Nectin-2-mediated entry of a syncytial strain of herpes simplex virus via pH-independent fusion with the plasma membrane of Chinese hamster ovary cells

Virology Journal - Tập 3 - Trang 1-10 - 2006
Mark G Delboy1, Jennifer L Patterson1, Aimee M Hollander1, Anthony V Nicola1
1Department of Microbiology and Immunology, Medical College of Virginia at Virginia Commonwealth University, Richmond, USA

Tóm tắt

Herpes simplex virus (HSV) can utilize multiple pathways to enter host cells. The factors that determine which route is taken are not clear. Chinese hamster ovary (CHO) cells that express glycoprotein D (gD)-binding receptors are model cells that support a pH-dependent, endocytic entry pathway for all HSV strains tested to date. Fusion-from-without (FFWO) is the induction of target cell fusion by addition of intact virions to cell monolayers in the absence of viral protein expression. The receptor requirements for HSV-induced FFWO are not known. We used the syncytial HSV-1 strain ANG path as a tool to evaluate the complex interplay between receptor usage, membrane fusion, and selection of entry pathway. Inhibitors of endocytosis and endosome acidification blocked ANG path entry into CHO cells expressing nectin-1 receptors, but not CHO-nectin-2 cells. Thus, under these conditions, nectin-2 mediates pH-independent entry at the plasma membrane. In addition, CHO-nectin-2 cells supported pH-dependent, endocytic entry of different strains of HSV-1, including rid1 and HFEM. The kinetics of ANG path entry was rapid (t1/2 of 5–10 min) regardless of entry route. However, HSV-1 ANG path entry by fusion with the CHO-nectin-2 cell plasma membrane was more efficient and resulted in larger syncytia. ANG path virions added to the surface of CHO-nectin-2 cells, but not receptor-negative CHO cells or CHO-nectin-1 cells, induced rapid FFWO. HSV-1 ANG path can enter CHO cells by either endocytic or non-endocytic pathways depending on whether nectin-1 or nectin-2 is present. In addition to these cellular receptors, one or more viral determinants is important for the selection of entry pathway. HSV-induced FFWO depends on the presence of an appropriate gD-receptor in the target membrane. Nectin-1 and nectin-2 target ANG path to divergent cellular pathways, and these receptors may have different roles in triggering viral membrane fusion.

Tài liệu tham khảo

Nicola AV, McEvoy AM, Straus SE: Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J Virol 2003,77(9):5324-5332. 10.1128/JVI.77.9.5324-5332.2003

Fuller AO, Spear PG: Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proc Natl Acad Sci U S A 1987,84(15):5454-5458. 10.1073/pnas.84.15.5454

Nicola AV, Straus SE: Cellular and viral requirements for rapid endocytic entry of herpes simplex virus. J Virol 2004,78(14):7508-7517. 10.1128/JVI.78.14.7508-7517.2004

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(11):6655-6663. 10.1128/JVI.79.11.6655-6663.2005

Gianni T, Campadelli-Fiume G, Menotti L: Entry of herpes simplex virus mediated by chimeric forms of nectin1 retargeted to endosomes or to lipid rafts occurs through acidic endosomes. J Virol 2004,78(22):12268-12276. 10.1128/JVI.78.22.12268-12276.2004

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(3):427-436. 10.1016/S0092-8674(00)81363-X

Cocchi F, Lopez M, Menotti L, Aoubala M, Dubreuil P, Campadelli-Fiume G: The V domain of herpesvirus Ig-like receptor (HIgR) contains a major functional region in herpes simplex virus-1 entry into cells and interacts physically with the viral glycoprotein D. Proc Natl Acad Sci U S A 1998,95(26):15700-15705. 10.1073/pnas.95.26.15700

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(5):305-319. 10.1002/1099-1654(200009/10)10:5<305::AID-RMV286>3.0.CO;2-T

Takahashi K, Nakanishi H, Miyahara M, Mandai K, Satoh K, Satoh A, Nishioka H, Aoki J, Nomoto A, Mizoguchi A, Takai Y: Nectin/PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J Cell Biol 1999,145(3):539-549. 10.1083/jcb.145.3.539

Warner MS, Geraghty RJ, Martinez WM, Montgomery RI, Whitbeck JC, Xu R, Eisenberg RJ, Cohen GH, Spear PG: A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 1998,246(1):179-189. 10.1006/viro.1998.9218

Sakisaka T, Takai Y: Biology and pathology of nectins and nectin-like molecules. Curr Opin Cell Biol 2004,16(5):513-521. 10.1016/j.ceb.2004.07.007

Krummenacher C, Baribaud I, Ponce de Leon M, Whitbeck JC, Lou H, Cohen GH, Eisenberg RJ: Localization of a binding site for herpes simplex virus glycoprotein D on herpesvirus entry mediator C by using antireceptor monoclonal antibodies. J Virol 2000,74(23):10863-10872. 10.1128/JVI.74.23.10863-10872.2000

Lopez M, Cocchi F, Menotti L, Avitabile E, Dubreuil P, Campadelli-Fiume G: Nectin2alpha (PRR2alpha or HveB) and nectin2delta are low-efficiency mediators for entry of herpes simplex virus mutants carrying the Leu25Pro substitution in glycoprotein D. J Virol 2000,74(3):1267-1274. 10.1128/JVI.74.3.1267-1274.2000

Martinez WM, Spear PG: Amino acid substitutions in the V domain of nectin-1 (HveC) that impair entry activity for herpes simplex virus types 1 and 2 but not for Pseudorabies virus or bovine herpesvirus 1. J Virol 2002,76(14):7255-7262. 10.1128/JVI.76.14.7255-7262.2002

Struyf F, Martinez WM, Spear PG: Mutations in the N-terminal domains of nectin-1 and nectin-2 reveal differences in requirements for entry of various alphaherpesviruses and for nectin-nectin interactions. J Virol 2002,76(24):12940-12950. 10.1128/JVI.76.24.12940-12950.2002

Martinez WM, Spear PG: Structural features of nectin-2 (HveB) required for herpes simplex virus entry. J Virol 2001,75(22):11185-11195. 10.1128/JVI.75.22.11185-11195.2001

Kwon H, Bai Q, Baek HJ, Felmet K, Burton EA, Goins WF, Cohen JB, Glorioso JC: Soluble V domain of Nectin-1/HveC enables entry of herpes simplex virus type 1 (HSV-1) into HSV-resistant cells by binding to viral glycoprotein D. J Virol 2006,80(1):138-148. 10.1128/JVI.80.1.138-148.2006

Yoon M, Spear PG: Random mutagenesis of the gene encoding a viral ligand for multiple cell entry receptors to obtain viral mutants altered for receptor usage. Proc Natl Acad Sci U S A 2004,101(49):17252-17257. 10.1073/pnas.0407892101

Connolly SA, Landsburg DJ, Carfi A, Wiley DC, Cohen GH, Eisenberg RJ: Structure-based mutagenesis of herpes simplex virus glycoprotein D defines three critical regions at the gD-HveA/HVEM binding interface. J Virol 2003,77(14):8127-8140. 10.1128/JVI.77.14.8127-8140.2003

Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, Cohen GH, Eisenberg RJ, Rosenberg RD, Spear PG: A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 1999,99(1):13-22. 10.1016/S0092-8674(00)80058-6

Cocchi F, Menotti L, Di Ninni V, Lopez M, Campadelli-Fiume G: The herpes simplex virus JMP mutant enters receptor-negative J cells through a novel pathway independent of the known receptors nectin1, HveA, and nectin2. J Virol 2004,78(9):4720-4729. 10.1128/JVI.78.9.4720-4729.2004

Perez A, Li QX, Perez-Romero P, Delassus G, Lopez SR, Sutter S, McLaren N, Fuller AO: A new class of receptor for herpes simplex virus has heptad repeat motifs that are common to membrane fusion proteins. J Virol 2005,79(12):7419-7430. 10.1128/JVI.79.12.7419-7430.2005

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(12):7609-7616. 10.1128/JVI.79.12.7609-7616.2005

Clement C, Tiwari V, Scanlan PM, Valyi-Nagy T, Yue BY, Shukla D: A novel role for phagocytosis-like uptake in herpes simplex virus entry. J Cell Biol 2006,174(7):1009-1021. 10.1083/jcb.200509155

Smith GA, Pomeranz L, Gross SP, Enquist LW: Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc Natl Acad Sci U S A 2004,101(45):16034-16039. 10.1073/pnas.0404686101

Whitbeck JC, Zuo Y, Milne RS, Cohen GH, Eisenberg RJ: Stable association of herpes simplex virus with target membranes is triggered by low pH in the presence of the gD receptor, HVEM. J Virol 2006,80(8):3773-3780. 10.1128/JVI.80.8.3773-3780.2006

Izumi KM, Stevens JG: Molecular and biological characterization of a herpes simplex virus type 1 (HSV-1) neuroinvasiveness gene. J Exp Med 1990,172(2):487-496. 10.1084/jem.172.2.487

Hoggan MD, Roizman B: The isolation and properties of a variant of herpes simplex producing multinucleated giant cellsin monolaer cultures in the presence of antibody. Am J Hyg 1959, 70: 208-219.

Walev I, Wollert KC, Weise K, Falke D: Characterization of fusion from without induced by herpes simplex virus. Arch Virol 1991,117(1-2):29-44. 10.1007/BF01310490

Marsh M, Helenius A: Virus entry: open sesame. Cell 2006,124(4):729-740. 10.1016/j.cell.2006.02.007

Manoj S, Jogger CR, Myscofski D, Yoon M, Spear PG: Mutations in herpes simplex virus glycoprotein D that prevent cell entry via nectins and alter cell tropism. Proc Natl Acad Sci U S A 2004,101(34):12414-12421. 10.1073/pnas.0404211101

Lingen M, Seck T, Weise K, Falke D: Two mutations in gB-1 and gD-1 of herpes simplex virus type 1 are involved in the "fusion from without" phenotype in different cell types. Virus Genes 1996,13(3):221-228. 10.1007/BF00366982

Zago A, Jogger CR, Spear PG: Use of herpes simplex virus and pseudorabies virus chimeric glycoprotein D molecules to identify regions critical for membrane fusion. Proc Natl Acad Sci U S A 2004,101(50):17498-17503. 10.1073/pnas.0408186101

Cocchi F, Fusco D, Menotti L, Gianni T, Eisenberg RJ, Cohen GH, Campadelli-Fiume G: The soluble ectodomain of herpes simplex virus gD contains a membrane-proximal pro-fusion domain and suffices to mediate virus entry. Proc Natl Acad Sci U S A 2004,101(19):7445-7450. 10.1073/pnas.0401883101

Krummenacher C, Supekar VM, Whitbeck JC, Lazear E, Connolly SA, Eisenberg RJ, Cohen GH, Wiley DC, Carfi A: Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. Embo J 2005,24(23):4144-4153. 10.1038/sj.emboj.7600875

Fusco D, Forghieri C, Campadelli-Fiume G: The pro-fusion domain of herpes simplex virus glycoprotein D (gD) interacts with the gD N terminus and is displaced by soluble forms of viral receptors. Proc Natl Acad Sci U S A 2005,102(26):9323-9328. 10.1073/pnas.0503907102

Pertel PE, Fridberg A, Parish ML, Spear PG: Cell fusion induced by herpes simplex virus glycoproteins gB, gD, and gH-gL requires a gD receptor but not necessarily heparan sulfate. Virology 2001, 279: 313-324. 10.1006/viro.2000.0713

Tiwari V, Clement C, Duncan MB, Chen J, Liu J, Shukla D: A role for 3-O-sulfated heparan sulfate in cell fusion induced by herpes simplex virus type 1. J Gen Virol 2004, 85: 805-809. 10.1099/vir.0.19641-0

Subramanian RP, Dunn JE, Geraghty RJ: The nectin-1alpha transmembrane domain, but not the cytoplasmic tail, influences cell fusion induced by HSV-1 glycoproteins. Virology 2005, 339: 176-191. 10.1016/j.virol.2005.05.031

Jones NA, Geraghty RJ: Fusion activity of lipid-anchored envelope glycoproteins of herpes simplex virus type 1. Virology 2004, 324: 213-228. 10.1016/j.virol.2004.03.024

Cairns TM, Milne RS, Ponce-de-Leon M, Tobin DK, Cohen GH, Eisenberg RJ: Structure-function analysis of herpes simplex virus type 1 gD and gH-gL: clues from gDgH chimeras. J Virol 2003, 77: 6731-6742. 10.1128/JVI.77.12.6731-6742.2003

Yoon M, Zago A, Shukla D, Spear PG: Mutations in the N termini of herpes simplex virus type 1 and 2 gDs alter functional interactions with the entry/fusion receptors HVEM, nectin-2, and 3-O-sulfated heparan sulfate but not with nectin-1. J Virol 2003, 77: 9221-9231. 10.1128/JVI.77.17.9221-9231.2003

Wildy P, Russell WC, Horne RW: The morphology of herpes virus. Virology 1960, 12: 204-222. 10.1016/0042-6822(60)90195-1