Three-dimensional structures of the A, B, and C capsids of rhesus monkey rhadinovirus: insights into gammaherpesvirus capsid assembly, maturation, and DNA packaging.
Rhesus monkey rhadinovirus (RRV) exhibits high levels of sequence homology to human gammaherpesviruses, such as Kaposi's sarcoma-associated herpesvirus, and grows to high titers in cell cultures, making it a good model system for studying gammaherpesvirus capsid structure and assembly. We have purified RRV A, B, and C capsids, thus for the first time allowing direct structure comparisons by electron cryomicroscopy and three-dimensional reconstruction. The results show that the shells of these capsids are identical and are each composed of 12 pentons, 150 hexons, and 320 triplexes. Structural differences were apparent inside the shells and through the penton channels. The A capsid is empty, and its penton channels are open. The B capsid contains a scaffolding core, and its penton channels are closed. The C capsid contains a DNA genome, which is closely packaged into regularly spaced density shells (25 A apart), and its penton channels are open. The different statuses of the penton channels suggest a functional role of the channels during capsid maturation, and the overall structural similarities of RRV capsids to alphaherpesvirus capsids suggest a common assembly and maturation pathway. The RRV A capsid reconstruction at a 15-A resolution, the best achieved for gammaherpesvirus particles, reveals overall structural similarities to alpha- and betaherpesvirus capsids. However, the outer regions of the capsid, including densities attributed to the Ta triplex and the small capsomer-interacting protein (SCIP or ORF65), exhibit prominent differences from their structural counterparts in alphaherpesviruses. This structural disparity suggests that SCIP and the triplex, together with tegument and envelope proteins, confer structural and potentially functional specificities to alpha-, beta-, and gammaherpesviruses.
Yu
Xue-Kui
XK
Department of PathologyLaboratory Medicine, University of Texas at Houston Medical School, Houston, Texas 77030, USA.
O'Connor
Christine M
CM
Atanasov
Ivo
I
Damania
Blossom
B
Kedes
Dean H
DH
Zhou
Z Hong
ZH
D000818:Animals; D002213:Capsid / Q000648:ultrastructure*; D002461:Cell Line, Transformed; D020285:Cryoelectron Microscopy; D004279:DNA, Viral / Q000378:metabolism*; D006566:Herpesviridae Infections / Q000821:virology; D021621:Imaging, Three-Dimensional; D008253:Macaca mulatta / Q000821:virology*; D018144:Rhadinovirus / Q000378:metabolism / Q000648:ultrastructure*; D019065:Virus Assembly
D004279:DNA, Viral