Penton Release from P22 Heat-Expanded Capsids Suggests Importance of Stabilizing Penton-Hexon Interactions during Capsid Maturation

Abstract

Bacteriophage assembly frequently begins with the formation of a precursor capsid that serves as a DNA packaging machine. The DNA packaging is accompanied by a morphogenesis of the small round precursor capsid into a large polyhedral DNA-containing mature phage. In vitro, this transformation can be induced by heat or chemical treatment of P22 procapsids. In this work, we examine bacteriophage P22 morphogenesis by comparing three-dimensional structures of capsids expanded both in vitro by heat treatment and in vivo by DNA packaging. The heat-expanded capsid reveals a structure that is virtually the same as the in vivo expanded capsid except that the pentons, normally present at the icosahedral fivefold positions, have been released. The similarities of these two capsid structures suggest that the mechanism of heat expansion is similar to in vivo expansion. The loss of the pentons further suggests the necessity of specific penton-hexon interactions during expansion. We propose a model whereby the penton-hexon interactions are stabilized through interactions of DNA, coat protein, and other minor proteins. When considered in the context of other studies using chemical or heat treatment of capsids, our study indicates that penton release may be a common trend among double-stranded DNA containing viruses.

The Role of Capsid Maturation on Adenovirus Priming for Sequential Uncoating

“…This difference indicates a role for the precursor proteins in preventing premature vertex release, particularly during the DNA packaging process. The need to reinforce vertex structures during morphogenesis has previously been hypothesized in other icosahedral viruses (55).…”

A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged

“…In the herpes simplex virus system, which has much in common with tailed bacteriophages , the maturing hexamers undergo extensive remodeling whereas pentamers make only small shifts (Heymann et al, 2003). When capsids of bacteriophage P22 are heated at 70°C, their pentamers are dislodged and their hexamers remain in place (Teschke et al, 2003).…”

A Molecular Staple: D-Loops in the I Domain of Bacteriophage P22 Coat Protein Make Important Intercapsomer Contacts Required for Procapsid Assembly

“…During the maturation process, the capsid diameter increases by about 10% (14,33). This expansion process can be mimicked in vitro by the addition of heat or destabilizing agents (34,35). Heat-expanded procapsids release coat proteins in penton positions from the capsid (35,36).…”

“…This expansion process can be mimicked in vitro by the addition of heat or destabilizing agents (34,35). Heat-expanded procapsids release coat proteins in penton positions from the capsid (35,36). The expansion process also results in changes in intersubunit contacts between coat subunits (35,37).…”