Abstract

Viruses, despite being relatively simple in structure and composition, have evolved a broad spectrum of mechanisms to exploit the host cell. To initiate effective infection, viruses or viral genomes have to enter cells. Recently studies have shown that apart from the direct fusion at the plasma membrane, endocytosis is more often the preferred means of entry into the host cell. Endocytosis is a complex phenomenon, that includes multiple pathways of membrane trafficking, such as clathrin-mediated endocytosis, caveolin-mediated endocytosis, macropinocytosis and phagocytosis. Endosomes offer a convenient and often rapid transit system across the plasma membrane and cytoplasm via the cellular microtubular network. They also provide protection to the virus from detection by the host’s innate immune defences. What is important, viruses are able to utilize not just one, but multiple uptake routes. Identification of these processes and factors will not only allow a better insight into pathogenic mechanism, but may identify novel targets for future therapeutic development. This review provides insight on recent developments in the rapidly evolving field of viral entry.

References

• 1. Amstutz B., Gastaldelli M., Kalin S., Imelli N., Boucke K., WandelerE., Mercer J., Hemmi S., Greber U.F.: Subversion of CtBP1–controlled macropinocytosis by human adenovirus serotype 3.EMBO J., 2008; 27: 956-969
  Google Scholar
• 2. Angulo A., Alcami A., Vinuela E.: Virus-host interactions inAfrican swine fever: the attachment to cellular receptors. Arch.Virol. Suppl., 1993; 7: 169-183
  Google Scholar
• 3. Bhattacharyya S., Warfield K.L., Ruthel G., Bavari S., Aman M.J.,Hope T.J.: Ebola virus uses clathrin-mediated endocytosis as anentry pathway. Virology, 2010; 401: 18-28
  Google Scholar
• 4. Comisso C., Davidson S.M., Soydaner-Azeloglu R.G., Parker S.J., Kamphorst J.J., Hackett S., Grabocka E., Nofal M., Drebin J.A.,Thompson C.B., Rabinowitz J.A., Metallo C.M., Vander Heiden M.G.,Bar-Sagi D.: Macropinocytosis of protein is an amino acid supplyroute in Ras-transformed cells. Nature, 2013; 497: 633-637
  Google Scholar
• 5. Doherty G.J, McMahon H.T.: Mechanisms of endocytosis. Annu.Rev. Biochem., 2009; 78: 857-902
  Google Scholar
• 6. Drebert Z., Golke A., Cymerys J., Słońska A., Chmielewska A.,Tucholska A., Bańbura M.W.: Equid herpesvirus type 1 (EHV-1)disrupts actin cytoskeleton during productive infection in equineleukocytes. Pol. J. Vet. Sci., 2015; 18: 107-112
  Google Scholar
• 7. Empig C.J., Goldsmith M.A.: Association of the caveola vesicularsystem with cellular entry by filoviruses. J. Virol., 2002; 76:5266-5270
  Google Scholar
• 8. Frampton A.R., Jr., Goins W.F., Cohen J.B., von Einem J., OsterriederN., O’Callaghan D.J., Glorioso J.C.: Equine herpesvirus 1 utilizes a novel herpesvirus entry receptor. J. Virol., 2005; 79:3169-3173
  Google Scholar
• 9. Frampton A.R. Jr., Stolz D.B., Uchida H., Goins W.F., Cohen J.B.,Glorioso J.C.: Equine herpesvirus 1 enters cells by two differentpathways, and infection requires the activation of the cellularkinase ROCK1. J. Virol., 2007; 81: 10879-10889
  Google Scholar
• 10. Ghigo E.: A dilemma for viruses and giant viruses: which endocyticpathway to use to enter cells? Intervirology, 2010; 53: 274-283
  Google Scholar
• 11. Ghigo E., Kartenbeck J., Lien P., Pelkmans L., Capo C., MegeJ.L., Raoult D.: Ameobal pathogen mimivirus infects macrophagesthrough phagocytosis. PLoS Pathog., 2008; 4: e1000087
  Google Scholar
• 12. Golke A., Słońska A., Cymerys J.: Pandemiczna grypa A(H1N1).Życie Wet., 2010; 85: 47-49
  Google Scholar
• 13. Gómez-Puertas P., Rodriguez F., Oviedo J.M., Brun A., AlonsoC., Escribano J.M.: The African swine fever virus proteins p54 andp30 are involved in two distinct steps of virus attachment andboth contribute to the antibody-mediated protective immuneresponse. Virology, 1998; 243: 461-471
  Google Scholar
• 14. Hernaez B., Alonso C.: Dynamin – and clathrin-dependentendocytosis in African swine fever virus entry. J. Virol., 2010;84: 2100-2109
  Google Scholar
• 15. Kalia M., Jameel S.: Virus entry paradigms. Amino Acids, 2011;41: 1147-1157
  Google Scholar
• 16. Kataoka C., Kaname Y., Taguwa S., Abe T., Fukuhara T., Tani H.,Moriishi K., Matsuura Y.: Baculovirus GP64-mediated entry intomammalian cells. J. Virol., 2012; 86: 2610-2620
  Google Scholar
• 17. Laakkonen J.P., Mäkelä A.R., Kakkonen E., Turkki P., KukkonenS., Peränen J., Ylä-Herttuala S., Airenne K.J., Oker-Blom C., Vihinen-RantaM., Marjomäki V.: Clathrin-independent entry of baculovirustriggers uptake of E. coli in non – phagocytic human cells.PLoS One, 2009; 4: e5093
