External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice

Szajner, Patricia; Weisberg, Andrea S.; Lebowitz, Jacob; Heuser, John E.; Moss, Bernard

doi:10.1083/jcb.200504026

Cited by 90 publications

(103 citation statements)

References 36 publications

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“…350 nm surrounded by an envelope consistent with one single membrane (Figures 1 and 2). This membrane is covered in the convex side by a thick (10 nm) layer of spikes, built by protein D13L (Dales and Mosbach, 1968;Grimley et al, 1970;Sodeik et al, 1994;Heuser, 2005;Szajner et al, 2005;Hyun et al, 2007). Nevertheless, this membrane is not fully continuous, and small overlapping areas could be found (Figures 1 and 2).…”

Section: Discussionmentioning

confidence: 99%

“…The fact that these membranes are devoid of the putative spike protein D13L suggests that this type of local curvature might be an intrinsic property of the viral membranes, which became flatter upon incorporation of the spikes. Actually, the presence of trimeric D13L spikes has been related to the generation of membrane curvature and rigidity (Dales and Mosbach, 1968;Heuser, 2005;Szajner et al, 2005;Hyun et al, 2007). It is thus tempting to suggest that the progressive disintegration of the spike palisade during the maturation Mohandas and Dales, 1995;Heuser, 2005), might be coupled to the loss of rigidity of the viral envelope.…”

Section: Discussionmentioning

confidence: 99%

“…The membranes near the condensation showed distortions and some discontinuities (Figures 2B and 2C, and Supplementary Movies 3 and 4 at http://www.biolcell.org/boc/101/ boc1010401add.htm). IVN particles also presented spikes, but, in this case, the coverage by the spike protein [D13L Heuser, 2005;Szajner et al, 2005)] was not continuous along the viral membrane (as shown in Figure 2D). The tomographic reconstructions allowed us to follow a spike palisade surrounding a well-swollen membrane (Figure 2D, area enclosed between green arrowheads, and Figure 2E), whereas, in other areas with membranes showing a more waved aspect, the spikes were not so well ordered ( Figure 2D, area between orange arrowheads, and Figure 2E).…”

Section: Ivn Structurementioning

confidence: 99%

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Membrane remodelling during vaccinia virus morphogenesis

Chichón

Rodriguez

Risco

et al. 2009

Biology of the Cell

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Background information. VACV (vaccinia virus) is one of the most complex viruses, with a size exceeding 300 nm and more than 100 structural proteins. Its assembly involves sequential interactions and important rearrangements of its structural components.Results. We have used electron tomography of sections of VACV-infected cells to follow, in three dimensions, the remodelling of the membrane components of the virus during envelope maturation. The tomograms obtained suggest that a number of independent 'crescents' interact with each other to enclose the volume of an incomplete ellipsoid in the viral factory area, attaining the overall shape and size characteristic of the first immature form of the virus [IV (immature virus)]. The incorporation of the DNA into these forms leads to particles with a nucleoid [IVN (IV with nucleoid)] that results in local disorganization of the envelope in regions near the condensed DNA. These particles suffer the progressive disappearance of the membrane outer spikes with a change in the shape of the membrane, becoming locally curled. The transformation of the IVN into the mature virus involves an extreme rearrangement of the particle envelope, which becomes fragmented and undulated. During this process, we also observed connections between the outer membranes with internal ones, suggesting that the latter originate from internalization of the IV envelope.Conclusions. The main features observed for VACV membrane maturation during morphogenesis resemble the breakdown and reassembly of cellular endomembranes.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Ivn Structurementioning

confidence: 99%

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Membrane remodelling during vaccinia virus morphogenesis

Chichón

Rodriguez

Risco

et al. 2009

Biology of the Cell

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“…4A, the mAb to HA decorated the perimeter of the IV as well as tubules near the IVs. (Note that the ring of labeling frequently appears to be inside the perimeter of the IV because of the thickness of the section and the exclusive labeling of the cut surface of the spherical particle as described (29). In Fig.…”

Section: Immunoelectron Microscopy Of Er-derived Tubules In Proximitymentioning

confidence: 99%

Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane

Husain

Weisberg

Moss

2006

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

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In thin sections of cells infected with vaccinia virus or other poxviruses, the viral membrane is first discerned as a crescent or circle lacking obvious continuity with a cellular organelle, presenting an appearance of de novo membrane biogenesis. This notion, which many consider heretical, is nevertheless consistent with the absence of a signature of endoplasmic reticulum (ER) trafficking, such as signal peptide cleavage or glycosylation, in any of the numerous viral membrane proteins. The purpose of this study was to determine whether an operative pathway exists between the ER and the immature virion membrane. We showed that the highly conserved A9 viral membrane protein was inserted into the ER of uninfected cells with the same topology as in viral membranes. Next, we found that replacement of the nonessential cytoplasmic tail of A9 with one containing COPII-binding sites reduced incorporation of the modified A9 into viral membranes and led to its accumulation in the Golgi apparatus, implying that A9 was inserted into the ER and then diverted from its natural path. Most importantly, we demonstrated cleavage of a heterologous signal peptide fused to the N-terminal region of A9 and localized the truncated protein in immature and mature virions. Additionally, immunoelectron micrographs showed A9 in tubules containing protein disulfide isomerase, an ER lumenal protein, near immature viral membranes. The present data provide strong evidence for an operative pathway from ER domains within the virus factory to the viral membrane. membrane protein trafficking ͉ vaccinia virus ͉ virus assembly

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“…While antibodies to envelope proteins were expected, we were surprised by how many of the immunodominant antigens were non-surface virion proteins or proteins found predominantly in infected cells. A significant component of the response is directed against core proteins (I1, L4, A10), and proteins that assist with viral morphogenesis (D13, A11) [15,16]. A second criterion for determining immunodominance, in addition to frequency of recognition, was array SI.…”

Section: Antibodies To Structural Proteins Dominate Primary and Seconmentioning

confidence: 99%

Proteome‐wide analysis of the serological response to vaccinia and smallpox

Molina²,

et al. 2007

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The eradication of smallpox by vaccination with vaccinia virus was probably one of the greatest achievements of vaccinology. However, the immunological basis of this protection is not fully understood. To this end, we have used protein microarrays of the vaccinia (Western Reserve, WR) proteome to profile antibody reactivities after primary infection or boosting with the licensed smallpox vaccine, Dryvax ® , and with archival convalescent smallpox sera. Some 25 antigens were consistently recognized by Dryvax ® sera, of which half were envelope proteins (notably, H3, A13, B5, and D8). The remainder consisted mainly of core proteins (e.g. A10, L4, and I1), proteins involved in intracellular morphogenesis (A11, D13), and the A-type inclusion protein, WR148. Convalescent smallpox sera also detected vaccinia antigens on the array, consistent with the notion that there is serological cross-reactivity between these two orthopox species that underlies protection. Moreover, the profiles of immunodominant antigens recognized by variola-infected individuals and Dryvax ® vaccinees were indistinguishable. This is the first description of antibody-specificity profiles induced after smallpox infection. The array data indicate that a significant component of the antibody response is not involved in virus neutralization, although these antigens should be considered alongside the envelope proteins as potential candidates for diagnostic and vaccine applications.

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External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice

Cited by 90 publications

References 36 publications

Membrane remodelling during vaccinia virus morphogenesis

Membrane remodelling during vaccinia virus morphogenesis

Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane

Proteome‐wide analysis of the serological response to vaccinia and smallpox

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