Protective CD8+ T-cell responses to cytomegalovirus driven by rAAV/GFP/IE1 loading of dendritic cells

Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH: Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Eng J Med. 1997, 336: 973-979. 10.1056/NEJM199704033361401. Adam E, Melnick JL, DeBakey ME: Cytomegalovirus infection and atherosclerosis. Cent Eur J Public Health. 1997, 5: 99-106. Bolovan-Fritts CA, Trout RN, Spector SA: Human cytomegalovirus-specific CD4+- T-cell cytokine response induces fractalkine in endothelial cells. J Virol. 2004, 78: 13174-13181. 10.1128/JVI.78.23.13173-13181.2004. Froberg MK, Adams A, Seacotte N: Cytomegalovirus infection accelerates inflammation in vascular tissue overexpressing monocyte chemoattractant protein-1. Circ Res. 2001, 89: 1224-1230. 10.1161/hh2401.100601. Kendall TJ, Wilson JE, Radio SJ, Kandolf R: Cytomegalovirus and other herpesviruses: do they have a role in the development of accelerated coronary arterial disease in human heart allografts?. J Heart Lung Transplant. 1992, 11: S14-20. Koskinen PK, Kallio EA, Tikkanen JM: Cytomegalovirus infection and cardiac allograft vasculopathy. Transpl Infect Dis. 1999, 1: 115-126. 10.1034/j.1399-3062.1999.010205.x. Koskinen P, Lemstrøm K, Mattila S: Cytomegalovirus infection associated accelerated heart allograft arteriosclerosis may impair the late function of the graft. Clin Transplant. 1996, 10: 487-493. Koskinen P, Lemström K, Bruggeman C: Acute cytomegalovirus infection induces a subendothelial inflammation (endothelialitis) in the allograft vascular wall. A possible linkage with enhanced allograft arteriosclerosis. Am J Pathol. 1994, 144: 41-50. Lozinguez O, Arnaud E, Velut JG: Cytomegalovirus and arterial disease. Current aspects. Arch Mal Coeur Vaiss. 1999, 92: 1205-1212. Melnick JL, Adam E, Debakey ME: Cytomegalovirus and atherosclerosis. Eur Heart J. 1993, 14 (suppl K): 30-38. Petrakopoulou P, Kübrich M, Pehlivanli S: Cytomegalovirus infection in heart transplant recipients is associated with impaired endothelial function. Circulation. 2004, 110: 207-212. 10.1161/01.CIR.0000138393.99310.1c. Scheller N, Furtwangler R, Sester U, Maier R, Breinig T, Meyerhans A: Human cytomegalovirus protein pp65: an efficient protein carrier system into human dendritic cell. Gene Ther. 2008, 15: 318-325. 10.1038/sj.gt.3303086. Schönian U, Maisch B: Cytomegalovirus associated diseases of the heart. Herz. 1992, 17: 85-90. Tu W, Potena L, Stepick-Biek P: T-cell immunity to subclinical cytomegalovirus infection reduces cardiac allograft disease. Circulation. 2006, 114: 1561-1564. 10.1161/CIRCULATIONAHA.105.607549. Zakliczyński M, Krynicka-Mazurek A, Pyka Ł: The influence of cytomegalovirus infection, confirmed by pp65 antigen presence, on the development of cardiac allograft vasculopathy. Transplant Proc. 2007, 39: 2866-2869. 10.1016/j.transproceed.2007.09.013. Paya CV: Prevention of cytomegalovirus disease in recipients of solid-organ transplants. Clin Infect Dis. 2001, 32: 596-603. 10.1086/318724. Zaia JA: Prevention of cytomegalovirus disease in hematopoietic stem cell transplantation. Clin Infec Dis. 2002, 35: 999-1004. 10.1086/342883. Borysiewicz L, Hickling J, Graham S, Sinclair J, Cranage M, Smith G, Sissons J: Human cytomegalovirus specific cytotoxic T cells relative treatment of stage specific CTL recognizing the 72 kD immediate early protein and glycoprotein B expressed by recombinant vaccinia viruses. J Exp Med. 1988, 168: 919-931. 10.1084/jem.168.3.919. McLaughlin-Taylor E, Pande H, Forman SJ, Tanamachi B, Li CR, Zaia JA, Greenberg PD, Riddell SR: Identification of the major late human cytomegalovirus matrix protein pp65 as a target antigen for CD8+ virus-specific cytotoxic T lymphocytes. J Med Virol. 1994, 43: 103-110. 