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Structure of viruses: a short history

  • Michael G. Rossmann (a1)
Abstract

This review is a partially personal account of the discovery of virus structure and its implication for virus function. Although I have endeavored to cover all aspects of structural virology and to acknowledge relevant individuals, I know that I have favored taking examples from my own experience in telling this story. I am anxious to apologize to all those who I might have unintentionally offended by omitting their work.

The first knowledge of virus structure was a result of Stanley's studies of tobacco mosaic virus (TMV) and the subsequent X-ray fiber diffraction analysis by Bernal and Fankuchen in the 1930s. At about the same time it became apparent that crystals of small RNA plant and animal viruses could diffract X-rays, demonstrating that viruses must have distinct and unique structures. More advances were made in the 1950s with the realization by Watson and Crick that viruses might have icosahedral symmetry. With the improvement of experimental and computational techniques in the 1970s, it became possible to determine the three-dimensional, near-atomic resolution structures of some small icosahedral plant and animal RNA viruses. It was a great surprise that the protecting capsids of the first virus structures to be determined had the same architecture. The capsid proteins of these viruses all had a ‘jelly-roll’ fold and, furthermore, the organization of the capsid protein in the virus were similar, suggesting a common ancestral virus from which many of today's viruses have evolved. By this time a more detailed structure of TMV had also been established, but both the architecture and capsid protein fold were quite different to that of the icosahedral viruses. The small icosahedral RNA virus structures were also informative of how and where cellular receptors, anti-viral compounds, and neutralizing antibodies bound to these viruses. However, larger lipid membrane enveloped viruses did not form sufficiently ordered crystals to obtain good X-ray diffraction. Starting in the 1990s, these enveloped viruses were studied by combining cryo-electron microscopy of the whole virus with X-ray crystallography of their protein components. These structures gave information on virus assembly, virus neutralization by antibodies, and virus fusion with and entry into the host cell. The same techniques were also employed in the study of complex bacteriophages that were too large to crystallize. Nevertheless, there still remained many pleomorphic, highly pathogenic viruses that lacked the icosahedral symmetry and homogeneity that had made the earlier structural investigations possible. Currently some of these viruses are starting to be studied by combining X-ray crystallography with cryo-electron tomography.

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*Author for correspondence: M. G. Rossmann, Department of Biological Sciences, 240 S. Martin Jischke Drive, Purdue University, West Lafayette, IN 47907-2032, USA. Tel.:(765) 494-4911; Fax: (765) 496-1189; Email: mr@purdue.edu
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Aathavan, K., Politzer, A. T., Kaplan, A., Moffitt, J. R., Chemla, Y. R., Grimes, S., Jardine, P. J., Anderson, D. L. & Bustamante, C. (2009). Substrate interactions and promiscuity in a viral DNA packaging motor. Nature 461, 669673.
Abad-Zapatero, C., Abdel-Meguid, S. S., Johnson, J. E., Leslie, A. G. W., Rayment, I., Rossmann, M. G., Suck, D. & Tsukihara, T. (1980). Structure of southern bean mosaic virus at 2·8 Å resolution. Nature 286, 3339.
Abrescia, N. G., Grimes, J. M., Kivela, H. M., Assenberg, R., Sutton, G. C., Butcher, S. J., Bamford, J. K., Bamford, D. H. & Stuart, D. I. (2008). Insights into virus evolution and membrane biogenesis from the structure of the marine lipid-containing bacteriophage PM2. Molecular Cell 31, 749761.
Abrescia, N. G. A., Cockburn, J. J. B., Grimes, J. M., Sutton, G. C., Diprose, J. M., Butcher, S. J., Fuller, S. D., San Martin, C., Burnett, R. M., Stuart, D. I., Bamford, D. H. & Bamford, J. K. H. (2004). Insights into assembly from structural analysis of bacteriophage PRD1. Nature 432, 6874.
