Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)

10.24072/pcjournal.154 - Peer Community Journal, Volume 2 (2022), article no. e44.

Get full text PDF Peer reviewed and recommended by PCI

Structural variations (SVs) constitute a significant source of genetic variability in virus genomes. Yet knowledge about SV variability and contribution to the evolutionary process in large double-stranded (ds)DNA viruses is limited. Cyprinid herpesvirus 3 (CyHV-3), also commonly known as koi herpesvirus (KHV), has the largest dsDNA genome within herpesviruses. This virus has become one of the biggest threats to common carp and koi farming, resulting in high morbidity and mortalities of fishes, serious environmental damage, and severe economic losses. A previous study analyzing CyHV-3 virulence evolution during serial passages onto carp cell cultures suggested that CyHV-3 evolves, at least in vitro, through an assembly of haplotypes that alternatively become dominant or under-represented. The present study investigates the SV diversity and dynamics in CyHV-3 genome during 99 serial passages in cell culture using, for the first time, ultra-deep whole-genome and amplicon-based sequencing. The results indicate that KHV polymorphism mostly involves SVs. These SVs display a wide distribution along the genome and exhibit high turnover dynamics with a clear bias towards inversion and deletion events. Analysis of the pathogenesis-associated ORF150 region in ten intermediate cell passages highlighted mainly deletion, inversion and insertion variations that deeply altered the structure of ORF150. Our findings indicate that SV turnovers and defective genomes represent key drivers in the viral population dynamics and in vitro evolution of KHV. Thus, the present study can contribute to the basic research needed to design safe live-attenuated vaccines, classically obtained by viral attenuation after serial passages in cell culture. 

Published online:
DOI: 10.24072/pcjournal.154
Fuandila, Nurul Novelia 1; Gosselin-Grenet, Anne-Sophie 2; Tilak, Marie-Ka 1; Bergmann, Sven M 3; Escoubas, Jean-Michel 4; Klafack, Sandro 5; Lusiastuti, Angela Mariana 6; Yuhana, Munti 7; Fiston-Lavier, Anna-Sophie 8; Avarre, Jean-Christophe 1; Cherif, Emira 1

1 ISEM, Univ Montpellier, CNRS, IRD, Montpellier, France
2 DGIMI, Univ Montpellier, INRAE, Montpellier, France
3 Institute of Infectology, Friedrich-Loeffer-Institut, Federal Research Institute for Animal Health, Greifswald-Insel Riems, Germany
4 IHPE, Univ Montpellier, CNRS, Ifremer, UPVD, Montpellier, France
5 Department of Experimental Animal Facilities and Biorisk Management, Friedrich-Loeffer-Institut, Federal Research Institute for Animal Health, Greifswald-Insel Riems, Germany
6 Fish Health Laboratory, Research Institute for Freshwater Aquaculture and Fisheries Extension, Bogor, Indonesia
7 Faculty of Fisheries and Marine Sciences, Bogor Agricultural University, Indonesia
8 Institut Universitaire de France (IUF), Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Fuandila, Nurul Novelia and Gosselin-Grenet, Anne-Sophie and Tilak, Marie-Ka and Bergmann, Sven M and Escoubas, Jean-Michel and Klafack, Sandro and Lusiastuti, Angela Mariana and Yuhana, Munti and Fiston-Lavier, Anna-Sophie and Avarre, Jean-Christophe and Cherif, Emira},
     title = {Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded {DNA} koi herpesvirus {(KHV)}},
     journal = {Peer Community Journal},
     eid = {e44},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.154},
     url = {}
AU  - Fuandila, Nurul Novelia
AU  - Gosselin-Grenet, Anne-Sophie
AU  - Tilak, Marie-Ka
AU  - Bergmann, Sven M
AU  - Escoubas, Jean-Michel
AU  - Klafack, Sandro
AU  - Lusiastuti, Angela Mariana
AU  - Yuhana, Munti
AU  - Fiston-Lavier, Anna-Sophie
AU  - Avarre, Jean-Christophe
AU  - Cherif, Emira
TI  - Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)
JO  - Peer Community Journal
PY  - 2022
DA  - 2022///
VL  - 2
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.154
ID  - 10_24072_pcjournal_154
ER  - 
%0 Journal Article
%A Fuandila, Nurul Novelia
%A Gosselin-Grenet, Anne-Sophie
%A Tilak, Marie-Ka
%A Bergmann, Sven M
%A Escoubas, Jean-Michel
%A Klafack, Sandro
%A Lusiastuti, Angela Mariana
%A Yuhana, Munti
%A Fiston-Lavier, Anna-Sophie
%A Avarre, Jean-Christophe
%A Cherif, Emira
%T Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV)
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%R 10.24072/pcjournal.154
%F 10_24072_pcjournal_154
Fuandila, Nurul Novelia; Gosselin-Grenet, Anne-Sophie; Tilak, Marie-Ka; Bergmann, Sven M; Escoubas, Jean-Michel; Klafack, Sandro; Lusiastuti, Angela Mariana; Yuhana, Munti; Fiston-Lavier, Anna-Sophie; Avarre, Jean-Christophe; Cherif, Emira. Structural variation turnovers and defective genomes: key drivers for the in vitro evolution of the large double-stranded DNA koi herpesvirus (KHV). Peer Community Journal, Volume 2 (2022), article  no. e44. doi : 10.24072/pcjournal.154.

