Memory CD8 T cell transcriptional plasticity

F1000Prime Reports

Volumn 7, Issue , 2015, Pages

  Youngblood, Ben ^a,b   Hale, J Scott ^a   Ahmed, Rafi ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; GRANZYME; HISTONE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; DNA METHYLATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIMARY IMMUNE RESPONSE; VIRUS INFECTION;

EID: 84928019813     PISSN: 20517599     EISSN: 20517599     Source Type: Journal    
DOI: 10.12703/P7-38     Document Type: Article

References (58)

1. Lau LL, Jamieson BD, Somasundaram T, Ahmed R: Cytotoxic T-cell memory without antigen. Nature 1994, 369:648-52.
2. Murali-Krishna K, Lau LL, Sambhara S, Lemonnier F, Altman J, Ahmed R: Persistence of memory CD8 T cells in MHC class I-deficient mice. Science (New York, NY) 1999, 286:1377-81.
3. Polic B, Kunkel D, Scheffold A, Rajewsky K: How alpha beta T cells deal with induced TCR alpha ablation. Proceedings of the National Academy of Sciences of the United States of America 2001, 98: 8744-9.
4. Mudd PA, Martins MA, Ericsen AJ, Tully DC, Power KA, Bean AT, Piaskowski SM, Duan L, Seese A, Gladden AD, Weisgrau KL, Furlott JR, Kim Y, Veloso de Santana, Marlon G, Rakasz E, Capuano S, Wilson NA, Bonaldo MC, Galler R, Allison DB, Piatak M, Haase AT, Lifson JD, Allen TM, Watkins DI: Vaccineinduced CD8+ T cells control AIDS virus replication. Nature 2012, 491: 129-33.
5. Ha S, Mueller SN, Wherry EJ, Barber DL, Aubert RD, Sharpe AH, Freeman GJ, Ahmed R: Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. The Journal of experimental medicine 2008, 205: 543-55.
6. Zhang Z, Jin B, Zhang J, Xu B, Wang H, Shi M, Wherry EJ, Lau, George KK, Wang F: Dynamic decrease in PD-1 expression correlates with HBV-specific memory CD8 T-cell development in acute self-limited hepatitis B patients. Journal of hepatology 2009, 50:1163-73.
7. Sallusto F, Lanzavecchia A, Araki K, Ahmed R: From vaccines to memory and back. Immunity 2010, 33:451-63.
8. Goldrath AW, Sivakumar PV, Glaccum M, Kennedy MK, Bevan MJ, Benoist C, Mathis D, Butz EA: Cytokine requirements for acute and Basal homeostatic proliferation of naive and memory CD8+ T cells. The Journal of experimental medicine 2002, 195:1515-22.
9. Zhang X, Sun S, Hwang I, Tough DF, Sprent J: Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 1998, 8:591-9.
10. Jameson SC: Maintaining the norm: T-cell homeostasis. Nature reviews. Immunology 2002, 2:547-56.
11. Lefrançois L, Masopust D: T cell immunity in lymphoid and nonlymphoid tissues. Current opinion in immunology 2002, 14:503-8.
12. Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A: Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999, 401:708-12.
13. Masopust D, Vezys V, Marzo AL, Lefrançois L: Preferential localization of effector memory cells in nonlymphoid tissue. Science (New York, NY) 2001, 291:2413-7.
14. Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, Almeida JR, Gostick E, Yu Z, Carpenito C, Wang E, Douek DC, Price DA, June CH, Marincola FM, Roederer M, Restifo NP: A human memory T cell subset with stem cell-like properties. Nature medicine 2011, 17:1290-7.
15. Klonowski KD, Williams KJ, Marzo AL, Blair DA, Lingenheld EG, Lefrançois L: Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 2004, 20:551-62.
16. Gebhardt T, Whitney PG, Zaid A, Mackay LK, Brooks AG, Heath WR, Carbone FR, Mueller SN: Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 2011, 477:216-9.
17. Casey KA, Fraser KA, Schenkel JM, Moran A, Abt MC, Beura LK, Lucas PJ, Artis D, Wherry EJ, Hogquist K, Vezys V, Masopust D: Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. Journal of immunology (Baltimore, Md.: 1950) 2012, 188:4866-75.
18. Masopust D, Vezys V, Wherry EJ, Barber DL, Ahmed R: Cutting edge: gut microenvironment promotes differentiation of a unique memory CD8 T cell population. Journal of immunology (Baltimore, Md.: 1950) 2006, 176:2079-83.
19. Mueller SN, Gebhardt T, Carbone FR, Heath WR: Memory T cell subsets, migration patterns, and tissue residence. Annual review of immunology 2013, 31:137-61.
20. Kaech SM, Hemby S, Kersh E, Ahmed R: Molecular and functional profiling of memory CD8 T cell differentiation. Cell 2002, 111:837-51.
