Vesicle formation by self-assembly of membrane-bound matrix proteins into a fluidlike budding domain

Shnyrova, Anna V.; Ayllón, Juan; Mikhalyov, Ilya; Villar, Enrique; Zimmerberg, Joshua; Frolov, Vadim A.

doi:10.1083/jcb.200705062

Cited by 53 publications

(63 citation statements)

References 39 publications

(80 reference statements)

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“…The matrix protein is also required for recruiting the nucleocapsid and glycoproteins into the virus (21). The relatively few particles that were observed to have at least a partial matrix protein layer presumably represent the virus immediately after budding, because this event requires the matrix protein arrays for the generation of membrane curvature (33). A similar observation has been hinted for the distribution of viral proteins in the organization of Sendai virus (17).…”

Section: Structural Comparison With Other Mononegavirales Matrix Protmentioning

confidence: 48%

Structure and assembly of a paramyxovirus matrix protein

Battisti

Meng

Winkler

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

120

138

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Many pleomorphic, lipid-enveloped viruses encode matrix proteins that direct their assembly and budding, but the mechanism of this process is unclear. We have combined X-ray crystallography and cryoelectron tomography to show that the matrix protein of Newcastle disease virus, a paramyxovirus and relative of measles virus, forms dimers that assemble into pseudotetrameric arrays that generate the membrane curvature necessary for virus budding. We show that the glycoproteins are anchored in the gaps between the matrix proteins and that the helical nucleocapsids are associated in register with the matrix arrays. About 90% of virions lack matrix arrays, suggesting that, in agreement with previous biological observations, the matrix protein needs to dissociate from the viral membrane during maturation, as is required for fusion and release of the nucleocapsid into the host's cytoplasm. Structure and sequence conservation imply that other paramyxovirus matrix proteins function similarly.

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Section: Structural Comparison With Other Mononegavirales Matrix Protmentioning

confidence: 48%

Structure and assembly of a paramyxovirus matrix protein

Battisti

Meng

Winkler

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

120

138

View full text Add to dashboard Cite

show abstract

“…GUVs have been effective in monitoring membrane curvature changes for the ENTH domain ( 37 ) and viral matrix proteins ( 40 ). In addition, they are relatively fl at (mean diameter, ‫ف‬ 30 M) in comparison to LUVs (mean diameter, ‫ف‬ 400 nm), so they can be used to assess if proteins induce membrane curvature changes on different membrane surfaces.…”

Section: Quantifi Cation Of Membrane Curvature Changes Using Guvsmentioning

confidence: 99%

C2 domain membrane penetration by group IVA cytosolic phospholipase A2 induces membrane curvature changes

Ward

Ropa

Adu-Gyamfi

et al. 2012

Journal of Lipid Research

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“…The M protein binds directly to the viral envelope. For most NSVs, the M protein is the primary force driving viral assembly, and the budding and formation of virus-like particles (VLPs) are critically dependent on the presence of viral M proteins (1)(2)(3)(4)(5)(6). In some NSVs, M-protein expression alone is sufficient for the formation and release of VLPs, such as the M proteins of human parainfluenza virus type 1 (7), Sendai virus (8), respiratory syncytial virus (RSV) (9), measles virus (10), Nipah virus (5), Newcastle disease virus (4), vesicular stomatitis virus (11), Ebola virus (12), and influenza A virus (13).…”

mentioning

confidence: 99%

Interaction of Human Parainfluenza Virus Type 3 Nucleoprotein with Matrix Protein Mediates Internal Viral Protein Assembly

Zhang

Zhong

Qin

et al. 2016

J Virol

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Human parainfluenza virus type 3 (HPIV3) belongs to the Paramyxoviridae family. Its three internal viral proteins, the nucleoprotein (N), the phosphoprotein (P), and the polymerase (L), form the ribonucleoprotein (RNP) complex, which encapsidates the viral genome and associates with the matrix protein (M) for virion assembly. We previously showed that the M protein expressed alone is sufficient to assemble and release virus-like particles (VLPs) and a mutant with the L305A point mutation in the M protein (M L305A ) has a VLP formation ability similar to that of wild-type M protein. In addition, recombinant HPIV3 (rHPIV3) containing the M L305A mutation (rHPIV3-M L305A ) could be successfully recovered. In the present study, we found that the titer of rHPIV3-M L305A was at least 10-fold lower than the titer of rHPIV3. Using VLP incorporation and coimmunoprecipitation assays, we found that VLPs expressing the M protein (M-VLPs) can efficiently incorporate N and P via an N-M or P-M interaction and M L305A -VLPs had an ability to incorporate P via a P-M interaction similar to that of M-VLPs but were unable to incorporate N and no longer interacted with N. Furthermore, we found that the incorporation of P into M L305A -VLPs but not M-VLPs was inhibited in the presence of N. In addition, we provide evidence that the C-terminal region of P is involved in its interaction with both N and M and N binding to the C-terminal region of P inhibits the incorporation of P into M L305A -VLPs. Our findings provide new molecular details to support the idea that the N-M interaction and not the P-M interaction is critical for packaging N and P into infectious viral particles. IMPORTANCEHuman parainfluenza virus type 3 (HPIV3) is a nonsegmented, negative-sense, single-stranded RNA virus that belongs to the Paramyxoviridae family and can cause lower respiratory tract infections in infants and young children as well as elderly or immunocompromised individuals. However, no effective vaccine has been developed or licensed. We used virus-like particle (VLP) incorporation and coimmunoprecipitation assays to determine how the M protein assembles internal viral proteins. We demonstrate that both nucleoprotein (N) and phosphoprotein (P) can incorporate into M-VLPs and N inhibits the M-P interaction via the binding of N to the C terminus of P. We also provide additional evidence that the N-M interaction but not the P-M interaction is critical for the regulation of HPIV3 assembly. Our studies provide a more complete characterization of HPIV3 virion assembly and substantiation that N interaction with M regulates internal viral organization. Human parainfluenza virus type 3 (HPIV3) is a negativestrand RNA virus (NSV) that belongs to the Paramyxoviridae family and often causes lower respiratory tract infections in infants and young children. The HPIV3 genome consists of 6 open reading frames that encode 6 structural proteins: the nucleoprotein (N), phosphoprotein (P), RNA-dependent RNA polymerase (L), matrix protein (M), and two glycoprotei...

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Vesicle formation by self-assembly of membrane-bound matrix proteins into a fluidlike budding domain

Cited by 53 publications

References 39 publications

Structure and assembly of a paramyxovirus matrix protein

Structure and assembly of a paramyxovirus matrix protein

C2 domain membrane penetration by group IVA cytosolic phospholipase A2 induces membrane curvature changes

Interaction of Human Parainfluenza Virus Type 3 Nucleoprotein with Matrix Protein Mediates Internal Viral Protein Assembly

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