  Google Scholar
• 18. Long G., Pan X., Kormelink R., Vlak J.M.: Functional entryof baculovirus into insect and mammalian cells is dependent onclathrin-mediated endocytosis. J. Virol., 2006; 80: 8830-8833
  Google Scholar
• 19. Lopez S., Arias C.: How viruses hijack endocytic machinery.Nature Education, 2010; 3: 16
  Google Scholar
• 20. Meier O., Greber U.F.: Adenovirus endocytosis. J. Gene. Med.,2004; 6 (Suppl. 1): S152-S163
  Google Scholar
• 21. Mundy D.I., Machleidt T., Ying Y.S., Anderson R.G., Bloom G.S.:Dual control of caveolar membrane traffic by microtubules andthe actin cytoskeleton. J. Cell Sci., 2002; 115: 4327-4339
  Google Scholar
• 22. Nichols B.J.: A distinct class of endosome mediates clathrinindependentendocytosis to the Golgi complex. Nat. Cell Biol.,2002; 4; 374-378
  Google Scholar
• 23. Parton R.G., Richards A.A.: Lipid rafts and caveolae as portalsfor endocytosis: new insights and common mechanisms. Traffic,2003; 4: 724-738
  Google Scholar
• 24. Parton R.G., Simons K.: The multiple faces of caveolae. Nat.Rev. Moll. Cell Biol., 2007; 8: 185-194
  Google Scholar
• 25. Pelkmans L., Kartenbeck J., Helenius A.: Caveolar endocytosisof simian virus 40 reveals a new two-step vesicular-transportpathway to the ER. Nat. Cell Biol., 2001; 3: 473-483
  Google Scholar
• 26. Pollard T.D., Earnshaw W.C.: Endocytosis and the endosomalmembrane system. W: Cell Biology, wyd. 2, Saunders/Elsevier,Philadelphia, 2008: 391-408
  Google Scholar
• 27. Rauma T., Tuukkanen J., Bergelson J.M., Denning G., HautalaT.: rab5 GTPase regulates adenovirus endocytosis. J. Virol., 1999;73: 9664-9668
  Google Scholar
• 28. Rossman J.S., Leser G.P., Lamb R.A.: Filamentous influenzavirus enters cells via macropinocytosis. J. Virol., 2012; 86: 10950-10960
  Google Scholar
• 29. Saeed M.F., Kolokoltsov A.A., Albrecht T., Davey R.A.: Cellularentry of Ebola virus involves uptake by a macropinocytosis-likemechanism and subsequent trafficking through early and lateendosomes. PLoS Pathog., 2010; 6: e1001110
  Google Scholar
• 30. Schelhaas M.: Come in and take your coat off – how hostcells provide endocytosis for virus entry. Cell. Microbiol., 2010;12: 1378-1388
  Google Scholar
• 31. Schelhaas M., Malmström J., Pelkmans L., Haugstetter J., EllgaardL., Grünewald K., Helenius A.: Simian virus 40 depends onER protein folding and quality control factors for entry into hostcells. Cell, 2007; 131: 516-529
  Google Scholar
• 32. Simonsen A., Wurmser A.E., Emr S.D., Stenmark H.: The roleof phosphoinositides in membrane transport. Curr. Opin. CellBiol., 2001; 13: 485-492
  Google Scholar
• 33. Sirena D., Lilienfeld B., Eisenhut M., Kälin S., Boucke K., BeerliR.R., Vogt L., Ruedl C., Bachmann M.F., Greber U.F., Hemmi S.: Thehuman membrane cofactor CD46 is a receptor for species B adenovirusserotype 3. J. Virol., 2004; 78: 4454-4462
  Google Scholar
• 34. Słońska A., Cymerys J., Godlewski M.M., Dzieciątkowski T.,Tucholska A., Chmielewska A., Golke A., Bańbura M.W.: Equineherpesvirus type 1 (EHV-1)-induced rearrangements of actin filamentsin productively infected primary murine neurons. Arch.Virol., 2014; 159: 1341-1349
  Google Scholar
• 35. Słońska A., Cymerys J., Skwarska J., Golke A., Bańbura M.W.:Influence of importin α/β and exportin 1 on equine herpesvirustype 1 (EHV-1) replication in primary murine neurons. Pol. J. Vet.Sci., 2013; 16: 749-751
  Google Scholar
• 36. Słońska A., Golke A., Solarska M., Cymerys J., DzieciątkowskiT., Bańbura M.: Wpływ zakażeń wirusowych na cytoszkielet komórkowy. Post. Mikrobiol., 2011; 50: 121-130
  Google Scholar
• 37. Słońska A., Polowy R., Golke A., Cymerys J.: Rola białek motorycznychcytoszkieletu w zakażeniu wirusowym. Postępy Hig.Med. Dośw., 2012; 66: 810-817
  Google Scholar
• 38. Stuart L.M., Ezekowitz R.A.: Phagocytosis: elegant complexity.Immunity, 2005; 22: 539-550
  Google Scholar
• 39. Taylor P.R., Martinez-Pomares L., Stacey M., Lin H.H., BrownG.D., Gordon S.: Macrophage receptors and immune recognition.Annu. Rev. Immunol., 2005; 23: 901-944
  Google Scholar
• 40. Van de Walle G.R., Peters S.T., VanderVen B.C., O’CallaghanD.J., Osterrieder N.: Equine herpesvirus 1 entry via endocytosisis facilitated by αV integrins and an RSD motif in glycoprotein D.J. Virol., 2008; 82: 11859-11868
  Google Scholar
• 41. Wickham T.J., Mathias P., Cheresh D.A., Nemerow G.R.: Integrinsαvβ3 and αvβ5 promote adenovirus internalization but notvirus attachment. Cell, 1993; 73: 309-319
  Google Scholar

Full text