REVIEW

Remodeling of host membranes during herpesvirus assembly and egress

  • Ying Lv 1,2 ,
  • Sheng Zhou 1,2 ,
  • Shengyan Gao 1 ,
  • Hongyu Deng , 1,2,3
Expand
  • 1. CAS Key Laboratory of Infection and Immunity, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
  • 2. University of Chinese Academy of Sciences, Beijing 100049, China
  • 3. CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China

Received date: 13 Feb 2018

Accepted date: 21 Aug 2018

Published date: 15 May 2019

Copyright

2018 The Author(s)

Abstract

Many viruses, enveloped or non-enveloped, remodel host membrane structures for their replication, assembly and escape from host cells. Herpesviruses are important human pathogens and cause many diseases. As large enveloped DNA viruses, herpesviruses undergo several complex steps to complete their life cycles and produce infectious progenies. Firstly, herpesvirus assembly initiates in the nucleus, producing nucleocapsids that are too large to cross through the nuclear pores. Nascent nucleocapsids instead bud at the inner nuclear membrane to form primary enveloped virions in the perinuclear space followed by fusion of the primary envelopes with the outer nuclear membrane, to translocate the nucleocapsids into the cytoplasm. Secondly, nucleocapsids obtain a series of tegument proteins in the cytoplasm and bud into vesicles derived from host organelles to acquire viral envelopes. The vesicles are then transported to and fuse with the plasma membrane to release the mature virions to the extracellular space. Therefore, at least two budding and fusion events take place at cellular membrane structures during herpesviruses assembly and egress, which induce membrane deformations. In this review, we describe and discuss how herpesviruses exploit and remodel host membrane structures to assemble and escape from the host cell.

Cite this article

Ying Lv , Sheng Zhou , Shengyan Gao , Hongyu Deng . Remodeling of host membranes during herpesvirus assembly and egress[J]. Protein & Cell, 2019 , 10(5) : 315 -326 . DOI: 10.1007/s13238-018-0577-9

1
Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT (2007) The molecular architecture of the nuclear pore complex. Nature 450:695–701

DOI

2
Baumann O, Walz B (2001) Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 205:149–214

DOI

3
Behnia R, Munro S (2005) Organelle identity and the signposts for membrane traffic. Nature 438:597–604

DOI

4
Beitia Ortiz de Zarate I, Kaelin K, Rozenberg F (2004) Effects of mutations in the cytoplasmic domain of herpes simplex virus type 1 glycoprotein B on intracellular transport and infectivity. J Virol 78:1540–1551

DOI

5
Bigalke JM, Heuser T, Nicastro D, Heldwein EE (2014) Membrane deformation and scission by the HSV-1 nuclear egress complex. Nat Commun 5:4131

DOI

6
Buckingham EM, Carpenter JE, Jackson W, Zerboni L, Arvin AM, Grose C (2015) Autophagic flux without a block differentiates varicella-zoster virus infection from herpes simplex virus infection. Proc Natl Acad Sci USA 112:256–261

DOI

7
Buckingham EM, Jarosinski KW, Jackson W, Carpenter JE, Grose C (2016) Exocytosis of varicella-zoster virus virions involves a convergence of endosomal and autophagy pathways. J Virol 90:8673–8685

DOI

8
Campadelli G, Brandimarti R, Di Lazzaro C, Ward PL, Roizman B, Torrisi MR (1993) Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc Natl Acad Sci USA 90:2798–2802

DOI

9
Cano-Monreal GL, Wylie KM, Cao F, Tavis JE, Morrison LA (2009) Herpes simplex virus 2 UL13 protein kinase disrupts nuclear lamins. Virology 392:137–147

DOI

10
Chang YE, Roizman B (1993) The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. J Virol 67:6348–6356

11
Chen S, Novick P,Ferro-Novick S (2013) ER structure and function. Curr Opin Cell Biol 25:428–433

DOI

12
Davison AJ, Eberle R, Ehlers B, Hayward GS, McGeoch DJ, Minson AC, Pellett PE, Roizman B, Studdert MJ, Thiry E (2009) The order Herpesvirales. Arch Virol 154:171–177

