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Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 285))

Abstract

Virus entry is initiated by recognition by receptors present on the surface of host cells. Receptors can be major mediators of virus tropism, and in many cases receptor interactions occur in an apparently programmed series of events utilizing multiple receptors. After receptor interaction, both enveloped and nonenveloped viruses must deliver their genome across either the endosomal or plasma membrane for infection to proceed. Genome delivery occurs either by membrane fusion (in the case of enveloped viruses) or by pore formation or other means of permeabilizing the lipid bilayer (in the case of nonenveloped viruses). For those viruses that enter cells via endosomes, specific receptor interactions (and the signaling events that ensue) may control the particular route of endocytosis and/or the ultimate destination of the incoming virus particles. Our conception of virus entry is increasingly becoming more complex; however, the specificity involved in entry processes, once ascertained, may ultimately lead to the production of effective antiviral agents.

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References

  • Ashok A, Atwood WJ (2003) Contrasting roles of endosomal pH and the cytoskeleton in infection of human glial cells by JC virus and Simian Virus 40. J Virol 77:1347–1356

    Article  PubMed  Google Scholar 

  • Baranowski E, Ruiz-Jarabo CM, Domingo E (2001) Evolution of cell recognition by viruses. Science 292:1102–1105

    Article  PubMed  Google Scholar 

  • Bayer N, Schober D, Huttinger M, Blaas D, Fuchs R (2001) Inhibition of clathrin-dependent endocytosis has multiple effects on human rhinovirus serotype 2 cell entry. J Biol Chem 276:3952–3962

    Article  PubMed  Google Scholar 

  • Bergelson JM, Cunningham JA, Droguett G, Kurt-Jones EA, Krithivas A, Hong JS, Horwitz MS, Crowell RL, Finberg RW (1997) Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275:1320–1323

    Article  PubMed  Google Scholar 

  • Berger EA, Murphy PM, Farber JM (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism and disease. Annu Rev Immunol 17:657–700

    Article  PubMed  Google Scholar 

  • Borsa J, Morash BD, Sargent MD, Copps TP, Lievaart PA, Szekely JG (1979) Two modes of entry of reovirus particles into L cells. J Gen Virol 45:161–170

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Carbone R, Fre S, Iannolo G, Belleudi F, Mancini P, Pelicci PG, Torrisi MR, Di Fiore PP (1997) Eps15 and Eps15R are essential components of the endocytic pathway. Cancer Res 57:5498–5504

    PubMed  Google Scholar 

  • Chandran K, Farsetta DL, Nibert ML (2002) Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein micro 1 mediates membrane disruption. J Virol 76:9920–9933

    Article  PubMed  Google Scholar 

  • Constantinescu SN, Cernescu CD, Popescu LM (1991) Effects of protein kinase C inhibitors on viral entry and infectivity. FEBS Lett 292:31–33

    Article  PubMed  Google Scholar 

  • DeTulleo L, Kirchausen T (1998) The clathrin endocytic pathway in viral infection. EMBO J 17:4585–4593

    Article  PubMed  Google Scholar 

  • Doxsey SJ, Brodsky FM, Blank GS, Helenius A (1987) Inhibition of endocytosis by anti-clathrin antibodies. Cell 50:453–463

    Article  PubMed  Google Scholar 

  • Ebert DH, Deussing J, Peters C, Dermody TS (2002) Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. J Biol Chem 277:24609–24617

    Article  PubMed  Google Scholar 

  • Fackler OT, Peterlin BM (2000) Endocytic entry of HIV-1. Curr Biol 10:1005–1008

    Article  PubMed  Google Scholar 

  • Fredericksen BL, Wei BL, Yao J, Luo T, Garcia JV (2002) Inhibition of endosomal/lysosomal degradation increases the infectivity of human immunodeficiency virus. J Virol 76:11440–11446

    Article  PubMed  Google Scholar 

  • Geijtenbeek TB, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, Nottet HS, KewalRamani VN, Littman DR, Figdor CG, van Kooyk Y (2000) DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587–597

    Article  PubMed  Google Scholar 

  • Gilbert JM, Benjamin TL (2000) Early steps of polyomavirus entry into cells. J Virol 74:8582–8588

    Article  PubMed  Google Scholar 

  • Girod A, Wobus CE, Zadori Z, Ried M, Leike K, Tijssen P, Kleinschmidt JA, Hallek M (2002) The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J Gen Virol 83:973–978

    PubMed  Google Scholar 

  • Golden JW, Linke J, Schmechel S, Thoemke K, Schiff LA (2002) Addition of exogenous protease facilitates reovirus infection in many restrictive cells. J Virol 76:7430–7443

