Infection history determines the differentiation state of human CD8+ T cells

Journal of Virology

Volumn 89, Issue 9, 2015, Pages 5110-5123

  van Aalderen, Michiel C ^a   Remmerswaal, Ester B M ^a   Verstegen, Niels J M ^a   Hombrink, Pleun ^b   ten Brinke, Anja ^b   Pircher, Hanspeter ^c   Kootstra, Neeltje A ^a   tenBerge, Ineke J M ^a   van Lier, René A W ^b  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b SANQUIN RESEARCH   (Netherlands)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD28 ANTIGEN; CD45RA ANTIGEN; CHEMOKINE RECEPTOR CCR7; EOMESODERMIN; EPITOPE; TRANSCRIPTION FACTOR T BET; EOMES PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21;

ADULT; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FEMALE; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN RESPIRATORY SYNCYTIAL VIRUS; INFLUENZA VIRUS A; LYMPHOCYTE DIFFERENTIATION; MALE; MIDDLE AGED; PRIMARY INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURFACE PROPERTY; VIRUS INFECTION; VIRUS LOAD; ADOLESCENT; CELL DIFFERENTIATION; CHEMISTRY; IMMUNOLOGY; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION; VIRUS; YOUNG ADULT;

HUMAN HERPESVIRUS 4; HUMAN HERPESVIRUS 5; HUMAN IMMUNODEFICIENCY VIRUS 1; INFLUENZA A VIRUS; RESPIRATORY SYNCYTIAL VIRUS;

ADOLESCENT; ADULT; ANTIGENS, CD; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; HUMANS; MALE; MIDDLE AGED; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTE SUBSETS; VIRUSES; YOUNG ADULT;

EID: 84928550643     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03478-14     Document Type: Article

References (52)

