- Open Access
Actin filaments disruption and stabilization affect measles virus maturation by different mechanisms
© Dietzel et al.; licensee BioMed Central Ltd. 2013
- Received: 3 May 2013
- Accepted: 26 July 2013
- Published: 2 August 2013
Cytoskeletal proteins are often involved in the virus life cycle, either at early steps during virus entry or at later steps during formation of new virus particles. Though actin filaments have been shown to play a role in the production of measles virus (MV), the importance of actin dynamics for virus assembly and budding steps is not known yet. Aim of this work was thus to analyze the distinctive consequences of F-actin stabilization or disruption for MV protein trafficking, particle assembly and virus release.
MV infection studies in the presence of inhibitors differently affecting the actin cytoskeleton revealed that not only actin disruption but also stabilization of actin filaments interfered with MV particle release. While overall viral protein synthesis, surface expression levels of the MV glycoproteins, and cell-associated infectivity was not altered, cell-free virus titers were decreased. Interestingly, the underlying mechanisms of interference with late MV maturation steps differed principally after F-actin disruption by Cytochalasin D (CD) and F-actin stabilization by Jasplakinolide (Jaspla). While intact actin filaments were shown to be required for transport of nucleocapsids and matrix proteins (M-RNPs) from inclusions to the plasma membrane, actin dynamics at the cytocortex that are blocked by Jaspla are necessary for final steps in virus assembly, in particular for the formation of viral buds and the pinching-off at the plasma membrane. Supporting our finding that F-actin disruption blocks M-RNP transport to the plasma membrane, cell-to-cell spread of MV infection was enhanced upon CD treatment. Due to the lack of M-glycoprotein-interactions at the cell surface, M-mediated fusion downregulation was hindered and a more rapid syncytia formation was observed.
While stable actin filaments are needed for intracellular trafficking of viral RNPs to the plasma membrane, and consequently for assembly at the cell surface and prevention of an overexerted fusion by the viral surface glycoproteins, actin dynamics are required for the final steps of budding at the plasma membrane.
- Measles virus
- Actin dynamics
Measles virus (MV) is a prototype member of the Morbillivirus genus in the family Paramyxoviridae. In virus particles, the negative-stranded RNA genome is encapsidated by the N, P and L proteins, and this ribonucleocapsid (RNP) is surrounded by a lipid bilayer. The two surface glycoproteins, the hemagglutinin H and the fusion protein F, protrude from the viral envelope. The matrix protein (M) is located at the inner surface of the lipid bilayer tethering the RNP to the envelope. Due to its interaction with the glycoproteins and the RNPs, the M protein is essential for MV assembly and particle formation. M binding to the cytoplasmic tails of the glycoproteins at the surface of infected cells is furthermore required to downregulate H/F-mediated cell-to-cell fusion of infected and neighboring uninfected cells [1–5].
The actin network is primarily associated with mechanical stability, cell motility and cell contraction. It is also important for chromosome movement during mitosis and for internal transport, particularly near the plasma membrane. Cargos can be transported either by riding on myosin motors along actin filaments or by pushing forces exerted by actin as it undergoes polymerization . Cytoskeletal actin not only has a central function in cell physiology but is also an essential component involved in the replication of many RNA and DNA viruses. The molecular mechanisms underlying this important host-virus interaction, however, are extremely diverse . For MV, several reports have shown that actin is involved in virus maturation at the plasma membrane. This idea was initially based on the findings that actin was identified as an internal component of MV particles [8, 9] and co-caps with MV H on infected cells . There is further ultrastructural evidence that actin filaments take part in the process of budding and protrude into viral buds [7, 8]. Very recently, it was furthermore proposed that F-actin associates with the MV M protein altering the interaction between M and H, hereby modulating MV cell-cell fusion and assembly .
