Epigenetic modifications induced by blimp-1 regulate CD8+ T cell memory progression during acute virus infection

Immunity

Volumn 39, Issue 4, 2013, Pages 661-675

  Shin, HyunMu ^a   Kapoor, VarunN ^a   Guan, Tianxia ^b,c   Kaech, SusanM ^b,c   Welsh, RaymondM ^a   Berg, LeslieJ ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CYTOKINE; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BLIMP 1; UNCLASSIFIED DRUG;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPIGENETICS; GENE SILENCING; GENOME; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD27; CD8-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; EPIGENESIS, GENETIC; HISTONE DEACETYLASE 2; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; IMMUNOLOGIC MEMORY; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; METHYLATION; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84885858374     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.08.032     Document Type: Article

References (47)

1. Ancelin K., Lange U.C., Hajkova P., Schneider R., Bannister A.J., Kouzarides T., Surani M.A. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat. Cell Biol. 2006, 8:623-630.
2. Araki Y., Wang Z., Zang C., Wood W.H., Schones D., Cui K., Roh T.Y., Lhotsky B., Wersto R.P., Peng W., et al. Genome-wide analysis of histone methylation reveals chromatin state-based regulation of gene transcription and function of memory CD8+ Tcells. Immunity 2009, 30:912-925.
3. Banerjee A., Gordon S.M., Intlekofer A.M., Paley M.A., Mooney E.C., Lindsten T., Wherry E.J., Reiner S.L. Cutting edge: The transcription factor eomesodermin enables CD8+ Tcells to compete for the memory cell niche. J.Immunol. 2010, 185:4988-4992.
4. Blattman J.N., Grayson J.M., Wherry E.J., Kaech S.M., Smith K.A., Ahmed R. Therapeutic use of IL-2 to enhance antiviral T-cell responses invivo. Nat. Med. 2003, 9:540-547.
5. Boyman O., Sprent J. The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 2012, 12:180-190.
6. Collins R., Cheng X. A case study in cross-talk: the histone lysine methyltransferases G9a and GLP. Nucleic Acids Res. 2010, 38:3503-3511.
7. de Jong R., Loenen W.A., Brouwer M., van Emmerik L., de Vries E.F., Borst J., van Lier R.A. Regulation of expression of CD27, a Tcell-specific member of a novel family of membrane receptors. J.Immunol. 1991, 146:2488-2494.
8. Doering T.A., Crawford A., Angelosanto J.M., Paley M.A., Ziegler C.G., Wherry E.J. Network analysis reveals centrally connected genes and pathways involved in CD8+ Tcell exhaustion versus memory. Immunity 2012, 37:1130-1144.
9. Dolfi D.V., Boesteanu A.C., Petrovas C., Xia D., Butz E.A., Katsikis P.D. Late signals from CD27 prevent Fas-dependent apoptosis of primary CD8+ Tcells. J.Immunol. 2008, 180:2912-2921.
10. Duttagupta P.A., Boesteanu A.C., Katsikis P.D. Costimulation signals for memory CD8+ Tcells during viral infections. Crit. Rev. Immunol. 2009, 29:469-486.
11. Gong D., Malek T.R. Cytokine-dependent Blimp-1 expression in activated Tcells inhibits IL-2 production. J.Immunol. 2007, 178:242-252.
12. Gyory I., Wu J., Fejér G., Seto E., Wright K.L. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol. 2004, 5:299-308.
13. Hendriks J., Gravestein L.A., Tesselaar K., van Lier R.A., Schumacher T.N., Borst J. CD27 is required for generation and long-term maintenance of Tcell immunity. Nat. Immunol. 2000, 1:433-440.
