Lipid-Containing Viruses: Bacteriophage PRD1 Assembly

Butcher, Sarah J.; Manole, Violeta; Karhu, Nelli J.

doi:10.1007/978-1-4614-0980-9_16

Cited by 16 publications

(24 citation statements)

References 72 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This is analogous to T4, where a separate terminase domain on the C terminus of gp17 recognizes the DNA, and then the N-terminal ATPase domain of gp17 drives the translocation (4). In the distantly related bacteriophage PRD1, the terminal protein that is covalently linked to the genome is required for packaging and is probably recognized by the packaging ATPase (8). Hence, the additional nucleotide-binding site on the suggested capsid-distal side of B204 (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Our biochemical and structural data, together with knowledge of the assembly of other membrane-containing, nontailed viruses such as PRD1 (8) and STIV (51), prompted us to propose an assembly pathway for STIV2 utilizing a multimeric ring of B204 assembled as a portal on the STIV2 procapsid for dsDNA translocation (Fig. 7).…”

Section: Discussionmentioning

confidence: 99%

“…gp16 stimulates the ATPase activity of gp17 50-fold (5). In some cases, such as the tailed phage 29 and the nontailed phage PRD1, the linear dsDNA genome is associated with covalently linked terminal proteins (6,7) recognized by the genome-packaging ATPase (8). The dsRNA virus 12 hexameric NTPase P4 combines both RNA translocation and NTPase hydrolysis into a single domain (9) and is a structural component of the virion (10).…”

mentioning

confidence: 99%

“…The dsRNA virus 12 hexameric NTPase P4 combines both RNA translocation and NTPase hydrolysis into a single domain (9) and is a structural component of the virion (10). The genome-packaging NTPases of some membrane-containing, nontailed dsDNA viruses, like PRD1, are also part of the virion as shown by gel analysis, mass spectrometry, and immunolabeling (8,(11)(12)(13). These PRD1-type NTPases have been recalcitrant to structural studies due to instability and insolubility (14), and consequently the catalytic cycles of these proteins are poorly understood.…”

mentioning

confidence: 99%

See 3 more Smart Citations

The Structure of the NTPase That Powers DNA Packaging into Sulfolobus Turreted Icosahedral Virus 2

Happonen

Oksanen

Liljeroos

et al. 2013

J Virol

Self Cite

View full text Add to dashboard Cite

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

The Structure of the NTPase That Powers DNA Packaging into Sulfolobus Turreted Icosahedral Virus 2

Happonen

Oksanen

Liljeroos

et al. 2013

J Virol

Self Cite

View full text Add to dashboard Cite

“…Of these viruses, the assembly of bacteriophage PRD1 has been the most extensively examined (9). The morphogenesis starts with a lipid vesicle containing viral membrane proteins pinching off from the host cytoplasmic membrane as capsid-associated proteins assemble along it, resulting in the formation of an empty procapsid.…”

Section: Importancementioning

confidence: 99%

The Minor Capsid Protein VP11 of Thermophilic Bacteriophage P23-77 Facilitates Virus Assembly by Using Lipid-Protein Interactions

Pawlowski

Moilanen

Rissanen

et al. 2015

J Virol

View full text Add to dashboard Cite

Thermus thermophilus bacteriophage P23-77 is the type member of a new virus family of icosahedral, tailless, inner-membranecontaining double-stranded DNA (dsDNA) viruses infecting thermophilic bacteria and halophilic archaea. The viruses have a unique capsid architecture consisting of two major capsid proteins assembled in various building blocks. We analyzed the function of the minor capsid protein VP11, which is the third known capsid component in bacteriophage P23-77. Our findings show that VP11 is a dynamically elongated dimer with a predominantly ␣-helical secondary structure and high thermal stability. The high proportion of basic amino acids in the protein enables electrostatic interaction with negatively charged molecules, including nucleic acid and large unilamellar lipid vesicles (LUVs). The plausible biological function of VP11 is elucidated by demonstrating the interactions of VP11 with Thermus-derived LUVs and with the major capsid proteins by means of the dynamic-lightscattering technique. In particular, the major capsid protein VP17 was able to link VP11-complexed LUVs into larger particles, whereas the other P23-77 major capsid protein, VP16, was unable to link VP11-comlexed LUVs. Our results rule out a previously suggested penton function for VP11. Instead, the electrostatic membrane association of VP11 triggers the binding of the major capsid protein VP17, thus facilitating a controlled incorporation of the two different major protein species into the assembling capsid. IMPORTANCEThe study of thermophilic viruses with inner membranes provides valuable insights into the mechanisms used for stabilization and assembly of protein-lipid systems at high temperatures. Our results reveal a novel way by which an internal membrane and outer capsid shell are linked in a virus that uses two different major protein species for capsid assembly. We show that a positive protein charge is important in order to form electrostatic interactions with the lipid surface, thereby facilitating the incorporation of other capsid proteins on the membrane surface. This implies an alternative function for basic proteins present in the virions of other lipid-containing thermophilic viruses, whose proposed role in genome packaging is based on their capability to bind DNA. The unique minor capsid protein of bacteriophage P23-77 resembles in its characteristics the scaffolding proteins of tailed phages, though it constitutes a substantial part of the mature virion. V iruses from extremely hot environments need to develop special strategies to cope with high temperature. Hence, they provide a valuable source for the detection of novel enzymes for biotechnology and industrial processes. Their relative simple structure makes them an ideal model system for studying life at high temperatures. With respect to extreme thermophilic bacteria, the virus studied best on the structural level is P23-77, a strictly lytic phage infecting Thermus thermophilus ATCC 33923 (1, 2, 3). P23-77 is a representative of the novel Sphaerolipoviri...

show abstract