De Novo Epigenetic Programs Inhibit PD-1 Blockade-Mediated T Cell Rejuvenation

Cell

Volumn 170, Issue 1, 2017, Pages 142-157.e19

  Ghoneim, Hazem E ^a   Fan, Yiping ^a   Moustaki, Ardiana ^a   Abdelsamed, Hossam A ^a   Dash, Pradyot ^a   Dogra, Pranay ^a   Carter, Robert ^a   Awad, Walid ^a   Neale, Geoff ^a   Thomas, Paul G ^a   Youngblood, Ben ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

CD8 T cells; DNA methylation; DNA demethylating agents; epigenetic modifications; exhaustion; immune checkpoint blockade; tumor

Indexed keywords

BISULFITE; CHEMOKINE RECEPTOR CCR7; DECITABINE; DNA METHYLTRANSFERASE 3A; EOMESODERMIN; GAMMA INTERFERON; INTERLEUKIN 2; KI 67 ANTIGEN; MYC PROTEIN; PROGRAMMED DEATH 1 RECEPTOR; TRANSCRIPTION FACTOR T BET; PDCD1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; IMMUNE RESPONSE; INFECTION; LIVER; LUNG; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REJUVENATION; SPLEEN; T LYMPHOCYTE ACTIVATION; VIRUS INFECTION; WHOLE GENOME SEQUENCING; ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CANCER TRANSPLANTATION; CYTOLOGY; FEMALE; GENETIC EPIGENESIS; IMMUNOLOGY; PROSTATIC NEOPLASMS; VIRUS DISEASES;

ADENOCARCINOMA; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; MALE; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; PROGRAMMED CELL DEATH 1 RECEPTOR; PROSTATIC NEOPLASMS; VIRUS DISEASES;

EID: 85021074576     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.06.007     Document Type: Article

References (39)

