High resolution structure of hexameric herpesvirus DNA-packaging motor elucidates revolving mechanism and ends 20-year fervent debate

Peixuan Guo

doi:10.1007/s13238-020-00714-w

Volume 11 Issue 5

May 2020

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Peixuan Guo. High resolution structure of hexameric herpesvirus DNA-packaging motor elucidates revolving mechanism and ends 20-year fervent debate[J]. Protein&Cell, 2020, 11(5): 311-315. doi: 10.1007/s13238-020-00714-w

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Peixuan Guo. High resolution structure of hexameric herpesvirus DNA-packaging motor elucidates revolving mechanism and ends 20-year fervent debate[J]. Protein&Cell, 2020, 11(5): 311-315. doi: 10.1007/s13238-020-00714-w

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High resolution structure of hexameric herpesvirus DNA-packaging motor elucidates revolving mechanism and ends 20-year fervent debate

doi: 10.1007/s13238-020-00714-w

Peixuan Guo^,

College of Pharmacy, College of Medicine, Dorothy M. Davis Heart and Lung Research Institute, and Comprehensive Cancer Center, The Ohio State University, Columbus, OH 43210, USA

Funds:

The research in Guo lab was supported by NIH grants R01EB019036, U01CA151648 and U01CA207946. Guo is the consultant of Oxford Nanopore Technologies

the cofounder of Shenzhen P&Z Bio-medical Co. Ltd, as well as cofounder of ExonanoRNA, LLC and its subsidiary Weina Biomedical LLC in Foshan. His Sylvan G. Frank Endowed Chair position in Pharmaceutics and Drug Delivery is funded by the CM Chen Foundation. Thanks to Zhefeng Li and Nicolas Burns for the preparation of the manuscript.

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References

[1]	Acosta E, Bowlin T, Brooks J, Chiang L, Hussein I, Kimberlin D, Kauvar LM, Leavitt R, Prichard M, Whitley R (2020) Advances in the development of therapeutics for cytomegalovirus infections. J Infect Dis 221:S32-S44
[2]	Arai S, Saijo S, Suzuki K, Mizutani K, Kakinuma Y, Ishizuka-Katsura Y, Ohsawa N, Terada T, Shirouzu M, Yokoyama S et al (2013) Rotation mechanism of Enterococcus hirae V1-ATPase based on asymmetric crystal structures. Nature 493:703-707
[3]	Baumann RG, Mullaney J, Black LW (2006) Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol 61:16-32
[4]	Chang CL, Zhang H, Shu D, Guo P, Savran CA (2008) Bright-field analysis of phi29 DNA packaging motor using a magnetomechanical system. Appl Phys Lett 93:153902
[5]	Chen W, Xiao H, Wang X, Song S, Han Z, Li X, Yang F, Wang L, Song, Liu H et al (2020) Structural changes of a bacteriophage upon DNA packaging and maturation. Protein Cell. https://doi.org/10.1007/s13238-020-00715-9
[6]	Dong Y, Zhang S, Wu Z, Li X, Wang WL, Zhu Y, Stoilova-McPhie S, Lu Y, Finley D, Mao Y (2019) Cryo-EM structures and dynamics of substrate-engaged human 26S proteasome. Nature 565:49-55
[7]	Goldner T, Hewlett G, Ettischer N, Ruebsamen-Schaeff H, Zimmermann H, Lischka P (2011) The novel anticytomegalovirus compound AIC246 (Letermovir) inhibits human cytomegalovirus replication through a specific antiviral mechanism that involves the viral terminase. J Virol 85:10884-10893
[8]	Guo P, Peterson C, Anderson D (1987a) Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi 29. J Mol Biol 197:229-236
[9]	Guo PX, Erickson S, Anderson D (1987b) A small viral RNA is required for in vitro packaging of bacteriophage phi 29 DNA. Science 236:690-694
[10]	Guo P, Zhang C, Chen C, Garver K, Trottier M (1998) Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol Cell 2:149-155
[11]	Guo P, Grainge I, Zhao Z, Vieweger M (2014) Two classes of nucleic acid translocation motors:rotation and revolution without rotation. Cell Biosci 4:54
[12]	Guo P, Driver D, Zhao Z, Zheng Z, Chan C, Cheng X (2019) Controlling the revolving and rotating motion direction of asymmetric hexameric nanomotor by arginine finger and channel chirality. ACS Nano 13:6207-6223
[13]	Hendrix RW (1978) Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci USA 75:4779-4783
[14]	Hugel T, Michaelis J, Hetherington CL, Jardine PJ, Grimes S, Walter JM, Falk W, Anderson DL, Bustamante C (2007) Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids. PLoS Biol 5:e59
[15]	Jimenez J, Santisteban A, Carazo JM, Carrascosa JL (1986) Computer graphic display method for visualizing three-dimensional biological structures. Science 232:1113-1115
[16]	Lyubimov AY, Costa A, Bleichert F, Botchan MR, Berger JM (2012) ATP-dependent conformational dynamics underlie the functional asymmetry of the replicative helicase from a minimalist eukaryote. Proc Natl Acad Sci USA 109:11999-12004
[17]	Martin A, Baker TA, Sauer RT (2005) Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines. Nature 437:1115-1120
[18]	Pi F, Vieweger M, Zhao Z, Wang S, Guo P (2016a) Discovery of a new method for potent drug development using power function of stoichiometry of homomeric biocomplexes or biological nanomotors. Expert Opin Drug Deliv 13:23-36
[19]	Pi F, Zhao Z, Chelikani V, Yoder K, Kvaratskhelia M, Guo P (2016b) Development of potent antiviral drugs inspired by viral hexameric DNA-packaging motors with revolving mechanism. J Virol 90:8036-8046
[20]	Puchades C, Rampello AJ, Shin M, Giuliano CJ, Wiseman RL, Glynn SE, Lander GC (2017) Structure of the mitochondrial inner membrane AAA+ protease YME1 gives insight into substrate processing. Science 358:eaao0464
[21]	Schwartz C, De Donatis GM, Zhang H, Fang H, Guo P (2013) Revolution rather than rotation of AAA+ hexameric phi29 nanomotor for viral dsDNA packaging without coiling. Virology 443:28-39
[22]	Shu D, Pi F, Wang C, Zhang P, Guo P (2015) New approach to develop ultra-high inhibitory drug using the power function of the stoichiometry of the targeted nanomachine or biocomplex. Nanomedicine 10:1881-1897
[23]	Soultanas P, Wigley DB (2001) Unwinding the ‘Gordian knot’ of helicase action. Trends Biochem Sci 26:47-54
[24]	Su M, Guo EZ, Ding X, Li Y, Tarrasch JT, Brooks CL 3rd, Xu Z, Skiniotis G (2017) Mechanism of Vps4 hexamer function revealed by cryo-EM. Sci Adv 3:e1700325
[25]	Sun S, Li L, Yang F, Wang X, Fan F, Yang M, Chen C, Li X, Wang HW, Sui SF (2017) Cryo-EM structures of the ATP-bound Vps 4(E233Q) hexamer and its complex with Vta1 at near-atomic resolution. Nat Commun 8:16064
[26]	Wang N, Zhao D, Wang J, Zhang Y, Wang M, Gao Y, Li F, Wang J, Bu Z, Rao Z et al (2019) Architecture of African swine fever virus and implications for viral assembly. Science 366:640-644
[27]	Wang N, Chen W, Zhu L, Feng R, Wang J, Zhu D, Zhang X, Liu H, Rao Z, Wang X (2020) Structures of the portal vertex reveal essential protein-protein interactions for Herpesvirus assembly and maturation. Protein Cell. https://doi.org/10.1007/s13238-020-00711-z
[28]	Yang Y, Yang P, Wang N, Zhu L, Zeng Y, Zhou ZH, Rao Z, Wang X (2020) Architecture of the herpesvirus genome-packaging complex and implications for DNA translocation. Protein Cell. https://doi.org/10.1007/s13238-020-00710-0
[29]	Yuan S, Wang J, Zhu D, Wang N, Gao Q, Chen W, Tang H, Wang J, Zhang X, Liu H et al (2018) Cryo-EM structure of a herpesvirus capsid at 31 A. Science 360:eaao7283
[30]	Zehr E, Szyk A, Piszczek G, Szczesna E, Zuo X, Roll-Mecak A (2017) Katanin spiral and ring structures shed light on power stroke for microtubule severing. Nat Struct Mol Biol 24:717-725
[31]	Zhao Z, Khisamutdinov E, Schwartz C, Guo P (2013) Mechanism of one-way traffic of hexameric phi29 DNA packaging motor with four electropositive relaying layers facilitating antiparallel revolution. ACS Nano 7:4082-4092
[32]	Zhao Z, De-Donatis GM, Schwartz C, Fang H, Li J, Guo P (2016) An arginine finger regulates the sequential action of asymmetrical hexameric ATPase in the double-stranded DNA translocation motor. Mol Cell Biol 36:2514-2523
[33]	Zhu L, Sun Y, Fan J, Zhu B, Cao L, Gao Q, Zhang Y, Liu H, Rao Z, Wang X (2018) Structures of Coxsackievirus A10 unveil the molecular mechanisms of receptor binding and viral uncoating. Nat Commun 9:4985