Complex Mechanisms for the Packaging of the UL16 Tegument Protein into Herpes Simplex Virus

Overview

Journal Virology

Specialty Microbiology

Date 2010 Jan 7

PMID 20051283

Citations 32

Authors

David G Meckes Jr

Jacob A Marsh

John W Wills

Affiliations

Soon will be listed here.

Abstract

The conserved UL16 tegument protein of herpes simplex virus exhibits dynamic capsid-binding properties with a release mechanism that is triggered during initial virus attachment events. In an effort to understand the capsid association and subsequent release of UL16, we sought to define the mechanism by which this protein is packaged into virions. The data presented here support a model for the addition of some UL16 to capsids prior to their arrival at the TGN. UL16 was found on capsids isolated from cells infected with viruses lacking UL36, UL37 or gE/gD, which are defective for budding and accumulate non-enveloped capsids in the cytoplasm. Additionally, membrane-flotation experiments showed that UL16 co-purified with cytoplasmic capsids that are not associated with membranes. Moreover, the amount of UL16 packaged into extracellular particles was severely reduced in the absence of two conserved binding partners, UL21 or UL11.

Citing Articles

The loss of both pUL16 and pUL21 in HSV-1 infected cells abolishes cytoplasmic envelopment.

Roddy K, Grzesik P, Smith B, Ko N, Vashee S, Desai P bioRxiv. 2024; .

PMID: 39574695 PMC: 11581036. DOI: 10.1101/2024.11.10.622843.

Disruption of herpes simplex virus type 2 pUL21 phosphorylation impairs secondary envelopment of cytoplasmic nucleocapsids.

Finnen R, Muradov J, Le Sage V, Banfield B J Virol. 2024; 98(9):e0065624.

PMID: 39136460 PMC: 11406914. DOI: 10.1128/jvi.00656-24.

The precise function of alphaherpesvirus tegument proteins and their interactions during the viral life cycle.

Cui Y, Wang M, Cheng A, Zhang W, Yang Q, Tian B Front Microbiol. 2024; 15:1431672.

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The Herpes Simplex Virus pUL16 and pUL21 Proteins Prevent Capsids from Docking at Nuclear Pore Complexes.

Thomas E, Finnen R, Mewburn J, Archer S, Banfield B PLoS Pathog. 2023; 19(12):e1011832.

PMID: 38039340 PMC: 10718459. DOI: 10.1371/journal.ppat.1011832.

Features and Functions of the Conserved Herpesvirus Tegument Protein UL11 and Its Binding Partners.

Yang L, Wang M, Cheng A, Yang Q, Wu Y, Huang J Front Microbiol. 2022; 13:829754.

PMID: 35722336 PMC: 9205190. DOI: 10.3389/fmicb.2022.829754.

References

Nalwanga D, Rempel S, Roizman B, Baines J . The UL 16 gene product of herpes simplex virus 1 is a virion protein that colocalizes with intranuclear capsid proteins. Virology. 1996; 226(2):236-42. DOI: 10.1006/viro.1996.0651. View

Maclean C, Clark B, McGeoch D . Gene UL11 of herpes simplex virus type 1 encodes a virion protein which is myristylated. J Gen Virol. 1989; 70 ( Pt 12):3147-57. DOI: 10.1099/0022-1317-70-12-3147. View

Meckes Jr D, Wills J . Dynamic interactions of the UL16 tegument protein with the capsid of herpes simplex virus. J Virol. 2007; 81(23):13028-36. PMC: 2169088. DOI: 10.1128/JVI.01306-07. View

Baird N, Yeh P, Courtney R, Wills J . Sequences in the UL11 tegument protein of herpes simplex virus that control association with detergent-resistant membranes. Virology. 2008; 374(2):315-21. PMC: 2409213. DOI: 10.1016/j.virol.2008.01.007. View

Takakuwa H, Goshima F, KOSHIZUKA T, Murata T, Daikoku T, Nishiyama Y . Herpes simplex virus encodes a virion-associated protein which promotes long cellular processes in over-expressing cells. Genes Cells. 2001; 6(11):955-66. DOI: 10.1046/j.1365-2443.2001.00475.x. View

