Changing the adenovirus fiber for retaining gene delivery efficacy in the presence of neutralizing antibodies
Prior infection has primed most adult humans for a rapid neutralizing antibody (NAb) response when re-exposed to adenovirus. NAb induction can severely limit the efficacy of systemic re-administration of adenoviral gene therapy. We hypothesized that changing the fiber knob could overcome NAb. Immune...
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Published in | Gene therapy Vol. 15; no. 12; pp. 921 - 929 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
01.06.2008
Nature Publishing Group |
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Abstract | Prior infection has primed most adult humans for a rapid neutralizing antibody (NAb) response when re-exposed to adenovirus. NAb induction can severely limit the efficacy of systemic re-administration of adenoviral gene therapy. We hypothesized that changing the fiber knob could overcome NAb. Immune-competent mice were exposed to serotype 5 adenovirus (Ad5)(GL), Ad5/3luc1, Ad5lucRGD or Ad5pK7(GL). Mice immunized with Ad5(GL) featured reduced intravenous Ad5(GL) gene transfer to most organs, including the liver, lung and spleen. Ad5(GL) gene transfer was affected much less by exposure to capsid-modified viruses. Anti-Ad5(GL) NAb blocked intravenous Ad5(GL) gene transfer to orthotopic lung cancer xenografts, whereas capsid-modified viruses were not affected. When gene transfer to fresh cancer and normal lung explants was analyzed, we found that capsid-modified viruses allowed effective gene delivery to tumors in the presence of anti-Ad5(GL) NAb, whereas Ad5(GL) was blocked. In contrast, crossblocking by NAbs induced by different viruses affected gene delivery to normal human lung explants, suggesting the importance of non-fiber-knob-mediated infection mechanisms. We conclude that changing the adenovirus fiber knob is sufficient to allow a relative degree of escape from preexisting NAb. If confirmed in trials, this approach might improve the efficacy of re-administration of adenoviral gene therapy to humans. |
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AbstractList | Prior infection has primed most adult humans for a rapid neutralizing antibody (NAb) response when re-exposed to adenovirus. NAb induction can severely limit the efficacy of systemic re-administration of adenoviral gene therapy. We hypothesized that changing the fiber knob could overcome NAb. Immune-competent mice were exposed to serotype 5 adenovirus (Ad5)(GL), Ad5/3luc1, Ad5lucRGD or Ad5pK7(GL). Mice immunized with Ad5(GL) featured reduced intravenous Ad5(GL) gene transfer to most organs, including the liver, lung and spleen. Ad5(GL) gene transfer was affected much less by exposure to capsid-modified viruses. Anti-Ad5(GL) NAb blocked intravenous Ad5(GL) gene transfer to orthotopic lung cancer xenografts, whereas capsid-modified viruses were not affected. When gene transfer to fresh cancer and normal lung explants was analyzed, we found that capsid-modified viruses allowed effective gene delivery to tumors in the presence of anti-Ad5(GL) NAb, whereas Ad5(GL) was blocked. In contrast, crossblocking by NAbs induced by different viruses affected gene delivery to normal human lung explants, suggesting the importance of non-fiber-knob-mediated infection mechanisms. We conclude that changing the adenovirus fiber knob is sufficient to allow a relative degree of escape from preexisting NAb. If confirmed in trials, this approach might improve the efficacy of re-administration of adenoviral gene therapy to humans. Prior infection has primed most adult humans for a