Common Evolutionary Origin of Procapsid Proteases, Phage Tail Tubes, and Tubes of Bacterial Type VI Secretion Systems - PubMed (original) (raw)

Common Evolutionary Origin of Procapsid Proteases, Phage Tail Tubes, and Tubes of Bacterial Type VI Secretion Systems

Andrei Fokine et al. Structure. 2016.

Abstract

Many large viruses, including tailed dsDNA bacteriophages and herpesviruses, assemble their capsids via formation of precursors, called procapsids or proheads. The prohead has an internal core, made of scaffolding proteins, and an outer shell, formed by the major capsid protein. The prohead usually contains a protease, which is activated during capsid maturation to destroy the inner core and liberate space for the genome. Here, we report a 2.0 Å resolution structure of the pentameric procapsid protease of bacteriophage T4, gene product (gp)21. The structure corresponds to the enzyme's pre-active state in which its N-terminal region blocks the catalytic center, demonstrating that the activation mechanism involves self-cleavage of nine N-terminal residues. We describe similarities and differences between T4 gp21 and related herpesvirus proteases. We found that gp21 and the herpesvirus proteases have similarity with proteins forming the tubes of phage tails and bacterial type VI secretion systems, suggesting their common evolutionary origin.

Keywords: bacterial type VI secretion system; bacteriophage; herpesvirus; phage tail tube; procapsid; prohead protease; self-cleavage; virus assembly.

Copyright © 2016 Elsevier Ltd. All rights reserved.

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Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Figure 1

Figure 1. Crystal structure of the T4 prohead protease pentamer

The polypeptide chains, shown as ribbons, are rainbow-colored from blue at the N-terminus to red at the C-terminus. Positions of the catalytic centers are shown by semitransparent spheres. (A) View along the five-fold axis of the pentamer. (B) View perpendicular to the five-fold axis.

Figure 2

Figure 2. Ribbon diagram of the gp21 monomer rainbow-colored from blue at the N-terminus to red at the C-terminus

Side chains of the residues 140 (Ser of the catalytic triad mutated to Ala), 85 (His of the triad mutated to Ala), and 168 (Asp of the catalytic triad) are shown in black.

Figure 3

Figure 3. Stereo view of the gp21 substrate binding site blocked by the N-terminal region of the polypeptide chain

The peptide bond between Glu9 and Thr10 is located near the side chain of residue 140, which is the catalytic Ser mutated to Ala.

Figure 4

Figure 4. Stereo view of superposition of T4 gp21 with the pseudorabies virus protease

The polypeptide chain of gp21 is rainbow-colored from blue at the N-terminus to red at the C- terminus. The polypeptide chain of the pseudorabies virus protease is shown in black. The C- terminal helical region of the pseudorabies virus protease, absent in gp21, is semitransparent. Residue numbers for the gp21 protein are shown in magenta.

Figure 5

Figure 5. Schematic diagrams showing topology of T4 gp21 (left) and the pseudorabies herpesvirus protease (right)

β–strands are represented by arrows, and α-helices are represented by cylinders. The C-terminal helical region of the pseudorabies virus protease, absent in gp21, is outlined by a grey rectangle.

Figure 6

Figure 6. Comparison of the T4 capsid assembly protease, gp21, with the T4 tail tube protein gp19

(A) Stereo view of the superposition of gp21 with gp19 (PDB ID: 5iv5). Region 10 - 116 of gp21 is rainbow–colored from blue at the N-terminus to yellow-green at the C- terminus. Region 36 – 160 of gp19 is shown in black. Residue numbers for the gp21 chain are shown in magenta. (B) Schematic diagram showing topology of the conserved structural motif. See also Figure S1

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