Transduction of primary lymphocytes with Epstein-Barr virus (EBV) latent membrane protein-specific T-cell receptor induces lysis of virus-infected cells: A novel strategy for the treatment of Hodgkin's disease and nasopharyngeal carcinoma

Journal of Clinical Immunology

Volumn 26, Issue 1, 2006, Pages 22-32

  Jurgens, Lisa A ^a,b   Khanna, Rajiv ^c   Weber, James ^a,b   Orentas, Rimas J ^a,b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b CHILDREN S HOSPITAL OF WISCONSIN   (United States)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Adoptive; Epstein Barr virus; Gene therapy; Immunotherapy; Retroviral transduction; T cell receptor

Indexed keywords

ANTIBODY; HISTOCOMPATIBILITY ANTIGEN A 23 ANTIGEN; HLA A2 ANTIGEN; HLA A24 ANTIGEN; HLA ANTIGEN; LATENT MEMBRANE PROTEIN 2; PLASMID VECTOR; RETROVIRUS VECTOR; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ARTICLE; B LYMPHOBLAST; CELL IMMORTALIZATION; CELL LINE; CELL SPECIFICITY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; EPSTEIN BARR VIRUS; GENETIC TRANSDUCTION; HODGKIN DISEASE; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR CLONING; MOUSE; NASOPHARYNX CARCINOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TISSUE CULTURE; VIRAL GENE DELIVERY SYSTEM;

AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; ANTIGENS, CD56; CELL LINE, TUMOR; HLA-A ANTIGENS; HODGKIN DISEASE; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MOLECULAR SEQUENCE DATA; NASOPHARYNGEAL NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTES, CYTOTOXIC; TRANSDUCTION, GENETIC; VIRAL MATRIX PROTEINS;

EID: 30944469906     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-006-6532-1     Document Type: Article

References (30)

1. Ambinder RF, Orentas R, Robertson KD: Epstein-Barr virus and Hodgkin's disease. In Cambridge Medical Reviews: Heamtological Oncology. Vol. 4, Armitage J, Newland A, Keating A, Burnett A (eds). Cambridge, Cambridge University Press, 1995, pp 1-20
2. Rooney CM, Smith CA, Ng CYC, Lettin S, Li C, Krance RA, Brenner MK, Heslop HE: Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 345:9-13, 1995
3. Riddell SR, Greenberg PD: T-cell therapy of cytomegalovirus and human immunodeficiency virus infection. J Antimicrob Chemoth 45:35-43, 2000
4. Levitskaya J, Coram M, Levitsky V: Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375:685-688, 1995
5. Lee SP, Thomas WA, Blake NW, Rickinson AB: Transporter (TAP)-independent processing of a multiple membrane-spanning protein, the Epstein-Barr virus latent membrane protein 2. Eur J Immunol 26:1875-1883, 1996
6. Hsu SM, Lin J, Xie SS, Hsu PL, Rich S: Abundant expression of transforming growth factor-beta 1 and -beta 2 by Hodgkin's Reed-Sternberg cells and by reactive T lymphocytes in Hodgkin's disease. Hum Pathol 24:249-255, 1993
7. Herbst H, Foss HD, Samol J, Araujol I, Klotzbach H, Krause H, Agathanggelou A, Niedobitek G, Stein H: Frequent expression of interleukin-10 by Epstein-Barr virus-harboring tumor cells of Hodgkin's disease. Blood 87:2918-2929, 1996
8. Herbst H, Samol J, Foss HD, Raff T, Niedobitek G: Modulation of interleukin-6 expression in Hodgkin and Reed-Sternberg cells by Epstein-Barr virus. J Pathol 182:299-306, 1997
9. Clay TM, Custer MC, Sachs H, Hwu P, Rosenberg SA, Nishimura MI: Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J Immunol 163:507-513, 1999
10. Orentas RJ, Roskopf SJ, Nolan GP, Nishimura MI: Retroviral transduction of a T cell receptor specific for an Epstein-Barr virus-encoded peptide. Clin Immunol 98:220-228, 2001
11. Khanna R, Burrows SR, Moss DJ, Silins SL: Peptide transporter (TAP-1 and TAP-2)-independent endogenous processing of Epstein-Barr virus (EBV) latent membrane protein 2A: Implications for cytotoxic T-lymphocyte control of EBV-associated malignancies. J Virol 70:5357-5362, 1996
12. Yassai M, Naumova E, Gorski J: Generation of TCR spectratypes by multiplex PCR for T cell repertoire analysis. In The Antigen T Cell Receptor: Selected Protocols and Applications, Oksenberg JR (ed). Austin, TX, Landes Bioscience, 1997, pp 326-372
13. Heslop HE, Ng CYC, Li C, Smith CA, Loftin SK, Krance RA, Brenner, MA, Rooney CM: Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat Med 2:551-555, 1996
14. Papadopoulos EB, Ladanyi M, Emanuel D, Mackinnon S, Boulad F, Carabasi MH, Castro-Malaspina H, Childs BH, Gillio AP, Small TN, Childs BH, Gillio AP, Small TN, Young JW, Kernan NA, O'Reilly RJ: Infusions of donor leukocytes to treat Epstein-Barr Virus-associated lymphoproliferative disorders after allogeneic bone marrow transplantation. N Engl J Med 330:1185-1191, 1994
15. Khanna R, Bell S, Sherritt M, Gailbraith A, Burrows SR, Rafter L, Clarke B, Slaughter R, Falk MC, Douglas J, Williams T, Elliot SL, Moss DJ: Activation and adoptive transfer of Epstein-Barr virus-specific cytotoxic T cells in solid organ transplant patients with posttransplant lymphoproliferative disease. Proc Natl Acad Sci USA 96:10391-10396, 1999
16. Comoli P, Labirio M, Basso S, Baldanti F, Grossi P, Furione M, Vigano M, Fiocchi R, Rossi G, Ginevri F, Gridelli B, Moretta A, Montagna D, Locatelli F, Gerna G, Maccario R: Infusions of autologous Epstein-Barr virus (EBV)-specific cytotoxic T cells for prevention of EBV-related lymphoproliferative disorder in solid organ transplant recipients with evidence of active virus replication. Blood 99:2592-2598, 2002
17. Chua D, Huang J, Zheng B, Lau SY, Luk W, Kwong DL, Sham JS, Moss D, Yuen KY, Im SW, Ng MH: Adoptive transfer of autologous Epstein-Barr virus-specific cytotoxic T Cells for nasopharygeal carcinoma. Int J Cancer 94:73-80, 2001
18. Roskrow MA, Suzuki N, Gan YJ, Sixbey JW, Ng CY, Kimbrough S, Hudson M, Brenner MK, Heslop HE, Rooney CM: Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes for the treatment of patients with EBV-positive relapsed Hodgkin's disease. Blood 91:2925-2934, 1998
19. Straathof K, Bollard CM, Rooney C, Heslop HE: Immunotherapy for Epstein-Barr virus-associated cancers in children. Oncologist 8:83-98, 2003
20. Rickinson AB, Murray RJ, Brooks JM, Moss DJ, Masucci M: T cell recognition of Epstein-Barr virus associated lymphomas. Cancer Surv 13:53-79, 1992
21. Lee SP, Chan ATC, Cheung ST, Thomas WA, Groom-Carter D, Dawson CW, Tsai CH, Leung SF, Johnson PJ, Huang DP: CTL Control of EBV in nasopharyngeal carcinoma (NPC): EBV-specific CTL responses in the blood and tumors of NPC patients and the antigen-processing function of the tumor cells. J Immunol 165:573-582, 2000
22. Brooks L, Yao QY, Rickinson AB, Young LS: Epstein-Barr virus latent gene transcription in nasopharyngeal carcinoma cells: coexpression of EBNA1, LMP1, and LMP2 transcripts. J Virol 66:2689-2697, 1992
23. Redchenko IV, Rickinson, AB: Accessing Epstein-Barr virus-specific T-cell memory with peptide-loaded dendritic cells. J Virol 73:334-342, 1999
24. Gakamsky DM, Luescher IF, Pecht I: T cell receptor-ligand interactions: A conformational preequilibrium or an induced fit. Proc Natl Acad Sci USA 101:9063-9066, 2004
25. Rubio-Godoy V, Dutoit V, Rimoldi D, Lienard D, Lejeune F, Speiser D, Guillame P, Serottini JC, Romero P, Valmori D: Discrepancy between ELISPOT IFN-γ secretion and binding of A2/peptide multimers to TCR reveals interclonal dissociation of CTL effector function from TCR-peptide/MHC complexes half-life. Proc Natl Acad Sci USA 98:10302-10307, 2001
26. Orentas RJ, Bircher LA, Roskopf S: Retroviral transfer of T-cell receptor genes produces cells with a broad range of lytic activity. Scand J Immunol 58:33-42, 2003
27. Ranieri E, Herr W, Gambotta A, Olson W, Rowe D, Robbins PD, Kierstead LS, Watkins SC, Gesualdo L, Storkus, WJ: Dendritic cells transduced with an adenovirus vector encoding Epstein-Barr virus latent membrane protein 2B: A new modality for vaccination. J Virol 73:10416-10425, 1999.
28. Gahn B, Siller-Lopez F, Pirooz AD, Yvon E, Gottschalk S, Longnecker R, Brenner MK, Heslop HE, Aguilar-Cordova E, Rooney CM: Adenoviral gene transfer into dendritic cells efficiently amplifies the immune response to LMP2A antigen: A potential treatment strategy for Epstein-Barr virus-positive Hodgkin's lymphoma. Int J Cancer 93:706-713, 2001
29. Stanislawski T, Voss RH, Lotz C, Sadovnikova E, Willemsen RA, Kuball J, Ruppert T, Bolhuis RL, Melief CJ, Huber S, Stauss HJ, Theobold M: Circumventing tolerance to a human MDM2-derived tumor antigen by TCR gene transfer. Nat Immunol 2:962-970, 2001
30. Rubinstein MP, Kadina AM, Salem ML, Nguyen CL, Gillanders WE, Nishimura ML, Cole DJ: Transfer of TCR genes into mature T cells is accompanied by the maintenance of parental T cell avidity. J Immunol 170:1209-1217, 2003