Peer reviewed and recommended by PCI : 10.24072/pci.infections.100001

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Akhtar, L. N.; Bowen, C. D.; Renner, D. W.; Pandey, U.; Della Fera, A. N.; Kimberlin, D. W.; Prichard, M. N.; Whitley, R. J.; Weitzman, M. D.; Szpara, M. L. Genotypic and Phenotypic Diversity of Herpes Simplex Virus 2 within the Infected Neonatal Population, mSphere, Volume 4 (2019) no. 1 | DOI

[2] Aoki, T.; Hirono, I.; Kurokawa, K.; Fukuda, H.; Nahary, R.; Eldar, A.; Davison, A. J.; Waltzek, T. B.; Bercovier, H.; Hedrick, R. P. Genome Sequences of Three Koi Herpesvirus Isolates Representing the Expanding Distribution of an Emerging Disease Threatening Koi and Common Carp Worldwide, Journal of Virology, Volume 81 (2007) no. 10, pp. 5058-5065 | DOI

[3] Boutier, M.; Ronsmans, M.; Rakus, K.; Jazowiecka-Rakus, J.; Vancsok, C.; Morvan, L.; Peñaranda, M. M. D.; Stone, D. M.; Way, K.; van Beurden, S. J.; Davison, A. J.; Vanderplasschen, A. Cyprinid Herpesvirus 3, Advances in Virus Research, Volume 93, Elsevier, 2015, pp. 161-256 | DOI

[4] Boutier, M.; Gao, Y.; Vancsok, C.; Suárez, N. M.; Davison, A. J.; Vanderplasschen, A. Identification of an essential virulence gene of cyprinid herpesvirus 3, Antiviral Research, Volume 145 (2017), pp. 60-69 | DOI

[5] Bull, J. C.; Godfray, H. C. J.; O'Reilly, D. R. A Few-Polyhedra Mutant and Wild-Type Nucleopolyhedrovirus Remain as a Stable Polymorphism during Serial Coinfection in Trichoplusia ni, Applied and Environmental Microbiology, Volume 69 (2003) no. 4, pp. 2052-2057 | DOI

[6] Bull, J. J.; Smithson, M. W.; Nuismer, S. L. Transmissible Viral Vaccines, Trends in Microbiology, Volume 26 (2018) no. 1, pp. 6-15 | DOI

[7] Calain, P.; Roux, L. Functional Characterisation of the Genomic and Antigenomic Promoters of Sendai Virus, Virology, Volume 212 (1995) no. 1, pp. 163-173 | DOI

[8] Cann, A.; Stanway, G.; Hughes, P.; Minor, P.; Evans, D.; Schild, G.; Almond, J. Reversion to neurovirulence of the live-attenuated Sabin type 3 oral pollovirus vaccine, Nucleic Acids Research, Volume 12 (1984) no. 20, pp. 7787-7792 | DOI

[9] Chateigner, A.; Bézier, A.; Labrousse, C.; Jiolle, D.; Barbe, V.; Herniou, E. Ultra Deep Sequencing of a Baculovirus Population Reveals Widespread Genomic Variations, Viruses, Volume 7 (2015) no. 7, pp. 3625-3646 | DOI

[10] Cherif, E. (2022). KHV_SVProject. OSF,

[11] Colgrove, R.; Diaz, F.; Newman, R.; Saif, S.; Shea, T.; Young, S.; Henn, M.; Knipe, D. M. Genomic sequences of a low passage herpes simplex virus 2 clinical isolate and its plaque-purified derivative strain, Virology, Volume 450-451 (2014), pp. 140-145 | DOI

[12] Cudini, J.; Roy, S.; Houldcroft, C. J.; Bryant, J. M.; Depledge, D. P.; Tutill, H.; Veys, P.; Williams, R.; Worth, A. J. J.; Tamuri, A. U.; Goldstein, R. A.; Breuer, J. Human cytomegalovirus haplotype reconstruction reveals high diversity due to superinfection and evidence of within-host recombination, Proceedings of the National Academy of Sciences, Volume 116 (2019) no. 12, pp. 5693-5698 | DOI

[13] E, X.; Kowalik, T. The DNA Damage Response Induced by Infection with Human Cytomegalovirus and Other Viruses, Viruses, Volume 6 (2014) no. 5, pp. 2155-2185 | DOI

[14] Fuchs, W.; Granzow, H.; Dauber, M.; Fichtner, D.; Mettenleiter, T. C. Identification of structural proteins of koi herpesvirus, Archives of Virology, Volume 159 (2014) no. 12, pp. 3257-3268 | DOI

[15] Gao, Y.; Suárez, N. M.; Wilkie, G. S.; Dong, C.; Bergmann, S.; Lee, P.-Y. A.; Davison, A. J.; Vanderplasschen, A. F. C.; Boutier, M. Genomic and biologic comparisons of cyprinid herpesvirus 3 strains, Veterinary Research, Volume 49 (2018) no. 1 | DOI

[16] Gotesman, M.; Kattlun, J.; Bergmann, S.; El-Matbouli, M. CyHV-3: the third cyprinid herpesvirus, Diseases of Aquatic Organisms, Volume 105 (2013) no. 2, pp. 163-174 | DOI

[17] Haenen, O. L. M. W. K. B. S. M. A. E. The emergence of koi herpesvirus and its significance to European aquaculture, Bulletin of the European Association of Fish Pathologists, Volume 24 (2004) no. 6, pp. 293-307

[18] Hammoumi, S.; Vallaeys, T.; Santika, A.; Leleux, P.; Borzym, E.; Klopp, C.; Avarre, J.-C. Targeted genomic enrichment and sequencing of CyHV-3 from carp tissues confirms low nucleotide diversity and mixed genotype infections, PeerJ, Volume 4 (2016) | DOI

[19] Hanley, K. A. The Double-Edged Sword: How Evolution Can Make or Break a Live-Attenuated Virus Vaccine, Evolution: Education and Outreach, Volume 4 (2011) no. 4, pp. 635-643 | DOI

[20] He, F.; Kwang, J. Identification and characterization of a new E3 ubiquitin ligase in white spot syndrome virus involved in virus latency, Virology Journal, Volume 5 (2008) no. 1 | DOI

[21] Hanley, K. A. The Double-Edged Sword: How Evolution Can Make or Break a Live-Attenuated Virus Vaccine, Evolution: Education and Outreach, Volume 4 (2011) no. 4, pp. 635-643 | DOI

[22] He, F.; Kwang, J. Identification and characterization of a new E3 ubiquitin ligase in white spot syndrome virus involved in virus latency, Virology Journal, Volume 5 (2008) no. 1 | DOI

[23] Hedrick, R. P.; Gilad, O.; Yun, S.; Spangenberg, J. V.; Marty, G. D.; Nordhausen, R. W.; Kebus, M. J.; Bercovier, H.; Eldar, A. A Herpesvirus Associated with Mass Mortality of Juvenile and Adult Koi, a Strain of Common Carp, Journal of Aquatic Animal Health, Volume 12 (2000) no. 1, pp. 44-57 | DOI