    Article  PubMed  Google Scholar 

  • Greber UF, Singh I, Helenius A (1994) Mechanisms of virus uncoating. Trends Microbiol 2:52–56

    Article  PubMed  Google Scholar 

  • Hay AJ, Wolstenholme AJ, Skehel JJ, Smith MH (1985) The molecular basis of the specific anti-influenza action of amantadine. EMBO J 4:3021–3024

    PubMed  Google Scholar 

  • Hofer F, Gruenberger M, Kowalski H, Machat H, Huettinger M, Kuechler E, Blass D (1994) Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Natl Acad Sci U S A 91:1839–1842

    PubMed  Google Scholar 

  • Hogle JM (2002) Poliovirus cell entry: Common structural themes in viral cell entry pathways. Annu Rev Microbiol 56:677–702

    Article  PubMed  Google Scholar 

  • Huber M, Brabec M, Bayer N, Blaas D, Fuchs R (2001) Elevated endosomal pH in HeLa cells overexpressing mutant dynamin can affect infection by pH-sensitive viruses. Traffic 2:727–736

    Article  PubMed  Google Scholar 

  • Hueffer K, Parker JS, Weichert WS, Geisel RE, J-Y. S, Parrish CR (2003) The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J Virol in press

    Google Scholar 

  • Iruzun A, Carrasco L (2001) Entry of poliovirus into cells is blocked by valinomycin and concanamycin A. Biochemistry 40:3589–3600

    Article  PubMed  Google Scholar 

  • Jin M, Park J, Lee S, Park B, Shin J, Song KJ, Ahn TI, Hwang SY, Ahn BY, Ahn K (2002) Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis. Virology 294:60–69

    Article  PubMed  Google Scholar 

  • Joki-Korpela P, Marjomaki V, Krogerus C, Heino J, Hyypia T (2001) Entry of human parechovirus 1. J Virol 75:1958–1967

    Article  PubMed  Google Scholar 

  • Kartenbeck J, Stukenbrok H, Helenius A (1989) Endocytosis of simian virus 40 into the endoplasmic reticulum. J Cell Biol 109:2721–2729

    Article  PubMed  Google Scholar 

  • Lamb RA (1993) Paramyxovirus fusion: a hypothesis for changes. Virology 197:1–11

    Article  PubMed  Google Scholar 

  • Lee S, Zhao Y, Anderson WF (1999) Receptor-mediated Moloney murine leukemia virus entry can occur independently of the clathrin-coated-pit-mediated endocytic pathway. J Virol 73:5994–6005

    PubMed  Google Scholar 

  • Lewis JK, Bothner B, Smith TJ, Siuzdak G (1998) Antiviral agent blocks breathing of the common cold virus. Proc Natl Acad Sci U S A 95:6774–6778

    Article  PubMed  Google Scholar 

  • Li E, Stupak D, Klemke R, Cheresh DA, Nemerow GR (1998) Adenovirus endocytosis via αV integrins requires phosphoinositide-3-OH kinase. J Virol 72:2055–2061

    PubMed  Google Scholar 

  • Liu J, Thorp SC (2002) Cell surface heparan sulfate and its roles in assisting viral infections. Med Res Rev 22:1–25

    Article  PubMed  Google Scholar 

  • Madshus IH, Sandvig K, Olsnes S, van Deurs B (1987) Effect of reduced endocytosis induced by hypotonic shock and potassium depletion on the infection of Hep 2 cells by picornaviruses. J Cell Physiol 131:14–22

    Article  PubMed  Google Scholar 

  • Marechal V, Prevost MC, Petit C, Perret E, Heard JM, Schwartz O (2001) Human immunodeficiency virus Type 1 entry into macrophages mediated by macropinocytosis. J Virol 75:11166–11177

    Article  PubMed  Google Scholar 

  • Marjomaki V, Pietiainen V, Matilainen H, Upla P, Ivaska J, Nissinen L, Reunanen H, Huttunen P, Hyypia T, Heino J (2002) Internalization of echovirus 1 in caveolae. J Virol 76:1856–1865

    Article  PubMed  Google Scholar 

  • Marsh M, Bron R (1997) SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J Cell Sci 110:95–103

    PubMed  Google Scholar 

  • Marsh M, Helenius A (1980) Adsorptive endocytosis of Semliki Forest virus. J Mol Biol 142:439–454

    Article  PubMed  Google Scholar 

  • Marsh M, Helenius A (1989) Virus entry into animal cells. Adv Virus Res 36:107–151

    PubMed  Google Scholar 

  • Marsh M, Pelchen-Matthews A (1994), The endocytic pathway and virus entry, in Cellular Receptors for Animal Viruses, Ed. Wimmer E, 215–240, Cold Spring Harbor Press, Cold Spring Harbor, NY

