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Review

A structural and functional perspective of alphavirus replication and assembly

, &
Pages 837-856 | Published online: 01 Sep 2009

Bibliography

  • Powers AM , BraultAC, ShirakoYet al.: Evolutionary relationships and systematics of the alphaviruses.J. Virol.75(21) , 10118–10131 (2001).
  • Enserink M : Infectious diseases. Chikungunya: no longer a third world disease.Science318(5858) , 1860–1861 (2007).
  • Mukhopadhyay S , ZhangW, GablerSet al.: Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses.Structure14(1) , 63–73 (2006).
  • Lescar J , RousselA, WienMWet al.: The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH.Cell105(1) , 137–148 (2001).
  • Strauss JH , StraussEG: The alphaviruses: gene expression, replication, and evolution.Microbiol. Rev.58(3) , 491–562 (1994).
  • Atkins GJ , FleetonMN, SheahanBJ: Therapeutic and prophylactic applications of alphavirus vectors.Expert Rev. Mol. Med.10 , e33 (2008).
  • Garmashova N , GorchakovR, VolkovaE, PaesslerS, FrolovaE, FrolovI: The Old World and New World alphaviruses use different virus-specific proteins for induction of transcriptional shutoff.J. Virol.81(5) , 2472–2484 (2007).
  • Weston J , VilloingS, BremontMet al.: Comparison of two aquatic alphaviruses, salmon pancreas disease virus and sleeping disease virus, by using genome sequence analysis, monoclonal reactivity, and cross-infection.J. Virol.76(12) , 6155–6163 (2002).
  • Weston JH , WelshMD, McLoughlinMF, ToddD: Salmon pancreas disease virus, an alphavirus infecting farmed Atlantic salmon, Salmo salar L.Virology256(2) , 188–195 (1999).
  • La Linn M , GardnerJ, WarrilowDet al.: Arbovirus of marine mammals: a new alphavirus isolated from the elephant seal louse, Lepidophthirus macrorhini.J. Virol.75(9) , 4103–4109 (2001).
  • Villoing S , BearzottiM, ChilmonczykS, CastricJ, BremontM: Rainbow trout sleeping disease virus is an atypical alphavirus.J. Virol.74(1) , 173–183 (2000).
  • Frey TK : Molecular biology of rubella virus.Adv. Virus Res.44 , 69–160 (1994).
  • Zhang W , MukhopadhyayS, PletnevSV, BakerTS, KuhnRJ, RossmannMG: Placement of the structural proteins in Sindbis virus.J. Virol.76(22) , 11645–11658 (2002).
  • Harrison SC , StrongRK, SchlesingerS, SchlesingerMJ: Crystallization of Sindbis virus and its nucleocapsid.J. Mol. Biol.226(1) , 277–280 (1992).
  • Fuller SD : The T=4 envelope of Sindbis virus is organized by interactions with a complementary T=3 capsid.Cell48(6) , 923–934 (1987).
  • Cheng RH , KuhnRJ, OlsonNHet al.: Nucleocapsid and glycoprotein organization in an enveloped virus.Cell80(4) , 621–630 (1995).
  • Mancini EJ , ClarkeM, GowenBE, RuttenT, FullerSD: Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus.Mol. Cell5(2) , 255–266 (2000).
  • Zhang W , FisherBR, OlsonNH, StraussJH, KuhnRJ, BakerTS: Aura virus structure suggests that the T=4 organization is a fundamental property of viral structural proteins.J. Virol.76(14) , 7239–7246 (2002).
  • Paredes AM , SimonMN, BrownDT: The mass of the Sindbis virus nucleocapsid suggests it has T = 4 icosahedral symmetry.Virology187(1) , 329–332 (1992).
  • Gaedigk-Nitschko K , SchlesingerMJ: The Sindbis virus 6K protein can be detected in virions and is acylated with fatty acids.Virology175(1) , 274–281 (1990).
  • Lusa S , GaroffH, LiljestromP: Fate of the 6K membrane protein of Semliki Forest virus during virus assembly.Virology185(2) , 843–846 (1991).
  • Kielian M , ChatterjeePK, GibbonsDL, LuYE: Specific roles for lipids in virus fusion and exit. Examples from the alphaviruses.Subcell. Biochem.34 , 409–455 (2000).
  • Schmidt MF : Acylation of viral spike glycoproteins: a feature of enveloped RNA viruses.Virology116(1) , 327–338 (1982).
  • Schmidt MF , BrachaM, SchlesingerMJ: Evidence for covalent attachment of fatty acids to Sindbis virus glycoproteins.Proc. Natl Acad. Sci. USA76(4) , 1687–1691 (1979).
  • von Bonsdorff CH , HarrisonSC: Sindbis virus glycoproteins form a regular icosahedral surface lattice.J. Virol.16(1) , 141–145 (1975).
  • Vogel RH , ProvencherSW, von Bonsdorff CH, Adrian M, Dubochet J: Envelope structure of Semliki Forest virus reconstructed from cryo-electron micrographs. Nature320(6062) , 533–535 (1986).
  • Paredes AM , BrownDT, RothnagelRet al.: Three-dimensional structure of a membrane-containing virus.Proc. Natl Acad. Sci. USA90(19) , 9095–9099 (1993).
  • Pletnev SV , ZhangW, MukhopadhyaySet al.: Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold.Cell105(1) , 127–136 (2001).
  • Smith TJ , ChengRH, OlsonNHet al.: Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy.Proc. Natl Acad. Sci. USA92(23) , 10648–10652 (1995).
