Adenovirus vector system: construction, history and therapeutic applications

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References

• 1. Warnock JN, Daigre C, Al-Rubeai M. Introduction to viral vectors. Methods Mol. Biol. 737, 1–25 (2011).
  Medline CASGoogle Scholar
• 2. Skubis-Zegadło J, Stachurska A, Małecki M. Vectrology of adeno-associated viruses (AAV). Med. Wieku Rozwoj. 17(3), 202–206 (2013).
  MedlineGoogle Scholar
• 3. Berkner KL. Development of adenovirus vectors for the expression of heterologous genes. Biotechniques 6(7), 616–629 (1998).
  Google Scholar
• 4. Singh S, Kumar R, Agrawal B. Adenoviral vector-based vaccines and gene therapies: current status and future prospects. In: Adenoviruses IntechOpen, London, UK (2019). • Includes information regarding adenovirus (AdV) vectors and how they offer several advantages over other viral vectors, including a broad range of tissue tropism, well-characterized genome and ease of genetic manipulation.
  Google Scholar
• 5. Zhang C, Zhou D. Adenoviral vector-based strategies against infectious disease and cancer. Hum. Vaccines Immunother. 12(8), 2064–2074 (2016).
  MedlineGoogle Scholar
• 6. Chen YH, Keiser MS, Davidson BL. Viral vectors for gene transfer. Curr. Protoc. Mouse Biol. 8(4), e58 (2018).
  MedlineGoogle Scholar
• 7. Hoeben RC, Uil TG. Adenovirus DNA replication. Cold Spring Harb. Perspect. Biol. 5(3), 1–11 (2013).
  Google Scholar
• 8. Rux JJ, Burnett RM. Adenovirus structure. Hum. Gene Ther. 15(12), 1167–1176 (2004).
  Medline CASGoogle Scholar
• 9. Brescia M, Janssen JM, Liu J, Gonçalves MAFV. High-capacity adenoviral vectors permit robust and versatile testing of DMD gene repair tools and strategies in human cells. Cells 9(4), 869 (2020).
  Medline CASGoogle Scholar
• 10. Gorsky K. Ghosts of gene therapies past – lessons learned from Jesse Gelsinger. Health Sci. Inq. 6(1), 2013–2016 (2019).
  Google Scholar
• 11. Cao W, Zhang J-L, Feng D-Y et al. The effect of adenovirus-conjugated NDRG2 on p53-mediated apoptosis of hepatocarcinoma cells through attenuation of nucleotide excision repair capacity. Biomaterials 35(3), 993–1003 (2014).
  Medline CASGoogle Scholar
• 12. Dormond E, Perrier M, Kamen A. From the first to the third generation adenoviral vector: what parameters are governing the production yield? Biotechnol. Adv. 27(2), 133–144 (2009).
  Medline CASGoogle Scholar
• 13. Rininger J, Fennell A, Barnes LS, Peterson C, Speidel J. Capacity analysis for viral vector manufacturing: is there enough? Bioprocess Int. (2019). https://bioprocessintl.com/manufacturing/emerging-therapeutics-manufacturing/capacity-analysis-for-viral-vector-manufacturing-is-there-enough/
  Google Scholar
• 14. Sekaly RP. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J. Exp. Med. 205(1), 7–12 (2008).
  Medline CASGoogle Scholar
• 15. Zhu FC, Hou LH, Li JX et al. Safety and immunogenicity of a novel recombinant adenovirus type-5 vector-based Ebola vaccine in healthy adults in China: preliminary report of a randomised, double-blind, placebo-controlled, phase 1 trial. Lancet 385(9984), 2272–2279 (2015).
  Medline CASGoogle Scholar
• 16. Von Seggern DJ, Nemerow GR. Adenoviral vectors for protein expression. Gene Expression Systems 111–156 (1999). www.ncbi.nlm.nih.gov/pmc/articles/PMC7150134/
  Google Scholar
• 17. Haviv YS. A simplified in vitro ligation approach to clone an E1B55k-deleted double-targeted conditionally-replicative adenovirus. Virol. J. 6, 18 (2009).
  MedlineGoogle Scholar
• 18. Mizuguchi H, Kay MA. Efficient construction of a recombinant adenovirus vector by an improved in vitro ligation method. Hum. Gene Ther. 9(17), 2577–2583 (1998).
  Medline CASGoogle Scholar
• 19. Mizuguchi H, Kay MA, Hayakawa T. Approaches for generating recombinant adenovirus vectors. Adv. Drug Deliv. Rev. 52(3), 165–176 (2001).
  Medline CASGoogle Scholar
• 20. Davis AR, Wivel NA, Palladino JL, Tao L, Wilson JM. Construction of adenoviral vectors. Mol. Biotechnol. 18(1), 63–70 (2001).
  Medline CASGoogle Scholar
• 21. Raymond CK, Pownder TA, Sexson SL. General method for plasmid construction using homologous recombination. Biotechniques 26(1), 134–141 (1999).
  CASGoogle Scholar
• 22. Vemula SV, Mittal SK. Production of adenovirus vectors and their use as a delivery system for influenza vaccines. Expert Opin. Biol. Ther. 10(10), 1469–1487 (2010).
  Medline CASGoogle Scholar
• 23. He TC, Zhou S, Da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc. Natl Acad. Sci. U. S. A. 95(5), 2509–2514 (1998).
  Medline CASGoogle Scholar
• 24. Aoki K, Barker C, Danthinne X, Imperiale MJ, Nabel GJ. Efficient generation of recombinant adenoviral vectors by Cre-lox recombination in vitro. Mol. Med. 5(4), 224–231 (1999).
  Medline CASGoogle Scholar
• 25. Hardy S, Kitamura M, Harris-Stansil T, Dai Y, Phipps ML. Construction of adenovirus vectors through Cre-lox recombination. J. Virol. 71(3), 1842–1849 (1997).
  Medline CASGoogle Scholar
• 26. Imelli N, Ruzsics Z, Puntener D, Gastaldelli M, Greber UF. Genetic reconstitution of the human adenovirus type 2 temperature-sensitive 1 mutant defective in endosomal escape. Virol. J. 6, 174 (2009).
  MedlineGoogle Scholar
• 27. Puntener D, Engelke MF, Ruzsics Z, Strunze S, Wilhelm C, Greber UF. Stepwise loss of fluorescent core protein V from human adenovirus during entry into cells. J. Virol. 85(1), 481–496 (2011).
  Medline CASGoogle Scholar
• 28. Ruzsics Z, Lemnitzer F, Thirion C. Engineering adenovirus genome by bacterial artificial chromosome (BAC) technology. Methods Mol. Biol. 1089, 143–158 (2014).
  Medline CASGoogle Scholar
• 29. Lewis TB, Glasgow JN, Harms AS, Standaert DG, Curiel DT. Fiber-modified adenovirus for central nervous system Parkinson's disease gene therapy. Viruses 6(8), 3293–3310 (2014).
  Medline CASGoogle Scholar
• 30. Kaufmann JK, Nettelbeck DM. Virus chimeras for gene therapy, vaccination, and oncolysis: adenoviruses and beyond. Trends Mol. Med. 18(7), 365–376 (2012).
  Medline CASGoogle Scholar
• 31. Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat. Rev. Drug Discov. 14(9), 642–662 (2015).
  Medline CASGoogle Scholar
• 32. Pesonen S, Kangasniemi L, Hemminki A. Oncolytic adenoviruses for the treatment of human cancer: focus on translational and clinical data. Mol. Pharm. 8(1), 12–28 (2011).
  Medline CASGoogle Scholar
• 33. 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. 122(1–2), 144–153 (2006).
  Medline CASGoogle Scholar
• 34. Sirena D, Lilienfeld B, Eisenhut M et al. The human membrane cofactor CD46 is a receptor for species B adenovirus serotype 3. J. Virol. 78(9), 4454–4462 (2004).
  Medline CASGoogle Scholar
• 35. Arnberg N, Kidd AH, Edlund K, Nilsson J, Pring-Akerblom P, Wadell G. Adenovirus type 37 binds to cell surface sialic acid through a charge-dependent interaction. Virology 302(1), 33–43 (2002).
  Medline CASGoogle Scholar
• 36. Yamamoto Y, Nagasato M, Yoshida T, Aoki K. Recent advances in genetic modification of adenovirus vectors for cancer treatment. Cancer Sci. 108(5), 831–837 (2017). • Highlights and describes recent genetic modifications being introduced into AdV vectors to modify their tissue tropism.
  Medline CASGoogle Scholar
• 37. Xu Z, Qiu Q, Tian J et al. Coagulation factor X shields adenovirus type 5 from attack by natural antibodies and complement. Nat. Med. 19(4), 452–457 (2013).
  Medline CASGoogle Scholar
• 38. Cong L, Ran FA, Cox D et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121), 819–823 (2013).
  Medline CASGoogle Scholar
• 39. Tang L, Gong M, Zhang P. In vitro CRISPR-Cas9-mediated efficient Ad5 vector modification. Biochem. Biophys. Res. Commun. 474(2), 395–399 (2016). • Reports the development of a CRISPR-Cas9-based in vitro large DNA vector editing system using an AdV serotype 5 (Ad5)-based vector as an example, which can help in achieving various therapeutic benefits.
  Medline CASGoogle Scholar
• 40. Li Q, Wang H, Gong C-Y et al. Efficient editing of an adenoviral vector genome with CRISPR/Cas9. Indian J. Microbiol. 61(1), 91–95 (2021).
  Medline CASGoogle Scholar
• 41. Jager L, Ehrhardt A. Persistence of high-capacity adenoviral vectors as replication-defective monomeric genomes in vitro and in murine liver. Hum. Gene Ther. 20(8), 883–896 (2009).
  Medline CASGoogle Scholar
• 42. Wilson JM, Engelhardt J. Adenovirus vectors for gene therapy. Biotechnol. Adv. 13(6), 421–433 (2013). • Provides complete information regarding the therapeutic action and safety of replication-competent and replication-defective AdVs.
  Google Scholar
• 43. Eriksson E, Milenova I, Wenthe J et al. Shaping the tumor stroma and sparking immune activation by CD40 and 4-1BB signaling induced by an armed oncolytic virus. Clin. Cancer Res. 23(19), 5846–5857 (2017). • Reports how LOAd703, a designed AdV armed with trimerized CD40L and 4-1BBL, activates immunity and simultaneously modulates the biology of the tumor stroma to support antitumor responses.
  Medline CASGoogle Scholar
• 44. Havunen R, Siurala M, Sorsa S et al. Oncolytic adenoviruses armed with tumor necrosis factor alpha and interleukin-2 enable successful adoptive cell therapy. Mol. Ther. Oncolytics 4, 77–86 (2017).
  Medline CASGoogle Scholar
• 45. Rosewell Shaw A, Suzuki M. Recent advances in oncolytic adenovirus therapies for cancer. Curr. Opin. Virol. 21, 9–15 (2016). • Discusses the genetic modification of oncolytic AdV on the basis of well-characterized natural AdV tropism, which can enhance/regulate AdV transduction and replication in specific cancer cell types.
  MedlineGoogle Scholar
• 46. Ranki T, Pesonen S, Hemminki A et al. Phase I study with ONCOS-102 for the treatment of solid tumors – an evaluation of clinical response and exploratory analyses of immune markers. J. Immunother. Cancer 4(1), 1–18 (2016).
  Google Scholar
• 47. Ene CI, Fueyo J, Lang FF. Delta-24 adenoviral therapy for glioblastoma: evolution from the bench to bedside and future considerations. Neurosurg. Focus 50(2), 1–6 (2021).
  Google Scholar
• 48. Qu J, Lu W, Chen M et al. Combined effect of recombinant human adenovirus p53 and curcumin in the treatment of liver cancer. Exp. Ther. Med. 20(5), 18 (2020).
  Medline CASGoogle Scholar
• 49. Tamura RE, De Luna IV, Lana MG, Strauss BE. Improving adenoviral vectors and strategies for prostate cancer gene therapy. Clinics (Sao Paulo) 73(Suppl. 1), e476s (2018).
  MedlineGoogle Scholar
• 50. Jaffe HA, Danel C, Longenecker G et al. Adenovirus-mediated in vivo gene transfer and expression in normal rat liver. Nat Genet. 1(5), 372–378 (1992).
  Medline CASGoogle Scholar
• 51. Davies JC, Geddes DM, Alton EW. Prospects for gene therapy in lung disease. Curr. Opin. Pharmacol. 1(3), 272–278 (2001).
  Medline CASGoogle Scholar
• 52. Griesenbach U, Ferrari S, Geddes DM, Alton EWFW. Gene therapy progress and prospects: cystic fibrosis. Gene Ther. 9(20), 1344–1350 (2002).
  Medline CASGoogle Scholar
• 53. Cao H, Ouyang H, Grasemann H et al. Transducing airway basal cells with a helper-dependent adenoviral vector for lung gene therapy. Hum. Gene Ther. 29(6), 643–652 (2018).
  Medline CASGoogle Scholar
• 54. Zheng C, Baum BJ, Iadarola MJ, O'Connell BC. Genomic integration and gene expression by a modified adenoviral vector. Nat. Biotechnol. 18(2), 176–180 (2000).
  Medline CASGoogle Scholar
• 55. Margolis DJ, Cromblehome T, Herlyn M et al. Phase I trial to evaluate the safety of H5.020CMV.PDGF-b and limb compression bandage for the treatment of venous leg ulcer: trial A. Hum. Gene Ther. 15(10), 1003–1019 (2004).
  Medline CASGoogle Scholar
• 56. Jaffe GJ, Ciulla TA, Ciardella AP et al. Dual antagonism of PDGF and VEGF in neovascular age-related macular degeneration: a phase IIb, multicenter, randomized controlled trial. Ophthalmology 124(2), 224–234 (2017).
  MedlineGoogle Scholar
• 57. Amini A, Moghaddam SM, Morris DL, Pourgholami MH. The critical role of vascular endothelial growth factor in tumor angiogenesis. Curr. Cancer Drug Targets 12(1), 23–43 (2012).
  Medline CASGoogle Scholar
• 58. Palmer DJ, Grove NC, Turner DL, Ng P. Gene editing with helper-dependent adenovirus can efficiently introduce multiple changes simultaneously over a large genomic region. Mol. Ther. Nucleic Acids 8, 101–110 (2017). • Reports high-efficiency gene editing by helper-dependent AdV vectors, which possess long homology arms that mediate gene editing.
  Medline CASGoogle Scholar
• 59. Cornu TI, Mussolino C, Cathomen T. Refining strategies to translate genome editing to the clinic. Nat. Med. 23(4), 415–423 (2017).
  Medline CASGoogle Scholar
• 60. Stephens CJ, Kashentseva E, Everett W, Kaliberova L, Curiel DT. Targeted in vivo knock-in of human alpha-1-antitrypsin cDNA using adenoviral delivery of CRISPR/Cas9. Gene Ther. 25(2), 139–156 (2018).
  Medline CASGoogle Scholar
• 61. Stephens CJ, Lauron EJ, Kashentseva E, Lu ZH, Yokoyama WM, Curiel DT. Long-term correction of hemophilia B using adenoviral delivery of CRISPR/Cas9. J. Control. Release 298, 128–141 (2019).
  Medline CASGoogle Scholar
• 62. Lino CA, Harper JC, Carney JP, Timlin JA. Delivering CRISPR: a review of the challenges and approaches. Drug Deliv. 25(1), 1234–1257 (2018).
  Medline CASGoogle Scholar
• 63. Ewer K, Sebastian S, Spencer AJ, Gilbert S, Hill AVS, Lambe T. Chimpanzee adenoviral vectors as vaccines for outbreak pathogens. Hum. Vaccines Immunother. 13(12), 3020–3032 (2017).
  MedlineGoogle Scholar
• 64. Guo J, Mondal M, Zhou D. Development of novel vaccine vectors: chimpanzee adenoviral vectors. Hum. Vaccines Immunother. 14(7), 1679–1685 (2018).
  MedlineGoogle Scholar
• 65. D'Souza MP, Yang OO. Adenovirus vectors as HIV-1 vaccines: where are we? What next? AIDS 29(4), 395–400 (2015). • Addresses the role of AdV vectors in the development of HIV-1 vaccines and the associated challenges.
  MedlineGoogle Scholar
• 66. Gu L, Icyuz M, Krendelchtchikova V, Krendelchtchikov A, Johnston AE, Matthews QL. Development of an Ad5H3 chimera using the ‘antigen capsid-incorporation’ strategy for an alternative vaccination approach. Open Virol. J. 10(1), 10–20 (2016).
  Medline CASGoogle Scholar
• 67. Zhu FC, Li YH, Guan XH et al. Safety, tolerability, and immunogenicity of a recombinant adenovirus type-5 vectored COVID-19 vaccine: a dose-escalation, open-label, non-randomised, first-in-human trial. Lancet 395(10240), 1845–1854 (2020).
  Medline CASGoogle Scholar
• 68. Folegatti PM, Ewer KJ, Aley PK et al. Safety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trial. Lancet 369(10249), 467–478 (2020).
  Google Scholar
• 69. Sadoff J, Le Gars M, Shukarev G et al. Interim results of a phase 1–2a trial of Ad26.COV2.S COVID-19 vaccine. N. Engl. J. Med. 384(19), 1824–1835 (2021).
  Medline CASGoogle Scholar
• 70. Jones I, Roy P. Sputnik V COVID-19 vaccine candidate appears safe and effective. Lancet 397(10275), 642–643 (2021).
  Medline CASGoogle Scholar