Functional hierarchy of herpes simplex virus 1 viral glycoproteins in cytoplasmic virion envelopment and egress

Journal of Virology

Volumn 86, Issue 8, 2012, Pages 4262-4270

  Chouljenko, Dmitry V ^a   Kim, In Joong ^a   Chouljenko, Vladimir N ^a   Subramanian, Ramesh ^a   Walker, Jason D ^a   Kousoulas, Konstantin G ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GLYCOPROTEIN D; GLYCOPROTEIN E; GLYCOPROTEIN K; GLYCOPROTEIN M; PROTEIN UL11; PROTEIN UL20; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CHLOROCEBUS; CONTROLLED STUDY; CYTOPLASM; HERPES SIMPLEX VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRAL GENETICS; VIRION; VIRUS ENVELOPE; VIRUS MORPHOGENESIS; VIRUS MUTANT; VIRUS PLAQUE; VIRUS RECOMBINANT; VIRUS RELEASE; VIRUS REPLICATION; WILD TYPE;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CYTOPLASM; GENE ORDER; GENETIC VECTORS; GLYCOPROTEINS; HERPESVIRUS 1, HUMAN; HUMANS; MUTATION; PHENOTYPE; PROTEIN BINDING; PROTEOME; VIRAL STRUCTURAL PROTEINS; VIRION; VIRUS RELEASE; VIRUS REPLICATION;

HUMAN HERPESVIRUS 1;

EID: 84861406745     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06766-11     Document Type: Article

References (57)

