1,861
Views
2
CrossRef citations to date
0
Altmetric
Review Article - Invited

Pathogenicity and virulence of human adenovirus F41: Possible links to severe hepatitis in children

Article: 2242544 | Received 16 May 2023, Accepted 25 Jul 2023, Published online: 06 Aug 2023

References

  • Rowe WP, Huebner RJ, Gilmore LK, et al. Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc Soc Exp Biol Med. 1953;84(3):570–21. doi: 10.3181/00379727-84-20714
  • Aoki K, Benkö M, Davison AJ, et al. Toward an integrated human adenovirus designation system that utilizes molecular and serological data and serves both clinical and fundamental virology.J Virol. 2011;85(11):5703–5704. doi: 10.1128/JVI.00491-11
  • Kajon AE, Echavarria M, de Jong JC. Designation of human adenovirus types based on sequence data: an unfinished debate. J Clin Virol. 2013;58(4):743–744. doi: 10.1016/j.jcv.2013.10.014
  • Seto D, Chodosh J, Brister JR, et al. Using the whole-genome sequence to characterize and name human adenoviruses. J Virol. 2011;85(11):5701–5702. doi: 10.1128/JVI.00354-11
  • Harrach B, Tarján ZL, Benkő M. Adenoviruses across the animal kingdom: a walk in the zoo. FEBS Lett. 2019;593(24):3660–3673. doi: 10.1002/1873-3468.13687
  • Hearing P. Adenoviridae: the viruses and their replication. In: Howley P, D Knipe, J Cohen, and B Damania, editors. Fields Virology: DNA Viruses. Netherlands: Walters Kluwer; 2021. p. 98–128.
  • Lion T, Wold WSM. Adenoviruses. In: PM H, K DM, C JL, and D BA, editors. Fields Virology: DNA Viruses. Netherlands: Walters Kluwer; 2021. p. 129–171.
  • Khanal S, Ghimire P, Dhamoon AS. The repertoire of adenovirus in human disease: the innocuous to the deadly. Biomedicines. 2018;6(1):30. doi: 10.3390/biomedicines6010030
  • Lynch JP 3rd, Kajon AE. Adenovirus: epidemiology, global spread of novel serotypes, and advances in treatment and prevention. Semin Respir Crit Care Med. 2016;37(4):586–602. doi: 10.1055/s-0036-1584923
  • Lynch JP 3rd, Kajon AE. Adenovirus: epidemiology, global spread of novel types, and approach to treatment. Semin Respir Crit Care Med. 2021;42(6):800–821. doi: 10.1055/s-0041-1733802
  • Flewett TH, Morris CA, Bryden AS, et al. Epidemic viral enteritis in a long-stay children’s ward. Lancet. 1975;1(7897):4–5. doi: 10.1016/s0140-6736(75)92370-3
  • Schoub BD, Koornhof HJ, Lecatsas G, et al. Letter: viruses in acute summer gastroenteritis in black infants. Lancet. 1975;1(7915):1093–1094. doi: 10.1016/s0140-6736(75)91869-3
  • de Jong JC, Wigand R, Kidd AH, et al. Candidate adenoviruses 40 and 41: fastidious adenoviruses from human infant stool. J Med Virol. 1983;11(3):215–231. doi: 10.1002/jmv.1890110305
  • Uhnoo I, Wadell G, Svensson L, et al. Two new serotypes of enteric adenovirus causing infantile diarrhoea. Dev Biol Stand. 1983;53:311–318.
  • Davison AJ, Telford EA, Watson MS, et al. The DNA sequence of adenovirus type 40. J Mol Biol. 1993;234(4):1308–1316. doi: 10.1006/jmbi.1993.1687
  • Mautner V, Steinthorsdottir V, Bailey A. Enteric adenoviruses. Curr Top Microbiol Immunol. 1995;199(Pt 3):229–282. doi: 10.1007/978-3-642-79586-2_12
  • Pérez-Illana M, Martínez M, Condezo GN, et al. Cryo-EM structure of enteric adenovirus HAdV-F41 highlights structural variations among human adenoviruses. Sci Adv. 2021;7(9):eabd9421. 2021 Feb 24. 10.1126/sciadv.abd9421
  • Rafie K, Lenman A, Fuchs J, et al. The structure of enteric human adenovirus 41-A leading cause of diarrhea in children. Sci Adv. 2021;7(2):eabe0974. doi: 10.1126/sciadv.abe0974
  • Albert MJ. Enteric adenoviruses. Brief review. Arch Virol. 1986;88(1–2):1–17. doi: 10.1007/BF01310885
  • Tiemessen CT, Kidd AH. The subgroup F adenoviruses. J Gen Virol. 1995;76(Pt 3):481–497. doi: 10.1099/0022-1317-76-3-481
  • Uhnoo I, Svensson L, Wadell G. Enteric adenoviruses. Baillieres Clin Gastroenterol. 1990;4(3):627–642. doi: 10.1016/0950-3528(90)90053-j
  • Wadell G, Allard A, Johannson M, et al. Enteric adenoviruses. In: Kapikian A, editor. Viral infections of the gastrointestinal tract. New York: Marcel Dekker; 1994. p. 57–74.
  • Wadell G, Allard A, Johansson M, et al. Enteric adenoviruses. Ciba Found Symp. 1987;128:63–91. doi: 10.1002/9780470513460.ch5
  • Whitelaw A, Davies H, Parry J. Electron microscopy of fatal adenovirus gastroenteritis. Lancet. 1977;1(8007):361. doi: 10.1016/s0140-6736(77)91158-8
  • de Souza EV, de Souza YFVP, Medeiros RS, et al. Diversity of enteric and non-enteric human adenovirus strains in Brazil, 2006-2011. Arch Virol. 2021;166(3):897–903. doi: 10.1007/s00705-020-04946-3
  • Hierholzer JC. Adenoviruses in the immunocompromised host. Clin Microbiol Rev. 1992;5(3):262–274. doi: 10.1128/CMR.5.3.262
  • Thea DM, Glass R, Grohmann GS, et al. Prevalence of enteric viruses among hospital patients with AIDS in Kinshasa, Zaire. Trans R Soc Trop Med Hyg. 1993b;87(3):263–266. doi: 10.1016/0035-9203(93)90119-b PMID: 8236386.
  • Thea DM, St Louis ME, Atido U, et al. A prospective study of diarrhea and HIV-1 infection among 429 Zairian infants. N Engl J Med. 1993a;329(23):1696–1702. doi: 10.1056/NEJM199312023292304
  • Kroes AC, de Klerk EP, Lankester AC, et al. Sequential emergence of multiple adenovirus serotypes after pediatric stem cell transplantation.J Clin Virol. J Clin Virol. 2007;38(4):341–347. doi: 10.1016/j.jcv.2007.01.001
  • Lion T, Kosulin K, Landlinger C, et al. Monitoring of adenovirus load in stool by real-time PCR permits early detection of impending invasive infection in patients after allogeneic stem cell transplantation. Leukemia. 2010;24(4):706–714. doi: 10.1038/leu.2010.4
  • Lion T. Adenovirus infections in immunocompetent and immunocompromised patients. Clin Microbiol Rev. 2014;27(3):441–462. doi: 10.1128/CMR.00116-13
  • Kosulin K. Intestinal HAdV infection: tissue specificity, persistence, and implications for antiviral therapy. Viruses. 2019;11(9):804. doi: 10.3390/v11090804
  • Green M, Wold WS, Mackey JK, et al. Analysis of human tonsil and cancer DNAs and RNAs for DNA sequences of group C (serotypes 1, 2, 5, and 6) human adenoviruses. Proc Natl Acad Sci U S A. 1979;76(12):6606–6610. doi: 10.1073/pnas.76.12.6606
  • Hogg JC. Role of latent viral infections in chronic obstructive pulmonary disease and asthma. Am J Respir Crit Care Med. 2001;164(10 Pt 2):S71–5. doi: 10.1164/ajrccm.164.supplement_2.2106063
  • Kosulin K, Geiger E, Vécsei A, et al. Persistence and reactivation of human adenoviruses in the gastrointestinal tract. Clin Microbiol Infect. 2016;22(4):.e381.1–.e381.8. doi: 10.1016/j.cmi.2015.12.013
  • Leung AY, Chan M, Cheng VC, et al. Quantification of adenovirus in the lower respiratory tract of patients without clinical adenovirus-related respiratory disease. Clin Infect Dis. 2005;40(10):1541–1544. doi: 10.1086/429627
  • Roy S, Calcedo R, Medina-Jaszek A, et al. Adenoviruses in lymphocytes of the human gastro-intestinal tract. PLoS One. 2011;6(9):e24859. doi: 10.1371/journal.pone.0024859
  • Fox JP, Brandt CD, Wassermann FE, et al. The virus watch program: a continuing surveillance of viral infections in metropolitan New York families. VI. Observations of adenovirus infections: virus excretion patterns, antibody response, efficiency of surveillance, patterns of infections, and relation to illness. Am J Epidemiol. 1969 Jan;89(1):25–50.
  • Fox JP, Hall CE, Cooney MK. The Seattle virus watch. VII. Observations of adenovirus infections. Am J Epidemiol. 1977;105(4):362–386. doi: 10.1093/oxfordjournals.aje.a112394
  • Garnett CT, Erdman D, Xu W, et al. Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J Virol. 2002;76(21):10608–10616. doi: 10.1128/jvi.76.21.10608-10616.2002
  • Garnett CT, Talekar G, Mahr JA, et al. Latent species C adenoviruses in human tonsil tissues. J Virol. 2009;83(6):2417–2428. doi: 10.1128/JVI.02392-08
  • Neumann R, Genersch E, Eggers HJ. Detection of adenovirus nucleic acid sequences in human tonsils in the absence of infectious virus. Virus Res. 1987;7(1):93–97. doi: 10.1016/0168-1702(87)90060-8
  • Lion T. Adenovirus persistence, reactivation, and clinical management. FEBS Lett. 2019;593(24):3571–3582. doi: 10.1002/1873-3468.13576
  • Hoffman JA. Adenovirus infections in solid organ transplant recipients. Curr Opin Organ Transplant. 2009;14(6):625–633. doi: 10.1097/MOT.0b013e3283324e1b
  • Lion T, Baumgartinger R, Watzinger F, et al. Molecular monitoring of adenovirus in peripheral blood after allogeneic bone marrow transplantation permits early diagnosis of disseminated disease. Blood. 2003;102(3):1114–1120. doi: 10.1182/blood-2002-07-2152
  • Zheng Y, Stamminger T, Hearing P. E2F/Rb family proteins mediate interferon induced repression of adenovirus immediate early transcription to promote persistent viral infection. PLOS Pathog. 2016;12(1):e1005415. doi: 10.1371/journal.ppat.1005415
  • Prasad V, Suomalainen M, Jasiqi Y, et al. The UPR sensor IRE1α and the adenovirus E3-19K glycoprotein sustain persistent and lytic infections. Nat Commun. 2020;11(1):1997. doi: 10.1038/s41467-020-15844-2
  • Bergelson JM, Cunningham JA, Droguett G, et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science. 1997;275(5304):1320–1323. doi: 10.1126/science.275.5304.1320
  • Roelvink PW, Lizonova A, Lee JG, et al. The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J Virol. 1998;72(10):7909–7915. doi: 10.1128/JVI.72.10.7909-7915.1998
  • Gaggar A, Shayakhmetov DM, Lieber A. CD46 is a cellular receptor for group B adenoviruses.Nat med. 2003;9(11):1408–1412.doi: 10.1038/nm952
  • 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
  • Yeh HY, Pieniazek N, Pieniazek D, et al. Genetic organization, size, and complete sequence of early region 3 genes of human adenovirus type 41. J Virol. 1996;70(4):2658–2663. doi: 10.1128/jvi.70.4.2658-2663.1996
  • Kidd AH, Chroboczek J, Cusack S, et al. Adenovirus type 40 virions contain two distinct fibers. Virology. 1993;192(1):73–84. doi: 10.1006/viro.1993.1009
  • Rajan A, Palm E, Trulsson F, et al. Heparan sulfate is a cellular receptor for enteric human adenoviruses. Viruses. 2021;13(2):298. doi: 10.3390/v13020298
  • Rajan A, Persson BD, Frängsmyr L, et al. Enteric species F human adenoviruses use laminin-binding integrins as co-receptors for infection of Ht-29 cells. Sci Rep. 2018;8(1):10019. doi: 10.1038/s41598-018-28255-7
  • Albinsson B, Kidd AH. Adenovirus type 41 lacks an RGD alpha(v)-integrin binding motif on the penton base and undergoes delayed uptake in A549 cells. Virus Res. 1999;64(2):125–136. doi: 10.1016/s0168-1702(99)00087-8
  • Favier AL, Burmeister WP, Chroboczek J. Unique physicochemical properties of human enteric Ad41 responsible for its survival and replication in the gastrointestinal tract. Virology. 2004;322(1):93–104. doi: 10.1016/j.virol.2004.01.020
  • Stewart RL, O’Connor KL. Clinical significance of the integrin α6β4 in human malignancies. Lab Invest. 2015;95(9):976–986. doi: 10.1038/labinvest.2015.82
  • Williams JM, Duckworth CA, Burkitt MD, et al. Epithelial cell shedding and barrier function: a matter of life and death at the small intestinal villus tip. Vet Pathol. 2015;52(3):445–455. doi: 10.1177/0300985814559404
  • Arnberg N. Adenovirus receptors: implications for targeting of viral vectors. Trends Pharmacol Sci. 2012;33(8):442–448. doi: 10.1016/j.tips.2012.04.005
  • Khare R, Reddy VS, Nemerow GR, et al. Identification of adenovirus serotype 5 hexon regions that interact with scavenger receptors.J Virol. 2012;86(4):2293–2301.doi: 10.1128/JVI.05760-11
  • Maler MD, Nielsen PJ, Stichling N, et al. Key role of the scavenger receptor MARCO in mediating adenovirus infection and subsequent innate responses of macrophages. MBio. 2017;8(4):e00670–17. doi: 10.1128/mBio.00670-17
  • Stichling N, Suomalainen M, Flatt JW, et al. Lung macrophage scavenger receptor SR-A6 (MARCO) is an adenovirus type-specific virus entry receptor. PLOS Pathog. 2018;14(3):e1006914. doi: 10.1371/journal.ppat.1006914
  • Greber UF, Flatt JW. Adenovirus entry: from infection to immunity. Annu Rev Virol. 2019;6(1):177–197. doi: 10.1146/annurev-virology-092818-015550
  • Greber UF, Singh I, Helenius A. Mechanisms of viral un coating. Trends Microbiol. 1994;2(2):52–56. doi: 10.1016/0966-842x(94)90126-0
  • Greber UF, Suomalainen M. Adenovirus entry: stability, uncoating, and nuclear import. Mol Microbiol. 2022;118(4):309–320. doi: 10.1111/mmi.14909
  • Greber UF, Willetts M, Webster P, et al. Stepwise dismantling of adenovirus 2 during entry into cells. Cell. 1993;75(3):477–486. doi: 10.1016/0092-8674(93)90382-z
  • Nakano MY, Boucke K, Suomalainen M, et al. The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J Virol. 2000;74(15):7085–7095. doi: 10.1128/jvi.74.15.7085-7095.2000
  • Puntener D, Engelke MF, Ruzsics Z, et al. Stepwise loss of fluorescent core protein V from human adenovirus during entry into cells. J Virol. 2011;85(1):481–496. doi: 10.1128/JVI.01571-10
  • Bremner KH, Scherer J, Yi J, et al. Adenovirus transport via direct interaction of cytoplasmic dynein with the viral capsid hexon subunit. Cell Host Microbe. 2009;6(6):523–535. doi: 10.1016/j.chom.2009.11.006
  • Dales S, Chardonnet Y. Early events in the interaction of adenoviruses with HeLa cells. IV. Association with microtubules and the nuclear pore complex during vectorial movement of the inoculum. Virology. 1973;56(2):465–483. doi: 10.1016/0042-6822(73)90050-0
  • Miles BD, Luftig RB, Weatherbee JA, et al. Quantitation of the interaction between adenovirus types 2 and 5 and microtubules inside infected cells. Virology. 1980;105(1):265–269. doi: 10.1016/0042-6822(80)90177-4
  • Wang IH, Burckhardt CJ, Yakimovich A, et al. Imaging, tracking and computational analyses of virus entry and egress with the cytoskeleton. Viruses. 2018;10(4):166. doi: 10.3390/v10040166
  • Scherer J, Vallee RB. Adenovirus recruits dynein by an evolutionary novel mechanism involving direct binding to Ph-primed hexon. Viruses. 2011;3(8):1417–1431. doi: 10.3390/v3081417
  • Zhou J, Scherer J, Yi J, et al. Role of kinesins in directed adenovirus transport and cytoplasmic exploration. PLOS Pathog. 2018;14(5):e1007055. doi: 10.1371/journal.ppat.1007055
  • Scherer J, Yi J, Vallee RB. Role of cytoplasmic dynein and kinesins in adenovirus transport. FEBS Lett. 2020;594(12):1838–1847. doi: 10.1002/1873-3468.13777
  • Cassany A, Ragues J, Guan T, et al. Nuclear import of adenovirus DNA involves direct interaction of hexon with an N-terminal domain of the nucleoporin Nup214. J Virol. 2015;89(3):1719–1730. doi: 10.1128/JVI.02639-14
  • Trotman LC, Mosberger N, Fornerod M, et al. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat Cell Biol. 2001;3(12):1092–1100. doi: 10.1038/ncb1201-1092
  • Wang IH, Burckhardt CJ, Yakimovich A, et al. The nuclear export factor CRM1 controls juxta-nuclear microtubule-dependent virus transport. J Cell Sci. 2017;130(13):2185–2195. doi: 10.1242/jcs.203794
  • Bauer M, Flatt JW, Seiler D, et al. The E3 ubiquitin ligase mind bomb 1 controls adenovirus genome release at the nuclear pore complex. Cell Rep. 2019;29(12):3785–3795.e8. doi: 10.1016/j.celrep.2019.11.064
  • Sarbanes SL, Blomen VA, Lam E, et al. E3 ubiquitin ligase mindbomb 1 facilitates nuclear delivery of adenovirus genomes. Proc Natl Acad Sci U S A. 2021;118(1):e2015794118. doi: 10.1073/pnas.2015794118
  • Shayakhmetov DM, Li ZY, Ternovoi V, et al. The interaction between the fiber knob domain and the cellular attachment receptor determines the intracellular trafficking route of adenoviruses. J Virol. 2003;77(6):3712–3723. doi: 10.1128/jvi.77.6.3712-3723.2003
  • Witt DJ, Bousquet EB. Comparison of enteric adenovirus infection in various human cell lines. J Virol Methods. 1988;20(4):295–308. doi: 10.1016/0166-0934(88)90133-4
  • Brown M, Wilson-Friesen HL, Doane F. A block in release of progeny virus and a high particle-to-infectious unit ratio contribute to poor growth of enteric adenovirus types 40 and 41 in cell culture. J Virol. 1992;66(5):3198–3205. doi: 10.1128/JVI.66.5.3198-3205.1992
  • Lemiale F, Haddada H, Nabel GJ, et al. Novel adenovirus vaccine vectors based on the enteric-tropic serotype 41. Vaccine. 2007;25(11):2074–2084. doi: 10.1016/j.vaccine.2006.11.025
  • Yamasaki S, Miura Y, Brown E, et al. Development of a method for effective amplification of human adenovirus 40. Arch Virol. 2010;155(7):1059–1068. doi: 10.1007/s00705-010-0683-3
  • Blackford AN, Grand RJ. Adenovirus E1B 55-kilodalton protein: multiple roles in viral infection and cell transformation. J Virol. 2009;83(9):4000–4012. doi: 10.1128/JVI.02417-08
  • Götting J, Cordes AK, Steinbrück L, et al. Molecular phylogeny of human adenovirus type 41 lineages. eCollection 2022 Virus Evol. 2022;8(2):veac098. doi: 10.1093/ve/veac098
  • Ebner K, Pinsker W, Lion T. Comparative sequence analysis of the hexon gene in the entire spectrum of human adenovirus serotypes: phylogenetic, taxonomic, and clinical implications. J Virol. 2005;79(20):12635–12642. doi: 10.1128/JVI.79.20.12635-12642.2005
  • Gilson T, Blanchette P, Ballmann MZ, et al. Using the E4orf6-based E3 ubiquitin ligase as a tool to analyze the evolution of adenoviruses. J Virol. 2016;90(16):7350–7367. doi: 10.1128/JVI.00420-16
  • Madisch I, Harste G, Pommer H, et al. Phylogenetic analysis of the main neutralization and hemagglutination determinants of all human adenovirus prototypes as a basis for molecular classification and taxonomy.J. Virol. 2005;79(24):15265–15276. doi: 10.1128/JVI.79.24.15265-15276.2005
  • Madisch I, Hofmayer S, Moritz C, et al. Phylogenetic analysis and structural predictions of human adenovirus penton proteins as a basis for tissue-specific adenovirus vector design. J Virol. 2007;81(15):8270–8281. doi: 10.1128/JVI.00048-07
  • Madisch I, Wölfel R, Harste G, et al. Molecular identification of adenovirus sequences: a rapid scheme for early typing of human adenoviruses in diagnostic samples of immunocompetent and immunodeficient patients. J Med Virol. 2006;78(9):1210–1217. doi: 10.1002/jmv.20683
  • Avvakumov N, Kajon AE, Hoeben RC, et al. Comprehensive sequence analysis of the E1A proteins of human and simian adenoviruses. Virology. 2004;329(2):477–492. doi: 10.1016/j.virol.2004.08.007
  • van Loon AE, Ligtenberg M, Reemst AM, et al. Structure and organization of the left-terminal DNA regions of fastidious adenovirus types 40 and 41. Gene. 1987;58(1):109–126. doi: 10.1016/0378-1119(87)90034-5
  • Cheng CY, Gilson T, Dallaire F, et al. The E4orf6/E1B55K E3 ubiquitin ligase complexes of human adenoviruses exhibit heterogeneity in composition and substrate specificity. J Virol. 2011;85(2):765–775. doi: 10.1128/JVI.01890-10
  • Cheng CY, Gilson T, Wimmer P, et al. Role of E1B55K in E4orf6/E1B55K E3 ligase complexes formed by different human adenovirus serotypes. J Virol. 2013;87(11):6232–6245. doi: 10.1128/JVI.00384-13
  • Cousin C, Winter N, Gomes SA, et al. Cellular transformation by E1 genes of enteric adenoviruses. Virology. 1991;181(1):277–287. doi: 10.1016/0042-6822(91)90493-u
  • Bailey A, Mautner V. Phylogenetic relationships among adenovirus serotypes. Virology. 1994;205(2):438–452. doi: 10.1006/viro.1994.1664
  • Lichtenstein DL, Toth K, Doronin K, et al. Functions and mechanisms of action of the adenovirus E3 proteins. Int Rev Immunol. 2004;23(1–2):75–111. doi: 10.1080/08830180490265556
  • Frietze KM, Campos SK, Kajon AE. No evidence of a death-like function for species B1 human adenovirus type 3 E3-9K during A549 cell line infection. BMC Res Notes. 2012;5(1):429. doi: 10.1186/1756-0500-5-429
  • Lu ZZ, Zou XH, Lastinger K, et al. Enhanced growth of recombinant human adenovirus type 41 (HAdV-41) carrying ADP gene. Virus Res. 2013;176(1–2):61–68. doi: 10.1016/j.virusres.2013.05.003
  • Mautner V, Mackay N. Enteric adenovirus type 40: complementation of the E4 defect in Ad2 dl808. Virology. 1991;183(1):433–436. doi: 10.1016/0042-6822(91)90161-4
  • Querido E, Blanchette P, Yan Q, et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 2001;15(23):3104–3117. doi: 10.1101/gad.926401
  • Schreiner S, Wimmer P, Dobner T. Adenovirus degradation of cellular proteins. Future Microbiol. 2012;7(2):211–225. doi: 10.2217/fmb.11.153
  • Blackford AN, Patel RN, Forrester NA, et al. Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc Natl Acad Sci U S A. 2010;107(27):12251–12256. doi: 10.1073/pnas.0914605107
  • Gilson T, Cheng CY, Hur WS, et al. Analysis of the Cullin binding sites of the E4orf6 proteins of human adenovirus E3 ubiquitin ligases. J Virol. 2014;88(7):3885–3897. doi: 10.1128/JVI.03579-13
  • Cheng L, Huang X, Li X, et al. Cryo-EM structures of two bovine adenovirus type 3 intermediates. Virology. 2014;450-451:174–181. doi: 10.1016/j.virol.2013.12.012
  • Kundhavai Natchiar S, Venkataraman S, Mullen TM, et al. Revised crystal structure of human adenovirus reveals the limits on protein IX quasi-equivalence and on analyzing large macromolecular complexes. J Mol Biol. 2018;430(21):4132–4141. doi: 10.1016/j.jmb.2018.08.011
  • Liu H, Jin L, Koh SB, et al. Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science. 2010;329(5995):1038–1043. doi: 10.1126/science.1187433
  • Marabini R, Condezo GN, Krupovic M, et al. Near-atomic structure of an atadenovirus reveals a conserved capsid-binding motif and intergenera variations in cementing proteins. Sci Adv. 2021;7(14):eabe6008. doi: 10.1126/sciadv.abe6008
  • Menéndez-Conejero R, Nguyen TH, Singh AK, et al. Structure of a reptilian adenovirus reveals a phage tailspike fold stabilizing a vertebrate virus capsid. Structure. 2017;25(10):1562–1573.e5. doi: 10.1016/j.str.2017.08.007
  • Reddy VS, Natchiar SK, Stewart PL, et al. Crystal structure of human adenovirus at 3.5 a resolution. Science. 2010;329(5995):1071–1075. doi: 10.1126/science.1187292
  • Yu X, Veesler D, Campbell MG, et al. Cryo-EM structure of human adenovirus D26 reveals the conservation of structural organization among human adenoviruses. Sci Adv. 2017;3(5):e1602670. doi: 10.1126/sciadv.1602670
  • Toogood CI, Hay RT. DNA sequence of the adenovirus type 41 hexon gene and predicted structure of the protein. J Gen Virol. 1988;69(Pt 9):2291–2301. doi: 10.1099/0022-1317-69-9-2291
  • Toogood CI, Murali R, Burnett RM, et al. The adenovirus type 40 hexon: sequence, predicted structure and relationship to other adenovirus hexons. J Gen Virol. 1989;70(Pt 12):3203–3214. doi: 10.1099/0022-1317-70-12-3203
  • Yu X, Mullen TM, Abrishami V, et al. Structure of a cell entry defective human adenovirus provides insights into precursor proteins and capsid maturation. J Mol Biol. 2022;434(2):167350. doi: 10.1016/j.jmb.2021.167350
  • Pieniazek NJ, Slemenda SB, Pieniazek D, et al. Human enteric adenovirus type 41 (Tak) contains a second fiber protein gene. Nucleic Acids Res. 1990;18(7):1901. doi: 10.1093/nar/18.7.1901
  • Yeh HY, Pieniazek N, Pieniazek D, et al. Human adenovirus type 41 contains two fibers. Virus Res. 1994;33(2):179–198. doi: 10.1016/0168-1702(94)90054-x
  • Seiradake E, Cusack S. Crystal structure of enteric adenovirus serotype 41 short fiber head. J Virol. 2005;79(22):14088–14094. doi: 10.1128/JVI.79.22.14088-14094.2005
  • Gallardo J, Pérez-Illana M, Martín-González N, et al. Adenovirus structure: what is new? Int J Mol Sci. 2021;22(10):5240. doi: 10.3390/ijms22105240
  • Dai X, Wu L, Sun R, et al. Atomic structures of minor proteins VI and VII in human adenovirus. J Virol. 2017;91(24):e00850–17. doi: 10.1128/JVI.00850-17
  • Nemerow GR, Stewart PL. Insights into adenovirus uncoating from interactions with integrins and mediators of host immunity. Viruses. 2016;8(12):337. doi: 10.3390/v8120337
  • Nguyen EK, Nemerow GR, Smith JG. Direct evidence from single-cell analysis that human {alpha}-defensins block adenovirus uncoating to neutralize infection. J Virol. 2010;84(8):4041–4049. doi: 10.1128/JVI.02471-09
  • Smith JG, Nemerow GR. Mechanism of adenovirus neutralization by human alpha-defensins. Cell Host Microbe. 2008;3(1):11–19. doi: 10.1016/j.chom.2007.12.001
  • Smith JG, Silvestry M, Lindert S, et al. Insight into the mechanisms of adenovirus capsid disassembly from studies of defensin neutralization. PLOS Pathog. 2010;6(6):e1000959. doi: 10.1371/journal.ppat.1000959
  • Flatt JW, Kim R, Smith JG, et al. An intrinsically disordered region of the adenovirus capsid is implicated in neutralization by human alpha defensin 5. PLoS One. 2013;8(4):e61571. Print 2013. doi: 10.1371/journal.pone.0061571
  • Beatty MS, Curiel DT. Chapter two–adenovirus strategies for tissue-specific targeting. Adv Cancer Res. 2012;115:39–67. doi: 10.1016/B978-0-12-398342-8.00002-1
  • Watanabe M, Nishikawaji Y, Kawakami H, et al. Adenovirus biology, recombinant adenovirus, and adenovirus usage in gene therapy. Viruses. 2021;13(12):2502. doi: 10.3390/v13122502
  • Wold WS, Toth K. Adenovirus vectors for gene therapy, vaccination and cancer gene therapy. Curr Gene Ther. 2013;13(6):421–433. doi: 10.2174/1566523213666131125095046
  • Buckinx R, Timmermans JP. Targeting the gastrointestinal tract with viral vectors: state of the art and possible applications in research and therapy. Histochem Cell Biol. 2016;146(6):709–720. doi: 10.1007/s00418-016-1496-6
  • Croyle MA, Stone M, Amidon GL, et al. In vitro and in vivo assessment of adenovirus 41 as a vector for gene delivery to the intestine. Gene Ther. 1998;5(5):645–654. doi: 10.1038/sj.gt.3300645
  • Grand RJ. A link between severe hepatitis in children and adenovirus 41 and adeno-associated virus 2 infections. J Gen Virol. 2022;103(11). doi: 10.1099/jgv.0.001783
  • Ilic I, Ilic M. Multi-country outbreak of severe acute hepatitis of unknown origin in children, 2022. Acta Paediatr. 2023;112(6):1148–1156. doi: 10.1111/apa.16685
  • Karpen SJ. Acute hepatitis in children in 2022 - human adenovirus 41? N Engl J Med. 2022;387(7):656–657. doi: 10.1056/NEJMe2208409
  • Matthews PC, Campbell C, Săndulescu O, et al. Acute severe hepatitis outbreak in children: A perfect storm. What do we know, and what questions remain? Front Pharmacol. 2022;13:1062408. doi: 10.3389/fphar.2022.1062408
  • Uwishema O, Mahmoud A, Wellington J, et al. A review on acute, severe hepatitis of unknown origin in children: A call for concern. Ann Med Surg (Lond). 2022;81:104457. doi: 10.1016/j.amsu.2022.104457
  • Wang C, Gao ZY, Walsh N, et al. Acute hepatitis of unknown aetiology among children around the world. Infect Dis Poverty. 2022;11(1):112. doi: 10.1186/s40249-022-01035-2
  • Bucuvalas J, Yazigi N, RH S Jr. Acute liver failure in children. vii Clin Liver Dis. 2006;10(1):149–168. doi: 10.1016/j.cld.2005.10.006
  • Squires RH Jr, Shneider BL, Bucuvalas J, et al. Acute liver failure in children: the first 348 patients in the pediatric acute liver failure study group. J Pediatr. 2006;148(5):652–658. doi: 10.1016/j.jpeds.2005.12.051
  • Kelgeri C, Couper M, Gupte GL, et al. Clinical spectrum of children with acute hepatitis of unknown cause. N Engl J Med. 2022;387(7):611–619. doi: 10.1056/NEJMoa2206704
  • Gutierrez Sanchez LH, Shiau H, Baker JM, et al. A case series of children with acute hepatitis and human adenovirus infection. N Engl J Med. 2022 2022 Aug 18;387(7):620–630. doi: 10.1056/NEJMoa2206294
  • Ho A, Orton R, Tayler R, et al. Nature. Adeno-associated virus 2 infection in children with non-A-E hepatitis. Online ahead of print;2023. doi: 10.1038/s41586-023-05948-2
  • Morfopoulou S, Buddle S, Montaguth OET, et al. Genomic investigations of unexplained acute hepatitis in children. Nature. 2023 Mar 30;617(7961):564–573. Online ahead of print. doi:10.1038/s41586-023-06003-w
  • Servellita V, Gonzalez AS, Lamson DM, et al. Adeno-associated virus type 2 in US children with acute severe hepatitis. Nature. 2023;617(7961):574–580. doi: 10.1038/s41586-023-05949-1 Online ahead of print.
  • Samulski RJ, Muzyczka N. AAV-Mediated gene therapy for research and therapeutic purposes. Annu Rev Virol. 2014;1(1):427–451. doi: 10.1146/annurev-virology-031413-085355
  • Kerr JR, Cotmore SF, Bloom R, editors et al. Parvoviruses. London. Hodder Arnold Publication; 2006. doi: 10.1201/b13393
  • Muzyczka N, Berns K. Parvoviridae: the viruses and their replication. Fields Virology. 2001;2:2327–2359.
  • Weitzman MD, Linden RM. Adeno-associated virus biology. Methods Mol Biol. 2011;807:1–23. doi: 10.1007/978-1-61779-370-7_1
  • Moullier P, Snyder RO. International efforts for recombinant adeno-associated viral vector reference standards. Mol Ther. 2008;16(7):1185–1188. doi: 10.1038/mt.2008.125
  • Boutin S, Monteilhet V, Veron P, et al. Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther. 2010;21(6):704–712. doi: 10.1089/hum.2009.182
  • Calcedo R, Vandenberghe LH, Gao G, et al. Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis. 2009;199(3):381–390. doi: 10.1086/595830
  • Louis Jeune V, Joergensen JA, Hajjar RJ, et al. Pre-existing anti-adeno-associated virus antibodies as a challenge in AAV gene therapy. Hum Gene Ther Methods. 2013;24(2):59–67. doi: 10.1089/hgtb.2012.243
  • Chirmule N, Propert K, Magosin S, et al. Immune responses to adenovirus and adeno-associated virus in humans. Gene Ther. 1999;6(9):1574–1583. doi: 10.1038/sj.gt.3300994
  • Calcedo R, Morizono H, Wang L, et al. Adeno-associated virus antibody profiles in newborns, children, and adolescents. Clin Vaccine Immunol. 2011;18(9):1586–1588. doi: 10.1128/CVI.05107-11
  • Erles K, Sebökovà P, Schlehofer JR. Update on the prevalence of serum antibodies (IgG and IgM) to adeno-associated virus (AAV). J Med Virol. 1999;59(3):406–411. doi: 10.1002/(SICI)1096-9071(199911)59:3<406:AID-JMV22>3.0.CO;2-N
  • Gao G, Vandenberghe LH, Alvira MR, et al. Clades of adeno-associated viruses are widely disseminated in human tissues. J Virol. 2004;78(12):6381–6388. doi: 10.1128/JVI.78.12.6381-6388.2004
  • Grossman Z, Mendelson E, Brok-Simoni F, et al. Detection of adeno-associated virus type 2 in human peripheral blood cells. J Gen Virol. 1992;73(Pt 4):961–966. doi: 10.1099/0022-1317-73-4-961
  • Sayyadi-Dehno Z, Seyed Khorrami SM, Ghavami N, et al. Molecular detection of adeno-associated virus DNA in cases of spontaneous and therapeutic abortion. Fetal Pediatr Pathol. 2019;38(3):206–214. doi: 10.1080/15513815.2019.1576817
  • Tobiasch E, Rabreau M, Geletneky K, et al. Detection of adeno-associated virus DNA in human genital tissue and in material from spontaneous abortion. J Med Virol. 1994;44(2):215–222. doi: 10.1002/jmv.1890440218
  • Walz CM, Anisi TR, Schlehofer JR, et al. Detection of infectious adeno-associated virus particles in human cervical biopsies. Virology. 1998;247(1):97–105. doi: 10.1006/viro.1998.9226
  • Hüser D, Khalid D, Lutter T, et al. High prevalence of infectious adeno-associated virus (AAV) in human peripheral blood mononuclear cells indicative of t lymphocytes as sites of AAV persistence. J Virol. 2017;91(4):e02137–16. doi: 10.1128/JVI.02137-16
  • Berns KI, Giraud C. Biology of adeno-associated virus. Curr Top Microbiol Immunol. 1996;218:1–23. doi: 10.1007/978-3-642-80207-2_1
  • Blacklow NR, Hoggan MD, Kapikian AZ, et al. Epidemiology of adenovirus-associated virus infection in a nursery population. Am J Epidemiol. 1968a;88(3):368–378. doi: 10.1093/oxfordjournals.aje.a120897
  • Blacklow NR, Hoggan MD, Rowe WP. Serologic evidence for human infection with adenovirus-associated viruses. J Natl Cancer Inst. 1968b;40(2):319–327.
  • Chand D, Mohr F, McMillan H, et al. Hepatotoxicity following administration of onasemnogene abeparvovec (AVXS-101) for the treatment of spinal muscular atrophy. J Hepatol. 2021;74(3):560–566. doi: 10.1016/j.jhep.2020.11.001
  • Chowdary P, Shapiro S, Makris M, et al. Phase 1-2 trial of AAVS3 gene therapy in patients with hemophilia B. N Engl J Med. 2022;387(3):237–247. doi: 10.1056/NEJMoa2119913
  • Mullard A. Gene therapy community grapples with toxicity issues, as pipeline matures. Nat Rev Drug Discov. 2021;20(11):804–805. doi: 10.1038/d41573-021-00164-x
  • Muzyczka N, Berns KI. AAV’s Golden Jubilee. Mol Ther. 2015;23(5):807–808. doi: 10.1038/mt.2015.55
  • Sant’anna TB, Araujo NM. Adeno-associated virus infection and its impact in human health: an overview. Virol J. 2022;19(1):173. doi: 10.1186/s12985-022-01900-4
  • La Bella T, Imbeaud S, Peneau C, et al. Adeno-associated virus in the liver: natural history and consequences in tumour development. Gut. 2020;69(4):737–747. doi: 10.1136/gutjnl-2019-318281
  • Nault JC, Datta S, Imbeaud S, et al. Recurrent AAV2-related insertional mutagenesis in human hepatocellular carcinomas.Nat Genet. 2015;47(10):1187–1193. doi: 10.1038/ng.3389
  • Nault JC, Datta S, Imbeaud S, et al. Adeno-associated virus type 2 as an oncogenic virus in human hepatocellular carcinoma. Mol Cell Oncol. 2016;3(2):e1095271. doi: 10.1080/23723556.2015.1095271
  • Tatsuno K, Midorikawa Y, Takayama T, et al. Impact of AAV2 and hepatitis B virus integration into genome on development of hepatocellular carcinoma in patients with prior hepatitis B virus infection. Clin Cancer Res. 2019;25(20):6217–6227. doi: 10.1158/1078-0432.CCR-18-4041
  • Berns KI, Byrne BJ, Flotte TR, et al. Adeno-Associated virus type 2 and hepatocellular carcinoma? Hum Gene Ther. 2015;26(12):779–781. doi: 10.1089/hum.2015.29014.kib
  • Büning H, Schmidt M. Adeno-associated vector toxicity-to be or not to be? Mol Ther. 2015;23(11):1673–1675. doi: 10.1038/mt.2015.182
  • Park KJ, Lee J, Park JH, et al. Adeno-associated virus 2-mediated hepatocellular carcinoma is very rare in Korean patients. Ann Lab Med. 2016;36(5):469–474. doi: 10.3343/alm.2016.36.5.469
  • Schäffer AA, Dominguez DA, Chapman LM, et al. Integration of adeno-associated virus (AAV) into the genomes of most Thai and Mongolian liver cancer patients does not induce oncogenesis. BMC Genomics. 2021;22(1):814. doi: 10.1186/s12864-021-08098-9
  • Kotin RM, Siniscalco M, Samulski RJ, et al. Site-specific integration by adeno-associated virus. Proc Natl Acad Sci, USA. 1990;87(6):2211–2215. doi: 10.1073/pnas.87.6.2211
  • Samulski RJ, Zhu X, Xiao X, et al. Targeted integration of adeno-associated virus (AAV) into human chromosome 19. Embo J. 1991;10(12):3941–3950. doi: 10.1002/j.1460-2075.1991.tb04964.x
  • Galibert L, Hyvönen A, Eriksson RAE, et al. Functional roles of the membrane associated AAV protein MAAP. Sci Rep. 2021;11(1):21698. doi: 10.1038/s41598-021-01220-7
  • Mietzsch M, Pénzes JJ, Agbandje-McKenna M. Twenty-five years of structural parvovirology. Viruses. 2019;11(4):362. doi: 10.3390/v11040362
  • Qiu J, Pintel DJ. The adeno-associated virus type 2 rep protein regulates RNA processing via interaction with the transcription template. Mol Cell Biol. 2002;22(11):3639–3652. doi: 10.1128/MCB.22.11.3639-3652.2002
  • Meyer NL, Chapman MS. Adeno-associated virus (AAV) cell entry: structural insights.Trends microbiol. 2022;30(5):432–451.doi: 10.1016/j.tim.2021.09.005
  • Meyer NL, Hu G, Davulcu O, et al. Structure of the gene therapy vector, adeno-associated virus with its cell receptor. AAVR Elife. 2019;8:e44707. doi: 10.7554/eLife.44707
  • Zhang R, Cao L, Cui M, et al. Adeno-associated virus 2 bound to its cellular receptor AAVR. Nat Microbiol. 2019a;4(4):675–682. doi: 10.1038/s41564-018-0356-7
  • Zhang R, Xu G, Cao L, et al. Divergent engagements between adeno-associated viruses with their cellular receptor AAVR. Nat Commun. 2019b;10(1):3760. doi: 10.1038/s41467-019-11668-x
  • Kambhampati AK, Burke RM, Dietz S, et al. Trends in acute hepatitis of unspecified etiology and adenovirus stool testing results in children - United States, 2017-2022. MMWR Morb Mortal Wkly Rep. 2022;71(24):797–802. doi: 10.15585/mmwr.mm7124e1
  • Leiskau C, Tsaka S, Meyer-Ruhnke L, et al. Acute severe non-A-E-hepatitis of unknown origin in children - a 30-year retrospective observational study from north-west Germany. Hepatol. 2023;78(5):971–978. doi: 10.1016/j.jhep.2022.12.012
  • Martin NA, Gonzalez G, Reynolds LJ, et al. Adeno-associated virus 2 and human adenovirus F41 in wastewater during outbreak of severe acute hepatitis in children, Ireland. Emerg Infect Dis. 2023;29(4):751–760. doi: 10.3201/eid2904.221878
  • Reyne MI, Allen DM, Levickas A, et al. Detection of human adenovirus F41 in wastewater and its relationship to clinical cases of acute hepatitis of unknown aetiology. Sci Total Environ. 2023;857(Pt 2):159579. doi: 10.1016/j.scitotenv.2022.159579
  • Messacar K, Baker RE, Park SW, et al. Preparing for uncertainty: endemic paediatric viral illnesses after COVID-19 pandemic disruption. Lancet. 2022;400(10364):1663–1665. doi: 10.1016/S0140-6736(22)01277-6
  • Al-Jwadi RF, Mills EHA, Torp-Pedersen C, et al. Consequences of COVID-19-related lockdowns and reopenings on emergency hospitalizations in pediatric patients in Denmark during 2020-2021. Eur J Pediatr. 2023;182(1):285–293. doi: 10.1007/s00431-022-04682-7
  • Amar S, Avni YS, O’Rourke N, et al. Prevalence of common infectious diseases after COVID-19 vaccination and easing of pandemic restrictions in Israel. JAMA Netw Open. 2022;5(2):e2146175. doi: 10.1001/jamanetworkopen.2021.46175
  • Benschop KS, Albert J, Anton A, et al. Re-emergence of enterovirus D68 in Europe after easing the COVID-19 lockdown, September 2021. Euro Surveill. 2021;26(45):2100998. doi: 10.2807/1560-7917.ES.2021.26.45.2100998
  • Eden JS, Sikazwe C, Xie R, et al. Off-season RSV epidemics in Australia after easing of COVID-19 restrictions. Nat Commun; 13(1):2884. doi: 10.1038/s41467-022-30485-3
  • Korokhov N, Mikheeva G, Krendelshchikov A, et al. Targeting of adenovirus via genetic modification of the viral capsid combined with a protein bridge. J Virol. 2003;77(24):12931–12940. doi: 10.1128/jvi.77.24.12931-12940.2003
  • Krasnykh VN, Douglas JT, van Beusechem VW. Genetic targeting of adenoviral vectors. Mol Ther. 2000;1(5 Pt 1):391–405. doi: 10.1006/mthe.2000.0062
  • Krasnykh VN, Mikheeva GV, Douglas JT, et al. Generation of recombinant adenovirus vectors with modified fibers for altering viral tropism. J Virol. 1996;70(10):6839–6846. doi: 10.1128/JVI.70.10.6839-6846.1996
  • Noureddini SC, Curiel DT. Genetic targeting strategies for adenovirus. Mol Pharm. 2005;2(5):341–347. doi: 10.1021/mp050045c
  • Wickham TJ, Tzeng E, Shears LL 2nd, et al. Increased in vitro and in vivo gene transfer by adenovirus vectors containing chimeric fiber proteins. J Virol. 1997;71(11):8221–8229. doi: 10.1128/JVI.71.11.8221-8229.1997
  • Nakamura T, Sato K, Hamada H. Reduction of natural adenovirus tropism to the liver by both ablation of fiber-coxsackievirus and adenovirus receptor interaction and use of replaceable short fiber. J Virol. 2003;77(4):2512–2521. doi: 10.1128/jvi.77.4.2512-2521.2003
  • Hsu HL, Brown A, Loveland AB, et al. Structural characterization of a novel human adeno-associated virus capsid with neurotropic properties. Nat Commun. 2020;11(1):3279. doi: 10.1038/s41467-020-17047-1
  • Brisca G, Mallamaci M, Tardini G, et al. Brisca-CoV-2 infection may present as acute hepatitis in children. Pediatr Infect Dis J. 2021;40(5):e214–e215. doi: 10.1097/INF.0000000000003098
  • Mameli S, Marcialis MA, Bassareo PP, et al. COVID-19 and hepatic damage: what we know? Panminerva Med. 2023;65(1):58–64. doi: 10.23736/S0031-0808.21.04239-7
  • Sun J, Aghemo A, Forner A, et al. COVID-19 and liver disease. Liver Int. 2020;40:1278–1281. doi: 10.1111/liv.14470
  • Wander P, Epstein M, Bernstein D. COVID-19 presenting as acute hepatitis. Am J Gastroenterol. 2020;115(6):941–942. doi: 10.14309/ajg.0000000000000660