rapid neutralizing antibody (NAb) response when re-exposed to adenovirus. NAb induction can severely limit the efficacy of systemic re-administration of adenoviral gene therapy. We hypothesized that changing the fiber knob could overcome NAb. Immune-competent mice were exposed to serotype 5 adenovirus (Ad5)(GL), Ad5/3luc1, Ad5lucRGD or Ad5pK7(GL). Mice immunized with Ad5(GL) featured reduced intravenous Ad5(GL) gene transfer to most organs, including the liver, lung and spleen. Ad5(GL) gene transfer was affected much less by exposure to capsid-modified viruses. Anti-Ad5(GL) NAb blocked intravenous Ad5(GL) gene transfer to orthotopic lung cancer xenografts, whereas capsid-modified viruses were not affected. When gene transfer to fresh cancer and normal lung explants was analyzed, we found that capsid-modified viruses allowed effective gene delivery to tumors in the presence of anti-Ad5(GL) NAb, whereas Ad5(GL) was blocked. In contrast, crossblocking by NAbs induced by different viruses affected gene delivery to normal human lung explants, suggesting the importance of non-fiber-knob-mediated infection mechanisms. We conclude that changing the adenovirus fiber knob is sufficient to allow a relative degree of escape from preexisting NAb. If confirmed in trials, this approach might improve the efficacy of re-administration of adenoviral gene therapy to humans. [PUBLICATION ABSTRACT] Prior infection has primed most adult humans for a rapid neutralizing antibody (NAb) response when re-exposed to adenovirus. NAb induction can severely limit the efficacy of systemic re-administration of adenoviral gene therapy. We hypothesized that changing the fiber knob could overcome NAb. Immune-competent mice were exposed to serotype 5 adenovirus (Ad5)(GL), Ad5/3luc1, Ad5lucRGD or Ad5pK7(GL). Mice immunized with Ad5(GL) featured reduced intravenous Ad5(GL) gene transfer to most organs, including the liver, lung and spleen. Ad5(GL) gene transfer was affected much less by exposure to capsid-modified viruses. Anti-Ad5(GL) NAb blocked intravenous Ad5(GL) gene transfer to orthotopic lung cancer xenografts, whereas capsid-modified viruses were not affected. When gene transfer to fresh cancer and normal lung explants was analyzed, we found that capsid-modified viruses allowed effective gene delivery to tumors in the presence of anti-Ad5(GL) NAb, whereas Ad5(GL) was blocked. In contrast, crossblocking by NAbs induced by different viruses affected gene delivery to normal human lung explants, suggesting the importance of non-fiber-knob-mediated infection mechanisms. We conclude that changing the adenovirus fiber knob is sufficient to allow a relative degree of escape from preexisting NAb. If confirmed in trials, this approach might improve the efficacy of re-administration of adenoviral gene therapy to humans. Gene Therapy (2008) 15, 921-929; doi: 10.1038/gt.2008.56; published online 10 April 2008 Keywords: cancer; neutralizing antibody; oncolytic adenovirus; seroswitching |
Audience | Academic |
Author | Kanerva, A Särkioja, M Ahonen, M T Raki, M Salo, J Hakkarainen, T Hemminki, A Pesonen, S |
