Skip to main content

Inside the Cell: Assembly of Filoviruses

  • Chapter
  • First Online:
Marburg- and Ebolaviruses

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 411))

Abstract

This chapter reviews our current knowledge about the spatiotemporal assembly of filoviral particles. We will follow particles from nucleocapsid entry into the cytoplasm until the nucleocapsids are enveloped at the plasma membrane. We will also highlight the currently open scientific questions surrounding filovirus assembly.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

References

  • Adu-Gyamfi E, Digman MA, Gratton E, Stahelin RV (2012) Single-particle tracking demonstrates that actin coordinates the movement of the Ebola virus matrix protein. Biophys J 103(9):L41–43. doi:10.1016/j.bpj.2012.09.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aman MJ, Bosio CM, Panchal RG, Burnett JC, Schmaljohn A, Bavari S (2003) Molecular mechanisms of filovirus cellular trafficking. Microbes Infect 5(7):639–649

    Article  CAS  PubMed  Google Scholar 

  • Ascenzi P, Bocedi A, Heptonstall J, Capobianchi MR, Di Caro A, Mastrangelo E, Bolognesi M, Ippolito G (2008) Ebolavirus and Marburgvirus: insight the Filoviridae family. Mol Aspects Med 29(3):151–185. doi:10.1016/j.mam.2007.09.005

    Article  CAS  PubMed  Google Scholar 

  • Bakker SE, Duquerroy S, Galloux M, Loney C, Conner E, ElĂ©ouĂ«t JF, Rey FA, Bhella D (2013) The respiratory syncytial virus nucleoprotein-RNA complex forms a left-handed helical nucleocapsid. J Gen Virol 94(Pt 8):1734–1738. doi:10.1099/vir.0.053025-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bamberg S, Kolesnikova L, Moller P, Klenk HD, Becker S (2005) VP24 of Marburg virus influences formation of infectious particles. J Virol 79(21):13421–13433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basler CF, Mikulasova A, Martinez-Sobrido L, Paragas J, MĂĽhlberger E, Bray M, Klenk HD, Palese P, GarcĂ­a-Sastre A (2003) The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J Virol 77(14):7945–7956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bavari S, Bosio CM, Wiegand E, Ruthel G, Will AB, Geisbert TW, Hevey M, Schmaljohn C, Schmaljohn A, Aman MJ (2002) Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J Exp Med 195(5):593–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker S, Rinne C, Hofsass U, Klenk HD, MĂĽhlberger E (1998) Interactions of Marburg virus nucleocapsid proteins. Virology 249(2):406–417

    Article  CAS  PubMed  Google Scholar 

  • Beer B, Kurth R, Bukreyev A (1999) Characteristics of Filoviridae: Marburg and Ebola viruses. Naturwissenschaften 86(1):8–17

    Article  CAS  PubMed  Google Scholar 

  • Beniac DR, Melito PL, Devarennes SL, Hiebert SL, Rabb MJ, Lamboo LL, Jones SM, Booth TF (2012) The organisation of Ebola virus reveals a capacity for extensive, modular polyploidy. PLoS ONE 7(1):e29608. doi:10.1371/journal.pone.0029608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bharat TA, Riches JD, Kolesnikova L, Welsch S, Krähling V, Davey N, Parsy ML, Becker S, Briggs JA (2011) Cryo-electron tomography of Marburg virus particles and their morphogenesis within infected cells. PLoS Biol 9(11):e1001196. doi:10.1371/journal.pbio.1001196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bharat TA, Noda T, Riches JD, Kraehling V, Kolesnikova L, Becker S, Kawaoka Y, Briggs JA (2012) Structural dissection of Ebola virus and its assembly determinants using cryo-electron tomography. Proc Natl Acad Sci USA 109(11):4275–4280. doi:10.1073/pnas.1120453109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biedenkopf N, Hartlieb B, Hoenen T, Becker S (2013) Phosphorylation of Ebola virus VP30 influences the composition of the viral nucleocapsid complex: impact on viral transcription and replication. J Biol Chem 288(16):11165–11174. doi:10.1074/jbc.M113.461285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biedenkopf N, Lier C, Becker S (2016) Dynamic phosphorylation of VP30 Is essential for Ebola Virus life cycle. J Virol 90(10):4914–4925. doi:10.1128/jvi.03257-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bieniasz PD (2006) Late budding domains and host proteins in enveloped virus release. Virology 344(1):55–63

    Article  CAS  PubMed  Google Scholar 

  • Bjorndal AS, Szekely L, Elgh F (2003) Ebola virus infection inversely correlates with the overall expression levels of promyelocytic leukaemia (PML) protein in cultured cells. BMC Microbiol 3(1):6

    Article  PubMed  PubMed Central  Google Scholar 

  • Boehmann Y, Enterlein S, Randolf A, MĂĽhlberger E (2005) A reconstituted replication and transcription system for Ebola virus Reston and comparison with Ebola virus Zaire. Virology 332(1):406–417. doi:10.1016/j.virol.2004.11.018