1. Appay V, Dunbar PR, Callan M, Klenerman P, Gillespie GM, Papagno L, Ogg GS, King A, Lechner F, Spina CA, Little S, Havlir DV, Richman DD, Gruener N, Pape G, Waters A, Easterbrook P, Salio M, Cerundolo V, McMichael AJ, Rowland-Jones SL. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat Med 8:379-385. http://dx.doi.org/10.1038/nm0402-379.
2. van Lier RA, ten Berge IJ, Gamadia LE. 2003. Human CD8(+) T-cell differentiation in response to viruses. Nat Rev Immunol 3:931-939. http://dx.doi.org/10.1038/nri1254.
3. van Aalderen MC, Remmerswaal EB, ten Berge IJ, van Lier RA. 2014. Blood and beyond: properties of circulating and tissue-resident human virus-specific alphabeta CD8(+) T cells. Eur J Immunol 44:934-944. http://dx.doi.org/10.1002/eji.201344269.
4. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-712. http://dx.doi.org/10.1038/44385.
5. Hislop AD, Gudgeon NH, Callan MF, Fazou C, Hasegawa H, Salmon M, Rickinson AB. 2001. EBV-specific CD8+ T cell memory: relationships between epitope specificity, cell phenotype, and immediate effector function. J Immunol 167:2019-2029. http://dx.doi.org/10.4049/jimmunol.167.4.2019.
6. van Aalderen MC, Remmerswaal EB, Heutinck KM, ten Brinke A, Pircher H, van Lier RA, ten Berge IJ. 2013. Phenotypic and functional characterization of circulating polyomavirus BK VP1-specific CD8+ T cells in healthy adults. J Virol 87:10263-10272. http://dx.doi.org/10.1128/JVI.01540-13.
7. Heidema J, de Bree GJ, De Graaff PM, van Maren WW, Hoogerhout P, Out TA, Kimpen JL, van Bleek GM. 2004. Human CD8(+) T cell responses against five newly identified respiratory syncytial virusderived epitopes. J Gen Virol 85:2365-2374. http://dx.doi.org/10.1099/vir.0.80131-0.
8. de Bree GJ, Heidema J, van Leeuwen EM, van Bleek GM, Jonkers RE, Jansen HM, van Lier RA, Out TA. 2005. Respiratory syncytial virusspecific CD8+ memory T cell responses in elderly persons. J Infect Dis 191:1710-1718. http://dx.doi.org/10.1086/429695.
9. Hoji A, Rinaldo CR, Jr. 2005. Human CD8+T cells specific for influenza A virusM1display broad expression of maturation-associated phenotypic markers and chemokine receptors. Immunology 115:239-245. http://dx.doi.org/10.1111/j.1365-2567.2005.02135.x.
10. He XS, Mahmood K, Maecker HT, Holmes TH, Kemble GW, Arvin AM, Greenberg HB. 2003. Analysis of the frequencies and of the memory T cell phenotypes of human CD8+T cells specific for influenza A viruses. J Infect Dis 187:1075-1084. http://dx.doi.org/10.1086/368218.
11. Hamann D, Baars PA, Rep MH, Hooibrink B, Kerkhof-Garde SR, Klein MR, van Lier RA. 1997. Phenotypic and functional separation of memory and effector human CD8+ T cells. J Exp Med 186:1407-1418. http://dx.doi.org/10.1084/jem.186.9.1407.
12. Romero P, Zippelius A, Kurth I, Pittet MJ, Touvrey C, Iancu EM, Corthesy P, Devevre E, Speiser DE, Rufer N. 2007. Four functionally distinct populations of human effector-memory CD8+ T lymphocytes. J Immunol 178: 4112-4119. http://dx.doi.org/10.4049/jimmunol.178.7.4112.
13. van Leeuwen EM, de Bree GJ, Remmerswaal EB, Yong SL, Tesselaar K, ten Berge IJ, van Lier RA. 2005. IL-7 receptor alpha chain expression distinguishes functional subsets of virus-specific human CD8+ T cells. Blood 106:2091-2098. http://dx.doi.org/10.1182/blood-2005-02-0449.
14. Gamadia LE, van Leeuwen EM, Remmerswaal EB, Yong SL, Surachno S, Wertheim-van Dillen PM, ten Berge IJ, van Lier RA. 2004. The size and phenotype of virus-specific T cell populations is determined by repetitive antigenic stimulation and environmental cytokines. J Immunol 172: 6107-6114. http://dx.doi.org/10.4049/jimmunol.172.10.6107.
15. van Leeuwen EM, Gamadia LE, Baars PA, Remmerswaal EB, ten Berge IJ, van Lier RA. 2002. Proliferation requirements of cytomegalovirusspecific, effector-type human CD8+ T cells. J Immunol 169:5838-5843. http://dx.doi.org/10.4049/jimmunol.169.10.5838.
16. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. 2000. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100:655-669. http://dx.doi.org/10.1016/S0092-8674(00)80702-3.
17. Szabo SJ, Sullivan BM, Stemmann C, Satoskar AR, Sleckman BP, Glimcher LH. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science 295:338-342. http://dx.doi.org/10.1126/science.1065543.
18. Pearce EL, Mullen AC, Martins GA, Krawczyk CM, Hutchins AS, Zediak VP, Banica M, DiCioccio CB, Gross DA, Mao CA, Shen H, Cereb N, Yang SY, Lindsten T, Rossant J, Hunter CA, Reiner SL. 2003. Control of effector CD8+ T cell function by the transcription factor eomesodermin. Science 302:1041-1043. http://dx.doi.org/10.1126/science.1090148.
