Epigenetic manipulation restores functions of defective CD8+ T Cells from chronic viral infection

Molecular Therapy

Volumn 22, Issue 9, 2014, Pages 1698-1706

  Zhang, Fuqin ^a,b   Zhou, Xiaohui ^b,c   Dispirito, Joanna R ^b   Wang, Chuan ^b,d   Wang, Ying ^a   Shen, Hao ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c FUDAN UNIVERSITY   (China)

^d SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; HISTONE H3; ENZYME INHIBITOR; HISTONE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; EPIGENETICS; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTIC CHORIOMENINGITIS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; T LYMPHOCYTE EXHAUSTION; T LYMPHOCYTE SUBPOPULATION; VIRUS PATHOGENESIS; ANIMAL; ARENAVIRUS INFECTION; C57BL MOUSE; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC EPIGENESIS; IMMUNOLOGY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; METABOLISM; PHYSIOLOGY; VETERINARY; VIROLOGY;

ADOPTIVE TRANSFER; ANIMALS; ARENAVIRIDAE INFECTIONS; CD8-POSITIVE T-LYMPHOCYTES; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENZYME INHIBITORS; EPIGENESIS, GENETIC; FEMALE; HISTONES; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL;

EID: 84964312648     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.91     Document Type: Article

References (42)