21. Wherry EJ, Ha S, Kaech SM, Haining WN, Sarkar S, Kalia V, Subramaniam S, Blattman JN, Barber DL, Ahmed R: Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007, 27:670-84.
22. Willinger T, Freeman T, Hasegawa H, McMichael AJ, Callan, Margaret FC: Molecular signatures distinguish human central memory from effector memory CD8 T cell subsets. Journal of immunology (Baltimore, Md.: 1950) 2005, 175:5895-903.
23. Wherry EJ, Teichgräber V, Becker TC, Masopust D, Kaech SM, Antia R, von Andrian, Ulrich H, Ahmed R: Lineage relationship and protective immunity of memory CD8 T cell subsets. Nature immunology 2003, 4:225-34.
24. Marzo AL, Klonowski KD, Le Bon A, Borrow P, Tough DF, Lefrançois L: Initial T cell frequency dictates memory CD8+ T cell lineage commitment. Nature immunology 2005, 6:793-9.
25. Jacob J, Baltimore D: Modelling T-cell memory by genetic marking of memory T cells in vivo. Nature 1999, 399:593-7.
26. Rutishauser RL, Martins GA, Kalachikov S, Chandele A, Parish IA, Meffre E, Jacob J, Calame K, Kaech SM: Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 2009, 31:296-308.
27. Kallies A, Xin A, Belz GT, Nutt SL: Blimp-1 transcription factor is required for the differentiation of effector CD8(+) T cells and memory responses. Immunity 2009, 31:283-95.
28. Masopust D, Ha S, Vezys V, Ahmed R: Stimulation history dictates memory CD8 T cell phenotype: implications for prime-boost vaccination. Journal of immunology (Baltimore, Md.: 1950) 2006, 177:831-9.
29. Wirth TC, Xue H, Rai D, Sabel JT, Bair T, Harty JT, Badovinac VP: Repetitive antigen stimulation induces stepwise transcriptome diversification but preserves a core signature of memory CD8(+) T cell differentiation. Immunity 2010, 33:128-40.
30. Wakim LM, Woodward-Davis A, Bevan MJ: Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:17872-9.
31. Wakim LM, Woodward-Davis A, Liu R, Hu Y, Villadangos J, Smyth G, Bevan MJ: The molecular signature of tissue resident memory CD8 T cells isolated from the brain. Journal of immunology (Baltimore, Md.: 1950) 2012, 189:3462-71.
32. Skon CN, Lee J, Anderson KG, Masopust D, Hogquist KA, Jameson SC: Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nature immunology 2013, 14:1285-93.
33. Araki Y, Wang Z, Zang C, Wood WH, Schones D, Cui K, Roh T, Lhotsky B, Wersto RP, Peng W, Becker KG, Zhao K, Weng N: Genome-wide analysis of histone methylation reveals chromatin state-based regulation of gene transcription and function of memory CD8+ T cells. Immunity 2009, 30:912-25.
34. Russ BE, Olshanksy M, Smallwood HS, Li J, Denton AE, Prier JE, Stock AT, Croom HA, Cullen JG, Nguyen, Michelle LT, Rowe S, Olson MR, Finkelstein DB, Kelso A, Thomas PG, Speed TP, Rao S, Turner SJ: Distinct epigenetic signatures delineate transcriptional programs during virus-specific CD8(+) T cell differentiation. Immunity 2014, 41:853-65.
35. Scharer CD, Barwick BG, Youngblood BA, Ahmed R, Boss JM: Global DNA methylation remodeling accompanies CD8 T cell effector function. Journal of immunology (Baltimore, Md.: 1950) 2013, 191:3419-29.
36. Angelosanto JM, Blackburn SD, Crawford A, Wherry EJ: Progressive loss of memory T cell potential and commitment to exhaustion during chronic viral infection. Journal of virology 2012, 86:8161-70.
37. Youngblood B, Oestreich KJ, Ha S, Duraiswamy J, Akondy RS, West EE, Wei Z, Lu P, Austin JW, Riley JL, Boss JM, Ahmed R: Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity 2011, 35:400-12.
38. Youngblood B, Noto A, Porichis F, Akondy RS, Ndhlovu ZM, Austin JW, Bordi R, Procopio FA, Miura T, Allen TM, Sidney J, Sette A, Walker BD, Ahmed R, Boss JM, Sékaly R, Kaufmann DE: Cutting edge: Prolonged exposure to HIV reinforces a poised epigenetic program for PD-1 expression in virus-specific CD8 T cells. Journal of immunology (Baltimore, Md.: 1950) 2013, 191:540-4.
39. Tubo NJ, Pagán AJ, Taylor JJ, Nelson RW, Linehan JL, Ertelt JM, Huseby ES, Way SS, Jenkins MK: Single naive CD4+ T cells from a diverse repertoire produce different effector cell types during infection. Cell 2013, 153:785-96.
40. Plumlee CR, Sheridan BS, Cicek BB, Lefrançois L: Environmental cues dictate the fate of individual CD8+ T cells responding to infection. Immunity 2013, 39:347-56.
41. Gerlach C, Rohr JC, Perié L, van Rooij N, van Heijst, Jeroen WJ, Velds A, Urbanus J, Naik SH, Jacobs H, Beltman JB, de Boer, Rob J, Schumacher, Ton NM: Heterogeneous differentiation patterns of individual CD8+ T cells. Science (New York, NY) 2013, 340:635-9.
42. Buchholz VR, Flossdorf M, Hensel I, Kretschmer L, Weissbrich B, Gräf P, Verschoor A, Schiemann M, Höfer T, Busch DH: Disparate individual fates compose robust CD8+ T cell immunity. Science (New York, NY) 2013, 340:630-5.
43. Schober SL, Kuo CT, Schluns KS, Lefrancois L, Leiden JM, Jameson SC: Expression of the transcription factor lung Krüppel-like factor is regulated by cytokines and correlates with survival of memory T cells in vitro and in vivo. Journal of immunology (Baltimore, Md.: 1950) 1999, 163:3662-7.
44. Ichii H, Sakamoto A, Hatano M, Okada S, Toyama H, Taki S, Arima M, Kuroda Y, Tokuhisa T: Role for Bcl-6 in the generation and maintenance of memory CD8+ T cells. Nature immunology 2002, 3:558-63.
45. Kelly J, Spolski R, Imada K, Bollenbacher J, Lee S, Leonard WJ: A role for Stat5 in CD8+ T cell homeostasis. Journal of immunology (Baltimore, Md.: 1950) 2003, 170:210-7.
46. Burchill MA, Goetz CA, Prlic M, O'Neil JJ, Harmon IR, Bensinger SJ, Turka LA, Brennan P, Jameson SC, Farrar MA: Distinct effects of STAT5 activation on CD4+ and CD8+ T cell homeostasis: development of CD4+CD25+ regulatory T cells versus CD8+ memory T cells. Journal of immunology (Baltimore, Md.: 1950) 2003, 171:5853-64.
47. Manders PM, Hunter PJ, Telaranta AI, Carr JM, Marshall JL, Carrasco M, Murakami Y, Palmowski MJ, Cerundolo V, Kaech SM, Ahmed R, Fearon DT: BCL6b mediates the enhanced magnitude of the secondary response of memory CD8+ T lymphocytes. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:7418-25.
48. Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT, Palanivel VR, Mullen AC, Gasink CR, Kaech SM, Miller JD, Gapin L, Ryan K, Russ AP, Lindsten T, Orange JS, Goldrath AW, Ahmed R, Reiner SL: Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nature immunology 2005, 6:1236-44.
49. Cannarile MA, Lind NA, Rivera R, Sheridan AD, Camfield KA, Wu BB, Cheung KP, Ding Z, Goldrath AW: Transcriptional regulator Id2 mediates CD8+ T cell immunity. Nature immunology 2006, 7:1317-25.
50. Yang CY, Best JA, Knell J, Yang E, Sheridan AD, Jesionek AK, Li HS, Rivera RR, Lind KC, D ' Cruz LM, Watowich SS, Murre C, Goldrath AW: The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8+ T cell subsets. Nature immunology 2011, 12:1221-9.
51. Yamada T, Park CS, Mamonkin M, Lacorazza HD: Transcription factor ELF4 controls the proliferation and homing of CD8+ T cells via the Krüppel-like factors KLF4 and KLF2. Nature immunology 2009, 10:618-26.
52. Zhou X, Yu S, Zhao D, Harty JT, Badovinac VP, Xue H: Differentiation and persistence of memory CD8(+) T cells depend on T cell factor 1. Immunity 2010, 33:229-40.
53. Grenningloh R, Tai T, Frahm N, Hongo TC, Chicoine AT, Brander C, Kaufmann DE, Ho I: Ets-1 maintains IL-7 receptor expression in peripheral T cells. Journal of immunology (Baltimore, Md.: 1950) 2011, 186:969-76.
54. Siegel AM, Heimall J, Freeman AF, Hsu AP, Brittain E, Brenchley JM, Douek DC, Fahle GH, Cohen JI, Holland SM, Milner JD: A critical role for STAT3 transcription factor signaling in the development and maintenance of human T cell memory. Immunity 2011, 35:806-18.
55. Cui W, Liu Y, Weinstein JS, Craft J, Kaech SM: An interleukin-21-interleukin-10-STAT3 pathway is critical for functional maturation of memory CD8+ T cells. Immunity 2011, 35:792-805.
56. Sullivan JA, Kim EH, Plisch EH, Peng SL, Suresh M: FOXO3 regulates CD8 T cell memory by T cell-intrinsic mechanisms. PLoS pathogens 2012, 8:e1002533.
57. Rao RR, Li Q, Gubbels Bupp, Melanie R, Shrikant PA: Transcription factor Foxo1 represses T-bet-mediated effector functions and promotes memory CD8(+) T cell differentiation. Immunity 2012, 36:374-87.
58. Nayar R, Schutten E, Bautista B, Daniels K, Prince AL, Enos M, Brehm MA, Swain SL, Welsh RM, Berg LJ: Graded levels of IRF4 regulate CD8+ T cell differentiation and expansion, but not attrition, in response to acute virus infection. Journal of immunology (Baltimore, Md.: 1950) 2014, 192:5881-93.