Prolonged Prophylactic Protection from Botulism with a Single Adenovirus Treatment Promoting Serum Expression of a VHH-Based Antitoxin Protein
Open accessAbstract
Current therapies for most acute toxin exposures are limited to administration of polyclonal antitoxin serum. We have shown that VHH-based neutralizing agents (VNAs) consisting of two or more linked, toxin-neutralizing heavy-chain-only VH domains (VHHs), each binding distinct epitopes, can potently protect animals from lethality in several intoxication models including Botulinum neurotoxin serotype A1 (BoNT/A1). Appending a 14 amino acid albumin binding peptide (ABP) to an anti-BoNT/A1 heterodimeric VNA (H7/B5) substantially improved serum stability and resulted in an effective VNA serum half-life of 1 to 2 days. A recombinant, replication-incompetent, adenoviral vector (Ad/VNA-BoNTA) was engineered that induces secretion of biologically active VNA, H7/B5/ABP (VNA-BoNTA), from transduced cells. Mice administered a single dose of Ad/VNA-BoNTA, or a different Ad/VNA, via different administration routes led to a wide range of VNA serum levels measured four days later; generally intravenous > intraperitoneal > intramuscular > subcutaneous. Ad/VNA-BoNTA treated mice were 100% protected from 10 LD50 of BoNT/A1 for more than six weeks and protection positively correlated with serum levels of VNA-BoNTA exceeding about 5 ng/ml. Some mice developed antibodies that inhibited VNA binding to target but these mice displayed no evidence of kidney damage due to deposition of immune complexes. Mice were also successfully protected from 10 LD50 BoNT/A1 when Ad/VNA-BoNTA was administered up to 1.5 hours post-intoxication, demonstrating rapid appearance of the protective VNA in serum following treatment. Genetic delivery of VNAs promises to be an effective method of providing prophylactic protection and/or acute treatments for many toxin-mediated diseases.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
VNAs with an estimated serum half-life of 1-2 days (with albumin-binding) should benefit from being encoded by mRNA (Mukherjee et al, 2014).
“Accordingly, VNAs with an estimated serum half‐life of 1–2 days (with albumin‐binding) should benefit from being encoded by mRNA (Mukherjee et al, 2014).”
From mRNA mediates passive vaccination against infectious agents, toxins, and tumors (2017) · cites this paper as Mukherjee et al, 2014
The Discussion (page not provided) estimates a 1–2-day serum half-life for the albumin-binding VNA in mice and says continuous genetic expression can improve VNA serum levels. The Introduction mentions RNA as a possible delivery vehicle, but the study tested adenoviral DNA delivery, not mRNA-encoded VNAs; it does not establish the claimed benefit of mRNA encoding. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe use of parenterally administered VNAs that potently neutralize botulinum neurotoxin serotype A (BoNT/A) has been previously reported.
“The use of parenterally administered VNAs that potently neutralize botulinum neurotoxin serotype A (BoNT/A) has been previously reported (Mukherjee et al, 2014).”
From mRNA mediates passive vaccination against infectious agents, toxins, and tumors (2017) · cites this paper as Mukherjee et al, 2014
For both VNAs, serum half-lives were calculated to be in the range of 24-36 h.
“For both VNAs, serum half‐lives were calculated to be in the range of 24–36 h which is in line with a previous report (Mukherjee et al, 2014).”
