Previous Article | Next Article 
Journal of Virology, February 2000, p. 1342-1354, Vol. 74, No. 3
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Molecular Tectonic Model of Virus Structural
Transitions: the Putative Cell Entry States of Poliovirus
David M.
Belnap,1
David J.
Filman,2
Benes L.
Trus,1,3
Naiqian
Cheng,1
Frank P.
Booy,1,
James F.
Conway,1
Stephen
Curry,2,
Chaitanya N.
Hiremath,2,§
Simon K.
Tsang,4
Alasdair C.
Steven,1 and
James M.
Hogle2,4,*
Laboratory of Structural Biology, National
Institute of Arthritis, Musculoskeletal and Skin
Diseases,1 and Computational Bioscience
and Engineering Laboratory, Center for Information
Technology,3 National Institutes of Health,
Bethesda, Maryland 20892; Department of Biological Chemistry
and Molecular Pharmacology, Harvard Medical School, Boston,
Massachusetts 021152; and Committee on
Higher Degrees in Biophysics, Harvard University, Cambridge,
Massachusetts 021384
Received 4 August 1999/Accepted 19 October 1999
Upon interacting with its receptor, poliovirus undergoes
conformational changes that are implicated in cell entry, including the
externalization of the viral protein VP4 and the N terminus of VP1. We
have determined the structures of native virions and of two putative
cell entry intermediates, the 135S and 80S particles, at ~22-Å
resolution by cryo-electron microscopy. The 135S and 80S particles are
both ~4% larger than the virion. Pseudoatomic models were
constructed by adjusting the beta-barrel domains of the three capsid
proteins VP1, VP2, and VP3 from their known positions in the virion to
fit the 135S and 80S reconstructions. Domain movements of up to 9 Å were detected, analogous to the shifting of tectonic plates. These
movements create gaps between adjacent subunits. The gaps at the sites
where VP1, VP2, and VP3 subunits meet are plausible candidates for the
emergence of VP4 and the N terminus of VP1. The implications of these
observations are discussed for models in which the externalized
components form a transmembrane pore through which viral RNA enters the
infected cell.
*
Corresponding author. Mailing address: Department of
Biological Chemistry and Molecular Pharmacology, Harvard Medical
School, Boston, MA 02115. Phone: (617) 432-3918. Fax: (617) 432-4360. E-mail: hogle{at}hogles.med.harvard.edu.

Present address: Department of Biochemistry, Wolfson Laboratory,
Imperial College, London SW7 1AY, United
Kingdom.

Present address: Biophysics Group, Blackett Laboratory, Imperial
College, London SW7 2BZ, United
Kingdom.
§
Present address: Fresenius Medical Care North America, Lexington,
MA
02420.
Journal of Virology, February 2000, p. 1342-1354, Vol. 74, No. 3
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Yamashita, T., Mori, Y., Miyazaki, N., Cheng, R. H., Yoshimura, M., Unno, H., Shima, R., Moriishi, K., Tsukihara, T., Li, T. C., Takeda, N., Miyamura, T., Matsuura, Y.
(2009). Biological and immunological characteristics of hepatitis E virus-like particles based on the crystal structure. Proc. Natl. Acad. Sci. USA
106: 12986-12991
[Abstract]
[Full Text]
-
Bourne, C. R., Finn, M. G., Zlotnick, A.
(2006). Global Structural Changes in Hepatitis B Virus Capsids Induced by the Assembly Effector HAP1. J. Virol.
80: 11055-11061
[Abstract]
[Full Text]
-
Agosto, M. A., Ivanovic, T., Nibert, M. L.
(2006). Mammalian reovirus, a nonfusogenic nonenveloped virus, forms size-selective pores in a model membrane. Proc. Natl. Acad. Sci. USA
103: 16496-16501
[Abstract]
[Full Text]
-
Stoeckl, L., Funk, A., Kopitzki, A., Brandenburg, B., Oess, S., Will, H., Sirma, H., Hildt, E.
(2006). Identification of a structural motif crucial for infectivity of hepatitis B viruses. Proc. Natl. Acad. Sci. USA
103: 6730-6734
[Abstract]
[Full Text]
-
Perez-Vargas, J., Romero, P., Lopez, S., Arias, C. F.
(2006). The Peptide-Binding and ATPase Domains of Recombinant hsc70 Are Required To Interact with Rotavirus and Reduce Its Infectivity.. J. Virol.
80: 3322-3331
[Abstract]
[Full Text]
-
Walukiewicz, H. E., Johnson, J. E., Schneemann, A.
(2006). Morphological Changes in the T=3 Capsid of Flock House Virus during Cell Entry. J. Virol.
80: 615-622
[Abstract]
[Full Text]
-
Kamper, N., Day, P. M., Nowak, T., Selinka, H.-C., Florin, L., Bolscher, J., Hilbig, L., Schiller, J. T., Sapp, M.
(2006). A Membrane-Destabilizing Peptide in Capsid Protein L2 Is Required for Egress of Papillomavirus Genomes from Endosomes. J. Virol.
80: 759-768
[Abstract]
[Full Text]
-
Farr, G. A., Cotmore, S. F., Tattersall, P.
(2006). VP2 Cleavage and the Leucine Ring at the Base of the Fivefold Cylinder Control pH-Dependent Externalization of both the VP1 N Terminus and the Genome of Minute Virus of Mice. J. Virol.
80: 161-171
[Abstract]
[Full Text]
-
Tuthill, T. J., Bubeck, D., Rowlands, D. J., Hogle, J. M.
(2006). 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: 172-180
[Abstract]
[Full Text]
-
Goodfellow, I. G., Evans, D. J., Blom, A. M., Kerrigan, D., Miners, J. S., Morgan, B. P., Spiller, O. B.
(2005). Inhibition of Coxsackie B Virus Infection by Soluble Forms of Its Receptors: Binding Affinities, Altered Particle Formation, and Competition with Cellular Receptors. J. Virol.
79: 12016-12024
[Abstract]
[Full Text]
-
Liu, W., Hsu, C.-H., Hong, Y.-R., Wu, S.-C., Wang, C.-H., Wu, Y.-M., Chao, C.-B., Lin, C.-S.
(2005). Early endocytosis pathways in SSN-1 cells infected by dragon grouper nervous necrosis virus. J. Gen. Virol.
86: 2553-2561
[Abstract]
[Full Text]
-
O'Donnell, V., LaRocco, M., Duque, H., Baxt, B.
(2005). Analysis of Foot-and-Mouth Disease Virus Internalization Events in Cultured Cells. J. Virol.
79: 8506-8518
[Abstract]
[Full Text]
-
Berryman, S., Clark, S., Monaghan, P., Jackson, T.
(2005). Early Events in Integrin {alpha}v{beta}6-Mediated Cell Entry of Foot-and-Mouth Disease Virus. J. Virol.
79: 8519-8534
[Abstract]
[Full Text]
-
Pesavento, J. B., Crawford, S. E., Roberts, E., Estes, M. K., Prasad, B. V. V.
(2005). pH-Induced Conformational Change of the Rotavirus VP4 Spike: Implications for Cell Entry and Antibody Neutralization. J. Virol.
79: 8572-8580
[Abstract]
[Full Text]
-
Bubeck, D., Filman, D. J., Cheng, N., Steven, A. C., Hogle, J. M., Belnap, D. M.
(2005). 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: 7745-7755
[Abstract]
[Full Text]
-
Bleker, S., Sonntag, F., Kleinschmidt, J. A.
(2005). Mutational Analysis of Narrow Pores at the Fivefold Symmetry Axes of Adeno-Associated Virus Type 2 Capsids Reveals a Dual Role in Genome Packaging and Activation of Phospholipase A2 Activity. J. Virol.
79: 2528-2540
[Abstract]
[Full Text]
-
Johansson, E. S., Xing, L., Cheng, R. H., Shafren, D. R.
(2004). Enhanced Cellular Receptor Usage by a Bioselected Variant of Coxsackievirus A21. J. Virol.
78: 12603-12612
[Abstract]
[Full Text]
-
Cavaldesi, M., Caruso, M., Sthandier, O., Amati, P., Garcia, M. I.
(2004). Conformational Changes of Murine Polyomavirus Capsid Proteins Induced by Sialic Acid Binding. J. Biol. Chem.
279: 41573-41579
[Abstract]
[Full Text]
-
Odegard, A. L., Chandran, K., Zhang, X., Parker, J. S. L., Baker, T. S., Nibert, M. L.
(2004). Putative Autocleavage of Outer Capsid Protein {micro}1, Allowing Release of Myristoylated Peptide {micro}1N during Particle Uncoating, Is Critical for Cell Entry by Reovirus. J. Virol.
78: 8732-8745
[Abstract]
[Full Text]
-
Monaghan, P., Cook, H., Jackson, T., Ryan, M., Wileman, T.
(2004). The ultrastructure of the developing replication site in foot-and-mouth disease virus-infected BHK-38 cells. J. Gen. Virol.
85: 933-946
[Abstract]
[Full Text]
-
Hewat, E. A., Blaas, D.
(2004). Cryoelectron Microscopy Analysis of the Structural Changes Associated with Human Rhinovirus Type 14 Uncoating. J. Virol.
78: 2935-2942
[Abstract]
[Full Text]
-
Reguera, J., Carreira, A., Riolobos, L., Almendral, J. M., Mateu, M. G.
(2004). Role of interfacial amino acid residues in assembly, stability, and conformation of a spherical virus capsid. Proc. Natl. Acad. Sci. USA
101: 2724-2729
[Abstract]
[Full Text]
-
Nurani, G., Lindqvist, B., Casasnovas, J. M.
(2003). Receptor Priming of Major Group Human Rhinoviruses for Uncoating and Entry at Mild Low-pH Environments. J. Virol.
77: 11985-11991
[Abstract]
[Full Text]
-
Verdaguer, N., Jimenez-Clavero, M. A., Fita, I., Ley, V.
(2003). Structure of Swine Vesicular Disease Virus: Mapping of Changes Occurring during Adaptation of Human Coxsackie B5 Virus To Infect Swine. J. Virol.
77: 9780-9789
[Abstract]
[Full Text]
-
Xing, L., Casasnovas, J. M., Cheng, R. H.
(2003). Structural Analysis of Human Rhinovirus Complexed with ICAM-1 Reveals the Dynamics of Receptor-Mediated Virus Uncoating. J. Virol.
77: 6101-6107
[Abstract]
[Full Text]
-
Danthi, P., Tosteson, M., Li, Q.-h., Chow, M.
(2003). Genome Delivery and Ion Channel Properties Are Altered in VP4 Mutants of Poliovirus. J. Virol.
77: 5266-5274
[Abstract]
[Full Text]
-
Paredes, A., Alwell-Warda, K., Weaver, S. C., Chiu, W., Watowich, S. J.
(2002). Structure of Isolated Nucleocapsids from Venezuelan Equine Encephalitis Virus and Implications for Assembly and Disassembly of Enveloped Virus. J. Virol.
77: 659-664
[Abstract]
[Full Text]
-
Chandran, K., Farsetta, D. L., Nibert, M. L.
(2002). Strategy for Nonenveloped Virus Entry: a Hydrophobic Conformer of the Reovirus Membrane Penetration Protein {micro}1 Mediates Membrane Disruption. J. Virol.
76: 9920-9933
[Abstract]
[Full Text]
-
Stuart, A. D., Eustace, H. E., McKee, T. A., Brown, T. D. K.
(2002). A Novel Cell Entry Pathway for a DAF-Using Human Enterovirus Is Dependent on Lipid Rafts. J. Virol.
76: 9307-9322
[Abstract]
[Full Text]
-
Cherkasova, E. A., Korotkova, E. A., Yakovenko, M. L., Ivanova, O. E., Eremeeva, T. P., Chumakov, K. M., Agol, V. I.
(2002). Long-Term Circulation of Vaccine-Derived Poliovirus That Causes Paralytic Disease. J. Virol.
76: 6791-6799
[Abstract]
[Full Text]
-
Bloom, M. E., Best, S. M., Hayes, S. F., Wells, R. D., Wolfinbarger, J. B., McKenna, R., Agbandje-McKenna, M.
(2001). Identification of Aleutian Mink Disease Parvovirus Capsid Sequences Mediating Antibody-Dependent Enhancement of Infection, Virus Neutralization, and Immune Complex Formation. J. Virol.
75: 11116-11127
[Abstract]
[Full Text]
-
Tsang, S. K., McDermott, B. M., Racaniello, V. R., Hogle, J. M.
(2001). Kinetic Analysis of the Effect of Poliovirus Receptor on Viral Uncoating: the Receptor as a Catalyst. J. Virol.
75: 4984-4989
[Abstract]
[Full Text]
-
Ishikawa, T., Beuron, F., Kessel, M., Wickner, S., Maurizi, M. R., Steven, A. C.
(2001). Translocation pathway of protein substrates in ClpAP protease. Proc. Natl. Acad. Sci. USA
10.1073/pnas.081543698v1
[Abstract]
[Full Text]
-
Joki-Korpela, P., Marjomäki, V., Krogerus, C., Heino, J., Hyypiä, T.
(2001). Entry of Human Parechovirus 1. J. Virol.
75: 1958-1967
[Abstract]
[Full Text]
-
Airaksinen, A., Roivainen, M., Hovi, T.
(2001). Coxsackievirus A9 VP1 Mutants with Enhanced or Hindered A Particle Formation and Decreased Infectivity. J. Virol.
75: 952-960
[Abstract]
[Full Text]
-
Jiménez-Clavero, M. A., Escribano-Romero, E., Douglas, A. J., Ley, V.
(2001). The N-Terminal Region of the VP1 Protein of Swine Vesicular Disease Virus Contains a Neutralization Site That Arises upon Cell Attachment and Is Involved in Viral Entry. J. Virol.
75: 1044-1047
[Abstract]
[Full Text]
-
Belnap, D. M., McDermott, B. M. Jr., Filman, D. J., Cheng, N., Trus, B. L., Zuccola, H. J., Racaniello, V. R., Hogle, J. M., Steven, A. C.
(2000). From the Cover: Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc. Natl. Acad. Sci. USA
97: 73-78
[Abstract]
[Full Text]
-
McDermott, B. M. Jr., Rux, A. H., Eisenberg, R. J., Cohen, G. H., Racaniello, V. R.
(2000). Two Distinct Binding Affinities of Poliovirus for Its Cellular Receptor. J. Biol. Chem.
275: 23089-23096
[Abstract]
[Full Text]
-
Ishikawa, T., Beuron, F., Kessel, M., Wickner, S., Maurizi, M. R., Steven, A. C.
(2001). Translocation pathway of protein substrates in ClpAP protease. Proc. Natl. Acad. Sci. USA
98: 4328-4333
[Abstract]
[Full Text]