Persistence of EBV Antigen-Specific CD8 T Cell Clonotypes during Homeostatic Immune Reconstitution in Cancer Patients

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Iancu, Emanuela M ^a   Gannon, Philippe O ^a   Laurent, Julien ^a,c   Gupta, Bhawna ^a,b   Romero, Pedro ^a,b   Michielin, Olivier ^a,b   Romano, Emanuela ^a   Speiser, Daniel E ^a,b   Rufer, Nathalie ^a,b  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c Merck Serono GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BUSULFAN; CD27 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CYCLOPHOSPHAMIDE; EOMESODERMIN; FLUDARABINE; FREUND ADJUVANT; INTERLEUKIN 7; L SELECTIN; MELAN A; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ADULT; AGED; ANTIGEN SPECIFICITY; ARTICLE; CANCER CHEMOTHERAPY; CANCER PATIENT; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; GENE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE HOMEOSTASIS; IMMUNE RECONSTITUTION; IMMUNE RESPONSE; IN VIVO STUDY; LYMPHOCYTE CLONE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE HOMEOSTASIS; MELANOMA; PERSISTENT VIRUS INFECTION; PRIMARY INFECTION; T CELL DEPLETION; TRBV20 GENE; TRBV29 GENE; VIRUS REACTIVATION;

ADULT; AGED; AMINO ACID SEQUENCE; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CLONE CELLS; HERPESVIRUS 4, HUMAN; HOMEOSTASIS; HUMANS; MELANOMA; MIDDLE AGED; RECEPTORS, ANTIGEN, T-CELL; TIME FACTORS;

EID: 84886439024     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078686     Document Type: Article

References (60)

1. Rickinson AB, Moss DJ, (1997) Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu Rev Immunol 15: 405-431. doi:10.1146/annurev.immunol.15.1.405. PubMed: 9143694.
2. Hislop AD, Taylor GS, Sauce D, Rickinson AB, (2007) Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu Rev Immunol 25: 587-617. doi:10.1146/annurev.immunol.25.022106.141553. PubMed: 17378764.
3. Torti N, Oxenius A, (2012) T cell memory in the context of persistent herpes viral infections. Viruses 4: 1116-1143. doi:10.3390/v4071116. PubMed: 22852044.
4. Wiesel M, Walton S, Richter K, Oxenius A, (2009) Virus-specific CD8 T cells: activation, differentiation and memory formation. APMIS 117: 356-381. doi:10.1111/j.1600-0463.2009.02459.x. PubMed: 19400862.
5. Obar JJ, Lefrançois L, (2010) Memory CD8+ T cell differentiation. Ann N Y Acad Sci 1183: 251-266. doi:10.1111/j.1749-6632.2009.05126.x. PubMed: 20146720.
6. Kaech SM, Cui W, (2012) Transcriptional control of effector and memory CD8(+) T cell differentiation. Nat Rev Immunol 12: 749-761. doi:10.1038/nri3307. PubMed: 23080391.
7. Rocha B, Tanchot C, (2006) The Tower of Babel of CD8+ T-cell memory: known facts, deserted roads, muddy waters, and possible dead ends. Immunol Rev 211: 182-196. doi:10.1111/j.0105-2896.2006.00378.x. PubMed: 16824127.
8. Surh CD, Sprent J, (2008) Homeostasis of naive and memory T cells. Immunity 29: 848-862. doi:10.1016/j.immuni.2008.11.002. PubMed: 19100699.
9. Gattinoni L, Klebanoff CA, Restifo NP, (2012) Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer 12: 671-684. doi:10.1038/nrc3322. PubMed: 22996603.
10. Appay V, van Lier RA, Sallusto F, Roederer M, (2008) Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73: 975-983. PubMed: 18785267.
11. Rufer N, (2005) Molecular tracking of antigen-specific T-cell clones during immune responses. Curr Opin Immunol 17: 441-447. doi:10.1016/j.coi.2005.06.003. PubMed: 15955685.
12. Price DA, Brenchley JM, Ruff LE, Betts MR, Hill BJ, et al. (2005) Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J Exp Med 202: 1349-1361. doi:10.1084/jem.20051357. PubMed: 16287711.
13. Speiser DE, Wieckowski S, Gupta B, Iancu EM, Baumgaertner P, et al. (2011) Single cell analysis reveals similar functional competence of dominant and nondominant CD8 T-cell clonotypes. Proc Natl Acad Sci U S A 108: 15318-15323. doi:10.1073/pnas.1105419108. PubMed: 21876175.
