Abstract
The effect of temperature on fusion of Sendai virus with target membranes and mobility of the viral glycoproteins was studied with fluorescence methods. When intact virus was used, the fusion threshold temperature (20–22°C) was not altered regardless of the different types of target membranes. Viral glycoprotein mobility in the intact virus increased with temperature, particularly sharply at the fusion threshold temperature. This effect was suppressed by the presence of erythrocyte ghosts and/or dextran sulfate in the virus suspension. In these cases also, no change in the fusion threshold temperature was observed. On the other hand, reconstituted viral envelopes (virosomes) bearing viral glycoproteins but lacking matrix proteins were capable of fusing with erythrocyte ghosts even at temperatures lower than the fusion threshold temperature and no fusion threshold temperature was observed over the range of 10–40°C. The mobility of viral glycoproteins on virosomes was much greater and virtually temperature-independent. The intact virus treated with an actin-affector, jasplakinolide, reduced the extent of fusion with erythrocyte ghosts and the mobility of viral glycoproteins, while the treatment of virosomes with the same drug did not affect the extent of fusion of virosomes with erythrocyte ghosts and the mobility of the glycoproteins. These results suggest that viral matrix proteins including actins affect viral glycoprotein mobility and may be responsible for the temperature threshold phenomenon observed in Sendai virus fusion.
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M.N. Al-Ahdal T.F. Abidi T.D. Flanagan (1986) ArticleTitleThe interaction of Sendai virus glycoprotein-bearing recombinant vesicles with cell surfaces Biochim. Biophys. Acta 854 157–168 Occurrence Handle3002466
A. Ali D.P. Nayak (2000) ArticleTitleAssembly of Sendai virus: M protein interacts with F and HN proteins and with the cytoplasmic tail and transmembrane domain of F protein Virol. 276 289–303 Occurrence Handle10.1006/viro.2000.0556
R.J.L. Allen (1940) ArticleTitleThe estimation of phosphorus Biochem. J. 34 858–865
S. Amselem Y. Barenholz A. Loyter S. Nir D. Lichtenberg (1986) ArticleTitleFusion of Sendai virus with negatively charged liposomes as studied by pyrene-labelled phospholipid liposomes Biochim. Biophys. Acta. 860 301–313 Occurrence Handle3017417
B. Aroeti T.M. Jovin Y.I. Henis (1990) ArticleTitleRotational mobility of Sendai virus glycoprotein in membranes of fused human erythrocytes and in the envelopes of cell-bound virions Biochemistry 29 9119–9125 Occurrence Handle10.1021/bi00491a004 Occurrence Handle2176844
A. Asano K. Sekiguchi (1978) ArticleTitleRedistribution of intramembrane particles of human erythrocytes induced by HVJ (Sendai virus): A prerequisite for the virus-induced cell fusion J. Supermolec. Struct. 9 441–452 Occurrence Handle10.1002/jss.400090314
S. Bagai A. Puri R. Blumenthal D.P. Sarkar (1993) ArticleTitleHemagglutinin-neuraminidase enhances F protein-mediated membrane fusion of reconstituted Sendai virus envelopes with cells J. Virol. 67 3312–3318 Occurrence Handle8388501
V. Bennett D.M. Gilligan (1993) ArticleTitleThe spectrin-based membrane skeleton and micro-scale organization of the plasma membrane Annu. Rev. Cell Biol. 9 27–66 Occurrence Handle10.1146/annurev.cb.09.110193.000331 Occurrence Handle8280463
M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal Biochem. 78 248–254
K.N. Burger G. Knoll A.J. Verkleij (1988) ArticleTitleInfluenza virus-model membrane interactions: A morphological approach using modern cryotechniques Biochim. Biophys. Acta 939 89–101 Occurrence Handle3349083
A. Garcia-Sastre J.A. Cabezas E. Villar (1989) ArticleTitleProtein of Newcastle disease virus envelope: Interaction between the outer hemagglutinidase glycoprotein and the inner non-glycosylated matrix protein Biochim. Biophys. Acta 999 171–175 Occurrence Handle2597705
R.M. Giuffre D.R. Tovell C.M. Kay D.L.J. Tyrrell (1982) ArticleTitleEvidence for an interaction between the membrane protein of a paramyxovirus and actin J. Virol. 42 963–968 Occurrence Handle6285006
A.M. Haywood B.P. Boyer (1982) ArticleTitleSendai virus membrane fusion: time course and effect of temperature, pH, calcium, and receptor concentration Biochemistry 21 6041–6046 Occurrence Handle10.1021/bi00267a003 Occurrence Handle6295454
Y.I. Henis Y. Herman-Barhom B. Aroeti O. Gutman (1989) ArticleTitleLateral mobility of both envelope proteins (F and HN) of Sendai virus in the cell membrane is essential for cell-cell fusion J. Biol. Chem. 264 17119–17125 Occurrence Handle2551896
J.A. Hewitt M.V. Nermut (1977) ArticleTitleA morphological study of the M-protein of Sendai virus J. Gen. Virol. 34 127–136 Occurrence Handle188976
D. Hoekstra (1990) ArticleTitleMembrane fusion of enveloped virus: Especially a matter of proteins J. Bioenerg. Biomembr. 22 121–155 Occurrence Handle10.1007/BF00762943 Occurrence Handle2109749
D. Hoekstra T. De Boer K. Klappe J. Wilschut (1984) ArticleTitleA fluorescence method for measuring the kinetic analysis of viral binding, dissociation and fusion, J Virol. 23 5675–5681
D. Hoekstra K. Klappe T. de Boer J. Wilschut (1985) ArticleTitleCharacterization of the fusogenic properties of Sendai virus: Kinetics of fusion with erythrocyte membranes Biochemistry 24 4739–4745 Occurrence Handle10.1021/bi00339a005 Occurrence Handle3000417
D. Hoekstra K. Klappe H. Hoff S. Nir (1989) ArticleTitleMechanism of fusion of Sendai virus: Role of hydrophobic interaction and mobility constrains of viral membrane proteins J. Biol. Chem. 264 17119–17125 Occurrence Handle2551896
T. Kanaseki K. Kawasaki M. Murata Y. Ikeuchi S. Ohnishi (1997) ArticleTitleStructural features of membrane fusion between influenza virus and liposomes as revealed by quick-freezing electron microscopy J. Cell Biol. 137 1041–1056 Occurrence Handle10.1083/jcb.137.5.1041 Occurrence Handle9166405
J. Kim K. Hama Y. Miyake Y. Okada (1979) ArticleTitleTransformation of intramembrane particles of HVJ (Sendai virus) envelopes from an invisible to visible form on aging of virions Virology 24 523–535 Occurrence Handle10.1016/0042-6822(79)90506-3
J.R. Lakowicz (1983) Principles of Fluorescence Spectroscopy Plenum NY
R.A. Lamb B.W.J. Mahy P.W. Choppin (1976) ArticleTitleThe synthesis of Sendai virus polypeptides in infected cells Virology 69 116–131 Occurrence Handle10.1016/0042-6822(76)90199-9 Occurrence Handle174287
U.K. Laemmli (1970) ArticleTitleCleavage of structural proteins during the assembly of the head of the bacteriophage T4 Nature 227 680–685 Occurrence Handle5432063
P.M. Lee R.J. Cherry T. Bachi (1983) ArticleTitleCorrelation of rotational mobility and flexibility of Sendai virus spike glycoproteins with fusion activity Virology 128 65–76 Occurrence Handle10.1016/0042-6822(83)90319-7 Occurrence Handle6192588
K. Leonards S. Ohki (1983) ArticleTitleIsolation and characterization of large (0.5–1.0 μm) cytoskeleton-free vesicles from human and rabbit erythrocytes Biochim. Biophys. Acta 728 383–393 Occurrence Handle6402012
D.S. Lyles M. McKenzie J.W. Parce (1992) ArticleTitleSubunit interactions of vesicular stomatitis virus envelope glycoprotein stabilized by binding to viral matrix protein J. Virology 66 349–358 Occurrence Handle1309251
T. Maeda A. Asano K. Ohki Y. Okada S. Ohnishi (1975) ArticleTitleA spin-label study on fusion of red blood cells induced by hemagglutinating virus of Japan Biochemistry. 14 3736–3741 Occurrence Handle10.1021/bi00688a003 Occurrence Handle169884
T. Mebatsion F. Weiland K.K. Conzelmann (1999) ArticleTitleMatrix protein of rabies virus is responsible for the assembly and budding of bullet-shaped particles and interacts with the transmembrane spike glycoprotein G J. Virol. 73 242–250 Occurrence Handle9847327
T. Miyake J. Kim Y. Okada (1978) ArticleTitleEffect of cytochalasin D on fusion of cells by HVJ (Sendai virus) Exp. Cell Res. 116 167–178 Occurrence Handle10.1016/0014-4827(78)90073-3 Occurrence Handle212281
K. Narayanan A. Maeda J. Maeda S. Makino (2000) ArticleTitleCharacterization of the coronovirus M protein and nucleocapside interaction in infected cells J. Virol. 74 8127–8134 Occurrence Handle10.1128/JVI.74.17.8127-8134.2000 Occurrence Handle10933723
S. Ohki T.D. Flanagan D. Hoekstra (1998) ArticleTitleProbe transfer with and without membrane fusion in a fluorescence fusion assay Biochemistry 37 7496–7503 Occurrence Handle10.1021/bi972016g Occurrence Handle9585563
