Post-imaging fiducial markers aid in the orientation determination of complexes with mixed or unknown symmetry

Journal of Structural Biology

Volumn 162, Issue 3, 2008, Pages 480-490

  Bubeck, Doryen ^a   Filman, David J ^b   Kuzmin, Mikhail ^a   Fuller, Stephen D ^a   Hogle, James M ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cryo electron microscopy; Enveloped virus; Image processing; Mixed symmetry; Non enveloped virus; Three dimensional electron microscopy; Unknown symmetry; Virus cell entry

Indexed keywords

ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; IMAGING; IMAGING SYSTEM; MEMBRANE COMPONENT; NONHUMAN; PRIORITY JOURNAL; SEMLIKI FOREST ALPHAVIRUS;

ALGORITHMS; CRYOELECTRON MICROSCOPY; HELA CELLS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; LIPOSOMES; MEMBRANE FUSION; MICROSCOPY, ELECTRON; RECEPTORS, VIRUS; REPRODUCIBILITY OF RESULTS; SEMLIKI FOREST VIRUS; SOFTWARE; VIRAL ENVELOPE PROTEINS;

POLIOVIRUS; RABBIT FIBROMA VIRUS; SEMLIKI FOREST VIRUS;

EID: 44649090598     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2008.03.006     Document Type: Article

References (48)

