Characterization of human adenovirus serotypes 5, 6, 11, and 35 as anticancer agents

Virology

Volumn 394, Issue 2, 2009, Pages 311-320

  Shashkova, Elena V ^a   May, Shannon M ^a   Barry, Michael A ^a  

^a MAYO CLINIC   (United States)

Author keywords

Adenovirus; Kupffer cells; Oncolytic viruses; Toxicity; Xenograft model antitumor assays

Indexed keywords

ALANINE AMINOTRANSFERASE; ANTINEOPLASTIC AGENT; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR; MEMBRANE COFACTOR PROTEIN; ONCOLYTIC ADENOVIRUS; ONCOLYTIC ADENOVIRUS SEROTYPE 11; ONCOLYTIC ADENOVIRUS SEROTYPE 35; ONCOLYTIC ADENOVIRUS SEROTYPE 5; ONCOLYTIC ADENOVIRUS SEROTYPE 6; ONCOLYTIC VIRUS; UNCLASSIFIED DRUG; VIROTHERAPY AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY TEST; DOSE RESPONSE; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KUPFFER CELL; LIVER CELL CARCINOMA; LIVER TOXICITY; MALE; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; OVARY CARCINOMA; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CARCINOMA; PROTEIN EXPRESSION;

ADENOVIRUSES, HUMAN; ANIMALS; ANTIGENS, CD46; BREAST NEOPLASMS; CARCINOMA, HEPATOCELLULAR; CELL LINE; CELL LINE, TUMOR; FEMALE; HEPATOCYTES; HUMANS; KUPFFER CELLS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, TRANSGENIC; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; OVARIAN NEOPLASMS; PROSTATIC NEOPLASMS; RECEPTORS, VIRUS; RECOVERIN; SEROTYPING;

ADENOVIRIDAE; HUMAN ADENOVIRUS; HUMAN ADENOVIRUS TYPE 5; MUS;

EID: 70449130491     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.08.038     Document Type: Article

References (49)