14. Hikono H., Kohlmeier J.E., Takamura S., Wittmer S.T., Roberts A.D., Woodland D.L. Activation phenotype, rather than central- or effector-memory phenotype, predicts the recall efficacy of memory CD8+ Tcells. J.Exp. Med. 2007, 204:1625-1636.
15. Hintzen R.Q., Lens S.M., Beckmann M.P., Goodwin R.G., Lynch D., van Lier R.A. Characterization of the human CD27 ligand, a novel member of the TNF gene family. J.Immunol. 1994, 152:1762-1773.
16. Ji Y., Pos Z., Rao M., Klebanoff C.A., Yu Z., Sukumar M., Reger R.N., Palmer D.C., Borman Z.A., Muranski P., et al. Repression of the DNA-binding inhibitor Id3 by Blimp-1 limits the formation of memory CD8+ Tcells. Nat. Immunol. 2011, 12:1230-1237.
17. Joshi N.S., Cui W., Chandele A., Lee H.K., Urso D.R., Hagman J., Gapin L., Kaech S.M. Inflammation directs memory precursor and short-lived effector CD8(+) Tcell fates via the graded expression of T-bet transcription factor. Immunity 2007, 27:281-295.
18. Kalia V., Sarkar S., Subramaniam S., Haining W.N., Smith K.A., Ahmed R. Prolonged interleukin-2Ralpha expression on virus-specific CD8+ Tcells favors terminal-effector differentiation invivo. Immunity 2010, 32:91-103.
19. Kallies A., Hawkins E.D., Belz G.T., Metcalf D., Hommel M., Corcoran L.M., Hodgkin P.D., Nutt S.L. Transcriptional repressor Blimp-1 is essential for Tcell homeostasis and self-tolerance. Nat. Immunol. 2006, 7:466-474.
20. Kallies A., Xin A., Belz G.T., Nutt S.L. Blimp-1 transcription factor is required for the differentiation of effector CD8(+) Tcells and memory responses. Immunity 2009, 31:283-295.
21. Kim H.P., Kelly J., Leonard W.J. The basis for IL-2-induced IL-2 receptor alpha chain gene regulation: importance of two widely separated IL-2 response elements. Immunity 2001, 15:159-172.
22. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
23. Kubicek S., O'Sullivan R.J., August E.M., Hickey E.R., Zhang Q., Teodoro M.L., Rea S., Mechtler K., Kowalski J.A., Homon C.A., et al. Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase. Mol. Cell 2007, 25:473-481.
24. Lehnertz B., Northrop J.P., Antignano F., Burrows K., Hadidi S., Mullaly S.C., Rossi F.M., Zaph C. Activating and inhibitory functions for the histone lysine methyltransferase G9a in T helper cell differentiation and function. J.Exp. Med. 2010, 207:915-922.
25. Malek T.R. The biology of interleukin-2. Annu. Rev. Immunol. 2008, 26:453-479.
26. Martins G., Calame K. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu. Rev. Immunol. 2008, 26:133-169.
27. Martins G.A., Cimmino L., Shapiro-Shelef M., Szabolcs M., Herron A., Magnusdottir E., Calame K. Transcriptional repressor Blimp-1 regulates Tcell homeostasis and function. Nat. Immunol. 2006, 7:457-465.
28. Martins G.A., Cimmino L., Liao J., Magnusdottir E., Calame K. Blimp-1 directly represses Il2 and the Il2 activator Fos, attenuating Tcell proliferation and survival. J.Exp. Med. 2008, 205:1959-1965.
29. Mitchell D.M., Ravkov E.V., Williams M.A. Distinct roles for IL-2 and IL-15 in the differentiation and survival of CD8+ effector and memory Tcells. J.Immunol. 2010, 184:6719-6730.
30. Nolte M.A., Arens R., van Os R., van Oosterwijk M., Hooibrink B., van Lier R.A., van Oers M.H. Immune activation modulates hematopoiesis through interactions between CD27 and CD70. Nat. Immunol. 2005, 6:412-418.
