In vivo and in vitro distribution of type 5 and fiber-modified oncolytic adenoviruses in human blood compartments

References

• Senac JS, Doronin K, Russell SJ, Jelinek DF, Greipp PR, Barry MA. Infection and killing of multiple myeloma by adenoviruses. Hum Gene Ther. 2010;21:179–90.
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Curiel DT. Current issues and future directions of oncolytic adenoviruses. Mol Ther. 2010;18: 243–50.
   PubMed Web of Science ®Google Scholar
• Lyons M, Onion D, Green NK, Aslan K, Rajaratnam R, Bazan-Peregrino M, . Adenovirus type 5 interactions with human blood cells may compromise systemic delivery. Mol Ther. 2006;14:118–28.
   PubMed Web of Science ®Google Scholar
• Carlisle RC, Di Y, Cerny AM, Sonnen AF, Sim RB, Green NK, . Human erythrocytes bind and inactivate type 5 adenovirus by presenting Coxsackie virus-adenovirus receptor and complement receptor 1. Blood. 2009;113: 1909–18.
   PubMed Web of Science ®Google Scholar
• Othman M, Labelle A, Mazzetti I, Elbatarny HS, Lillicrap D. Adenovirus-induced thrombocytopenia: the role of von Willebrand factor and P-selectin in mediating accelerated platelet clearance. Blood. 2007;109:2832–9.
   PubMed Web of Science ®Google Scholar
• Baker AH. Shedding light on tumor targeting by adenovirus. Mol Ther. 2007;15:841–2.
   Google Scholar
• Worgall S, Leopold PL, Wolff G, Ferris B, Van Roijen N, Crystal RG. Role of alveolar macrophages in rapid elimination of adenovirus vectors administered to the epithelial surface of the respiratory tract. Hum Gene Ther. 1997;8: 1675–84.
   PubMed Web of Science ®Google Scholar
• Shimony N, Elkin G, Kolodkin-Gal D, Krasny L, Urieli-Shoval S, Haviv YS. Analysis of adenoviral attachment to human platelets. Virol J. 2009;6:25.
   PubMedGoogle Scholar
• Perlman J, Gibson C, Pounds SB, Gu Z, Bankowski MJ, Hayden RT. Quantitative real-time PCR detection of adenovirus in clinical blood specimens: a comparison of plasma, whole blood and peripheral blood mononuclear cells. J Clin Virol. 2007;40:295–300.
   Google Scholar
• Shike H, Shimizu C, Kanegaye J, Foley JL, Burns JC. Quantitation of adenovirus genome during acute infection in normal children. Pediatr Infect Dis J. 2005;24:29–33.
   Google Scholar
• Cerullo V, Pesonen S, Diaconu I, Escutenaire S, Arstila PT, Ugolini M, . Oncolytic adenovirus coding for granulocyte macrophage colony-stimulating factor induces antitumoral immunity in cancer patients. Cancer Res. 2010;70: 4297–309.
   PubMed Web of Science ®Google Scholar
• Cichon G, Schmidt HH, Benhidjeb T, Loser P, Ziemer S, Haas R, . Intravenous administration of recombinant adenoviruses causes thrombocytopenia, anemia and erythroblastosis in rabbits. J Gene Med. 1999;1:360–71.
   PubMedGoogle Scholar
• Lozier JN, Csako G, Mondoro TH, Krizek DM, Metzger ME, Costello R, . Toxicity of a first-generation adenoviral vector in rhesus macaques. Hum Gene Ther. 2002;13: 113–24.
   PubMed Web of Science ®Google Scholar
• Varnavski AN, Calcedo R, Bove M, Gao G, Wilson JM. Evaluation of toxicity from high-dose systemic administration of recombinant adenovirus vector in vector-naive and pre-immunized mice. Gene Ther. 2005;12:427–36.
   PubMed Web of Science ®Google Scholar
• Pesonen S, Nokisalmi P, Escutenaire S, Sarkioja M, Raki M, Cerullo V, . Prolonged systemic circulation of chimeric oncolytic adenovirus Ad5/3-Cox2L-D24 in patients with metastatic and refractory solid tumors. Gene Ther. 2010; 17:892–904.
