1932

Abstract

Most DNA viruses replicate in the nucleus and exit it either by passing through the nuclear pores or by rupturing the nuclear envelope. Unusually, herpesviruses have evolved a complex mechanism of nuclear escape whereby nascent capsids bud at the inner nuclear membrane to form perinuclear virions that subsequently fuse with the outer nuclear membrane, releasing capsids into the cytosol. Although this general scheme is accepted in the field, the players and their roles are still debated. Recent studies illuminated critical mechanistic features of this enigmatic process and uncovered surprising parallels with a novel cellular nuclear export process. This review summarizes our current understanding of nuclear egress in herpesviruses, examines the experimental evidence and models, and outlines outstanding questions with the goal of stimulating new research in this area.

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2016-09-29
2024-06-22
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Literature Cited

  1. Welsch S, Muller B, Kräusslich HG. 1.  2007. More than one door—budding of enveloped viruses through cellular membranes. FEBS Lett 581:2089–97 [Google Scholar]
  2. Mettenleiter TC. 2.  2015. Breaching the barrier—the nuclear envelope in virus infection. J. Mol. Biol. 428:1949–61 [Google Scholar]
  3. Weller SK, Coen DM. 3.  2012. Herpes simplex viruses: mechanisms of DNA replication. Cold Spring Harb. Perspect. Biol. 4:a013011 [Google Scholar]
  4. Pante N, Kann M. 4.  2002. Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol. Biol. Cell 13:425–34 [Google Scholar]
  5. Johnson DC, Baines JD. 5.  2011. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 9:382–94 [Google Scholar]
  6. Mettenleiter TC, Muller F, Granzow H, Klupp BG. 6.  2013. The way out: what we know and do not know about herpesvirus nuclear egress. Cell. Microbiol. 15:170–78 [Google Scholar]
  7. Campadelli-Fiume G, Farabegoli F, Di Gaeta S, Roizman B. 7.  1991. Origin of unenveloped capsids in the cytoplasm of cells infected with herpes simplex virus 1. J. Virol. 65:1589–95 [Google Scholar]
  8. Campadelli-Fiume G. 8.  2007. The egress of alphaherpesviruses from the cell. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis A Arvin, G Campadelli-Fiume, E Mocarski, PS Moore, B Roizman et al.151–62 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  9. Reynolds AE, Wills EG, Roller RJ, Ryckman BJ, Baines JD. 9.  2002. 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. 76:8939–52 [Google Scholar]
  10. Ryckman BJ, Roller RJ. 10.  2004. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. J. Virol. 78:399–412 [Google Scholar]
  11. Klupp BG, Granzow H, Mettenleiter TC. 11.  2001. Effect of the pseudorabies virus US3 protein on nuclear membrane localization of the UL34 protein and virus egress from the nucleus. J. Gen. Virol. 82:2363–71 [Google Scholar]
  12. Desai P, Sexton GL, McCaffery JM, Person S. 12.  2001. A null mutation in the gene encoding the herpes simplex virus type 1 UL37 polypeptide abrogates virus maturation. J. Virol. 75:10259–71 [Google Scholar]
  13. Brack AR, Klupp BG, Granzow H, Tirabassi R, Enquist LW, Mettenleiter TC. 13.  2000. Role of the cytoplasmic tail of pseudorabies virus glycoprotein E in virion formation. J. Virol. 74:4004–16 [Google Scholar]
  14. Leege T, Granzow H, Fuchs W, Klupp BG, Mettenleiter TC. 14.  2009. Phenotypic similarities and differences between UL37-deleted pseudorabies virus and herpes simplex virus type 1. J. Gen. Virol. 90:1560–68 [Google Scholar]
  15. Desai PJ. 15.  2000. 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. 74:11608–18 [Google Scholar]
  16. Farnsworth A, Goldsmith K, Johnson DC. 16.  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. 77:8481–94 [Google Scholar]