[24] Jeffares, D. C.; Jolly, C.; Hoti, M.; Speed, D.; Shaw, L.; Rallis, C.; Balloux, F.; Dessimoz, C.; Bähler, J.; Sedlazeck, F. J. Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast, Nature Communications, Volume 8 (2017) no. 1 | DOI

[25] Kew, O. M.; Sutter, R. W.; de Gourville, E. M.; Dowdle, W. R.; Pallansch, M. A. Vaccine-derived polioviruses and the endgame strategy for global polio eradication, Annual Review of Microbiology, Volume 59 (2005) no. 1, pp. 587-635 | DOI

[26] Klafack, S.; Fiston-Lavier, A.-S.; Bergmann, S.; Hammoumi, S.; Schröder, L.; Fuchs, W.; Lusiastuti, A.; Lee, P.-Y.; Heredia, S.; Gosselin-Grenet, A.-S.; Avarre, J.-C. Cyprinid herpesvirus 3 Evolves In Vitro through an Assemblage of Haplotypes that Alternatively Become Dominant or Under-Represented, Viruses, Volume 11 (2019) no. 8 | DOI

[27] Klafack, S.; Wang, Q.; Zeng, W.; Wang, Y.; Li, Y.; Zheng, S.; Kempter, J.; Lee, P.-Y.; Matras, M.; Bergmann, S. M. Genetic Variability of Koi Herpesvirus In vitro—A Natural Event?, Frontiers in Microbiology, Volume 8 (2017) | DOI

[28] Kolb, A. W.; Lewin, A. C.; Moeller Trane, R.; McLellan, G. J.; Brandt, C. R. Phylogenetic and recombination analysis of the herpesvirus genus varicellovirus, BMC Genomics, Volume 18 (2017) no. 1 | DOI

[29] Kulkarni, A. S.; Fortunato, E. A. Stimulation of Homology-Directed Repair at I-SceI-Induced DNA Breaks during the Permissive Life Cycle of Human Cytomegalovirus, Journal of Virology, Volume 85 (2011) no. 12, pp. 6049-6054 | DOI

[30] Lauring, A. S.; Andino, R. Quasispecies Theory and the Behavior of RNA Viruses, PLoS Pathogens, Volume 6 (2010) no. 7 | DOI

[31] Lauring, A. S.; Jones, J. O.; Andino, R. Rationalizing the development of live attenuated virus vaccines, Nature Biotechnology, Volume 28 (2010) no. 6, pp. 573-579 | DOI

[32] Lecompte, L.; Peterlongo, P.; Lavenier, D.; Lemaitre, C. SVJedi: genotyping structural variations with long reads, Bioinformatics, Volume 36 (2020) no. 17, pp. 4568-4575 | DOI

[33] Li, D.; Lott, W. B.; Lowry, K.; Jones, A.; Thu, H. M.; Aaskov, J. Defective Interfering Viral Particles in Acute Dengue Infections, PLoS ONE, Volume 6 (2011) no. 4 | DOI

[34] Li, H. Minimap2: pairwise alignment for nucleotide sequences, Bioinformatics, Volume 34 (2018) no. 18, pp. 3094-3100 | DOI

[35] Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The Sequence Alignment/Map format and SAMtools, Bioinformatics, Volume 25 (2009) no. 16, pp. 2078-2079 | DOI

[36] Li, W.; Lee, X.; Weng, S.; He, J.; Dong, C. Whole-genome sequence of a novel Chinese cyprinid herpesvirus 3 isolate reveals the existence of a distinct European genotype in East Asia, Veterinary Microbiology, Volume 175 (2015) no. 2-4, pp. 185-194 | DOI

[37] Loiseau, V.; Herniou, E. A.; Moreau, Y.; Lévêque, N.; Meignin, C.; Daeffler, L.; Federici, B.; Cordaux, R.; Gilbert, C. Wide spectrum and high frequency of genomic structural variation, including transposable elements, in large double-stranded DNA viruses, Virus Evolution, Volume 6 (2020) no. 1 | DOI

[38] López-Muñoz, A. D.; Rastrojo, A.; Martín, R.; Alcamí, A. Herpes simplex virus 2 (HSV-2) evolves faster in cell culture than HSV-1 by generating greater genetic diversity, PLOS Pathogens, Volume 17 (2021) no. 8 | DOI

[39] Marriott, A. C.; Dimmock, N. J. Defective interfering viruses and their potential as antiviral agents, Reviews in Medical Virology, Volume 20 (2010) no. 1, pp. 51-62 | DOI

[40] Martin, S.; Leggett, R. M. Alvis: a tool for contig and read ALignment VISualisation and chimera detection, BMC Bioinformatics, Volume 22 (2021) no. 1 | DOI

[41] Minor, P. D. Live attenuated vaccines: Historical successes and current challenges, Virology, Volume 479-480 (2015), pp. 379-392 | DOI

[42] Molenkamp, R.; Rozier, B. C. D.; Greve, S.; Spaan, W. J. M.; Snijder, E. J. Isolation and Characterization of an Arterivirus Defective Interfering RNA Genome, Journal of Virology, Volume 74 (2000) no. 7, pp. 3156-3165 | DOI

[43] Muslin; Kain; Bessaud; Blondel; Delpeyroux Recombination in Enteroviruses, a Multi-Step Modular Evolutionary Process, Viruses, Volume 11 (2019) no. 9 | DOI

[44] O'Hara, P. J.; Nichol, S. T.; Horodyski, F. M.; Holland, J. J. Vesicular stomatitis virus defective interfering particles can contain extensive genomic sequence rearrangements and base substitutions, Cell, Volume 36 (1984) no. 4, pp. 915-924 | DOI

[45] Pereira-Gómez, M.; Carrau, L.; Fajardo, Á.; Moreno, P.; Moratorio, G. Altering Compositional Properties of Viral Genomes to Design Live-Attenuated Vaccines, Frontiers in Microbiology, Volume 12 (2021) | DOI

[46] Pérez-Losada, M.; Arenas, M.; Galán, J. C.; Palero, F.; González-Candelas, F. Recombination in viruses: Mechanisms, methods of study, and evolutionary consequences, Infection, Genetics and Evolution, Volume 30 (2015), pp. 296-307 | DOI

[47] Portner, A.; Kingsbury, D. W. Homologous Interference by Incomplete Sendai Virus Particles: Changes in Virus-Specific Ribonucleic Acid Synthesis, Journal of Virology, Volume 8 (1971) no. 4, pp. 388-394 | DOI

[48] Rakus, K.; Ouyang, P.; Boutier, M.; Ronsmans, M.; Reschner, A.; Vancsok, C.; Jazowiecka-Rakus, J.; Vanderplasschen, A. Cyprinid herpesvirus 3: an interesting virus for applied and fundamental research, Veterinary Research, Volume 44 (2013) no. 1 | DOI

[49] Ramírez, F.; Ryan, D. P.; Grüning, B.; Bhardwaj, V.; Kilpert, F.; Richter, A. S.; Heyne, S.; Dündar, F.; Manke, T. deepTools2: a next generation web server for deep-sequencing data analysis, Nucleic Acids Research, Volume 44 (2016) no. W1 | DOI

[50] Renner, D. W.; Szpara, M. L. Impacts of Genome-Wide Analyses on Our Understanding of Human Herpesvirus Diversity and Evolution, Journal of Virology, Volume 92 (2018) no. 1 | DOI

[51] Renzette, N.; Pokalyuk, C.; Gibson, L.; Bhattacharjee, B.; Schleiss, M. R.; Hamprecht, K.; Yamamoto, A. Y.; Mussi-Pinhata, M. M.; Britt, W. J.; Jensen, J. D.; Kowalik, T. F. Limits and patterns of cytomegalovirus genomic diversity in humans, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 30 | DOI

[52] Sanjuán, R.; Domingo-Calap, P. Mechanisms of viral mutation, Cellular and Molecular Life Sciences, Volume 73 (2016) no. 23, pp. 4433-4448 | DOI

[53] Sedlazeck, F. J.; Rescheneder, P.; Smolka, M.; Fang, H.; Nattestad, M.; von Haeseler, A.; Schatz, M. C. Accurate detection of complex structural variations using single-molecule sequencing, Nature Methods, Volume 15 (2018) no. 6, pp. 461-468 | DOI