  • Zhang W , HeilM, KuhnRJ, BakerTS: Heparin binding sites on Ross River virus revealed by electron cryo-microscopy.Virology332(2) , 511–518 (2005).
  • Davis NL , PenceDF, MeyerWJ, SchmaljohnAL, JohnstonRE: Alternative forms of a strain-specific neutralizing antigenic site on the Sindbis virus E2 glycoprotein.Virology161(1) , 101–108 (1987).
  • Meyer WJ , JohnstonRE: Structural rearrangement of infecting Sindbis virions at the cell surface: mapping of newly accessible epitopes.J. Virol.67(9) , 5117–5125 (1993).
  • Strauss EG , StecDS, SchmaljohnAL, StraussJH: Identification of antigenically important domains in the glycoproteins of Sindbis virus by analysis of antibody escape variants.J. Virol.65(9) , 4654–4664 (1991).
  • von Bonsdorff CH , HarrisonSC: Hexagonal glycoprotein arrays from Sindbis virus membranes.J. Virol.28(2) , 578–583 (1978).
  • Wu SR , HaagL, SjobergM, GaroffH, HammarL: The dynamic envelope of a fusion class II virus. E3 domain of glycoprotein E2 precursor in Semliki Forest virus provides a unique contact with the fusion protein E1.J. Biol. Chem.283(39) , 26452–26460 (2008).
  • Ferlenghi I , GowenB, de Haas F et al.: The first step: activation of the Semliki Forest virus spike protein precursor causes a localized conformational change in the trimeric spike. J. Mol. Biol.283(1) , 71–81 (1998).
  • Paredes AM , HeidnerH, Thuman-CommikeP, PrasadBV, JohnstonRE, ChiuW: Structural localization of the E3 glycoprotein in attenuated Sindbis virus mutants.J. Virol.72(2) , 1534–1541 (1998).
  • Parrott MM , SitarskiSA, ArnoldRJ, PictonLK, HillRB, MukhopadhyayS: Role of conserved cysteines in the alphavirus E3 protein.J. Virol.83(6) , 2584–2591 (2009).
  • Lobigs M , ZhaoHX, GaroffH: Function of Semliki Forest virus E3 peptide in virus assembly: replacement of E3 with an artificial signal peptide abolishes spike heterodimerization and surface expression of E1.J. Virol.64(9) , 4346–4355 (1990).
  • Lobigs M , GaroffH: Fusion function of the Semliki Forest virus spike is activated by proteolytic cleavage of the envelope glycoprotein precursor p62.J. Virol.64(3) , 1233–1240 (1990).
  • Wahlberg JM , BoereWA, GaroffH: The heterodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation.J. Virol.63(12) , 4991–4997 (1989).
  • Ryman KD , KlimstraWB, JohnstonRE: Attenuation of Sindbis virus variants incorporating uncleaved PE2 glycoprotein is correlated with attachment to cell-surface heparan sulfate.Virology322(1) , 1–12 (2004).
  • Heidner HW , McKnightKL, DavisNL, JohnstonRE: Lethality of PE2 incorporation into Sindbis virus can be suppressed by second-site mutations in E3 and E2.J. Virol.68(4) , 2683–2692 (1994).
  • Knight RL , SchultzKL, KentRJ, VenkatesanM, GriffinDE: Role of N-linked glycosylation for Sindbis virus infection and replication in vertebrate and invertebrate systems.J. Virol.83(11) , 5640–5647 (2009).
  • Ryman KD , GardnerCL, BurkeCW, MeierKC, ThompsonJM, KlimstraWB: Heparan sulfate binding can contribute to the neurovirulence of neuroadapted and nonneuroadapted Sindbis viruses.J. Virol.81(7) , 3563–3573 (2007).
  • Bear JS , ByrnesAP, GriffinDE: Heparin-binding and patterns of virulence for two recombinant strains of Sindbis virus.Virology347(1) , 183–190 (2006).
  • Tucker PC , LeeSH, BuiN, MartinieD, GriffinDE: Amino acid changes in the Sindbis virus E2 glycoprotein that increase neurovirulence improve entry into neuroblastoma cells.J. Virol.71(8) , 6106–6112 (1997).
  • Myles KM , PierroDJ, OlsonKE: Deletions in the putative cell receptor-binding domain of Sindbis virus strain MRE16 E2 glycoprotein reduce midgut infectivity in Aedes aegypti.J. Virol.77(16) , 8872–8881 (2003).
  • Navaratnarajah CK , KuhnRJ: Functional characterization of the Sindbis virus E2 glycoprotein by transposon linker-insertion mutagenesis.Virology363(1) , 134–147 (2007).
  • Sharp JS , NelsonS, BrownD, TomerKB: Structural characterization of the E2 glycoprotein from Sindbis by lysine biotinylation and LC-MS/MS.Virology348(1) , 216–223 (2006).
  • Helenius A , von Bonsdorff CH: Semliki Forest virus membrane proteins. Preparation and characterization of spike complexes soluble in detergent-free medium. Biochim. Biophys. Acta436(4) , 895–899 (1976).
  • Kielian M , HeleniusA: pH-induced alterations in the fusogenic spike protein of Semliki Forest virus.J. Cell. Biol.101(6) , 2284–2291 (1985).
  • Wengler G , ReyFA: The isolation of the ectodomain of the alphavirus E1 protein as a soluble hemagglutinin and its crystallization.Virology257(2) , 472–482 (1999).
  • Roussel A , LescarJ, VaneyMC, WenglerG, ReyFA: Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus.Structure14(1) , 75–86 (2006).