1. Abbink P., Lemckert A.A., Ewald B.A., Lynch D.M., Denholtz M., Smits S., Holterman L., Damen I., Vogels R., Thorner A.R., O'Brien K.L., Carville A., Mansfield K.G., Goudsmit J., Havenga M.J., and Barouch D.H. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J. Virol. 81 (2007) 4654-4663
2. Adhikary A.K., Banik U., Numaga J., Suzuki E., Inada T., and Okabe N. Heterogeneity of the fibre sequence in subgenus C adenoviruses. J. Clin. Pathol. 57 (2004) 612-617
3. Barton K.N., Paielli D., Zhang Y., Koul S., Brown S.L., Lu M., Seely J., Kim J.H., and Freytag S.O. Second-generation replication-competent oncolytic adenovirus armed with improved suicide genes and ADP gene demonstrates greater efficacy without increased toxicity. Mol. Ther. 13 (2006) 347-356
4. Bergelson J.M., Cunningham J.A., Droguett G., Kurt-Jones E.A., Krithivas A., Hong J.S., Horwitz M.S., Crowell R.L., and Finberg R.W. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275 (1997) 1320-1323
5. Campos S.K., and Barry M.A. Current advances and future challenges in adenoviral vector biology and targeting. Curr. Gene Ther. 7 (2007) 189-204
6. Capone S., Meola A., Ercole B.B., Vitelli A., Pezzanera M., Ruggeri L., Davies M.E., Tafi R., Santini C., Luzzago A., Fu T.M., Bett A., Colloca S., Cortese R., Nicosia A., and Folgori A. A novel adenovirus type 6 (Ad6)-based hepatitis C virus vector that overcomes preexisting anti-ad5 immunity and induces potent and broad cellular immune responses in rhesus macaques. J. Virol. 80 (2006) 1688-1699
7. Cattaneo R., Miest T., Shashkova E.V., and Barry M.A. Reprogrammed viruses as cancer therapeutics: targeted, armed and shielded. Nat. Rev. Microbiol. 6 (2008) 529-540
8. Chen Y., Yu D.C., Charlton D., and Henderson D.R. Pre-existent adenovirus antibody inhibits systemic toxicity and antitumor activity of CN706 in the nude mouse LNCaP xenograft model: implications and proposals for human therapy. Hum. Gene Ther. 11 (2000) 1553-1567
9. Dechecchi M.C., Tamanini A., Bonizzato A., and Cabrini G. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology 268 (2000) 382-390
10. Demers G.W., Johnson D.E., Tsai V., Wen S.F., Quijano E., Machemer T., Philopena J., Ramachandra M., Howe J.A., Shabram P., Ralston R., and Engler H. Pharmacologic indicators of antitumor efficacy for oncolytic virotherapy. Cancer Res. 63 (2003) 4003-4008
11. Doronin K., Toth K., Kuppuswamy M., Ward P., Tollefson A.E., and Wold W.S. Tumor-specific, replication-competent adenovirus vectors overexpressing the adenovirus death protein. J. Virol. 74 (2000) 6147-6155
12. Gaggar A., Shayakhmetov D.M., and Lieber A. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9 (2003) 1408-1412
13. Garber K. China approves world's first oncolytic virus therapy for cancer treatment. J. Natl. Cancer Inst. 98 (2006) 298-300
14. Garnett C.T., Talekar G., Mahr J.A., Huang W., Zhang Y., Ornelles D.A., and Gooding L.R. Latent species C adenoviruses in human tonsil tissues. J. Virol. 83 (2009) 2417-2428
15. Holterman L., Vogels R., van der Vlugt R., Sieuwerts M., Grimbergen J., Kaspers J., Geelen E., van der Helm E., Lemckert A., Gillissen G., Verhaagh S., Custers J., Zuijdgeest D., Berkhout B., Bakker M., Quax P., Goudsmit J., and Havenga M. Novel replication-incompetent vector derived from adenovirus type 11 (Ad11) for vaccination and gene therapy: low seroprevalence and non-cross-reactivity with Ad5. J. Virol. 78 (2004) 13207-13215
16. Kalyuzhniy O., Di Paolo N.C., Silvestry M., Hofherr S.E., Barry M.A., Stewart P.L., and Shayakhmetov D.M. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 5483-5488
17. Kojaoghlanian T., Flomenberg P., and Horwitz M.S. The impact of adenovirus infection on the immunocompromised host. Rev. Med. Virol. 13 (2003) 155-171
18. Kuhn I., Harden P., Bauzon M., Chartier C., Nye J., Thorne S., Reid T., Ni S., Lieber A., Fisher K., Seymour L., Rubanyi G.M., Harkins R.N., and Hermiston T.W. Directed evolution generates a novel oncolytic virus for the treatment of colon cancer. PLoS ONE 3 (2008) e2409
19. Leopold P.L., and Crystal R.G. Intracellular trafficking of adenovirus: many means to many ends. Adv. Drug Deliv. Rev. 59 (2007) 810-821
20. Li E., Brown S.L., Stupack D.G., Puente X.S., Cheresh D.A., and Nemerow G.R. Integrin alpha(v)beta1 is an adenovirus coreceptor. J. Virol. 75 (2001) 5405-5409
21. Liu A.Y. Differential expression of cell surface molecules in prostate cancer cells. Cancer Res. 60 (2000) 3429-3434
22. Manickan E., Smith J.S., Tian J., Eggerman T.L., Lozier J.N., Muller J., and Byrnes A.P. Rapid Kupffer cell death after intravenous injection of adenovirus vectors. Mol. Ther. 13 (2006) 108-117
23. Mrkic B., Pavlovic J., Rulicke T., Volpe P., Buchholz C.J., Hourcade D., Atkinson J.P., Aguzzi A., and Cattaneo R. Measles virus spread and pathogenesis in genetically modified mice. J. Virol. 72 (1998) 7420-7427
24. Nwanegbo E., Vardas E., Gao W., Whittle H., Sun H., Rowe D., Robbins P.D., and Gambotto A. Prevalence of neutralizing antibodies to adenoviral serotypes 5 and 35 in the adult populations of The Gambia, South Africa, and the United States. Clin. Diagn. Lab. Immunol. 11 (2004) 351-357