1. Kaech, SM, Wherry, EJ and Ahmed, R (2002). Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2: 251-262.
2. Wherry, EJ and Ahmed, R (2004). Memory CD8 T-cell differentiation during viral infection. J Virol 78: 5535-5545.
3. Kaech, SM and Wherry, EJ (2007). Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 27: 393-405.
4. Williams, MA and Bevan, MJ (2007). Effector and memory CTL differentiation. Annu Rev Immunol 25: 171-192.
5. Barber, DL, Wherry, EJ, Masopust, D, Zhu, B, Allison, JP, Sharpe, AH et al. (2006). Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
6. Shin, H, Blackburn, SD, Intlekofer, AM, Kao, C, Angelosanto, JM, Reiner, SL et al. (2009). A role for the transcriptional repressor Blimp-1 in CD8(+) T cell exhaustion during chronic viral infection. Immunity 31: 309-320.
7. Shin, H and Wherry, EJ (2007). CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol 19: 408-415.
8. Kim, PS and Ahmed, R (2010). Features of responding T cells in cancer and chronic infection. Curr Opin Immunol 22: 223-230.
9. Wanczyk, M, Roszczenko, K, Marcinkiewicz, K, Bojarczuk, K, Kowara, M and Winiarska, M (2011). HDACi-going through the mechanisms. Front Biosci (Landmark Ed) 16: 340-359.
10. Sanders, VM (2006). Epigenetic regulation of Th1 and Th2 cell development. Brain Behav Immun 20: 317-324.
11. Ansel, KM, Lee, DU and Rao, A (2003). An epigenetic view of helper T cell differentiation. Nat Immunol 4: 616-623.
12. Fields, PE, Kim, ST and Flavell, RA (2002). Cutting edge: changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation. J Immunol 169: 647-650.
13. Northrop, JK, Thomas, RM, Wells, AD and Shen, H (2006). Epigenetic remodeling of the IL-2 and IFN-gamma loci in memory CD8 T cells is influenced by CD4 T cells. J Immunol 177: 1062-1069.
14. Kersh, EN, Fitzpatrick, DR, Murali-Krishna, K, Shires, J, Speck, SH, Boss, JM et al. (2006). Rapid demethylation of the IFN-gamma gene occurs in memory but not naive CD8 T cells. J Immunol 176: 4083-4093.
15. Blackburn, SD, Crawford, A, Shin, H, Polley, A, Freeman, GJ and Wherry, EJ (2010). Tissue-specific differences in PD-1 and PD-L1 expression during chronic viral infection: implications for CD8 T-cell exhaustion. J Virol 84: 2078-2089.
16. Virgin, HW, Wherry, EJ and Ahmed, R (2009). Redefining chronic viral infection. Cell 138: 30-50.
17. Koike, T (2012). Interferon-γ-independent suppression of Th17 cell differentiation by T-bet expression in mice with autoimmune arthritis. Arthritis Rheum 64: 40-41.
18. Quigley, M, Pereyra, F, Nilsson, B, Porichis, F, Fonseca, C, Eichbaum, Q et al. (2010). Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat Med 16: 1147-1151.
19. Crawford, A, Angelosanto, JM, Nadwodny, KL, Blackburn, SD and Wherry, EJ (2011). A role for the chemokine RANTES in regulating CD8 T cell responses during chronic viral infection. Plos Pathog 7: e1002098.
20. Wilson, EB and Brooks, DG (2013). Decoding the complexity of type I interferon to treat persistent viral infections. Trends Microbiol 21: 634-640.
21. Wilson, EB, Yamada, DH, Elsaesser, H, Herskovitz, J, Deng, J, Cheng, G et al. (2013). Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340: 202-207.
22. Wilson, EB and Brooks, DG (2013). Interfering with type I interferon: A novel approach to purge persistent viral infection. Cell Cycle 12: 2919-2920.
23. Yi, JS, Cox, MA and Zajac, AJ (2010). T-cell exhaustion: characteristics, causes and conversion. Immunology 129: 474-481.
24. Cox, MA, Harrington, LE and Zajac, AJ (2011). Cytokines and the inception of CD8 T cell responses. Trends Immunol 32: 180-186.
25. Youngblood, B, Wherry, EJ and Ahmed, R (2012). Acquired transcriptional programming in functional and exhausted virus-specific CD8 T cells. Curr Opin HIV AIDS 7: 50-57.
26. Wherry, E. J. (2010). T cell exhaustion. Nat Immunol 131, 492-499.
27. Butler, NS, Moebius, J, Pewe, LL, Traore, B, Doumbo, OK, Tygrett, LT et al. (2012). Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nat Immunol 13: 188-195.
28. Elsaesser, H, Sauer, K and Brooks, DG (2009). IL-21 is required to control chronic viral infection. Science 324: 1569-1572.
29. Brooks, DG, Ha, SJ, Elsaesser, H, Sharpe, AH, Freeman, GJ and Oldstone, MB (2008). IL-10 and PD-L1 operate through distinct pathways to suppress T-cell activity during persistent viral infection. Proc Natl Acad Sci USA 105: 20428-20433.
30. Brooks, DG, Lee, AM, Elsaesser, H, McGavern, DB and Oldstone, MB (2008). IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J Exp Med 205: 533-541.
31. Brooks, DG, Trifilo, MJ, Edelmann, KH, Teyton, L, McGavern, DB and Oldstone, MB (2006). Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 12: 1301-1309.
32. West, EE, Jin, HT, Rasheed, AU, Penaloza-Macmaster, P, Ha, SJ, Tan, WG et al. (2013). PD-L1 blockade synergizes with IL-2 therapy in reinvigorating exhausted T cells. J Clin Invest 123: 2604-2615.
33. Scharer, CD, Barwick, BG, Youngblood, BA, Ahmed, R and Boss, JM (2013). Global DNA methylation remodeling accompanies CD8 T cell effector function. J Immunol 191: 3419-3429.
34. Angelosanto, JM, Blackburn, SD, Crawford, A and Wherry, EJ (2012). Progressive loss of memory T cell potential and commitment to exhaustion during chronic viral infection. J Virol 86: 8161-8170.
35. Youngblood, B, Oestreich, KJ, Ha, SJ, Duraiswamy, J, Akondy, RS, West, EE et al. (2011). Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity 35: 400-412.
36. Wherry, EJ, Blattman, JN and Ahmed, R (2005). Low CD8 T-cell proliferative potential and high viral load limit the effectiveness of therapeutic vaccination. J Virol 79: 8960-8968.
37. Wherry, EJ, Barber, DL, Kaech, SM, Blattman, JN and Ahmed, R (2004). Antigenindependent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci USA 101: 16004-16009.
38. Wherry, EJ (2011). T cell exhaustion. Nat Immunol 12: 492-499.
39. Doering, TA, Crawford, A, Angelosanto, JM, Paley, MA, Ziegler, CG and Wherry, EJ (2012). Network analysis reveals centrally connected genes and pathways involved in CD8+ T cell exhaustion versus memory. Immunity 37: 1130-1144.
40. Murali-Krishna, K, Altman, JD, Suresh, M, Sourdive, DJ, Zajac, AJ, Miller, JD et al. (1998). Counting antigen-specific CD8 T cells: A reevaluation of bystander activation during viral infection. Immunity 8: 177-187.
41. Hudrisier, D, Oldstone, MB and Gairin, JE (1997). The signal sequence of lymphocytic choriomeningitis virus contains an immunodominant cytotoxic T cell epitope that is restricted by both H-2D(b) and H-2K(b) molecules. Virology 234: 62-73.
42. Dispirito, JR and Shen, H (2010). Histone acetylation at the single-cell level: A marker of memory CD8+ T cell differentiation and functionality. J Immunol 184: 4631-4636.