  • Rey FA , HeinzFX, MandlC, KunzC, HarrisonSC: The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution.Nature375(6529) , 291–298 (1995).
  • Strauss JH , StraussEG: Virus evolution: how does an enveloped virus make a regular structure?Cell105(1) , 5–8 (2001).
  • Gibbons DL , ReillyB, AhnAet al.: Purification and crystallization reveal two types of interactions of the fusion protein homotrimer of Semliki Forest virus.J. Virol.78(7) , 3514–3523 (2004).
  • Gibbons DL , VaneyMC, RousselAet al.: Conformational change and protein–protein interactions of the fusion protein of Semliki Forest virus.Nature427(6972) , 320–325 (2004).
  • Wengler G , KoschinskiA, DreyerF: Entry of alphaviruses at the plasma membrane converts the viral surface proteins into an ion-permeable pore that can be detected by electrophysiological analyses of whole-cell membrane currents.J. Gen. Virol.84(Pt 1) , 173–181 (2003).
  • Gibbons DL , ErkI, ReillyBet al.: Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography.Cell114(5) , 573–583 (2003).
  • Anthony RP , BrownDT: Protein–protein interactions in an alphavirus membrane.J. Virol.65(3) , 1187–1194 (1991).
  • Wahlberg JM , BronR, WilschutJ, GaroffH: Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein.J. Virol.66(12) , 7309–7318 (1992).
  • Ahn A , KlimjackMR, ChatterjeePK, KielianM: An epitope of the Semliki Forest virus fusion protein exposed during virus–membrane fusion.J. Virol.73(12) , 10029–10039 (1999).
  • Qin ZL , ZhengY, KielianM: Role of conserved histidine residues in the low-pH dependence of the Semliki Forest virus fusion protein.J. Virol.83(9) , 4670–4677 (2009).
  • Kielian M , KlimjackMR, GhoshS, DuffusWA: Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus.J. Cell. Biol.134(4) , 863–872 (1996).
  • Duffus WA , Levy-MintzP, KlimjackMR, KielianM: Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly.J. Virol.69(4) , 2471–2479 (1995).
  • Hernandez R , LuoT, BrownDT: Exposure to low pH is not required for penetration of mosquito cells by Sindbis virus.J. Virol.75(4) , 2010–2013 (2001).
  • McInerney GM , SmitJM, LiljestromP, WilschutJ: Semliki Forest virus produced in the absence of the 6K protein has an altered spike structure as revealed by decreased membrane fusion capacity.Virology325(2) , 200–206 (2004).
  • Gaedigk-Nitschko K , DingMX, LevyMA, SchlesingerMJ: Site-directed mutations in the Sindbis virus 6K protein reveal sites for fatty acylation and the underacylated protein affects virus release and virion structure.Virology175(1) , 282–291 (1990).
  • Liljestrom P , LusaS, HuylebroeckD, GaroffH: In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release.J. Virol.65(8) , 4107–4113 (1991).
  • Loewy A , SmythJ, von Bonsdorff CH, Liljestrom P, Schlesinger MJ: The 6-kilodalton membrane protein of Semliki Forest virus is involved in the budding process. J. Virol.69(1) , 469–475 (1995).
  • Liljestrom P , GaroffH: Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor.J. Virol.65(1) , 147–154 (1991).
  • Ivanova L , LustigS, SchlesingerMJ: A pseudo-revertant of a Sindbis virus 6K protein mutant, which corrects for aberrant particle formation, contains two new mutations that map to the ectodomain of the E2 glycoprotein.Virology206(2) , 1027–1034 (1995).
  • Yao JS , StraussEG, StraussJH: Interactions between PE2, E1, and 6K required for assembly of alphaviruses studied with chimeric viruses.J. Virol.70(11) , 7910–7920 (1996).
  • Sanz MA , CarrascoL: Sindbis virus variant with a deletion in the 6K gene shows defects in glycoprotein processing and trafficking: lack of complementation by a wild-type 6K gene in trans.J. Virol.75(16) , 7778–7784 (2001).
  • Sanz MA , MadanV, CarrascoL, NievaJL: Interfacial domains in Sindbis virus 6K protein. Detection and functional characterization.J. Biol. Chem.278(3) , 2051–2057 (2003).
  • Sanz MA , PerezL, CarrascoL: Semliki Forest virus 6K protein modifies membrane permeability after inducible expression in Escherichia coli cells.J. Biol. Chem.269(16) , 12106–12110 (1994).
  • Melton JV , EwartGD, WeirRC, BoardPG, LeeE, GagePW: Alphavirus 6K proteins form ion channels.J. Biol. Chem.277(49) , 46923–46931 (2002).
  • Madan V , SanzMA, CarrascoL: Requirement of the vesicular system for membrane permeabilization by Sindbis virus.Virology332(1) , 307–315 (2005).
  • Madan V , CastelloA, CarrascoL: Viroporins from RNA viruses induce caspase-dependent apoptosis.Cell. Microbiol.10(2) , 437–451 (2008).
  • Gonzalez ME , CarrascoL: Viroporins.FEBS Lett.552(1) , 28–34 (2003).
  • Strauss EG , LenchesEM, Stamreich-MartinMA: Growth and release of several alphaviruses in chick and BHK cells.J. Gen. Virol.49(2) , 297–307 (1980).
  • Waite MR , BrownDT, PfefferkornER: Inhibition of Sindbis virus release by media of low ionic strength: an electron microscope study.J. Virol.10(3) , 537–544 (1972).