S. Ohki K. Arnold N. Srinivasakumar T.D. Flanagan (1992) ArticleTitleEffect of anionic polymers on fusion of Sendai virus with human erythrocyte ghosts Antiviral Research 18 163–177 Occurrence Handle10.1016/0166-3542(92)90036-5 Occurrence Handle1329648
D.E. Ott L.V. Coren B.P. Kane D.G. Busch D.G. Johnson R.C. Sowder II E.N. Chertova L.O. Arthur L.E. Henderson (1996) ArticleTitleCytoskeletal proteins inside human immunodeficiency virus type I virion J. Virol. 70 7734–7743 Occurrence Handle8892894
C.A. Pasternak K.J. Micklem (1973) ArticleTitlePermeability changes during cell fusion J. Membrane Biol. 14 293–303
M.E. Peeples (1991) Paramyxovirus M proteins: Pulling it all together and taking it on the road D.W Kingsbury (Eds) Paramyxoviruses Plenum Press New York 427–456
E.A. Repasky C.C. Gregorio (1992) Plasma membrane skeletons P Yeagle (Eds) The Structure of Biological Membranes CRC Press Boca Raton, FL 449–505
C.M. Sanderson N.L. McQueen D.P. Nayak (1993) ArticleTitleSendai virus assembly: M protein binds to viral glycoproteins in transit through the secretory pathway J. Virol. 67 651–663 Occurrence Handle8380460
C.M. Sanderson H.-H. Wu D.P. Nayak (1994) ArticleTitleSendai virus M protein binds independently to either the F or the HN glycoprotein in vivo J. Virol. 68 69–76 Occurrence Handle8254778
K. Shimizu N. Ishida (1975) ArticleTitleThe smallest protein of Sendai virus: its candidate function of binding nucleocapsid to envelope Virology 67 427–436 Occurrence Handle10.1016/0042-6822(75)90444-4 Occurrence Handle171833
M. Shinitzky Y. Barenholz (1974) ArticleTitleDynamics of the hydrocarbon layer in liposomes of lecithin and sphingomyelin containing diacetylphosphate, J Biol. Chem. 249 2652–2657
A.E. Spruce A. Iwata W. Almers (1991) ArticleTitlePatch clamp studies of single cell-fusion events mediated by a viral fusion protein, Proc Natl. Acad. Sci. USA. 88 3623–3627
T.L. Steck J.A. Kant (1974) ArticleTitlePreparation of impermeable ghosts and inside-out vesicles from human erythrocyte membranes Methods Enzymol. 31 172–180 Occurrence Handle4370662
T. Takimoto K. Gopal Murti T. Bousse R.A. Scroggs A. Porter (2001) ArticleTitleRole of matrix and fusion proteins in budding of Sendai virus J. Virol. 75 11384–11391 Occurrence Handle10.1128/JVI.75.23.11384-11391.2001 Occurrence Handle11689619
D.L. Tyrrel E. Norrby (1978) ArticleTitleStructural polypeptides of measles virus J. Gen. Virol. 39 219–229 Occurrence Handle650174
M. Wagner T.D. Flanagan S. Ohki (1998) ArticleTitleEffects of anionic and nonionic polymers on fusion and binding of Sendai virus to human erythrocyte ghosts Antiviral Res. 39 113–127 Occurrence Handle10.1016/S0166-3542(98)00036-9 Occurrence Handle9806488
J.M. White (1992) ArticleTitleMembrane fusion Science 258 917–924 Occurrence Handle1439803
W. Wray T. Boulikas V.P. Wray R. Hancock (1981) ArticleTitleSilver staining of proteins in polyacrylamide gels Analytical Biochem. 118 197–203 Occurrence Handle10.1016/0003-2697(81)90179-2
L.E. Wybenga R.F. Epand S. Nir J.W.K. Chu F.J. Sharon T.D. Flanagan R. Epand (1996) ArticleTitleGlycophorin as a receptor for Sendai virus Biochemistry 35 9513–9518 Occurrence Handle10.1021/bi9606152 Occurrence Handle8755731
X. Yu X. Yuan Z. Matsuda T.H. Lee M. Essex (1992) ArticleTitleThe matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions J. Virol. 66 4966–4971 Occurrence Handle1629961
J. Zimmerberg M. Curran F.S. Cohen (1991) ArticleTitleA lipid/protein complex hypothesis for exocytotic fusion pore formation, Ann N.Y. Acad. Sci. 635 307–317
O. Zschornig K. Arnold S. Ohki (1993) ArticleTitleEffect of glycosaminoglycans and PEG on fusion of Sendai virus with phosphatidylserine vesicles Biochim. Biophys. Acta. 1148 1–6 Occurrence Handle8388724
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Ohki, S., Thacore, H. & Flanagan, T.D. Effects of Temperature on Viral Glycoprotein Mobility and a Possible Role of Internal “Viroskeleton” Proteins in Sendai Virus Fusion. J Membrane Biol 199, 73–83 (2004). https://doi.org/10.1007/s00232-004-0678-7
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DOI: https://doi.org/10.1007/s00232-004-0678-7