From structure of the complex to understanding of the biology

Michael G Rossmann,Marc C Morais,Andrei Fokine,Laura M Palermo,Petr G Leiman,Mikhail M Shneider,Anthony J Battisti,Vadim V Mesyanzhinov,Victor A Kostyuchenko,Shuji Kanamaru,Colin R Parrish,Valorie D Bowman,Susan Hafenstein,Chuan Xiao,Paul R Chipman,Fumio Arisaka

doi:10.1107/s0907444906047330

Abstract

The most extensive structural information on viruses relates to apparently icosahedral virions and is based on X-ray crystallography and on cryo-electron microscopy (cryo-EM) single-particle reconstructions. Both techniques lean heavily on imposing icosahedral symmetry, thereby obscuring any deviation from the assumed symmetry. However, tailed bacteriophages have icosahedral or prolate icosahedral heads that have one obvious unique vertex where the genome can enter for DNA packaging and exit when infecting a host cell. The presence of the tail allows cryo-EM reconstructions in which the special vertex is used to orient the head in a unique manner. Some very large dsDNA icosahedral viruses also develop special vertices thought to be required for infecting host cells. Similarly, preliminary cryo-EM data for the small ssDNA canine parvovirus complexed with receptor suggests that these viruses, previously considered to be accurately icosahedral, might have some asymmetric properties that generate one preferred receptor-binding site on the viral surface. Comparisons are made between rhinoviruses that bind receptor molecules uniformly to all 60 equivalent binding sites, canine parvovirus, which appears to have a preferred receptor-binding site, and bacteriophage T4, which gains major biological advantages on account of its unique vertex and tail organelle.

Highlights

There are two themes which underlie this paper: the power of combining X-ray crystallography with cryo-electron microscopy and the role played by specialized vertices in otherwise highly symmetrical icosahedral viruses
Structural virologists have been accustomed to thinking of many viruses as having perfect icosahedral symmetry, the breakdown of icosahedral symmetry has been recorded for Mimvirus (Fig. 1a; Xiao et al, 2005) and for Paramecium bursaria chlorella virus type 1 (PBCV-1; Nandhagopal et al, 2002; Yan et al, 2000; Fig. 1b)
The -barrel has large insertions between -strands. These insertions form most of the capsid surface and create small protruding ‘spikes’ around the icosahedral threefold axes in canine parvovirus (CPV; Tsao et al, 1991) and feline panleukopenia virus (FPV; Agbandje et al, 1993)

Summary

Introduction

There are two themes which underlie this paper: the power of combining X-ray crystallography with cryo-electron microscopy (cryo-EM) and the role played by specialized vertices in otherwise highly symmetrical icosahedral viruses. Structural virologists have been accustomed to thinking of many viruses as having perfect icosahedral symmetry, the breakdown of icosahedral symmetry has been recorded for Mimvirus (Fig. 1a; Xiao et al, 2005) and for Paramecium bursaria chlorella virus type 1 (PBCV-1; Nandhagopal et al, 2002; Yan et al, 2000; Fig. 1b). In the former, some suitably oriented particles can be seen to have a tail prior to infecting a host (Fig. 1a; Xiao et al, 2005). It has been shown that PBCV-1 (Fig. 1b) forms a transient tail prior to host infection (Van Etten et al, 1991), as is the case for the lipid-containing PRD1 bacteriophage (Grahn et al, 2005)

Picornaviruses

10 Rossmann et al Virus structure

Parvoviruses

Bacteriophage T4: the head capsid

Bacteriophage T4: the tail

Conclusion