  17. Roberts AP, Abaitua F, O'Hare P, McNab D, Rixon FJ, Pasdeloup D. 17.  2009. Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J. Virol. 83:105–16 [Google Scholar]
  18. Fulmer PA, Melancon JM, Baines JD, Kousoulas KG. 18.  2007. UL20 protein functions precede and are required for the UL11 functions of herpes simplex virus type 1 cytoplasmic virion envelopment. J. Virol. 81:3097–108 [Google Scholar]
  19. Klupp BG, Granzow H, Mettenleiter TC. 19.  2000. Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J. Virol. 74:10063–73 [Google Scholar]
  20. Granzow H, Klupp BG, Fuchs W, Veits J, Osterrieder N, Mettenleiter TC. 20.  2001. Egress of alphaherpesviruses: comparative ultrastructural study. J. Virol. 75:3675–84 [Google Scholar]
  21. Gershon AA, Sherman DL, Zhu Z, Gabel CA, Ambron RT, Gershon MD. 21.  1994. Intracellular transport of newly synthesized varicella-zoster virus: final envelopment in the trans-Golgi network. J. Virol. 68:6372–90 [Google Scholar]
  22. Skepper JN, Whiteley A, Browne H, Minson A. 22.  2001. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment → deenvelopment → reenvelopment pathway. J. Virol. 75:5697–702 [Google Scholar]
  23. Fuchs W, Klupp BG, Granzow H, Osterrieder N, Mettenleiter TC. 23.  2002. 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. 76:364–78 [Google Scholar]
  24. Meinke P, Schirmer EC. 24.  2015. LINC'ing form and function at the nuclear envelope. FEBS Lett 589:2514–21 [Google Scholar]
  25. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK. 25.  et al. 2008. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22:832–53 [Google Scholar]
  26. Goldberg MW, Fiserova J, Huttenlauch I, Stick R. 26.  2008. A new model for nuclear lamina organization. Biochem. Soc. Trans. 36:1339–43 [Google Scholar]
  27. Meier J, Georgatos SD. 27.  1994. Type B lamins remain associated with the integral nuclear envelope protein p58 during mitosis: implications for nuclear reassembly. EMBO J 13:1888–98 [Google Scholar]
  28. Roller RJ, Zhou Y, Schnetzer R, Ferguson J, DeSalvo D. 28.  2000. Herpes simplex virus type 1 UL34 gene product is required for viral envelopment. J. Virol. 74:117–29 [Google Scholar]
  29. Bubeck A, Wagner M, Ruzsics Z, Lotzerich M, Iglesias M. 29.  et al. 2004. Comprehensive mutational analysis of a herpesvirus gene in the viral genome context reveals a region essential for virus replication. J. Virol. 78:8026–35 [Google Scholar]
  30. Muranyi W, Haas J, Wagner M, Krohne G, Koszinowski UH. 30.  2002. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 297:854–57 [Google Scholar]
  31. Farina A, Feederle R, Raffa S, Gonnella R, Santarelli R. 31.  et al. 2005. BFRF1 of Epstein-Barr virus is essential for efficient primary viral envelopment and egress. J. Virol. 79:3703–12 [Google Scholar]
  32. Chang YE, Roizman B. 32.  1993. The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. J. Virol. 67:6348–56 [Google Scholar]
  33. Reynolds AE, Ryckman BJ, Baines JD, Zhou Y, Liang L, Roller RJ. 33.  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. 75:8803–17 [Google Scholar]
  34. Shiba C, Daikoku T, Goshima F, Takakuwa H, Yamauchi Y. 34.  et al. 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. 81:2397–405 [Google Scholar]
  35. Funk C, Ott M, Raschbichler V, Nagel CH, Binz A. 35.  et al. 2015. The herpes simplex virus protein pUL31 escorts nucleocapsids to sites of nuclear egress, a process coordinated by its N-terminal domain. PLOS Pathog 11:e1004957 [Google Scholar]
  36. Gonnella R, Farina A, Santarelli R, Raffa S, Feederle R. 36.  et al. 2005. Characterization and intracellular localization of the Epstein-Barr virus protein BFLF2: interactions with BFRF1 and with the nuclear lamina. J. Virol. 79:3713–27 [Google Scholar]