10.1002/jmv.1890430119. Lee HR, Kim DJ, Lee JM, Choi CY, Ahn BY: Ability of the human cytomegalovirus IE1 protein to modulate sumoylation of PML correlates with its functional activities in transcriptional regulation and infectivity in cultured fibroblast cells. J Virol. 2004, 78: 6527-6542. 10.1128/JVI.78.12.6527-6542.2004. Vaz-Santiago J, Lulé J, Rohrlich P, Jacquier C, Gibert N: Ex vivo stimulation and expansion of both CD4+ and CD8+ T cells from peripheral blood mononuclear cells of human cytomegalovirus-seropositive blood donors by using a soluble recombinant chimeric protein, IE1-pp65. J Virol. 2001, 75: 7840-7847. 10.1128/JVI.75.17.7840-7847.2001. Reddehase MJ, Koszinowski UH: Significance of herpesvirus immediate-early gene expression in cellular immunity to cytomegalovirus infection. Nature. 1984, 312: 369-371. 10.1038/312369a0. Chiriva-Internati M, Liu Y, Weidanz JA, Grizzi F, You H, Zhou W: Testing recombinant adeno-associated virus-gene loading of dendritic cell for generating potent cytotoxic T lymphocytes against a prototype self-antigen, multiple myeloma HM1.24. Blood. 2003, 102: 3100-3107. 10.1182/blood-2002-11-3580. Liu Y, Chiriva-Internati M, Grizzi F, Salati E, Roman J, Lim S: Rapid induction of cytotoxic t-cell antigen gene deliver into human dendritic cells by an adeno-associated virus vector. Cancer Gene Ther. 2001, 8: 948-957. 10.1038/sj.cgt.7700391. Ponnazhagan S, Mahendra G, Curiel D, Shaw D: Adeno-associated virus type 2-mediated transduction of human monocyte-derived dendritic cells: implications for ex vivo immunotherapy. J Virol. 2001, 10: 9493-9501. 10.1128/JVI.75.19.9493-9501.2001. Romani NS, Gruner D, Brang E, Kampgen E, Lenz A, Trockenbacher B, Konwalinka G, Fritsch PO, Steinman RM, Schuler G: Proliferating dendritic cell progenitors in human blood. J Exp Med. 1994, 180: 83-93. 10.1084/jem.180.1.83. Sallusto F, Lanzavecchia A: Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med. 1994, 179: 1109-1118. 10.1084/jem.179.4.1109. Chiriva-Internati M, Liu Y, Salati E, Zhou W, Wang Z, Grizzi F, Roman JJ, Lim SH, Hermonat PL: Efficient generation of cytotoxic T lymphocytes against cervical cancer cells by adeno-associated virus/human papillomavirus type 16 E7 antigen gene transduction into dendritic cells. Eur J Immunol. 2002, 32: 30-38. 10.1002/1521-4141(200201)32:1<30::AID-IMMU30>3.0.CO;2-E. Young JW, Inaba K: Dendritic cells as adjuvants for class I major histocompatibility complex-restricted antitumor immunity. J Exp Med. 1996, 183: 7-11. 10.1084/jem.183.1.7. Liu Y, Santin AD, Mane M, Chiriva-Internati M, Parham GP, Ravaggi A, Hermonat PL: Transduction and utility of the granulocyte-macrophage colony stimulating factor gene into dendritic cells by adeno-associated virus. J Interferon Cytokine Res. 2000, 20: 21-30. 10.1089/107999000312702. Pala P, Verhoef A, Lamb JR, Openshaw PJ: Single cell analysis of cytokine expression kinetics by human CD4+ T-cell clones during activation or tolerance induction. Immunology. 2000, 100: 209-216. 10.1046/j.1365-2567.2000.00036.x. Veldwijk MR, Topaly J, Laufs S, Hengge UR, Wenz F, Zeller WJ, Fruehauf S: Development and optimization of a real time quantitative PCR-based method for the titration of AAV-2 vector stocks. Mol Ther. 2002, 6: 272-278. 10.1006/mthe.2002.0659. Yu Y, Wen B, Niu D, Chen M, Qiu L: Induction of Protective Immunity Against Scrub Typhus with a 56-Kilodalton Recombinant Antigen Fused with a 47-Kilodalton Antigen of Orientia tsutsugamushi Karp. Am J Trop Med Hyg. 2005, 72: 458-464. Podsakoff G, Wong KK, Chatterjee S: Efficient gene transfer into nondividing cells by adeno-associated virus-based vectors. J Virol. 1994, 68 (9): 5656-5666. Polic B, Hengel H, Krmpotic A, Trgovcich J, Pavic I, Luccaronin P, Jonjic S, Koszinowski UH: Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J Exp Med. 1998, 188: 1047-1054. 