Interferon-gamma expressing EBV LMP2A-specific T cells for cellular immunotherapy

Cellular Immunology

Volumn 246, Issue 2, 2007, Pages 81-91

  Sun, Qi ^a   Brewer, Nargisa ^a   Dunham, Kimberly ^a   Chen, Lipai ^a   Bao, Lei ^a   Burton, Robert ^a   Lucas, Kenneth G ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

EBV; Hodgkin's lymphoma; Iimmunotherapy; Interferon gamma; T cells; Tumor antigens

Indexed keywords

CD27 ANTIGEN; CD28 ANTIGEN; CD45RA ANTIGEN; CD45RO ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; LATENT MEMBRANE PROTEIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN;

ADOPTIVE IMMUNOTHERAPY; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; EPSTEIN BARR VIRUS; EXOCYTOSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; T LYMPHOCYTE; TARGET CELL; TH1 CELL; TH2 CELL;

ANTIGENS, CD27; ANTIGENS, CD28; ANTIGENS, CD45; CELL LINE, TUMOR; EPITOPES; EPSTEIN-BARR VIRUS INFECTIONS; EXOCYTOSIS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; INTERLEUKINS; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC; TUMOR VIRUS INFECTIONS; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 34548145158     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2007.06.004     Document Type: Article

References (57)

1. Flavell K.J., and Murray P.G. Hodgkin's disease and the Epstein-Barr virus. Mol. Pathol. 53 (2000) 262-269
2. Grasser F.A., Murray P.G., Kremmer E., Klein K., Remberger K., Feiden W., Reynolds G., Niedobitek G., Young L.S., and Mueller-Lantzsch N. Monoclonal antibodies directed against the Epstein-Barr virus-encoded nuclear antigen 1 (EBNA1): immunohistologic detection of EBNA1 in the malignant cells of Hodgkin's disease. Blood 84 (1994) 3792-3798
3. Herbst H., Dallenbach F., Hummel M., Niedobitek G., Pileri S., Muller- Lantzsch N., and Stein H. Epstein-Barr virus latent membrane protein expression in Hodgkin and Reed-Sternberg cells. Proc. Natl. Acad. Sci. USA 88 (1991) 4766-4770
4. Pallesen G., Hamilton-Dutoit S.J., Rowe M., and Young L.S. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet 337 (1991) 320-322
5. Lee S.P., Constandinou C.M., Thomas W.A., Croom-Carter D., Blake N.W., Murray P.G., Crocker J., and Rickinson A.B. Antigen presenting phenotype of Hodgkin Reed-Sternberg cells: analysis of the HLA class I processing pathway and the effects of interleukin-10 on Epstein-Barr virus-specific cytotoxic T-cell recognition. Blood 92 (1998) 1020-1030
6. Murray P.G., Constandinou C.M., Crocker J., Young L.S., and Ambinder R.F. Analysis of major histocompatibility complex class I, TAP expression, and LMP2 epitope sequence in Epstein-Barr virus-positive Hodgkin's disease. Blood 92 (1998) 2477
7. Tzardi M., Kouvidou C., Papakonstantinou E., Datseris G., Darivianaki K., Karidi E., Eliopoulos G., Delidis G., Rontogianni D., and Kanavaros P. Major histocompatibility complex (MHC)-I and MHC-II expression in Hodgkin's disease in relation to the presence of Epstein-Barr virus (EBV). Anticancer Res. 16 (1996) 827-831
8. Sing A.P., Ambinder R.F., Hong D.J., Jensen M., Batten W., Petersdorf E., and Greenberg P.D. Isolation of Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes that lyse Reed-Sternberg cells: implications for immune-mediated therapy of EBV+ Hodgkin's disease. Blood 89 (1997) 1978-1986
9. Murray R.J., Kurilla M.G., Brooks J.M., Thomas W.A., Rowe M., Kieff E., and Rickinson A.B. 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 (1992) 157-168
10. Lee S.P., Tierney R.J., Thomas W.A., Brooks J.M., and Rickinson A.B. Conserved CTL epitopes within EBV latent membrane protein 2: a potential target for CTL-based tumor therapy. J. Immunol. 158 (1997) 3325-3334
11. Doherty P.C., and Christensen J.P. Accessing complexity: the dynamics of virus-specific T cell responses. Annu. Rev. Immunol. 18 (2000) 561-592
12. Keever C.A., Small T.N., Flomenberg N., Heller G., Pekle K., Black P., Pecora A., Gillio A., Kernan N.A., and O'Reilly R.J. Immune reconstitution following bone marrow transplantation: comparison of recipients of T-cell depleted marrow with recipients of conventional marrow grafts. Blood 73 (1989) 1340-1350
13. Riddell S.R., Watanabe K.S., Goodrich J.M., Li C.R., Agha M.E., and Greenberg P.D. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257 (1992) 238-241
14. Rooney C.M., Smith C.A., Ng C.Y., Loftin S., Li C., Krance R.A., Brenner M.K., and Heslop H.E. Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 345 (1995) 9-13
15. Emanuel D.J., Lucas K.G., Mallory Jr. G.B., Edwards-Brown M.K., Pollok K.E., Conrad P.D., Robertson K.A., and Smith F.O. Treatment of posttransplant lymphoproliferative disease in the central nervous system of a lung transplant recipient using allogeneic leukocytes. Transplant 63 (1997) 1691-1694
16. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., Topalian S.L., Sherry R., Restifo N.P., Hubicki A.M., Robinson M.R., Raffeld M., Duray P., Seipp C.A., Rogers-Freezer L., Morton K.E., Mavroukakis S.A., White D.E., and Rosenberg S.A. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298 (2002) 850-854
17. Roskrow M.A., Suzuki N., Gan Y., Sixbey J.W., Ng C.Y., Kimbrough S., Hudson M., Brenner M.K., Heslop H.E., and Rooney C.M. Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes for the treatment of patients with EBV-positive relapsed Hodgkin's disease. Blood 91 (1998) 2925-2934
18. Sun Q., Burton R.L., Reddy V., and Lucas K.G. Safety of allogeneic Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes for patients with refractory EBV-related lymphoma. Br. J. Haematol. 118 (2002) 799-808
19. Lucas K.G., Salzman D., Garcia A., and Sun Q. Adoptive Immunotherapy with allogeneic Epstein-Barr virus (EBV)-specific cytotoxic T-lymphocytes for recurrent, EBV-positive Hodgkin disease. Cancer 100 (2004) 1892-1901
20. Bollard C.M., Aguilar L., Straathof K.C., Gahn B., Huls M.H., Rousseau A., Sixbey J., Gresik M.V., Carrum G., Hudson M., Dilloo D., Gee A., Brenner M.K., Rooney C.M., and Heslop H.E. Cytotoxic T lymphocyte therapy for Epstein-Barr Virus+ Hodgkin's disease. J. Exp. Med. 200 (2004) 1623-1633
21. Powell Jr. D.J., Dudley M.E., Hogan K.A., Wunderlich J.R., and Rosenberg S.A. Adoptive transfer of vaccine-induced peripheral blood mononuclear cells to patients with metastatic melanoma following lymphodepletion. J. Immunol. 177 (2006) 6527-6539
22. Sun Q., Pollok K.E., Burton R.L., Dai L.J., Britt W., Emanuel D.J., and Lucas K.G. Simultaneous ex vivo expansion of cytomegalovirus and Epstein-Barr virus-specific cytotoxic T lymphocytes using B-lymphoblastoid cell lines expressing cytomegalovirus pp65. Blood 94 (1999) 3242-3250
23. Sun Q., Burton R.L., and Lucas K.G. Cytokine production and cytolytic mechanism of CD4+ cytotoxic T lymphocytes in ex vivo expanded therapeutic Epstein-Barr virus-specific T-cell cultures. Blood 99 (2002) 3302-3309
24. Gahn B., Siller-Lopez F., Pirooz A.D., Yvon E., Gottschalk S., Longnecker R., Brenner M.K., Heslop H.E., Aguilar-Cordova E., and Rooney C.M. 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 (2001) 706-713
25. Lautscham G., Haigh T., Mayrhofer S., Taylor G., Croom-Carter D., Leese A., Gadola S., Cerundolo V., Rickinson A., and Blake N. Identification of a TAP-independent, immunoproteasome-dependent CD8+ T-Cell epitope in Epstein-Barr virus latent membrane protein 2. J. Virol. 77 (2003) 2757-2761
26. Lee S.P., Thomas W.A., Murray R.J., Khanim F., Kaur S., Young L.S., Rowe M., Kurilla M., and Rickinson A.B. HLA A2.1-restricted cytotoxic T cells recognizing a range of Epstein-Barr virus isolates through a defined epitope in latent membrane protein LMP2. J. Virol. 67 (1993) 7428-7435
27. Sun Q., Burton R.L., Pollok K.E., Emanuel D.J., and Lucas K.G. CD4(+) Epstein-Barr virus-specific cytotoxic T-lymphocytes from human umbilical cord blood. Cell. Immunol. 195 (1999) 81-88
28. Manz R., Assenmacher M., Pfluger E., Miltenyi S., and Radbruch A. Analysis and sorting of live cells according to secreted molecules, relocated to a cell-surface affinity matrix. Proc. Natl. Acad. Sci. USA 92 (1995) 1921
29. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., and Koup R.A. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281 (2003) 65-78
30. Gervois N., Guilloux Y., Diez E., and Jotereau F. Suboptimal activation of melanoma infiltrating lymphocytes (TIL) due to low avidity of TCR/MHC-tumor peptide interactions. J. Exp. Med. 183 (1996) 2403-2407
31. Valitutti S., Muller S., Dessing M., and Lanzavecchia A. Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J. Exp. Med. 183 (1996) 1917-1921
32. Tosato G. The Epstein-Barr virus and the immune system. Adv. Cancer Res. 49 (1987) 75-125
33. Khanna R., Burrows S.R., Kurilla M.G., Jacob C.A., Misko I.S., Sculley T.B., Kieff E., and Moss D.J. Localization of Epstein-Barr virus cytotoxic T cell epitopes using recombinant vaccinia: implications for vaccine development. J. Exp. Med. 176 (1992) 169-176
34. Lautscham G., Mayrhofer S., Taylor G., Haigh T., Leese A., Rickinson A., and Blake N. Processing of a multiple membrane spanning Epstein-Barr virus protein for CD8+ T cell recognition reveals a proteasome-dependent, transporter associated with antigen processing-independent pathway. J. Exp. Med. 194 (2001) 1053-1068
35. Munz C., Bickham K.L., Subklewe M., Tsang M.L., Chahroudi A., Kurilla M.G., Zhang D.O.M., and Steinman R.M. Human CD4+ T lymphocytes consistently respond to the latent Epstein-Barr virus nuclear antigen EBNA1. J. Exp. Med. 191 (2000) 1649-1660
36. Bickham K., Munz C., Tsang M.L., Larsson M., Fonteneau J.F., Bhardwaj N., and Steinman R. EBNA1-specific CD4+ T cells in healthy carriers of Epstein-Barr virus are primarily Th1 in function. J. Clin. Invest. 107 (2001) 121-130
37. Paludan C., Bickham K., Nikiforow S., Tsang M.L., Goodman K., Hanekom W.A., Fonteneau J.F., Stevanovic S., and Munz C. Epstein-Barr nuclear antigen 1-specific CD4+ Th1 cells kill Burkitt's lymphoma cells. J. Immunol. 169 (2002) 1593-1603
38. Levitskaya J., Coram M., Levitsky V., Imreh S., Steigerwald-Mullen P.M., Klein G., Kurilla M.G., and Masucci M.G. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375 (1995) 685-688
39. Leen A., Meij P., Redchenko I., Middeldorp J., Bloemena E., Rickinson A., and Blake N. Differential immunogenicity of Epstein-Barr virus latent-cycle proteins for human CD4+ T-helper 1 responses. J. Virol. 75 (2001) 8649-8659
40. Meij P., Leen A., Rickinson A.B., Verkoeijen S., Vervoort M.B., Bloemena E., and Middeldorp J.M. Identification and prevalence of CD8(+) T-cell responses directed against Epstein-Barr virus-encoded latent membrane protein 1 and latent membrane protein 2. Int. J. Cancer 99 (2002) 93-99
41. Ranieri E., Herr W., Gambotto A., Olson W., Rowe D., Robbins P.D., Kierstead L.S., Watkins S.C., Gesualdo L., and Storkus W.J. Dendritic cells transduced with an adenovirus vector encoding Epstein-Barr virus latent membrane protein 2B: a new modality for vaccination. J. Virol. 73 (1999) 10416-10425
42. Su Z., Peluso M.V., Raffegerst S.H., Schendel D.J., and Roskrow M.A. The generation of LMP2a-specific cytotoxic T lymphocytes for the treatment of patients with Epstein-Barr virus-positive Hodgkin disease. Eur. J. Immunol. 31 (2001) 947-958
43. Leen A., Ratnayake M., Foster A., Heym K., Ahmed N., Rooney C.M., and Gottschalk S. Contact-activated monocytes: efficient antigen presenting cells for the stimulation of antigen-specific T cells. J. Immunother. 30 (2007) 96-107
44. Koehne G., Smith K.M., Ferguson T.L., Williams R.Y., Heller G., Pamer E.G., Dupont B., and O'Reilly R.J. Quantitation, selection, and functional characterization of Epstein-Barr virus-specific and alloreactive T cells detected by intracellular interferon-gamma production and growth of cytotoxic precursors. Blood 99 (2002) 1730-1740
45. Feuchtinger T., Lang P., Hamprecht K., Schumm M., Greil J., Jahn G., Niethammer D., and Einsele H. Isolation and expansion of human adenovirus-specific CD4+ and CD8+ T cells according to IFN-gamma secretion for adjuvant immunotherapy. Exp. Hematol. 32 (2004) 282-289
46. Rauser G., Einsele H., Sinzger C., Wernet D., Kuntz G., Assenmacher M., Campbell J.D.M., and Topp M.S. Rapid generation of combined CMV-specific CD4+ and CD8+ T-cell lines for adoptive transfer into recipients of allogeneic stem cell transplants. Blood 103 (2004) 3565-3572
47. Oelke M., Kurokawa T., Hentrich I., Behringer D., Cerundolo V., Lindemann A., and Mackensen A. Functional characterization of CD8+ antigen-specific cytotoxic T lymphocytes after enrichment based on cytokine secretion: comparison with the MHC-tetramer technology. Scand. J. Immunol. 52 (2000) 544-549
48. Becker C., Pohla H., Frankenberger B., Schuler T., Assenmacher M., Schendel D.J., and Blankenstein T. Adoptive tumor therapy with T lymphocytes enriched through an IFN-[gamma] capture assay. Nat. Med. 7 (2001) 1159-1162
49. Herbst H., Foss H.D., Samol J., Araujo I., Klotzbach H., Krause H., Agathanggelou A., Niedobitek G., and Stein H. Frequent expression of interleukin-10 by Epstein-Barr virus-harboring tumor cells of Hodgkin's disease. Blood 87 (1996) 2918
50. Champagne P., Ogg G.S., King A.S., Knabenhans C., Ellefsen K., Nobile M., Appay V., Rizzardi G.P., Fleury S., Lipp M., Forster R., Rowland-Jones S., Sekaly R.P., McMichael A.J., and Pantaleo G. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410 (2001) 106-111
51. Geginat J., Lanzavecchia A., and Sallusto F. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101 (2003) 4260-4266
52. Hendriks J., Gravestein L.A., Tesselaar K., van Lier R.A.W., Schumacher T.N.M., and Borst J. CD27 is required for generation and long-term maintenance of T cell immunity. Nat. Immunol. 1 (2000) 433-440
53. Powell Jr. D.J., Dudley M.E., Robbins P.F., and Rosenberg S.A. Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105 (2005) 241-250
54. Riddell S.R., and Greenberg P.D. The use of anti-CD3 and anti-CD28 monoclonal antibodies to clone and expand human antigen-specific T cells. J. Immunol. Methods 128 (1990) 189-201
55. Yee C., Thompson J.A., Byrd D., Riddell S.R., Roche P., Celis E., and Greenberg P.D. 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. USA 99 (2002) 16168-16173
56. Gottschalk S., Edwards O.L., Sili U., Huls M.H., Goltsova T., Davis A.R., Heslop H.E., and Rooney C.M. Generating CTLs against the subdominant Epstein-Barr virus LMP1 antigen for the adoptive immunotherapy of EBV-associated malignancies. Blood 101 (2003) 1905-1912
57. Leen A., Ratnayake M., Foster A., Heym K., Ahmed N., Rooney C.M., and Gottschalk S. Contact-activated monocytes: efficient antigen presenting cells for the stimulation of antigen-specific T cells. J. Immunother. 30 (2007) 96-107