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Research Article

Functional Hierarchy of Herpes Simplex Virus Type-1 Membrane Proteins in Corneal Infection and Virus Transmission to Ganglionic Neurons

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Pages 1169-1177 | Received 30 Jan 2014, Accepted 13 Mar 2014, Published online: 21 Apr 2014

References

  • Liesegang TJ, Melton LJ III, Daly PJ, Ilstrup DM. Epidemiology of ocular herpes simplex. Incidence in Rochester, Minn, 1950 through 1982. Arch Ophthalmol 1989;107:1155–1159
  • Liesegang TJ. Herpes simplex virus epidemiology and ocular importance. Cornea 2001;20:1–13
  • Cockerham G. Primary graft failure caused by herpes simplex virus type 1. Cornea 2001;20:774–775
  • Cockerham GC, Krafft AE, McLean IW. Herpes simplex virus in primary graft failure. Arch Ophthalmol 1997;115:586–589
  • De Kesel RJ, Koppen C, Ieven M, Zeyen T. Primary graft failure caused by herpes simplex virus type 1. Cornea 2001;20:187–190
  • Tullo A. Pathogenesis and management of herpes simplex virus keratitis. Eye (Lond) 2003;17:919–922
  • Antinone SE, Smith GA. Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J Virol 2010;84:1504–1512
  • Fatahzadeh M, Schwartz RA. Human herpes simplex virus infections: epidemiology, pathogenesis, symptomatology, diagnosis, and management. J Am Acad Dermatol 2007;57:737–763; quiz 64–66
  • Smith G. Herpesvirus transport to the nervous system and back again. Annu Rev Microbiol 2012;66:153–176
  • Connolly SA, Jackson JO, Jardetzky TS, Longnecker R. Fusing structure and function: a structural view of the herpesvirus entry machinery. Nat Rev Microbiol 2011;9:369–381
  • Nicola AV, Hou J, Major EO, Straus SE. Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J Virol 2005;79:7609–7616
  • Qie L, Marcellino D, Herold BC. Herpes simplex virus entry is associated with tyrosine phosphorylation of cellular proteins. Virology 1999;256:220–227
  • Milne RS, Nicola AV, Whitbeck JC, Eisenberg RJ, Cohen GH. Glycoprotein D receptor-dependent, low-pH-independent endocytic entry of herpes simplex virus type 1. J Virol 2005;79:6655–6663
  • Mettenleiter TC, Klupp BG, Granzow H. Herpesvirus assembly: an update. Virus Res. 2009;143:222–234
  • Johnson DC, Baines JD. Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 2011;9:382–394
  • Diefenbach RJ, Miranda-Saksena M, Douglas MW, Cunningham AL. Transport and egress of herpes simplex virus in neurons. Rev Med Virol 2008;18:35–51
  • Montgomery RI, Warner MS, Lum BJ, Spear PG. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 1996;87:427–436
  • Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 1998;280:1618–1620
  • Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, et al. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 1999;99:13–22
  • Campadelli-Fiume G, Cocchi F, Menotti L, Lopez M. The novel receptors that mediate the entry of herpes simplex viruses and animal alphaherpesviruses into cells. Rev Med Virol 2000;10:305–319
  • Spear PG, Eisenberg RJ, Cohen GH. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 2000;275:1–8
  • Spear PG, Longnecker R. Herpesvirus entry: an update. J Virol 2003;77:10179–10185
  • Satoh T, Arii J, Suenaga T, Wang J, Kogure A, Uehori J, et al. PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 2008;132:935–944
  • Hannah BP, Heldwein EE, Bender FC, Cohen GH, Eisenberg RJ. Mutational evidence of internal fusion loops in herpes simplex virus glycoprotein B. J Virol 2007;81:4858–4865
  • Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, Harrison SC. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 2006;313:217–220
  • Kousoulas KG, Person S, Holland TC. Timing of some of the molecular events required for cell fusion induced by herpes simplex virus type 1. J Virol 1978;27:505–512
  • Goldgeier M, Alessi C, Muhlbauer JE. Immediate noninvasive diagnosis of herpesvirus by confocal scanning laser microscopy. J Am Acad Dermatol 2002;46:783–785
  • Roizman B, Knipe D, Whitley R. Herpes simplex viruses. In: Knipe D, Howley P, editors. Fields virology, 5th ed. Philadelphia: Lippincott Willams & Wilkins; 2007. pp 2501–2601
  • Turner A, Bruun B, Minson T, Browne H. 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 1998;72:873–875
  • Muggeridge MI. Characterization of cell-cell fusion mediated by herpes simplex virus 2 glycoproteins gB, gD, gH and gL in transfected cells. J Gen Virol 2000;81:2017–2027
  • Baines JD, Ward PL, Campadelli-Fiume G, Roizman B. The UL20 gene of herpes simplex virus 1 encodes a function necessary for viral egress. J Virol 1991;65:6414–6424
  • McLean G, Rixon F, Langeland N, Haarr L, Marsden H. Identification and characterization of the virion protein products of herpes simplex virus type 1 gene UL47. J Gen Virol 1990;71:2953–2960
  • Foster TP, Melancon JM, Olivier TL, Kousoulas KG. Herpes simplex virus type 1 glycoprotein K and the UL20 protein are interdependent for intracellular trafficking and trans-Golgi network localization. J Virol 2004;78:13262–13277
  • Jacobson JG, Chen SH, Cook WJ, Kramer MF, Coen DM. Importance of the herpes simplex virus UL24 gene for productive ganglionic infection in mice. Virology 1998;242:161–169
  • Sanders PG, Wilkie NM, Davison AJ. Thymidine kinase deletion mutants of herpes simplex virus type 1. J Gen Virol 1982;63:277–295
  • Bond VC, Person S. Fine structure physical map locations of alterations that affect cell fusion in herpes simplex virus type 1. Virology 1984;132:368–376
  • Debroy C, Pederson N, Person S. Nucleotide sequence of a herpes simplex virus type 1 gene that causes cell fusion. Virology 1985;145:36–48
  • Hutchinson L, Goldsmith K, Snoddy D, Ghosh H, Graham FL, Johnson DC. Identification and characterization of a novel herpes simplex virus glycoprotein, gK, involved in cell fusion. J Virol 1992;66:5603–5609
  • Pogue-Geile KL, Lee GT, Shapira SK, Spear PG. Fine mapping of mutations in the fusion-inducing MP strain of herpes simplex virus type 1. Virology 1984;136:100–109
  • Pogue-Geile KL, Spear PG. The single base pair substitution responsible for the syn phenotype of herpes simplex virus type 1, strain MP. Virology 1987;157:67–74
  • Ruyechan WT, Morse LS, Knipe DM, Roizman B. 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 1979;29:677–697
  • Bzik DJ, Fox BA, DeLuca NA, Person S. 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 1984;137:185–190
  • Pellett PE, Kousoulas KG, Pereira L, Roizman B. 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 antibody-resistant mutants. J Virol 1985;53:243–253
  • Melancon JM, Luna RE, Foster TP, Kousoulas KG. 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 2005;79:299–313
  • Foster TP, Rybachuk GV, Kousoulas KG. Glycoprotein K specified by herpes simplex virus type 1 is expressed on virions as a Golgi complex-dependent glycosylated species and functions in virion entry. J Virol 2001;75:12431–12438
  • Chouljenko VN, Iyer AV, Chowdhury S, Chouljenko DV, Kousoulas KG. The amino terminus of herpes simplex virus type 1 glycoprotein K (gK) modulates gB-mediated virus-induced cell fusion and virion egress. J Virol 2009;83:12301–12313
  • Chouljenko VN, Iyer AV, Chowdhury S, Kim J, Kousoulas KG. The herpes simplex virus type 1 UL20 protein and the amino terminus of glycoprotein K (gK) physically interact with gB. J Virol 2010;84:8596–8606
  • Kim IJ, Chouljenko VN, Walker JD, Kousoulas KG. Herpes simplex virus 1 glycoprotein M and the membrane-associated protein UL11 are required for virus-induced cell fusion and efficient virus entry. J Virol 2013;87:8029–8037
  • Chouljenko DV, Kim IJ, Chouljenko VN, Subramanian R, Walker JD, Kousoulas KG. Functional hierarchy of herpes simplex virus 1 viral glycoproteins in cytoplasmic virion envelopment and egress. J Virol 2012;86:4262–4270
  • Leege T, Fuchs W, Granzow H, Kopp M, Klupp BG, Mettenleiter TC. Effects of simultaneous deletion of pUL11 and glycoprotein M on virion maturation of herpes simplex virus type 1. J Virol 2009;83:896–907
  • Koyano S, Mar EC, Stamey FR, Inoue N. Glycoproteins M and N of human herpesvirus 8 form a complex and inhibit cell fusion. J Gen Virol 2003;84:1485–1491
  • Klupp BG, Nixdorf R, Mettenleiter TC. Pseudorabies virus glycoprotein M inhibits membrane fusion. J Virol 2000;74:6760–6768
  • Balan P, Davis-Poynter N, Bell S, Atkinson H, Browne H, Minson T. 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 1994;75:1245–1258
  • Collins WJ, Johnson DC. Herpes simplex virus gE/gI expressed in epithelial cells interferes with cell-to-cell spread. J Virol 2003;77:2686–2695
  • McGraw HM, Friedman HM. Herpes simplex virus type 1 glycoprotein E mediates retrograde spread from epithelial cells to neurites. J Virol 2009;83:4791–4799
  • Baines JD, Jacob RJ, Simmerman L, Roizman B. The herpes simplex virus 1 UL11 proteins are associated with cytoplasmic and nuclear membranes and with nuclear bodies of infected cells. J Virol 1995;69:825–833
  • Loomis JS, Bowzard JB, Courtney RJ, Wills JW. Intracellular trafficking of the UL11 tegument protein of herpes simplex virus type 1. J Virol 2001;75:12209–12219
  • MacLean CA, Clark B, McGeoch DJ. Gene UL11 of herpes simplex virus type 1 encodes a virion protein which is myristylated. J Gen Virol 1989;70:3147–3157
  • Baird NL, Yeh PC, Courtney RJ, Wills JW. Sequences in the UL11 tegument protein of herpes simplex virus that control association with detergent-resistant membranes. Virology 2008;374:315–321
  • Farnsworth A, Wisner TW, Johnson DC. 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 2007;81:319–331
  • Loomis JS, Courtney RJ, Wills JW. Binding partners for the UL11 tegument protein of herpes simplex virus type 1. J Virol 2003;77:11417–11424
  • Han J, Chadha P, Starkey JL, Wills JW. Function of glycoprotein E of herpes simplex virus requires coordinated assembly of three tegument proteins on its cytoplasmic tail. Proc Natl Acad Sci USA 2012;109:19798–19803
  • Fulmer PA, Melancon JM, Baines JD, Kousoulas KG. UL20 protein functions precede and are required for the UL11 functions of herpes simplex virus type 1 cytoplasmic virion envelopment. J Virol 2007;81:3097–3108
  • Kopp M, Granzow H, Fuchs W, Klupp BG, Mundt E, Karger A, et al. The pseudorabies virus UL11 protein is a virion component involved in secondary envelopment in the cytoplasm. J Virol 2003;77:5339–5351
  • Seo JY, Britt WJ. Cytoplasmic envelopment of human cytomegalovirus requires the postlocalization function of tegument protein pp28 within the assembly compartment. J Virol 2007;81:6536–6547
  • Silva MC, Yu QC, Enquist L, Shenk T. Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument-associated capsids. J Virol 2003;77:10594–10605
  • Tanaka M, Kagawa H, Yamanashi Y, Sata T, Kawaguchi Y. 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 2003;77:1382–1391
  • Lee HC, Chouljenko VN, Chouljenko DV, Boudreaux MJ, Kousoulas KG. 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 2009;83:6115–6124
  • Tischer BK, von Einem J, Kaufer B, Osterrieder N. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. BioTechniques. 2006;40:191–197
  • Saied AA, Chouljenko VN, Subramanian R, Kousoulas KG. A Replication Competent HSV-1(McKrae) with a Mutation in the Amino-terminus of Glycoprotein K (gK) is Unable to Infect Mouse Trigeminal Ganglia after Cornea Infection. Curr Eye Res 2014. [epub ahead of print]
  • Subramanian R, D'Auvergne O, Kong H, Kousoulas KG. The cytoplasmic terminus of Kaposi's sarcoma-associated herpesvirus glycoprotein B is not essential for virion egress and infectivity. J Virol 2008;82:7144–7154
  • Subramanian R, Sehgal I, D'Auvergne O, Kousoulas KG. 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 2010;84:1704–1714
  • David AT, Saied A, Charles A, Subramanian R, Chouljenko VN, Kousoulas KG. 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 2012;3:e00144–12
  • David AT, Baghian A, Foster TP, Chouljenko VN, Kousoulas KG. The herpes simplex virus type 1 (HSV-1) glycoprotein K(gK) is essential for viral corneal spread and neuroinvasiveness. Curr Eye Res 2008;33:455–467
  • Sedarati F, Stevens JG. Biological basis for virulence of three strains of herpes simplex virus type 1. J Gen Virol 1987;68:2389–2395
  • Macdonald SJ, Mostafa HH, Morrison LA, Davido DJ. Genome sequence of herpes simplex virus 1 strain McKrae. J Virol 2012;86:9540–9541
  • Macdonald SJ, Mostafa HH, Morrison LA, Davido DJ. Genome sequence of herpes simplex virus 1 strain KOS. J Virol 2012;86:6371–6372
  • Szpara ML, Parsons L, Enquist LW. Sequence variability in clinical and laboratory isolates of herpes simplex virus 1 reveals new mutations. J Virol 2010;84:5303–5313
  • Chowdhury S, Naderi M, Chouljenko VN, Walker JD, Kousoulas KG. 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 alpha. Virol J 2012;9:1--8

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