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. 2013 Jul 10;790:167–177. doi: 10.1007/978-1-4614-7651-1_9

Entry of Rhabdoviruses Into Animal Cells

Andrew D Regan 4, Gary R Whittaker 4,✉
Editors: Stefan Pöhlmann1,2, Graham Simmons3
PMCID: PMC7123998  PMID: 23884591

Abstract

Entry is the first step in the infectious life cycle of a virus. In the case of rhabdoviruses, entry is facilitated exclusively by the envelope glycoprotein G and its interactions with the host cell. For vesicular stomatitis virus (VSV), attachment to the cell surface was thought to be facilitated by interactions with the lipid phosphatidylserine, however recent work suggests that it is in fact initiated by recognition of proteinaeous receptors. Clathrin-mediated endocytosis delivers the virions into endosomes where they have been proposed to traffic to multi-vesicular bodies. There, the viral envelope fuses with internal vesicles in a process mediated by glycoprotein G in a pH- and phosphatidylserine-dependent manner. A clear mechanistic understanding of glycoprotein G mediated fusion has yet to be obtained, however current data suggests that it is likely facilitated by events distinct from Class I or Class II fusion proteins of other viruses. Rhabdoviruses are also notable in that their fusion protein exists in a reversible pH-dependent equilibrium, which prevents irreversible preactivation during assembly, and may prove to be relevant in the mediation of cell-to-cell fusion - an alternate form of viral spread.

Keywords: Membrane Fusion, Rabies Virus, Vesicular Stomatitis Virus, Venezuelan Equine Encephalitis Virus, Viral Haemorrhagic Septicaemia Virus

References

  • 1.Fauquet C.M., Mayo M.A., Maniloff J., et al., editors. Virus Taxonomy. San Diego: Elsevier Academic Press; 2005. [Google Scholar]
  • 2.Bearzotti M., Delmas B., Lamoureux A., et al. Fish rhabdovirus cell entry is mediated by fibronectin. J Virol. 1999;73(9):7703–7709. doi: 10.1128/jvi.73.9.7703-7709.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Lafon M. Rabies virus receptors. J Neurovirol. 2005;11(1):82–87. doi: 10.1080/13550280590900427. [DOI] [PubMed] [Google Scholar]
  • 4.Wunner W.H., Reagan K.J., Koprowski H. Characterization of saturable binding sites for rabies virus. J Virol. 1984;50(3):691–697. doi: 10.1128/jvi.50.3.691-697.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Altstiel L.D., Landsberger F.R. Lipid-protein interactions between the surface glycoprotein of vesicular stomatitis virus and the lipid bilayer. Virology. 1981;115(1):1–9. doi: 10.1016/0042-6822(81)90083-0. [DOI] [PubMed] [Google Scholar]
  • 6.Gaudin Y., Ruigrok R.W., Knossow M., et al. Low-pH conformational changes of rabies virus glycoprotein and their role in membrane fusion. J Virol. 1993;67(3):1365–1372. doi: 10.1128/jvi.67.3.1365-1372.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Konieczko E.M., Whitaker-Dowling P.A., Widnell C.C. Membrane fusion as a determinant of the infectibility of cells by vesicular stomatitis virus. Virology. 1994;199(1):200–211. doi: 10.1006/viro.1994.1112. [DOI] [PubMed] [Google Scholar]
  • 8.Lecocq-Xhonneux F., Thiry M., Dheur I., et al. A recombinant viral haemorrhagic septicaemia virus glycoprotein expressed in insect cells induces protective immunity in rainbow trout. J Gen Virol. 1994;75:1579–1587. doi: 10.1099/0022-1317-75-7-1579. [DOI] [PubMed] [Google Scholar]
  • 9.Coll J.M. The glycoprotein G of rhabdoviruses. Arch Virol. 1995;140(5):827–851. doi: 10.1007/BF01314961. [DOI] [PubMed] [Google Scholar]