From mRNA mediates passive vaccination against infectious agents, toxins, and tumors (2017) · cites this paper as Mukherjee et al, 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Characteristics of a human cell line transformed by DNA from human adenovirus type 5
Graham, F. L., Russell, W. C., Smiley, J., & Nairn, R. (1977) · Journal of General Virology · doi:10.1099/0022-1317-36-1-59 · Cited by 4,793 · see citing works
A simplified system for generating recombinant adenoviruses
He, T., Zhou, S., da Costa, L. T., Yu, J., Kinzler, K. W., & Vogelstein, B. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.5.2509 · Cited by 3,209 · see citing works
Nanobodies: natural single-domain antibodies
Muyldermans, S. (2013) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-063011-092449 · Cited by 2,304 · see citing works
The polypeptides of adenovirus
Maizel, J. V., WHITE, D. O., & Scharff, M. D. (1968) · Virology · doi:10.1016/0042-6822(68)90121-9 · Cited by 883 · see citing works
A protocol for rapid generation of recombinant adenoviruses using the AdEasy system
Luo, J., Deng, Z.-L., Luo, X., Tang, N., Song, W.-X., Chen, J., Sharff, K. A., Luu, H. H., Haydon, R. C., Kinzler, K. W., et al. (2007) · Nature Protocols · doi:10.1038/nprot.2007.135 · Cited by 854 · see citing works
Strategies for extended serum half-life of protein therapeutics
Kontermann, R. E. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.06.012 · Cited by 576 · see citing works
Fallaux, F. J., Kranenburg, O., Cramer, S. J., Houweling, A., van Ormondt, H., Hoeben, R. C., & van der Eb, A. J. (1996) · Human Gene Therapy · doi:10.1089/hum.1996.7.2-215 · Cited by 512 · see citing works
Innate Immune Mechanisms Dominate Elimination of Adenoviral Vectors Following In Vivo Administration
Worgall, S., Wolff, G., Falck-Pedersen, E., & Crystal, R. G. (1997) · Human Gene Therapy · doi:10.1089/hum.1997.8.1-37 · Cited by 491 · see citing works
Lieber, A., He, C. Y., Meuse, L. A., Schowalter, D., Kirillova, I., Winther, B., & Kay, M. A. (1997) · Journal of Virology · doi:10.1128/jvi.71.11.8798-8807.1997 · Cited by 412 · see citing works
Stable antibody expression at therapeutic levels using the 2A peptide
Fang, J., Qian, J., Yi, S., Harding, T. C., Tu, G. H., VanRoey, M. J., & Jooss, K. U. (2005) · Nature Biotechnology · doi:10.1038/nbt1087 · Cited by 370 · see citing works
Nanobodies and Their Potential Applications
Hassanzadeh‐Ghassabeh, G., Devoogdt, N., Pauw, P. E. M. D., Vincke, C., & Muyldermans, S. (2013) · Nanomedicine · doi:10.2217/nnm.13.86 · Cited by 328 · see citing works
Tao, N., Gao, G., Parr, M. J., Johnston, J., Baradet, T. C., Wilson, J. M., Barsoum, J., & Fawell, S. E. (2001) · Molecular Therapy · doi:10.1006/mthe.2000.0227 · Cited by 321 · see citing works
Production of first generation adenovirus vectors: a review
Danthinne, X., & Imperiale, M. J. (2000) · Gene Therapy · doi:10.1038/sj.gt.3301301 · Cited by 230 · see citing works
Pharmacokinetics and biodistribution of genetically engineered antibodies
Batra, S. K., Jain, M., Wittel, U. A., Chauhan, S. C., & Colcher, D. M. (2002) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(02)00352-x · Cited by 218 · see citing works
Shayakhmetov, D. M., Li, Z.-Y., Ni, S., & Lieber, A. (2004) · Journal of Virology · doi:10.1128/jvi.78.10.5368-5381.2004 · Cited by 210 · see citing works
Wolff, G., Worgall, S., van Rooijen, N., Song, W., Harvey, B., & Crystal, R. G. (1997) · Journal of Virology · doi:10.1128/jvi.71.1.624-629.1997 · Cited by 210 · see citing works
Casadevall, A. (2002) · Emerging infectious diseases · doi:10.3201/eid0808.010516 · Cited by 164 · see citing works
Nguyen, A., Reyes, A. E., Zhang, M., McDonald, P., Wong, W., Damico, L. A., & Dennis, M. S. (2006) · Protein Engineering Design and Selection · doi:10.1093/protein/gzl011 · Cited by 141 · see citing works
Mátrai, J., Cantore, A., Bartholomae, C. C., Annoni, A., Wang, W., Acosta-Sanchez, A., Samara-Kuko, E., De Waele, L., Ma, L., Genovese, P., et al. (2011) · Hepatology · doi:10.1002/hep.24230 · Cited by 139 · see citing works
Annoni, A., Brown, B. D., Cantore, A., Sergi, L. S., Naldini, L., & Roncarolo, M. (2009) · Blood · doi:10.1182/blood-2009-04-214569 · Cited by 135 · see citing works
Monegal, A., Ami, D., Martinelli, C., Huang, H., Aliprandi, M., Capasso, P., Francavilla, C., Ossolengo, G., & de Marco, A. (2009) · Protein Engineering Design and Selection · doi:10.1093/protein/gzp002 · Cited by 131 · see citing works
Lewis, A. D., Chen, R., Montefiori, D. C., Johnson, P. R., & Clark, K. R. (2002) · Journal of Virology · doi:10.1128/jvi.76.17.8769-8775.2002 · Cited by 124 · see citing works
Antitoxins: novel strategies to target agents of bioterrorism
Rainey, G. J., & Young, J. A. T. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro977 · Cited by 109 · see citing works
Tremblay, J. M., Mukherjee, J., Leysath, C. E., Debatis, M. E., Ofori, K., Baldwin, K., Boucher, C., Peters, R., Beamer, G., Sheoran, A. S., et al. (2013) · Infection and Immunity · doi:10.1128/iai.01033-13 · Cited by 102 · see citing works
Self-citationFang, J., Yi, S., Simmons, A. D., Tu, G. H., Nguyen, M., Harding, T. C., VanRoey, M. J., & Jooss, K. U. (2007) · Molecular Therapy · doi:10.1038/sj.mt.6300142 · Cited by 98 · see citing works
Mukherjee, J., Tremblay, J. M., Leysath, C. E., Ofori, K., Baldwin, K., Feng, X., Bedenice, D., Webb, R. P., Wright, P. M., Smith, L. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029941 · Cited by 91 · see citing works
Self-citationAdenovirus Strategies for Tissue-Specific Targeting
Beatty, M. S., & Curiel, D. T. (2012) · Advances in cancer research · doi:10.1016/b978-0-12-398342-8.00002-1 · Cited by 71 · see citing works
Self-citationVance, D. J., Tremblay, J. M., Mantis, N. J., & Shoemaker, C. B. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.519207 · Cited by 70 · see citing works
Self-citationVerheesen, P., Roussis, A., de Haard, H., Groot, A. J., Stam, J. C., den Dunnen, J. T., Frants, R. R., Verkleij, A. J., Verrips, C. T., & van der Maarel, S. M. (2006) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2006.05.011 · Cited by 69 · see citing works
Zuber, C., Mitteregger, G., Schuhmann, N., Rey, C., Knackmuss, S. H. J., Rupprecht, W., Reusch, U., Pace, C., Little, M., Kretzschmar, H. A., et al. (2008) · Journal of General Virology · doi:10.1099/vir.0.83670-0 · Cited by 59 · see citing works
Improvements in adenoviral vector technology: overcoming barriers for gene therapy
Parks, R. J. (2000) · Clinical Genetics · doi:10.1034/j.1399-0004.2000.580101.x · Cited by 55 · see citing works
Genetic delivery of an anti-RSV antibody to protect against pulmonary infection with RSV
Skaricic, D., Traube, C., De, B., Joh, J., Boyer, J., Crystal, R. G., & Worgall, S. (2008) · Virology · doi:10.1016/j.virol.2008.04.016 · Cited by 54 · see citing works
Jiang, M., Shi, W., Zhang, Q., Wang, X., Guo, M., Cui, Z., Su, C., Yang, Q. K., Li, Y., Sham, J. S. T., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-0746 · Cited by 53 · see citing works