Klupp B, Bottcher S, Granzow H, Kopp M, Mettenleiter T . Complex formation between the UL16 and UL21 tegument proteins of pseudorabies virus. J Virol. 2005; 79(3):1510-22. PMC: 544144. DOI: 10.1128/JVI.79.3.1510-1522.2005. View

Baines J, Jacob R, Simmerman L, Roizman B . The herpes simplex virus 1 UL11 proteins are associated with cytoplasmic and nuclear membranes and with nuclear bodies of infected cells. J Virol. 1995; 69(2):825-33. PMC: 188648. DOI: 10.1128/JVI.69.2.825-833.1995. View

Silva M, Yu Q, Enquist L, Shenk T . Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument-associated capsids. J Virol. 2003; 77(19):10594-605. PMC: 228509. DOI: 10.1128/jvi.77.19.10594-10605.2003. View

Loomis J, Courtney R, Wills J . Binding partners for the UL11 tegument protein of herpes simplex virus type 1. J Virol. 2003; 77(21):11417-24. PMC: 229364. DOI: 10.1128/jvi.77.21.11417-11424.2003. View

10.

Yeh P, Meckes Jr D, Wills J . Analysis of the interaction between the UL11 and UL16 tegument proteins of herpes simplex virus. J Virol. 2008; 82(21):10693-700. PMC: 2573186. DOI: 10.1128/JVI.01230-08. View

11.

Baines J, Roizman B . The UL11 gene of herpes simplex virus 1 encodes a function that facilitates nucleocapsid envelopment and egress from cells. J Virol. 1992; 66(8):5168-74. PMC: 241400. DOI: 10.1128/JVI.66.8.5168-5174.1992. View

12.

Baines J, Roizman B . The open reading frames UL3, UL4, UL10, and UL16 are dispensable for the replication of herpes simplex virus 1 in cell culture. J Virol. 1991; 65(2):938-44. PMC: 239835. DOI: 10.1128/JVI.65.2.938-944.1991. View

13.

Saldanha C, Lubinski J, Martin C, Nagashunmugam T, Wang L, van Der Keyl H . Herpes simplex virus type 1 glycoprotein E domains involved in virus spread and disease. J Virol. 2000; 74(15):6712-9. PMC: 112186. DOI: 10.1128/jvi.74.15.6712-6719.2000. View

14.

Desai P . A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J Virol. 2000; 74(24):11608-18. PMC: 112442. DOI: 10.1128/jvi.74.24.11608-11618.2000. View

15.

Kopp M, Granzow H, Fuchs W, Klupp B, Mundt E, Karger A . The pseudorabies virus UL11 protein is a virion component involved in secondary envelopment in the cytoplasm. J Virol. 2003; 77(9):5339-51. PMC: 153988. DOI: 10.1128/jvi.77.9.5339-5351.2003. View

16.

Loomis J, Courtney R, Wills J . Packaging determinants in the UL11 tegument protein of herpes simplex virus type 1. J Virol. 2006; 80(21):10534-41. PMC: 1641780. DOI: 10.1128/JVI.01172-06. View

17.

Farnsworth A, Goldsmith K, Johnson D . Herpes simplex virus glycoproteins gD and gE/gI serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm. J Virol. 2003; 77(15):8481-94. PMC: 165244. DOI: 10.1128/jvi.77.15.8481-8494.2003. View

18.

Desai P, DeLuca N, Glorioso J, Person S . Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 abrogate capsid formation and cleavage of replicated DNA. J Virol. 1993; 67(3):1357-64. PMC: 237505. DOI: 10.1128/JVI.67.3.1357-1364.1993. View

19.

Schmitz J, Albright A, Kinchington P, Jenkins F . The UL37 protein of herpes simplex virus type 1 is associated with the tegument of purified virions. Virology. 1995; 206(2):1055-65. DOI: 10.1006/viro.1995.1028. View

20.

Kopp M, Granzow H, Fuchs W, Klupp B, Mettenleiter T . Simultaneous deletion of pseudorabies virus tegument protein UL11 and glycoprotein M severely impairs secondary envelopment. J Virol. 2004; 78(6):3024-34. PMC: 353770. DOI: 10.1128/jvi.78.6.3024-3034.2004. View