Overcoming pre-existing adenovirus immunity by genetic engineering of adenovirus-based vectors

Expert Opinion on Biological Therapy

Volumn 9, Issue 12, 2009, Pages 1521-1531

  S Seregin, Sergey ^a   Amalfitano, Andrea ^a,b  

^a 4194 Biomedical and Physical Sciences Bldg ^*  (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Adaptive immunity; Cellular responses; Humoral responses; Innate immunity; Neutralizing antibodies; Recombinant adenovirus

Indexed keywords

ADENOVIRUS VECTOR;

ADENOVIRUS; CHIMERA; CLINICAL TRIAL; DNA MODIFICATION; GENETIC ENGINEERING; GENOME; HUMAN; IMMUNE RESPONSE; IMMUNITY; MUCOSAL IMMUNITY; REVIEW; SEROTYPE; T LYMPHOCYTE; VIRUS CAPSID;

ADAPTIVE IMMUNITY; ADENOVIRIDAE; ANIMALS; CAPSID PROTEINS; GENETIC ENGINEERING; GENETIC VECTORS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; VACCINES, SYNTHETIC;

ADENOVIRIDAE; MIRIDAE;

EID: 70450164178     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712590903307388     Document Type: Review

References (82)

1. Buchbinder SP, Mehrotra DV, Duerr A, et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the STEP Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008;372(9653):1881-1893
2. Zak DE, Aderem A. Systems biology of innate immunity. Immunol Rev 2009;227(1):264-282
3. Cohen J. AIDS research. Did Merck's failed HIV vaccine cause harm? Science 2007;318(5853):1048-1049
4. Perreau M, Pantaleo G, Kremer EJ. Activation of a dendritic cell-T cell axis by Ad5 immune complexes creates an improved environment for replication of HIV in T cells. J Exp Med 2008;205(12):2717-2725
5. Sekaly RP. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J Exp Med 2008;205(1):7-12
6. Hutnick NA, Carnathan DG, Dubey SA, et al. Baseline Ad5 serostatus does not predict Ad5 HIV vaccine-induced expansion of adenovirus-specific CD4+ T cells. Nat Med 2009;15(8):876-878
7. O'Brien KL, Liu J, King SL, et al. Adenovirus-specific immunity after immunization with an Ad5 HIV-1 vaccine candidate in humans. Nat Med 2009;15(8):873-875
8. Stamatatos L, Morris L, Burton DR, Mascola JR. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat Med 2009;15(8):866-870
9. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003;302(5644):415-419
10. Seggewiss R, Dunbar CE. A new direction for gene therapy: intrathymic T cell-specific lentiviral gene transfer. J Clin Invest 2005;115(8):2064-2067
11. Puck JM, Malech HL. Gene therapy for immune disorders: good news tempered by bad news. J Allergy Clin Immunol 2006;117(4):865-869
12. Donsante A, Miller DG, Li Y, et al. AAV vector integration sites in mouse hepatocellular carcinoma. Science 2007;317(5837):477
13. Dave UP, Akagi K, Tripathi R, et al. Murine leukemias with retroviral insertions at Lmo2 are predictive of the leukemias induced in SCID-X1 patients following retroviral gene therapy. PLoS Genet 2009;5(5):e1000491. Published online 22 May 2009, doi:10.1371/journal.pgen.1000491
14. Harui A, Suzuki S, Kochanek S, Mitani K. Frequency and stability of chromosomal integration of adenovirus vectors. J Virol 1999;73(7):6141-6146
15. Schoggins JW, Nociari M, Philpott N, Falck-Pedersen E. Influence of fiber detargeting on adenovirus-mediated innate and adaptive immune activation. J Virol 2005;79(18):11627-11637
16. Croyle MA, Le HT, Linse KD, et al. PEGylated helper-dependent adenoviral vectors: highly efficient vectors with an enhanced safety profile. Gene Ther 2005;12(7):579-587
17. Weaver EA, Barry MA. Effects of shielding adenoviral vectors with polyethylene glycol (PEG) on Vector-specific and vaccine-mediated immune responses. Hum Gene Ther 2008;19(12):1369-1382