  • Gonzalez ME , CarrascoL: Human immunodeficiency virus type 1 VPU protein affects Sindbis virus glycoprotein processing and enhances membrane permeabilization.Virology279(1) , 201–209 (2001).
  • Lee S , OwenKE, ChoiHKet al.: Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly.Structure4(5) , 531–541 (1996).
  • Skoging U , VihinenM, NilssonL, LiljestromP: Aromatic interactions define the binding of the alphavirus spike to its nucleocapsid.Structure4(5) , 519–529 (1996).
  • Wilkinson TA , TellinghuisenTL, KuhnRJ, PostCB: Association of sindbis virus capsid protein with phospholipid membranes and the E2 glycoprotein: implications for alphavirus assembly.Biochemistry44(8) , 2800–2810 (2005).
  • Coombs KM , BrownDT: Form-determining functions in Sindbis virus nucleocapsids: nucleosomelike organization of the nucleocapsid.J. Virol.63(2) , 883–891 (1989).
  • Choi HK , TongL, MinorWet al.: Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion.Nature354(6348) , 37–43 (1991).
  • Choi HK , LuG, LeeS, WenglerG, RossmannMG: Structure of Semliki Forest virus core protein.Proteins27(3) , 345–359 (1997).
  • Hahn CS , StraussJH: Site-directed mutagenesis of the proposed catalytic amino acids of the Sindbis virus capsid protein autoprotease.J. Virol.64(6) , 3069–3073 (1990).
  • Melancon P , GaroffH: Processing of the Semliki Forest virus structural polyprotein: role of the capsid protease.J. Virol.61(5) , 1301–1309 (1987).
  • Smith AL , TignorGH: Host cell receptors for two strains of Sindbis virus.Arch. Virol.66(1) , 11–26 (1980).
  • Ludwig GV , KondigJP, SmithJF: A putative receptor for Venezuelan equine encephalitis virus from mosquito cells.J. Virol.70(8) , 5592–5599 (1996).
  • Wang KS , KuhnRJ, StraussEG, OuS, StraussJH: High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells.J. Virol.66(8) , 4992–5001 (1992).
  • Strauss JH , RümenapfT, WeirRC, KuhnRJ, WangK, StraussEG: Cellular receptors for alphaviruses. In: Cellular Receptors for Animal Viruses. Wimmer E (Ed.). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA 141–163 (1994).
  • Lustig S , JacksonAC, HahnCS, GriffinDE, StraussEG, StraussJH: Molecular basis of Sindbis virus neurovirulence in mice.J. Virol.62(7) , 2329–2336 (1988).
  • Tucker PC , GriffinDE: Mechanism of altered Sindbis virus neurovirulence associated with a single-amino-acid change in the E2 glycoprotein.J. Virol.65(3) , 1551–1557 (1991).
  • Flynn DC , MeyerWJ, MackenzieJM Jr, Johnston RE: A conformational change in Sindbis virus glycoproteins E1 and E2 is detected at the plasma membrane as a consequence of early virus–cell interaction. J. Virol.64(8) , 3643–3653 (1990).
  • Abell BA , BrownDT: Sindbis virus membrane fusion is mediated by reduction of glycoprotein disulfide bridges at the cell surface.J. Virol.67(9) , 5496–5501 (1993).
  • Anthony RP , ParedesAM, BrownDT: Disulfide bonds are essential for the stability of the Sindbis virus envelope.Virology190(1) , 330–336 (1992).
  • Glomb-Reinmund S , KielianM: The role of low pH and disulfide shuffling in the entry and fusion of Semliki Forest virus and Sindbis virus.Virology248(2) , 372–381 (1998).
  • Helenius A , KartenbeckJ, SimonsK, FriesE: On the entry of Semliki forest virus into BHK-21 cells.J. Cell. Biol.84(2) , 404–420 (1980).
  • Marsh M , BolzauE, HeleniusA: Penetration of Semliki Forest virus from acidic prelysosomal vacuoles.Cell32(3) , 931–940 (1983).
  • DeTulleo L , KirchhausenT: The clathrin endocytic pathway in viral infection.EMBO J.17(16) , 4585–4593 (1998).
  • Hammar L , MarkarianS, HaagL, LankinenH, SalmiA, ChengRH: Prefusion rearrangements resulting in fusion peptide exposure in Semliki Forest virus.J. Biol. Chem.278(9) , 7189–7198 (2003).
  • Gibbons DL , AhnA, ChatterjeePK, KielianM: Formation and characterization of the trimeric form of the fusion prGibbonsotein of Semliki Forest virus.J. Virol.74(17) , 7772–7780 (2000).
  • Kielian MC , HeleniusA: Role of cholesterol in fusion of Semliki Forest virus with membranes.J. Virol.52(1) , 281–283 (1984).
  • Ahn A , GibbonsDL, KielianM: The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains.J. Virol.76(7) , 3267–3275 (2002).
  • Phalen T , KielianM: Cholesterol is required for infection by Semliki Forest virus.J. Cell. Biol.112(4) , 615–623 (1991).
  • Helenius A : Semliki Forest virus penetration from endosomes: a morphological study.Biol. Cell51(2) , 181–185 (1984).
  • Wengler G , WurknerD: Identification of a sequence element in the alphavirus core protein which mediates interaction of cores with ribosomes and the disassembly of cores.Virology191(2) , 880–888 (1992).
  • Wengler G , GrosC: Analyses of the role of structural changes in the regulation of uncoating and assembly of alphavirus cores.Virology222(1) , 123–132 (1996).
  • Li G , RiceCM: The signal for translational readthrough of a UGA codon in Sindbis virus RNA involves a single cytidine residue immediately downstream of the termination codon.J. Virol.67(8) , 5062–5067 (1993).
  • Takkinen K : Complete nucleotide sequence of the nonstructural protein genes of Semliki Forest virus.Nucleic Acids Res.14(14) , 5667–5682 (1986).
  • Cross RK : Identification of a unique guanine-7-methyltransferase in Semliki Forest virus (SFV) infected cell extracts.Virology130(2) , 452–463 (1983).
  • Laakkonen P , HyvonenM, PeranenJ, KaariainenL: Expression of Semliki Forest virus nsP1-specific methyltransferase in insect cells and in Escherichia coli.J. Virol.68(11) , 7418–7425 (1994).
  • Mi S , StollarV: Expression of Sindbis virus nsP1 and methyltransferase activity in Escherichia coli.Virology184(1) , 423–427 (1991).
  • Laakkonen P , AholaT, KaariainenL: The effects of palmitoylation on membrane association of Semliki Forest virus RNA capping enzyme.J. Biol. Chem.271(45) , 28567–28571 (1996).
  • Ahola T , LampioA, AuvinenP, KaariainenL: Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity.EMBO J.18(11) , 3164–3172 (1999).
  • Wang YF , SawickiSG, SawickiDL: Sindbis virus nsP1 functions in negative-strand RNA synthesis.J. Virol.65(2) , 985–988 (1991).
  • Gomez de Cedron M , EhsaniN, MikkolaML, GarciaJA, KaariainenL: RNA helicase activity of Semliki Forest virus replicase protein NSP2.FEBS Lett.448(1) , 19–22 (1999).
  • Rikkonen M , PeranenJ, KaariainenL: ATPase and GTPase activities associated with Semliki Forest virus nonstructural protein nsP2.J. Virol.68(9) , 5804–5810 (1994).
  • Vasiljeva L , MeritsA, AuvinenP, KaariainenL: Identification of a novel function of the alphavirus capping apparatus. RNA 5´-triphosphatase activity of Nsp2.J. Biol. Chem.275(23) , 17281–17287 (2000).
  • Strauss EG , De Groot RJ, Levinson R, Strauss JH: Identification of the active site residues in the nsP2 proteinase of Sindbis virus. Virology191(2) , 932–940 (1992).
  • Vasiljeva L , ValmuL, KaariainenL, MeritsA: Site-specific protease activity of the carboxyl-terminal domain of Semliki Forest virus replicase protein nsP2.J. Biol. Chem.276(33) , 30786–30793 (2001).
  • Mayuri, Geders TW , SmithJL, KuhnRJ: Role for conserved residues of Sindbis virus nonstructural protein 2 methyltransferase-like domain in regulation of minus-strand synthesis and development of cytopathic infection.J. Virol.82(15) , 7284–7297 (2008).
  • Russo AT , WhiteMA, WatowichSJ: The crystal structure of the Venezuelan equine encephalitis alphavirus nsP2 protease.Structure14(9) , 1449–1458 (2006).
  • de Groot RJ , HardyWR, ShirakoY, StraussJH: Cleavage-site preferences of Sindbis virus polyproteins containing the non-structural proteinase. Evidence for temporal regulation of polyprotein processing in vivo.EMBO J.9(8) , 2631–2638 (1990).
  • Peranen J , RikkonenM, LiljestromP, KaariainenL: Nuclear localization of Semliki Forest virus-specific nonstructural protein nsP2.J. Virol.64(5) , 1888–1896 (1990).
  • Kaariainen L , AholaT: Functions of alphavirus nonstructural proteins in RNA replication.Prog. Nucleic Acid Res. Mol. Biol.71 , 187–222 (2002).
  • Tamm K , MeritsA, SarandI: Mutations in the nuclear localization signal of nsP2 influencing RNA synthesis, protein expression and cytotoxicity of Semliki Forest virus.J. Gen. Virol.89(Pt 3) , 676–686 (2008).
  • Hahn YS , StraussEG, StraussJH: Mapping of RNA- temperature-sensitive mutants of Sindbis virus: assignment of complementation groups A, B, and G to nonstructural proteins.J. Virol.63(7) , 3142–3150 (1989).
  • Lemm JA , RumenapfT, StraussEG, StraussJH, RiceCM: Polypeptide requirements for assembly of functional Sindbis virus replication complexes: a model for the temporal regulation of minus- and plus-strand RNA synthesis.EMBO J.13(12) , 2925–2934 (1994).
  • Shirako Y , StraussJH: Regulation of Sindbis virus RNA replication: uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand RNA synthesis.J. Virol.68(3) , 1874–1885 (1994).
  • Park E , GriffinDE: The nsP3 macro domain is important for Sindbis virus replication in neurons and neurovirulence in mice.Virology388(2) , 305–314 (2009).
  • Tuittila M , HinkkanenAE: Amino acid mutations in the replicase protein nsP3 of Semliki Forest virus cumulatively affect neurovirulence.J. Gen. Virol.84(Pt 6) , 1525–1533 (2003).
  • Allen MD , BuckleAM, CordellSC, LoweJ, BycroftM: The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A.J. Mol. Biol.330(3) , 503–511 (2003).
  • Letunic I , CopleyRR, PilsB, PinkertS, SchultzJ, BorkP: SMART 5: domains in the context of genomes and networks.Nucleic Acids Res.34(Database issue) , D257–D260 (2006).
  • Malet H , CoutardB, JamalSet al.: The crystal structures of Chikungunya and Venezuelan equine encephalitis virus nsP3 macro domains define a conserved adenosine binding pocket.J. Virol.83(13) , 6534–6545 (2009).
  • Vihinen H , SaarinenJ: Phosphorylation site analysis of Semliki Forest virus nonstructural protein 3.J. Biol. Chem.275(36) , 27775–27783 (2000).
  • Vihinen H , AholaT, TuittilaM, MeritsA, KaariainenL: Elimination of phosphorylation sites of Semliki Forest virus replicase protein nsP3.J. Biol. Chem.276(8) , 5745–5752 (2001).
  • Gorchakov R , GarmashovaN, FrolovaE, FrolovI: Different types of nsP3-containing protein complexes in Sindbis virus-infected cells.J. Virol.82(20) , 10088–10101 (2008).
  • Kamer G , ArgosP: Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses.Nucleic Acids Res.12(18) , 7269–7282 (1984).
  • Hahn YS , GrakouiA, RiceCM, StraussEG, StraussJH: Mapping of RNA- temperature-sensitive mutants of Sindbis virus: complementation group F mutants have lesions in nsP4.J. Virol.63(3) , 1194–1202 (1989).
  • Shirako Y , StraussEG, StraussJH: Suppressor mutations that allow Sindbis virus RNA polymerase to function with nonaromatic amino acids at the N-terminus: evidence for interaction between nsP1 and nsP4 in minus-strand RNA synthesis.Virology276(1) , 148–160 (2000).
  • Fata CL , SawickiSG, SawickiDL: Modification of Asn374 of nsP1 suppresses a Sindbis virus nsP4 minus-strand polymerase mutant.J. Virol.76(17) , 8641–8649 (2002).
  • de Groot RJ , RumenapfT, KuhnRJ, StraussEG, StraussJH: Sindbis virus RNA polymerase is degraded by the N-end rule pathway.Proc. Natl Acad. Sci. USA88(20) , 8967–8971 (1991).
  • Shirako Y , StraussJH: Requirement for an aromatic amino acid or histidine at the N terminus of Sindbis virus RNA polymerase.J. Virol.72(3) , 2310–2315 (1998).
  • Tomar S , HardyRW, SmithJL, KuhnRJ: Catalytic core of alphavirus nonstructural protein nsP4 possesses terminal adenylyltransferase activity.J. Virol.80(20) , 9962–9969 (2006).
  • Froshauer S , KartenbeckJ, HeleniusA: Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes.J. Cell. Biol.107(6 Pt 1) , 2075–2086 (1988).
  • Kujala P , IkaheimonenA, EhsaniN, VihinenH, AuvinenP, KaariainenL: Biogenesis of the Semliki Forest virus RNA replication complex.J. Virol.75(8) , 3873–3884 (2001).
  • Kuhn RJ , NiestersHG, HongZ, StraussJH: Infectious RNA transcripts from Ross River virus cDNA clones and the construction and characterization of defined chimeras with Sindbis virus.Virology182(2) , 430–441 (1991).
  • Barton DJ , SawickiSG, SawickiDL: Solubilization and immunoprecipitation of alphavirus replication complexes.J. Virol.65(3) , 1496–1506 (1991).
  • Gorchakov R , FrolovaE, SawickiS, AtashevaS, SawickiD, FrolovI: A new role for ns polyprotein cleavage in Sindbis virus replication.J. Virol.82(13) , 6218–6231 (2008).
  • Mai J , SawickiS, SawickiD: Fate of minus strand templates and replication complexes produced by a P23-cleavage defective mutant of Sindbis virus.J. Virol.83(17) , 8553–8564 (2009).
  • Shirako Y , StraussJH: Cleavage between nsP1 and nsP2 initiates the processing pathway of Sindbis virus nonstructural polyprotein P123.Virology177(1) , 54–64 (1990).
  • Lemm JA , BergqvistA, ReadCM, RiceCM: Template-dependent initiation of Sindbis virus RNA replication in vitro.J. Virol.72(8) , 6546–6553 (1998).
  • Wang YF , SawickiSG, SawickiDL: Alphavirus nsP3 functions to form replication complexes transcribing negative-strand RNA.J. Virol.68(10) , 6466–6475 (1994).
  • Raju R , HuangHV: Analysis of Sindbis virus promoter recognition in vivo, using novel vectors with two subgenomic mRNA promoters.J. Virol.65(5) , 2501–2510 (1991).
  • Frolov I , HardyR, RiceCM: Cis-acting RNA elements at the 5´ end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis.RNA7(11) , 1638–1651 (2001).
  • Ou JH , StraussEG, StraussJH: The 5´-terminal sequences of the genomic RNAs of several alphaviruses.J. Mol. Biol.168(1) , 1–15 (1983).
  • Kuhn RJ , HongZ, StraussJH: Mutagenesis of the 3´ nontranslated region of Sindbis virus RNA.J. Virol.64(4) , 1465–1476 (1990).
  • Hardy RW : The role of the 3´ terminus of the Sindbis virus genome in minus-strand initiation site selection.Virology345(2) , 520–531 (2006).
  • Pushko P , ParkerM, LudwigGV, DavisNL, JohnstonRE, SmithJF: Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo.Virology239(2) , 389–401 (1997).
  • Frolov I , HoffmanTA, PragaiBMet al.: Alphavirus-based expression vectors: strategies and applications.Proc. Natl Acad. Sci. USA93(21) , 11371–11377 (1996).
  • Ou JH , TrentDW, StraussJH: The 3´-non-coding regions of alphavirus RNAs contain repeating sequences.J. Mol. Biol.156(4) , 719–730 (1982).
  • Weiss B , NitschkoH, GhattasI, WrightR, SchlesingerS: Evidence for specificity in the encapsidation of Sindbis virus RNAs.J. Virol.63(12) , 5310–5318 (1989).
  • Tellinghuisen TL , KuhnRJ: Nucleic acid-dependent cross-linking of the nucleocapsid protein of Sindbis virus.J. Virol.74(9) , 4302–4309 (2000).
  • Linger BR , KunovskaL, KuhnRJ, GoldenBL: Sindbis virus nucleocapsid assembly: RNA folding promotes capsid protein dimerization.RNA10(1) , 128–138 (2004).
  • Wengler G : Identification of a transfer of viral core protein to cellular ribosomes during the early stages of alphavirus infection.Virology134(2) , 435–442 (1984).
  • Tellinghuisen TL , HamburgerAE, FisherBR, OstendorpR, KuhnRJ: In vitro assembly of alphavirus cores by using nucleocapsid protein expressed in Escherichia coli.J. Virol.73(7) , 5309–5319 (1999).
  • Tellinghuisen TL , PereraR, KuhnRJ: In vitro assembly of Sindbis virus core-like particles from crosslinked dimers of truncated and mutant capsid proteins.J. Virol.75(6) , 2810–2817 (2001).
  • Weiss B , Geigenmuller-GnirkeU, SchlesingerS: Interactions between Sindbis virus RNAs and a 68 amino acid derivative of the viral capsid protein further defines the capsid binding site.Nucleic Acids Res.22(5) , 780–786 (1994).
  • Owen KE , KuhnRJ: Identification of a region in the Sindbis virus nucleocapsid protein that is involved in specificity of RNA encapsidation.J. Virol.70(5) , 2757–2763 (1996).
  • Warrier R , LingerBR, GoldenBL, KuhnRJ: Role of Sindbis virus capsid protein region II in nucleocapsid core assembly and encapsidation of genomic RNA.J. Virol.82(9) , 4461–4470 (2008).
  • Perera R , NavaratnarajahC, KuhnRJ: A heterologous coiled coil can substitute for helix I of the Sindbis virus capsid protein.J. Virol.77(15) , 8345–8353 (2003).
  • Hong EM , PereraR, KuhnRJ: Alphavirus capsid protein helix I controls a checkpoint in nucleocapsid core assembly.J. Virol.80(18) , 8848–8855 (2006).
  • Skoging-Nyberg U , LiljestromP: M-X-I motif of Semliki Forest virus capsid protein affects nucleocapsid assembly.J. Virol.75(10) , 4625–4632 (2001).
  • Ferreira D , HernandezR, HortonM, BrownDT: Morphological variants of Sindbis virus produced by a mutation in the capsid protein.Virology307(1) , 54–66 (2003).
  • Garoff H , HuylebroeckD, RobinsonA, TillmanU, LiljestromP: The signal sequence of the p62 protein of Semliki Forest virus is involved in initiation but not in completing chain translocation.J. Cell. Biol.111(3) , 867–876 (1990).
  • Johnson DC , SchlesingerMJ, ElsonEL: Fluorescence photobleaching recovery measurements reveal differences in envelopment of Sindbis and vesicular stomatitis viruses.Cell23(2) , 423–431 (1981).
  • Sefton BM : Immediate glycosylation of Sindbis virus membrane proteins.Cell10(4) , 659–668 (1977).
  • Hsieh P , RobbinsPW: Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells.J. Biol. Chem.259(4) , 2375–2382 (1984).
  • Knight RL , SchultzKL, KentRJ, VenkatesanM, GriffinDE: Role of N-linked glycosylation for Sindbis virus infection and replication in vertebrate and invertebrate systems.J. Virol.83(11) , 5640–5647 (2009).
  • Liu N , BrownDT: Phosphorylation and dephosphorylation events play critical roles in Sindbis virus maturation.Virology196(2) , 703–711 (1993).
  • Liu LN , LeeH, HernandezR, BrownDT: Mutations in the endo domain of Sindbis virus glycoprotein E2 block phosphorylation, reorientation of the endo domain, and nucleocapsid binding.Virology222(1) , 236–246 (1996).
  • Gaedigk-Nitschko K , SchlesingerMJ: Site-directed mutations in Sindbis virus E2 glycoprotein‘s cytoplasmic domain and the 6K protein lead to similar defects in virus assembly and budding.Virology183(1) , 206–214 (1991).
  • Ivanova L , SchlesingerMJ: Site-directed mutations in the Sindbis virus E2 glycoprotein identify palmitoylation sites and affect virus budding.J. Virol.67(5) , 2546–2551 (1993).
  • Salminen A , WahlbergJM, LobigsM, LiljestromP, GaroffH: Membrane fusion process of Semliki Forest virus. II: Cleavage-dependent reorganization of the spike protein complex controls virus entry.J. Cell. Biol.116(2) , 349–357 (1992).
  • Yu IM , ZhangW, HoldawayHAet al.: Structure of the immature dengue virus at low pH primes proteolytic maturation.Science319(5871) , 1834–1837 (2008).
  • Zhao H , GaroffH: Role of cell surface spikes in alphavirus budding.J. Virol.66(12) , 7089–7095 (1992).
  • Strauss JH , StraussEG, KuhnRJ: Budding of alphaviruses.Trends Microbiol.3(9) , 346–350 (1995).
  • Liu N , BrownDT: Transient translocation of the cytoplasmic (endo) domain of a type I membrane glycoprotein into cellular membranes.J. Cell. Biol.120(4) , 877–883 (1993).