Acharya, R., Fry, E., Stuart, D., Fox, G., Rowlands, D. & Brown, F. (1989). The three-dimensional structure of foot-and-mouth disease virus at 2·9 Å resolution. Nature 337, 709716.
Adrian, M., Dubochet, J., Lepault, J. & McDowall, A. W. (1984). Cryo-electron microscopy of viruses. Nature 308, 3236.
Agbandje, M., McKenna, R., Rossmann, M. G., Strassheim, M. L. & Parrish, C. R. (1993). Structure determination of feline panleukopenia virus empty particles. Proteins 16, 155171.
Agbandje-McKenna, M., Llamas-Saiz, A. L., Wang, F., Tattersall, P. & Rossmann, M. G. (1998). Functional implications of the structure of the murine parvovirus, minute virus of mice. Structure 6, 13691381.
Åkervall, K., Strandberg, B., Rossmann, M. G., Bengtsson, U., Fridborg, K., Johannisen, H., Kannan, K. K., Lövgren, S., Petef, G., Öberg, B., Eaker, D., Hjertén, S., Rydén, L. & Moring, I. (1972). X-ray diffraction studies of the structure of satellite tobacco necrosis virus. Cold Spring Harbor Symposia on Quantitative Biology 36, 469483.
Aksyuk, A. A., Kurochkina, L. P., Fokine, A., Forouhar, F., Mesyanzhinov, V. V., Tong, L. & Rossmann, M. G. (2011). Structural conservation of the Myoviridae phage tail sheath protein fold. Structure 19, 18851894.
Aksyuk, A. A., Leiman, P. G., Kurochkina, L. P., Schneider, M. M., Kostyuchenko, V. A., Mesyanzhinov, V. V. & Rossmann, M. G. (2009a). The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO Journal 28, 821829.
Aksyuk, A. A., Leiman, P. G., Shneider, M. M., Mesyanzhinov, V. V. & Rossmann, M. G. (2009b). The structure of gene product 6 of bacteriophage T4, the hinge-pin of the baseplate. Structure 17, 800808.
Allison, S. L., Schalich, J., Stiasny, K., Mandl, C. W. & Heinz, F. X. (2001). Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. Journal of Virology 75, 42684275.
Allison, S. L., Schalich, J., Stiasny, K., Mandl, C. W., Kunz, C. & Heinz, F. X. (1995). Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. Journal of Virology 69, 695700.
Allison, S. L., Stiasny, K., Stadler, K., Mandl, C. W. & Heinz, F. X. (1999). Mapping of functional elements in the stem-anchor region of tick-borne encephalitis virus envelope protein E. Journal of Virology 73, 56055612.
Argos, P. & Rossmann, M. G. (1974). Determining heavy-atom positions using non-crystallographic symmetry. Acta Crystallographica Section A 30, 672677.
Arndt, U. W. & Wonacott, A. J. (1977). The Rotation Method in Crystallography: Data Collection from Macromolecular Crystals. Amsterdam: North-Holland.
Arnold, E., Himmel, D. M. & Rossmann, M. G. (2012). International Tables for Crystallography, Volume F, Crystallography of Biological Macromolecules. West Sussex, UK: John Wiley & Sons, Ltd.
Arnold, E., Vriend, G., Luo, M., Griffith, J. P., Kamer, G., Erickson, J. W., Johnson, J. E. & Rossmann, M. G. (1987). The structure determination of a common cold virus, human rhinovirus 14. Acta Crystallographica Section A 43, 346361.
Athappilly, F. K., Murali, R., Rux, J. J., Cai, Z. & Burnett, R. M. (1994). The refined crystal structure of hexon, the major coat protein of adenovirus type 2, at 2·9 Å resolution. Journal of Molecular Biology 242, 430455.
Baker, M. L., Jiang, W., Rixon, F. J. & Chiu, W. (2005). Common ancestry of herpesvirus and tailed DNA bacteriophages. Journal of Virology 79, 1496714970.
