Atomic structure of the 75 MDa extremophile Sulfolobus turreted icosahedral virus determined by CryoEM and X-ray crystallography

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 14, 2013, Pages 5504-5509

  Veesler, David ^a   Ng, Thiam Seng ^b,c   Sendamarai, Anoop K ^d,e   Eilers, Brian J ^d   Lawrence, C Martin ^d   Lok, Shee Mei ^b,c   Young, Mark J ^d   Johnson, John E ^a   Fu, Chi Yu ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d MONTANA STATE UNIVERSITY   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Archaea; Electron microscopy; PRD1 Adeno viral lineage; Single particle reconstruction; Virus assembly

Indexed keywords

MEMBRANE PROTEIN; POLYPEPTIDE;

ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; EUKARYOTE EVOLUTION; EVOLUTION; GENE PRODUCT; OPTICAL RESOLUTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SULFOLOBUS; SULFOLOBUS TURRETED ICOSAHEDRAL VIRUS; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS ISOLATION; VIRUS MORPHOLOGY; X RAY CRYSTALLOGRAPHY;

CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; MEMBRANE PROTEINS; MODELS, MOLECULAR; RUDIVIRIDAE; SULFOLOBUS;

BACTERIA (MICROORGANISMS); EUKARYOTA; MIRIDAE; SULFOLOBUS SOLFATARICUS; SULFOLOBUS TURRETED ICOSAHEDRAL VIRUS;

EID: 84875859692     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300601110     Document Type: Article

References (44)

1. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc Natl Acad Sci USA 74(11):5088-5090.
2. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87(12):4576-4579.
3. Prangishvili D, Forterre P, Garrett RA (2006) Viruses of the Archaea: A unifying view. Nat Rev Microbiol 4(11):837-848.
4. Aalto AP, et al. (2012) Snapshot of virus evolution in hypersaline environments from the characterization of a membrane-containing Salisaeta icosahedral phage1. Proc Natl Acad Sci USA 109(18):7079-7084.
5. Reddy VS, Natchiar SK, Stewart PL, Nemerow GR (2010) Crystal structure of human adenovirus at 3.5 A resolution. Science 329(5995):1071-1075.
6. Liu H, et al. (2010) Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 329(5995):1038-1043.
7. Rux JJ, Kuser PR, Burnett RM (2003) Structural and phylogenetic analysis of adenovirus hexons by use of high-resolution x-ray crystallographic, molecular modeling, and sequence-based methods. J Virol 77(17):9553-9566.
8. Nandhagopal N, et al. (2002) The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc Natl Acad Sci USA 99(23):14758-14763.
9. Bahar MW, Graham SC, Stuart DI, Grimes JM (2011) Insights into the evolution of a complex virus from the crystal structure of vaccinia virus D13. Structure 19(7): 1011-1020.
10. Zhang X, et al. (2012) Structure of Sputnik, a virophage, at 3.5-Å resolution. Proc Natl Acad Sci USA 109(45):18431-18436.
11. Cockburn JJB, et al. (2004) Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432(7013):122-125.
12. Abrescia NGA, et al. (2004) Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432(7013):68-74.
13. Abrescia NGA, et al. (2008) Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Mol Cell 31(5): 749-761.
14. Jaatinen ST, Happonen LJ, Laurinmäki P, Butcher SJ, Bamford DH (2008) Biochemical and structural characterisation of membrane-containing icosahedral dsDNA bacteriophages infecting thermophilic Thermus thermophilus. Virology 379(1):10-19.
15. Laurinmäki PA, Huiskonen JT, Bamford DH, Butcher SJ (2005) Membrane proteins modulate the bilayer curvature in the bacterial virus Bam35. Structure 13(12): 1819-1828.
16. Jäälinoja HT, et al. (2008) Structure and host-cell interaction of SH1, a membranecontaining, halophilic euryarchaeal virus. Proc Natl Acad Sci USA 105(23):8008-8013.
17. Jaakkola ST, et al. (2012) Closely related archaeal Haloarcula hispanica icosahedral viruses HHIV-2 and SH1 have nonhomologous genes encoding host recognition functions. J Virol 86(9):4734-4742.
18. Khayat R, et al. (2005) Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proc Natl Acad Sci USA 102(52): 18944-18949.
19. Rice G, et al. (2004) The structure of a thermophilic archaeal virus shows a doublestranded DNA viral capsid type that spans all domains of life. Proc Natl Acad Sci USA 101(20):7716-7720.
20. Snyder JC, Young MJ (2011) Advances in understanding archaea-virus interactions in controlled and natural environments. Curr Opin Microbiol 14(4):497-503.
21. Lawrence CM, et al. (2009) Structural and functional studies of archaeal viruses. J Biol Chem 284(19):12599-12603.
22. Maaty WSA, et al. (2006) Characterization of the archaeal thermophile Sulfolobus turreted icosahedral virus validates an evolutionary link among double-stranded DNA viruses from all domains of life. J Virol 80(15):7625-7635.
23. Khayat R, Fu C-Y, Ortmann AC, Young MJ, Johnson JE (2010) The architecture and chemical stability of the archaeal Sulfolobus turreted icosahedral virus. J Virol 84(18): 9575-9583.
24. Fu C-Y, et al. (2010) In vivo assembly of an archaeal virus studied with whole-cell electron cryotomography. Structure 18(12):1579-1586.
25. Fu C-Y, Johnson JE (2012) Structure and cell biology of archaeal virus STIV. Curr Opin Virol 2(2):122-127.
26. Brumfield SK, et al. (2009) Particle assembly and ultrastructural features associated with replication of the lytic archaeal virus sulfolobus turreted icosahedral virus. J Virol 83(12):5964-5970.
27. Quax TEF, Krupovic M, Lucas S, Forterre P, Prangishvili D (2010) The Sulfolobus rodshaped virus 2 encodes a prominent structural component of the unique virion release system in Archaea. Virology 404(1):1-4.
28. Rosenthal PB, Henderson R (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 333(4):721-745.
29. Xiao L, Honig B (1999) Electrostatic contributions to the stability of hyperthermophilic proteins. J Mol Biol 289(5):1435-1444.
30. Benson SD, Bamford JK, Bamford DH, Burnett RM (1999) Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98(6): 825-833.
31. Ge M, Xia X-Y, Pan X-M (2008) Salt bridges in the hyperthermophilic protein Ssh10b are resilient to temperature increases. J Biol Chem 283(46):31690-31696.
32. Song L, et al. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274(5294):1859-1866.
33. Zubieta C, Schoehn G, Chroboczek J, Cusack S (2005) The structure of the human adenovirus 2 penton. Mol Cell 17(1):121-135.
34. Bebeacua C, et al. (2012) Visualizing a complete Siphoviridae member by singleparticle electron microscopy: The structure of lactococcal phage TP901-1. J Virol 87(2): 1061-1068.
35. Holm L, Rosenström P (2010) Dali server: Conservation mapping in 3D. Nucleic Acids Res 38(Web Server issue):W545-W549.
36. Konings WN, Albers S-V, Koning S, Driessen AJM (2002) The cell membrane plays a crucial role in survival of bacteria and archaea in extreme environments. Antonie van Leeuwenhoek 81(1-4):61-72.
37. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 305(3):567-580.
38. Veesler D, Johnson JE (2012) Virus maturation. Annu Rev Biophys 41:473-496.
39. Roseman AM (2004) FindEM-a fast, efficient program for automatic selection of particles from electron micrographs. J Struct Biol 145(1-2):91-99.
40. Lander GC, et al. (2009) Appion: An integrated, database-driven pipeline to facilitate EM image processing. J Struct Biol 166(1):95-102.
41. Mindell JA, Grigorieff N (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142(3):334-347.
42. Grigorieff N (2007) FREALIGN: High-resolution refinement of single particle structures. J Struct Biol 157(1):117-125.
43. Goddard TD, Huang CC, Ferrin TE (2007) Visualizing density maps with UCSF Chimera. J Struct Biol 157(1):281-287.
44. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.