Sepúlveda, J., Mukherjee, J., Tzipori, S. R., Simpson, L. L., & Shoemaker, C. B. (2009) · Infection and Immunity · doi:10.1128/iai.01084-09 · Cited by 49 · see citing works
Self-citationAdenovirus technology for gene manipulation and functional studies
Wang, Y., & Huang, S. (2000) · Drug Discovery Today · doi:10.1016/s1359-6446(99)01433-6 · Cited by 49 · see citing works
Rapid/Sustained Anti-anthrax Passive Immunity Mediated by Co-administration of Ad/AAV
De, B. P., Hackett, N. R., Crystal, R. G., & Boyer, J. L. (2007) · Molecular Therapy · doi:10.1038/sj.mt.6300344 · Cited by 45 · see citing works
Utilizing adenovirus vectors for gene delivery in cancer
Kasala, D., Choi, J.-W., Kim, S. W., & Yun, C. (2014) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2014.874414 · Cited by 43 · see citing works
Baculovirus Expression of a Human G2-Specific, Neutralizing IgG Monoclonal Antibody to Puumala Virus
Liang, M., Guttieri, M. C., Lundkvist, Å., & Schmaljohn, C. S. (1997) · Virology · doi:10.1006/viro.1997.8695 · Cited by 38 · see citing works
A quantitative assay for measuring clearance of adenovirus vectors by Kupffer cells
Smith, J. S., Xu, Z., & Byrnes, A. P. (2007) · Journal of Virological Methods · doi:10.1016/j.jviromet.2007.08.009 · Cited by 38 · see citing works
High In Vivo Production of a Model Monoclonal Antibody on Adenoviral Gene Transfer
Noël, D., Pelegrín, M., Kramer, S., Jacquet, C., Skander, N., & Piechaczyk, M. (2002) · Human Gene Therapy · doi:10.1089/10430340260185111 · Cited by 35 · see citing works
Леонидовна, Т. И., Sedova, E. S., Gribova, I. Y., Ivanova, T. I., Vasilev, L. A., Rutovskaya, M. V., Lysenko, A. A., Шмаров, М. М., Logunov, D. Y., Naroditsky, B. S., et al. (2012) · Antiviral Research · doi:10.1016/j.antiviral.2012.12.021 · Cited by 34 · see citing works
Meng, Q., Garcia-Rodriguez, C., Manzanarez, G., Silberg, M. A., Conrad, F., Bettencourt, J. D., Pan, X., Breece, T., To, R., Li, M., et al. (2012) · Analytical Biochemistry · doi:10.1016/j.ab.2012.08.005 · Cited by 34 · see citing works
Kasuya, K., Boyer, J. L., Tan, Y., Alipui, D. O., Hackett, N. R., & Crystal, R. G. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2004.10.018 · Cited by 33 · see citing works
Sofer-Podesta, C., Ang, J., Hackett, N. R., Senina, S., Perlin, D. S., Crystal, R. G., & Boyer, J. L. (2009) · Infection and Immunity · doi:10.1128/iai.00856-08 · Cited by 33 · see citing works
Morimoto, K., Schnell, M. J., Pulmanausahakul, R., McGettigan, J. P., Foley, H. D., Faber, M., Hooper, D. C., & Dietzschold, B. (2001) · Journal of Immunological Methods · doi:10.1016/s0022-1759(01)00353-2 · Cited by 26 · see citing works
Pharmacological Interventions for Improving Adenovirus Usage in Gene Therapy
Haisma, H. J., & Bellu, A. R. (2010) · Molecular Pharmaceutics · doi:10.1021/mp100310h · Cited by 26 · see citing works
López‐Requena, A., Burrone, Ó. R., & Cesco-Gaspere, M. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00159 · Cited by 25 · see citing works
Affinity Maturation of Single-Domain Antibodies by Yeast Surface Display
Koide, A., & Koide, S. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-968-6_26 · Cited by 23 · see citing works
Current strategies for designing antidotes against botulinum neurotoxins
Patel, K. B., Cai, S., & Singh, B. R. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2014.884066 · Cited by 20 · see citing works
Generation and monitoring of cell lines producing humanized antibodies.