10.1084/jem.188.6.1047. Reddehase MJ, Weiland F, Munch K, Jonjic S, Luske A, Koszinowski UH: Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs. J Virol. 1985, 55: 264-273. Selin LK, Nahill SR, Welsh RM: Cross-reactivities in memory cytotoxic T lymphocyte recognition of heterologous viruses. J Exp Med. 1994, 179: 1933-1943. 10.1084/jem.179.6.1933. Steffens HP, Kurz S, Holtappels R, Reddehase MJ: Preemptive CD8 T-cell immunotherapy of acute cytomegalovirus infection prevents lethal disease, limits the burden of latent viral genomes, and reduces the risk of virus recurrence. J Virol. 1998, 72: 1797-1804. Fisher-Adams G, Wong KK, Podsakoff G, Forman SJ, Chatterjee S: Integration of adeno-associated virus vectors in CD34+ human hematopoietic progenitor cells after transduction. Blood. 1996, 88: 492-504. Hermonat PL, Muzyczka N: Use of adeno-associated virus as a mammalian DNA cloning vector: transduction of neomycin resistance into mammalian tissue culture cells. Proc Natl Acad Sci USA. 1984, 81: 6466-6470. 10.1073/pnas.81.20.6466. Zhou SZ, Broxmeyer HE, Cooper S, Harrington MA, Srivastava A: Adeno-associated virus 2-mediated gene transfer in murine hematopoietic progenitor cells. Exp Hematol. 1993, 21: 928-933. Ghazal P, Visser AE, Gustems M, García R, Borst EM, Sullivan K, Messerle M, Angulo A: Elimination of ie1 significantly attenuates murine cytomegalovirus virulence but does not alter replicative capacity in cell culture. J Virol. 2005, 79: 7182-7194. 10.1128/JVI.79.11.7182-7194.2005. Malone CL, Vesole DH, Stinski MF: Transactivation of a human cytomegalovirus early promoter by gene products from the immediate-early gene IE2 and augmentation by IE1: mutational analysis of the viral proteins. J Virol. 1990, 64 (4): 1498-1506. Stenberg RM, Fotney J, Barlow SW, Magrane BP, Nelson JA, Ghazal P: Promoter-specific trans activation and repression by human cytomegalovirus immediate-early proteins involves common and unique protein domains. J Virol. 1990, 64: 1556-1565. Poma EE, Kowalik TF, Zhu L, Sinclair JH, Huang ES: The human cytomegalovirus IE1–72 protein interacts with the cellular p107 protein and relieves p107-mediated transcriptional repression of an E2F-responsive promoter. J Virol. 1996, 70: 7867-7877. Chee AV, Roizman B: Herpes simplex virus 1 gene products occlude the interferon signaling pathway at multiple sites. J Virol. 2004, 78: 4185-4196. 10.1128/JVI.78.8.4185-4196.2004. Wiebusch L, Hagemeier C: Human cytomegalovirus 86-kilodalton IE2 protein blocks cell cycle progression in G1. J Virol. 1999, 73: 9274-9283. Zhu H, Shen Y, Shenk T: Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol. 1995, 69: 7960-7970. Pahl-Seibert MF, Juelch M, Podlech J, Thomas D, Deegen P, Reddehase MJ, Holtappels R: Highly protective in vivo function of cytomegalovirus IE1 epitope-specific memory CD8 T cells purified by T-cell receptor-based cell sorting. J Virol. 2005, 79: 5400-5413. 10.1128/JVI.79.9.5400-5413.2005. Retière C, Prod'homme V, Imbert-Marcille BM, Bonneville M, Vié H, Hallet M: Generation of cytomegalovirus-specific human T-lymphocyte clones by using autologous B-lymphoblastoid cells with stable expression of pp65 or IE1 proteins: a tool to study the fine specificity of the antiviral response. J Virol. 2000, 74: 3948-3952. 10.1128/JVI.74.9.3948-3952.2000. Slezak SL, Bettinotti M, Selleri S, Adams S, Marincola FM, Stroncek DF: CMV pp65 and IE-1 T cell epitopes recognized by healthy subjects. J Transl Med. 2007, 5: 17-10.1186/1479-5876-5-17. Collaco RF, Cao X, Trempe JP: A helper virus-free packaging system for recombinant adeno-associated virus vectors. Gene. 1999, 397-405. 10.1016/S0378-1119(99)00347-9.