulatory T cell elimination. Cancer Immunol. Immunother. 59, 137-148 (2010).
30. Alyamkina, E. A. et al. Combined therapy with cyclophosphamide and DNA preparation inhibits the tumor growth in mice. Genet. Vaccines Ther. 7, 12 (2009).
31. Takamura, S. et al. Premature Terminal Exhaustion of Friend Virus-Specific Effector CD8+ T Cells by Rapid Induction of Multiple Inhibitory Receptors. J. Immunol. 184, 4696-4707 (2010).
32. Barber, D. L. et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687 (2006).
33. Anderson, A. C. Tim-3, a negative regulator of anti-tumor immunity. Curr. Opin. Immunol. 24, 213-216 (2012).
34. Pages, F., Galon, J. & Fridman, W. H. The essential role of the in situ immune reaction in human colorectal cancer. J. Leukoc. Biol. 84, 981-987 (2008).
35. Wherry, E. J. T cell exhaustion. Nat. Immunol. 12, 492-499 (2011).
36. Elmansy, H. et al. Prognostic impact of apoptosis marker Fas (CD95) and its ligand (FasL) on bladder cancer in Egypt: study of the effect of schistosomiasis. Ecancermedicalscience 6, 278 (2012).
37. Albers, A. E. et al. Spontaneous apoptosis of tumor-specific tetramer+ CD8+ T lymphocytes in the peripheral circulation of patients with head and neck cancer. Head Neck 31, 773-781 (2009).
38. Sehrawat, S. et al. Galectin-9/TIM-3 interaction regulates virus-specific primary and memory CD8 T cell response. PLoS Pathog. 6, e1000882 (2010).
39. Leitner, J. et al. TIM-3 does not act as a receptor for galectin-9. PLoS Pathog. 9, e1003253 (2013).
40. van Esch, E. M. et al. Expression of coinhibitory receptors on T cells in the microenvironment of usual vulvar intraepithelial neoplasia is related to proinflammatory effector T cells and an increased recurrence-free survival. Int. J. Cancer. 136, E95-106 (2015).
41. Meggyes, M. et al. Peripheral blood TIM-3 positive NK and CD8+ T cells throughout pregnancy: TIM-3/galectin-9 interaction and its possible role during pregnancy. PLoS One. 9, e92371 (2014).
42. Mengshol, J. A. et al. A crucial role for Kupffer cell-derived galectin-9 in regulation of T cell immunity in hepatitis C infection. PLoS One 5, e9504 (2010).
43. Reddy, P. B. et al. Influence of galectin-9/Tim-3 interaction on herpes simplex virus-1 latency. J. Immunol. 187, 5745-5755 (2011).
44. Ghiringhelli, F. et al. CD4+ CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur. J. Immunol. 34, 336-344 (2004).
45. Viaud, S. et al. Cyclophosphamide induces differentiation of Th17 cells in cancer patients. Cancer Res. 71, 661-665 (2011).
46. Awwad, M. & North, R. J. Cyclophosphamide (Cy)-facilitated adoptive immunotherapy of a Cy-resistant tumour. Evidence that Cy permits the expression of adoptive T-cell mediated immunity by removing suppressor T cells rather than by reducing tumour burden. Immunology 65, 87-92 (1988).
47. Ercolini, A. M. et al. Recruitment of latent pools of high-avidity CD8(+) T cells to the antitumor immune response. J. Exp. Med. 201, 1591-1602 (2005).
48. Mkrtichyan, M. et al. Anti-PD-1 synergizes with cyclophosphamide to induce potent anti-tumor vaccine effects through novel mechanisms. Eur. J. Immunol. 41, 2977-2986 (2011).
49. Hirschhorn-Cymerman, D. et al. OX40 engagement and chemotherapy combination provides potent antitumor immunity with concomitant regulatory T cell apoptosis. J. Exp. Med. 206, 1103-1116 (2009).
50. Wang, F. et al. Tim-3-Galectin-9 pathway involves the suppression induced by CD4+ CD25+ regulatory T cells. Immunobiology 214, 342-349 (2009).