    Article  CAS  PubMed  Google Scholar 

  • Booth TF, Rabb MJ, Beniac DR (2013) How do filovirus filaments bend without breaking? Trends Microbiol 21(11):583–593. doi:10.1016/j.tim.2013.08.001

    Article  CAS  PubMed  Google Scholar 

  • Bornholdt ZA, Noda T, Abelson DM, Halfmann P, Wood MR, Kawaoka Y, Saphire EO (2013) Structural rearrangement of Ebola Virus VP40 begets multiple functions in the virus life cycle. Cell 154(4):763–774. doi:10.1016/j.cell.2013.07.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calistri A, Salata C, Parolin C, PalĂą G (2009) Role of multivesicular bodies and their components in the egress of enveloped RNA viruses. Rev Med Virol 19(1):31–45. doi:10.1002/rmv.588

    Article  CAS  PubMed  Google Scholar 

  • Desfosses A, Goret G, Farias Estrozi L, Ruigrok RW, Gutsche I (2011) Nucleoprotein-RNA orientation in the measles virus nucleocapsid by three-dimensional electron microscopy. J Virol 85(3):1391–1395. doi:10.1128/jvi.01459-10

    Article  CAS  PubMed  Google Scholar 

  • DiCarlo A, Möller P, Lander A, Kolesnikova L, Becker S (2007) Nucleocapsid formation and RNA synthesis of Marburg virus is dependent on two coiled coil motifs in the nucleoprotein. Virol J 4:105. doi:10.1186/1743-422x-4-105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dolnik O, Kolesnikova L, Becker S (2008) Filoviruses: interactions with the host cell. Cell Mol Life Sci 65(5):756–776. doi:10.1007/s00018-007-7406-2

    Article  CAS  PubMed  Google Scholar 

  • Dolnik O, Kolesnikova L, Stevermann L, Becker S (2010) Tsg101 is recruited by a late domain of the nucleocapsid protein to support budding of Marburg virus-like particles. J Virol 84(15):7847–7856. doi:10.1128/jvi.00476-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dolnik O, Kolesnikova L, Welsch S, Strecker T, Schudt G, Becker S (2014) Interaction with tsg101 is necessary for the efficient transport and release of nucleocapsids in marburg virus-infected cells. PLoS Pathog 10(10):e1004463. doi:10.1371/journal.ppat.1004463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Du X, Yang H (2013) Endosomal cholesterol trafficking: protein factors at a glance. Acta Biochim Biophys Sin (Shanghai) 45(1):11–17. doi:10.1093/abbs/gms095

    Article  CAS  Google Scholar 

  • Egelman EH, Wu SS, Amrein M, Portner A, Murti G (1989) The Sendai virus nucleocapsid exists in at least four different helical states. J Virol 63(5):2233–2243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elliott LH, Kiley MP, McCormick JB (1985) Descriptive analysis of Ebola virus proteins. Virology 147(1):169–176

    Article  CAS  PubMed  Google Scholar 

  • Ellis DS, Stamford S, Lloyd G, Bowen ET, Platt GS, Way H, Simpson DI (1979) Ebola and Marburg viruses: I. Some ultrastructural differences between strains when grown in Vero cells. J Med Virol 4(3):201–211

    Article  CAS  PubMed  Google Scholar 

  • Enterlein S, Volchkov V, Weik M, Kolesnikova L, Volchkova V, Klenk HD, MĂĽhlberger E (2006) Rescue of recombinant Marburg virus from cDNA is dependent on nucleocapsid protein VP30. J Virol 80(2):1038–1043. doi:10.1128/jvi.80.2.1038-1043.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feldmann H, Kiley MP (1999) Classification, structure, and replication of filoviruses. Curr Top Microbiol Immunol 235:1–21

    CAS  PubMed  Google Scholar 

  • Feldmann H, Bugany H, Mahner F, Klenk HD, Drenckhahn D, Schnittler HJ (1996) Filovirus-induced endothelial leakage triggered by infected monocytes/macrophages. J Virol 70(4):2208–2214

    CAS  PubMed  PubMed Central  Google Scholar 

  • GarcĂ­a M, Cooper A, Shi W, Bornmann W, Carrion R, Kalman D, Nabel GJ (2012) Productive replication of Ebola virus is regulated by the c-Abl1 tyrosine kinase. Sci Transl Med 4(123):123ra124. doi:10.1126/scitranslmed.3003500

  • Ge P, Tsao J, Schein S, Green TJ, Luo M, Zhou ZH (2010) Cryo-EM model of the bullet-shaped vesicular stomatitis virus. Science 327(5966):689–693. doi:10.1126/science.1181766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geisbert TW, Jahrling PB (1995) Differentiation of filoviruses by electron microscopy. Virus Res 39(2–3):129–150