  • 10.Balch W.E., Elliott M.M., Keller D.S. ATP-coupled transport of vesicular stomatitis virus G protein between the endoplasmic reticulum and the Golgi. J Biol Chem. 1986;261(31):14681–14689. [PubMed] [Google Scholar]
  • 11.Doms R.W., Keller D.S., Helenius A., et al. Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J Cell Biol. 1987;105(5):1957–1969. doi: 10.1083/jcb.105.5.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Gaudin Y., Ruigrok R.W., Tuffereau C., et al. Rabies virus glycoprotein is a trimer. Virology. 1992;187(2):627–632. doi: 10.1016/0042-6822(92)90465-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Kreis T.E., Lodish H.F. Oligomerization is essential for transport of vesicular stomatitis viral glycoprotein to the cell surface. Cell. 1986;46(6):929–937. doi: 10.1016/0092-8674(86)90075-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Lyles D.S., Varela V.A., Parce J.W. Dynamic nature of the quaternary structure of the vesicular stomatitis virus envelope glycoprotein. Biochemistry. 1990;29(10):2442–2449. doi: 10.1021/bi00462a002. [DOI] [PubMed] [Google Scholar]
  • 15.Whitt M.A., Buonocore L., Prehaud C., et al. Membrane fusion activity, oligomerization, and assembly of the rabies virus glycoprotein. Virology. 1991;185(2):681–688. doi: 10.1016/0042-6822(91)90539-N. [DOI] [PubMed] [Google Scholar]
  • 16.Wilcox M.D., McKenzie M.O., Parce J.W., et al. Subunit interactions of vesicular stomatitis virus envelope glycoprotein influenced by detergent micelles and lipid bilayers. Biochemistry. 1992;31(43):10458–10464. doi: 10.1021/bi00158a007. [DOI] [PubMed] [Google Scholar]
  • 17.Zagouras P., Ruusala A., Rose J.K. Dissociation and reassociation of oligomeric viral glycoprotein subunits in the endoplasmic reticulum. J Virol. 1991;65(4):1976–1984. doi: 10.1128/jvi.65.4.1976-1984.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Schlegel R., Willingham M.C., Pastan I.H. Saturable binding sites for vesicular stomatitis virus on the surface of Vero cells. J Virol. 1982;43(3):871–875. doi: 10.1128/jvi.43.3.871-875.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Conti C., Hauttecoeur B., Morelec M.J., et al. Inhibition of rabies virus infection by a soluble membrane fraction from the rat central nervous system. Arch Virol. 1988;98(1–2):73–86. doi: 10.1007/BF01321007. [DOI] [PubMed] [Google Scholar]
  • 20.Conti C., Mastromarino P., Ciuffarella M.G., et al. Characterization of rat brain cellular membrane components acting as receptors for vesicular stomatitis virus. Brief report. Arch Virol. 1988;99(3–4):261–269. doi: 10.1007/BF01311075. [DOI] [PubMed] [Google Scholar]
  • 21.Mastromarino P., Conti C., Goldoni P., et al. Characterization of membrane components of the erythrocyte involved in vesicular stomatitis virus attachment and fusion at acidic pH. J Gen Virol. 1987;68:2359–2369. doi: 10.1099/0022-1317-68-9-2359. [DOI] [PubMed] [Google Scholar]
  • 22.Schlegel R., Tralka T.S., Willingham M.C., et al. Inhibition of VSVbinding and infectivity by phosphatidylserine: Is phosphatidylserine a VSV-binding site? Cell. 1983;32(2):639–646. doi: 10.1016/0092-8674(83)90483-X. [DOI] [PubMed] [Google Scholar]
  • 23.Coll J.M. Heptad-repeat sequences in the glycoprotein of rhabdoviruses. Virus Genes. 1995;10(2):107–114. doi: 10.1007/BF01702591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Coll J.M. Synthetic peptides from the heptad repeats of the glycoproteins of rabies, vesicular stomatitis and fish rhabdoviruses bind phosphatidylserine. Arch Virol. 1997;142(10):2089–2097. doi: 10.1007/s007050050227. [DOI] [PubMed] [Google Scholar]
  • 25.Hall M.P., Burson K.K., Huestis W.H. Interactions of a vesicular stomatitis virus G protein fragment with phosphatidylserine: NMR and fluorescence studies. Biochim Biophys Acta. 1998;1415(1):101–113. doi: 10.1016/S0005-2736(98)00186-2. [DOI] [PubMed] [Google Scholar]
  • 26.Morrot G., Herve P., Zachowski A., et al. Aminophospholipid translocase of human erythrocytes: Phospholipid substrate specificity and effect of cholesterol. Biochemistry. 1989;28(8):3456–3462. doi: 10.1021/bi00434a046. [DOI] [PubMed] [Google Scholar]
  • 27.Zachowski A., Favre E., Cribier S., et al. Outside-inside translocation of aminophospholipids in the human erythrocyte membrane is mediated by a specific enzyme. Biochemistry. 1986;25(9):2585–2590. doi: 10.1021/bi00357a046. [DOI] [PubMed] [Google Scholar]
  • 28.Coil D.A., Miller A.D. Phosphatidylserine is not the cell surface receptor for vesicular stomatitis virus. J Virol. 2004;78(20):10920–10926. doi: 10.1128/JVI.78.20.10920-10926.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Carneiro F.A., Lapido-Loureiro P.A., Cordo S.M., et al. Probing the interaction between vesicular stomatitis virus and phosphatidylserine. Eur Biophys. 2006;35(2):145–154. doi: 10.1007/s00249-005-0012-z. [DOI] [PubMed] [Google Scholar]
  • 30.Burrage T.G., Tignor G.H., Smith A.L. Rabies virus binding at neuromuscular junctions. Virus Res. 1985;2(3):273–289. doi: 10.1016/0168-1702(85)90014-0. [DOI] [PubMed] [Google Scholar]
  • 31.Castellanos J.E., Castaneda D.R., Velandia A.E., et al. Partial inhibition of the in vitro infection of adult mouse dorsal root ganglion neurons by rabies virus using nicotinic antagonists. Neurosci Lett. 1997;229(3):198–200. doi: 10.1016/S0304-3940(97)00440-0. [DOI] [PubMed] [Google Scholar]
  • 32.Gastka M., Horvath J., Lentz T.L. Rabies virus binding to the nicotinic acetylcholine receptor alpha subunit demonstrated by virus overlay protein binding assay. J Gen Virol. 1996;77:2437–2440. doi: 10.1099/0022-1317-77-10-2437. [DOI] [PubMed] [Google Scholar]
  • 33.Lentz T.L., Benson R.J., Klimowicz D., et al. Binding of rabies virus to purified Torpedo acetylcholine receptor. Brain Res. 1986;387(3):211–219. doi: 10.1016/0169-328x(86)90027-6. [DOI] [PubMed] [Google Scholar]
  • 34.Lentz T.L., Burrage T.G., Smith A.L., et al. Is the acetylcholine receptor a rabies virus receptor? Science. 1982;215(4529):182–184. doi: 10.1126/science.7053569. [DOI] [PubMed] [Google Scholar]
  • 35.Lewis P., Fu Y., Lentz T. Rabies virus entry at the neuromuscular junction in nerve-muscle cocultures. Muscle Nerve. 2000;23(5):720–730. doi: 10.1002/(SICI)1097-4598(200005)23:5<720::AID-MUS9>3.0.CO;2-5. [DOI] [PubMed] [Google Scholar]
  • 36.Superti F., Seganti L., Ruggeri F.M., et al. Entry pathway of vesicular stomatitis virus into different host cells. J Gen Virol. 1987;68:387–399. doi: 10.1099/0022-1317-68-2-387. [DOI] [PubMed] [Google Scholar]
  • 37.Matlin K.S., Reggio H., Helenius A., et al. Pathway of vesicular stomatitis virus leading to infection. J Mol Biol. 1982;156:609–631. doi: 10.1016/0022-2836(82)90269-8. [DOI] [PubMed] [Google Scholar]
  • 38.Cernescu C., Constantinescu S.N., Popescu L.M. Electron microscopic observations of vesicular stomatitis virus particles penetration in human fibroblasts. Rev Roum Virol. 1990;41:93–96. [PubMed] [Google Scholar]
  • 39.Sun X., Yau V.K., Briggs B.J., et al. Role of clathrin-mediated endocytosis during vesicular stomatitis virus entry into host cells. Virology. 2005;338(1):53–60. doi: 10.1016/j.virol.2005.05.006. [DOI] [PubMed] [Google Scholar]
  • 40.Kolokoltsov A.A., Fleming E.H., Davey R.A. Venezuelan equine encephalitis virus entry mechanism requires late endosome formation and resists cellmembrane cholesterol depletion. Virology. 2006;347(2):333–342. doi: 10.1016/j.virol.2005.11.051. [DOI] [PubMed] [Google Scholar]
  • 41.Daro E., Sheff D., Gomez M., et al. Inhibition of endosome function in CHO cells bearing atemperature-sensitive defect in the coatomer (COPI) component epsilon-COP. J Cell Biol. 1997;139(7):1747–1759. doi: 10.1083/jcb.139.7.1747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Pelkmans L., Fava E., Grabner H., et al. Genome-wide analysis of human kinases in clathrin-and caveolae/ raft-mediated endocytosis. Nature. 2005;436(7047):78–86. doi: 10.1038/nature03571. [DOI] [PubMed] [Google Scholar]
  • 43.Fuller S., von Bonsdorff C.H., Simons K. Vesicular stomatitis virus infects and matures only through the basolateral surface of the polarized epithelial cell line, MDCK. Cell. 1984;38(l):65–77. doi: 10.1016/0092-8674(84)90527-0. [DOI] [PubMed] [Google Scholar]
  • 44.Gottlieb T.A., Ivanov I.E., Adesnik M., et al. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol. 1993;120(3):695–710. doi: 10.1083/jcb.120.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Blumenthal R., Bali-Puri A., Walter A., et al. pH-dependent fusion of vesicular stomatitis virus with Vero cells. Measurement by dequenching of octadecyl rhodamine fluorescence. J Biol Chem. 1987;262(28):13614–13619. [PubMed] [Google Scholar]
  • 46.Florkiewicz R.Z., Rose J.K. A cell line expressing vesicular stomatitis virus glycoprotein fuses at low pH. Science. 1984;225(4663):721–723. doi: 10.1126/science.6087454. [DOI] [PubMed] [Google Scholar]
  • 47.Hernandez L.D., Hoffman L.R., Wolfsberg T.G., et al. Virus-cell and cell-cell fusion. Annu Rev Cell Dev Biol. 1996;12:627–661. doi: 10.1146/annurev.cellbio.12.1.627. [DOI] [PubMed] [Google Scholar]
  • 48.Matlin K.S., Reggio H., Helenius A., et al. Pathway of vesicular stomatitis virus entry leading to infection. J Mol Biol. 1982;156(3):609–631. doi: 10.1016/0022-2836(82)90269-8. [DOI] [PubMed] [Google Scholar]
  • 49.White J., Matlin K., Helenius A. Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J Cell Biol. 1981;89(3):674–679. doi: 10.1083/jcb.89.3.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Carneiro F.A., Ferradosa A.S., Da Poian A.T. Low pH-induced conformational changes in vesicular stomatitis virus glycoprotein involve dramatic structure reorganization. J Biol Chem. 2001;276(l):62–67. doi: 10.1074/jbc.M008753200. [DOI] [PubMed] [Google Scholar]
  • 51.Pak C.C., Puri A., Blumenthal R. Conformational changes and fusion activity of vesicular stomatitis virus glycoprotein: [125I]iodonaphthyl azide photolabeling studies in biological membranes. Biochemistry. 1997;36(29):8890–8896. doi: 10.1021/bi9702851. [DOI] [PubMed] [Google Scholar]
  • 52.Gaudin Y., Tuffereau C., Durrer P., et al. Biological function of the low-pH, fusion-inactive conformation of rabies virus glycoprotein (G): G is transported in a fusion-inactive state-like conformation. J Virol. 1995;69(9):5528–5534. doi: 10.1128/jvi.69.9.5528-5534.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Gaudin Y. Reversibility in fusion protein conformational changes. The intriguing case of rhabdo virus-induced membrane fusion. Subcell Biochem. 2000;34:379–408. doi: 10.1007/0-306-46824-7_10. [DOI] [PubMed] [Google Scholar]