1. Angelosanto, J.M., Blackburn, S.D., Crawford, A., Wherry, E.J., Progressive loss of memory T cell potential and commitment to exhaustion during chronic viral infection. J. Virol. 86 (2012), 8161–8170.
2. Bintu, L., Yong, J., Antebi, Y.E., McCue, K., Kazuki, Y., Uno, N., Oshimura, M., Elowitz, M.B., Dynamics of epigenetic regulation at the single-cell level. Science 351 (2016), 720–724.
3. Bird, A., DNA methylation patterns and epigenetic memory. Genes Dev. 16 (2002), 6–21.
4. Cedar, H., Bergman, Y., Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10 (2009), 295–304.
5. Chiappinelli, K.B., Strissel, P.L., Desrichard, A., Li, H., Henke, C., Akman, B., Hein, A., Rote, N.S., Cope, L.M., Snyder, A., et al. Inhibiting DNA methylation causes an interferon response in cancer via dsRNA including endogenous retroviruses. Cell, 164, 2016, 1073.
6. Crompton, J.G., Narayanan, M., Cuddapah, S., Roychoudhuri, R., Ji, Y., Yang, W., Patel, S.J., Sukumar, M., Palmer, D.C., Peng, W., et al. Lineage relationship of CD8 T cell subsets is revealed by progressive changes in the epigenetic landscape. Cell Mol Immunol 13 (2016), 502–513.
7. Curran, M.A., Allison, J.P., Tumor vaccines expressing flt3 ligand synergize with ctla-4 blockade to reject preimplanted tumors. Cancer Res. 69 (2009), 7747–7755.
8. Dash, P., McClaren, J.L., Oguin, T.H. 3rd, Rothwell, W., Todd, B., Morris, M.Y., Becksfort, J., Reynolds, C., Brown, S.A., Doherty, P.C., Thomas, P.G., Paired analysis of TCRα and TCRβ chains at the single-cell level in mice. J. Clin. Invest. 121 (2011), 288–295.
9. Dash, P., Wang, G.C., Thomas, P.G., Single-cell analysis of T-cell receptor αβ repertoire. Methods Mol. Biol. 1343 (2015), 181–197.
10. Foster, B.A., Gingrich, J.R., Kwon, E.D., Madias, C., Greenberg, N.M., Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res. 57 (1997), 3325–3330.
11. Ghoneim, H.E., Zamora, A.E., Thomas, P.G., Youngblood, B.A., Cell-intrinsic barriers of T cell-based immunotherapy. Trends Mol. Med. 22 (2016), 1000–1011.
12. Ha, S.J., Mueller, S.N., Wherry, E.J., Barber, D.L., Aubert, R.D., Sharpe, A.H., Freeman, G.J., Ahmed, R., Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J. Exp. Med. 205 (2008), 543–555.
13. Im, S.J., Hashimoto, M., Gerner, M.Y., Lee, J., Kissick, H.T., Burger, M.C., Shan, Q., Hale, J.S., Lee, J., Nasti, T.H., et al. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature 537 (2016), 417–421.
14. Jin, H.T., Anderson, A.C., Tan, W.G., West, E.E., Ha, S.J., Araki, K., Freeman, G.J., Kuchroo, V.K., Ahmed, R., Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 107 (2010), 14733–14738.
15. Kaech, S.M., Cui, W., Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Rev. Immunol. 12 (2012), 749–761.
16. Lefranc, M.P., Giudicelli, V., Ginestoux, C., Jabado-Michaloud, J., Folch, G., Bellahcene, F., Wu, Y., Gemrot, E., Brochet, X., Lane, J., et al. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 37 (2009), D1006–D1012.
17. Li, H., Chiappinelli, K.B., Guzzetta, A.A., Easwaran, H., Yen, R.W., Vatapalli, R., Topper, M.J., Luo, J., Connolly, R.M., Azad, N.S., et al. Immune regulation by low doses of the DNA methyltransferase inhibitor 5-azacitidine in common human epithelial cancers. Oncotarget 5 (2014), 587–598.
18. Matloubian, M., Somasundaram, T., Kolhekar, S.R., Selvakumar, R., Ahmed, R., Genetic basis of viral persistence: single amino acid change in the viral glycoprotein affects ability of lymphocytic choriomeningitis virus to persist in adult mice. J. Exp. Med. 172 (1990), 1043–1048.
19. Pastor, W.A., Aravind, L., Rao, A., TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol. 14 (2013), 341–356.
20. Pauken, K.E., Sammons, M.A., Odorizzi, P.M., Manne, S., Godec, J., Khan, O., Drake, A.M., Chen, Z., Sen, D.R., Kurachi, M., et al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354 (2016), 1160–1165.
21. Ribas, A., Hamid, O., Daud, A., Hodi, F.S., Wolchok, J.D., Kefford, R., Joshua, A.M., Patnaik, A., Hwu, W.J., Weber, J.S., et al. Association of pembrolizumab with tumor response and survival among patients with advanced melanoma. JAMA 315 (2016), 1600–1609.
22. Roulois, D., Loo Yau, H., Singhania, R., Wang, Y., Danesh, A., Shen, S.Y., Han, H., Liang, G., Jones, P.A., Pugh, T.J., et al. DNA-demethylating agents target colorectal cancer cells by inducing viral mimicry by endogenous transcripts. Cell 162 (2015), 961–973.
23. Russ, B.E., Olshanksy, M., Smallwood, H.S., Li, J., Denton, A.E., Prier, J.E., Stock, A.T., Croom, H.A., Cullen, J.G., Nguyen, M.L., et al. Distinct epigenetic signatures delineate transcriptional programs during virus-specific CD8(+) T cell differentiation. Immunity 41 (2014), 853–865.
24. Scharer, C.D., Barwick, B.G., Youngblood, B.A., Ahmed, R., Boss, J.M., Global DNA methylation remodeling accompanies CD8 T cell effector function. J Immunol. 191 (2013), 3419–3429.
25. Sharma, P., Allison, J.P., The future of immune checkpoint therapy. Science 348 (2015), 56–61.
26. Sharma, P., Allison, J.P., Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell 161 (2015), 205–214.
27. Speiser, D.E., Utzschneider, D.T., Oberle, S.G., Münz, C., Romero, P., Zehn, D., T cell differentiation in chronic infection and cancer: functional adaptation or exhaustion?. Nat. Rev. Immunol. 14 (2014), 768–774.
28. Thomas, P.G., Handel, A., Doherty, P.C., La Gruta, N.L., Ecological analysis of antigen-specific CTL repertoires defines the relationship between naive and immune T-cell populations. Proc. Natl. Acad. Sci. USA 110 (2013), 1839–1844.
29. Trinh, B.N., Long, T.I., Laird, P.W., DNA methylation analysis by MethyLight technology. Methods 25 (2001), 456–462.
30. Utzschneider, D.T., Charmoy, M., Chennupati, V., Pousse, L., Ferreira, D.P., Calderon-Copete, S., Danilo, M., Alfei, F., Hofmann, M., Wieland, D., et al. T cell factor 1-expressing memory-like CD8(+) T cells sustain the immune response to chronic viral infections. Immunity 45 (2016), 415–427.
31. Utzschneider, D.T., Legat, A., Fuertes Marraco, S.A., Carrié, L., Luescher, I., Speiser, D.E., Zehn, D., T cells maintain an exhausted phenotype after antigen withdrawal and population reexpansion. Nat. Immunol. 14 (2013), 603–610.
32. Vaquerizas, J.M., Kummerfeld, S.K., Teichmann, S.A., Luscombe, N.M., A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 10 (2009), 252–263.
33. Wang, L., Amoozgar, Z., Huang, J., Saleh, M.H., Xing, D., Orsulic, S., Goldberg, M.S., Decitabine enhances lymphocyte migration and function and synergizes with CTLA-4 blockade in a murine ovarian cancer model. Cancer Immunol. Res. 3 (2015), 1030–1041.
34. Wang, R., Dillon, C.P., Shi, L.Z., Milasta, S., Carter, R., Finkelstein, D., McCormick, L.L., Fitzgerald, P., Chi, H., Munger, J., Green, D.R., The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 35 (2011), 871–882.
35. Wherry, E.J., T cell exhaustion. Nat. Immunol. 12 (2011), 492–499.
36. Wherry, E.J., Blattman, J.N., Murali-Krishna, K., van der Most, R., Ahmed, R., Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77 (2003), 4911–4927.
37. Wu, H., Xu, T., Feng, H., Chen, L., Li, B., Yao, B., Qin, Z., Jin, P., Conneely, K.N., Detection of differentially methylated regions from whole-genome bisulfite sequencing data without replicates. Nucleic Acids Res., 43, 2015, e141.
38. Youngblood, B., Oestreich, K.J., Ha, S.J., Duraiswamy, J., Akondy, R.S., West, E.E., Wei, Z., Lu, P., Austin, J.W., Riley, J.L., et al. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity 35 (2011), 400–412.
39. Yu, P., Steel, J.C., Zhang, M., Morris, J.C., Waitz, R., Fasso, M., Allison, J.P., Waldmann, T.A., Simultaneous inhibition of two regulatory T-cell subsets enhanced Interleukin-15 efficacy in a prostate tumor model. Proc. Natl. Acad. Sci. USA 109 (2012), 6187–6192.