1. Agirrezabala X., Martin-Benito J., Caston J.R., Miranda R., Valpuesta J.M., and Carrascosa J.L. Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J. 24 (2005) 3820-3829
2. Baker T.S., and Cheng R.H. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116 (1996) 120-130
3. Baker T.S., Olson N.H., and Fuller S.D. Adding the third dimension to virus lifecycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol. Mol. Bio. Rev. 63 1 (1999) 237
4. Belnap D.M., Filman D.J., Trus B.L., Cheng N., Booy F.P., Conway J.F., Curry S., Hiremath C.N., Tsang S.K., Steven A.C., and Hogle J.M. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74 (2000) 1342-1354
5. Belnap D.M., McDermott Jr. B.M., Filman D.J., Cheng N., Trus B.L., Zuccola H.J., Racaniello V.R., Hogle J.M., and Steven A.C. Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc. Natl. Acad. Sci. USA 97 (2000) 73-78
6. Bohm J., Lambert O., Frangakis A.S., Letellier L., Baumeister W., and Rigaud J.L. FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. Curr. Biol. 11 (2001) 1168-1175
7. Box G., and Muller M. A note on the generation of random normal deviates. Ann. Math. Stat. 29 (1958) 610-611
8. Briggs J.A., Huiskonen J.T., Fernando K.V., Gilbert R.J., Scotti P., Butcher S.J., and Fuller S.D. Classification and three-dimensional reconstruction of unevenly distributed or symmetry mismatched features of icosahedral particles. J. Struct. Biol. 150 (2005) 332-339
9. Bubeck D., Filman D.J., Cheng N., Steven A.C., Hogle J.M., and Belnap D.M. The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79 (2005) 7745-7755
10. Bubeck D., Filman D.J., and Hogle J.M. Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat. Struct. Mol. Biol. 12 (2005) 615-618
11. Cerritelli M.E., Trus B.L., Smith C.S., Cheng N., Conway J.F., and Steven A.C. A second symmetry mismatch at the portal vertex of bacteriophage T7: 8-fold symmetry in the procapsid core. J. Mol. Biol. 327 (2003) 1-6
12. Chiu W., Baker M.L., Jiang W., Dougherty M., and Schmid M.F. Electron cryomicroscopy of biological machines at subnanometer resolution. Structure 13 (2005) 363-372
13. Collaborative Computational Project, N. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
14. Conway J.F., and Steven A.C. Methods for reconstructing density maps of "single" particles from cryoelectron micrographs to subnanometer resolution. J. Struct. Biol. 128 (1999) 106-118
15. Conway J.F., Wikoff W.R., Cheng N., Duda R.L., Hendrix R.W., Johnson J.E., and Steven A.C. Virus maturation involving large subunit rotations and local refolding. Science 292 (2001) 744-748
16. Crowther R.A., Amos L.A., Finch J.T., De Rosier D.J., and Klug A. Three dimensional reconstructions of spherical viruses by fourier synthesis from electron micrographs. Nature 226 (1970) 421-425
17. Dubochet J., Adrian M., Chang J.J., Homo J.C., Lepault J., McDowall A.W., and Schultz P. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21 (1988) 129-228
18. Fokine A., Kostyuchenko V.A., Efimov A.V., Kurochkina L.P., Sykilinda N.N., Robben J., Volckaert G., Hoenger A., Chipman P.R., Battisti A.J., Rossmann M.G., and Mesyanzhinov V.V. A three-dimensional cryo-electron microscopy structure of the bacteriophage phiKZ head. J. Mol. Biol. 352 (2005) 117-124
19. Fuller S.D. The T = 4 envelope of Sindbis virus is organized by complementary interactions with a T = 3 icosahedral capsid. Cell 48 (1987) 923-934
20. Fuller S.D., Butcher S.J., Cheng R.H., and Baker T.S. Three-dimensional reconstruction of icosahedral particles -The uncommon line. J. Struct. Biol. 116 (1996) 48-55
21. Fuller S.D., Berriman J.A., Butcher S.J., and Gowen B.E. Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex. Cell 81 (1995) 715-725
22. Gibbons D.L., Erk I., Reilly B., Navaza J., Kielian M., Rey F.A., and Lepault J. Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography. Cell 114 (2003) 573-583
23. Gibbons D.L., Ahn A., Liao M., Hammar L., Cheng R.H., and Kielian M. Multistep regulation of membrane insertion of the fusion peptide of Semliki Forest virus. J. Virol. 78 (2004) 3312-3318
24. Glomb-Reinmund S., and Kielian M. fus-1, A pH shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit. J. Virol. 72 (1998) 4281-4287
25. He Y., Bowman V.D., Mueller S., Bator C.M., Bella J., Peng X., Baker T.S., Wimmer E., Kuhn R.J., and Rossmann M.G. Interaction of the poliovirus receptor with poliovirus. Proc. Natl. Acad. Sci. USA 97 (2000) 79-84
26. He Y., Mueller S., Chipman P.R., Bator C.M., Peng X., Bowman V.D., Mukhopadhyay S., Wimmer E., Kuhn R.J., and Rossmann M.G. Complexes of poliovirus serotypes with their common cellular receptor, CD155. J. Virol. 77 (2003) 4827-4835
27. Heymann J.B. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133 (2001) 156-169
28. Hogle J.M. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56 (2002) 677-702
29. Hogle J.M., Chow M., and Filman D.J. Three-dimensional structure of poliovirus at 2.9 A resolution. Science 229 (1985) 1358-1365
30. Jiang W., Chang J., Jakana J., Weigele P., King J., and Chiu W. Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439 (2006) 612-616
31. Joklik E.K., and Darnell Jr. J.E. The adsorption and early fate of purified poliovirus in HeLa cells. Virology 13 (1961) 439-447
32. Kolatkar P.R., Bella J., Olson N.H., Bator C.M., Baker T.S., and Rossmann M.G. Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J. 18 (1999) 6249-6259
33. Liao M., and Kielian M. Site-directed antibodies against the stem region reveal low pH-induced conformational changes of the Semliki Forest virus fusion protein. J. Virol. 80 (2006) 9599-9607
34. Lata R., Conway J.F., Cheng N., Duda R.L., Hendrix R.W., Wikoff W.R., Johnson J.E., Tsuruta H., and Steven A.C. Maturation dynamics of a viral capsid: visualization of transitional intermediate states. Cell 100 (2000) 253-263
35. Mancini E.J., Clarke M., Gowen B.E., Rutten T., and Fuller S.D. Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus. Mol. Cell 5 (2000) 255-266
36. McDermott Jr. B.M., Rux A.H., Eisenberg R.J., Cohen G.H., and Racaniello V.R. Two distinct binding affinities of poliovirus for its cellular receptor. J. Biol. Chem. 275 (2000) 23089-23096
37. Morais M.C., Tao Y., Olson N.H., Grimes S., Jardine P.J., Anderson D.L., Baker T.S., and Rossmann M.G. Cryoelectron-microscopy image reconstruction of symmetry mismatches in bacteriophage phi29. J. Struct. Biol. 135 (2001) 38-46
38. Paredes A.M., Ferreira D., Horton M., Saad A., Tsuruta H., Johnston R., Klimstra W., Ryman K., Hernandez R., Chiu W., and Brown D.T. Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virology 324 (2004) 373-386
39. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
40. Saban S.D., Nepomuceno R.R., Gritton L.D., Nemerow G.R., and Stewart P.L. CryoEM structure at 9 A resolution of an adenovirus vector targeted to hematopoietic cells. J. Mol. Biol. 349 (2005) 526-537
41. Tao Y., Olson N.H., Xu W., Anderson D.L., Rossmann M.G., and Baker T.S. Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95 (1998) 431-437
42. Thomas, W., Kelley, C., 1991. GNUPLOT 3.0, An Interactive Plotting Program.
43. Tuthill T.J., Bubeck D., Rowlands D.J., and Hogle J.M. Characterization of early steps in the poliovirus infection process: receptor-decorated liposomes induce conversion of the virus to membrane-anchored entry-intermediate particles. J. Virol. 80 (2006) 172-180
44. White J., and Helenius A. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc. Natl. Acad. Sci. USA 77 (1980) 3273-3277
45. Wikoff W.R., Conway J.F., Tang J., Lee K.K., Gan L., Cheng N., Duda R.L., Hendrix R.W., Steven A.C., and Johnson J.E. Time-resolved molecular dynamics of bacteriophage HK97 capsid maturation interpreted by electron cryo-microscopy and X-ray crystallography. J. Struct. Biol. 153 (2006) 300-306
46. Wu S., Haag L., Hammar L., Wu B., Garrof H., Xing L., Murata K., and Cheng R.H. The dynamic envelope of a fusion class II virus. J. Biol. Chem. 282 (2007) 6752-6762
47. Xing L., Tjarnlund K., Lindqvist B., Kaplan G.G., Feigelstock D., Cheng R.H., and Casasnovas J.M. Distinct cellular receptor interactions in poliovirus and rhinoviruses. EMBO J. 19 (2000) 1207-1216
48. Yeates T.O., Jacobson D.H., Martin A., Wychowski C., Girard M., Filman D.J., and Hogle J.M. Three-dimensional structure of a mouse-adapted type 2/type 1 poliovirus chimera. EMBO J. 10 (1991) 2331-2341