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

Conway, James F.; Cheng, Naiqian; Ross, Philip D.; Hendrix, Roger W.; Duda, Robert L.; Steven, Alasdair C.

doi:10.1016/j.jsb.2006.11.006

Cited by 35 publications

(53 citation statements)

References 37 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The presence of reversible steps in the overall unidirectional maturation pathway of the PC appears to be an additional feature shared by these viruses, as shown here for the dsRNA bacteriophage 6 (Fig. 3) and previously for several tailed dsDNA phages (67)(68)(69). The interaction between the PC and the packaging machinery displays substantial flexibility, especially in the 6 and T4 systems ( Fig.…”

Section: Discussionsupporting

confidence: 76%

Rescue of Maturation Off-Pathway Products in the Assembly of Pseudomonas Phage ϕ6

Sun

Pirttimaa

Bamford

et al. 2013

J Virol

View full text Add to dashboard Cite

Many complex viruses use an assembly pathway in which their genome is packaged into an empty procapsid which subsequently matures into its final expanded form. We utilized Pseudomonas phage 6, a well-established virus assembly model, to probe the plasticity of the procapsid maturation pathway. The 6 packaging nucleoside triphosphatase (NTPase), which powers sequential translocation of the three viral genomic single-stranded RNA molecules to the procapsid during capsid maturation, is part of the mature 6 virion but may spontaneously be dissociated from the procapsid shell. We demonstrate that the dissociation of NTPase subunits results in premature capsid expansion, which is detected as a change in the sedimentation velocity and as defects in RNA packaging and transcription activity. However, this dead-end conformation of the procapsids was rescued by the addition of purified NTPase hexamers, which efficiently associated on the NTPase-deficient particles and subsequently drove their contraction to the compact naive conformation. The resulting particles regained their biological and enzymatic activities, directing them into a productive maturation pathway. These observations imply that the maturation pathways of complex viruses may contain reversible steps that allow the rescue of the off-pathway conformation in an overall unidirectional virion assembly pathway. Furthermore, we provide direct experimental evidence that particles which have different physical properties (distinct sedimentation velocities and conformations) display different stages of the genome packaging program and show that the transcriptional activity of the 6 procapsids correlates with the number of associated NTPase subunits.

show abstract

Section: Discussionsupporting

confidence: 76%

Rescue of Maturation Off-Pathway Products in the Assembly of Pseudomonas Phage ϕ6

Sun

Pirttimaa

Bamford

et al. 2013

J Virol

View full text Add to dashboard Cite

show abstract

“…The ⌬ domain thus may adopt at least two conformations: a disordered one in expanded tubes and a more ordered/rigid one triggered by Ca 2ϩ in contracted tubes and in procapsid I. A similar disordering of the HK97 ⌬ domain of hexons but not pentons has been observed in heated prohead I, which also returns to the starting state on cooling (4).…”

Section: Discussionmentioning

confidence: 59%

In Vitro Assembly of the T=13 Procapsid of Bacteriophage T5 with Its Scaffolding Domain

Huet

Conway

Letellìer

et al. 2010

J Virol

Self Cite

View full text Add to dashboard Cite

The Siphoviridae coliphage T5 differs from other members of this family by the size of its genome (121 kbp) and by its large icosahedral capsid (90 nm), which is organized with T‫31؍‬ geometry. T5 does not encode a separate scaffolding protein, but its head protein, pb8, contains a 159-residue aminoterminal scaffolding domain (⌬ domain) that is the mature capsid. We have deciphered the early events of T5 shell assembly starting from purified pb8 with its ⌬ domain (pb8p). The self assembly of pb8p is regulated by salt conditions and leads to structures with distinct morphologies. Expanded tubes are formed in the presence of NaCl, whereas Ca 2؉ promotes the association of pb8p into contracted tubes and procapsids. Procapsids display an angular organization and 20-nm-long internal radial structures identified as the ⌬ domain. The T5 head maturation protease pb11 specifically cleaves the ⌬ domain of contracted and expanded tubes. Ca 2؉ is not required for proteolytic activity but for the organization of the ⌬ domain. Taken together, these data indicate that pb8p carries all of the information in its primary sequence to assemble in vitro without the requirement of the portal and accessory proteins. Furthermore, Ca 2؉ plays a key role in introducing the conformational diversity that permits the formation of a stable procapsid. Phage T5 is the first example of a viral capsid consisting of quasi-equivalent hexamers and pentamers whose assembly can be carried out in vitro, starting from the major head protein with its scaffolding domain, and whose endpoint is an icosahedral T‫31؍‬ particle.