14. Iancu EM, Corthesy P, Baumgaertner P, Devevre E, Voelter V, et al. (2009) Clonotype selection and composition of human CD8 T cells specific for persistent herpes viruses varies with differentiation but is stable over time. J Immunol 183: 319-331. doi:10.4049/jimmunol.0803647. PubMed: 19542443.
15. Speiser DE, Baumgaertner P, Barbey C, Rubio-Godoy V, Moulin A, et al. (2006) A novel approach to characterize clonality and differentiation of human melanoma-specific T cell responses: spontaneous priming and efficient boosting by vaccination. J Immunol 177: 1338-1348. PubMed: 16818795.
16. Derré L, Bruyninx M, Baumgaertner P, Devevre E, Corthesy P, et al. (2007) In Vivo Persistence of Codominant Human CD8+ T Cell Clonotypes Is Not Limited by Replicative Senescence or Functional Alteration. J Immunol 179: 2368-2379. PubMed: 17675498.
17. Annels NE, Callan MF, Tan L, Rickinson AB, (2000) Changing patterns of dominant TCR usage with maturation of an EBV-specific cytotoxic T cell response. J Immunol 165: 4831-4841. PubMed: 11046006.
18. Naumova EN, Gorski J, Naumov YN, (2009) Two compensatory pathways maintain long-term stability and diversity in CD8 T cell memory repertoires. J Immunol 183: 2851-2858. doi:10.4049/jimmunol.0900162. PubMed: 19635925.
19. Posavad CM, Huang ML, Barcy S, Koelle DM, Corey L, (2000) Long term persistence of herpes simplex virus-specific CD8+ CTL in persons with frequently recurring genital herpes. J Immunol 165: 1146-1152. PubMed: 10878394.
20. Barcy S, Huang ML, Corey L, Koelle DM, (2005) Longitudinal analysis of herpes simplex virus-specific CD4+ cell clonotypes in infected tissues and blood. J Infect Dis 191: 2012-2021. doi:10.1086/430389. PubMed: 15897986.
21. Levitsky V, de Campos-Lima PO, Frisan T, Masucci MG, (1998) The clonal composition of a peptide-specific oligoclonal CTL repertoire selected in response to persistent EBV infection is stable over time. J Immunol 161: 594-601. PubMed: 9670932.
22. van Bockel DJ, Price DA, Munier ML, Venturi V, Asher TE, et al. (2011) Persistent survival of prevalent clonotypes within an immunodominant HIV gag-specific CD8+ T cell response. J Immunol 186: 359-371. doi:10.4049/jimmunol.1001807. PubMed: 21135165.
23. Klarenbeek PL, Remmerswaal EB, ten Berge IJ, Doorenspleet ME, van Schaik BD, et al. (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. PubMed: 23028307.
24. Appay V, Voelter V, Rufer N, Reynard S, Jandus C, et al. (2007) Combination of transient lymphodepletion with busulfan and fludarabine and peptide vaccination in a phase I clinical trial for patients with advanced melanoma. J Immunother 30: 240-250. doi:10.1097/01.cji.0000211332.68643.98. PubMed: 17471171.
25. Laurent J, Speiser DE, Appay V, Touvrey C, Vicari M, et al. (2010) Impact of 3 different short-term chemotherapy regimens on lymphocyte-depletion and reconstitution in melanoma patients. J Immunother 33: 723-734. doi:10.1097/CJI.0b013e3181ea7e6e. PubMed: 20664354.
26. Romero P, Dunbar PR, Valmori D, Pittet M, Ogg GS, et al. (1998) Ex vivo staining of metastatic lymph nodes by class I major histocompatibility complex tetramers reveals high numbers of antigen-experienced tumor-specific cytolytic T lymphocytes. J Exp Med 188: 1641-1650. doi:10.1084/jem.188.9.1641. PubMed: 9802976.
27. Rufer N, Reichenbach P, Romero P, (2005) Methods for the ex vivo characterization of human CD8+ T subsets based on gene expression and replicative history analysis. Methods Mol Med 109: 265-284. PubMed: 15585927.
28. Gupta B, Iancu EM, Gannon PO, Wieckowski S, Baitsch L, et al. (2012) Simultaneous coexpression of memory-related and effector-related genes by individual human CD8 T cells depends on antigen specificity and differentiation. J Immunother 35: 488-501. doi:10.1097/CJI.0b013e31826183a7. PubMed: 22735807.
