The Pivotal Roles of US3 Protein in Cell-to-Cell Spread and Virion Nuclear Egress of Duck Plague Virus.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
28 04 2020
Historique:
received: 05 11 2019
accepted: 10 04 2020
entrez: 30 4 2020
pubmed: 30 4 2020
medline: 26 11 2020
Statut: epublish

Résumé

The duck plague virus (DPV) US3 protein, a homolog of the herpes simplex virus-1 (HSV-1) US3 protein that is reported to be critical for viral replication, has been minimally studied. Therefore, to investigate the function of the DPV US3 protein, we used scarless Red recombination technology based on an infectious bacterial artificial chromosome (BAC) containing the DPV Chinese virulent strain (CHv) genome and successfully constructed and rescued a US3-deleted mutant and the corresponding revertant virus (BAC-CHv-ΔUS3 and BAC-CHv-ΔUS3R, respectively). For viral growth characteristics, compared to the parental and revertant viruses, the US3-deleted mutant showed an approximately 100-fold reduction in viral titers but no significant reduction in genome copies, indicating that the US3-deleted mutant exhibited decreased viral replication but not decreased viral DNA generation. In addition, the US3-deleted mutant formed viral plaques that were 33% smaller on average than those formed by the parental and revertant viruses, demonstrating that US3 protein affected the viral cell-to-cell spread of DPV. Finally, the results of electron microscopy showed that the deletion of US3 resulted in a large number of virions accumulating in the nucleus and perinuclear space, thus blocking virion nuclear egress. In this study, we found that the DPV US3 protein played pivotal roles in viral replication by promoting viral cell-to-cell spread and virion nuclear egress, which may provide some references for research on the function of the DPV US3 protein.

Identifiants

pubmed: 32346128
doi: 10.1038/s41598-020-64190-2
pii: 10.1038/s41598-020-64190-2
pmc: PMC7189242
doi:

Substances chimiques

Viral Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

7181

Références

Cheng, A. Duck plague (ed. Cheng A.) 1–4 (Beijing, 2015).
Ying, W. et al. Complete genomic sequence of Chinese virulent duck enteritis virus. Journal of Virology 86, 5965, https://doi.org/10.1128/JVI.00529-12 (2012).
doi: 10.1128/JVI.00529-12
Ying, W. et al. Comparative genomic analysis of duck enteritis virus strains. Journal of Virology 86, 13841–13842, https://doi.org/10.1128/JVI.01517-12 (2012).
doi: 10.1128/JVI.01517-12
Liu, C. et al. Duck enteritis virus UL54 is an IE protein primarily located in the nucleus. Virology Journal 12, 198, https://doi.org/10.1186/s12985-015-0424-z (2015).
doi: 10.1186/s12985-015-0424-z pubmed: 26606920 pmcid: 4658773
Liu, C. et al. Characterization of nucleocytoplasmic shuttling and intracellular localization signals in Duck Enteritis Virus UL54. Biochimie 127, 86–94, https://doi.org/10.1016/j.biochi (2016).
doi: 10.1016/j.biochi pubmed: 27157269
Liu, C. et al. Regulation of viral gene expression by duck enteritis virus UL54. Scientific Reports 7, 1076, https://doi.org/10.1038/s41598-017-01161-0 (2017).
doi: 10.1038/s41598-017-01161-0 pubmed: 28432334 pmcid: 5430722
Gao, X. et al. Duck enteritis virus (DEV) UL54 protein, a novel partner, interacts with DEV UL24 protein. Virology Journal 14, 166, https://doi.org/10.1186/s12985-017-0830-5 (2017).
doi: 10.1186/s12985-017-0830-5 pubmed: 28851454 pmcid: 5575879
Hu, X. et al. The duck enteritis virus early protein, UL13, found in both nucleus and cytoplasm, influences viral replication in cell culture. Poultry Science 96, https://doi.org/10.3382/ps/pex043 (2017).
Gao, J. et al. Identification and characterization of the duck enteritis virus (DEV) US2 gene. Genetics & Molecular Research Gmr 14, 13779, https://doi.org/10.4238/2015 (2015).
doi: 10.4238/2015
Zhao, C. et al. Molecular characterization and antiapoptotic function analysis of the duck plague virus Us5 gene. Scientific Reports 9, 1–14, https://doi.org/10.1038/s41598-019-41311-0 (2019).
doi: 10.1038/s41598-019-41311-0
Zhang, D. et al. Molecular characterization of the duck enteritis virus US10 protein. Virology Journal 14, 183, https://doi.org/10.1186/s12985-017-0841-2 (2017).
doi: 10.1186/s12985-017-0841-2 pubmed: 28931412 pmcid: 5607491
He, Q. et al. Replication kinetics of duck enteritis virus UL16 gene in vitro. Virology Journal 9, 1–4, https://doi.org/10.1186/1743-422X-9-281 (2012).
doi: 10.1186/1743-422X-9-281
Ming-Sheng, C. et al. Characterization of the duck plague virus UL35 gene. Intervirology 53, 408–416, https://doi.org/10.1159/000317291 (2010).
doi: 10.1159/000317291
He, T. et al. Molecular characterization of duck enteritis virus UL41 protein. Virology Journal 15, 12, https://doi.org/10.1186/s12985-018-0928-4 (2018).
doi: 10.1186/s12985-018-0928-4 pubmed: 29334975 pmcid: 5769551
Zhang, S. et al. Characterization of duck enteritis virus UL53 gene and glycoprotein K. Virology Journal 8, 235–235, https://doi.org/10.1186/1743-422X-8-235 (2011).
doi: 10.1186/1743-422X-8-235 pubmed: 21586146 pmcid: 3120784
Wu, Y. et al. Establishment of real-time quantitative reverse transcription polymerase chain reaction assay for transcriptional analysis of duck enteritis virus UL55 gene. Virology Journal 8, 266 (2011).
doi: 10.1186/1743-422X-8-266
You, Y. et al. Duck plague virus Glycoprotein J is functional but slightly impaired in viral replication and cell-to-cell spread. Scientific Reports 8, 4069, https://doi.org/10.1038/s41598-018-22447-x (2018).
doi: 10.1038/s41598-018-22447-x pubmed: 29511274 pmcid: 5840427
Ma, Y., Zeng, Q., Wang, M., Cheng, A. & Chen, X. US10 Protein Is Crucial but not Indispensable for Duck Enteritis Virus Infection in Vitro. Scientific Reports 8, 16510, https://doi.org/10.1038/s41598-018-34503-7 (2018).
doi: 10.1038/s41598-018-34503-7 pubmed: 30405139 pmcid: 6220328
Wu, Y. et al. Preliminary study of the UL55 gene based on infectious Chinese virulent duck enteritis virus bacterial artificial chromosome clone. Virology Journal 14, 78, https://doi.org/10.1186/s12985-017-0748-y (2017).
doi: 10.1186/s12985-017-0748-y pubmed: 28407817 pmcid: 5390382
Akihisa, K. et al. Identification of proteins phosphorylated directly by the Us3 protein kinase encoded by herpes simplex virus 1. Journal of Virology 79, 9325–9331 (2005).
doi: 10.1128/JVI.79.14.9325-9331.2005
Akihisa, K. et al. Herpes simplex virus 1 protein kinase Us3 and major tegument protein UL47 reciprocally regulate their subcellular localization in infected cells. Journal of Virology 85, 9599, https://doi.org/10.1128/JVI.00845-11 (2011).
doi: 10.1128/JVI.00845-11
Kato, A. et al. Herpes simplex virus 1 protein kinase Us3 phosphorylates viral envelope glycoprotein B and regulates its expression on the cell surface. Journal of Virology 83, 250–261 (2009).
doi: 10.1128/JVI.01451-08
Mou, F., Forest, T. & Baines, J. D. US3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. Journal of Virology 81, 6459–6470, https://doi.org/10.1128/JVI.01451-08 (2007).
doi: 10.1128/JVI.01451-08 pubmed: 17428859 pmcid: 1900093
Wang, K., Ni, L., Wang, S. & Zheng, C. Herpes Simplex Virus 1 Protein Kinase US3 Hyperphosphorylates p65/RelA and Dampens NF-κB Activation. Journal of Virology 88, 7941–7951, https://doi.org/10.1128/JVI.03394-13 (2014).
doi: 10.1128/JVI.03394-13 pubmed: 24807716 pmcid: 4097809
Shuai, W., Kezhen, W., Rongtuan, L. & Chunfu, Z. Herpes Simplex Virus 1 Serine/Threonine Kinase US3 Hyperphosphorylates IRF3 and Inhibits Beta Interferon Production. Journal of Virology 87, 12814–12827, https://doi.org/10.1128/JVI.02355-13 (2013).
doi: 10.1128/JVI.02355-13
Céline, V. D. B. et al. Alphaherpesvirus US3-mediated reorganization of the actin cytoskeleton is mediated by group A p21-activated kinases. Proceedings of the National Academy of Sciences of the United States of America 106, 8707–8712, https://doi.org/10.1073/pnas.0900436106 (2009).
doi: 10.1073/pnas.0900436106
Ching-Dong, C. et al. Suppression of apoptosis by pseudorabies virus Us3 protein kinase through the activation of PI3-K/Akt and NF-κB pathways. Research in Veterinary Science 95, 764–774, https://doi.org/10.1016/j.rvsc (2013).
doi: 10.1016/j.rvsc
Reynolds, A. E., Wills, E. G., Roller, R. J., Ryckman, B. J. & Baines, J. D. Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. Journal of Virology 76, 8939 (2002).
doi: 10.1128/JVI.76.17.8939-8952.2002
Zhuoming, L. et al. Herpes simplex virus 1 UL47 interacts with viral nuclear egress factors UL31, UL34, and Us3 and regulates viral nuclear egress. Journal of Virology 88, 4657, https://doi.org/10.1128/JVI.00137-14 (2014).
doi: 10.1128/JVI.00137-14
Takahiko, I., Ken, S., Jun, A. & Yasushi, K. Effects of phosphorylation of herpes simplex virus 1 envelope glycoprotein B by Us3 kinase in vivo and in vitro. Journal of Virology 84, 153, https://doi.org/10.1128/JVI.01447-09 (2010).
doi: 10.1128/JVI.01447-09
Mou, F., Wills, E. G., Park, R. & Baines, J. D. Effects of lamin A/C, lamin B1, and viral US3 kinase activity on viral infectivity, virion egress, and the targeting of herpes simplex virus U(L)34-encoded protein to the inner nuclear membrane. Journal of Virology 82, 8094, https://doi.org/10.1128/JVI.00874-08 (2008).
doi: 10.1128/JVI.00874-08 pubmed: 18524819 pmcid: 2519571
Favoreel, H. W., Minnebruggen, G. V., Adriaensen, D. & Nauwynck, H. J. Cytoskeletal rearrangements and cell extensions induced by the US3 kinase of an alphaherpesvirus are associated with enhanced spread. Proceedings of the National Academy of Sciences of the United States of America 102, 8990 (2005).
doi: 10.1073/pnas.0409099102
Deng, L. et al. Suppression of NF-κB Activity: A Viral Immune Evasion Mechanism. Viruses 10, 409, https://doi.org/10.3390/v10080409 (2018).
doi: 10.3390/v10080409 pmcid: 6115930
You, Y. et al. The suppression of apoptosis by α-herpesvirus. Cell Death & Disease 8, e2749, https://doi.org/10.1038/cddis (2017).
doi: 10.1038/cddis
Wu, Y. Genome analysis of duck plague virus Chinese virulent strain and preliminary study of UL55 gene fuction. Sichuan Agricultural University (2015).
Tischer, B. K., Smith, G. A. & Osterrieder, N. En passant mutagenesis: a two step markerless red recombination system. Methods Mol Biol 634, 421–430, https://doi.org/10.1007/978-1-60761-652-8_30 (2010).
doi: 10.1007/978-1-60761-652-8_30 pubmed: 20677001
Daniel, S., Caleb, M. K., Kaufer, B. B. & Nikolaus, O. Enzymatically inactive U(S)3 protein kinase of Marek’s disease virus (MDV) is capable of depolymerizing F-actin but results in accumulation of virions in perinuclear invaginations and reduced virus growth. Virology 375, 37–47, https://doi.org/10.1016/j.virol (2008).
doi: 10.1016/j.virol