Though there is conclusive evidence that intact actin filaments are important for MV replication, it is not yet defined if a stable actin cytoskeleton is sufficient, or if actin dynamics are required. Aim of this study was thus to analyze the effects of actin-disrupting and actin-stabilizing drugs to define if actin filaments as structural components or rather actin dynamics and treadmilling are essential for MV maturation. Actin treadmilling is a process in which actin filament length remains approximately constant but actin monomers preferentially join with the barbed ends and dissociate from the pointed ends of filaments. This oriented renewal of actin within microfilaments causes a treadmilling involving both, actin monomers and actin-binding proteins. Jasplakinolide (Jaspla) is a cyclic peptide isolated from a marine sponge that binds to and stabilizes filamentous actin, inducing a blockade of actin treadmilling [12, 13]. In contrast to Jaspla, Cytochalasin D (CD), a fungal metabolite, serves as an actin capping compound that binds to the barbed (+) end of actin filaments and shifts the polymerization-depolymerization equilibrium towards depolymerization of F-actin .
With our studies on MV replication in the presence of CD and Jaspla, we show that defects in actin polymerisation and defects in actin depolymerisation can both interfere with late virus assembly and budding steps without impairing overall viral protein synthesis, cell-associated infectivity or the surface transport of the MV glycoproteins. Most interestingly, the underlying mechanism of interference with late MV maturation steps by CD and Jaspla differs principally. While intact actin filaments that can be disrupted by CD treatment are required for M-RNP cotransport from the cytoplasm to the plasma membrane, actin dynamics at the cytocortex blocked by Jaspla are necessary for later steps in virus maturation at the plasma membrane. Supporting our finding that actin disruption blocks M-RNP transport to the plasma membrane, cell-to-cell spread of MV infection was enhanced upon CD treatment. Due to the lack of M-glycoprotein-interaction at the cell surface, M-mediated fusion downregulation is hindered and a more rapid syncytia formation is observed in CD-treated cells.
Actin disruption and stabilization affect virus release without influencing the amount of cell-associated infectivity
Viral protein expression is not altered upon inhibitor treatment
Cytochalasin D but not Jasplakinolide treatment leads to retention of M-RNP complexes in the cytoplasm
Actin disruption by Cytochalasin D increases cell-to-cell fusion
Actin stabilization by Jasplakinolide affects late MV maturation steps
Consistent with an earlier report using Cytochalasin B , we found that CD inhibited MV replication. Actin inhibitors specifically seem to block late virus assembly and budding steps, because inhibition of earlier replication steps such as RNA synthesis would be reflected in decreased overall virus protein expression levels and reduced titers of both, released virus and cell-associated infectivity. After actin disruption by CD, M-RNP complexes were retained in the cytoplasm implicating a role for intact actin filaments in M-RNP transport. Consistent with M acting as a fusion downregulator, we found an increased cell-to-cell fusion after actin disruption due to the lack of M-glycoprotein interaction at the plasma membrane. Similar to actin disruption, actin stabilization by Jaspla led to decreased cell-free virus titers. However, the underlying molecular mechanism is clearly different. Block of actin dynamics by Jaspla did not result in the intracellular retention of M-RNP complexes. Immunofluorescence and electron microscopic observations rather indicate a defect in bud formation and subsequent pinching-off.
Actin filaments (disrupted by CD) but not actin treadmilling (blocked by Jaspla) are needed for transport of M and MV nucleocapsids from the cytoplasm to the cell surface. Yet, actin dynamics seem to play a role in budding of mature virions at the plasma membrane. Even if an early report in chronically MV-infected cells had suggested that RNP but not the M transport to the cell surface depends on intact actin filaments , we and others have shown in more recent studies that M interacts with RNPs in viral inclusions and movement of viral RNPs to the plasma membrane occurs as co-transport with the M protein [5, 20, 21]. In agreement with the idea that actin filaments serve as tracks for movement of M-coated RNPs to the cell surface, disruption of the actin filaments resulted in an intracellular retention of both, M and RNPs. A very recent report proposes that interaction with the cytoskeleton is mediated by direct binding of F-actin to phenylalanine 50 in the M protein . The direct interaction of MV M and actin is in line with findings for the M proteins of Newcastle disease virus and Sendai virus  that also serve as the recognition site for actin. However, it remains to be elucidated if M binds directly to actin, or if interaction is mediated via motor proteins. The latter might be supported by our finding that Jaspla treatment did not affect the M-RNP trafficking to the cell periphery. While movement along non-dynamic actin filaments must be assumed to be less efficient, motor proteins would still be able to transport cargo (M-RNPs) along stabilized actin filaments.
In contrast to many other viral matrix proteins , MV M protein does not possess any known late domain motif. Therefore budding does not depend on the cellular endosomal sorting complex required for transport (ESCRT) machinery . Given that MV M-RNPs interact with the actin cytoskeleton and that the actin motor protein Myosin Vb interacts with members of the Rab11 family , a mechanism of late domain independent budding might be used by MV. The idea of a M-Rab11 interaction is indeed supported by the very recent finding that apical release from polarized epithelial cells depends on the Rab11A-dependent apical recycling endosomal pathway .
Multifunctional involvement of actin microfilaments during viral infection has been documented in many studies. Dependence of viruses on actin, however, differs drastically not only between different DNA and RNA virus families, but even between closely related virus family members. Thus, it must be concluded that each virus has evolved its own mechanism to interact with the cellular cytoskeleton machinery ensuring optimal replication. In contrast to our findings, HPIV-3 needs intact actin filaments for viral RNA synthesis . Consequently, actin disruption led to a reduction of HPIV-3 release due to lack of viral proteins. For the budding process of HPIV-3, microtubules rather than actin filaments are important . Since Cytochalasin B had no negative effect on VSV release, it was supposed that actin is not involved in VSV replication . However, interaction of VSV M with dynamin was recently shown to be required for assembly . Treatment of Rotavirus infected polarized epithelial cells with Jaspla did not reduce overall virus release but altered the budding polarity from apical to bipolar . MV is also released apically from polarized epithelia [31–33], but actin treadmilling does not seem to play a role in polarized MV release since treatment of MV-infected polarized MDCK cells with Jaspla did not alter budding polarity (Dietzel, unpublished observation).
As in MV infection, disruption of the actin cytoskeleton reduced release and viral infectivity of HIV . Recent cryo electron tomography studies have shown that HIV budding at the plasma membrane can be divided into different categories with respect to their actin context . Even if most of the budding sites were found adjacent to filamentous actin, only half of them were associated with filopodia-like structures characterized by a parallel actin organization. The rest of the buds were found with cortical actin parallel to the plasma membrane, or with cortical actin directed towards or protruding into the budding site. Even if actin filaments have been shown to protrude into budding MV particles [8, 18], one might speculate that highly pleomorphic MV particles also bud in different forms. Though we cannot rule out that the only partial block of virus release observed upon Jaspla treatment is due to an incomplete stabilization of actin filaments at the used concentrations, it might be speculated that only budding forms that have a distinctive requirement for actin dynamics or treadmilling are affected by cytocortical actin stabilization.
Recent observations have shown that the interaction of the MV glycoprotein complex with receptors on lymphocytes and dendritic cells (DCs) initiate cytoskeletal dynamics. In DCs, MV binding initiates host cell cytoskeletal dynamics needed for viral uptake and the establishment of functional synapses with T cells. Furthermore, MV binding to T cells causes a loss of polarization, adhesion and motility by actin cytoskeletal paralysis . It is therefore highly likely that integrity and dynamics of actin filaments not only play an important role in virus maturation at the plasma membrane, but are also involved in MV-mediated immunosuppression.
This paper demonstrates that intact actin filaments are required for M-RNP transport to the plasma membrane, and are thus needed to initiate assembly at the plasma membrane and to downregulate cell-to-cell fusion mediated by surface-expressed viral glycoproteins. We furthermore provide first conclusive evidence that actin dynamics are critically required in later steps in MV maturation, particularly for bud formation and the final pinching-off.
Cells and viruses
MDCK cells were cultured and infected in Minimal Essential Medium (MEM) supplemented with 10% fetal calf serum (FCS), Penicillin and Streptomycin. Vero cells were maintained in Dulbecco’s MEM supplemented with 10% FCS and antibiotics. Cells were infected during seeding with the MV Edmonston strain at an MOI of 10 (MDCK cells) or an MOI of 1 (Vero cells), respectively.
Inhibitor treatment and virus growth analysis
Inhibitor stocks were prepared in DMSO at concentrations of 4 mM Cytochalasin D (Sigma-Aldrich) and 0.1 mM Jasplakinolide (Calbiochem), respectively. Different dilutions of the inhibitors were assessed (1–4 μM CD and 50–200 nM Jaspla) to determine appropriate working concentrations that have maximal effects on the actin cytoskeleton without causing a loss of cell viability. In all experiments, 4 μM CD were used. Jaspla was used in a concentration of 100 nM and 200 nM for MDCK and Vero cells, respectively. Inhibitors were diluted to final concentrations in cell culture medium with 2% FCS and added to infected cells at 12 h p.i.. To prevent syncytia formation in MV-infected cells, a fusion inhibitory peptide (FIP, Bachem) was added at a concentration of 0.1 mM . Cell supernatants were taken at 24, 36, 48, 60 and 72 h p.i. for plaque titration. To determine cell-associated infectivity at 24, 48 and 72 h p.i., cells were scraped into OptiMEM (Invitrogen). After one freeze-thaw cycle using liquid nitrogen and a 37°C water bath, lysates were clarified by low-speed centrifugation, and the supernatant was used for plaque titration.
Inhibitor-treated and control cells grown on Permanox ChamberSlides were immunostained at 48 h p.i.. To stain filamentous actin, cells were fixed with 2% paraformaldehyde (PFA) in DMEM for 15 min and subsequently permeabilized with 0.2% Triton X-100 in PBS for 10 min at room temperature. Filamentous actin was detected using 12.5 μg/ml Phalloidin-FITC (Sigma-Aldrich). M and N protein costaining was performed as described previously . Briefly, cells were fixed and permeabilized with cold methanol/acetone (1:1) for 5 min. Cells were then incubated with a mouse monoclonal M-antibody (MAB8910, Millipore) and an N-specific polyclonal rabbit antiserum. Primary antibodies were detected using AF568- or 488-coupled secondary antibodies, respectively. For costaining of M and H, cell were fixed with 2% PFA and permeabilized with 0.2% Triton X-100. H protein was detected using a monoclonal antibody from mouse and an AF488-labeled secondary antibody. Subsequently, a saturation step with 5% mouse serum was performed. To stain the M protein, the M specific monoclonal antibody MAB8910 was labeled with AF555 using a Zenon labeling kit (Invitrogen) and added to the cells for 60 min on ice. Finally, cells were mounted in Mowiol and confocal fluorescence images were recorded using a Zeiss Axioplan2 LSM510.
Surface biotinylation and western blot analysis
At 48 h p.i., infected and inhibitor-treated MDCK cells were surface biotinylated using S-NHS-Biotin (Calbiochem) as described earlier . For actin, tubulin and MV-N staining, cell lysates were directly subjected to SDS-PAGE and transferred to nitrocellulose. Actin and tubulin were detected using specific mouse antibodies (Sigma-Aldrich, dilution 1:1000) and an AF680-coupled secondary antibody (Invitrogen, dilution 1:5000). N was detected using an N-specific rabbit polyclonal antiserum  at a dilution of 1:1000, and an IRDye800-conjugated secondary antibody (Biomol, dilution 1:5000). Residual supernatants were divided into three parts and used for immunoprecipitation of M, H and F. H was precipitated by K83 , F was precipitated with an Fcyt antiserum , and M was precipitated by incubation with MAB8910. After addition of 20 μl of a suspension of protein A-sepharose CL-4B (Sigma-Aldrich), immuncomplexes were washed and subjected to SDS-PAGE under reducing conditions. After blotting to nitrocellulose, M was detected using MAB8910 and an AF680-conjugated secondary antibody. Immunoprecipitated and surface-biotinylated H and F proteins were detected using Streptavidin-AF680. Labelled proteins were detected by the Odyssey infrared-imaging system (LI-COR).
MDCK cells were grown to 80% confluency and then cotransfected with pCG-MV H and pCG-MV F  using Lipofectamine 2000 (Invitrogen) according to the manufacturer’s protocol. Inhibitors and FIP were added in MEM 2% FCS at 6 h p.t. and cells were further incubated for 18 h (24 h p.t.).
MDCK cells were either infected with MV, or were cotransfected with MV-H and F in the presence of FIP, to prevent fusion. Inhibitors were added at the times indicated. At 48 h p.i. or 24 h post transfection, cells were detached by accutase (Sigma-Aldrich). Untreated Vero cells were also detached using accutase and mixed with MDCK cells at a ratio of 3:1 for infected, and 30:1 for transfected MDCK cells. Cocultures were incubated in DMEM 10% FCS for 5 h in the absence of FIP to allow fusion. Then, cells were fixed and stained by a 1:10-diluted Giemsa staining solution. Cell-to-cell fusion was quantified as described previously  by counting and averaging the number of nuclei of 20 randomly chosen syncytia.
MV-infected cells were fixed for ultrastructural analysis cells by adding a 2× fixation solution containing 0.2 M PHEM [120 mM piperazine-N,N=−bis(2-ethanesulfonic acid) (PIPES), 50 mM HEPES, 4 mM MgCl2, 20 mM EGTA (pH6.9)], 8% PFA and 0.2% glutaraldehyde to the medium. After incubation for 30 min at room temperature, cells were scraped off and pelleted. The supernatant was discarded and 4% PFA in DMEM was added to the cell pellet. Subsequently, samples were processed as described previously . Briefly, cells were postfixed for 60 min with 1% osmium tetroxide in 50 mM HEPES buffer (pH7.5). After washings, samples were stained overnight in a 2% aqueous uranyl acetate solution. Then, cells were dehydrated, and embedded in a mixture of Epon and Araldite. Ultrathin sections of the cells were stained with uranyl acetate and lead citrate and analyzed by using a JEM 1400 transmission electron microscope at 120 kV.
We thank Roberto Cattaneo (Rochester, USA) and Jürgen Schneider-Schaulies (Würzburg, Germany) for providing MV-specific antibodies. This work was funded by grants of the German Research Foundation (DFG; MA 1886/6-1; SFB 593 TP B11).
- Cathomen T, Mrkic B, Spehner D, Drillien R, Naef R, Pavlovic J, Aguzzi A, Billeter MA, Cattaneo R: A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J 1998, 17: 3899-3908.PubMedPubMed CentralView ArticleGoogle Scholar
- Cathomen T, Naim HY, Cattaneo R: Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 1998, 72: 1224-1234.PubMedPubMed CentralGoogle Scholar
- Moll M, Klenk HD, Maisner A: Importance of the cytoplasmic tails of the measles virus glycoproteins for fusogenic activity and the generation of recombinant measles viruses. J Virol 2002, 76: 7174-7186.PubMedPubMed CentralView ArticleGoogle Scholar
- Tahara M, Takeda M, Yanagi Y: Altered interaction of the matrix protein with the cytoplasmic tail of hemagglutinin modulates measles virus growth by affecting virus assembly and cell-cell fusion. J Virol 2007, 81: 6827-6836.PubMedPubMed CentralView ArticleGoogle Scholar
- Runkler N, Pohl C, Schneider-Schaulies S, Klenk HD, Maisner A: Measles virus nucleocapsid transport to the plasma membrane requires stable expression and surface accumulation of the viral matrix protein. Cell Microbiol 2007, 9: 1203-1214.PubMedView ArticleGoogle Scholar
- Welch MD, Mullins RD: Cellular control of actin nucleation. Annu Rev Cell Dev Biol 2002, 18: 247-288.PubMedView ArticleGoogle Scholar
- Taylor MP, Koyuncu OO, Enquist LW: Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 2011, 9: 427-439.PubMedPubMed CentralView ArticleGoogle Scholar
- Bohn W, Rutter G, Hohenberg H, Mannweiler K, Nobis P: Involvement of actin filaments in budding of measles virus: studies on cytoskeletons of infected cells. Virology 1986, 149: 91-106.PubMedView ArticleGoogle Scholar
- Moyer SA, Baker SC, Horikami SM: Host cell proteins required for measles virus reproduction. J Gen Virol 1990,71(Pt 4):775-783.PubMedView ArticleGoogle Scholar
- Sundqvist KG, Ehrnst A: Cytoskeletal control of surface membrane mobility. Nature 1976, 264: 226-231.PubMedView ArticleGoogle Scholar
- Wakimoto H, Shimodo M, Satoh Y, Kitagawa Y, Takeuchi K, Gotoh B, Itoh M: F-actin modulates measles virus cell-cell fusion and assembly by altering the interaction between the matrix protein and the cytoplasmic tail of hemagglutinin. J Virol 2013, 87: 1974-1984.PubMedPubMed CentralView ArticleGoogle Scholar
- Bubb MR, Senderowicz AM, Sausville EA, Duncan KL, Korn ED: Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 1994, 269: 14869-14871.PubMedGoogle Scholar
- Gardet A, Breton M, Trugnan G, Chwetzoff S: Role for actin in the polarized release of rotavirus. J Virol 2007, 81: 4892-4894.PubMedPubMed CentralView ArticleGoogle Scholar
- Lin DC, Tobin KD, Grumet M, Lin S: Cytochalasins inhibit nuclei-induced actin polymerization by blocking filament elongation. J Cell Biol 1980, 84: 455-460.PubMedView ArticleGoogle Scholar
- Lázaro-Diéguez F, Aguado C, Mato E, Sánchez-Ruíz Y, Esteban I, Alberch J, Knecht E, Egea G: Dynamics of an F-actin aggresome generated by the actin-stabilizing toxin jasplakinolide. J Cell Sci 2008, 121: 1415-1425.PubMedView ArticleGoogle Scholar
- Chernomordik LV, Sowers AE: Evidence that the spectrin network and a nonosmotic force control the fusion product morphology in electrofused erythrocyte ghosts. Biophys J 1991, 60: 1026-1037.PubMedPubMed CentralView ArticleGoogle Scholar
- Schowalter RM, Wurth MA, Aguilar HC, Lee B, Moncman CL, McCann RO, Dutch RE: Rho GTPase activity modulates paramyxovirus fusion protein-mediated cell-cell fusion. Virology 2006, 350: 323-334.PubMedView ArticleGoogle Scholar
- Stallcup KC, Raine CS, Fields BN: Cytochalasin B inhibits the maturation of measles virus. Virology 1983, 124: 59-74.PubMedView ArticleGoogle Scholar
- Tyrrell DL, Ehrnst A: Transmembrane communication in cells chronically infected with measles virus. J Cell Biol 1979, 81: 396-402.PubMedView ArticleGoogle Scholar
- Riedl P, Moll M, Klenk HD, Maisner A: Measles virus matrix protein is not cotransported with the viral glycoproteins but requires virus infection for efficient surface targeting. Virus Res 2002, 83: 1-12.PubMedView ArticleGoogle Scholar
- Iwasaki M, Takeda M, Shirogane Y, Nakatsu Y, Nakamura T, Yanagi Y: The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol 2009, 83: 10374-10383.PubMedPubMed CentralView ArticleGoogle Scholar
- Giuffre RM, Tovell DR, Kay CM, Tyrrell DL: Evidence for an interaction between the membrane protein of a paramyxovirus and actin. J Virol 1982, 42: 963-968.PubMedPubMed CentralGoogle Scholar
- Ren X, Hurley JH: Proline-rich regions and motifs in trafficking: from ESCRT interaction to viral exploitation. Traffic 2011, 12: 1282-1290.PubMedPubMed CentralView ArticleGoogle Scholar
- Salditt A, Koethe S, Pohl C, Harms H, Kolesnikova L, Becker S, Schneider-Schaulies S: Measles virus M protein-driven particle production does not involve the endosomal sorting complex required for transport (ESCRT) system. J Gen Virol 2010, 91: 1464-1472.PubMedView ArticleGoogle Scholar
- Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO, Provance DW, Mercer JA, Bähler M, Goldenring JR: Myosin vb is associated with plasma membrane recycling systems. Mol Biol Cell 2001, 12: 1843-1857.PubMedPubMed CentralView ArticleGoogle Scholar
- Nakatsu Y, Ma X, Seki F, Suzuki T, Iwasaki M, Yanagi Y, Komase K, Takeda M: Intracellular transport of the measles virus ribonucleoprotein complex is mediated by Rab11A-positive recycling endosomes and drives virus release from the apical membrane of polarized epithelial cells. J Virol 2013, 87: 4683-4693.PubMedPubMed CentralView ArticleGoogle Scholar
- Gupta S, De BP, Drazba JA, Banerjee AK: Involvement of actin microfilaments in the replication of human parainfluenza virus type 3. J Virol 1998, 72: 2655-2662.PubMedPubMed CentralGoogle Scholar
- Bose S, Malur A, Banerjee AK: Polarity of human parainfluenza virus type 3 infection in polarized human lung epithelial A549 cells: role of microfilament and microtubule. J Virol 2001, 75: 1984-1989.PubMedPubMed CentralView ArticleGoogle Scholar
- Griffin JA, Compans RW: Effect of cytochalasin B on the maturation of enveloped viruses. J Exp Med 1979, 150: 379-391.PubMedView ArticleGoogle Scholar
- Raux H, Obiang L, Richard N, Harper F, Blondel D, Gaudin Y: The matrix protein of vesicular stomatitis virus binds dynamin for efficient viral assembly. J Virol 2010, 84: 12609-12618.PubMedPubMed CentralView ArticleGoogle Scholar
- Blau DM, Compans RW: Entry and release of measles virus are polarized in epithelial cells. Virology 1995, 210: 91-99.PubMedView ArticleGoogle Scholar
- Maisner A, Klenk H, Herrler G: Polarized budding of measles virus is not determined by viral surface glycoproteins. J Virol 1998, 72: 5276-5278.PubMedPubMed CentralGoogle Scholar
- Naim HY, Ehler E, Billeter MA: Measles virus matrix protein specifies apical virus release and glycoprotein sorting in epithelial cells. EMBO J 2000, 19: 3576-3585.PubMedPubMed CentralView ArticleGoogle Scholar
- Jolly C, Mitar I, Sattentau QJ: Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J Virol 2007, 81: 5547-5560.PubMedPubMed CentralView ArticleGoogle Scholar
- Carlson LA, De Marco A, Oberwinkler H, Habermann A, Briggs JA, Kräusslich HG, Grünewald K: Cryo electron tomography of native HIV-1 budding sites. PLoS Pathog 2010, 6: e1001173.PubMedPubMed CentralView ArticleGoogle Scholar
- Avota E, Gassert E, Schneider-Schaulies S: Cytoskeletal dynamics: concepts in measles virus replication and immunomodulation. Viruses 2011, 3: 102-117.PubMedPubMed CentralView ArticleGoogle Scholar
- Runkler N, Dietzel E, Moll M, Klenk HD, Maisner A: Glycoprotein targeting signals influence the distribution of measles virus envelope proteins and virus spread in lymphocytes. J Gen Virol 2008, 89: 687-696.PubMedView ArticleGoogle Scholar
- Maisner A, Mrkic B, Herrler G, Moll M, Billeter MA, Cattaneo R, Klenk HD: Recombinant measles virus requiring an exogenous protease for activation of infectivity. J Gen Virol 2000, 81: 441-449.PubMedView ArticleGoogle Scholar
- Cathomen T, Buchholz CJ, Spielhofer P, Cattaneo R: Preferential initiation at the second AUG of the measles virus F mRNA: a role for the long untranslated region. Virology 1995, 214: 628-632.PubMedView ArticleGoogle Scholar
- Thiel L, Diederich S, Erbar S, Pfaff D, Augustin HG, Maisner A: Ephrin-B2 expression critically influences nipah virus infection independent of its cytoplasmic tail. Virol J 2008, 5: 163.PubMedPubMed CentralView ArticleGoogle Scholar
- Lamp B, Dietzel E, Kolesnikova L, Sauerhering L, Erbar S, Weingartl H, Maisner A: Nipah virus entry and egress from polarized epithelial cells. J Virol 2013, 87: 3143-3154.PubMedPubMed CentralView ArticleGoogle Scholar
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