The Birnavirus Crystal Structure Reveals Structural Relationships among Icosahedral Viruses

Coulibaly, F.; Chevalier, Christophe; Gutsche, Irina; Pous, Joan; Navaza, Jorge; Bressanelli, Stéphane; Delmas, Bernard; Rey, F.A.

doi:10.1016/j.cell.2005.01.009

Cited by 282 publications

(277 citation statements)

References 52 publications

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“…By contrast, z scores among homologous jelly-roll proteins from distantly related viruses are much greater (e.g., z ϭ 10-20, refs. [16][17][18][19]. Moreover, in contrast to these examples, the jelly-roll domains in viral capsids interact differently from polyhedrin jelly-roll domains in polyhedra, as described in Fig.…”

Section: Polyhedra Consist Of Disulfide-linked Tetrahedral Clusters Omentioning

confidence: 85%

The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses

Coulibaly

Chiu

Gutmann

et al. 2009

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

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Baculoviruses are ubiquitous insect viruses well known for their use as bioinsecticides, gene therapy vectors, and protein expression systems. Overexpression of recombinant proteins in insect cell culture utilizes the strong promoter of the polyhedrin gene. In infected larvae, the polyhedrin protein forms robust intracellular crystals called polyhedra, which protect encased virions for prolonged periods in the environment. Polyhedra are produced by two unrelated families of insect viruses, baculoviruses and cypoviruses. The atomic structure of cypovirus polyhedra revealed an intricate packing of trimers, which are interconnected by a projecting N-terminal helical arm of the polyhedrin molecule. Baculovirus and cypovirus polyhedra share nearly identical lattices, and the Nterminal region of the otherwise unrelated baculovirus polyhedrin protein sequence is also predicted to be ␣-helical. These results suggest homology between the proteins and a common structural basis for viral polyhedra. Here, we present the 2.2-Å structure of baculovirus polyhedra determined by x-ray crystallography from microcrystals produced in vivo. We show that the underlying molecular organization is, in fact, very different. Although both polyhedra have nearly identical unit cell dimensions and share I23 symmetry, the polyhedrin molecules are structurally unrelated and pack differently in the crystals. In particular, disulfide bonds and domain-swapped N-terminal domains stabilize the building blocks of baculovirus polyhedra and interlocking C-terminal arms join unit cells together. We show that the N-terminal projecting helical arms have different structural roles in baculovirus and cypovirus polyhedra and conclude that there is no structural evidence for a common evolutionary origin for both classes of polyhedra.in vivo crystallization ͉ molecular arms ͉ occlusion body ͉ self-assembly ͉ virus evolution

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Section: Polyhedra Consist Of Disulfide-linked Tetrahedral Clusters Omentioning

confidence: 85%

The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses

Coulibaly

Chiu

Gutmann

et al. 2009

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

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“…4, C and D show that the cis-isomerization of Pro 16 induces a reorientation of the second helix. In fact, the hydrophobic side of the second helix (16 -22) turns toward the hydrophobic side of the first helix (3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15) and the hydrophobic residues Phe 1 and Phe 3 . The trans to cis isomerization of Pro 16 results in the spatial clustering of hydrophobic residues of pep46 and thus may play an important role in membrane permeabilization.…”

Section: Visualization Of the Pores By Electronmentioning

confidence: 99%

“…Backbone atoms Heavy atoms (3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15) 0.41 Ϯ 0.18 1.49 Ϯ 0.44 (17)(18)(19)(20)(21)(22) 0.36 Ϯ 0.17 0.92 Ϯ 0.30 (3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22) 0.77 Ϯ 0.33 1.63 Ϯ 0.48 (18)(19)(20)(21)(22)(23)(24)(25)(26)(27) 0.87 Ϯ 0.39 1.14 Ϯ 0.40 (27)(28)(29)(30)…”

Section: Pairwise Rms Deviation (å)unclassified

“…The release of this peptide associated to pore formation (13) and structural rearrangements of the remaining domain of 1 (1 C) (14) are thought to lead to virus entry into the cell. Birnaviruses only possess a single-layered capsid (15) that is assumed to be competent for both virus translocation and genome replication-transcription. For all dsRNA 5 viruses, the mechanisms of membrane destabilization associated to entry remain hypothetical.…”

mentioning

confidence: 99%

“…The capsid of birnaviruses is formed by 260 VP2 protein trimers (15,16) which obey T ϭ 13laevo icosahedral symmetry (17,18). VP3, the second major viral protein, binds the RNAdependent RNA polymerase VP1 and the genomic dsRNA (19,20).…”

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confidence: 99%

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Infectious Bursal Disease Virus, a Non-enveloped Virus, Possesses a Capsid-associated Peptide That Deforms and Perforates Biological Membranes

Galloux

Libersou

Morellet

et al. 2007

Journal of Biological Chemistry

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Double-stranded RNA (dsRNA) virions constitute transcriptionally competent machines that must translocate across cell membranes to function within the cytoplasm. The entry mechanism of such non-enveloped viruses is not well described. Birnaviruses are unique among dsRNA viruses because they possess a single shell competent for entry. We hereby report how infectious bursal disease virus, an avian birnavirus, can disrupt cell membranes and enter into its target cells. One of its four structural peptides, pep46 (a 46-amino acid amphiphilic peptide) deforms synthetic membranes and induces pores visualized by electron cryomicroscopy, having a diameter of less than 10 nm. Using both biological and synthetic membranes, the pore-forming domain of pep46 was identified as its N terminus moiety (pep22). The N and C termini of pep22 are shown to be accessible during membrane destabilization and pore formation. NMR studies show that pep46 inserted into micelles displays a cis-trans proline isomerization at position 16 that we propose to be associated to the pore formation process. Reverse genetic experiments confirm that the amphiphilicity and proline isomerization of pep46 are both essential to the viral cycle. Furthermore, we show that virus infectivity and its membrane activity (probably because of the release of pep46 from virions) are controlled differently by calcium concentration, suggesting that entry is performed in two steps, endocytosis followed by endosome permeabilization. Our findings reveal a possible entry pathway of infectious bursal disease virus: in endosomes containing viruses, the lowering of the calcium concentration promotes the release of pep46 that induces the formation of pores in the endosomal membrane.

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Birnaviruses

Delmas

2015

Encyclopedia of Life Sciences

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Birnaviruses are bisegmented double‐stranded RNA viruses infecting animals belonging to different vertebrate and invertebrate phyla. Most of the research efforts on birnaviruses have focused on infectious bursal disease virus ( IBDV ), which is responsible for important losses in the poultry industry. Another economically important birnavirus is infectious pancreatic necrosis virus ( IPNV ) of salmonids. Other birnaviruses (<10) have been isolated from diseased animals, established cell lines or identified by deep sequencing. The reverse genetic systems that have been engineered for IBDV and IPNV at the end of the 1990s have been powerful tools to dissect the molecular biology of these viruses. During these past 10 years, resolution of the 3D ‐structures of several birnavirus proteins (including their unique replicase/transcriptase, their protease, their capsid protein and ultimately their complete capsid) by X‐ray radiocrystallography, NMR and cryo‐electron microscopy shed light on important properties and characteristics of these viruses. Key Concepts Birnaviruses are nonenveloped double‐stranded RNA viruses with representatives able to infect animals of invertebrate and vertebrate phyla, but not yet found infecting mammals. The birnavirus capsid possess a T = 13 laevo icosahedral symmetry. Entry of birnavirus into a cell is mediated by a capsid‐associated peptide that deforms and perforates membranes. The birnavirus virus protein 4 (VP4) protease possess a serine‐lysine catalytic dyad and is homologous to the protease domain of bacterial and organelle ATP‐dependent Lon proteases. The birnavirus capsid protein VP2 is structurally homologous to the capsid protein of positive‐strand viruses, just like the T = 3 nodaviruses and T = 4 tetraviruses. The palm subdomain‐based active site of the birnavirus RNA‐dependent RNA‐polymerases is internally permuted to the unique C‐A‐B motif arrangement, a feature shared with permutotetraviruses, a group of positive‐strand RNA viruses. The capsid proteins of birnaviruses display a high structural polymorphism of their assemblies.

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The Birnavirus Crystal Structure Reveals Structural Relationships among Icosahedral Viruses

Cited by 282 publications

References 52 publications

The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses

The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses

Infectious Bursal Disease Virus, a Non-enveloped Virus, Possesses a Capsid-associated Peptide That Deforms and Perforates Biological Membranes

Birnaviruses

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