Proft, A. et al. The Role of the Equine Herpesvirus Type 1 (EHV-1) US3-Encoded Protein Kinase in Actin Reorganization and Nuclear Egress. Viruses 8, 275 (2016).
doi: 10.3390/v8100275
Wisner, T. W. et al. Herpesvirus gB-Induced Fusion between the Virion Envelope and Outer Nuclear Membrane during Virus Egress Is Regulated by the Viral US3 Kinase. Journal of Virology 83, 3115–3126, https://doi.org/10.1128/JVI.01462-08 (2009).
doi: 10.1128/JVI.01462-08 pubmed: 19158241 pmcid: 2655551
Wisner, T. W. et al. Herpesvirus gB-induced fusion between the virion envelope and outer nuclear membrane during virus egress is regulated by the viral US3 kinase. Journal of Virology 83, 3115–3126, https://doi.org/10.1128/JVI.01462-08 (2009).
doi: 10.1128/JVI.01462-08 pubmed: 19158241 pmcid: 2655551
Mettenleiter, T. C., Müller, F., Granzow, H. & Klupp, B. G. The way out: what we know and do not know about herpesvirus nuclear egress. Cellular Microbiology 15, 170–178 (2013).
doi: 10.1111/cmi.12044
Roller, R. J., Zhou, Y., Schnetzer, R., Ferguson, J. & Desalvo, D. Herpes simplex virus type 1 U(L)34 gene product is required for viral envelopment. Journal of Virology 74, 117 (2000).
doi: 10.1128/JVI.74.1.117-129.2000
Chang, Y. E. et al. The null mutant of the U(L)31 gene of herpes simplex virus 1: construction and phenotype in infected cells. Journal of Virology 71, 8307–8315 (1997).
doi: 10.1128/JVI.71.11.8307-8315.1997
Carmichael, J. C., Yokota, H., Craven, R. C., Schmitt, A. & Wills, J. W. The HSV-1 mechanisms of cell-to-cell spread and fusion are critically dependent on host PTP1B. Plos Pathogens 14, e1007054 (2018).
doi: 10.1371/journal.ppat.1007054
Quentin, S. Avoiding the void: cell-to-cell spread of human viruses. Nature Reviews Microbiology 6, 815–826, https://doi.org/10.1038/nrmicro1972 (2008).
doi: 10.1038/nrmicro1972
Thary, J., Céline, V. D. B., Cliff, V. W., Leen, V. T. & Favoreel, H. W. Pseudorabies virus US3 triggers RhoA phosphorylation to reorganize the actin cytoskeleton. Journal of General Virology 96, 2328–2335, https://doi.org/10.1099/vir.0.000152 (2015).
doi: 10.1099/vir.0.000152
Thary, J. et al. Alphaherpesviral US3 kinase induces cofilin dephosphorylation to reorganize the actin cytoskeleton. Journal of Virology 87, 4121–4126, https://doi.org/10.1128/JVI.03107-12 (2013).
doi: 10.1128/JVI.03107-12

Auteurs

Liyao Deng (L)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Mingshu Wang (M)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China. mshwang@163.com.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China. mshwang@163.com.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China. mshwang@163.com.

Anchun Cheng (A)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China. chenganchun@vip.163.com.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China. chenganchun@vip.163.com.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China. chenganchun@vip.163.com.

Qiao Yang (Q)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Ying Wu (Y)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Renyong Jia (R)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Shun Chen (S)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Dekang Zhu (D)

Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Mafeng Liu (M)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Xinxin Zhao (X)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Shaqiu Zhang (S)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Juan Huang (J)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Xumin Ou (X)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Sai Mao (S)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Ling Zhang (L)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Yunya Liu (Y)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Yanling Yu (Y)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Bin Tian (B)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Leichang Pan (L)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Mujeeb Ur Rehman (MU)

Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Xiaoyue Chen (X)

Avian Disease Research Center, College of Veterinary Medicine of Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.
Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Wenjiang, 611130, People's Republic of China.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH