Adoptive Transfer of EBV Specific CD8+ T Cell Clones Can Transiently Control EBV Infection in Humanized Mice

PLoS Pathogens

Volumn 10, Issue 8, 2014, Pages

  Antsiferova, Olga ^a   Müller, Anne ^a   Rämer, Patrick C ^a   Chijioke, Obinna ^a   Chatterjee, Bithi ^a   Raykova, Ana ^a   Planas, Raquel ^b   Sospedra, Mireia ^b   Shumilov, Anatoliy ^c   Tsai, Ming Han ^c   Delecluse, Henri Jacques ^c   Münz, Christian ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; EPSTEIN BARR VIRUS ANTIGEN; GAG PROTEIN; GAMMA INTERFERON; HLA A ANTIGEN; HLA B ANTIGEN; HLA DQB1 ANTIGEN; IMMEDIATE EARLY PROTEIN BZLF1; LATENT MEMBRANE PROTEIN 2;

ADOPTIVE IMMUNOTHERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CANCER INCIDENCE; CD3+ T LYMPHOCYTE; CD34 SELECTION; CD4 CD8 RATIO; CD8+ T LYMPHOCYTE; CELL CLONING; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DEGRANULATION ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPSTEIN BARR VIRUS INFECTION; FLOW CYTOMETRY; GENE REARRANGEMENT; GENOTYPE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INFECTION CONTROL; LYMPHOBLASTOID CELL LINE; LYMPHOCYTE TRANSFORMATION; MOUSE; NEWBORN; NONHUMAN; PATHOGEN CLEARANCE; REAL TIME POLYMERASE CHAIN REACTION; VIREMIA; VIRUS LOAD; VIRUS REPLICATION; ADOPTIVE TRANSFER; ANIMAL; B LYMPHOCYTE; IMMUNOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VIROLOGY; VIRUS CELL TRANSFORMATION;

ADOPTIVE TRANSFER; ANIMALS; B-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL TRANSFORMATION, VIRAL; EPSTEIN-BARR VIRUS INFECTIONS; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; REAL-TIME POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84926176003     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004333     Document Type: Article

References (50)

1. Young LS, Rickinson AB, (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4: 757–768.
2. Kutok JL, Wang F, (2006) Spectrum of Epstein-Barr virus-associated diseases. Annu Rev Pathol 1: 375–404.
3. Miller G, El-Guindy A, Countryman J, Ye J, Gradoville L, (2007) Lytic cycle switches of oncogenic human gammaherpesviruses. Adv Cancer Res 97: 81–109.
4. 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.
5. Münz C, Bickham KL, Subklewe M, Tsang ML, Chahroudi A, et al. (2000) Human CD4+ T lymphocytes consistently respond to the latent Epstein-Barr virus nuclear antigen EBNA1. J Exp Med 191: 1649–1660.
6. Murray RJ, Kurilla MG, Brooks JM, Thomas WA, Rowe M, et al. (1992) Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV-positive malignancies. J Exp Med 176: 157–168.
7. Adhikary D, Behrends U, Moosmann A, Witter K, Bornkamm GW, et al. (2006) Control of Epstein-Barr virus infection in vitro by T helper cells specific for virion glycoproteins. J Exp Med 203: 995–1006.
8. Steven NM, Annels NE, Kumar A, Leese AM, Kurilla MG, et al. (1997) Immediate early and early lytic cycle proteins are frequent targets of the Epstein-Barr virus-induced cytotoxic T cell response. J Exp Med 185: 1605–1617.
9. Cho YG, Gordadze AV, Ling PD, Wang F, (1999) Evolution of two types of rhesus lymphocryptovirus similar to type 1 and type 2 Epstein-Barr virus. J Virol 73: 9206–9212.
10. Leung C, Chijioke O, Gujer C, Chatterjee B, Antsiferova O, et al. (2013) Infectious diseases in humanized mice. Eur J Immunol 43: 2246–2254.
11. Ohashi M, Fogg MH, Orlova N, Quink C, Wang F, (2012) An Epstein-Barr virus encoded inhibitor of Colony Stimulating Factor-1 signaling is an important determinant for acute and persistent EBV infection. PLoS Pathog 8: e1003095.
12. Marr-Belvin AK, Carville AK, Fahey MA, Boisvert K, Klumpp SA, et al. (2008) Rhesus lymphocryptovirus type 1-associated B-cell nasal lymphoma in SIV-infected rhesus macaques. Vet Pathol 45: 914–921.
13. Strowig T, Gurer C, Ploss A, Liu YF, Arrey F, et al. (2009) Priming of protective T cell responses against virus-induced tumors in mice with human immune system components. J Exp Med 206: 1423–1434.
14. Chijioke O, Müller A, Feederle R, Barros MH, Krieg C, et al. (2013) Natural killer cells prevent infectious mononucleosis features by targeting lytic Epstein-Barr virus infection. Cell Rep 5: 1489–1498.
15. Strowig T, Chijioke O, Carrega P, Arrey F, Meixlsperger S, et al. (2010) Human NK cells of mice with reconstituted human immune system components require preactivation to acquire functional competence. Blood 116: 4158–4167.
16. Gurer C, Strowig T, Brilot F, Pack M, Trumpfheller C, et al. (2008) Targeting the nuclear antigen 1 of Epstein Barr virus to the human endocytic receptor DEC-205 stimulates protective T-cell responses. Blood 112: 1231–1239.
17. Meixlsperger S, Leung CS, Ramer PC, Pack M, Vanoaica LD, et al. (2013) CD141+ dendritic cells produce prominent amounts of IFN-alpha after dsRNA recognition and can be targeted via DEC-205 in humanized mice. Blood 121: 5034–5044.
18. White RE, Ramer PC, Naresh KN, Meixlsperger S, Pinaud L, et al. (2012) EBNA3B-deficient EBV promotes B cell lymphomagenesis in humanized mice and is found in human tumors. J Clin Invest 122: 1487–1502.
19. Tsai MH, Raykova A, Klinke O, Bernhardt K, Gartner K, et al. (2013) Spontaneous Lytic Replication and Epitheliotropism Define an Epstein-Barr Virus Strain Found in Carcinomas. Cell Rep 5: 458–70.
20. Berger C, Day P, Meier G, Zingg W, Bossart W, et al. (2001) Dynamics of Epstein-Barr virus DNA levels in serum during EBV-associated disease. J Med Virol 64: 505–512.
21. Fonteneau JF, Larsson M, Somersan S, Sanders C, Münz C, et al. (2001) Generation of high quantities of viral and tumor-specific human CD4+ and CD8+ T-cell clones using peptide pulsed mature dendritic cells. J Immunol Methods 258: 111–126.
22. Yousef S, Planas R, Chakroun K, Hoffmeister-Ullerich S, Binder TM, et al. (2012) TCR bias and HLA cross-restriction are strategies of human brain-infiltrating JC virus-specific CD4+ T cells during viral infection. J Immunol 189: 3618–3630.
23. Ressing ME, Keating SE, van Leeuwen D, Koppers-Lalic D, Pappworth IY, et al. (2005) Impaired transporter associated with antigen processing-dependent peptide transport during productive EBV infection. J Immunol 174: 6829–6838.
24. Feederle R, Kost M, Baumann M, Janz A, Drouet E, et al. (2000) The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. Embo J 19: 3080–3089.
25. Katsumura KR, Maruo S, Wu Y, Kanda T, Takada K, (2009) Quantitative evaluation of the role of Epstein-Barr virus immediate-early protein BZLF1 in B-cell transformation. J Gen Virol 90: 2331–2341.
26. Hong GK, Gulley ML, Feng WH, Delecluse HJ, Holley-Guthrie E, et al. (2005) Epstein-Barr virus lytic infection contributes to lymphoproliferative disease in a SCID mouse model. J Virol 79: 13993–14003.
27. Shultz LD, Saito Y, Najima Y, Tanaka S, Ochi T, et al. (2010) Generation of functional human T-cell subsets with HLA-restricted immune responses in HLA class I expressing NOD/SCID/IL2r gammanull humanized mice. Proc Natl Acad Sci U S A 107: 13022–13027.
28. Ma SD, Hegde S, Young KH, Sullivan R, Rajesh D, et al. (2011) A new model of Epstein-Barr virus infection reveals an important role for early lytic viral protein expression in the development of lymphomas. J Virol 85: 165–177.
29. Melenhorst JJ, Leen AM, Bollard CM, Quigley MF, Price DA, et al. (2010) Allogeneic virus-specific T cells with HLA alloreactivity do not produce GVHD in human subjects. Blood 116: 4700–4702.
30. Leen AM, Bollard CM, Mendizabal AM, Shpall EJ, Szabolcs P, et al. (2013) Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation. Blood 121: 5113–5123.
31. Luzuriaga K, Sullivan JL, (2010) Infectious mononucleosis. N Engl J Med 362: 1993–2000.
32. Callan MF, Tan L, Annels N, Ogg GS, Wilson JD, et al. (1998) Direct visualization of antigen-specific CD8+ T cells during the primary immune response to Epstein-Barr virus In vivo. J Exp Med 187: 1395–1402.
33. Abbott RJ, Quinn LL, Leese AM, Scholes HM, Pachnio A, et al. (2013) CD8+ T cell responses to lytic EBV infection: late antigen specificities as subdominant components of the total response. J Immunol 191: 5398–5409.
34. Pudney VA, Leese AM, Rickinson AB, Hislop AD, (2005) CD8+ immunodominance among Epstein-Barr virus lytic cycle antigens directly reflects the efficiency of antigen presentation in lytically infected cells. J Exp Med 201: 349–360.
35. Rooney CM, Smith CA, Ng CY, Loftin S, Li C, et al. (1995) Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 345: 9–13.
36. Adhikary D, Behrends U, Boerschmann H, Pfunder A, Burdach S, et al. (2007) Immunodominance of lytic cycle antigens in Epstein-Barr virus-specific CD4+ T cell preparations for therapy. PLoS ONE 2: e583.
37. Haque T, Wilkie GM, Taylor C, Amlot PL, Murad P, et al. (2002) Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 360: 436–442.
38. Haque T, Wilkie GM, Jones MM, Higgins CD, Urquhart G, et al. (2007) Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 110: 1123–1131.
39. Doubrovina E, Oflaz-Sozmen B, Prockop SE, Kernan NA, Abramson S, et al. (2012) Adoptive immunotherapy with unselected or EBV-specific T cells for biopsy-proven EBV+ lymphomas after allogeneic hematopoietic cell transplantation. Blood 119: 2644–2656.
40. Bolton DL, Minang JT, Trivett MT, Song K, Tuscher JJ, et al. (2010) Trafficking, persistence, and activation state of adoptively transferred allogeneic and autologous Simian Immunodeficiency Virus-specific CD8+ T cell clones during acute and chronic infection of rhesus macaques. J Immunol 184: 303–314.
41. Sokal EM, Hoppenbrouwers K, Vandermeulen C, Moutschen M, Leonard P, et al. (2007) Recombinant gp350 vaccine for infectious mononucleosis: a phase 2, randomized, double-blind, placebo-controlled trial to evaluate the safety, immunogenicity, and efficacy of an Epstein-Barr virus vaccine in healthy young adults. J Infect Dis 196: 1749–1753.
42. Cui X, Cao Z, Sen G, Chattopadhyay G, Fuller DH, et al. (2013) A novel tetrameric gp350 1–470 as a potential Epstein-Barr virus vaccine. Vaccine 31: 3039–3045.
43. Ogembo JG, Kannan L, Ghiran I, Nicholson-Weller A, Finberg RW, et al. (2013) Human complement receptor type 1/CD35 is an Epstein-Barr Virus receptor. Cell Rep 3: 371–385.
44. Hui EP, Taylor GS, Jia H, Ma BB, Chan SL, et al. (2013) Phase I trial of recombinant modified vaccinia ankara encoding Epstein-Barr viral tumor antigens in nasopharyngeal carcinoma patients. Cancer Res 73: 1676–1688.
45. Taylor GS, Haigh TA, Gudgeon NH, Phelps RJ, Lee SP, et al. (2004) Dual stimulation of Epstein-Barr Virus (EBV)-specific CD4+- and CD8+-T-cell responses by a chimeric antigen construct: potential therapeutic vaccine for EBV-positive nasopharyngeal carcinoma. J Virol 78: 768–778.
46. Ruiss R, Jochum S, Wanner G, Reisbach G, Hammerschmidt W, et al. (2011) A virus-like particle-based Epstein-Barr virus vaccine. J Virol 85: 13105–13113.
47. Feederle R, Shannon-Lowe C, Baldwin G, Delecluse HJ, (2005) Defective infectious particles and rare packaged genomes produced by cells carrying terminal-repeat-negative Epstein-Barr virus. J Virol 79: 7641–7647.
48. Adhikary D, Behrends U, Feederle R, Delecluse HJ, Mautner J, (2008) Standardized and highly efficient expansion of Epstein-Barr virus-specific CD4+ T cells by using virus-like particles. J Virol 82: 3903–3911.
49. Pavlova S, Feederle R, Gartner K, Fuchs W, Granzow H, et al. (2013) An Epstein-Barr virus mutant produces immunogenic defective particles devoid of viral DNA. J Virol 87: 2011–2022.
50. Leung CS, Maurer MA, Meixlsperger S, Lippmann A, Cheong C, et al. (2013) Robust T cell stimulation by Epstein-Barr virus-transformed B cells after antigen targeting to DEC-205. Blood 121: 1584–94.