Losman, M. J., Qu, Z., Krishnan, I., Wang, J., Hansen, H. J., Goldenberg, D. M., & Leung, S. (1999) · PubMed · Cited by 5 · see citing works
Flagged first, then by citations
1 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Nanobodies as therapeutics: big opportunities for small antibodies
Steeland, S., Vandenbroucke, R. E., & Libert, C. (2016) · Drug Discovery Today · doi:10.1016/j.drudis.2016.04.003 · Cited by 462 · see citing works
mRNA mediates passive vaccination against infectious agents, toxins, and tumors
Thran, M., Mukherjee, J., Pönisch, M., Fiedler, K., Thess, A., Mui, B. L., Hope, M. J., Tam, Y. K., Horscroft, N., Heidenreich, R., et al. (2017) · EMBO Molecular Medicine · doi:10.15252/emmm.201707678 · Cited by 166 · see citing works
“The use of parenterally administered VNAs that potently neutralize botulinum neurotoxin serotype A (BoNT/A) has been previously reported (Mukherjee et al, 2014).”
BackgroundMethodResultInfluentialSelf-citationAn engineered enzyme that targets circulating lactate to alleviate intracellular NADH:NAD+ imbalance
Patgiri, A., Skinner, O. S., Miyazaki, Y., Schleifer, G., Marutani, E., Shah, H., Sharma, R., Goodman, R. P., To, T., Bao, X. R., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-019-0377-7 · Cited by 154 · see citing works
mRNA as novel technology for passive immunotherapy
Schlake, T., Theß, A., Thran, M., & Jordan, I. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2935-4 · Cited by 132 · see citing works
mRNA: A Novel Avenue to Antibody Therapy?
Schlake, T., Thran, M., Fiedler, K., Heidenreich, R., Petsch, B., & Fotin‐Mleczek, M. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.03.002 · Cited by 90 · see citing works
Godakova, S. A., Noskov, A. N., Vinogradova, I. D., Ugriumova, G. A., Solovyev, A. I., Esmagambetov, I. B., Ильдарович, Т. А., Logunov, D. Y., Naroditsky, B. S., Shcheblyakov, D. V., et al. (2019) · Toxins · doi:10.3390/toxins11080464 · Cited by 78 · see citing works
Mejías, M. P., Hiriart, Y., Lauché, C., Fernández‐Brando, R. J., Pardo, R., Bruballa, A. C., Ramos, M. V. C. C., Goldbaum, F. A., Palermo, M. S., & Zylberman, V. (2016) · Scientific Reports · doi:10.1038/srep24913 · Cited by 64 · see citing works
Huang, N.-J., Pishesha, N., Mukherjee, J., Zhang, S., Deshycka, R., Sudaryo, V., Dong, M., Shoemaker, C. B., & Lodish, H. F. (2017) · Nature Communications · doi:10.1038/s41467-017-00448-0 · Cited by 59 · see citing works
Self-citationState of play and clinical prospects of antibody gene transfer
Hollevoet, K., & Declerck, P. J. (2017) · Journal of Translational Medicine · doi:10.1186/s12967-017-1234-4 · Cited by 55 · see citing works
Schmidt, D., Beamer, G., Tremblay, J. M., Steele, J. A., Kim, H. B., Wang, Y., Debatis, M., Sun, X., Kashentseva, E. A., Dmitriev, I. P., et al. (2016) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00730-15 · Cited by 47 · see citing works
Self-citationLam, K. H., Tremblay, J. M., Vazquez-Cintron, E. J., Perry, K., Ondeck, C. A., Webb, R. P., McNutt, P. M., Shoemaker, C. B., & Jin, R. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.107 · Cited by 40 · see citing works
Self-citationMoayeri, M., Leysath, C. E., Tremblay, J. M., Vrentas, C. E., Crown, D., Leppla, S. H., & Shoemaker, C. B. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.627943 · Cited by 39 · see citing works