29. Lefranc MP, Giudicelli V, Ginestoux C, Bodmer J, Müller W, et al. (1999) IMGT, the international ImMunoGeneTics database. Nucleic Acids Res 27: 209-212. doi:10.1093/nar/27.1.209. PubMed: 9847182.
30. Roux E, Helg C, Dumont-Girard F, Chapuis B, Jeannet M, et al. (1996) Analysis of T-cell repopulation after allogeneic bone marrow transplantation: significant differences between recipients of T-cell depleted and unmanipulated grafts. Blood 87: 3984-3992. PubMed: 8611731.
31. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, et al. (2005) Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 23: 2346-2357. doi:10.1200/JCO.2005.00.240. PubMed: 15800326.
32. Wills MR, Okecha G, Weekes MP, Gandhi MK, Sissons PJ, et al. (2002) Identification of naive or antigen-experienced human CD8(+) T cells by expression of costimulation and chemokine receptors: analysis of the human cytomegalovirus-specific CD8(+) T cell response. J Immunol 168: 5455-5464. PubMed: 12023339.
33. Nystad TW, Myrmel H, (2007) Prevalence of primary versus reactivated Epstein-Barr virus infection in patients with VCA IgG-, VCA IgM- and EBNA-1-antibodies and suspected infectious mononucleosis. J Clin Virol 38: 292-297. doi:10.1016/j.jcv.2007.01.006. PubMed: 17336144.
34. Wieckowski S, Baumgaertner P, Corthesy P, Voelter V, Romero P, et al. (2009) Fine structural variations of alphabetaTCRs selected by vaccination with natural versus altered self-antigen in melanoma patients. J Immunol 183: 5397-5406. doi:10.4049/jimmunol.0901460. PubMed: 19786555.
35. Venturi V, Chin HY, Asher TE, Ladell K, Scheinberg P, et al. (2008) TCR beta-chain sharing in human CD8+ T cell responses to cytomegalovirus and EBV. J Immunol 181: 7853-7862. PubMed: 19017975.
36. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, et al. (2002) Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 99: 16168-16173. doi:10.1073/pnas.242600099. PubMed: 12427970.
37. Dudley ME, Wunderlich JR, Yang JC, Hwu P, Schwartzentruber DJ, et al. (2002) A phase I study of nonmyeloablative chemotherapy and adoptive transfer of autologous tumor antigen-specific T lymphocytes in patients with metastatic melanoma. J Immunother 25: 243-251. doi:10.1097/00002371-200205000-00007. PubMed: 12000866.
38. Wang A, Chandran S, Shah SA, Chiu Y, Paria BC, et al. (2012) The stoichiometric production of IL-2 and IFN-gamma mRNA defines memory T cells that can self-renew after adoptive transfer in humans. Sci Transl Med 4: 149ra120.
39. Mueller TF, (2003) Phenotypic changes with immunosuppression in human recipients. Front Biosci 8: d1254-d1274. doi:10.2741/1182. PubMed: 12957847.
40. Havenith SH, Remmerswaal EB, Bemelman FJ, Yong SL, van Donselaar-van der Pant KA, et al. (2012) Rapid T cell repopulation after rabbit anti-thymocyte globulin (rATG) treatment is driven mainly by cytomegalovirus. Clin Exp Immunol 169: 292-301. doi:10.1111/j.1365-2249.2012.04622.x. PubMed: 22861369.
41. Miles JJ, Bulek AM, Cole DK, Gostick E, Schauenburg AJ, et al. (2010) Genetic and structural basis for selection of a ubiquitous T cell receptor deployed in Epstein-Barr virus infection. PLOS Pathog 6: e1001198. PubMed: 21124993.
42. Price DA, Asher TE, Wilson NA, Nason MC, Brenchley JM, et al. (2009) Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. J Exp Med 206: 923-936. doi:10.1084/jem.20081127. PubMed: 19349463.
43. Iglesias MC, Almeida JR, Fastenackels S, van Bockel DJ, Hashimoto M, et al. (2011) Escape from highly effective public CD8+ T-cell clonotypes by HIV. Blood 118: 2138-2149. doi:10.1182/blood-2011-01-328781. PubMed: 21734237.