18. Lin SW, Cun AS, Harris-McCoy K, Ertl HC. Intramuscular rather than oral administration of replication-defective adenoviral vaccine vector induces specific CD8+ T cell responses in the gut. Vaccine 2007;25(12):2187-2193
19. McConnell MJ, Danthinne X, Imperiale MJ. Characterization of a permissive epitope insertion site in adenovirus hexon. J Virol 2006;80(11):5361-5370
20. Abe S, Okuda K, Ura T, et al. Adenovirus type 5 with modified hexons induces robust transgene-specific immune responses in mice with pre-existing immunity against adenovirus type 5. J Gene Med 2009;11(7):570-579
21. Worgall S, Krause A, Rivara M, et al. Protection against P. aeruginosa with an adenovirus vector containing an OprF epitope in the capsid. J Clin Invest 2005;115(5):1281-1289
22. Sarkioja M, Pesonen S, Raki M, et al. Changing the adenovirus fiber for retaining gene delivery efficacy in the presence of neutralizing antibodies. Gene Ther 2008;15(12):921-929
23. Krause A, Joh JH, Hackett NR, et al. Epitopes expressed in different adenovirus capsid proteins induce different levels of epitope-specific immunity. J Virol 2006;80(11):5523-5530
24. Yang TC, Dayball K, Wan YH, Bramson J. Detailed analysis of the CD8+ T-cell response following adenovirus vaccination. J Virol 2003;77(24):13407- 13411
25. Hackett NR, Kaminsky SM, Sondhi D, Crystal RG. Antivector and antitransgene host responses in gene therapy. Curr Opin Mol Ther 2000;2(4):376-382
26. Boyer JL, Kobinger G, Wilson JM, Crystal RG. Adenovirus-based genetic vaccines for biodefense. Hum Gene Ther 2005;16(2):157-168
27. Barouch DH, Nabel GJ. Adenovirus vector-based vaccines for human immunodeficiency virus type 1. Hum Gene Ther 2005;16(2):149-156
28. Sullivan NJ, Sanchez A, Rollin PE, et al. Development of a preventive vaccine for Ebola virus infection in primates. Nature 2000;408(6812):605-609
29. Millar J, Dissanayake D, Yang TC, et al. The magnitude of the CD8+ T cell response produced by recombinant virus vectors is a function of both the antigen and the vector. Cell Immunol 2007;250(1-2):55-67
30. Liu J, O'Brien KL, Lynch DM, et al. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 2009;457(7225):87-91
31. Mutwiri G, Bateman C, Baca-Estrada ME, et al. Induction of immune responses in newborn lambs following enteric immunization with a human adenovirus vaccine vector. Vaccine 2000;19(9-10):1284-1293
32. Abbink P, Lemckert AA, Ewald BA, et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol 2007;81(9):4654-4663
33. Pinto AR, Fitzgerald JC, Giles-Davis W, et al. Induction of CD8+ T cells to an HIV-1 antigen through a prime boost regimen with heterologous E1-deleted adenoviral vaccine carriers. J Immunol 2003;171(12):6774-6779
34. Reyes-Sandoval A, Sridhar S, Berthoud T, et al. Single-dose immunogenicity and protective efficacy of simian adenoviral vectors against Plasmodium berghei. Eur J Immunol 2008;38(3):732-741
35. Schirmbeck R, Reimann J, Kochanek S, Kreppel F. The immunogenicity of adenovirus vectors limits the multispecificity of CD8 T-cell responses to vector-encoded transgenic antigens. Mol Ther 2008;16(9):1609-1616
36. Shiver JW, Fu TM, Chen L, et al. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 2002;415(6869):331-335
37. Lasaro MO, Ertl HC. New insights on adenovirus as vaccine vectors. Mol Ther 2009;17(8):1333-1339
38. Cohen P. Immunity's yin and yang. A successful vaccine must first avoid being eliminated by pre-existing immunity before it can promote a protective immune response. IAVI Rep 2006;10(1):1-5
39. Molinier-Frenkel V, Gahery-Segard H, Mehtali M, et al. Immune response to recombinant adenovirus in humans: capsid components from viral input are targets for vector-specific cytotoxic T lymphocytes. J Virol 2000;74(16):7678-7682
40. Molinier-Frenkel V, Lengagne R, Gaden F, et al. Adenovirus hexon protein is a potent adjuvant for activation of a cellular immune response. J Virol 2002;76(1):127-135
41. Sumida SM, Truitt DM, Kishko MG, et al. Neutralizing antibodies and CD8+ T lymphocytes both contribute to immunity to adenovirus serotype 5 vaccine vectors. J Virol 2004;78(6):2666-2673
42. Flomenberg P, Piaskowski V, Truitt RL, Casper JT. Characterization of human proliferative T cell responses to adenovirus. J Infect Dis 1995;171(5):1090-1096
43. Tang J, Olive M, Champagne K, et al. Adenovirus hexon T-cell epitope is recognized by most adults and is restricted by HLA DP4, the most common class II allele. Gene Ther 2004;11(18):1408-1415
44. Tang J, Olive M, Pulmanausahakul R, et al. Human CD8+ cytotoxic T cell responses to adenovirus capsid proteins. Virology 2006;350(2):312-322
45. Hashimoto M, Boyer JL, Hackett NR, et al. Induction of protective immunity to anthrax lethal toxin with a nonhuman primate adenovirus-based vaccine in the presence of preexisting anti-human adenovirus immunity. Infect Immun 2005;73(10):6885-6891
46. O'Riordan CR, Lachapelle A, Delgado C, et al. PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody in vitro and in vivo. Hum Gene Ther 1999;10(8):1349-1358
47. Matthews C, Jenkins G, Hilfinger J, Davidson B. Poly-L-lysine improves gene transfer with adenovirus formulated in PLGA microspheres. Gene Ther 1999;6(9):1558-1564
48. Lee SG, Yoon SJ, Kim CD, et al. Enhancement of adenoviral transduction with polycationic liposomes in vivo. Cancer Gene Ther 2000;7(10):1329-1335
49. Croyle MA, Chirmule N, Zhang Y, Wilson JM. PEGylation of E1-deleted adenovirus vectors allows significant gene expression on readministration to liver. Hum Gene Ther 2002;13(15):1887-1900
50. Wortmann A, Vohringer S, Engler T, et al. Fully detargeted polyethylene glycol-coated adenovirus vectors are potent genetic vaccines and escape from pre-existing anti-adenovirus antibodies. Mol Ther 2008;16(1):154-162
51. Ogawara K, Rots MG, Kok RJ, et al. A novel strategy to modify adenovirus tropism and enhance transgene delivery to activated vascular endothelial cells in vitro and in vivo. Hum Gene Ther 2004;15(5):433-443
52. Parks RJ. Adenovirus protein IX: a new look at an old protein. Mol Ther 2005;11(1):19-25
53. Rux JJ, Burnett RM. Adenovirus structure. Hum Gene Ther 2004;15(12):1167-1176
54. Vellinga J, Van der Heijdt S, Hoeben RC. The adenovirus capsid: major progress in minor proteins. J Gen Virol 2005;86(Pt 6):1581-1588
55. Einfeld DA, Brough DE, Roelvink PW, et al. Construction of a pseudoreceptor that mediates transduction by adenoviruses expressing a ligand in fiber or penton base. J Virol 1999;73(11):9130-9136
56. Wickham TJ, Segal DM, Roelvink PW, et al. Targeted adenovirus gene transfer to endothelial and smooth muscle cells by using bispecific antibodies. J Virol 1996;70(10):6831-6838
57. McConnell MJ, Hanna PC, Imperiale MJ. Cytokine response and survival of mice immunized with an adenovirus expressing Bacillus anthracis protective antigen domain 4. Infect Immun 2006;74(2):1009-1015
58. Belousova N, Krendelchtchikova V, Curiel DT, Krasnykh V. Modulation of adenovirus vector tropism via incorporation of polypeptide ligands into the fiber protein. J Virol 2002;76(17):8621-8631
59. Matthews QL, Sibley DA, Wu H, et al. Genetic incorporation of a herpes simplex virus type 1 thymidine kinase and firefly luciferase fusion into the adenovirus protein IX for functional display on the virion. Mol Imaging 2006;5(4):510-519
60. Worgall S, Busch A, Rivara M, et al. Modification to the capsid of the adenovirus vector that enhances dendritic cell infection and transgene-specific cellular immune responses. J Virol 2004;78(5):2572-2580
