Herpes simplex virus 1 glycoprotein m and the membrane-associated protein UL11 are required for virus-induced cell fusion and efficient virus entry

Journal of Virology

Volumn 87, Issue 14, 2013, Pages 8029-8037

  Kim, In Joong ^a   Chouljenko, Vladimir N ^a   Walker, Jason D ^a   Kousoulas, Konstantin G ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GLYCOPROTEIN B; GLYCOPROTEIN D; GLYCOPROTEIN E; GLYCOPROTEIN H; GLYCOPROTEIN M; MEMBRANE PROTEIN; PROTEIN C; UL11 PROTEIN; UL20 PROTEIN; UNCLASSIFIED DRUG; VALINE; VIRUS GLYCOPROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUSION; CELL SURFACE; CONTROLLED STUDY; GENE DELETION; GLYCOPROTEIN M GENE; HERPES SIMPLEX VIRUS 1; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; UL11 GENE; VIRUS ENTRY; VIRUS GENE; VIRUS MUTANT; VIRUS RECOMBINANT; VIRUS STRAIN; WILD TYPE;

BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE DELETION; GIANT CELLS; HERPESVIRUS 1, HUMAN; IMMUNOPRECIPITATION; KINETICS; MUTATION; VIRAL FUSION PROTEINS; VIRAL MATRIX PROTEINS; VIRAL STRUCTURAL PROTEINS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 84880265668     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01181-13     Document Type: Article

References (58)

1. Roizman B, Knipe D, Whitley R. 2007. Herpes simplex viruses, p 2501-2601. In Knipe D, Howley P (ed), Fields virology, 5th ed, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Baines JD, Ward PL, Campadelli-Fiume G, Roizman B. 1991. The UL20 gene of herpes simplex virus 1 encodes a function necessary for viral egress. J. Virol. 65:6414-6424.
3. McLean G, Rixon F, Langeland N, Haarr L, Marsden H. 1990. Identification and characterization of the virion protein products of herpes simplex virus type 1 gene UL47. J. Gen. Virol. 71:2953-2960.
4. Melancon JM, Foster TP, Kousoulas KG. 2004. Genetic analysis of the herpes simplex virus type 1 UL20 protein domains involved in cytoplasmic virion envelopment and virus-induced cell fusion. J. Virol. 78:7329-7343.
5. Jacobson JG, Chen SH, Cook WJ, Kramer MF, Coen DM. 1998. Importance of the herpes simplex virus UL24 gene for productive ganglionic infection in mice. Virology 242:161-169.
6. Sanders PG, Wilkie NM, Davison AJ. 1982. Thymidine kinase deletion mutants of herpes simplex virus type 1. J. Gen. Virol. 63:277-295.
7. Bzik DJ, Fox BA, DeLuca NA, Person S. 1984. Nucleotide sequence of a region of the herpes simplex virus type 1 gB glycoprotein gene: mutations affecting rate of virus entry and cell fusion. Virology 137:185-190.
8. Pellett PE, Kousoulas KG, Pereira L, Roizman B. 1985. Anatomy of the herpes simplex virus 1 strain F glycoprotein B gene: primary sequence and predicted protein structure of the wild type and of monoclonal antibodyresistant mutants. J. Virol. 53:243-253.
9. Bond VC, Person S. 1984. Fine structure physical map locations of alterations that affect cell fusion in herpes simplex virus type 1. Virology 132: 368-376.
10. Debroy C, Pederson N, Person S. 1985. Nucleotide sequence of a herpes simplex virus type 1 gene that causes cell fusion. Virology 145:36-48.
11. Hutchinson L, Goldsmith K, Snoddy D, Ghosh H, Graham FL, Johnson DC. 1992. Identification and characterization of a novel herpes simplex virus glycoprotein, gK, involved in cell fusion. J. Virol. 66:5603-5609.
12. Pogue-Geile KL, Lee GT, Shapira SK, Spear PG. 1984. Fine mapping of mutations in the fusion-inducingMPstrain of herpes simplex virus type 1. Virology 136:100-109.
13. Pogue-Geile KL, Spear PG. 1987. The single base pair substitution responsible for the syn phenotype of herpes simplex virus type 1, strain MP. Virology 157:67-74.
14. Ruyechan WT, Morse LS, Knipe DM, Roizman B. 1979. Molecular genetics of herpes simplex virus. II. Mapping of the major viral glycoproteins and of the genetic loci specifying the social behavior of infected cells. J. Virol. 29:677-697.
15. 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.
16. Campadelli-Fiume G, Cocchi F, Menotti L, Lopez M. 2000. The novel receptors that mediate the entry of herpes simplex viruses and animal alphaherpesviruses into cells. Rev. Med. Virol. 10:305-319.
17. Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618-1620.
18. Montgomery RI, Warner MS, Lum BJ, Spear PG. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87:427-436.
19. Satoh T, Arii J, Suenaga T, Wang J, Kogure A, Uehori J, Arase N, Shiratori I, Tanaka S, Kawaguchi Y, Spear PG, Lanier LL, Arase H. 2008. PILRα is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132:935-944.
20. Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, Cohen GH, Eisenberg RJ, Rosenberg RD, Spear PG. 1999. A novel role for 3-Osulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22.
21. Spear PG, Eisenberg RJ, Cohen GH. 2000. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275:1-8.
22. Spear PG, Longnecker R. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
23. Hannah BP, Heldwein EE, Bender FC, Cohen GH, Eisenberg RJ. 2007. Mutational evidence of internal fusion loops in herpes simplex virus glycoprotein B. J. Virol. 81:4858-4865.
24. Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, Harrison SC. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
25. Muggeridge MI. 2000. Characterization of cell-cell fusion mediated by herpes simplex virus 2 glycoproteins gB, gD, gH and gL in transfected cells. J. Gen. Virol. 81:2017-2027.
26. Turner A, Bruun B, Minson T, Browne H. 1998. Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. J. Virol. 72: 873-875.
27. Kousoulas KG, Person S, Holland TC. 1978. Timing of some of the molecular events required for cell fusion induced by herpes simplex virus type 1. J. Virol. 27:505-512.
28. 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.
29. 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.
30. 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.
31. 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.
32. Leege T, Fuchs W, Granzow H, Kopp M, Klupp BG, Mettenleiter TC. 2009. Effects of simultaneous deletion of pUL11 and glycoprotein M on virion maturation of herpes simplex virus type 1. J. Virol. 83:896-907.
33. Crump CM, Bruun B, Bell S, Pomeranz LE, Minson T, Browne HM. 2004. Alphaherpesvirus glycoprotein M causes the relocalization of plasma membrane proteins. J. Gen. Virol. 85:3517-3527.
34. Klupp BG, Nixdorf R, Mettenleiter TC. 2000. Pseudorabies virus glycoprotein M inhibits membrane fusion. J. Virol. 74:6760-6768.
35. Koyano S, Mar EC, Stamey FR, Inoue N. 2003. Glycoproteins M and N of human herpesvirus 8 form a complex and inhibit cell fusion. J. Gen. Virol. 84:1485-1491.
36. Balan P, Davis-Poynter N, Bell S, Atkinson H, Browne H, Minson T. 1994. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. J. Gen. Virol. 75(Part 6):1245-1258.
37. Davis-Poynter N, Bell S, Minson T, Browne H. 1994. Analysis of the contributions of herpes simplex virus type 1 membrane proteins to the induction of cell-cell fusion. J. Virol. 68:7586-7590.
38. Yeh PC, Meckes DG, Jr, Wills JW. 2008. Analysis of the interaction between the UL11 and UL16 tegument proteins of herpes simplex virus. J. Virol. 82:10693-10700.
39. Baird NL, Yeh PC, Courtney RJ, Wills JW. 2008. Sequences in the UL11 tegument protein of herpes simplex virus that control association with detergent-resistant membranes. Virology 374:315-321.
40. Loomis JS, Bowzard JB, Courtney RJ, Wills JW. 2001. Intracellular trafficking of the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 75:12209-12219.
41. Loomis JS, Courtney RJ, Wills JW. 2003. Binding partners for the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 77:11417-11424.
42. Yeh PC, Han J, Chadha P, Meckes DG, Jr, Ward MD, Semmes OJ, Wills JW. 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.
43. Han J, Chadha P, Starkey JL, Wills JW. 2012. Function of glycoprotein E of herpes simplex virus requires coordinated assembly of three tegument Kim et al. proteins on its cytoplasmic tail. Proc. Natl. Acad. Sci. U. S. A. 109:19798-19803.
44. Chouljenko DV, Kim IJ, Chouljenko VN, Subramanian R, Walker JD, Kousoulas KG. 2012. Functional hierarchy of herpes simplex virus 1 viral glycoproteins in cytoplasmic virion envelopment and egress. J. Virol. 86: 4262-4270.
45. 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.
46. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step red-mediated recombination for versatile high-efficiency markerlessDNA manipulation in Escherichia coli. Biotechniques 40:191-197.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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.
52. Jambunathan N, Chowdhury S, Subramanian R, Chouljenko VN, Walker JD, Kousoulas KG. 2011. Site-specific proteolytic cleavage of the amino terminus of herpes simplex virus glycoprotein K on virion particles inhibits virus entry. J. Virol. 85:12910-12918.
53. Baghian A, Huang L, Newman S, Jayachandra S, Kousoulas KG. 1993. Truncation of the carboxy-terminal 28 amino acids of glycoprotein B specified by herpes simplex virus type 1 mutant amb1511-7 causes extensive cell fusion. J. Virol. 67:2396-2401.
54. Foster TP, Melancon JM, Kousoulas KG. 2001. An alpha-helical domain within the carboxyl terminus of herpes simplex virus type 1 (HSV-1) glycoprotein B (gB) is associated with cell fusion and resistance to heparin inhibition of cell fusion. Virology 287:18-29.
55. Silverman JL, Greene NG, King DS, Heldwein EE. 2012. Membrane requirement for folding of the herpes simplex virus 1 gB cytodomain suggests a unique mechanism of fusion regulation. J. Virol. 86:8171-8184.
56. Maringer K, Stylianou J, Elliott G. 2012. A network of protein interactions around the herpes simplex virus tegument protein VP22. J. Virol. 86:12971-12982.
57. Chowdhury S, Chouljenko VN, Nadheri M, Kousoulas KG. 2013. The amino terminus of herpes simplex virus 1 glycoprotein K is required for virion entry via the paired immunoglobulin-like type-2 receptor alpha. J. Virol. 87:3305-3313.
58. Loret S, Guay G, Lippe R. 2008. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J. Virol. 82:8605-8618.