Self-citationHerrera, C., Tremblay, J. M., Shoemaker, C. B., & Mantis, N. J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.658070 · Cited by 36 · see citing works
Self-citationVrentas, C. E., Moayeri, M., Keefer, A. B., Greaney, A. J., Tremblay, J. M., O’Mard, D., Leppla, S. H., & Shoemaker, C. B. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.749184 · Cited by 35 · see citing works
Self-citationSingle Domain Antibody application in bacterial infection diagnosis and neutralization
Qin, Q., Liu, H., He, W., Guo, Y., Zhang, J., She, J., Zheng, F., Zhang, S., Muyldermans, S., & Wen, Y. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1014377 · Cited by 34 · see citing works
Tremblay, J. M., Vazquez-Cintron, E. J., Lam, K. H., Mukherjee, J., Bedenice, D., Ondeck, C. A., Conroy, M. T., Bodt, S. M. L., Winner, B. M., Webb, R. P., et al. (2020) · Toxins · doi:10.3390/toxins12100611 · Cited by 28 · see citing works
Self-citationHerrera, C., Klokk, T. I., Cole, R. W., Sandvig, K., & Mantis, N. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156893 · Cited by 28 · see citing works
Sheoran, A. S., Dmitriev, I. P., Kashentseva, E. A., Cohen, O., Mukherjee, J., Debatis, M. E., Shearer, J. P., Tremblay, J. M., Beamer, G., Curiel, D. T., et al. (2014) · Infection and Immunity · doi:10.1128/iai.02360-14 · Cited by 24 · see citing works
Self-citationNanobodies: The potential application in bacterial treatment and diagnosis
Yu, S., Zhang, L., Wang, A., Jin, Y., & Zhou, D. (2023) · Biochemical Pharmacology · doi:10.1016/j.bcp.2023.115640 · Cited by 24 · see citing works
Yang, Z., Shi, L., Yu, H., Zhang, Y., Chen, K. Y., Fleur, A. S., Bai, G., & Feng, H. (2016) · Pathogens and Disease · doi:10.1093/femspd/ftw078 · Cited by 23 · see citing works
Moayeri, M., Tremblay, J. M., Debatis, M. E., Dmitriev, I. P., Kashentseva, E. A., Yeh, A. J., Cheung, G. Y. C., Curiel, D. T., Leppla, S. H., & Shoemaker, C. B. (2016) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00611-15 · Cited by 22 · see citing works
Self-citationMukherjee, J., Ondeck, C. A., Tremblay, J. M., Archer, J. F., Debatis, M. E., Foss, A. D., Awata, J., Erasmus, J. H., McNutt, P. M., & Shoemaker, C. B. (2022) · Scientific Reports · doi:10.1038/s41598-022-15876-2 · Cited by 19 · see citing works
Self-citationHeat-Labile Enterotoxin IIa, a Platform To Deliver Heterologous Proteins into Neurons
Chen, C., Przedpelski, A., Tepp, W. H., Pellett, S., Johnson, E. A., & Barbieri, J. T. (2015) · mBio · doi:10.1128/mbio.00734-15 · Cited by 18 · see citing works
Egorova, D. A., Sv, T., Shcheblyakov, D. V., Dolzhikova, I. V., Щербинин, Д. Н., Zubkova, O. V., Ivanova, T. I., Ильдарович, Т. А., Шмаров, М. М., Logunov, D. Y., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150958 · Cited by 18 · see citing works
rAAV expressing recombinant neutralizing antibody for the botulinum neurotoxin type A prophylaxis
Derkaev, A. A., Ryabova, E. I., Esmagambetov, I. B., Shcheblyakov, D. V., Godakova, S. A., Vinogradova, I. D., Noskov, A. N., Logunov, D. Y., Naroditsky, B. S., & Al, G. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.960937 · Cited by 15 · see citing works
