Generating CTLs against the subdominant EBV LMP antigens by transient expression of an A20 inhibitor with EBV LMP proteins in human DCs

Gene Therapy

Volumn 19, Issue 8, 2012, Pages 818-827

  Hong, B ^a   Peng, G ^b   Berry, L ^a   Gottschalk, S ^c   Jung, J U ^a   Chen, S Y ^a   Huang, X F ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CENTER FOR CELL AND GENE THERAPY   (United States)

Author keywords

A20; cytotoxic T lymphocyte; dendritic cells; epstein barr virus; latent membrane proteins

Indexed keywords

A20 PROTEIN; LATENT MEMBRANE PROTEIN 1; LATENT MEMBRANE PROTEIN 2; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL SPECIFICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EPSTEIN BARR VIRUS; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSIENT EXPRESSION; TUMOR XENOGRAFT;

ANIMALS; DENDRITIC CELLS; DNA-BINDING PROTEINS; IMMUNOTHERAPY, ADOPTIVE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOCYTE ACTIVATION; LYMPHOMA, NON-HODGKIN; MICE; MICE, SCID; NUCLEAR PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TRANSFECTION; VIRAL MATRIX PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

HUMAN HERPESVIRUS 4; MUS;

EID: 84864878507     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2011.160     Document Type: Article

References (50)