   Google Scholar
• Nokisalmi P, Pesonen S, Escutenaire S, Sarkioja M, Raki M, Cerullo V, . Oncolytic adenovirus ICOVIR-7 in patients with advanced and refractory solid tumors. Clin Cancer Res. 2010;16:3035–43.
   PubMed Web of Science ®Google Scholar
• Flomenberg P, Gutierrez E, Piaskowski V, Casper JT. Detection of adenovirus DNA in peripheral blood mononuclear cells by polymerase chain reaction assay. J Med Virol. 1997;51:182–8.
   PubMed Web of Science ®Google Scholar
• Durepaire N, Rogez JP, Verdier M, Rogez S, Weinbreck P, Denis F. Detection of adenovirus DNA by polymerase chain reaction in peripheral blood lymphocytes from HIV-infected patients and a control group: preliminary results. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;14: 189–90.
   Google Scholar
• Qiao J, Kottke T, Willmon C, Galivo F, Wongthida P, Diaz RM, . Purging metastases in lymphoid organs using a combination of antigen-nonspecific adoptive T cell therapy, oncolytic virotherapy and immunotherapy. Nat Med. 2008; 14:37–44.
   PubMed Web of Science ®Google Scholar
• Ilett EJ, Prestwich RJ, Kottke T, Errington F, Thompson JM, Harrington KJ, . Dendritic cells and T cells deliver oncolytic reovirus for tumour killing despite pre-existing anti-viral immunity. Gene Ther. 2009;16:689–99.
   PubMed Web of Science ®Google Scholar
• Yotnda P, Savoldo B, Charlet-Berguerand N, Rooney C, Brenner M. Targeted delivery of adenoviral vectors by cytotoxic T cells. Blood. 2004;104:2272–80.
   Web of Science ®Google Scholar
• Pesonen S, Cerullo V, Escutenaire S, Raki M, Kangasniemi L, Karli E, . Treatment of cancer patients with integrin-targeted oncolytic adenoviruses Ad5-D24-RGD and Ad5-RGD-D24-GMCSF. Paper presented at the Annual Meeting of American Society of Gene and Cell Therapy; 19–22 May 2010; Washington, DC, USA.
   Google Scholar
• Koski A, Kangasniemi L, Escutenaire S, Pesonen S, Cerullo V, Diaconu I, . Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther. 2010;18:1874–84.
   PubMed Web of Science ®Google Scholar
• Alvarez-Lafuente R, Garcia-Montojo M, De Las Heras V, Bartolome M, Arroyo R. Interferon-beta treatment and active replication of the JC virus in relapsing-remitting multiple sclerosis patients. Eur J Neurol. 2007;14:233–6.
   Google Scholar
• Suzuki K, Fueyo J, Krasnykh V, Reynolds PN, Curiel DT, Alemany R. A conditionally replicative adenovirus with enhanced infectivity shows improved oncolytic potency. Clin Cancer Res. 2001;7:120–6.
   PubMed Web of Science ®Google Scholar
• Bauerschmitz GJ, Guse K, Kanerva A, Menzel A, Herrmann I, Desmond RA, . Triple-targeted oncolytic adenoviruses featuring the cox2 promoter, E1A transcomplementation, and serotype chimerism for enhanced selectivity for ovarian cancer cells. Mol Ther. 2006;14:164–74.
   PubMed Web of Science ®Google Scholar
• Rojas JJ, Cascallo M, Guedan S, Gros A, Martinez-Quintanilla J, Hemminki A, . A modified E2F-1 promoter improves the efficacy to toxicity ratio of oncolytic adenoviruses. Gene Ther. 2009;16:1441–51.
   PubMed Web of Science ®Google Scholar
• Reid T, Galanis E, Abbruzzese J, Sze D, Wein LM, Andrews J, . Hepatic arterial infusion of a replication-selective oncolytic adenovirus (dl1520): phase II viral, immunologic, and clinical endpoints. Cancer Res. 2002;62:6070–9.