Baker, T. S., Caspar, D. L. & Murakami, W. T. (1983). Polyoma virus ‘hexamer’ tubes consist of paired pentamers. Nature 303, 446448.
Baker, T. S., Newcomb, W. W., Olson, N. H., Cowsert, L. M., Olson, C. & Brown, J. C. (1991). Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophysical Journal 60, 14451456.
Bamford, D. H., Grimes, J. M. & Stuart, D. I. (2005). What does structure tell us about virus evolution? Current Opinion in Structural Biology 15, 655663.
Bartual, S. G., Otero, J. M., Garcia-Doval, C., Llamas-Saiz, A. L., Kahn, R., Fox, G. C. & van Raaij, M. J. (2010). Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proceedings of the National Academy of Sciences of the United States of America 107, 2028720292.
Battisti, A. J., Meng, G., Winkler, D. C., McGinnes, L. W., Plevka, P., Steven, A. C., Morrison, T. G. & Rossmann, M. G. (2012). Structure and assembly of a paramyxovirus matrix protein. Proceedings of the National Academy of Sciences of the United States of America 109, 1399614000.
Bella, J., Kolatkar, P. R., Marlor, C. W., Greve, J. M. & Rossmann, M. G. (1998). The structure of the two amino-terminal domains of human ICAM-1 suggests how it functions as a rhinovirus receptor and as an LFA-1 integrin ligand. Proceedings of the National Academy of Sciences of the United States of America 95, 41404145.
Bella, J., Kolatkar, P. R., Marlor, C. W., Greve, J. M. & Rossmann, M. G. (1999). The structure of the two amino-terminal domains of human intercellular adhesion molecule-1 suggests how it functions as a rhinovirus receptor. Virus Research 62, 107117.
Benson, S. D., Bamford, J. K. H., Bamford, D. H. & Burnett, R. M. (2004). Does common architecture reveal a viral lineage spanning all three domains of life? Molecular Cell 16, 673685.
Berget, P. B. & King, J. (1978). Isolation and characterization of precursors in T4 baseplate assembly. The complex of gene 10 and gene 11 products. Journal of Molecular Biology 124, 469486.
Bernal, J. D. & Fankuchen, I. (1937). Structure types of protein crystals from virus-infected plants. Nature 139, 923924.
Bernal, J. D. & Fankuchen, I. (1941). X-Ray and crystallographic studies of plant virus preparations : I. Introduction and preparation of specimens. II. Modes of aggregation of the virus particles. III. (1) The structure of the particles and (2) biological implications. Journal of General Physiology 25, 111165.
Bloomer, A. C., Champness, J. N., Bricogne, G., Staden, R. & Klug, A. (1978). Protein disk of tobacco mosaic virus at 2·8 Å resolution showing the interactions within and between subunits. Nature 276, 362368.
Bostina, M., Bubeck, D., Schwartz, C., Nicastro, D., Filman, D. J. & Hogle, J. M. (2007). Single particle cryoelectron tomography characterization of the structure and structural variability of poliovirus-receptor-membrane complex at 30 Å resolution. Journal of Structural Biology 160, 200210.
Bostina, M., Levy, H., Filman, D. J. & Hogle, J. M. (2011). Poliovirus RNA is released from the capsid near a twofold symmetry axis. Journal of Virology 83, 776783.
Bragg, W. H. & Bragg, W. L. (1913). The reflection of X-rays in crystals. Proceedings of the Royal Society of London. Series A, Mathematical and Physical Sciences 88, 428438.
Bragg, W. L. (1913). The structure of some crystals as indicated by their diffraction of X-rays. Proceedings of the Royal Society of London. Series A, Mathematical and Physical Sciences 89, 248277.
Brenner, S. & Horne, R. W. (1959). A negative staining method for high resolution electron microscopy of viruses. Biochimica et Biophysica Acta 34, 103110.
Bressanelli, S., Stiasny, K., Allison, S. L., Stura, E. A., Duquerroy, S., Lescar, J., Heinz, F. X. & Rey, F. A. (2004). Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO Journal 23, 728738.