61. Kurachi S, Koizumi N, Sakurai F, et al. Characterization of capsid-modified adenovirus vectors containing heterologous peptides in the fiber knob, protein IX, or hexon. Gene Ther 2007;14(3):266-274
62. Worgall S, Krause A, Qiu J, et al. Protective immunity to Pseudomonas aeruginosa induced with a capsid-modified adenovirus expressing P. aeruginosa OprF. J Virol 2007;81(24):13801-13808
63. Bailey A, Mautner V. Phylogenetic relationships among adenovirus serotypes. Virology 1994;205(2):438-452
64. Russell WC. Update on adenovirus and its vectors. J Gen Virol 2000;81(Pt 11):2573-2604
65. Gall J, Kass-Eisler A, Leinwand L, Falck-Pedersen E. Adenovirus type 5 and 7 capsid chimera: fiber replacement alters receptor tropism without affecting primary immune neutralization epitopes. J Virol 1996;70(4):2116-2123
66. Gall JG, Crystal RG, Falck-Pedersen E. Construction and characterization of hexon-chimeric adenoviruses: specification of adenovirus serotype. J Virol 1998;72(12):10260-10264
67. Roy S, Shirley PS, McClelland A, Kaleko M. Circumvention of immunity to the adenovirus major coat protein hexon. J Virol 1998;72(8):6875-6879
68. Wu H, Dmitriev I, Kashentseva E, et al. Construction and characterization of adenovirus serotype 5 packaged by serotype 3 hexon. J Virol 2002;76(24):12775-12782
69. Myhre S, Henning P, Granio O, et al. Decreased immune reactivity towards a knobless, affibody-targeted adenovirus type 5 vector. Gene Ther 2007;14(4):376-381
70. Wu H, Curiel DT. Fiber-modified adenoviruses for targeted gene therapy. Methods Mol Biol 2008;434:113-132
71. Noureddini SC, Curiel DT. Genetic targeting strategies for adenovirus. Mol Pharm 2005;2(5):341-347
72. Nakayama M, Both GW, Banizs B, et al. An adenovirus serotype 5 vector with fibers derived from ovine atadenovirus demonstrates CAR-independent tropism and unique biodistribution in mice. Virology 2006;350(1):103-115
73. Roy S, Clawson DS, Calcedo R, et al. Use of chimeric adenoviral vectors to assess capsid neutralization determinants. Virology 2005;333(2):207-214
74. Ritter T, Lehmann M, Volk HD. Improvements in gene therapy: averting the immune response to adenoviral vectors. BioDrugs 2002;16(1):3-10
75. Pichla-Gollon SL, Drinker M, Zhou X, et al. Structure-based identification of a major neutralizing site in an adenovirus hexon. J Virol 2007;81(4):1680-1689
76. Youil R, Toner TJ, Su Q, et al. Hexon gene switch strategy for the generation of chimeric recombinant adenovirus. Hum Gene Ther 2002;13(2):311-320
77. Roberts DM, Nanda A, Havenga MJ, et al. Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 2006;441(7090):239-243
78. Barouch DH, Pau MG, Custers JH, et al. Immunogenicity of recombinant adenovirus serotype 35 vaccine in the presence of pre-existing anti-Ad5 immunity. J Immunol 2004;172(10):6290-6297
79. Liu J, Ewald BA, Lynch DM, et al. Magnitude and phenotype of cellular immune responses elicited by recombinant adenovirus vectors and heterologous prime-boost regimens in rhesus monkeys. J Virol 2008;82(10):4844-4852
80. McCoy K, Tatsis N, Korioth-Schmitz B, et al. Effect of preexisting immunity to adenovirus human serotype 5 antigens on the immune responses of nonhuman primates to vaccine regimens based on human- or chimpanzee-derived adenovirus vectors. J Virol 2007;81(12):6594-6604
81. Hartman ZC, Appledorn DM, Serra D, et al. Replication-attenuated human adenoviral type 4 vectors elicit capsid dependent enhanced innate immune responses that are partially dependent upon interactions with the complement system. Virology 2008;374(2):453-467
82. Hensley SE, Cun AS, Giles-Davis W, et al. Type I interferon inhibits antibody responses induced by a chimpanzee adenovirus vector. Mol Ther 2007;15(2):393-403