25. Post D.E., Sandberg E.M., Kyle M.M., Devi N.S., Brat D.J., Xu Z., Tighiouart M., and Van Meir E.G. Targeted cancer gene therapy using a hypoxia inducible factor dependent oncolytic adenovirus armed with interleukin-4. Cancer Res. 67 (2007) 6872-6881
26. Roelvink P.W., Lizonova A., Lee J.G., Li Y., Bergelson J.M., Finberg R.W., Brough D.E., Kovesdi I., and Wickham T.J. The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J. Virol. 72 (1998) 7909-7915
27. Rux J.J., and Burnett R.M. Adenovirus structure. Hum.Gene Ther. 15 (2004) 1167-1176
28. Sakurai F., Kawabata K., Koizumi N., Inoue N., Okabe M., Yamaguchi T., Hayakawa T., and Mizuguchi H. Adenovirus serotype 35 vector-mediated transduction into human CD46-transgenic mice. Gene Ther. 13 (2006) 1118-1126
29. Sakurai F., Nakamura S., Akitomo K., Shibata H., Terao K., Kawabata K., Hayakawa T., and Mizuguchi H. Transduction properties of adenovirus serotype 35 vectors after intravenous administration into nonhuman primates. Mol.Ther. 16 (2008) 726-733
30. Sandberg L., Papareddy P., Silver J., Bergh A., and Mei Y.F. Replication-competent Ad11p vector (RCAd11p) efficiently transduces and replicates in hormone-refractory metastatic prostate cancer cells. Hum. Gene Ther. 20 (2009) 361-373
31. Schmitz H., Wigand R., and Heinrich W. Worldwide epidemiology of human adenovirus infections. Am. J. Epidemiol. 117 (1983) 455-466
32. Segerman A., Atkinson J.P., Marttila M., Dennerquist V., Wadell G., and Arnberg N. Adenovirus type 11 uses CD46 as a cellular receptor. J. Virol. 77 (2003) 9183-9191
33. Seshidhar R.P., Ganesh S., Limbach M.P., Brann T., Pinkstaff A., Kaloss M., Kaleko M., and Connelly S. Development of adenovirus serotype 35 as a gene transfer vector. Virology 311 (2003) 384-393
34. Shashkova E.V., Doronin K., Senac J.S., and Barry M.A. Macrophage depletion combined with anticoagulant therapy increases therapeutic window of systemic treatment with oncolytic adenovirus. Cancer Res. 68 (2008) 5896-5904
35. Shashkova E.V., Kuppuswamy M.N., Wold W.S., and Doronin K. Anticancer activity of oncolytic adenovirus vector armed with IFN-alpha and ADP is enhanced by pharmacologically controlled expression of TRAIL. Cancer Gene Ther. 15 (2008) 61-72
36. Shashkova E.V., Spencer J.F., Wold W.S., and Doronin K. Targeting Interferon-alpha Increases Antitumor Efficacy and Reduces Hepatotoxicity of E1A-mutated Spread-enhanced Oncolytic Adenovirus. Mol. Ther. 15 (2007) 598-607
37. Shayakhmetov D.M., and Lieber A. Dependence of adenovirus infectivity on length of the fiber shaft domain. J. Virol. 74 (2000) 10274-10286
38. Small E.J., Carducci M.A., Burke J.M., Rodriguez R., Fong L., van Ummersen L., Yu D.C., Aimi J., Ando D., Working P., Kirn D., and Wilding G. 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. 14 (2006) 107-117
39. Smith J.S., Xu Z., Tian J., Stevenson S.C., and Byrnes A.P. Interaction of systemically delivered adenovirus vectors with Kupffer cells in mouse liver. Hum. Gene Ther. 19 (2008) 547-554
40. Stone D., Liu Y., Li Z.Y., Tuve S., Strauss R., and Lieber A. Comparison of adenoviruses from species B, C, E, and F after intravenous delivery. Mol. Ther. 15 (2007) 2146-2153
41. Tao N., Gao G.P., Parr M., Johnston J., Baradet T., Wilson J.M., Barsoum J., and Fawell S.E. Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. Mol. Ther. 3 (2001) 28-35
42. Tuve S., Wang H., Jacobs J.D., Yumul R.C., Smith D.F., and Lieber A. Role of cellular heparan sulfate proteoglycans in infection of human adenovirus serotype 3 and 35. PLoS Pathog. 4 (2008) e1000189
43. Tuve S., Wang H., Ware C., Liu Y., Gaggar A., Bernt K., Shayakhmetov D., Li Z., Strauss R., Stone D., and Lieber A. A new group B adenovirus receptor is expressed at high levels on human stem and tumor cells. J. Virol. 80 (2006) 12109-12120
44. Vigant F., Descamps D., Jullienne B., Esselin S., Connault E., Opolon P., Tordjmann T., Vigne E., Perricaudet M., and Benihoud K. Substitution of hexon hypervariable region 5 of adenovirus serotype 5 abrogates blood factor binding and limits gene transfer to liver. Mol. Ther. 16 (2008) 1474-1480
45. Vogels R., Zuijdgeest D., van Rijnsoever R., Hartkoorn E., Damen I., de Bethune M.P., Kostense S., Penders G., Helmus N., Koudstaal W., Cecchini M., Wetterwald A., Sprangers M., Lemckert A., Ophorst O., Koel B., van Meerendonk M., Quax P., Panitti L., Grimbergen J., Bout A., Goudsmit J., and Havenga M. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J. Virol. 77 (2003) 8263-8271
46. Waddington S.N., McVey J.H., Bhella D., Parker A.L., Barker K., Atoda H., Pink R., Buckley S.M., Greig J.A., Denby L., Custers J., Morita T., Francischetti I.M., Monteiro R.Q., Barouch D.H., van Rooijen N., Napoli C., Havenga M.J., Nicklin S.A., and Baker A.H. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 132 (2008) 397-409
47. Wickham T.J., Mathias P., Cheresh D.A., and Nemerow G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73 (1993) 309-319
48. Worgall S., Wolff G., Falck-Pedersen E., and Crystal R.G. Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum. Gene Ther. 8 (1997) 37-44
49. Xu Z., Tian J., Smith J.S., and Byrnes A.P. Clearance of adenovirus by Kupffer cells is mediated by scavenger receptors, natural antibodies, and complement. J. Virol. 82 (2008) 11705-11713