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CitedBy_id | crossref_primary_10_1021_mp100219n crossref_primary_10_1158_1078_0432_CCR_09_3167 crossref_primary_10_1038_gt_2010_17 crossref_primary_10_1158_1078_0432_CCR_13_1471 crossref_primary_10_1186_s40425_016_0121_5 crossref_primary_10_1371_journal_pone_0182715 crossref_primary_10_1016_j_jconrel_2011_06_014 crossref_primary_10_1517_14712590903307388 crossref_primary_10_1038_mto_2014_2 crossref_primary_10_1038_nrmicro3140 crossref_primary_10_1038_s41417_020_00226_z crossref_primary_10_2217_fvl_10_59 crossref_primary_10_1016_j_vaccine_2008_12_051 crossref_primary_10_1016_j_molmed_2012_04_008 crossref_primary_10_3390_v14122727 crossref_primary_10_1002_jgm_1565 crossref_primary_10_1038_s41598_018_30947_z crossref_primary_10_1089_hum_2018_240 crossref_primary_10_1158_1078_0432_CCR_12_2546 crossref_primary_10_1038_cgt_2010_79 crossref_primary_10_1038_gt_2011_54 crossref_primary_10_1080_2162402X_2016_1265717 crossref_primary_10_3390_v7112923 crossref_primary_10_3390_v2102196 crossref_primary_10_1038_mt_2011_113 crossref_primary_10_1021_mp1002174 crossref_primary_10_1016_j_addr_2020_10_017 crossref_primary_10_1021_acsnano_6b06182 crossref_primary_10_1517_14712590903187053 |
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Keywords | seroswitching neutralizing antibody oncolytic adenovirus cancer Virus Adenoviridae Antibody Malignant tumor Gene therapy Vector Cancer |
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7 M Hashimoto (BFgt200856_CR13) 2005; 73 Y Chen (BFgt200856_CR8) 2000; 11 A Hemminki (BFgt200856_CR14) 2001; 4 H Gahery-Segard (BFgt200856_CR11) 1998; 72 D Stone (BFgt200856_CR37) 2005; 79 F Lemiale (BFgt200856_CR38) 2007; 25 NS Ihrcke (BFgt200856_CR33) 1993; 14 S Ni (BFgt200856_CR21) 2006; 13 DM McDonald (BFgt200856_CR32) 2003; 9 DS Bangari (BFgt200856_CR7) 2006; 6 A Hemminki (BFgt200856_CR25) 2002; 13 A Hemminki (BFgt200856_CR15) 2002; 94 A Hemminki (BFgt200856_CR28) 2003; 7 M Sarkioja (BFgt200856_CR23) 2006; 107 DM Roberts (BFgt200856_CR36) 2006; 441 A Immonen (BFgt200856_CR1) 2004; 10 AM Crompton (BFgt200856_CR5) 2007; 7 A Kanerva (BFgt200856_CR19) 2005; 37 A Kanerva (BFgt200856_CR24) 2002; 8 TA Smith (BFgt200856_CR30) 2003; 14 J Gall (BFgt200856_CR35) 1996; 70 A Kanerva (BFgt200856_CR17) 2003; 8 Z Peng (BFgt200856_CR2) 2005; 16 M Raki (BFgt200856_CR6) 2006; 14 N Shinoura (BFgt200856_CR18) 1999; 59 TA Smith (BFgt200856_CR29) 2003; 14 |
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Snippet | Prior infection has primed most adult humans for a rapid neutralizing antibody (NAb) response when re-exposed to adenovirus. NAb induction can severely limit... |
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SubjectTerms | Adenoviridae - genetics Adenoviruses Anesthesia. Intensive care medicine. Transfusions. Cell therapy and gene therapy Animals Antibodies Antibodies, Viral - immunology Antigens, Viral - genetics Antigens, Viral - immunology Applied cell therapy and gene therapy Biological and medical sciences Biomedical and Life Sciences Biomedicine Biotechnology Cancer Capsid Proteins - genetics Carcinoma, Non-Small-Cell Lung - therapy Care and treatment Cell Biology Development and progression Explants Fundamental and applied biological sciences. Psychology Gene Expression Gene Therapy Gene transfer Genetic aspects Genetic Engineering Genetic Therapy - methods Genetic Vectors - administration & dosage Genetic Vectors - genetics Health aspects Health. Pharmaceutical industry Human Genetics Humans Immunology Industrial applications and implications. Economical aspects Infections Intravenous administration Lung - immunology Lung - virology Lung cancer Lung Neoplasms - immunology Lung Neoplasms - therapy Medical sciences Mice Mice, Inbred ICR Mice, Nude Nanotechnology original-article Patient outcomes Rodents Spleen Transduction, Genetic Transfusions. Complications. Transfusion reactions. Cell and gene therapy Tumors Viral antibodies Viruses Xenograft Model Antitumor Assays Xenografts |
Title | Changing the adenovirus fiber for retaining gene delivery efficacy in the presence of neutralizing antibodies |
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