  • 54.Colman P.M., Lawrence M.C. The structural biology of type I viral membrane fusion. Nat Rev Mol Cell Biol. 2003;4(4):309–319. doi: 10.1038/nrm1076. [DOI] [PubMed] [Google Scholar]
  • 55.Le Blanc I., Luyet P.P., Pons V., et al. Endosome-to-cytosol transport of viral nucleocapsids. Nat Cell Biol. 2005;7(7):653–664. doi: 10.1038/ncb1269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Matsuo H., Chevallier J., Mayran N., et al. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science. 2004;303(5657):531–534. doi: 10.1126/science.1092425. [DOI] [PubMed] [Google Scholar]
  • 57.Uchil P., Mothes W. Viral entry: A detour through multivesicular bodies. Nat Cell Biol. 2005;7(7):641–642. doi: 10.1038/ncb0705-641. [DOI] [PubMed] [Google Scholar]
  • 58.Earp L.J., Delos S.E., Park H.E., et al. The many mechanisms of viral membrane fusion proteins. Curr Top Microbiol Immunol. 2005;285:25–66. doi: 10.1007/3-540-26764-6_2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Zhang L., Ghosh H.P. Characterization of the putative fusogenic domain in vesicular stomatitis virus glycoprotein G. J Virol. 1994;68(4):2186–2193. doi: 10.1128/jvi.68.4.2186-2193.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Kielian M. Class II virus membrane fusion proteins. Virology. 2006;344(1):38–47. doi: 10.1016/j.virol.2005.09.036. [DOI] [PubMed] [Google Scholar]
  • 61.Durrer P., Gaudin Y., Ruigrok R.W., et al. Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses. J Biol Chem. 1995;270(29):17575–17581. doi: 10.1074/jbc.270.29.17575. [DOI] [PubMed] [Google Scholar]
  • 62.Fredericksen B.L., Whitt M.A. Vesicular stomatitis virus glycoprotein mutations that affect membrane fusion activity and abolish virus infectivity. J Virol. 1995;69(3):1435–1443. doi: 10.1128/jvi.69.3.1435-1443.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Li Y., Drone C., Sat E., et al. Mutational analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains. J Virol. 1993;67(7):4070–4077. doi: 10.1128/jvi.67.7.4070-4077.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Shokralla S., He Y., Wanas E., et al. Mutations in a carboxy-terminal region of vesicular stomatitis virus glycoprotein G that affect membrane fusion activity. Virology. 1998;75:39–50. doi: 10.1006/viro.1997.8986. [DOI] [PubMed] [Google Scholar]
  • 65.Gaudin Y., Raux H., Flamand A., et al. Identification of amino acids controlling the low-pH-induced conformational change of rabies virus glycoprotein. J Virol. 1996;70:7371–7378. doi: 10.1128/jvi.70.11.7371-7378.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Shokralla S., Chernish R., Ghosh H.P. Effect of double-site mutations of vesicular stomatitis virus glycoprotein G on membrane fusion activity. Virology. 1999;256:119–129. doi: 10.1006/viro.1999.9606. [DOI] [PubMed] [Google Scholar]
  • 67.Carneiro F.A., Stauffer F., Lima C.S., et al. Membrane fusion induced by vesicular stomatitis virus depends on histidine protonation. J Biol Chem. 2003;278(16):13789–13794. doi: 10.1074/jbc.M210615200. [DOI] [PubMed] [Google Scholar]
  • 68.Nunez E., Fernandez A.M., Estepa A., et al. Phospholipid interactions of a peptide from the fusion-related domain of the glycoprotein of VHSV, a fish rhabdovirus. Virology. 1998;243(2):322–330. doi: 10.1006/viro.1998.9076. [DOI] [PubMed] [Google Scholar]
  • 69.Carneiro F.A., Bianconi M.L., Weissmuller G., et al. Membrane recognition by vesicular stomatits virus involves enthalpy-driven protein-lipid interactions. J Virol. 2002;76:3756–3764. doi: 10.1128/JVI.76.8.3756-3764.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Estepa A.M., Rocha A.I., Mas V., et al. A protein G fragment from the salmonid viral hemorrhagic septicemia rhabdovirus induces cell-to-cell fusion and membrane phosphatidylserine translocation at low pH. J Biol Chem. 2001;276(49):46268–46275. doi: 10.1074/jbc.M108682200. [DOI] [PubMed] [Google Scholar]
  • 71.Jeetendra E., Ghosh K., Odell D., et al. The membrane-proximal region of vesicular stomatitis virus glycoprotein G ectodomain is critical for fusion and virus infectivity. J Virol. 2003;77(23):12807–12818. doi: 10.1128/JVI.77.23.12807-12818.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Jeetendra E., Robison C.S., Albritton L.M., et al. The membrane-proximal domain of vesicular stomatitis virus G protein functions as a membrane fusion potentiator and can induce hemifusion. J Virol. 2002;76(23):12300–12311. doi: 10.1128/JVI.76.23.12300-12311.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Langosch D., Brosig B., Pipkorn R. Peptide mimics of the vesicular stomatitis virus G-protein transmembrane segment drive membrane fusion in vitro. J Biol Chem. 2001;276(34):32016–32021. doi: 10.1074/jbc.M102579200. [DOI] [PubMed] [Google Scholar]
  • 74.Cleverley D.Z., Lenard J. The transmembrane domain in viral fusion: Essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc Natl Acad Sci USA. 1998;95(7):3425–3430. doi: 10.1073/pnas.95.7.3425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Odell D., Wanas E., Yan J., et al. Influence of membrane anchoring and cytoplasmic domains on the fusogenic activity of vesicular stomatitis virus glycoprotein G. J Virol. 1997;71(10):7996–8000. doi: 10.1128/jvi.71.10.7996-8000.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Skehel J.J., Wiley D.C. Receptor binding and membrane fusion in virus entry: The influenza hemagglutinin. Annu Rev Biochem. 2000;69:531–569. doi: 10.1146/annurev.biochem.69.1.531. [DOI] [PubMed] [Google Scholar]
  • 77.Roberts P.C., Kipperman T., Compans R.W. Vesicular stomatitis virus G protein acquires pH-independent fusion activity during transport in a polarized endometrial cell line. J Virol. 1999;73(12):10447–10457. doi: 10.1128/jvi.73.12.10447-10457.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 78.Simmons G., Reeves J.D., Rennekamp A.J., et al. Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proc Natl Acad Sci USA. 2004;101(12):4240–4245. doi: 10.1073/pnas.0306446101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Tscherne D.M., Jones C.T., Evans M.J., et al. Time-and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J Virol. 2006;80(4):1734–1741. doi: 10.1128/JVI.80.4.1734-1741.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Chu V.C., McElroy L.J., Chu V., et al. The avian coronavirus infectious bronchitis virus undergoes direct low-pH-dependent fusion activation during entry into host cells. J Virol. 2006;80(7):3180–3188. doi: 10.1128/JVI.80.7.3180-3188.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Finke S., Conzelmann K.K. Recombinant rhabdo viruses: Vectors for vaccine development and gene therapy. Curr Top Microbiol Immunol. 2005;292:165–200. doi: 10.1007/3-540-27485-5_8. [DOI] [PubMed] [Google Scholar]
  • 82.Roche S., Bressanelli S., Rey F.A., Gaudin Y. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science. 2006;313(5784):187–191. doi: 10.1126/science.1127683. [DOI] [PubMed] [Google Scholar]

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