44. Berger CT, Frahm N, Price DA, Mothe B, Ghebremichael M, et al. (2011) High-functional-avidity cytotoxic T lymphocyte responses to HLA-B-restricted Gag-derived epitopes associated with relative HIV control. J Virol 85: 9334-9345. doi:10.1128/JVI.00460-11. PubMed: 21752903.
45. Vojnov L, Martins MA, Almeida JR, Ende Z, Rakasz EG, et al. (2011) GagCM9-specific CD8+ T cells expressing limited public TCR clonotypes do not suppress SIV replication in vivo. PLOS ONE 6: e23515. doi:10.1371/journal.pone.0023515. PubMed: 21887264.
46. Day EK, Carmichael AJ, ten Berge IJ, Waller EC, Sissons JG, et al. (2007) Rapid CD8+ T cell repertoire focusing and selection of high-affinity clones into memory following primary infection with a persistent human virus: human cytomegalovirus. J Immunol 179: 3203-3213. PubMed: 17709536.
47. Williams KM, Hakim FT, Gress RE, (2007) T cell immune reconstitution following lymphodepletion. Semin Immunol 19: 318-330. doi:10.1016/j.smim.2007.10.004. PubMed: 18023361.
48. van Heijst JW, Gerlach C, Swart E, Sie D, Nunes-Alves C, et al. (2009) Recruitment of antigen-specific CD8+ T cells in response to infection is markedly efficient. Science 325: 1265-1269. doi:10.1126/science.1175455. PubMed: 19729659.
49. Blackman MA, Woodland DL, (2011) The narrowing of the CD8 T cell repertoire in old age. Curr Opin Immunol 23: 537-542. doi:10.1016/j.coi.2011.05.005. PubMed: 21652194.
50. Peixoto A, Evaristo C, Munitic I, Monteiro M, Charbit A, et al. (2007) CD8 single-cell gene coexpression reveals three different effector types present at distinct phases of the immune response. J Exp Med 204: 1193-1205. doi:10.1084/jem.20062349. PubMed: 17485515.
51. Flatz L, Roychoudhuri R, Honda M, Filali-Mouhim A, Goulet JP, et al. (2011) Single-cell gene-expression profiling reveals qualitatively distinct CD8 T cells elicited by different gene-based vaccines. Proc Natl Acad Sci U S A 108: 5724-5729. doi:10.1073/pnas.1013084108. PubMed: 21422297.
52. Bachmann MF, Wolint P, Schwarz K, Jäger P, Oxenius A, (2005) Functional properties and lineage relationship of CD8+ T cell subsets identified by expression of IL-7 receptor alpha and CD62L. J Immunol 175: 4686-4696. PubMed: 16177116.
53. Huster KM, Koffler M, Stemberger C, Schiemann M, Wagner H, et al. (2006) Unidirectional development of CD8+ central memory T cells into protective Listeria-specific effector memory T cells. Eur J Immunol 36: 1453-1464. doi:10.1002/eji.200635874. PubMed: 16637009.
54. Wang X, Berger C, Wong CW, Forman SJ, Riddell SR, et al. (2011) Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. Blood 117: 1888-1898. doi:10.1182/blood-2010-10-310599. PubMed: 21123821.
55. Chapuis AG, Thompson JA, Margolin KA, Rodmyre R, Lai IP, et al. (2012) Transferred melanoma-specific CD8+ T cells persist, mediate tumor regression, and acquire central memory phenotype. Proc Natl Acad Sci U S A 109: 4592-4597. doi:10.1073/pnas.1113748109. PubMed: 22393002.
56. Fonseca SG, Procopio FA, Goulet JP, Yassine-Diab B, Ancuta P, et al. (2011) Unique features of memory T cells in HIV elite controllers: a systems biology perspective. Curr Opin HIV AIDS 6: 188-196. doi:10.1097/COH.0b013e32834589a1. PubMed: 21430529.
57. Ochsenbein AF, Riddell SR, Brown M, Corey L, Baerlocher GM, et al. (2004) CD27 expression promotes long-term survival of functional effector-memory CD8+ cytotoxic T lymphocytes in HIV-infected patients. J Exp Med 200: 1407-1417. doi:10.1084/jem.20040717. PubMed: 15583014.
58. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, et al. (2003) Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 4: 1191-1198. doi:10.1038/ni1009. PubMed: 14625547.
59. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, et al. (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114: 535-546. doi:10.1182/blood-2009-03-211714. PubMed: 19451549.
60. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, et al. (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29: 917-924. doi:10.1200/JCO.2010.32.2537. PubMed: 21282551.