1. Atanasiu D, et al. 2007. Bimolecular complementation reveals that glycoproteins gB and gH/gL of herpes simplex virus interact with each other during cell fusion. Proc. Natl. Acad. Sci. U. S. A. 104:18718-18723.
2. Avitabile E, Forghieri C, Campadelli-Fiume G. 2007. Complexes between herpes simplex virus glycoproteins gD, gB, and gH detected in cells by complementation of split enhanced green fluorescent protein. J. Virol. 81:11532-11537.
3. Avitabile E, Forghieri C, Campadelli-Fiume G. 2009. Cross talk among the glycoproteins involved in herpes simplex virus entry and fusion: the interaction between gB and gH/gL does not necessarily require gD. J. Virol. 83:10752-10760.
4. Avitabile E, Lombardi G, Campadelli-Fiume G. 2003. Herpes simplex virus glycoprotein K, but not its syncytial allele, inhibits cell-cell fusion mediated by the four fusogenic glycoproteins, gD, gB, gH, and gL. J. Virol. 77:6836-6844.
5. Baines JD, Roizman B. 1993. The UL10 gene of herpes simplex virus 1 encodes a novel viral glycoprotein, gM, which is present in the virion and in the plasma membrane of infected cells. J. Virol. 67:1441-1452.
6. Browne H, Bell S, Minson T. 2004. Analysis of the requirement for glycoprotein M in herpes simplex virus type 1 morphogenesis. J. Virol. 78:1039-1041.
7. Browne H, Bell S, Minson T, Wilson DW. 1996. An endoplasmic reticulum-retained herpes simplex virus glycoprotein H is absent from secreted virions: evidence for reenvelopment during egress. J. Virol. 70: 4311-4316.
8. Cai WH, Gu B, Person S. 1988. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J. Virol. 62:2596-2604.
9. Calistri A, et al. 2007. Intracellular trafficking and maturation of herpes simplex virus type 1 gB and virus egress require functional biogenesis of multivesicular bodies. J. Virol. 81:11468-11478.
10. Campadelli-Fiume G, Farabegoli F, Di Gaeta S, Roizman B. 1991. Origin of unenveloped capsids in the cytoplasm of cells infected with herpes simplex virus 1. J. Virol. 65:1589-1595.
11. Chi JH, Harley CA, Mukhopadhyay A, Wilson DW. 2005. The cytoplasmic tail of herpes simplex virus envelope glycoprotein D binds to the tegument protein VP22 and to capsids. J. Gen. Virol. 86:253-261.
12. Chouljenko VN, Iyer AV, Chowdhury S, Chouljenko DV, Kousoulas KG. 2009. The amino terminus of herpes simplex virus type 1 glycoprotein K (gK) modulates gB-mediated virus-induced cell fusion and virion egress. J. Virol. 83:12301-12313.
13. Chouljenko VN, Iyer AV, Chowdhury S, Kim J, Kousoulas KG. 2010. The herpes simplex virus type 1 UL20 protein and the amino terminus of glycoprotein K (gK) physically interact with gB. J. Virol. 84:8596-8606.
14. Connolly SA, Jackson JO, Jardetzky TS, Longnecker R. 2011. Fusing structure and function: a structural view of the herpesvirus entry machinery. Nat. Rev. Microbiol. 9:369-381.
15. Dijkstra JM, Mettenleiter TC, Klupp BG. 1997. Intracellular processing of pseudorabies virus glycoprotein M (gM): gM of strain Bartha lacks N-glycosylation. Virology 237:113-122.
16. 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.
17. Farnsworth A, Johnson DC. 2006. Herpes simplex virus gE/gI must accumulate in the trans-Golgi network at early times and then redistribute to cell junctions to promote cell-cell spread. J. Virol. 80:3167-3179.
18. Farnsworth A, Wisner TW, Johnson DC. 2007. Cytoplasmic residues of herpes simplex virus glycoprotein gE required for secondary envelopment and binding of tegument proteins VP22 and UL11 to gE and gD. J. Virol. 81:319-331.
19. Forrester A, et al. 1992. Construction and properties of a mutant of herpes simplex virus type 1 with glycoproteinHcoding sequences deleted. J. Virol. 66:341-348.
20. Foster TP, Alvarez X, Kousoulas KG. 2003. Plasma membrane topology of syncytial domains of herpes simplex virus type 1 glycoprotein K (gK): the UL20 protein enables cell surface localization of gK but not gKmediated cell-to-cell fusion. J. Virol. 77:499-510.
21. Foster TP, Chouljenko VN, Kousoulas KG. 2008. Functional and physical interactions of the herpes simplex virus type 1 UL20 membrane protein with glycoprotein K. J. Virol. 82:6310-6323.
22. Foster TP, Kousoulas KG. 1999. Genetic analysis of the role of herpes simplex virus type 1 glycoprotein K in infectious virus production and egress. J. Virol. 73:8457-8468.
23. Foster TP, Melancon JM, Baines JD, Kousoulas KG. 2004. The herpes simplex virus type 1 UL20 protein modulates membrane fusion events during cytoplasmic virion morphogenesis and virus-induced cell fusion. J. Virol. 78:5347-5357.
24. Foster TP, Melancon JM, Olivier TL, Kousoulas KG. 2004. Herpes simplex virus type 1 glycoprotein K and the UL20 protein are interdependent for intracellular trafficking and trans-Golgi network localization. J. Virol. 78:13262-13277.
25. Foster TP, Rybachuk GV, Kousoulas KG. 2001. Glycoprotein K specified by herpes simplex virus type 1 is expressed on virions as a Golgi complexdependent glycosylated species and functions in virion entry. J. Virol. 75:12431-12438.
26. Fuchs W, et al. 2002. Physical interaction between envelope glycoproteins E and M of pseudorabies virus and the major tegument protein UL49. J. Virol. 76:8208-8217.
27. Fulmer PA, Melancon JM, Baines JD, Kousoulas KG. 2007. UL20 protein functions precede and are required for the UL11 functions of herpes simplex virus type 1 cytoplasmic virion envelopment. J. Virol. 81: 3097-3108.
28. Gianni T, Amasio M, Campadelli-Fiume G. 2009. Herpes simplex virus gD forms distinct complexes with fusion executors gB and gH/gL in part through the C-terminal profusion domain. J. Biol. Chem. 284:17370-17382.