  37. Lotzerich M, Ruzsics Z, Koszinowski UH. 37.  2006. Functional domains of murine cytomegalovirus nuclear egress protein M53/p38. J. Virol. 80:73–84 [Google Scholar]
  38. Bigalke JM, Heldwein EE. 38.  2015. Structural basis of membrane budding by the nuclear egress complex of herpesviruses. EMBO J 34:2921–36 [Google Scholar]
  39. Lye MF, Sharma M, El Omari K, Filman DJ, Schuermann JP. 39.  et al. 2015. Unexpected features and mechanism of heterodimer formation of a herpesvirus nuclear egress complex. EMBO J 34:2937–52 [Google Scholar]
  40. Walzer SA, Egerer-Sieber C, Sticht H, Sevvana M, Hohl K. 40.  et al. 2015. Crystal structure of the human cytomegalovirus pUL50-pUL53 core nuclear egress complex provides insight into a unique assembly scaffold for virus-host protein interactions. J. Biol. Chem. 290:27452–58 [Google Scholar]
  41. Zeev-Ben-Mordehai T, Weberruss M, Lorenz M, Cheleski J, Hellberg T. 41.  et al. 2015. Crystal structure of the herpesvirus nuclear egress complex provides insights into inner nuclear membrane remodeling. Cell Rep 13:2645–52 [Google Scholar]
  42. Hetzer MW. 42.  2010. The nuclear envelope. Cold Spring Harb. Perspect. Biol. 2:a000539 [Google Scholar]
  43. Peter M, Sanghera JS, Pelech SL, Nigg EA. 43.  1992. Mitogen-activated protein kinases phosphorylate nuclear lamins and display sequence specificity overlapping that of mitotic protein kinase p34cdc2. Eur. J. Biochem. 205:287–94 [Google Scholar]
  44. Likhacheva EV, Bogachev SS. 44.  2001. Lamins and their functions in cell cycle. Membr. Cell Biol. 14:565–77 [Google Scholar]
  45. Fields AP, Thompson LJ. 45.  1995. The regulation of mitotic nuclear envelope breakdown: a role for multiple lamin kinases. Prog. Cell Cycle Res. 1:271–86 [Google Scholar]
  46. Reynolds AE, Liang L, Baines JD. 46.  2004. Conformational changes in the nuclear lamina induced by herpes simplex virus type 1 require genes UL31 and UL34. J. Virol. 78:5564–75 [Google Scholar]
  47. Bjerke SL, Roller RJ. 47.  2006. Roles for herpes simplex virus type 1 UL34 and US3 proteins in disrupting the nuclear lamina during herpes simplex virus type 1 egress. Virology 347:261–76 [Google Scholar]
  48. Leach NR, Roller RJ. 48.  2010. Significance of host cell kinases in herpes simplex virus type 1 egress and lamin-associated protein disassembly from the nuclear lamina. Virology 406:127–37 [Google Scholar]
  49. Cano-Monreal GL, Wylie KM, Cao F, Tavis JE, Morrison LA. 49.  2009. Herpes simplex virus 2 UL13 protein kinase disrupts nuclear lamins. Virology 392:137–47 [Google Scholar]
  50. Park R, Baines JD. 50.  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 [Google Scholar]
  51. Gershburg E, Pagano JS. 51.  2008. Conserved herpesvirus protein kinases. Biochim. Biophys. Acta 1784:203–12 [Google Scholar]
  52. Purves FC, Longnecker RM, Leader DP, Roizman B. 52.  1987. Herpes simplex virus 1 protein kinase is encoded by open reading frame US3 which is not essential for virus growth in cell culture. J. Virol. 61:2896–901 [Google Scholar]
  53. Mou F, Forest T, Baines JD. 53.  2007. US3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. J. Virol. 81:6459–70 [Google Scholar]
  54. Coulter LJ, Moss HW, Lang J, McGeoch DJ. 54.  1993. A mutant of herpes simplex virus type 1 in which the UL13 protein kinase gene is disrupted. J. Gen. Virol. 74:Part 3387–95 [Google Scholar]
  55. Hamirally S, Kamil JP, Ndassa-Colday YM, Lin AJ, Jahng WJ. 55.  et al. 2009. Viral mimicry of Cdc2/cyclin-dependent kinase 1 mediates disruption of nuclear lamina during human cytomegalovirus nuclear egress. PLOS Pathog 5:e1000275 [Google Scholar]
  56. Lee CP, Huang YH, Lin SF, Chang Y, Chang YH. 56.  et al. 2008. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J. Virol. 82:11913–26 [Google Scholar]
  57. Sharma M, Kamil JP, Coughlin M, Reim NI, Coen DM. 57.  2014. Human cytomegalovirus UL50 and UL53 recruit viral protein kinase UL97, not protein kinase C, for disruption of nuclear lamina and nuclear egress in infected cells. J. Virol. 88:249–62 [Google Scholar]
  58. Gershburg E, Raffa S, Torrisi MR, Pagano JS. 58.  2007. Epstein-Barr virus-encoded protein kinase (BGLF4) is involved in production of infectious virus. J. Virol. 81:5407–12 [Google Scholar]
  59. Prichard MN, Gao N, Jairath S, Mulamba G, Krosky P. 59.  et al. 1999. A recombinant human cytomegalovirus with a large deletion in UL97 has a severe replication deficiency. J. Virol. 73:5663–70 [Google Scholar]
  60. Milbradt J, Webel R, Auerochs S, Sticht H, Marschall M. 60.  2010. Novel mode of phosphorylation-triggered reorganization of the nuclear lamina during nuclear egress of human cytomegalovirus. J. Biol. Chem. 285:13979–89 [Google Scholar]
  61. Kuny CV, Chinchilla K, Culbertson MR, Kalejta RF. 61.  2010. Cyclin-dependent kinase-like function is shared by the beta- and gamma- subset of the conserved herpesvirus protein kinases. PLOS Pathog 6:e1001092 [Google Scholar]
  62. Kawaguchi Y, Kato K. 62.  2003. Protein kinases conserved in herpesviruses potentially share a function mimicking the cellular protein kinase Cdc2. Rev. Med. Virol. 13:331–40 [Google Scholar]
  63. Simpson-Holley M, Baines J, Roller R, Knipe DM. 63.  2004. Herpes simplex virus 1 UL31 and UL34 gene products promote the late maturation of viral replication compartments to the nuclear periphery. J. Virol. 78:5591–600 [Google Scholar]
  64. Morris JB, Hofemeister H, O'Hare P. 64.  2007. Herpes simplex virus infection induces phosphorylation and delocalization of emerin, a key inner nuclear membrane protein. J. Virol. 81:4429–37 [Google Scholar]
  65. Leach N, Bjerke SL, Christensen DK, Bouchard JM, Mou F. 65.  et al. 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. 81:10792–803 [Google Scholar]
  66. Tandon R, Mocarski ES, Conway JF. 66.  2015. The A, B, Cs of herpesvirus capsids. Viruses 7:899–914 [Google Scholar]
  67. Zhou ZH, He J, Jakana J, Tatman JD, Rixon FJ, Chiu W. 67.  1995. Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat. Struct. Biol. 2:1026–30 [Google Scholar]
  68. Newcomb WW, Juhas RM, Thomsen DR, Homa FL, Burch AD. 68.  et al. 2001. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol. 75:10923–32 [Google Scholar]
  69. Cardone G, Winkler DC, Trus BL, Cheng N, Heuser JE. 69.  et al. 2007. Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361:426–34 [Google Scholar]
  70. Baines JD. 70.  2011. Herpes simplex virus capsid assembly and DNA packaging: a present and future antiviral drug target. Trends Microbiol 19:606–13 [Google Scholar]
  71. Stow ND. 71.  2001. Packaging of genomic and amplicon DNA by the herpes simplex virus type 1 UL25-null mutant KUL25NS. J. Virol. 75:10755–65 [Google Scholar]
  72. Salmon B, Cunningham C, Davison AJ, Harris WJ, Baines JD. 72.  1998. The herpes simplex virus type 1 UL17 gene encodes virion tegument proteins that are required for cleavage and packaging of viral DNA. J. Virol. 72:3779–88 [Google Scholar]
  73. Trus BL, Newcomb WW, Cheng N, Cardone G, Marekov L. 73.  et al. 2007. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol. Cell 26:479–89 [Google Scholar]
  74. Toropova K, Huffman JB, Homa FL, Conway JF. 74.  2011. The herpes simplex virus 1 UL17 protein is the second constituent of the capsid vertex-specific component required for DNA packaging and retention. J. Virol. 85:7513–22 [Google Scholar]
  75. Leelawong M, Guo D, Smith GA. 75.  2011. A physical link between the pseudorabies virus capsid and the nuclear egress complex. J. Virol. 85:11675–84 [Google Scholar]
  76. Yang K, Baines JD. 76.  2011. Selection of HSV capsids for envelopment involves interaction between capsid surface components pUL31, pUL17, and pUL25. PNAS 108:14276–81 [Google Scholar]
  77. Yang K, Wills E, Lim HY, Zhou ZH, Baines JD. 77.  2014. Association of herpes simplex virus pUL31 with capsid vertices and components of the capsid vertex-specific complex. J. Virol. 88:3815–25 [Google Scholar]
  78. Klupp BG, Granzow H, Mettenleiter TC. 78.  2011. Nuclear envelope breakdown can substitute for primary envelopment-mediated nuclear egress of herpesviruses. J. Virol. 85:8285–92 [Google Scholar]
  79. Klupp BG, Granzow H, Fuchs W, Keil GM, Finke S, Mettenleiter TC. 79.  2007. Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. PNAS 104:7241–46 [Google Scholar]
  80. Desai PJ, Pryce EN, Henson BW, Luitweiler EM, Cothran J. 80.  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. 86:594–98 [Google Scholar]
  81. Luitweiler EM, Henson BW, Pryce EN, Patel V, Coombs G. 81.  et al. 2013. Interactions of the Kaposi's sarcoma-associated herpesvirus nuclear egress complex: ORF69 is a potent factor for remodeling cellular membranes. J. Virol. 87:3915–29 [Google Scholar]
  82. Bigalke JM, Heuser T, Nicastro D, Heldwein EE. 82.  2014. Membrane deformation and scission by the HSV-1 nuclear egress complex. Nat. Commun. 5:4131 [Google Scholar]
  83. Lorenz M, Vollmer B, Unsay JD, Klupp BG, Garcia-Saez AJ. 83.  et al. 2015. A single herpesvirus protein can mediate vesicle formation in the nuclear envelope. J. Biol. Chem. 290:6962–74 [Google Scholar]
  84. Hagen C, Dent KC, Zeev-Ben-Mordehai T, Grange M, Bosse JB. 84.  et al. 2015. Structural basis of vesicle formation at the inner nuclear membrane. Cell 163:1692–701 [Google Scholar]
  85. Roller RJ, Bjerke SL, Haugo AC, Hanson S. 85.  2010. 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. 84:3921–34 [Google Scholar]
  86. Bjerke SL, Cowan JM, Kerr JK, Reynolds AE, Baines JD, Roller RJ. 86.  2003. Effects of charged cluster mutations on the function of herpes simplex virus type 1 UL34 protein. J. Virol. 77:7601–10 [Google Scholar]
  87. Mettenleiter T. 87.  2016. Molecular basis of herpesvirus nuclear egress: the prototypic vesicular nucleo-cytoplasmic transport Presented at Viruses: At the Forefront of Virus-Host Interactions, Basel, Switz. [Google Scholar]
  88. Briggs JA, Riches JD, Glass B, Bartonova V, Zanetti G, Kräusslich HG. 88.  2009. Structure and assembly of immature HIV. PNAS 106:11090–95 [Google Scholar]
  89. Schur FK, Hagen WJ, Rumlova M, Ruml T, Muller B. 89.  et al. 2015. Structure of the immature HIV-1 capsid in intact virus particles at 8.8 Å resolution. Nature 517:505–8 [Google Scholar]
  90. Heuser J. 90.  2005. Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic “honeycomb” surface coat. J. Cell Biol. 169:269–83 [Google Scholar]
  91. Hyun JK, Accurso C, Hijnen M, Schult P, Pettikiriarachchi A. 91.  et al. 2011. Membrane remodeling by the double-barrel scaffolding protein of poxvirus. PLOS Pathog 7:e1002239 [Google Scholar]
  92. Condit RC, Moussatche N, Traktman P. 92.  2006. In a nutshell: structure and assembly of the vaccinia virion. Adv. Virus Res. 66:31–124 [Google Scholar]
  93. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH. 93.  2009. Membrane scission by the ESCRT-III complex. Nature 458:172–77 [Google Scholar]
  94. Effantin G, Dordor A, Sandrin V, Martinelli N, Sundquist WI. 94.  et al. 2013. ESCRT-III CHMP2A and CHMP3 form variable helical polymers in vitro and act synergistically during HIV-1 budding. Cell. Microbiol. 15:213–26 [Google Scholar]
  95. Gross I, Hohenberg H, Wilk T, Wiegers K, Grattinger M. 95.  et al. 2000. A conformational switch controlling HIV-1 morphogenesis. EMBO J 19:103–13 [Google Scholar]
  96. Carlson LA, Hurley JH. 96.  2012. In vitro reconstitution of the ordered assembly of the endosomal sorting complex required for transport at membrane-bound HIV-1 Gag clusters. PNAS 109:16928–33 [Google Scholar]
  97. Hurley JH. 97.  2015. ESCRTs are everywhere. EMBO J 34:2398–407 [Google Scholar]
  98. Crump CM, Yates C, Minson T. 98.  2007. Herpes simplex virus type 1 cytoplasmic envelopment requires functional Vps4. J. Virol. 81:7380–87 [Google Scholar]
  99. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG. 99.  2015. ESCRT-III controls nuclear envelope reformation. Nature 522:236–39 [Google Scholar]
  100. Maric M, Shao J, Ryan RJ, Wong CS, Gonzalez-Alegre P, Roller RJ. 100.  2011. A functional role for TorsinA in herpes simplex virus 1 nuclear egress. J. Virol. 85:9667–79 [Google Scholar]
  101. Turner EM, Brown RS, Laudermilch E, Tsai PL, Schlieker C. 101.  2015. The Torsin activator LULL1 is required for efficient growth of herpes simplex virus 1. J. Virol. 89:8444–52 [Google Scholar]
  102. Nery FC, Zeng J, Niland BP, Hewett J, Farley J. 102.  et al. 2008. TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J. Cell Sci. 121:3476–86 [Google Scholar]
  103. Mou F, Wills E, Baines JD. 103.  2009. Phosphorylation of the UL31 protein of herpes simplex virus 1 by the US3-encoded kinase regulates localization of the nuclear envelopment complex and egress of nucleocapsids. J. Virol. 83:5181–91 [Google Scholar]
  104. Eisenberg RJ, Atanasiu D, Cairns TM, Gallagher JR, Krummenacher C, Cohen GH. 104.  2012. Herpes virus fusion and entry: a story with many characters. Viruses 4:800–32 [Google Scholar]
  105. Stannard LM, Himmelhoch S, Wynchank S. 105.  1996. Intra-nuclear localization of two envelope proteins, gB and gD, of herpes simplex virus. Arch. Virol. 141:505–24 [Google Scholar]
  106. Farnsworth A, Wisner TW, Webb M, Roller R, Cohen G. 106.  et al. 2007. Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane. PNAS 104:10187–92 [Google Scholar]
  107. Torrisi MR, Di Lazzaro C, Pavan A, Pereira L, Campadelli-Fiume G. 107.  1992. Herpes simplex virus envelopment and maturation studied by fracture label. J. Virol. 66:554–61 [Google Scholar]
  108. Wright CC, Wisner TW, Hannah BP, Eisenberg RJ, Cohen GH, Johnson DC. 108.  2009. Fusion between perinuclear virions and the outer nuclear membrane requires the fusogenic activity of herpes simplex virus gB. J. Virol. 83:11847–56 [Google Scholar]
  109. Klupp B, Altenschmidt J, Granzow H, Fuchs W, Mettenleiter TC. 109.  2008. Glycoproteins required for entry are not necessary for egress of pseudorabies virus. J. Virol. 82:6299–309 [Google Scholar]
  110. Lee SK, Longnecker R. 110.  1997. The Epstein-Barr virus glycoprotein 110 carboxy-terminal tail domain is essential for lytic virus replication. J. Virol. 71:4092–97 [Google Scholar]
  111. Krishnan HH, Sharma-Walia N, Zeng L, Gao SJ, Chandran B. 111.  2005. Envelope glycoprotein gB of Kaposi's sarcoma-associated herpesvirus is essential for egress from infected cells. J. Virol. 79:10952–67 [Google Scholar]
  112. Nozawa N, Kawaguchi Y, Tanaka M, Kato A, Kato A. 112.  et al. 2005. Herpes simplex virus type 1 UL51 protein is involved in maturation and egress of virus particles. J. Virol. 79:6947–56 [Google Scholar]
  113. Whealy ME, Card JP, Meade RP, Robbins AK, Enquist LW. 113.  1991. Effect of brefeldin A on alphaherpesvirus membrane protein glycosylation and virus egress. J. Virol. 65:1066–81 [Google Scholar]
  114. Milbradt J, Kraut A, Hutterer C, Sonntag E, Schmeiser C. 114.  et al. 2014. Proteomic analysis of the multimeric nuclear egress complex of human cytomegalovirus. Mol. Cell Proteomics 13:2132–46 [Google Scholar]
  115. Sharma M, Kamil JP, Coen DM. 115.  2016. Preparation of the human cytomegalovirus nuclear egress complex and associated proteins. Methods Enzymol 569:517–26 [Google Scholar]
  116. Lemnitzer F, Raschbichler V, Kolodziejczak D, Israel L, Imhof A. 116.  et al. 2013. Mouse cytomegalovirus egress protein pM50 interacts with cellular endophilin-A2. Cell Microbiol 15:335–51 [Google Scholar]
  117. Lee CP, Liu PT, Kung HN, Su MT, Chua HH. 117.  et al. 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 [Google Scholar]
  118. Le Sage V, Jung M, Alter JD, Wills EG, Johnston SM. 118.  et al. 2013. The herpes simplex virus 2 UL21 protein is essential for virus propagation. J. Virol. 87:5904–15 [Google Scholar]
  119. Liu Z, Kato A, Shindo K, Noda T, Sagara H. 119.  et al. 2014. Herpes simplex virus 1 UL47 interacts with viral nuclear egress factors UL31, UL34, and US3 and regulates viral nuclear egress. J. Virol. 88:4657–67 [Google Scholar]
  120. Maruzuru Y, Shindo K, Liu Z, Oyama M, Kozuka-Hata H. 120.  et al. 2014. Role of herpes simplex virus 1 immediate early protein ICP22 in viral nuclear egress. J. Virol. 88:7445–54 [Google Scholar]
  121. Speese SD, Ashley J, Jokhi V, Nunnari J, Barria R. 121.  et al. 2012. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149:832–46 [Google Scholar]
  122. Kim CE, Perez A, Perkins G, Ellisman MH, Dauer WT. 122.  2010. A molecular mechanism underlying the neural-specific defect in torsinA mutant mice. PNAS 107:9861–66 [Google Scholar]
  123. Goodchild RE, Kim CE, Dauer WT. 123.  2005. Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 48:923–32 [Google Scholar]
  124. Jokhi V, Ashley J, Nunnari J, Noma A, Ito N. 124.  et al. 2013. Torsin mediates primary envelopment of large ribonucleoprotein granules at the nuclear envelope. Cell Rep 3:988–95 [Google Scholar]
  125. Yuan M, Huang Z, Wei D, Hu Z, Yang K, Pang Y. 125.  2011. Identification of Autographa californica nucleopolyhedrovirus ac93 as a core gene and its requirement for intranuclear microvesicle formation and nuclear egress of nucleocapsids. J. Virol. 85:11664–74 [Google Scholar]
  126. Shen H, Chen K. 126.  2012. BM61 of Bombyx mori nucleopolyhedrovirus: its involvement in the egress of nucleocapsids from the nucleus. FEBS Lett 586:990–95 [Google Scholar]
  127. Stoltz DB, Krell P, Cook D, MacKinnon EA, Lucarotti CJ. 127.  1988. An unusual virus from the parasitic wasp Cotesia melanoscela. Virology 162:311–20 [Google Scholar]
  128. Stoltz DB, Vinson SB. 128.  1979. Viruses and parasitism in insects. Adv. Virus Res. 24:125–71 [Google Scholar]
  129. Cohen S, Marr AK, Garcin P, Pante N. 129.  2011. Nuclear envelope disruption involving host caspases plays a role in the parvovirus replication cycle. J. Virol. 85:4863–74 [Google Scholar]
  130. Raghava S, Giorda KM, Romano FB, Heuck AP, Hebert DN. 130.  2013. SV40 late protein VP4 forms toroidal pores to disrupt membranes for viral release. Biochemistry 52:3939–48 [Google Scholar]
  131. Tollefson AE, Scaria A, Hermiston TW, Ryerse JS, Wold LJ, Wold WS. 131.  1996. The adenovirus death protein (E3-11.6K) is required at very late stages of infection for efficient cell lysis and release of adenovirus from infected cells. J. Virol. 70:2296–306 [Google Scholar]
  132. Kobiler O, Drayman N, Butin-Israeli V, Oppenheim A. 132.  2012. Virus strategies for passing the nuclear envelope barrier. Nucleus 3:526–39 [Google Scholar]
  133. Grimm KS, Klupp BG, Granzow H, Muller FM, Fuchs W, Mettenleiter TC. 133.  2012. Analysis of viral and cellular factors influencing herpesvirus-induced nuclear envelope breakdown. J. Virol. 86:6512–21 [Google Scholar]
  134. Maric M, Haugo AC, Dauer W, Johnson D, Roller RJ. 134.  2014. Nuclear envelope breakdown induced by herpes simplex virus type 1 involves the activity of viral fusion proteins. Virology 460–461:128–37 [Google Scholar]
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