  • Metsikko K , GaroffH: Oligomers of the cytoplasmic domain of the p62/E2 membrane protein of Semliki Forest virus bind to the nucleocapsid in vitro.J. Virol.64(10) , 4678–4683 (1990).
  • Suomalainen M , LiljestromP, GaroffH: Spike protein–nucleocapsid interactions drive the budding of alphaviruses.J. Virol.66(8) , 4737–4747 (1992).
  • Kail M , HollinsheadM, AnsorgeWet al.: The cytoplasmic domain of alphavirus E2 glycoprotein contains a short linear recognition signal required for viral budding.EMBO J.10(9) , 2343–2351 (1991).
  • Garoff H , SimonsK: Location of the spike glycoproteins in the Semliki Forest virus membrane.Proc. Natl Acad. Sci. USA71(10) , 3988–3992 (1974).
  • Lu YE , CasseseT, KielianM: The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence.J. Virol.73(5) , 4272–4278 (1999).
  • Lee H , RickerPD, BrownDT: The configuration of Sindbis virus envelope proteins is stabilized by the nucleocapsid protein.Virology204(1) , 471–474 (1994).
  • Lee H , BrownDT: Mutations in an exposed domain of Sindbis virus capsid protein result in the production of noninfectious virions and morphological variants.Virology202(1) , 390–400 (1994).
  • Forsell K , XingL, KozlovskaT, ChengRH, GaroffH: Membrane proteins organize a symmetrical virus.EMBO J.19(19) , 5081–5091 (2000).
  • West J , HernandezR, FerreiraD, BrownDT: Mutations in the endodomain of Sindbis virus glycoprotein E2 define sequences critical for virus assembly.J. Virol.80(9) , 4458–4468 (2006).
  • Helenius A , KartenbeckJ: The effects of octylglucoside on the Semliki Forest virus membrane. Evidence for a spike-protein–nucleocapsid interaction.Eur. J. Biochem.106(2) , 613–618 (1980).
  • Zhao H , LindqvistB, GaroffH, von Bonsdorff CH, Liljestrom P: A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding. EMBO J.13(18) , 4204–4211 (1994).
  • Lopez S , YaoJS, KuhnRJ, StraussEG, StraussJH: Nucleocapsid–glycoprotein interactions required for assembly of alphaviruses.J. Virol.68(3) , 1316–1323 (1994).
  • Strauss EG , LenchesEM, StraussJH: Molecular genetic evidence that the hydrophobic anchors of glycoproteins E2 and E1 interact during assembly of alphaviruses.J. Virol.76(20) , 10188–10194 (2002).
  • Hernandez R , LeeH, NelsonC, BrownDT: A single deletion in the membrane-proximal region of the Sindbis virus glycoprotein E2 endodomain blocks virus assembly.J. Virol.74(9) , 4220–4228 (2000).
  • Garmashova N , GorchakovR, FrolovaE, FrolovI: Sindbis virus nonstructural protein nsP2 is cytotoxic and inhibits cellular transcription.J. Virol.80(12) , 5686–5696 (2006).
  • Gorchakov R , FrolovaE, FrolovI: Inhibition of transcription and translation in Sindbis virus-infected cells.J. Virol.79(15) , 9397–9409 (2005).
  • Aguilar PV , WeaverSC, BaslerCF: Capsid protein of eastern equine encephalitis virus inhibits host cell gene expression.J. Virol.81(8) , 3866–3876 (2007).
  • Ventoso I , SanzMA, MolinaS, BerlangaJJ, CarrascoL, EstebanM: Translational resistance of late alphavirus mRNA to eIF2α phosphorylation: a strategy to overcome the antiviral effect of protein kinase PKR.Genes Dev.20(1) , 87–100 (2006).
  • Levine B , HuangQ, IsaacsJT, ReedJC, GriffinDE, HardwickJM: Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene.Nature361(6414) , 739–742 (1993).
  • Lewis J , WesselinghSL, GriffinDE, HardwickJM: Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence.J. Virol.70(3) , 1828–1835 (1996).
  • Glasgow GM , McGeeMM, TarbattCJ, MooneyDA, SheahanBJ, AtkinsGJ: The Semliki Forest virus vector induces p53-independent apoptosis.J. Gen. Virol.79(Pt 10) , 2405–2410 (1998).
  • Joe AK , FooHH, KleemanL, LevineB: The transmembrane domains of Sindbis virus envelope glycoproteins induce cell death.J. Virol.72(5) , 3935–3943 (1998).
  • Jan JT , GriffinDE: Induction of apoptosis by Sindbis virus occurs at cell entry and does not require virus replication.J. Virol.73(12) , 10296–10302 (1999).
  • Griffin DE , HardwickJM: Regulators of apoptosis on the road to persistent alphavirus infection.Annu. Rev. Microbiol.51 , 565–592 (1997).
  • Li ML , StollarV: Alphaviruses and apoptosis.Int. Rev. Immunol.23(1–2) , 7–24 (2004).
  • Atasheva S , GorchakovR, EnglishR, FrolovI, FrolovaE: Development of Sindbis viruses encoding nsP2/GFP chimeric proteins and their application for studying nsP2 functioning.J. Virol.81(10) , 5046–5057 (2007).
  • Lundstrom K : Alphavirus vectors for gene therapy applications. In: Cancer Drug Discovery and Development: Gene Therapy for Cancer. Hunt KK, Vorburger SA, Swisher SG (Eds). Human Press, Totowa, NJ, USA 109–119 (2007).

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