show abstract

“…Some capsids undergo buckling transitions, where the capsid, once assembled, undergoes a change in morphology from being more spherical to a more faceted (or more ''icosahedron-like'') form (22,23). For capsids that undergo such transitions (distinguished from capsid ''swelling events'' below), this change in morphology is crucial to the continuation of the virus life cycle.…”

Section: Resultsmentioning

confidence: 99%

Geometric considerations in virus capsid size specificity, auxiliary requirements, and buckling

Mannige

Brooks²

2009

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

View full text Add to dashboard Cite

Spherical capsids are shells of protein subunits that protect the genomes of many viral strains. Although nature displays a range of spherical capsid sizes (reflected by the number of subunits in the formation), specific strains display stringent requirements for forming capsids of specific sizes, a requirement that appears crucial to infectivity. Despite its importance in pathogenicity, little is known regarding the determinants of capsid size. Still less is known about exactly which capsids can undergo maturation events such as buckling transitions-postcapsid-assembly events that are crucial to some virus strains. We show that the exclusive determinant of capsid size is hexamer shape, as defined by subunit-subunit dihedral angles. This conclusion arises from considering the dihedral angle patterns within hexamers belonging to natural canonical capsids and geometric capsid models (deltahedra). From simple geometric models and an understanding of endo angle propagation discussed here, we then suggest that buckling transitions may be available only to capsids of certain size (specifically, T < 7 capsids are precluded from such transformations) and that T > 7 capsids require the help of auxiliary mechanisms for proper capsid formation. These predictions, arising from simple geometry and modeling, are backed by a body of empirical evidence, further reinforcing the extent to which the evolution of the atomistically complex virus capsid may be principled around simple geometric design/requirements. auxiliary proteins ͉ capsid buckling ͉ deltahedra ͉ endo angle constraint A large number of human-and crop-infecting viruses are protected by spherical capsids (shells) of various sizes that are primarily made up of self-organizing protein subunits (1, 2). Caspar and Klug's (3) seminal article on quasi-equivalence explained how an infinite range of capsid sizes can be ''constructed'' by combining 60T subunits or 12 pentamers (5-valent subunit clusters) and a variable number of hexamers [10 ϫ (T Ϫ 1)] into a closed spherical shell (T ʦ {1,3,4,7, . . .} and is the triangulation number described in ref.3).From the range of possible sizes, generally, subunits from specific viral strains assemble into capsids of specific sizes; the inability to form those native sizes is believed to result in the loss of infectivity. For example, the sobemovirus and birnavirus capsids (4, 5) shown in Fig. 1A are known to be pathogenic primarily in their native T ϭ 3 and T ϭ 13 capsid forms, respectively. Despite its importance in pathogenicity, our picture of capsid size specificity is incomplete. In the present report, we are interested in the structural features (constraints), if any exist, that differentiate between capsids of different sizes (capsid design criteria). An appreciation of these concepts is pressing from a nanotechnological perspective [for the rational design of artificial scalable assemblies that build on current practices, such as in the use of protein fusion and symmetry properties by Padilla et al. (6)] and a therapeutic p...

show abstract

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

Cited by 35 publications

References 37 publications

Rescue of Maturation Off-Pathway Products in the Assembly of Pseudomonas Phage ϕ6

Rescue of Maturation Off-Pathway Products in the Assembly of Pseudomonas Phage ϕ6

In Vitro Assembly of the T=13 Procapsid of Bacteriophage T5 with Its Scaffolding Domain

Geometric considerations in virus capsid size specificity, auxiliary requirements, and buckling

Contact Info

Product

Resources

About