DOI

13
Desai PJ, Pryce EN, Henson BW, Luitweiler EM, Cothran J (2012) Reconstitution of the Kaposi’s sarcoma-associated herpesvirus nuclear egress complex and formation of nuclear membrane vesicles by coexpression of ORF67 and ORF69 gene products. J Virol 86:594–598

DOI

14
DuRaine G, Wisner TW, Howard P, Williams M,Johnson DC (2017) Herpes simplex virus gE/gI and US9 promote both envelopment and sorting of virus particles in the cytoplasm of neurons, two processes that precede anterograde transport in axons. J Virol.https://doi.org/10.1128/JVI.00050-17

DOI

15
Farnsworth A, Goldsmith K, Johnson DC (2003) Herpes simplex virus glycoproteins gD and gE/gI serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm. J Virol 77:8481–8494

DOI

16
Farnsworth A, Wisner TW, Webb M, Roller R, Cohen G, Eisenberg R, Johnson DC (2007) Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane. Proc Natl Acad Sci USA 104:10187–10192

DOI

17
Gao J, Hay TJM, Banfield BW (2017) The product of the herpes simplex virus 2 UL16 gene is critical for the egress of capsids from the nuclei of infected cells. J Virol.https://doi.org/10.1128/JVI.00350-17

DOI

18
Gershburg S,Geltz J, Peterson KE, Halford WP, Gershburg E (2015) The UL13 and US3 protein kinases of herpes simplex virus 1 cooperate to promote the assembly and release of mature, infectious virions. PLoS ONE 10:e0131420

DOI

19
Goldberg MW, Fiserova J, Huttenlauch I, Stick R (2008) A new model for nuclear lamina organization. Biochem Soc Trans 36:1339–1343

DOI

20
Granato M, Santarelli R, Farina A,Gonnella R, Lotti LV, Faggioni A, Cirone M (2014) Epstein-Barr virus blocks the autophagic flux and appropriates the autophagic machinery to enhance viral replication. J Virol 88:12715–12726

DOI

21
Granzow H, Klupp BG, Fuchs W, Veits J, Osterrieder N, Mettenleiter TC (2001) Egress of alphaherpesviruses: comparative ultrastructural study. J Virol 75:3675–3684

DOI

22
Grimm KS, Klupp BG, Granzow H, Muller FM, Fuchs W, Mettenleiter TC (2012) Analysis of viral and cellular factors influencing herpesvirus-induced nuclear envelope breakdown. J Virol 86:6512–6521

DOI

23
Gu F, Crump C, Thomas G (2001) Trans-Golgi network sorting. Cell Mol Life Sci 58:1067–1084

DOI

24
Guo H, Wang L, Peng L, Zhou ZH, Deng H (2009) Open reading frame 33 of a gammaherpesvirus encodes a tegument protein essential for virion morphogenesis and egress. J Virol 83:10582–10595

DOI

25
Guo H, Shen S,Wang L, Deng H (2010) Role of tegument proteins in herpesvirus assembly and egress. Protein Cell 1:987–998

DOI

26
Guttinger S, Laurell E, Kutay U (2009) Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 10:178–191

DOI

27
Hagen C, Dent KC, Zeev-Ben-Mordehai T, Grange M, Bosse JB, Whittle C, Klupp BG, Siebert CA, Vasishtan D, Bauerlein FJ (2015) Structural basis of vesicle formation at the inner nuclear membrane. Cell 163:1692–1701

DOI

28
Hampton CM, Strauss JD, Ke Z,Dillard RS, Hammonds JE, Alonas E, Desai TM, Marin M, Storms RE, Leon F (2017) Correlated fluorescence microscopy and cryo-electron tomography of virusinfected or transfected mammalian cells. Nat Protoc 12:150–167

DOI

29
Han J, Chadha P, Starkey JL, Wills JW (2012) Function of glycoprotein E of herpes simplex virus requires coordinated assembly of three tegument proteins on its cytoplasmic tail. Proc Natl Acad Sci USA 109:19798–19803

DOI

30
Harley CA, Dasgupta A, Wilson DW (2001) Characterization of herpes simplex virus-containing organelles by subcellular fractionation: role for organelle acidification in assembly of infectious particles. J Virol 75:1236–1251

DOI

31
Heald R, McKeon F (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61:579–589

DOI

32
Hirohata Y, Arii J, Liu Z, Shindo K, Oyama M, Kozuka-Hata H, Sagara H, Kato A, Kawaguchi Y (2015) Herpes simplex virus 1 recruits CD98 heavy chain and beta1 integrin to the nuclear membrane for Viral de-envelopment. J Virol 89:7799–7812

DOI

33
Hofemeister H, O’Hare P (2008) Nuclear pore composition and gating in herpes simplex virus-infected cells. J Virol 82:8392–8399

DOI

34
Hogue IB, Bosse JB, Hu J-R, Thiberge SY, Enquist LW (2014) Cellular mechanisms of alpha herpesvirus egress: live cell fluorescence microscopy of pseudorabies virus exocytosis. PLoS Pathog 10:e1004535

DOI

35
Homman-Loudiyi M, Hultenby K, Britt W, Soderberg-Naucler C (2003) Envelopment of human cytomegalovirus occurs by budding into Golgi-derived vacuole compartments positive for gB, Rab 3, trans-golgi network 46, and mannosidase II. J Virol 77:3191–3203

DOI

36
Jia X, Shen S, Lv Y, Zhang Z, Guo H, Deng H (2016) Tegument protein ORF45 plays an essential role in virion morphogenesis of murine gammaherpesvirus 68. J Virol 90:7587–7592

DOI

37
Johnson DC, Baines JD (2011) Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 9:382–394

DOI

38
Johnson DC, Webb M, Wisner TW, Brunetti C (2001) Herpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread. J Virol 75:821–833

DOI

39
Klupp BG, Granzow H, Mettenleiter TC (2000) Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J Virol 74:10063–10073

DOI

40
Klupp BG, Granzow H, Fuchs W, Keil GM, Finke S, Mettenleiter TC (2007) Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci USA 104:7241–7246

DOI

41
Klupp BG, Hellberg T, Granzow H, Franzke K, Dominguez Gonzalez B, Goodchild RE, Mettenleiter TC (2017) Integrity of the linker of nucleoskeleton and cytoskeleton is required for efficient herpesvirus nuclear egress. J Virol 91:e0033017

DOI

42
Kobayashi S, Iwamoto M, Haraguchi T (2016) Live correlative lightelectron microscopy to observe molecular dynamics in high resolution. Microscopy (Oxf) 65:296–308

DOI

43
Kochin V, Shimi T, Torvaldson E, Adam SA, Goldman A, Pack CG, Melo-Cardenas J, Imanishi SY, Goldman RD, Eriksson JE (2014) Interphase phosphorylation of lamin A. J Cell Sci 127:2683–2696

DOI

44
Kurokawa K, Ishii M, Suda Y, Ichihara A, Nakano A (2013) Live cell visualization of Golgi membrane dynamics by super-resolution confocal live imaging microscopy. Methods Cell Biol 118:235–242

DOI

45
Le Sage V, Jung M, Alter JD, Wills EG, Johnston SM, Kawaguchi Y, Baines JD, Banfield BW (2013) The herpes simplex virus 2 UL21 protein is essential for virus propagation. J Virol 87:5904–5915

DOI

46
Leach N, Bjerke SL, Christensen DK, Bouchard JM, Mou F, Park R, Baines J, Haraguchi T, Roller RJ (2007) Emerin is hyperphosphorylated and redistributed in herpes simplex virus type 1-infected cells in a manner dependent on both UL34 and US3. J Virol 81:10792–10803

DOI

47
Lee CP, Chen MR (2010) Escape of herpesviruses from the nucleus. Rev Med Virol 20:214–230

DOI

48
Lee CP, Huang YH, Lin SF, Chang Y, Chang YH, Takada K, Chen MR (2008) Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J Virol 82:11913–11926

DOI

49
Lee CP, Liu PT, Kung HN, Su MT, Chua HH, Chang YH, Chang CW, Tsai CH, Liu FT, Chen MR (2012) The ESCRT machinery is recruited by the viral BFRF1 protein to the nucleus-associated membrane for the maturation of Epstein-Barr Virus. PLoS Pathog 8:e1002904

DOI

50
Lee CP, Liu GT, Kung HN, Liu PT, Liao YT, Chow LP, Chang LS, Chang YH, Chang CW, Shu WC (2016) The ubiquitin ligase itch and ubiquitination regulate BFRF1-mediated nuclear envelope modification for Epstein-Barr virus maturation. J Virol 90:8994–9007

DOI

51
Li D, Shao L,Chen BC, Zhang X, Zhang M, Moses B, Milkie DE, Beach JR, Hammer JA 3rd, Pasham M (2015) Extendedresolution structured illumination imaging of endocytic and cytoskeletal dynamics. Science 349:aab3500

DOI

52
Liu Z, Kato A, Shindo K, Noda T, Sagara H, Kawaoka Y, Arii J, Kawaguchi Y (2014) Herpes simplex virus 1 UL47 interacts with viral nuclear egress factors UL31, UL34, and Us3 and regulates viral nuclear egress. J Virol 88:4657–4667

DOI

53
Liu Z, Kato A, Oyama M, Kozuka-Hata H, Arii J, Kawaguchi Y (2015) Role of host cell p32 in herpes simplex virus 1 de-envelopment during viral nuclear egress. J Virol 89:8982–8998

DOI

54
Liu GT, Kung HN, Chen CK, Huang C, Wang YL, Yu CP, Lee CP (2018) Improving nuclear envelope dynamics by EBV BFRF1 facilitates intranuclear component clearance through autophagy. FASEB J 32(7):3968–3983. https://doi.org/10.1096/fj. 201701253R

DOI

55
Lorenz M, Vollmer B, Unsay JD, Klupp BG, Garcia-Saez AJ, Mettenleiter TC, Antonin W (2015) A single herpesvirus protein can mediate vesicle formation in the nuclear envelope. J Biol Chem 290:6962–6974

DOI

56
Maeda F, Arii J, Hirohata Y,Maruzuru Y, Koyanagi N, Kato A, Kawaguchi Y (2017) Herpes simplex virus 1 UL34 protein regulates the global architecture of the endoplasmic reticulum in infected cells. J Virol.https://doi.org/10.1128/JVI.00271-17

DOI

57
Maric M, Haugo AC, Dauer W, Johnson D, Roller RJ (2014) Nuclear envelope breakdown induced by herpes simplex virus type 1 involves the activity of viral fusion proteins. Virology 460– 461:128–137

DOI

58
Marschall M, Marzi A, aus dem Siepen P, Jochmann R, Kalmer M, Auerochs S, Lischka P, Leis M, Stamminger T (2005) Cellular p32 recruits cytomegalovirus kinase pUL97 to redistribute the nuclear lamina. J Biol Chem 280:33357–33367

DOI

59
Maruzuru Y, Shindo K, Liu Z,Oyama M, Kozuka-Hata H, Arii J, Kato A, Kawaguchi Y (2014) Role of herpes simplex virus 1 immediate early protein ICP22 in viral nuclear egress. J Virol 88:7445–7454

DOI

60
Mauthe M, Langereis M, Jung J, Zhou X, Jones A, Omta W, Tooze SA, Stork B, Paludan SR, Ahola T (2016) An siRNA screen for ATG protein depletion reveals the extent of the unconventional functions of the autophagy proteome in virus replication. J Cell Biol 214:619–635

DOI

61
McMillan TN, Johnson DC (2001) Cytoplasmic domain of herpes simplex virus gE causes accumulation in the trans-Golgi network, a site of virus envelopment and sorting of virions to cell junctions. J Virol 75:1928–1940

DOI

62
Mettenleiter TC, Klupp BG, Granzow H (2009) Herpesvirus assembly: an update. Virus Res 143:222–234

DOI

63
Milbradt J,Webel R, Auerochs S, Sticht H, Marschall M (2010) Novel mode of phosphorylation-triggered reorganization of the nuclear lamina during nuclear egress of human cytomegalovirus. J Biol Chem 285:13979–13989

DOI

64
Milbradt J, Hutterer C, Bahsi H, Wagner S, Sonntag E, Horn AH, Kaufer BB, Mori Y, Sticht H, Fossen T (2016) The prolyl isomerase Pin1 promotes the herpesvirus-induced phosphorylation-dependent disassembly of the nuclear lamina required for nucleocytoplasmic egress. PLoS Pathog 12:e1005825

DOI

65
Miller S, Krijnse-Locker J(2008) Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6:363–374

DOI

66
Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140:313–326

DOI

67
Morris JB, Hofemeister H, O’Hare P (2007) Herpes simplex virus infection induces phosphorylation and delocalization of emerin, a key inner nuclear membrane protein. J Virol 81:4429–4437

DOI

68
Mou F, Wills E, Baines JD (2009) Phosphorylation of the U(L)31 protein of herpes simplex virus 1 by the U(S)3-encoded kinase regulates localization of the nuclear envelopment complex and egress of nucleocapsids. J Virol 83:5181–5191

DOI

69
Munz C (2017) The autophagic machinery in viral exocytosis. Front Microbiol 8:269

DOI

70
Nagel CH, Dohner K, Fathollahy M, Strive T, Borst EM, Messerle M, Sodeik B (2008) Nuclear egress and envelopment of herpes simplex virus capsids analyzed with dual-color fluorescence HSV1(17+). J Virol 82:3109–3124

DOI

71
Nanbo A, Noda T, Ohba Y (2018) Epstein-Barr virus acquires its final envelope on intracellular compartments with Golgi markers. Front Microbiol 9:454

DOI

72
Nowag H, Guhl B, Thriene K, Romao S, Ziegler U, Dengjel J, Munz C (2014) Macroautophagy proteins assist Epstein Barr virus production and get incorporated into the virus particles. EBioMedicine 1:116–125

DOI

73
Owen D, Crump C, Graham S (2015) Tegument assembly and secondary envelopment of alphaherpesviruses. Viruses 7:5084–5114

DOI

74
Park R, Baines JD (2006) Herpes simplex virus type 1 infection induces activation and recruitment of protein kinase C to the nuclear membrane and increased phosphorylation of lamin B. J Virol 80:494–504

DOI

75
Peng L, Ryazantsev S, Sun R, Zhou ZH (2010) Three-dimensional visualization of gammaherpesvirus life cycle in host cells by electron tomography. Structure 18:47–58

DOI

76
Peter M, Nakagawa J, Doree M, Labbe J, Nigg E (1990) In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 61:591–602

DOI

77
Reichelt M, Joubert L, Perrino J, Koh AL, Phanwar I, Arvin AM (2012) 3D reconstruction of VZV infected cell nuclei and PML nuclear cages by serial section array scanning electron microscopy and electron tomography. PLoS Pathog 8:e1002740

DOI

78
Remillard-Labrosse G,Mihai C, Duron J, Guay G, Lippe R (2009) Protein kinase D-dependent trafficking of the large Herpes simplex virus type 1 capsids from the TGN to plasma membrane. Traffic 10:1074–1083

DOI

79
Reynolds AE, Ryckman BJ, Baines JD, Zhou Y, Liang L, Roller RJ (2001) UL31 and UL34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J Virol 75:8803–8817

DOI

80
Reynolds AE, Liang L, Baines JD (2004) Conformational changes in the nuclear lamina induced by herpes simplex virus type 1 require genes U(L)31 and U(L)34. J Virol 78:5564–5575

DOI

81
Richetta C, Faure M (2013) Autophagy in antiviral innate immunity. Cell Microbiol 15:368–376

DOI

82
Roberts KL, Baines JD (2010) Myosin Va enhances secretion of herpes simplex virus 1 virions and cell surface expression of viral glycoproteins. J Virol 84:9889–9896

DOI

83
Scott ES, O’Hare P (2001) Fate of the inner nuclear membrane protein lamin B receptor and nuclear lamins in herpes simplex virus type 1 infection. J Virol 75:8818–8830

DOI

84
Sharma M, Coen DM (2014) Comparison of effects of inhibitors of viral and cellular protein kinases on human cytomegalovirus disruption of nuclear lamina and nuclear egress. J Virol 88:10982–10985

DOI

85
Shiba C, Daikoku T, Goshima F, Takakuwa H, Yamauchi Y, Koiwai O, Nishiyama Y (2000) The UL34 gene product of herpes simplex virus type 2 is a tail-anchored type II membrane protein that is significant for virus envelopment. J Gen Virol 81:2397–2405

DOI

86
Simpson-Holley M, Colgrove RC, Nalepa G, Harper JW, Knipe DM (2005) Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. J Virol 79:12840–12851

DOI

87
Spear PG, Longnecker R (2003) Herpesvirus entry: an update. J Virol 77:10179–10185

DOI

88
Stewart CL, Roux KJ, Burke B (2007) Blurring the boundary: the nuclear envelope extends its reach. Science 318:1408–1412

DOI

89
Sugimoto K, Uema M, Sagara H, Tanaka M, Sata T, Hashimoto Y,Kawaguchi Y (2008) Simultaneous tracking of capsid, tegument, and envelope protein localization in living cells infected with triply fluorescent herpes simplex virus 1. J Virol 82:5198–5211

DOI

90
Sutter E, de Oliveira AP, Tobler K, Schraner EM, Sonda S, Kaech A, Lucas MS, Ackermann M, Wild P (2012) Herpes simplex virus 1 induces de novo phospholipid synthesis. Virology 429:124–135

DOI

91
Turcotte S, Letellier J, Lippe R (2005) Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J Virol 79:8847–8860

DOI

92
van Genderen IL, Brandimarti R, Torrisi MR, Campadelli G,van Meer G (1994) The phospholipid composition of extracellular herpes simplex virions differs from that of host cell nuclei. Virology 200:831–836

DOI

93
Van Minnebruggen G, Favoreel HW, Nauwynck HJ (2004) Internalization of pseudorabies virus glycoprotein B is mediated by an interaction between the YQRL motif in its cytoplasmic domain and the clathrin-associated AP-2 adaptor complex. J Virol 78:8852–8859

DOI

94
Villinger C, Neusser G, Kranz C, Walther P, Mertens T (2015) 3D analysis of HCMV induced-nuclear membrane structures by FIB/ SEM tomography: insight into an unprecedented membrane morphology. Viruses 7:5686–5704

DOI

95
Wang Y, Yang Y, Wu S, Pan S, Zhou C, Ma Y, Ru Y, Dong S, He B, Zhang C (2014) p32 is a novel target for viral protein ICP34. 5 of herpes simplex virus type 1 and facilitates viral nuclear egress. J Biol Chem 289:35795–35805

DOI

96
Wild P, Senn C, Manera CL, Sutter E, Schraner EM, Tobler K, Ackermann M, Ziegler U, Lucas MS, Kaech A (2009) Exploring the nuclear envelope of herpes simplex virus 1-infected cells by high-resolution microscopy. J Virol 83:408–419

DOI

97
Wisner TW, Wright CC, Kato A, Kawaguchi Y, Mou F, Baines JD, Roller RJ, Johnson DC (2009) Herpesvirus gB-induced fusion between the virion envelope and outer nuclear membrane during virus egress is regulated by the viral US3 kinase. J Virol 83:3115–3126

DOI

98
Wu S, Pan S, Zhang L, Baines J, Roller R, Ames J, Yang M, Wang J, Chen D, Liu Y(2016) Herpes simplex virus 1 induces phosphorylation and reorganization of lamin A/C through the gamma134.5 protein that facilitates nuclear egress. J Virol 90:10414–10422

DOI

99
Yang B, Liu XJ, Yao Y,Jiang X, Wang XZ, Yang H, Sun JY, Miao Y, Wang W, Huang ZL (2018) WDR5 facilitates human cytomegalovirus replication by promoting capsid nuclear egress. J Virol 92:e00207–00218

DOI

100
Zeev-Ben-Mordehai T, Weberruss M, Lorenz M, Cheleski J, Hellberg T, Whittle C, El Omari K, Vasishtan D, Dent KC, Harlos K(2015) Crystal structure of the herpesvirus nuclear egress complex provides insights into inner nuclear membrane remodeling. Cell Rep 13:2645–2652

DOI

101
Zhu Z, Hao Y, Gershon MD, Ambron RT, Gershon AA (1996) Targeting of glycoprotein I (gE) of varicella-zoster virus to the trans-Golgi network by an AYRV sequence and an acidic amino acid-rich patch in the cytosolic domain of the molecule. J Virol 70:6563–6575

Outlines

/