Brinton, M. A. (2002). The molecular biology of West Nile virus: a new invader of the western hemisphere. Annual Review of Microbiology 56, 371402.
Brown, J. C. & Newcomb, W. W. (2011). Herpesvirus capsid assembly: insights from structural analysis. Current Opinion in Virology 1, 142149.
Browning, C., Shneider, M. M., Bowman, V. D., Schwarzer, D. & Leiman, P. G. (2012). Phage pierces the host cell membrane with the iron-loaded spike. Structure 20, 326339.
Buehner, M., Ford, G. C., Moras, D., Olsen, K. W. & Rossmann, M. G. (1974). Structure determination of crystalline lobster D-glyceraldehyde-3-phosphate dehydrogenase. Journal of Molecular Biology 82, 563585.
Burke, D. S. & Monath, T. P. (2001). Flaviviruses. In Fields Virology (eds. Knipe, D. M. & Howley, P. M.), pp. 10431125. Philadelphia: Lippincott Williams & Wilkins.
Butler, P. J. & Klug, A. (1972). Assembly of tobacco mosaic virus in vitro: effect of state of polymerization of the protein component. Proceedings of the National Academy of Sciences of the United States of America 69, 29502953.
Büttner, C. R., Chechik, M., Ortiz-Lombardia, M., Smits, C., Ebong, I. O., Chechik, V., Jeschke, G., Dykeman, E., Benini, S., Robinson, C. V., Alonso, J. C. & Antson, A. A. (2012). Structural basis for DNA recognition and loading into a viral packaging motor. Proceedings of the National Academy of Sciences of the United States of America 109, 811816.
Calendar, R. (2006). The Bacteriophages (ed. Calendar, R.). New York: Oxford University Press.
Canaan, S., Zadori, Z., Ghomashchi, F., Bollinger, J., Sadilek, M., Moreau, M. E., Tijssen, P. & Gelb, M. H. (2004). Interfacial enzymology of parvovirus phospholipases A2. The Journal of Biological Chemistry 279, 1450214508.
Caspar, D. L. D. (1956). Structure of bushy stunt virus. Nature 177, 475476.
Caspar, D. L. D. & Klug, A. (1962). Physical principles in the construction of regular viruses. Cold Spring Harbor Symposia on Quantitative Biology 27, 124.
Champness, J. N., Bloomer, A. C., Bricogne, G., Butler, P. G. & Klug, A. (1976). The structure of the protein disk of tobacco mosaic virus to 5 Å resolution. Nature 259, 2024.
Chapman, M. S. & Rossmann, M. G. (1996). Structural refinement of the DNA-containing capsid of canine parvovirus using RSRef, a resolution-dependent stereochemically restrained real-space refinement method. Acta Crystallographica Section D: Biological Crystallography 52, 129142.
Chapman, M. S., Tsao, J. & Rossmann, M. G. (1992). Ab initio phase determination for spherical viruses: parameter determination for spherical-shell models. Acta Crystallogaphica Section A 48, 301312.
Chen, Z. G., Stauffacher, C., Li, Y., Schmidt, T., Bomu, W., Kamer, G., Shanks, M., Lomonossoff, G. & Johnson, J. E. (1989). Protein-RNA interactions in an icosahedral virus at 3·0 Å resolution. Science 245, 154159.
Cheng, R. H., Kuhn, R. J., Olson, N. H., Rossmann, M. G., Choi, H. K., Smith, T. J. & Baker, T. S. (1995). Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 80, 621630.
Cherrier, M. V., Kostyuchenko, V. A., Xiao, C., Bowman, V. D., Battisti, A. J., Yan, X., Chipman, P. R., Baker, T. S., Van Etten, J. L. & Rossmann, M. G. (2009). An icosahedral algal virus has a complex unique vertex decorated by a spike. Proceedings of the National Academy of Sciences of the United States of America 106, 1108511089.
Choi, H. K., Tong, L., Minor, W., Dumas, P., