Single particle cryoelectron tomography characterization of the structure and structural variability of poliovirus-receptor-membrane complex at 30 Å resolution

Journal of Structural Biology

Volumn 160, Issue 2, 2007, Pages 200-210

  Bostina, Mihnea ^a   Bubeck, Doryen ^a   Schwartz, Cindi ^b   Nicastro, Daniela ^b   Filman, David J ^a   Hogle, James M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Cell entry; Cryoelectron tomography; Poliovirus; Virus receptor membrane complex

Indexed keywords

MEMBRANE RECEPTOR;

ARTICLE; CLASSIFICATION; COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; CRYOELECTRON TOMOGRAPHY; IMAGE ANALYSIS; IMAGE PROCESSING; IN VITRO STUDY; MEMBRANE STRUCTURE; MICROSCOPE IMAGE; NONHUMAN; POLIOMYELITIS VIRUS; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; TOMOGRAPHY; VIRUS CELL INTERACTION; VIRUS PARTICLE;

ARTIFACTS; BIOPHYSICS; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; FOURIER ANALYSIS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; LIPOSOMES; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR CONFORMATION; POLIOVIRUS; RECEPTORS, VIRUS; TOMOGRAPHY; VIRION;

POLIOVIRUS;

EID: 35148838173     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2007.08.009     Document Type: Article

References (54)

1. Baumeister W. From proteomic inventory to architecture. FEBS Lett. 579 (2005) 933-937
2. Beck M., Forster F., Ecke M., Plitzko J.M., Melchior F., Gerisch G., Baumeister W., and Medalia O. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306 (2004) 1387-1390
3. 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
4. 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
5. Bohm J., Frangakis A.S., Hegerl R., Nickell S., Typke D., and Baumeister W. Toward detecting and identifying macromolecules in a cellular context: template matching applied to electron tomograms. Proc. Natl. Acad. Sci. USA 97 (2000) 14245-14250
6. Brandenburg B., Lee L.Y., Lakadamyali M., Rust M.J., Zhuang X., and Hogle J.M. Imaging poliovirus entry in live cells. PLoS Biol. 5 7 (2007) e183
7. 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-Å resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79 (2005) 7745-7755
8. 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
9. Cardone G., Winkler D.C., Trus B.L., Cheng N., Heuser J.E., Newcomb W.W., Brown J.C., and Steven A.C. Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361 (2007) 426-434
10. Chang J.T., Schmid M.F., Rixon F.J., and Chiu W. Electron cryotomography reveals the portal in the herpesvirus capsid. J. Virol. 81 (2007) 2065-2068
11. Cheng Y., Boll W., Kirchhausen T., Harrison S.C., and Walz T. Cryo-electron tomography of clathrin-coated vesicles: structural implications for coat assembly. J. Mol. Biol. 365 (2007) 892-899
12. Cheng Y., Zak O., Aisen P., Harrison S.C., and Walz T. Structure of the human transferrin receptor-transferrin complex. Cell 116 (2004) 565-576
13. Danthi P., Tosteson M., Li Q.H., and Chow M. Genome delivery and ion channel properties are altered in VP4 mutants of poliovirus. J. Virol. 77 (2003) 5266-5274
14. Deng B., O'Connor C.M., Kedes D.H., and Zhou Z.H. Direct visualization of the putative portal in the Kaposi's sarcoma-associated herpesvirus capsid by cryoelectron tomography. J. Virol. 81 (2007) 3640-3644
15. Diday E. La methode de nuees dynamiques. Rev. Stat. Appl. 19 (1971) 19-34
16. 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
17. Forster F., Medalia O., Zauberman N., Baumeister W., and Fass D. Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102 (2005) 4729-4734
18. Fotin A., Cheng Y., Sliz P., Grigorieff N., Harrison S.C., Kirchhausen T., and Walz T. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432 (2004) 573-579
19. Frangakis A.S., Bohm J., Forster F., Nickell S., Nicastro D., Typke D., Hegerl R., and Baumeister W. Identification of macromolecular complexes in cryoelectron tomograms of phantom cells. Proc. Natl. Acad. Sci. USA 99 (2002) 14153-14158
20. In: Frank J. (Ed). Electron Tomography: Methods for Three-dimensional Visualization of Structures in the Cell. second ed. (2006), Springer
21. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
22. Fricks C.E., and Hogle J.M. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64 (1990) 1934-1945
23. Garvalov B.K., Zuber B., Bouchet-Marquis C., Kudryashev M., Gruska M., Beck M., Leis A., Frischknecht F., Bradke F., Baumeister W., et al. Luminal particles within cellular microtubules. J. Cell Biol. 174 (2006) 759-765
24. Grunewald K., and Cyrklaff M. Structure of complex viruses and virus-infected cells by electron cryo tomography. Curr. Opin. Microbiol. 9 (2006) 437-442
25. Grunewald K., Desai P., Winkler D.C., Heymann J.B., Belnap D.M., Baumeister W., and Steven A.C. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302 (2003) 1396-1398
26. Harris A., Cardone G., Winkler D.C., Heymann J.B., Brecher M., White J.M., and Steven A.C. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl. Acad. Sci. USA 103 (2006) 19123-19127
27. 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
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 Å resolution. Science 229 (1985) 1358-1365
30. Joklik W.K., and Darnell Jr. J.E. The adsorption and early fate of purified poliovirus in HeLa cells. Virology 13 (1961) 439-447
31. Kremer J.R., Mastronarde D.N., and McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116 (1996) 71-76
32. Lucic V., Forster F., and Baumeister W. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 74 (2005) 833-865
33. Ludtke S.J., Chen D.H., Song J.L., Chuang D.T., and Chiu W. Seeing GroEL at 6 A resolution by single particle electron cryomicroscopy. Structure 12 (2004) 1129-1136
34. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152 (2005) 36-51
35. McIntosh R., Nicastro D., and Mastronarde D. New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol. 15 (2005) 43-51
36. Medalia O., Weber I., Frangakis A.S., Nicastro D., Gerisch G., and Baumeister W. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298 (2002) 1209-1213
37. Mendelsohn C.L., Wimmer E., and Racaniello V.R. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56 (1989) 855-865
38. Murphy G.E., Leadbetter J.R., and Jensen G.J. In situ structure of the complete Treponema primitia flagellar motor. Nature 442 (2006) 1062-1064
39. Nicastro D., McIntosh J.R., and Baumeister W. 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102 (2005) 15889-15894
40. Nicastro D., Schwartz C., Pierson J., Gaudette R., Porter M.E., and McIntosh J.R. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313 (2006) 944-948
41. Nickell S., Mihalache O., Beck F., Hegerl R., Korinek A., and Baumeister W. Structural analysis of the 26S proteasome by cryoelectron tomography. Biochem. Biophys. Res. Commun. 353 (2007) 115-120
42. Ortiz J.O., Forster F., Kurner J., Linaroudis A.A., and Baumeister W. Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition. J. Struct. Biol. 156 (2006) 334-341
43. 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
44. Rosenthal P.B., and Henderson R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333 (2003) 721-745
45. Saxton W.O., and Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127 (1982) 127-138
46. Schmid M.F., Paredes A.M., Khant H.A., Soyer F., Aldrich H.C., Chiu W., and Shively J.M. Structure of Halothiobacillus neapolitanus Carboxysomes by Cryo-electron Tomography. J. Mol. Biol. 364 (2006) 526-535
47. Subramaniam S. Bridging the imaging gap: visualizing subcellular architecture with electron tomography. Curr. Opin. Microbiol. 8 (2005) 316-322
48. Tosteson M.T., and Chow M. Characterization of the ion channels formed by poliovirus in planar lipid membranes. J. Virol. 71 (1997) 507-511
49. Tosteson M.T., Wang H., Naumov A., and Chow M. Poliovirus binding to its receptor in lipid bilayers results in particle-specific, temperature-sensitive channels. J. Gen. Virol. 85 (2004) 1581-1589
50. 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
51. van Heel M., and Schatz M. Fourier shell correlation threshold criteria. J. Struct. Biol. 151 (2005) 250-262
52. Walz J., Typke D., Nitsch M., Koster A.J., Hegerl R., and Baumeister W. Electron tomography of single ice-embedded macromolecules: three-dimensional alignment and classification. J. Struct. Biol. 120 (1997) 387-395
53. Zanetti, G., Briggs, J.A., Grunewald, K., Sattentau, Q.J., Fuller, S.D., 2007. Cryo-electron tomographic structure of an immunodeficiency virus envelope complex in situ. PLoS Pathog 2.
54. Zhu P., Liu J., Bess Jr. J., Chertova E., Lifson J.D., Grise H., Ofek G.A., Taylor K.A., and Roux K.H. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441 (2006) 847-852