29. Gross ST, Harley CA, Wilson DW. 2003. The cytoplasmic tail of herpes simplex virus glycoprotein H binds to the tegument protein VP16 in vitro and in vivo. Virology 317:1-12.
30. Han J, Chadha P, Meckes DG, Jr, Baird NL, Wills JW. 2011. Interaction and interdependent packaging of tegument protein UL11 and glycoprotein E of herpes simplex virus. J. Virol. 85:9437-9446.
31. Jayachandra S, Baghian A, Kousoulas KG. 1997. Herpes simplex virus type 1 glycoprotein K is not essential for infectious virus production in actively replicating cells but is required for efficient envelopment and translocation of infectious virions from the cytoplasm to the extracellular space. J. Virol. 71:5012-5024.
32. Johnson DC, Baines JD. 2011. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 9:382-394.
33. Johnson DC, Huber MT. 2002. Directed egress of animal viruses promotes cell-to-cell spread. J. Virol. 76:1-8.
34. Johnson DC, Wisner TW, Wright CC. 2011. Herpes simplex virus glycoproteins gB and gD function in a redundant fashion to promote secondary envelopment. J. Virol. 85:4910-4926.
35. Kopp M, Granzow H, Fuchs W, Klupp B, Mettenleiter TC. 2004. Simultaneous deletion of pseudorabies virus tegument protein UL11 and glycoproteinMseverely impairs secondary envelopment. J. Virol. 78:3024-3034.
36. Lee HC, Chouljenko VN, Chouljenko DV, Boudreaux MJ, Kousoulas KG. 2009. The herpes simplex virus type 1 glycoprotein D (gD) cytoplasmic terminus and full-length gE are not essential and do not function in a redundant manner for cytoplasmic virion envelopment and egress. J. Virol. 83:6115-6124.
37. Leege T, et al. 2009. Effects of simultaneous deletion of pUL11 and glycoprotein M on virion maturation of herpes simplex virus type 1. J. Virol. 83:896-907.
38. Ligas MW, Johnson DC. 1988. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by beta-galactosidase sequences binds to but is unable to penetrate into cells. J. Virol. 62:1486-1494.
39. MacLean CA, Robertson LM, Jamieson FE. 1993. Characterization of the UL10 gene product of herpes simplex virus type 1 and investigation of its role in vivo. J. Gen. Virol. 74(Pt 6):975-983.
40. Melancon JM, Fulmer PA, Kousoulas KG. 2007. The herpes simplex virus UL20 protein functions in glycoprotein K (gK) intracellular transport and virus-induced cell fusion are independent of UL20 functions in cytoplasmic virion envelopment. Virol. J. 4:120.
41. Melancon JM, Luna RE, Foster TP, Kousoulas KG. 2005. Herpes simplex virus type 1 gK is required for gB-mediated virus-induced cell fusion, while neither gB and gK nor gB and UL20p function redundantly in virion de-envelopment. J. Virol. 79:299-313.
42. Mettenleiter TC, Klupp BG, Granzow H. 2009. Herpesvirus assembly: an update. Virus Res. 143:222-234.
43. O'Regan KJ, Bucks MA, Murphy MA, Wills JW, Courtney RJ. 2007. A conserved region of the herpes simplex virus type 1 tegument protein VP22 facilitates interaction with the cytoplasmic tail of glycoprotein E (gE). Virology 358:192-200.
44. Osterrieder N, et al. 1996. The equine herpesvirus 1 glycoprotein gp21/22a, the herpes simplex virus type 1 gM homolog, is involved in virus penetration and cell-to-cell spread of virions. J. Virol. 70:4110-4115.
45. Reynolds AE, Wills EG, Roller RJ, Ryckman BJ, Baines JD. 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. 76:8939-8952.
46. Sarmiento M, Batterson WW. 1992. Glycerol shock treatment facilitates purification of herpes simplex virus. J. Virol. Methods 36:151-157.
47. Skepper JN, Whiteley A, Browne H, Minson A. 2001. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment → deenvelopment reenvelopment pathway. J. Virol. 75:5697-5702.
48. Stylianou J, Maringer K, Cook R, Bernard E, Elliott G. 2009. Virion incorporation of the herpes simplex virus type 1 tegument protein VP22 occurs via glycoprotein E-specific recruitment to the late secretory pathway. J. Virol. 83:5204-5218.
49. Subramanian R, D'Auvergne O, Kong H, Kousoulas KG. 2008. The cytoplasmic terminus of Kaposi's sarcoma-associated herpesvirus glycoprotein B is not essential for virion egress and infectivity. J. Virol. 82: 7144-7154.
50. Subramanian R, Sehgal I, D'Auvergne O, Kousoulas KG. 2010. Kaposi's sarcoma-associated herpesvirus glycoproteins B and K8.1 regulate virion egress and synthesis of vascular endothelial growth factor and viral interleukin-6 in BCBL-1 cells. J. Virol. 84:1704-1714.
51. Sugimoto K, et al. 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.
52. Tanaka M, Kagawa H, Yamanashi Y, Sata T, Kawaguchi Y. 2003. Construction of an excisable bacterial artificial chromosome containing a full-length infectious clone of herpes simplex virus type 1: viruses reconstituted from the clone exhibit wild-type properties in vitro and in vivo. J. Virol. 77:1382-1391.
53. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40:191-197.
54. 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.
55. Whiteley A, Bruun B, Minson T, Browne H. 1999. Effects of targeting herpes simplex virus type 1 gD to the endoplasmic reticulum and trans-Golgi network. J. Virol. 73:9515-9520.
56. Wisner TW, Johnson DC. 2004. Redistribution of cellular and herpes simplex virus proteins from the trans-Golgi network to cell junctions without enveloped capsids. J. Virol. 78:11519-11535.
57. Yeh PC, et al. 2011. Direct and specific binding of the UL16 tegument protein of herpes simplex virus to the cytoplasmic tail of glycoprotein E. J. Virol. 85:9425-9436.