Nuclear Envelope Breakdown Induced by Herpes Simplex Virus Type 1 Involves the Activity of Viral Fusion Proteins

Overview

Journal Virology

Specialty Microbiology

Date 2014 Jul 11

PMID 25010278

Citations 14

Authors

Martina Maric

Alison C Haugo

William Dauer

David Johnson

Richard J Roller

Affiliations

Soon will be listed here.

Abstract

Herpesvirus infection reorganizes components of the nuclear lamina usually without loss of integrity of the nuclear membranes. We report that wild-type HSV infection can cause dissolution of the nuclear envelope in transformed mouse embryonic fibroblasts that do not express torsinA. Nuclear envelope breakdown is accompanied by an eight-fold inhibition of virus replication. Breakdown of the membrane is much more limited during infection with viruses that lack the gB and gH genes, suggesting that breakdown involves factors that promote fusion at the nuclear membrane. Nuclear envelope breakdown is also inhibited during infection with virus that does not express UL34, but is enhanced when the US3 gene is deleted, suggesting that envelope breakdown may be enhanced by nuclear lamina disruption. Nuclear envelope breakdown cannot compensate for deletion of the UL34 gene suggesting that mixing of nuclear and cytoplasmic contents is insufficient to bypass loss of the normal nuclear egress pathway.

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References

Simpson-Holley M, Colgrove R, Nalepa G, Harper J, Knipe D . Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. J Virol. 2005; 79(20):12840-51. PMC: 1235858. DOI: 10.1128/JVI.79.20.12840-12851.2005. View

Chang Y, Van Sant C, Krug P, Sears A, Roizman B . The null mutant of the U(L)31 gene of herpes simplex virus 1: construction and phenotype in infected cells. J Virol. 1997; 71(11):8307-15. PMC: 192289. DOI: 10.1128/JVI.71.11.8307-8315.1997. View

Vargas J, Hatch E, Anderson D, Hetzer M . Transient nuclear envelope rupturing during interphase in human cancer cells. Nucleus. 2012; 3(1):88-100. PMC: 3342953. DOI: 10.4161/nucl.18954. View

Granata A, Schiavo G, Warner T . TorsinA and dystonia: from nuclear envelope to synapse. J Neurochem. 2009; 109(6):1596-609. DOI: 10.1111/j.1471-4159.2009.06095.x. View

Bjerke S, Roller R . Roles for herpes simplex virus type 1 UL34 and US3 proteins in disrupting the nuclear lamina during herpes simplex virus type 1 egress. Virology. 2006; 347(2):261-76. PMC: 2993110. DOI: 10.1016/j.virol.2005.11.053. View

Chen X, Hu X, Wu S, Zhang Y, Xiao B, Shang H . RNA interference-mediated inhibition of wild-type Torsin A expression increases apoptosis caused by oxidative stress in cultured cells. Neurochem Res. 2010; 35(8):1214-23. DOI: 10.1007/s11064-010-0177-4. View

Klupp B, Granzow H, Fuchs W, Keil G, Finke S, Mettenleiter T . Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci U S A. 2007; 104(17):7241-6. PMC: 1855391. DOI: 10.1073/pnas.0701757104. View

Klupp B, Granzow H, Mettenleiter T . Effect of the pseudorabies virus US3 protein on nuclear membrane localization of the UL34 protein and virus egress from the nucleus. J Gen Virol. 2001; 82(Pt 10):2363-2371. DOI: 10.1099/0022-1317-82-10-2363. View

Kim C, Perez A, Perkins G, Ellisman M, Dauer W . A molecular mechanism underlying the neural-specific defect in torsinA mutant mice. Proc Natl Acad Sci U S A. 2010; 107(21):9861-6. PMC: 2906867. DOI: 10.1073/pnas.0912877107. View

10.

Klupp B, Granzow H, Mettenleiter T . Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J Virol. 2000; 74(21):10063-73. PMC: 102045. DOI: 10.1128/jvi.74.21.10063-10073.2000. View

11.

Roller R, Bjerke S, Haugo A, Hanson S . Analysis of a charge cluster mutation of herpes simplex virus type 1 UL34 and its extragenic suppressor suggests a novel interaction between pUL34 and pUL31 that is necessary for membrane curvature around capsids. J Virol. 2010; 84(8):3921-34. PMC: 2849510. DOI: 10.1128/JVI.01638-09. View

12.

Roller R, Haugo A, Kopping N . Intragenic and extragenic suppression of a mutation in herpes simplex virus 1 UL34 that affects both nuclear envelope targeting and membrane budding. J Virol. 2011; 85(22):11615-25. PMC: 3209301. DOI: 10.1128/JVI.05730-11. View

13.

Reynolds A, Wills E, Roller R, Ryckman B, Baines J . Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J Virol. 2002; 76(17):8939-52. PMC: 136992. DOI: 10.1128/jvi.76.17.8939-8952.2002. View

14.

Nery F, Zeng J, Niland B, Hewett J, Farley J, Irimia D . TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J Cell Sci. 2008; 121(Pt 20):3476-86. PMC: 3539201. DOI: 10.1242/jcs.029454. View

15.

Fuchs W, Klupp B, Granzow H, Osterrieder N, Mettenleiter T . The interacting UL31 and UL34 gene products of pseudorabies virus are involved in egress from the host-cell nucleus and represent components of primary enveloped but not mature virions. J Virol. 2001; 76(1):364-78. PMC: 135715. DOI: 10.1128/jvi.76.1.364-378.2002. View

16.

Speese S, Ashley J, Jokhi V, Nunnari J, Barria R, Li Y . Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell. 2012; 149(4):832-46. PMC: 3371233. DOI: 10.1016/j.cell.2012.03.032. View

17.

Leach N, Bjerke S, Christensen D, Bouchard J, Mou F, Park R . Emerin is hyperphosphorylated and redistributed in herpes simplex virus type 1-infected cells in a manner dependent on both UL34 and US3. J Virol. 2007; 81(19):10792-803. PMC: 2045475. DOI: 10.1128/JVI.00196-07. View

18.

Hewett J, Tannous B, Niland B, Nery F, Zeng J, Li Y . Mutant torsinA interferes with protein processing through the secretory pathway in DYT1 dystonia cells. Proc Natl Acad Sci U S A. 2007; 104(17):7271-6. PMC: 1855419. DOI: 10.1073/pnas.0701185104. View

19.

Hewett J, Ziefer P, Bergeron D, Naismith T, Boston H, Slater D . TorsinA in PC12 cells: localization in the endoplasmic reticulum and response to stress. J Neurosci Res. 2003; 72(2):158-68. DOI: 10.1002/jnr.10567. View

20.

Naismith T, Heuser J, Breakefield X, Hanson P . TorsinA in the nuclear envelope. Proc Natl Acad Sci U S A. 2004; 101(20):7612-7. PMC: 419654. DOI: 10.1073/pnas.0308760101. View