1. Diebold SS. Activation of dendritic cells by toll-like receptors and C-type lectins. Handb Exp Pharmacol 2009; 188: 3-30.
2. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4: 499-511.
3. Beutler B, Rietschel ET. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 2003; 3: 169-176.
4. Janeway Jr CA, Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20: 197-216.
5. Shen L, Evel-Kabler K, Strube R, Chen SY. Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific anti-tumor immunity. Nat Biotechnol 2004; 22: 1546-1553.
6. Song XT, Evel-Kabler K, Shen L, Rollins L, Huang XF, Chen SY. A20 is an antigen presentation attenuator, and its inhibition overcomes regulatory T cell-mediated suppression. Nat Med 2008; 14: 258-265.
7. Boone DL, Turer EE, Lee EG, Ahmad RC, Wheeler MT, Tsui C et al. The ubiquitinmodifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004; 5: 1052-1060.
8. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP et al. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000; 289: 2350-2354.
9. Sarma V, Lin Z, Clark L, Rust BM, Tewari M, Noelle RJ et al. Activation of the B-cell surface receptor CD40 induces A20, a novel zinc finger protein that inhibits apoptosis. J Biol Chem 1995; 270: 12343-12346.
10. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S et al. Deubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004; 430: 694-699.
11. Saitoh T, Yamamoto M, Miyagishi M, Taira K, Nakanishi M, Fujita T et al. A20 is a negative regulator of IFN regulatory factor 3 signaling. J Immunol 2005; 174: 1507-1512.
12. Poppema S, Potters M, Visser L, van den Berg AM. Immune escape mechanisms in Hodgkin's disease. Ann Oncol 1998; 9 (Suppl 5): S21-4.
13. Heslop HE, Ng CY, Li C, Smith CA, Loftin SK, Krance RA et al. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat Med 1996; 2: 551-555.
14. Rooney CM, Smith CA, Ng CY, Loftin SK, Sixbey JW, Gan Y et al. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 1998; 92: 1549-1555.
15. Bollard CM, Gottschalk S, Huls MH, Molldrem J, Przepiorka D, Rooney CM et al. In vivo expansion of LMP 1-and 2-specific T-cells in a patient who received donor-derived EBV-specific T-cells after allogeneic stem cell transplantation. Leuk Lymphoma 2006; 47: 837-842.
16. Straathof KC, Leen AM, Buza EL, Taylor G, Huls MH, Heslop HE et al. Characterization of latent membrane protein 2 specificity in CTL lines from patients with EBV-positive nasopharyngeal carcinoma and lymphoma. J Immunol 2005; 175: 4137-4147.
17. Busson P, Edwards RH, Tursz T, Raab-Traub N. Sequence polymorphism in the Epstein-Barr virus latent membrane protein (LMP)-2 gene. J Gen Virol 1995; 76. (Pt 1): 139-145.
18. Lee SP, Thomas WA, Murray RJ, Khanim F, Kaur S, Young LS et al. 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 1993; 67: 7428-7435.
19. Murray PG, Constandinou CM, Crocker J, Young LS, Ambinder RF. Analysis of major histocompatibility complex class I, TAP expression, and LMP2 epitope sequence in Epstein-Barr virus-positive Hodgkin's disease. Blood 1998; 92: 2477-2483.
20. Duraiswamy J, Bharadwaj M, Tellam J, Connolly G, Cooper L, Moss D et al. Induction of therapeutic T-cell responses to subdominant tumor-associated viral oncogene after immunization with replication-incompetent polyepitope adenovirus vaccine. Cancer Res 2004; 64: 1483-1489.
21. Wang JH, Yan YW, Garrett TP, Liu JH, Rodgers DW, Garlick RL et al. Atomic structure of a fragment of human CD4 containing two immunoglobulin-like domains. Nature 1990; 348: 411-418.
22. Khanna R, Burrows SR, Nicholls J, Poulsen LM. Identification of cytotoxic T cell epitopes within Epstein-Barr virus (EBV) oncogene latent membrane protein 1 (LMP1): evidence for HLA A2 supertype-restricted immune recognition of EBV-infected cells by LMP1-specific cytotoxic T lymphocytes. Eur J Immunol 1998; 28: 451-458.
23. Bollard CM, Straathof KC, Huls MH, Leen A, Lacuesta K, Davis A et al. The generation and characterization of LMP2-specific CTLs for use as adoptive transfer from patients with relapsed EBV-positive Hodgkin disease. J Immunother 2004; 27: 317-327.
24. Khanna R, Burrows SR, Moss DJ. Immune regulation in Epstein-Barr virusassociated diseases. Microbiol Rev 1995; 59: 387-405.
25. Rickinson AB, Moss DJ. Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu Rev Immunol 1997; 15: 405-431.
26. Gottschalk S, Edwards OL, Sili U, Huls MH, Goltsova T, Davis AR et al. Generating CTLs against the subdominant Epstein-Barr virus LMP1 antigen for the adoptive immunotherapy of EBV-associated malignancies. Blood 2003; 101: 1905-1912.
27. Laherty CD, Hu HM, Opipari AW, Wang F, Dixit VM. The Epstein-Barr virus LMP1 gene product induces A20 zinc finger protein expression by activating nuclear factor kappa B. J Biol Chem 1992; 267: 24157-24160.
28. Hong B, Song XT, Rollins L, Berry L, Huang XF, Chen SY. Mucosal and systemic anti-HIV immunity controlled by A20 in mouse dendritic cells. J Clin Invest 2011; 121: 739-751.
29. Song XT, Evel-Kabler K, Rollins L, Aldrich M, Gao F, Huang XF et al. An alternative and effective HIV vaccination approach based on inhibition of antigen presentation attenuators in dendritic cells. PLoS Med 2006; 3: e11.
30. Pittet MJ, Zippelius A, Speiser DE, Assenmacher M, Guillaume P, Valmori D et al. Ex vivo IFN-gamma secretion by circulating CD8 T lymphocytes: implications of a novel approach for T cell monitoring in infectious and malignant diseases. J Immunol 2001; 166: 7634-7640.
31. Tussey L, Speller S, Gallimore A, Vessey R. Functionally distinct CD8+ memory T cell subsets in persistent EBV infection are differentiated by migratory receptor expression. Eur J Immunol 2000; 30: 1823-1829.
32. Saito M, Nagasawa M, Takada H, Hara T, Tsuchiya S, Agematsu K et al. Defective IL-10 signaling in hyper-IgE syndrome results in impaired generation of tolerogenic dendritic cells and induced regulatory T cells. J Exp Med 2011; 208: 235-249.
33. Song XT, Turnis ME, Zhou X, Zhu W, Hong BX, Rollins L et al. A Th1-inducing adenoviral vaccine for boosting adoptively transferred T cells. Mol Ther 2011; 19: 211-217.
34. Marshall NA, Christie LE, Munro LR, Culligan DJ, Johnston PW, Barker RN et al. Immunosuppressive regulatory T cells are abundant in the reactive lymphocytes of Hodgkin lymphoma. Blood 2004; 103: 1755-1762.
35. Poppema S, van den Berg A. Interaction between host T cells and Reed-Sternberg cells in Hodgkin lymphomas. Semin Cancer Biol 2000; 10: 345-350.
36. Fiebiger E, Meraner P, Weber E, Fang IF, Stingl G, Ploegh H et al. Cytokines regulate proteolysis in major histocompatibility complex class II-dependent antigen presentation by dendritic cells. J Exp Med 2001; 193: 881-892.
37. Weiss JM, Subleski JJ, Wigginton JM, Wiltrout RH. Immunotherapy of cancer by IL-12-based cytokine combinations. Expert Opin Biol Ther 2007; 7: 1705-1721.
38. Breckpot K, Aerts-Toegaert C, Heirman C, Peeters U, Beyaert R, Aerts JL et al. Attenuated expression of A20 markedly increases the efficacy of double-stranded RNA-activated dendritic cells as an anti-cancer vaccine. J Immunol 2009; 182: 860-870.
39. Sica A, Saccani A, Bottazzi B, Polentarutti N, Vecchi A, van Damme J et al. Autocrine production of IL-10 mediates defective IL-12 production and NF-kappa B activation in tumor-associated macrophages. J Immunol 2000; 164: 762-767.
40. Gottschalk S, Rooney CM, Heslop HE. Post-transplant lymphoproliferative disorders. Annu Rev Med 2005; 56: 29-44.
41. Bollard CM, Aguilar L, Straathof KC, Gahn B, Huls MH, Rousseau A et al. Cytotoxic T lymphocyte therapy for Epstein-Barr virus+Hodgkin's disease. J Exp Med 2004; 200: 1623-1633.
42. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252.
43. Hong B, Ren W, Song XT, Evel-Kabler K, Chen SY, Huang XF. Human suppressor of cytokine signaling 1 controls immunostimulatory activity of monocyte-derived dendritic cells. Cancer Res 2009; 69: 8076-8084.
44. Schroers R, Huang XF, Hammer J, Zhang J, Chen SY. Identification of HLA DR7-restricted epitopes from human telomerase reverse transcriptase recognized by CD4+ T-helper cells. Cancer Res 2002; 62: 2600-2605.
45. Schroers R, Shen L, Rollins L, Rooney CM, Slawin K, Sonderstrup G et al. Human telomerase reverse transcriptase-specific T-helper responses induced by promiscuous major histocompatibility complex class II-restricted epitopes. Clin Cancer Res 2003; 9: 4743-4755.
46. Duraiswamy J, Sherritt M, Thomson S, Tellam J, Cooper L, Connolly G et al. Therapeutic LMP1 polyepitope vaccine for EBV-associated Hodgkin disease and nasopharyngeal carcinoma. Blood 2003; 101: 3150-3156.
47. van der Bruggen P, Bastin J, Gajewski T, Coulie PG, Boel P, De Smet C et al. A peptide encoded by human gene MAGE-3 and presented by HLA-A2 induces cytolytic T lymphocytes that recognize tumor cells expressing MAGE-3. Eur J Immunol 1994; 24: 3038-3043.
48. De Angelis B, Dotti G, Quintarelli C, Huye LE, Zhang L, Zhang M et al. Generation of Epstein-Barr virus-specific cytotoxic T lymphocytes resistant to the immunosuppressive drug tacrolimus (FK506). Blood 2009; 114: 4784-4791.
49. Vera JF, Hoyos V, Savoldo B, Quintarelli C, Giordano Attianese GM, Leen AM et al. Genetic manipulation of tumor-specific cytotoxic T lymphocytes to restore responsiveness to IL-7. Mol Ther 2009; 17: 880-888.
50. Savoldo B, Rooney CM, Di Stasi A, Abken H, Hombach A, Foster AE et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 2007; 110: 2620-2630.