    Google Scholar 

  • Marsh M, Pelchen-Matthews A (2000) Endocytosis in viral replication. Traffic 1:525–532

    Article  PubMed  Google Scholar 

  • Matlin KS, Reggio H, Helenius A, Simons K (1981) Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 91:601–613

    Article  PubMed  Google Scholar 

  • Matlin KS, Reggio H, Helenius A, Simons K (1982) Pathway of vesicular stomatitis virus leading to infection. J Mol Biol 156:609–631

    Article  PubMed  Google Scholar 

  • Meier O, Boucke K, Hammer SV, Keller S, Stidwill RP, Hemmi S, Greber UF (2002) Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 158:1119–1131

    Article  PubMed  Google Scholar 

  • Mettenleiter TC (2002) Brief overview on cellular virus receptors. Virus Res 82:3–8

    Article  PubMed  Google Scholar 

  • Miller N, Hutt-Fletcher LM (1992) Epstein-Barr virus enters B cells and epithelial cells by different routes. J Virol 66:3409–3414

    PubMed  Google Scholar 

  • Miyazawa N, Crystal RG, Leopold PL (2001) Adenovirus serotype 7 retention in a late endosomal compartment prior to cytosol escape is modulated by fiber protein. J Virol 75:1387–1400

    Article  PubMed  Google Scholar 

  • Mothes W, Boerger AL, Narayan S, Cunningham JM, Young JAT (2000) Retroviral entry mediated by receptor priming and low pH triggering of and envelope glycoprotein. Cell 103:679–689

    Article  PubMed  Google Scholar 

  • Nemerow GR (2000) Cell receptors involved in adenovirus entry. Virology 274:1–4

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Nomoto A, Koike S, Aoki J (1994) Tissue tropism and species specificity of poliovirus infection. Trends Microbiol 2:47–51

    Article  PubMed  Google Scholar 

  • Norkin LC (1999) Simian virus 40 infection via MHC class I molecules and caveolae. Immunol Rev 168:13–22

    PubMed  Google Scholar 

  • Norkin LC, Anderson HA, Wolfrom SA, Oppenheim A (2002) Caveolar endocytosis of simian virus 40 is followed by brefeldin A-sensitive transport to the endoplasmic reticulum, where the virus disassembles. J Virol 76:5156–5166

    Article  PubMed  Google Scholar 

  • O'Hara B, Olson W (2002) HIV entry inhibitors in clinical development. Curr Opin Pharmacol 2:523

    Article  PubMed  Google Scholar 

  • Oldstone MB, Homann D, Lewicki H, Stevenson D (2002) One, two, or three step: measles virus receptor dance. Virology 299:162–163

    Article  PubMed  Google Scholar 

  • Overbaugh J, Miller AD, Eiden MV (2001) Receptors and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins. Microbiol Mol Biol Rev 65:371–389

    Article  PubMed  Google Scholar 

  • Parker JS, Murphy WJ, Wang D, O'Brien SJ, Parrish CR (2001) Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J Virol 75:3896–3902

    Article  PubMed  Google Scholar 

  • Parker JS, Parrish CR (2000) Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J Virol 74:1919–1930

    Article  PubMed  Google Scholar 

  • Pelkmans L, J. K, Helenius A (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular transport pathway to the ER. Nat Cell Biol 3:473–483

    Article  PubMed  Google Scholar 

  • Pelkmans L, Puntener D, Helenius A (2002) Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296:535–539

    Article  PubMed  Google Scholar 

  • Perez L, Carrasco L (1993) Entry of poliovirus into cells does not require a low-pH step. J Virol 67:4543–4548

    PubMed  Google Scholar 

  • Pho MT, Ashok A, Atwood WJ (2000) JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J Virol 74:2288–2292

    Article  PubMed  Google Scholar 

  • Pinto LH, Holsinger LJ, Lamb RA (1992) Influenza virus M2 protein has ion channel activity. Cell 69:517–528

    Article  PubMed  Google Scholar 

  • Poranen MM, Daugelavicius R, Bamford DH (2002) Common principles in viral entry. Annu Rev Microbiol 56:521–538

    Article  PubMed  Google Scholar 

  • Racaniello VR (1996) Early events in poliovirus infection: virus-receptor interactions. Proc Natl Acad Sci U S A 93:11378–11381

    Article  PubMed  Google Scholar 

  • Rauma T, Tuukkanen J, Bergelson JM, Denning G, Hautala T (1999) rab5 GTPase regulates adenovirus endocytosis. J Virol 73:9664–9668

    PubMed  Google Scholar 

  • Richards AA, Stang E, Pepperkok R, Parton RG (2002) Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol Biol Cell 13:1750–1764

    Article  PubMed  Google Scholar 

  • Richterova Z, Liebl D, Horak M, Palkova Z, Stokrova J, Hozak P, Korb J, Forstova J (2001) Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J Virol 75:10880–10891

    Article  PubMed  Google Scholar 

  • Root CR, Wills EG, McNair LL, Whittaker GR (2000) Entry of influenza viruses into cells is inhibited by a highly specific protein kinase C inhibitor. J Gen Virol 81:2697–2705

    PubMed  Google Scholar 

  • Ross SR, Schofield JJ, Farr CJ, Bucan M (2002) Mouse transferrin receptor 1 is the cell entry receptor for mouse mammary tumor virus. Proc Natl Acad Sci USA 99:12386–12390

    Article  PubMed  Google Scholar 

  • Rotbart HA (2002) Treatment of picornavirus infections. Antiviral Res 53:83–98

    Article  PubMed  Google Scholar 

  • Russell DG, Marsh M (2001), Endocytosis in pathogen entry and replication, in Endocytosis, Ed. Marsh M, 247–280, Oxford University Press, Oxford

    Google Scholar 

  • Schneider-Schaulies J (2000) Cellular receptors for viruses: links to tropism and pathogenesis. J Gen Virol 81:1413–1429

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Sieczkarski SB, Brown HA, Whittaker GR (2003) The role of protein kinase C βII in influenza virus entry via late endosomes. J Virol 77:460–469

    Article  PubMed  Google Scholar 

  • Sieczkarski SB, Whittaker GR (2002) Dissecting virus entry via endocytosis. J Gen Virol 83:1535–1545

    PubMed  Google Scholar 

  • Sieczkarski SB, Whittaker GR (2002) Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 76:10455–10464

    Article  PubMed  Google Scholar 

  • Sieczkarski SB, Whittaker GR (2003) Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4:333–343

    PubMed  Google Scholar 

  • Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569

    Article  PubMed  Google Scholar 

  • Smyth MS, Martin JH (2002) Picornavirus uncoating. Mol Pathol 55:214–219

    Article  PubMed  Google Scholar 

  • Somsel Rodman J, Wandinger-Ness A (2000) Rab GTPases coordinate endocytosis. J Cell Sci 113:183–192

    PubMed  Google Scholar 

  • Spear P (2002) Viral interactions with receptors in cell junctions and effects on junctional stability. Dev Cell 3:462–464

    Article  PubMed  Google Scholar 

  • Spear PG (1993) Entry of alphaherpesviruses into cells. Semin Virol 4:167–180

    Article  Google Scholar 

  • Stuart AD, Eustace HE, McKee TA, Brown TD (2002) A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J Virol 76:9307–9322

    Article  PubMed  Google Scholar 

  • Sturzenbecker LJ, Nibert M, Furlong D, Fields BN (1987) Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J Virol 61:2351–2361

    PubMed  Google Scholar 

  • Suikkanen S, Saajarvi K, Hirsimaki J, Valilehto O, Reunanen H, Vihinen-Ranta M, Vuento M (2002) Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J Virol 76:4401–4411

    Article  PubMed  Google Scholar 

  • Tucker SP, Wimmer E, Compans RW (1994), Expression of viral receptors and the vectorial release of viruses in polarized cells, in Cellular Receptors for Animal Viruses, Ed. Wimmer E, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Walters RW, Freimuth P, Moninger TO, Ganske I, Zabner J, Welsh MJ (2002) Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 110:789–799

    Article  PubMed  Google Scholar 

  • Wimmer E (1994), Cellular Receptors for Animal Viruses, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Yanagi Y, Ono N, Tatsuo H, Hashimoto K, Minagawa H (2002) Measles virus receptor SLAM (CD150). Virology 299:155–161

    Article  PubMed  Google Scholar 

  • Young JAT (2001), Virus Entry and Uncoating, in Fields Virology, Ed. Knipe DM Howley PM, Lippincott Williams and Wilkins, Philadelphia, PA

    Google Scholar 

  • Zadori Z, Szelei J, Lacoste MC, Li Y, Gariepy S, Raymond P, Allaire M, Nabi IR, Tijssen P (2001) A viral phospholipase A2 is required for parvovirus infectivity. Dev Cell 1:291–302

    Article  PubMed  Google Scholar 

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Sieczkarski, S.B., Whittaker, G.R. (2004). Viral Entry. In: Marsh, M. (eds) Membrane Trafficking in Viral Replication. Current Topics in Microbiology and Immunology, vol 285. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-26764-6_1

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