The amino terminus of herpes simplex virus 1 glycoprotein K is required for virion entry via the paired immunoglobulin-like type-2 receptor alpha

Journal of Virology

Volumn 87, Issue 6, 2013, Pages 3305-3313

  Chowdhury, Sona ^a   Chouljenko, Vladimir N ^a   Naderi, Misagh ^a   Kousoulas, Konstantin G ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HERPESVIRUS ENTRY MEDIATOR; IMMUNOGLOBULIN LIKE TYPE 2 RECEPTOR ALPHA; NECTIN 1; RECEPTOR; UL20 PROTEIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS GLYCOPROTEIN K; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CARBOXY TERMINAL SEQUENCE; CELL FUSION; CELL MEMBRANE; CHO CELL; CONTROLLED STUDY; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MEMBRANE FUSION; MOLECULAR CLONING; NONHUMAN; PH; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS GENOME; VIRUS MUTANT; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DNA MUTATIONAL ANALYSIS; HERPESVIRUS 1, HUMAN; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE GLYCOPROTEINS; PROTEIN INTERACTION MAPPING; RECEPTORS, IMMUNOLOGIC; RECEPTORS, VIRUS; SEQUENCE DELETION; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84874704500     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02982-12     Document Type: Article

References (49)

1. 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.
2. Herold BC, WuDunn D, Soltys N, Spear PG. 1991. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J. Virol. 65:1090-1098.
3. Shukla D, Spear PG. 2001. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J. Clin. Investig. 108:503-510.
4. 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.
5. 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.
6. 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.
7. Arii J, Goto H, Suenaga T, Oyama M, Kozuka-Hata H, Imai T, Minowa A, Akashi H, Arase H, Kawaoka Y, Kawaguchi Y. 2010. Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1. Nature 467:859-862.
8. 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. PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132:935-944.
9. Suenaga T, Satoh T, Somboonthum P, Kawaguchi Y, Mori Y, Arase H. 2010. Myelin-associated glycoprotein mediates membrane fusion and entry of neurotropic herpesviruses. Proc. Natl. Acad. Sci. U. S. A. 107:866-871.
10. Atanasiu D, Saw WT, Cohen GH, Eisenberg RJ. 2010. Cascade of events governing cell-cell fusion induced by herpes simplex virus glycoproteins gD, gH/gL, and gB. J. Virol. 84:12292-12299.
11. Atanasiu D, Whitbeck JC, Cairns TM, Reilly B, Cohen GH, Eisenberg RJ. 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.
12. 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.
13. Milne RS, Nicola AV, Whitbeck JC, Eisenberg RJ, Cohen GH. 2005. Glycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1. J. Virol. 79:6655-6663.
14. Nicola AV, McEvoy AM, Straus SE. 2003. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J. Virol. 77:5324-5332.
15. Arii J, Uema M, Morimoto T, Sagara H, Akashi H, Ono E, Arase H, Kawaguchi Y. 2009. Entry of herpes simplex virus 1 and other alphaherpesviruses via the paired immunoglobulin-like type 2 receptor alpha. J. Virol. 83:4520-4527.
16. Mott KR, Perng GC, Osorio Y, Kousoulas KG, Ghiasi H. 2007. A recombinant herpes simplex virus type 1 expressing two additional copies of gK is more pathogenic than wild-type virus in two different strains of mice. J. Virol. 81:12962-12972.
17. Osorio Y, Mott KR, Jabbar AM, Moreno A, Foster TP, Kousoulas KG, Ghiasi H. 2007. Epitope mapping of HSV-1 glycoprotein K (gK) reveals a T cell epitope located within the signal domain of gK. Virus Res. 128:71-80.
18. 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.
19. Foster TP, Melancon JM, Olivier TL, Kousoulas KG. 2004. Herpes simplex virus type 1 glycoprotein K and the UL20 protein are interdepen dent for intracellular trafficking and trans-Golgi network localization. J. Virol. 78:13262-13277.
20. 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.
21. 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.
22. 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.
23. 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.
24. David AT, Baghian A, Foster TP, Chouljenko VN, Kousoulas KG. 2008. The herpes simplex virus type 1 (HSV-1) glycoprotein K(gK) is essential for viral corneal spread and neuroinvasiveness. Curr. Eye Res. 33:455-467.
25. Aggarwal A, Miranda-Saksena M, Boadle RA, Kelly BJ, Diefenbach RJ, Alam W, Cunningham AL. 2012. Ultrastructural visualization of individual tegument protein dissociation during entry of herpes simplex virus 1 into human and rat dorsal root ganglion neurons. J. Virol. 86:6123-6137.
26. Chowdhury S, Naderi M, Chouljenko VN, Walker JD, Kousoulas KG. 2012. Amino acid differences in glycoproteins B (gB), C (gC), H (gH) and L(gL) are associated with enhanced herpes simplex virus type-1 (McKrae) entry via the paired immunoglobulin-like type-2 receptor. Virol. J. 9:112.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. Le Blanc I, Luyet PP, Pons V, Ferguson C, Emans N, Petiot A, Mayran N, Demaurex N, Faure J, Sadoul R, Parton RG, Gruenberg J. 2005. Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7:653-664.
39. Dietz P, Klupp BG, Fuchs W, Kollner B, Weiland E, Mettenleiter TC. 2000. Pseudorabies virus glycoprotein K requires the UL20 gene product for processing. J. Virol. 74:5083-5090.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. Kaufman HE, Ellison ED, Waltman SR. 1969. Double-stranded RNA, an interferon inducer, in herpes simplex keratitis. Am. J. Ophthalmol. 68: 486-491.
47. Halford WP, Balliet JW, Gebhardt BM. 2004. Re-evaluating natural resistance to herpes simplex virus type 1. J. Virol. 78:10086-10095.
48. Bzik DJ, Person S. 1981. Dependence of herpes simplex virus type 1-induced cell fusion on cell type. Virology 110:35-42.
49. David AT, Saied A, Charles A, Subramanian R, Chouljenko VN, Kousoulas KG. 2012. A herpes simplex virus 1 (McKrae) mutant lacking the glycoprotein K gene is unable to infect via neuronal axons and egress from neuronal cell bodies. mBio 3:e00144-00112. doi:10.1128 /mBio.00144-12.