    Article  CAS  PubMed  Google Scholar 

  • Gomis-Ruth FX, Dessen A, Timmins J, Bracher A, Kolesnikowa L, Becker S, Klenk HD, Weissenhorn W (2003) The matrix protein VP40 from Ebola virus octamerizes into pore-like structures with specific RNA binding properties. Structure (Camb) 11(4):423–433

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Groseth A, Feldmann H, Theriault S, Mehmetoglu G, Flick R (2005) RNA polymerase I-driven minigenome system for Ebola viruses. J Virol 79(7):4425–4433. doi:10.1128/jvi.79.7.4425-4433.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groseth A, Charton JE, Sauerborn M, Feldmann F, Jones SM, Hoenen T, Feldmann H (2009) The Ebola virus ribonucleoprotein complex: a novel VP30-L interaction identified. Virus Res 140(1–2):8–14. doi:10.1016/j.virusres.2008.10.017

    Article  CAS  PubMed  Google Scholar 

  • Gurel PS, Hatch AL, Higgs HN (2014) Connecting the Cytoskeleton to the Endoplasmic Reticulum and Golgi. Curr Biol 24(14):R660–R672. doi:10.1016/j.cub.2014.05.033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Z, Harty RN (2005) Packaging of actin into Ebola virus VLPs. Virol J 2(1):92

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han Z, Boshra H, Sunyer JO, Zwiers SH, Paragas J, Harty RN (2003) Biochemical and functional characterization of the Ebola virus VP24 protein: implications for a role in virus assembly and budding. J Virol 77(3):1793–1800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison MS, Sakaguchi T, Schmitt AP (2010) Paramyxovirus assembly and budding: building particles that transmit infections. Int J Biochem Cell Biol 42(9):1416–1429. doi:10.1016/j.biocel.2010.04.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartlieb B, Weissenhorn W (2006) Filovirus assembly and budding. Virology 344(1):64–70. doi:10.1016/j.virol.2005.09.018

    Article  CAS  PubMed  Google Scholar 

  • Hartlieb B, Modrof J, MĂĽhlberger E, Klenk H-D, Becker S (2003) Oligomerization of Ebola virus VP30 is essential for viral transcription and can be inhibited by a synthetic peptide. J Biol Chem 278(43):41830–41836

    Article  CAS  PubMed  Google Scholar 

  • Hartlieb B, Muziol T, Weissenhorn W, Becker S (2007) Crystal structure of the C-terminal domain of Ebola virus VP30 reveals a role in transcription and nucleocapsid association. Proc Natl Acad Sci USA 104(2):624–629. doi:10.1073/pnas.0606730104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harty RN, Brown ME, Wang G, Huibregtse J, Hayes FP (2000) A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc Natl Acad Sci USA 97(25):13871–13876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haywood AM (2010) Membrane uncoating of intact enveloped viruses. J Virol 84(21):10946–10955. doi:10.1128/jvi.00229-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henne WM, Buchkovich NJ, Emr SD (2011) The ESCRT pathway. Dev Cell 21(1):77–91. doi:10.1016/j.devcel.2011.05.015

    Article  CAS  PubMed  Google Scholar 

  • Hermesh O, Jansen RP (2013) Take the (RN) A-train: localization of mRNA to the endoplasmic reticulum. Biochim Biophys Acta 1833(11):2519–2525. doi:10.1016/j.bbamcr.2013.01.013

  • Hoenen T, Volchkov V, Kolesnikova L, Mittler E, Timmins J, Ottmann M, Reynard O, Becker S, Weissenhorn W (2005) VP40 Octamers are essential for ebola virus replication. J Virol 79(3):1898–1905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoenen T, Groseth A, Kolesnikova L, Theriault S, Ebihara H, Hartlieb B, Bamberg S, Feldmann H, Ströher U, Becker S (2006) Infection of naive target cells with virus-like particles: implications for the function of ebola virus VP24. J Virol 80(14):7260–7264. doi:10.1128/jvi.00051-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoenen T, Biedenkopf N, Zielecki F, Jung S, Groseth A, Feldmann H, Becker S (2010a) Oligomerization of Ebola virus VP40 is essential for particle morphogenesis and regulation of viral transcription. J Virol 84(14):7053–7063. doi:10.1128/jvi.00737-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoenen T, Jung S, Herwig A, Groseth A, Becker S (2010b) Both matrix proteins of Ebola virus contribute to the regulation of viral genome replication and transcription. Virology 403(1):56–66. doi:10.1016/j.virol.2010.04.002

    Article  CAS  PubMed  Google Scholar 

  • Hoenen T, Groseth A, de Kok-Mercado F, Kuhn JH, Wahl-Jensen V (2011) Minigenomes, transcription and replication competent virus-like particles and beyond: reverse genetics systems for filoviruses and other negative stranded hemorrhagic fever viruses. Antiviral Res 91(2):195–208. doi:10.1016/j.antiviral.2011.06.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoenen T, Shabman RS, Groseth A, Herwig A, Weber M, Schudt G, Dolnik O, Basler CF, Becker S, Feldmann H (2012) Inclusion bodies are a site of ebolavirus replication. J Virol 86(21):11779–11788. doi:10.1128/jvi.01525-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Xu L, Sun Y, Nabel GJ (2002) The assembly of Ebola virus nucleocapsid requires virion-associated proteins 35 and 24 and posttranslational modification of nucleoprotein. Mol Cell 10(2):307–316

    Article  PubMed  Google Scholar 

  • Iwasa A, Halfmann P, Noda T, Oyama M, Kozuka-Hata H, Watanabe S, Shimojima M, Watanabe T, Kawaoka Y (2011) Contribution of Sec61α to the life cycle of Ebola virus. J Infect Dis 204(Suppl 3):S919–926. doi:10.1093/infdis/jir324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jasenosky LD, Kawaoka Y (2004) Filovirus budding. Virus Res 106(2):181–188

    Article  CAS  PubMed  Google Scholar 

  • Jasenosky LD, Neumann G, Lukashevich I, Kawaoka Y (2001) Ebola virus VP40-induced particle formation and association with the lipid bilayer. J Virol 75(11):5205–5214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiley MP, Cox NJ, Elliott LH, Sanchez A, DeFries R, Buchmeier MJ, Richman DD, McCormick JB (1988) Physicochemical properties of Marburg virus: evidence for three distinct virus strains and their relationship to Ebola virus. J Gen Virol 69(Pt 8):1957–1967

    Article  PubMed  Google Scholar 

  • King G, Sharom FJ (2012) Proteins that bind and move lipids: MsbA and NPC1. Crit Rev Biochem Mol Biol 47(1):75–95. doi:10.3109/10409238.2011.636505

    Article  CAS  PubMed  Google Scholar 

  • Koehler A, Kolesnikova L, Welzel U, Schudt G, Herwig A, Becker S (2015) A single amino acid change in the Marburg virus matrix protein VP40 provides a replicative advantage in a species-specific manner. J Virol. doi:10.1128/jvi.02670-15

    PubMed  Google Scholar 

  • Kolesnikova L, Muhlberger E, Ryabchikova E, Becker S (2000) Ultrastructural organization of recombinant Marburg virus nucleoprotein: comparison with Marburg virus inclusions. J Virol 74(8):3899–3904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolesnikova L, Bugany H, Klenk HD, Becker S (2002) VP40, the matrix protein of Marburg virus, is associated with membranes of the late endosomal compartment. J Virol 76(4):1825–1838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolesnikova L, Bamberg S, Berghofer B, Becker S (2004a) The matrix protein of Marburg virus is transported to the plasma membrane along cellular membranes: exploiting the retrograde late endosomal pathway. J Virol 78(5):2382–2393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolesnikova L, Berghofer B, Bamberg S, Becker S (2004b) Multivesicular bodies as a platform for formation of the Marburg virus envelope. J Virol 78(22):12277–12287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolesnikova L, Bohil AB, Cheney RE, Becker S (2007a) Budding of Marburgvirus is associated with filopodia. Cell Microbiol 9(4):939–951

    Article  CAS  PubMed  Google Scholar 

  • Kolesnikova L, Ryabchikova E, Shestopalov A, Becker S (2007b) Basolateral budding of Marburg virus: VP40 retargets viral glycoprotein GP to the basolateral surface. J Infect Dis 196(Suppl 2):S232–236. doi:10.1086/520584

    Article  PubMed  Google Scholar 

  • Kolesnikova L, Strecker T, Morita E, Zielecki F, Mittler E, Crump C, Becker S (2009) Vacuolar protein sorting pathway contributes to the release of Marburg virus. J Virol 83(5):2327–2337. doi:10.1128/jvi.02184-08

    Article  CAS  PubMed  Google Scholar 

  • Kolesnikova L, Mittler E, Schudt G, Shams-Eldin H, Becker S (2012) Phosphorylation of Marburg virus matrix protein VP40 triggers assembly of nucleocapsids with the viral envelope at the plasma membrane. Cell Microbiol 14(2):182–197. doi:10.1111/j.1462-5822.2011.01709.x

    Article  CAS  PubMed  Google Scholar 

  • Licata JM, Simpson-Holley M, Wright NT, Han Z, Paragas J, Harty RN (2003) Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. J Virol 77(3):1812–1819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Licata JM, Johnson RF, Han Z, Harty RN (2004) Contribution of ebola virus glycoprotein, nucleoprotein, and VP24 to budding of VP40 virus-like particles. J Virol 78(14):7344–7351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu J, Qu Y, Liu Y, Jambusaria R, Han Z, Ruthel G, Freedman BD, Harty RN (2013) Host IQGAP1 and Ebola virus VP40 interactions facilitate virus-like particle egress. J Virol 87(13):7777–7780. doi:10.1128/jvi.00470-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez MJ, Volchkova VA, Raoul H, Alazard-Dany N, Reynard O, Volchkov VE (2011) Role of VP30 phosphorylation in the Ebola virus replication cycle. J Infect Dis 204(Suppl 3):S934–940. doi:10.1093/infdis/jir320

    Article  CAS  PubMed  Google Scholar 

  • MartĂ­nez MJ, Biedenkopf N, Volchkova V, Hartlieb B, Alazard-Dany N, Reynard O, Becker S, Volchkov V (2008) Role of Ebola virus VP30 in transcription reinitiation. J Virol 82(24):12569–12573. doi:10.1128/jvi.01395-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martin-Serrano J, Zang T, Bieniasz PD (2001) HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat Med 7(12):1313–1319

    Article  CAS  PubMed  Google Scholar 

  • Mateo M, Reid SP, Leung LW, Basler CF, Volchkov VE (2010) Ebolavirus VP24 binding to karyopherins is required for inhibition of interferon signaling. J Virol 84(2):1169–1175. doi:10.1128/jvi.01372-09

    Article  CAS  PubMed  Google Scholar 

  • Mateo M, Carbonnelle C, Martinez MJ, Reynard O, Page A, Volchkova VA, Volchkov VE (2011) Knockdown of Ebola virus VP24 impairs viral nucleocapsid assembly and prevents virus replication. J Infect Dis 204(Suppl 3):S892–896. doi:10.1093/infdis/jir311

    Article  CAS  PubMed  Google Scholar 

  • Mavrakis M, Kolesnikova L, Schoehn G, Becker S, Ruigrok RW (2002) Morphology of Marburg virus NP-RNA. Virology 296(2):300–307

    Article  CAS  PubMed  Google Scholar 

  • Miller EH, Chandran K (2012) Filovirus entry into cells - new insights. Curr Opin Virol 2(2):206–214. doi:10.1016/j.coviro.2012.02.015

    Article  CAS  PubMed  Google Scholar 

  • Mittler E, Kolesnikova L, Strecker T, Garten W, Becker S (2007) Role of the transmembrane domain of marburg virus surface protein GP in assembly of the viral envelope. J Virol 81(8):3942–3948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler E, Kolesnikova L, Herwig A, Dolnik O, Becker S (2013) Assembly of the Marburg virus envelope. Cell Microbiol 15(2):270–284. doi:10.1111/cmi.12076

    Article  CAS  PubMed  Google Scholar 

  • Modrof J, Möritz C, Kolesnikova L, Konakova T, Hartlieb B, Randolf A, MĂĽhlberger E, Becker S (2001) Phosphorylation of Marburg virus VP30 at serines 40 and 42 is critical for its interaction with NP inclusions. Virology 287(1):171–182. doi:10.1006/viro.2001.1027

  • Modrof J, Muhlberger E, Klenk HD, Becker S (2002) Phosphorylation of VP30 impairs ebola virus transcription. J Biol Chem 277(36):33099–33104

    Article  CAS  PubMed  Google Scholar 

  • Modrof J, Becker S, Muehlberger E (2003) Ebola virus transcription activator VP30 is a zinc-binding protein. J Virol 77(5):3334–3338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moller P, Pariente N, Klenk HD, Becker S (2005) Homo-oligomerization of Marburgvirus VP35 is essential for its function in replication and transcription. J Virol 79(23):14876–14886. doi:10.1128/JVI.79.23.14876-14886.2005

  • MĂĽhlberger E (2007) Filovirus replication and transcription. Future Virol 2(2):205–215. doi:10.2217/17460794.2.2.205

    Article  PubMed  PubMed Central  Google Scholar 

  • MĂĽhlberger E, Trommer S, Funke C, Volchkov V, Klenk HD, Becker S (1996) Termini of all mRNA species of Marburg virus: sequence and secondary structure. Virology 223(2):376–380

    Article  PubMed  Google Scholar 

  • MĂĽhlberger E, Lotfering B, Klenk HD, Becker S (1998) Three of the four nucleocapsid proteins of Marburg virus, NP, VP35, and L, are sufficient to mediate replication and transcription of Marburg virus-specific monocistronic minigenomes. J Virol 72(11):8756–8764

    PubMed  PubMed Central  Google Scholar 

  • MĂĽhlberger E, Weik M, Volchkov VE, Klenk HD, Becker S (1999) Comparison of the transcription and replication strategies of marburg virus and Ebola virus by using artificial replication systems. J Virol 73(3):2333–2342

    PubMed  PubMed Central  Google Scholar 

  • Murphy FA, van der Groen G, Whiteflied SG, Lange JV (1978) Ebola and Marburg virus morphology and taxonomy. In: S. P (ed) Ebola virus haemorrhagic fever. Elsevier/North Holland, Amsterdam, pp 61–84

    Google Scholar 

  • Nanbo A, Watanabe S, Halfmann P, Kawaoka Y (2013) The spatio-temporal distribution dynamics of Ebola virus proteins and RNA in infected cells. Sci Rep 3:1206. doi:10.1038/srep01206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neumann G, Ebihara H, Takada A, Noda T, Kobasa D, Jasenosky LD, Watanabe S, Kim JH, Feldmann H, Kawaoka Y (2005) Ebola virus VP40 late domains are not essential for viral replication in cell culture. J Virol 79(16):10300–10307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noda T, Sagara H, Suzuki E, Takada A, Kida H, Kawaoka Y (2002) Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol 76(10):4855–4865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noda T, Aoyama K, Sagara H, Kida H, Kawaoka Y (2005) Nucleocapsid-like structures of Ebola virus reconstructed using electron tomography. J Vet Med Sci 67(3):325–328

    Article  PubMed  Google Scholar 

  • Noda T, Ebihara H, Muramoto Y, Fujii K, Takada A, Sagara H, Kim JH, Kida H, Feldmann H, Kawaoka Y (2006) Assembly and budding of Ebolavirus. PLoS Pathog 2(9):e99. doi:10.1371/journal.ppat.0020099

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Noda T, Halfmann P, Sagara H, Kawaoka Y (2007a) Regions in Ebola virus VP24 that are important for nucleocapsid formation. J Infect Dis 196(Suppl 2):S247–250. doi:10.1086/520596

    Article  CAS  PubMed  Google Scholar 

  • Noda T, Watanabe S, Sagara H, Kawaoka Y (2007b) Mapping of the VP40-binding regions of the nucleoprotein of Ebola virus. J Virol 81(7):3554–3562. doi:10.1128/jvi.02183-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noda T, Hagiwara K, Sagara H, Kawaoka Y (2010) Characterization of the Ebola virus nucleoprotein-RNA complex. J Gen Virol 91(Pt 6):1478–1483. doi:10.1099/vir.0.019794-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noda T, Kolesnikova L, Becker S, Kawaoka Y (2011) The importance of the NP: VP35 ratio in Ebola virus nucleocapsid formation. J Infect Dis 204(Suppl 3):S878–883. doi:10.1093/infdis/jir310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okumura A, Pitha PM, Harty RN (2008) ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc Natl Acad Sci USA 105(10):3974–3979. doi:10.1073/pnas.0710629105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olejnik J, Ryabchikova E, Corley RB, MĂĽhlberger E (2011) Intracellular events and cell fate in filovirus infection. Viruses 3(8):1501–1531. doi:10.3390/v3081501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panchal RG, Ruthel G, Kenny TA, Kallstrom GH, Lane D, Badie SS, Li L, Bavari S, Aman MJ (2003) In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding. Proc Natl Acad Sci USA 100(26):15936–15941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters D, MĂĽller G, Slenczka WG (1971) Morphology, development, and classification of the Marburg virus. Marburg virus disease. Springer, Berlin

    Google Scholar 

  • Puhka M, Vihinen H, Joensuu M, Jokitalo E (2007) Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. J Cell Biol 179(5):895–909. doi:10.1083/jcb.200705112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puhka M, Joensuu M, Vihinen H, Belevich I, Jokitalo E (2012) Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells. Mol Biol Cell 23(13):2424–2432. doi:10.1091/mbc.E10-12-0950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid DW, Nicchitta CV (2012) Primary role for endoplasmic reticulum-bound ribosomes in cellular translation identified by ribosome profiling. J Biol Chem 287(8):5518–5527. doi:10.1074/jbc.M111.312280

    Article  CAS  PubMed  Google Scholar 

  • Reid SP, Cárdenas WB, Basler CF (2005) Homo-oligomerization facilitates the interferon-antagonist activity of the ebolavirus VP35 protein. Virology 341(2):179–189. doi:10.1016/j.virol.2005.06.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid SP, Leung LW, Hartman AL, Martinez O, Shaw ML, Carbonnelle C, Volchkov VE, Nichol ST, Basler CF (2006) Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J Virol 80(11):5156–5167. doi:10.1128/jvi.02349-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruthel G, Demmin GL, Kallstrom G, Javid MP, Badie SS, Will AB, Nelle T, Schokman R, Nguyen TL, Carra JH, Bavari S, Aman MJ (2005) Association of ebola virus matrix protein VP40 with microtubules. J Virol 79(8):4709–4719. doi:10.1128/jvi.79.8.4709-4719.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez A, Kiley MP (1987) Identification and analysis of Ebola virus messenger RNA. Virology 157(2):414–420

    Article  CAS  PubMed  Google Scholar 

  • Sanchez A, Khan AS, Zaki SR, Nabel GJ, Ksiazek TG, Peters CJ (2001) Filoviridae: Marburg and Ebola viruses. In: Knipe DM, Howley PM (eds) Fields virology (4th edn). Lippincott, Williams & Wilkins, Philadelphia

    Google Scholar 

  • Sanger C, Muhlberger E, Ryabchikova E, Kolesnikova L, Klenk HD, Becker S (2001) Sorting of Marburg virus surface protein and virus release take place at opposite surfaces of infected polarized epithelial cells. J Virol 75(3):1274–1283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sattentau Q (2008) Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6(11):815–826. doi:10.1038/nrmicro1972

    Article  CAS  PubMed  Google Scholar 

  • Schibli DJ, Weissenhorn W (2004) Class I and class II viral fusion protein structures reveal similar principles in membrane fusion. Mol Membr Biol 21(6):361–371. doi:10.1080/09687860400017784

    Article  CAS  PubMed  Google Scholar 

  • Schoehn G, Mavrakis M, Albertini A, Wade R, Hoenger A, Ruigrok RW (2004) The 12 A structure of trypsin-treated measles virus N-RNA. J Mol Biol 339(2):301–312. doi:10.1016/j.jmb.2004.03.073

    Article  CAS  PubMed  Google Scholar 

  • Schudt G, Kolesnikova L, Dolnik O, Sodeik B, Becker S (2013) Live-cell imaging of Marburg virus-infected cells uncovers actin-dependent transport of nucleocapsids over long distances. Proc Natl Acad Sci USA 110(35):14402–14407. doi:10.1073/pnas.1307681110

  • Schudt G, Dolnik O, Kolesnikova L, Biedenkopf N, Herwig A, Becker S (2015) Transport of Ebolavirus nucleocapsids is dependent on actin polymerization: live-cell imaging analysis of Ebolavirus-infected cells. J Infect Dis 212(Suppl 2):S160–166. doi:10.1093/infdis/jiv083

    Article  PubMed  Google Scholar 

  • Scianimanico S, Schoehn G, Timmins J, Ruigrok RH, Klenk HD, Weissenhorn W (2000) Membrane association induces a conformational change in the Ebola virus matrix protein. EMBO J 19(24):6732–6741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shabman RS, Hoenen T, Groseth A, Jabado O, Binning JM, Amarasinghe GK, Feldmann H, Basler CF (2013) An upstream open reading frame modulates ebola virus polymerase translation and virus replication. PLoS Pathog 9(1):e1003147. doi:10.1371/journal.ppat.1003147

  • Shabman RS, Jabado OJ, Mire CE, Stockwell TB, Edwards M, Mahajan M, Geisbert TW, Basler CF (2014) Deep sequencing identifies noncanonical editing of Ebola and Marburg Virus RNAs in infected cells. MBio 5(6). doi:10.1128/mBio.02011-14

  • Shao S, Hegde RS (2011) Membrane protein insertion at the endoplasmic reticulum. Annu Rev Cell Dev Biol 27:25–56. doi:10.1146/annurev-cellbio-092910-154125

  • Sharpe HJ, Stevens TJ, Munro S (2010) A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142(1):158–169. doi:10.1016/j.cell.2010.05.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shibata Y, Voeltz GK, Rapoport TA (2006) Rough sheets and smooth tubules. Cell 126(3):435–439. doi:10.1016/j.cell.2006.07.019

    Article  CAS  PubMed  Google Scholar 

  • Spiegelberg L, Wahl-Jensen V, Kolesnikova L, Feldmann H, Becker S, Hoenen T (2011) Genus-specific recruitment of filovirus ribonucleoprotein complexes into budding particles. J Gen Virol 92(Pt 12):2900–2905. doi:10.1099/vir.0.036863-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stahelin RV (2014) Membrane binding and bending in Ebola VP40 assembly and egress. Front Microbiol 5:300. doi:10.3389/fmicb.2014.00300

    PubMed  PubMed Central  Google Scholar 

  • Starostin EL (2006) On the perfect hexagonal packing of rods. J Phys: Condens Matter 18(14):S187–S204

    CAS  Google Scholar 

  • Swenson DL, Warfield KL, Kuehl K, Larsen T, Hevey MC, Schmaljohn A, Bavari S, Aman MJ (2004) Generation of Marburg virus-like particles by co-expression of glycoprotein and matrix protein. FEMS Immunol Med Microbiol 40(1):27–31

    Article  CAS  PubMed  Google Scholar 

  • Swenson DL, Warfield KL, Negley DL, Schmaljohn A, Aman MJ, Bavari S (2005) Virus-like particles exhibit potential as a pan-filovirus vaccine for both Ebola and Marburg viral infections. Vaccine 23(23):3033–3042. doi:10.1016/j.vaccine.2004.11.070

    Article  CAS  PubMed  Google Scholar 

  • Timmins J, Scianimanico S, Schoehn G, Weissenhorn W (2001) Vesicular release of ebola virus matrix protein VP40. Virology 283(1):1–6

    Article  CAS  PubMed  Google Scholar 

  • Timmins J, Schoehn G, Ricard-Blum S, Scianimanico S, Vernet T, Ruigrok RW, Weissenhorn W (2003) Ebola virus matrix protein VP40 interaction with human cellular factors Tsg101 and Nedd4. J Mol Biol 326(2):493–502

    Article  CAS  PubMed  Google Scholar 

  • Trunschke M, Conrad D, Enterlein S, Olejnik J, Brauburger K, MĂĽhlberger E (2013) The L-VP35 and L-L interaction domains reside in the amino terminus of the Ebola virus L protein and are potential targets for antivirals. Virology 441(2):135–145. doi:10.1016/j.virol.2013.03.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urata S, Yasuda J (2010) Regulation of Marburg virus (MARV) budding by Nedd4.1: a different WW domain of Nedd4.1 is critical for binding to MARV and Ebola virus VP40. J Gen Virol 91(Pt 1):228–234. doi:10.1099/vir.0.015495-0

  • Urata S, Noda T, Kawaoka Y, Morikawa S, Yokosawa H, Yasuda J (2007) Interaction of Tsg101 with Marburg Virus VP40 depends on the PPPY Motif, but not the PT/SAP motif as in the case of Ebola Virus, and Tsg101 plays a critical role in the budding of Marburg virus-like particles induced by VP40, NP, and GP. J Virol 81(9):4895–4899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warfield KL, Bosio CM, Welcher BC, Deal EM, Mohamadzadeh M, Schmaljohn A, Aman MJ, Bavari S (2003) Ebola virus-like particles protect from lethal Ebola virus infection. Proc Natl Acad Sci USA 100(26):15889–15894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warfield KL, Swenson DL, Negley DL, Schmaljohn AL, Aman MJ, Bavari S (2004) Marburg virus-like particles protect guinea pigs from lethal Marburg virus infection. Vaccine 22(25–26):3495–3502. doi:10.1016/j.vaccine.2004.01.063

    Article  CAS  PubMed  Google Scholar 

  • Warfield KL, Swenson DL, Demmin G, Bavari S (2005) Filovirus-like particles as vaccines and discovery tools. Expert Rev Vaccines 4(3):429–440. doi:10.1586/14760584.4.3.429

    Article  CAS  PubMed  Google Scholar 

  • Watanabe S, Watanabe T, Noda T, Takada A, Feldmann H, Jasenosky LD, Kawaoka Y (2004) Production of novel Ebola virus-like particles from cDNAs: an alternative to Ebola Virus generation by reverse genetics. J Virol 78(2):999–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe S, Noda T, Kawaoka Y (2006) Functional mapping of the nucleoprotein of Ebola virus. J Virol 80(8):3743–3751. doi:10.1128/jvi.80.8.3743-3751.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe S, Noda T, Halfmann P, Jasenosky L, Kawaoka Y (2007) Ebola virus (EBOV) VP24 inhibits transcription and replication of the EBOV genome. J Infect Dis 196(Suppl 2):S284–290. doi:10.1086/520582

    Article  CAS  PubMed  Google Scholar 

  • Watt A, Moukambi F, Banadyga L, Groseth A, Callison J, Herwig A, Ebihara H, Feldmann H, Hoenen T (2014) A novel life cycle modeling system for Ebola virus shows a genome length-dependent role of VP24 in virus infectivity. J Virol 88(18):10511–10524. doi:10.1128/jvi.01272-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weik M, Modrof J, Klenk HD, Becker S, MĂĽhlberger E (2002) Ebola virus VP30-mediated transcription is regulated by RNA secondary structure formation. J Virol 76(17):8532–8539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weis BL, Schleiff E, Zerges W (2013) Protein targeting to subcellular organelles via MRNA localization. Biochim Biophys Acta 1833(2):260–273

    Google Scholar 

  • Welsch S, Kolesnikova L, Krähling V, Riches JD, Becker S, Briggs JA (2010) Electron tomography reveals the steps in filovirus budding. PLoS Pathog 6(4):e1000875. doi:10.1371/journal.ppat.1000875

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wenigenrath J, Kolesnikova L, Hoenen T, Mittler E, Becker S (2010) Establishment and application of an infectious virus-like particle system for Marburg virus. J Gen Virol 91(Pt 5):1325–1334. doi:10.1099/vir.0.018226-0

    Article  CAS  PubMed  Google Scholar 

  • Whelan SP, Barr JN, Wertz GW (2004) Transcription and replication of nonsegmented negative-strand RNA viruses. Curr Top Microbiol Immunol 283:61–119

    CAS  PubMed  Google Scholar 

  • Yamayoshi S, Noda T, Ebihara H, Goto H, Morikawa Y, Lukashevich IS, Neumann G, Feldmann H, Kawaoka Y (2008) Ebola virus matrix protein VP40 uses the COPII transport system for its intracellular transport. Cell Host Microbe 3(3):168–177. doi:10.1016/j.chom.2008.02.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuda J, Nakao M, Kawaoka Y, Shida H (2003) Nedd4 regulates egress of Ebola virus-like particles from host cells. J Virol 77(18):9987–9992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Larissa Kolesnikova or Stephan Becker .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Kolesnikova, L., Nanbo, A., Becker, S., Kawaoka, Y. (2017). Inside the Cell: Assembly of Filoviruses. In: MĂĽhlberger, E., Hensley, L., Towner, J. (eds) Marburg- and Ebolaviruses. Current Topics in Microbiology and Immunology, vol 411. Springer, Cham. https://doi.org/10.1007/82_2017_15

Download citation

Publish with us

Policies and ethics