Neutralizing monoclonal antibodies protect against human adenovirus type 55 infection in transgenic mice and tree shrews

References

• Hierholzer JC, Pumarola A, Rodriguez-Torres A, et al. Occurrence of respiratory illness due to an atypical strain of adenovirus type 11 during a large outbreak in Spanish military recruits. Am J Epidemiol. 1974;99(6):434–442. doi:10.1093/oxfordjournals.aje.a121632
   PubMed Web of Science ®Google Scholar
• Chen SY, Liu W, Xu Y, et al. Epidemiology and genetic variabilities of human adenovirus type 55 reveal relative genome stability across time and geographic space in China. Front Microbiol. 2020;11:606195. doi:10.3389/fmicb.2020.606195
   PubMed Web of Science ®Google Scholar
• Hang J, Kajon AE, Graf PCF, et al. Human adenovirus type 55 distribution, regional persistence, and genetic variability. Emerg Infect Dis. 2020;26(7):1497–1505. doi:10.3201/eid2607.191707
   PubMed Web of Science ®Google Scholar
• Liu MC, Xu Q, Li TT, et al. Prevalence of human infection with respiratory adenovirus in China: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2023;17(2):e0011151.
   PubMed Web of Science ®Google Scholar
• Yoo H, Gu SH, Jung J, et al. Febrile respiratory illness associated with Human Adenovirus Type 55 in South Korea Military, 2014-2016. Emerg Infect Dis. 2017;23(6):1016–1020. doi:10.3201/eid2306.161848
   PubMed Web of Science ®Google Scholar
• Heo JY, Noh JY, Jeong HW, et al. Molecular epidemiology of Human Adenovirus-associated febrile respiratory illness in soldiers, South Korea. Emerg Infect Dis. 2018;24(7):1221–1227. doi:10.3201/eid2407.171222
   PubMed Web of Science ®Google Scholar
• Park SY, Ko JH, Monoldorova S, et al. Seroprevalence of neutralizing antibodies against human adenovirus type 55 in the South Korean military, 2018-2019. PLoS One. 2020;15(7):e0236040.
   PubMed Web of Science ®Google Scholar
• Gu L, Qu J, Sun B, et al. Sustained viremia and high viral load in respiratory tract secretions are predictors for death in immunocompetent adults with adenovirus pneumonia. PLoS One. 2016;11(8):e0160777.
   PubMed Web of Science ®Google Scholar
• Zhang D, Chen Y, Shi T, et al. Severe pneumonia caused by human adenovirus type 55 in children. Front Pediatr. 2022;10:1002052. doi:10.3389/fped.2022.1002052
   PubMedGoogle Scholar
• Zhang SY, Luo Y-P, Huang D-D, et al. Fatal pneumonia cases caused by human adenovirus 55 in immunocompetent adults. Infect Dis (Lond). 2016;48(1):40–47. doi:10.3109/23744235.2015.1055585
   PubMed Web of Science ®Google Scholar
• Jing S, Zhang J, Cao M, et al. Household transmission of human adenovirus type 55 in case of fatal acute respiratory disease. Emerg Infect Dis. 2019;25(9):1756–1758. doi:10.3201/eid2509.181937
   PubMed Web of Science ®Google Scholar
• Park JY, Kim BJ, Lee EJ, et al. Clinical features and courses of adenovirus pneumonia in healthy young adults during an outbreak among Korean military personnel. PLoS One. 2017;12(1):e0170592.
   PubMed Web of Science ®Google Scholar
• Chmielewicz B, Benzler J, Pauli G, et al. Respiratory disease caused by a species B2 adenovirus in a military camp in Turkey. J Med Virol. 2005;77(2):232–237. doi:10.1002/jmv.20441
   PubMed Web of Science ®Google Scholar
• Salama M, Amitai Z, Nutman A, et al. Outbreak of adenovirus type 55 infection in Israel. J Clin Virol. 2016;78:31–35. doi:10.1016/j.jcv.2016.03.002
   PubMed Web of Science ®Google Scholar
• Lafolie J, et al. Severe pneumonia associated with adenovirus type 55 infection, France, 2014. Emerg Infect Dis. 2016;22(11):2012–2014.
   PubMed Web of Science ®Google Scholar
• Sun B, He H, Wang Z, et al. Emergent severe acute respiratory distress syndrome caused by adenovirus type 55 in immunocompetent adults in 2013: a prospective observational study. Crit Care. 2014;18(4):456. doi:10.1186/s13054-014-0456-6
   PubMed Web of Science ®Google Scholar
• Dodge MJ, MacNeil KM, Tessier TM, et al. Emerging antiviral therapeutics for human adenovirus infection: recent developments and novel strategies. Antiviral Res. 2021;188:105034. doi:10.1016/j.antiviral.2021.105034
   PubMed Web of Science ®Google Scholar
• Struble EB, Rawson JMO, Stantchev T, et al. Uses and challenges of antiviral polyclonal and monoclonal antibody therapies. Pharmaceutics. 2023;15(5):1538. doi:10.3390/pharmaceutics15051538
   PubMed Web of Science ®Google Scholar
• Yuan Y, Jiao B, Qu L, et al. The development of COVID-19 treatment. Front Immunol. 2023;14:1125246. doi:10.3389/fimmu.2023.1125246
   PubMedGoogle Scholar
• Feng Y, et al. Human desmoglein-2 and human CD46 mediate human adenovirus type 55 infection, but human desmoglein-2 plays the major roles. J Virol. 2020;94(17):e00747–20.
   PubMed Web of Science ®Google Scholar
• Stasiak AC, Stehle T. Human adenovirus binding to host cell receptors: a structural view. Med Microbiol Immunol. 2020;209(3):325–333. doi:10.1007/s00430-019-00645-2
   PubMed Web of Science ®Google Scholar
• Scherer J, Yi J, Vallee RB. Role of cytoplasmic dynein and kinesins in adenovirus transport. FEBS Lett. 2020;594(12):1838–1847.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Bradley RR, Lynch DM, Iampietro MJ, et al. Adenovirus serotype 5 neutralizing antibodies target both hexon and fiber following vaccination and natural infection. J Virol. 2012;86(1):625–629. doi:10.1128/JVI.06254-11
   PubMed Web of Science ®Google Scholar
• Bradley RR, Maxfield LF, Lynch DM, et al. Adenovirus serotype 5-specific neutralizing antibodies target multiple hexon hypervariable regions. J Virol. 2012;86(2):1267–1272. doi:10.1128/JVI.06165-11
   PubMed Web of Science ®Google Scholar
• Feng Y, Sun X, Ye X, et al. Hexon and fiber of adenovirus type 14 and 55 are major targets of neutralizing antibody but only fiber-specific antibody contributes to cross-neutralizing activity. Virology. 2018;518:272–283. doi:10.1016/j.virol.2018.03.002
   PubMed Web of Science ®Google Scholar
• Chen L, Lu J, Yue J, et al. A humanized anti-human adenovirus 55 monoclonal antibody with good neutralization ability. Front Immunol. 2023;14:1132822. doi:10.3389/fimmu.2023.1132822
   PubMed Web of Science ®Google Scholar
• Tian X, Fan Y, Liu ZW, et al. Broadly neutralizing monoclonal antibodies against human adenovirus types 55, 14p, 7, and 11 generated with recombinant type 11 fiber knob. Emerg Microbes Infect. 2018;7(1):206.
   PubMedGoogle Scholar
• Smith JG, Cassany A, Gerace L, et al. Neutralizing antibody blocks adenovirus infection by arresting microtubule-dependent cytoplasmic transport. J Virol. 2008;82(13):6492–6500. doi:10.1128/JVI.00557-08
   PubMed Web of Science ®Google Scholar
• McEwan WA, Hauler F, Williams CR, et al. Regulation of virus neutralization and the persistent fraction by TRIM21. J Virol. 2012;86(16):8482–8491. doi:10.1128/JVI.00728-12
   PubMed Web of Science ®Google Scholar
• Varghese R, Mikyas Y, Stewart PL, et al. Postentry neutralization of adenovirus type 5 by an antihexon antibody. J Virol. 2004;78(22):12320–12332. doi:10.1128/JVI.78.22.12320-12332.2004
   PubMed Web of Science ®Google Scholar
• Walsh MP, Seto J, Jones MS, et al. Computational analysis identifies human adenovirus type 55 as a re-emergent acute respiratory disease pathogen. J Clin Microbiol. 2010;48(3):991–993. doi:10.1128/JCM.01694-09
   PubMed Web of Science ®Google Scholar
• Tian X, Fan Y, Wang C, et al. Seroprevalence of neutralizing antibodies against six human adenovirus types indicates the low level of herd immunity in young children from Guangzhou, China. Virol Sin. 2021;36(3):373–381. doi:10.1007/s12250-020-00307-1
   PubMed Web of Science ®Google Scholar
• Zheng XH, Rong X, Feng Y, et al. Seroprevalence of neutralizing antibodies against adenovirus type 14 and 55 in healthy adults in Southern China. Emerg Microbes Infect. 2017;6(6):e43.
   PubMedGoogle Scholar
• Sumida SM, Truitt DM, Lemckert AAC, et al. Neutralizing antibodies to adenovirus serotype 5 vaccine vectors are directed primarily against the adenovirus hexon protein. J Immunol. 2005;174(11):7179–7185. doi:10.4049/jimmunol.174.11.7179
   PubMed Web of Science ®Google Scholar
• Sundling C, Li Y, Huynh N, et al. High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci Transl Med. 2012;4(142):142ra96.
   PubMed Web of Science ®Google Scholar
• Meng W, Pan W, Zhang AJX, et al. Rapid generation of human-like neutralizing monoclonal antibodies in urgent preparedness for influenza pandemics and virulent infectious diseases. PLoS One. 2013;8(6):e66276. doi:10.1371/journal.pone.0066276
   PubMed Web of Science ®Google Scholar
• Zhang Q, Gui M, Niu X, et al. Potent neutralizing monoclonal antibodies against Ebola virus infection. Sci Rep. 2016;6:25856. doi:10.1038/srep25856
   PubMed Web of Science ®Google Scholar
• Li X, Zhou Z, Liu W, et al. Chinese tree shrew: a permissive model for in vitro and in vivo replication of human adenovirus species B. Emerg Microbes Infect. 2021;10(1):424–438. doi:10.1080/22221751.2021.1895679
   PubMed Web of Science ®Google Scholar
• Zhang F, Wang L, Niu X, et al. Phenotypic characterization of Chinese rhesus macaque plasmablasts for cloning antigen-specific monoclonal antibodies. Front Immunol. 2019;10:2426. doi:10.3389/fimmu.2019.02426
   PubMed Web of Science ®Google Scholar
• Brochet X, Lefranc MP, Giudicelli V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 2008;36(Web Server issue):W503–W508.
   PubMedGoogle Scholar
• Giudicelli V, Brochet X, Lefranc MP. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb Protoc. 2011;2011(6):695–715.
   PubMedGoogle Scholar
• Liu X, Qu L, Ye X, et al. Incorporation of NS1 and prM/M are important to confer effective protection of adenovirus-vectored Zika virus vaccine carrying E protein. NPJ Vaccines. 2018;3:29. doi:10.1038/s41541-018-0072-6
   PubMed Web of Science ®Google Scholar
• Havenga M, Vogels R, Zuijdgeest D, et al. Novel replication-incompetent adenoviral B-group vectors: high vector stability and yield in PER.C6 cells. J Gen Virol. 2006;87(Pt 8):2135–2143. doi:10.1099/vir.0.81956-0
   PubMedGoogle Scholar
• Dallaire F, Schreiner S, Blair GE, et al. The human adenovirus type 5 E4orf6/E1B55K E3 ubiquitin ligase complex enhances E1A functional activity. mSphere. 2016;1(1).
   Web of Science ®Google Scholar
• Woo JL, Berk AJ. Adenovirus ubiquitin-protein ligase stimulates viral late mRNA NuclearExport. J Virol. 2007;81(2):575–587. doi:10.1128/JVI.01725-06
   PubMed Web of Science ®Google Scholar
• Wohlfart C. Neutralization of adenoviruses: kinetics, stoichiometry, and mechanisms. J Virol. 1988;62(7):2321–2328. doi:10.1128/jvi.62.7.2321-2328.1988
   PubMed Web of Science ®Google Scholar
• Feng Y, Yuan M, Powers JM, et al. Broadly neutralizing antibodies against sarbecoviruses generated by immunization of macaques with an AS03-adjuvanted COVID-19 vaccine. Sci Transl Med. 2023;15(695):eadg7404. doi:10.1126/scitranslmed.adg7404
   PubMed Web of Science ®Google Scholar
• Yang Z, Dam K-MA, Bridges MD, et al. Neutralizing antibodies induced in immunized macaques recognize the CD4-binding site on an occluded-open HIV-1 envelope trimer. Nat Commun. 2022;13(1):732. doi:10.1038/s41467-022-28424-3
   PubMed Web of Science ®Google Scholar
• Yu H, Liu B, Zhang Y, et al. Somatically hypermutated antibodies isolated from SARS-CoV-2 Delta infected patients cross-neutralize heterologous variants. Nat Commun. 2023;14(1):1058. doi:10.1038/s41467-023-36761-0
   PubMed Web of Science ®Google Scholar
• Lu J, Wang R, Huang Y, et al. A novel human monoclonal antibody potently neutralizes human adenovirus serotype 7 by primarily targeting the adenovirus hexon protein. Virology. 2020;543:20–26. doi:10.1016/j.virol.2019.12.005
   PubMed Web of Science ®Google Scholar
• Abboud N, Casadevall A. Immunogenicity of Bacillus anthracis protective antigen domains and efficacy of elicited antibody responses depend on host genetic background. Clin Vaccine Immunol. 2008;15(7):1115–1123. doi:10.1128/CVI.00015-08
   PubMed Web of Science ®Google Scholar
• Pusnik J, Monzon-Posadas WO, Zorn J, et al. SARS-CoV-2 humoral and cellular immunity following different combinations of vaccination and breakthrough infection. Nat Commun. 2023;14(1):572. doi:10.1038/s41467-023-36250-4
   PubMed Web of Science ®Google Scholar
• Yuseff MI, Pierobon P, Reversat A, et al. How B cells capture, process and present antigens: a crucial role for cell polarity. Nat Rev Immunol. 2013;13(7):475–486. doi:10.1038/nri3469
   PubMed Web of Science ®Google Scholar
• Wohlfart CE, Svensson UK, Everitt E. Interaction between HeLa cells and adenovirus type 2 virions neutralized by different antisera. J Virol. 1985;56(3):896–903. doi:10.1128/jvi.56.3.896-903.1985
   PubMed Web of Science ®Google Scholar
• Jennings MR, Parks RJ. Human adenovirus gene expression and replication is regulated through dynamic changes in nucleoprotein structure throughout infection. Viruses. 2023;15(1):161. doi:10.3390/v15010161
   PubMed Web of Science ®Google Scholar