31. Obar J.J., Lefrançois L. Memory CD8+ Tcell differentiation. Ann. N Y Acad. Sci. 2010, 1183:251-266.
32. Ohinata Y., Payer B., O'Carroll D., Ancelin K., Ono Y., Sano M., Barton S.C., Obukhanych T., Nussenzweig M., Tarakhovsky A., et al. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 2005, 436:207-213.
33. Peperzak V., Veraar E.A., Keller A.M., Xiao Y., Borst J. The Pim kinase pathway contributes to survival signaling in primed CD8+ Tcells upon CD27 costimulation. J.Immunol. 2010, 185:6670-6678.
34. Peperzak V., Xiao Y., Veraar E.A., Borst J. CD27 sustains survival of CTLs in virus-infected nonlymphoid tissue in mice by inducing autocrine IL-2 production. J.Clin. Invest. 2010, 120:168-178.
35. Pipkin M.E., Sacks J.A., Cruz-Guilloty F., Lichtenheld M.G., Bevan M.J., Rao A. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic Tcells. Immunity 2010, 32:79-90.
36. Piskurich J.F., Lin K.I., Lin Y., Wang Y., Ting J.P., Calame K. BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells. Nat. Immunol. 2000, 1:526-532.
37. Razvi E.S., Jiang Z., Woda B.A., Welsh R.M. Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, lpr, and Bcl-2-transgenic mice. Am. J. Pathol. 1995, 147:79-91.
38. Rutishauser R.L., Martins G.A., Kalachikov S., Chandele A., Parish I.A., Meffre E., Jacob J., Calame K., Kaech S.M. Transcriptional repressor Blimp-1 promotes CD8(+) Tcell terminal differentiation and represses the acquisition of central memory Tcell properties. Immunity 2009, 31:296-308.
39. Sarkar S., Kalia V., Haining W.N., Konieczny B.T., Subramaniam S., Ahmed R. Functional and genomic profiling of effector CD8 Tcell subsets with distinct memory fates. J.Exp. Med. 2008, 205:625-640.
40. Shi M., Lin T.H., Appell K.C., Berg L.J. Cell cycle progression following naive Tcell activation is independent of Jak3/common gamma-chain cytokine signals. J.Immunol. 2009, 183:4493-4501.
41. Shin H., Blackburn S.D., Intlekofer A.M., Kao C., Angelosanto J.M., Reiner S.L., Wherry E.J. A role for the transcriptional repressor Blimp-1 in CD8(+) Tcell exhaustion during chronic viral infection. Immunity 2009, 31:309-320.
42. Smith M.A., Wright G., Wu J., Tailor P., Ozato K., Chen X., Wei S., Piskurich J.F., Ting J.P., Wright K.L. Positive regulatory domain I (PRDM1) and IRF8/PU.1 counter-regulate MHC class II transactivator (CIITA) expression during dendritic cell maturation. J.Biol. Chem. 2011, 286:7893-7904.
43. Su S.T., Ying H.Y., Chiu Y.K., Lin F.R., Chen M.Y., Lin K.I. Involvement of histone demethylase LSD1 in Blimp-1-mediated gene repression during plasma cell differentiation. Mol. Cell. Biol. 2009, 29:1421-1431.
44. Thomas L.R., Miyashita H., Cobb R.M., Pierce S., Tachibana M., Hobeika E., Reth M., Shinkai Y., Oltz E.M. Functional analysis of histone methyltransferase g9a in B and T lymphocytes. J.Immunol. 2008, 181:485-493.
45. Weng N.P., Araki Y., Subedi K. The molecular basis of the memory Tcell response: differential gene expression and its epigenetic regulation. Nat. Rev. Immunol. 2012, 12:306-315.
46. Williams M.A., Tyznik A.J., Bevan M.J. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory Tcells. Nature 2006, 441:890-893.
47. Yu J., Angelin-Duclos C., Greenwood J., Liao J., Calame K. Transcriptional repression by blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol. Cell. Biol. 2000, 20:2592-2603.