   PubMed Web of Science ®Google Scholar
• DeWeese TL, van der Poel H, Li S, Mikhak B, Drew R, Goemann M, . A phase I trial of CV706, a replication-competent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res. 2001;61:7464–72.
   PubMed Web of Science ®Google Scholar
• Small EJ, Carducci MA, Burke JM, Rodriguez R, Fong L, van Ummersen L, . A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol Ther. 2006; 14:107–17.
   PubMed Web of Science ®Google Scholar
• Reinhold MI, Lindberg FP, Plas D, Reynolds S, Peters MG, Brown EJ. In vivo expression of alternatively spliced forms of integrin-associated protein (CD47). J Cell Sci. 1995; 108:3419–25.
   PubMed Web of Science ®Google Scholar
• Coulombel L, Auffray I, Gaugler MH, Rosemblatt M. Expression and function of integrins on hematopoietic progenitor cells. Acta Haematol. 1997;97:13–21.
   Google Scholar
• Dmitriev I, Krasnykh V, Miller CR, Wang M, Kashentseva E, Mikheeva G, . An adenovirus vector with genetically modified fibers demonstrates expanded tropism via utilization of a coxsackievirus and adenovirus receptor-independent cell entry mechanism. J Virol. 1998;72:9706–13.
   PubMed Web of Science ®Google Scholar
• Kanerva A, Mikheeva GV, Krasnykh V, Coolidge CJ, Lam JT, Mahasreshti PJ, . Targeting adenovirus to the serotype 3 receptor increases gene transfer efficiency to ovarian cancer cells. Clin Cancer Res. 2002;8:275–80.
   PubMed Web of Science ®Google Scholar
• Kanerva A, Wang M, Bauerschmitz GJ, Lam JT, Desmond RA, Bhoola SM, . Gene transfer to ovarian cancer versus normal tissues with fiber-modified adenoviruses. Mol Ther. 2002;5:695–704.
   PubMed Web of Science ®Google Scholar
• Willmon C, Harrington K, Kottke T, Prestwich R, Melcher A, Vile R. Cell carriers for oncolytic viruses: Fed Ex for cancer therapy. Mol Ther. 2009;17:1667–76.
   PubMed Web of Science ®Google Scholar
• Leon RP, Hedlund T, Meech SJ, Li S, Schaack J, Hunger SP, . Adenoviral-mediated gene transfer in lymphocytes. Proc Natl Acad Sci U S A. 1998;95:13159–64.
   PubMed Web of Science ®Google Scholar
• Cotter MJ, Zaiss AK, Muruve DA. Neutrophils interact with adenovirus vectors via Fc receptors and complement receptor 1. J Virol. 2005;79:14622–31.
   PubMed Web of Science ®Google Scholar
• Schierer S, Hesse A, Muller I, Kampgen E, Curiel DT, Schuler G, . Modulation of viability and maturation of human monocyte-derived dendritic cells by oncolytic adenoviruses. Int J Cancer. 2008;122:219–29.
   PubMedGoogle Scholar
• Short JJ, Pereboev AV, Kawakami Y, Vasu C, Holterman MJ, Curiel DT. Adenovirus serotype 3 utilizes CD80 (B7.1) and CD86 (B7.2) as cellular attachment receptors. Virology. 2004;322:349–59.
   PubMed Web of Science ®Google Scholar
• Short JJ, Vasu C, Holterman MJ, Curiel DT, Pereboev A. Members of adenovirus species B utilize CD80 and CD86 as cellular attachment receptors. Virus Res. 2006;122: 144–53.
   Google Scholar
• Lavery D, Fu SM, Lufkin T, Chen-Kiang S. Productive infection of cultured human lymphoid cells by adenovirus. J Virol. 1987;61:1466–72.
   PubMed Web of Science ®Google Scholar
• Danielsson A, Elgue G, Nilsson BM, Nilsson B, Lambris JD, Totterman TH, . An ex vivo loop system models the toxicity and efficacy of PEGylated and unmodified adenovirus serotype 5 in whole human blood. Gene Ther. 2010; 17:752–62.
   PubMed Web of Science ®Google Scholar