19. Kaech SM, Cui W. 2012. Transcriptional control of effector and memory CD8+T cell differentiation. Nat Rev Immunol 12:749-761. http://dx.doi.org/10.1038/nri3307.
20. Intlekofer AM, Takemoto N, Kao C, Banerjee A, Schambach F, Northrop JK, Shen H, Wherry EJ, Reiner SL. 2007. Requirement for T-bet in the aberrant differentiation of unhelped memoryCD8+T cells. J ExpMed 204:2015-2021. http://dx.doi.org/10.1084/jem.20070841.
21. Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, Hagman J, Gapin L, Kaech SM. 2007. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295. http://dx.doi.org/10.1016/j.immuni.2007.07.010.
22. 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. 2005. Effector and memory CD8+T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6:1236-1244. http://dx.doi.org/10.1038/ni1268.
23. Takemoto N, Intlekofer AM, Northrup JT, Wherry EJ, Reiner SL. 2006. Cutting edge: IL-12 inversely regulates T-bet and eomesodermin expression during pathogen-induced CD8+ T cell differentiation. J Immunol 177:7515-7519. http://dx.doi.org/10.4049/jimmunol.177.11.7515.
24. Banerjee A, Gordon SM, Intlekofer AM, Paley MA, Mooney EC, Lindsten T, Wherry EJ, Reiner SL. 2010. Cutting edge: the transcription factor eomesodermin enables CD8+ T cells to compete for the memory cell niche. J Immunol 185:4988-4992. http://dx.doi.org/10.4049/jimmunol.1002042.
25. McLane LM, Banerjee PP, Cosma GL, Makedonas G, Wherry EJ, Orange JS, Betts MR. 2013. Differential localization of T-bet and Eomes in CD8 T cell memory populations. J Immunol 190:3207-3215. http://dx.doi.org/10.4049/jimmunol.1201556.
26. Smith C, Elhassen D, Gras S, Wynn KK, Dasari V, Tellam J, Tey SK, Rehan S, Liu YC, Rossjohn J, Burrows SR, Khanna R. 2012. Endogenous antigen presentation impacts on T-box transcription factor expression and functional maturation of CD8+ T cells. Blood 120:3237-3245. http://dx.doi.org/10.1182/blood-2012-03-420182.
27. Knox JJ, Cosma GL, Betts MR, McLane LM. 2014. Characterization of T-bet and Eomes in peripheral human immune cells. Front Immunol 5:217. http://dx.doi.org/10.3389/fimmu.2014.00217.
28. Dolfi DV, Mansfield KD, Polley AM, Doyle SA, Freeman GJ, Pircher H, Schmader KE, Wherry EJ. 2013. Increased T-bet is associated with senescence of influenza virus-specificCD8T cells in aged humans. J Leukoc Biol 93:825-836. http://dx.doi.org/10.1189/jlb.0912438.
29. Buggert M, Tauriainen J, Yamamoto T, Frederiksen J, Ivarsson MA, Michaelsson J, Lund O, Hejdeman B, Jansson M, Sonnerborg A, Koup RA, Betts MR, Karlsson AC. 2014. T-bet and Eomes are differentially linked to the exhausted phenotype of CD8+T cells in HIV infection. PLoS Pathog 10:e1004251. http://dx.doi.org/10.1371/journal.ppat.1004251.
30. Geskus RB. 2000. On the inclusion of prevalent cases in HIV/AIDS natural history studies through a marker-based estimate of time since seroconversion. Stat Med 19:1753-1769. http://dx.doi.org/10.1002/1097-0258(20000715)19:13<1753::AID-SIM487>3.0.CO;2-F.
31. Marcolino I, Przybylski GK, Koschella M, Schmidt CA, Voehringer D, Schlesier M, Pircher H. 2004. Frequent expression of the natural killer cell receptor KLRG1 in human cord blood T cells: correlation with replicative history. Eur J Immunol 34:2672-2680. http://dx.doi.org/10.1002/eji.200425282.
32. Klarenbeek PL, Remmerswaal EB, ten Berge IJ, Doorenspleet ME, van Schaik BD, Esveldt RE, Koch SD, ten Brinke A, van Kampen AH, Bemelman FJ, Tak PP, Baas F, de Vries N, van Lier RA. 2012. Deep sequencing of antiviral T-cell responses to HCMV and EBV in humans reveals a stable repertoire that is maintained for many years. PLoS Pathog 8:e1002889. http://dx.doi.org/10.1371/journal.ppat.1002889.
33. van Manen D, Delaneau O, Kootstra NA, Boeser-Nunnink BD, Limou S, Bol SM, Burger JA, Zwinderman AH, Moerland PD, van 't Slot R, Zagury JF, van 't Wout AB, Schuitemaker H. 2011. Genome-wide association scan in HIV-1-infected individuals identifying variants influencing disease course. PLoS One 6:e22208. http://dx.doi.org/10.1371/journal.pone.0022208.
34. Papagno L, Spina CA, Marchant A, Salio M, Rufer N, Little S, Dong T, Chesney G, Waters A, Easterbrook P, Dunbar PR, Shepherd D, Cerundolo V, Emery V, Griffiths P, Conlon C, McMichael AJ, Richman DD, Rowland-Jones SL, Appay V. 2004. Immune activation and CD8+ T-cell differentiation towards senescence in HIV-1 infection. PLoS Biol 2:E20. http://dx.doi.org/10.1371/journal.pbio.0020020.
35. Gamadia LE, Rentenaar RJ, Baars PA, Remmerswaal EB, Surachno S, Weel JF, Toebes M, Schumacher TN, ten Berge IJ, van Lier RA. 2001. Differentiation of cytomegalovirus-specific CD8(+) T cells in healthy and immunosuppressed virus carriers. Blood 98:754-761. http://dx.doi.org/10.1182/blood. V98.3.754.
