TY - JOUR
T1 - Honey bee deformed wing virus structures reveal that conformational changes accompany genome release
AU - Organtini, Lindsey J.
AU - Shingler, Kristin L.
AU - Ashley, Robert E.
AU - Capaldi, Elizabeth A.
AU - Durrani, Kulsoom
AU - Dryden, Kelly A.
AU - Makhov, Alexander M.
AU - Conway, James F.
AU - Pizzorno, Marie C.
AU - Hafenstein, Susan
N1 - Funding Information:
This work was supported in part by Pennsylvania Department of Health CURE funds. Research reported in this publication was also supported by the Office of the Director, National Institutes of Health, under awards S10OD019995 and S10OD011986, as well as NIH grants R01AI107121 (S.H.) and T32CA060395 (L.J.O.). The UVA MEMC equipment was partially funded by grants from the NIH for the Titan Krios (S10-RR025067) and the Falcon II direct detector (S10-OD018149). The content is solely our responsibility and does not necessarily represent the official views of the National Institutes of Health. We declare that we have no potential conflicts of interest. L.J.O. and K.L.S. prepared all samples for cryo-EM and data collection. K.L.S. and K.D. performed proof-of-principle experiments. R.E.A. collected negative-stain and LaB6 data and analyzed initial data. E.A.C. and M.C.P. provided DWV-infected honey bees and performed molecular biological assays. K.A.D., A.M.M., and J.F.C. acquired and interpreted cryo-EM data. L.J.O. performed cryo-EM and negative-stain image processing and model prediction, S.H. and L.J.O. analyzed the data and interpreted the structures. L.J.O., K.L.S., J.F.C, M.C.P., and S.H. oversaw the project and wrote the manuscript.
Publisher Copyright:
© 2017 American Society for Microbiology.
PY - 2017
Y1 - 2017
N2 - The picornavirus-like deformed wing virus (DWV) has been directly linked to colony collapse; however, little is known about the mechanisms of host attachment or entry for DWV or its molecular and structural details. Here we report the three-dimensional (3-D) structures of DWV capsids isolated from infected honey bees, including the immature procapsid, the genome-filled virion, the putative entry intermediate (A-particle), and the empty capsid that remains after genome release. The capsids are decorated by large spikes around the 5-fold vertices. The 5-fold spikes had an open flower-like conformation for the procapsid and genome-filled capsids, whereas the putative A-particle and empty capsids that had released the genome had a closed tube-like spike conformation. Between the two conformations, the spikes undergo a significant hinge-like movement that we predicted using a Robetta model of the structure comprising the spike. We conclude that the spike structures likely serve a function during host entry, changing conformation to release the genome, and that the genome may escape from a 5-fold vertex to initiate infection. Finally, the structures illustrate that, similarly to picornaviruses, DWV forms alternate particle conformations implicated in assembly, host attachment, and RNA release.
AB - The picornavirus-like deformed wing virus (DWV) has been directly linked to colony collapse; however, little is known about the mechanisms of host attachment or entry for DWV or its molecular and structural details. Here we report the three-dimensional (3-D) structures of DWV capsids isolated from infected honey bees, including the immature procapsid, the genome-filled virion, the putative entry intermediate (A-particle), and the empty capsid that remains after genome release. The capsids are decorated by large spikes around the 5-fold vertices. The 5-fold spikes had an open flower-like conformation for the procapsid and genome-filled capsids, whereas the putative A-particle and empty capsids that had released the genome had a closed tube-like spike conformation. Between the two conformations, the spikes undergo a significant hinge-like movement that we predicted using a Robetta model of the structure comprising the spike. We conclude that the spike structures likely serve a function during host entry, changing conformation to release the genome, and that the genome may escape from a 5-fold vertex to initiate infection. Finally, the structures illustrate that, similarly to picornaviruses, DWV forms alternate particle conformations implicated in assembly, host attachment, and RNA release.
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U2 - 10.1128/JVI.01795-16
DO - 10.1128/JVI.01795-16
M3 - Article
C2 - 27852845
AN - SCOPUS:85008601782
SN - 0022-538X
VL - 91
JO - Journal of virology
JF - Journal of virology
IS - 2
M1 - e01795-16
ER -