Thran, M., Poenisch, M., Danz, H., Horscroft, N., Ichtchenko, K., Tzipori, S. R., & Shoemaker, C. B. (2023) · Scientific Reports · doi:10.1038/s41598-023-41092-7 · Cited by 10 · see citing works
Self-citationVermeire, G., Smidt, E. D., Casteels, P., Geukens, N., Declerck, P. J., & Hollevoet, K. (2020) · Cancer Gene Therapy · doi:10.1038/s41417-020-0204-9 · Cited by 8 · see citing works
Ganji, A., Islami, M., Ejtehadifar, M., Zarei-Mehrvarz, E., & Darvish, M. (2019) · Reviews in Medical Microbiology · doi:10.1097/mrm.0000000000000175 · Cited by 8 · see citing works
Phagocytic clearance of targeted cells with a synthetic ligand
Yamato, Y., & Suzuki, J. (2025) · Nature Biomedical Engineering · doi:10.1038/s41551-025-01483-9 · Cited by 4 · see citing works
Botulinum toxin: Bio Warfare Agent and Vaccine Development
Sharma, A. (2021) · Clinical Research and Trials · doi:10.15761/crt.1000348 · Cited by 4 · see citing works
Vaccine delivery strategies against botulism
Yan, Y., Díaz-Arévalo, D., Wang, H., Chen, Y., & Zeng, M. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-821222-6.00009-9 · Cited by 2 · see citing works
Mukherjee, J., Tremblay, J. M., Debatis, M. E., Foss, A. D., Awata, J., & Shoemaker, C. B. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.02.433625
Self-citationChandel, N. S. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737201527.793569961
VHH engineering and utilization for blood-brain barrier transport and anti-infectious diseases
Pérez, J. F., Asano, R., Uto, Y., Tsumoto, K., & Nakakido, M. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-29808-0.00069-8
Chu, Y., Wang, X., Hua, Y., Chen, Q., Li, C., Zhang, H., Liu, N., Wang, Z. D., Zhao, Z., & Zheng, A. (2026) · ACS Applied Bio Materials · doi:10.1021/acsabm.6c00848
- Authors
- Mukherjee, J., Dmitriev, I., Debatis, M., Tremblay, J. M., Beamer, G., Kashentseva, E. A., Curiel, D. T., & Shoemaker, C. B.
- Affiliations
- Tufts University (US)
- Washington University in St. Louis (US)
- Corresponding author
- Shoemaker, Charles B.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2014-08-29
- Volume
- 9
- Issue
- 8
- Pages
- e106422
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4149568
- OpenAlex
- W1978487895
- Cited by
- 37
- References
- 51
- Citations by year
- 2026: 1 · 2025: 2 · 2023: 2 · 2022: 4 · 2021: 2 · 2020: 6 · 2019: 3 · 2018: 1 · 2017: 3 · 2016: 9 · 2015: 3 · 2014: 1
- FWCI
- 3.48
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health (R21/R33, AI057159)
- National Institute of Allergy and Infectious Diseases (AI057159, AI101403, U54AI057159, R21AI101403, R21/R33 AI101403)
- Topics
- Health Sciences › Medicine › Neurology › Botulinum Toxin and Related Neurological Disorders
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Monoclonal and Polyclonal Antibodies Research
- Life Sciences › Immunology and Microbiology › Immunology › Toxin Mechanisms and Immunotoxins
- Keywords
- botulism, nanobodies, adenoviral vector, recombinant protein delivery, serum half-life, prophylactic protection, toxin neutralization, immune complex deposition, toxin-mediated disease
- MeSH terms
- Dependovirus, Animals, Botulinum Antitoxin, Botulism, Disease Models, Animal, Genetic Vectors, Vaccination, Mice, Antibodies, Neutralizing
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review