36. Kimura MY, Pobezinsky LA, Guinter TI, Thomas J, Adams A, Park JH, Tai X, Singer A. 2013. IL-7 signaling must be intermittent, not continuous, during CD8(+) T cell homeostasis to promote cell survival instead of cell death. Nat Immunol 14:143-151. http://dx.doi.org/10.1038/ni.2494.
37. Susanto O, Trapani JA, Brasacchio D. 2012. Controversies in granzyme biology. Tissue Antigens 80:477-487. http://dx.doi.org/10.1111/tan.12014.
38. Bovenschen N, Kummer JA. 2010. Orphan granzymes find a home. Immunol Rev 235:117-127. http://dx.doi.org/10.1111/j.0105-2896.2010.00889.x.
39. Zhong C, Li C, Wang X, Toyoda T, Gao G, Fan Z. 2012. Granzyme K inhibits replication of influenza virus through cleaving the nuclear transport complex importin alpha1/beta dimer of infected host cells. Cell Death Differ 19:882-890. http://dx.doi.org/10.1038/cdd.2011.178.
40. Henson SM, Akbar AN. 2009. KLRG1-more than a marker for T cell senescence. Age 31:285-291. http://dx.doi.org/10.1007/s11357-009-9100-9.
41. Voehringer D, Koschella M, Pircher H. 2002. Lack of proliferative capacity of human effector and memory T cells expressing killer cell lectinlike receptor G1 (KLRG1). Blood 100:3698-3702. http://dx.doi.org/10.1182/blood-2002-02-0657.
42. Bratke K, Kuepper M, Bade B, Virchow JC, Jr, Luttmann W. 2005. Differential expression of human granzymes A, B, and K in natural killer cells and during CD8+ T cell differentiation in peripheral blood. Eur J Immunol 35:2608-2616. http://dx.doi.org/10.1002/eji.200526122.
43. Jagannathan P, Osborne CM, Royce C, Manion MM, Tilton JC, Li L, Fischer S, Hallahan CW, Metcalf JA, McLaughlin M, Pipeling M, McDyer JF, Manley TJ, Meier JL, Altman JD, Hertel L, Davey RT, Jr, Connors M, Migueles SA. 2009. Comparisons of CD8+T cells specific for human immunodeficiency virus, hepatitis C virus, and cytomegalovirus reveal differences in frequency, immunodominance, phenotype, and interleukin-2 responsiveness. J Virol 83:2728-2742. http://dx.doi.org/10.1128/JVI.02128-08.
44. Hersperger AR, Martin JN, Shin LY, Sheth PM, Kovacs CM, Cosma GL, Makedonas G, Pereyra F, Walker BD, Kaul R, Deeks SG, Betts MR. 2011. Increased HIV-specific CD8+T-cell cytotoxic potential in HIV elite controllers is associated with T-bet expression. Blood 117:3799-3808. http://dx.doi.org/10.1182/blood-2010-12-322727.
45. Miyazaki I, Cheung RK, Dosch HM. 1993. Viral interleukin 10 is critical for the induction of B cell growth transformation by Epstein-Barr virus. J Exp Med 178:439-447. http://dx.doi.org/10.1084/jem.178.2.439.
46. Cheung TC, Humphreys IR, Potter KG, Norris PS, Shumway HM, Tran BR, Patterson G, Jean-Jacques R, Yoon M, Spear PG, Murphy KM, Lurain NS, Benedict CA, Ware CF. 2005. Evolutionarily divergent herpesviruses modulate T cell activation by targeting the herpesvirus entry mediator cosignaling pathway. Proc Natl Acad Sci USA 102:13218-13223. http://dx.doi.org/10.1073/pnas.0506172102.
47. Avdic S, Cao JZ, Cheung AK, Abendroth A, Slobedman B. 2011. Viral interleukin-10 expressed by human cytomegalovirus during the latent phase of infection modulates latently infected myeloid cell differentiation. J Virol 85:7465-7471. http://dx.doi.org/10.1128/JVI.00088-11.
48. Majumder B, Janket ML, Schafer EA, Schaubert K, Huang XL, Kan-Mitchell J, Rinaldo CR, Jr, Ayyavoo V. 2005. Human immunodeficiency virus type 1 Vpr impairs dendritic cell maturation and T-cell activation: implications for viral immune escape. J Virol 79:7990-8003. http://dx.doi.org/10.1128/JVI.79.13.7990-8003.2005.
49. Kurachi M, Barnitz RA, Yosef N, Odorizzi PM, DiIorio MA, Lemieux ME, Yates K, Godec J, Klatt MG, Regev A, Wherry EJ, Haining WN. 2014. The transcription factor BATF operates as an essential differentiation checkpoint in early effector CD8+T cells. Nat Immunol 15:373-383. http://dx.doi.org/10.1038/ni.2834.
50. Cruz-Guilloty F, Pipkin ME, Djuretic IM, Levanon D, Lotem J, Lichtenheld MG, Groner Y, Rao A. 2009. Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J Exp Med 206:51-59. http://dx.doi.org/10.1084/jem.20081242.
51. Djuretic IM, Levanon D, Negreanu V, Groner Y, Rao A, Ansel KM. 2007. Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells. Nat Immunol 8:145-153. http://dx.doi.org/10.1038/ni1424.
52. Hertoghs KM, Moerland PD, van Stijn A, Remmerswaal EB, Yong SL, van de Berg PJ, van Ham SM, Baas F, ten Berge IJ, van Lier RA. 2010. Molecular profiling of cytomegalovirus-induced human CD8+T cell differentiation. J Clin Invest 120:4077-4090. http://dx.doi.org/10.1172/JCI42758.