[54] Shekar, M.; Venugopal, M. N. Identification and characterization of novel double zinc fingers encoded by putative proteins in genome of white spot syndrome virus, Archives of Virology, Volume 164 (2019) no. 4, pp. 961-969 | DOI

[55] Spatz, S. J. Accumulation of attenuating mutations in varying proportions within a high passage very virulent plus strain of Gallid herpesvirus type 2, Virus Research, Volume 149 (2010) no. 2, pp. 135-142 | DOI

[56] Sunarto, A.; McColl, K. A.; Crane, M. S. J.; Sumiati, T.; Hyatt, A. D.; Barnes, A. C.; Walker, P. J. Isolation and characterization of koi herpesvirus (KHV) from Indonesia: identification of a new genetic lineage, Journal of Fish Diseases, Volume 34 (2010) no. 2, pp. 87-101 | DOI

[57] Szpara, M. L.; Van Doorslaer, K. Mechanisms of DNA Virus Evolution, Encyclopedia of Virology, Elsevier, 2021, pp. 71-78 | DOI

[58] Tomer, E.; Cohen, E. M.; Drayman, N.; Afriat, A.; Weitzman, M. D.; Zaritsky, A.; Kobiler, O. Coalescing replication compartments provide the opportunity for recombination between coinfecting herpesviruses, The FASEB Journal, Volume 33 (2019) no. 8, pp. 9388-9403 | DOI

[59] Vancsok, C.; Peñaranda, M. M. D.; Raj, V. S.; Leroy, B.; Jazowiecka-Rakus, J.; Boutier, M.; Gao, Y.; Wilkie, G. S.; Suárez, N. M.; Wattiez, R.; Gillet, L.; Davison, A. J.; Vanderplasschen, A. F. C. Proteomic and Functional Analyses of the Virion Transmembrane Proteome of Cyprinid Herpesvirus 3, Journal of Virology, Volume 91 (2017) no. 21 | DOI

[60] Vignuzzi, M.; López, C. B. Defective viral genomes are key drivers of the virus–host interaction, Nature Microbiology, Volume 4 (2019) no. 7, pp. 1075-1087 | DOI

[61] Wang, Z.-H.; Ke, F.; Zhang, Q.-Y.; Gui, J.-F. Structural and Functional Diversity among Five RING Finger Proteins from Carassius Auratus Herpesvirus (CaHV), Viruses, Volume 13 (2021) no. 2 | DOI

[62] White, R.; Pellefigues, C.; Ronchese, F.; Lamiable, O.; Eccles, D. Investigation of chimeric reads using the MinION, F1000Research, Volume 6 (2017) | DOI

[63] Wilkinson, D.; Weller, S. The Role of DNA Recombination in Herpes Simplex Virus DNA Replication, IUBMB Life (International Union of Biochemistry and Molecular Biology: Life), Volume 55 (2003) no. 8, pp. 451-458 | DOI

[64] Xiao, Y.; Lidsky, P. V.; Shirogane, Y.; Aviner, R.; Wu, C.-T.; Li, W.; Zheng, W.; Talbot, D.; Catching, A.; Doitsh, G.; Su, W.; Gekko, C. E.; Nayak, A.; Ernst, J. D.; Brodsky, L.; Brodsky, E.; Rousseau, E.; Capponi, S.; Bianco, S.; Nakamura, R.; Jackson, P. K.; Frydman, J.; Andino, R. A defective viral genome strategy elicits broad protective immunity against respiratory viruses, Cell, Volume 184 (2021) no. 25 | DOI

[65] Yeh, M. T.; Bujaki, E.; Dolan, P. T.; Smith, M.; Wahid, R.; Konz, J.; Weiner, A. J.; Bandyopadhyay, A. S.; Van Damme, P.; De Coster, I.; Revets, H.; Macadam, A.; Andino, R. Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence, Cell Host amp; Microbe, Volume 27 (2020) no. 5 | DOI

[66] Zhang, Y.; Li, L.-F.; Munir, M.; Qiu, H.-J. RING-Domain E3 Ligase-Mediated Host–Virus Interactions: Orchestrating Immune Responses by the Host and Antagonizing Immune Defense by Viruses, Frontiers in Immunology, Volume 9 (2018) | DOI

Cited by Sources: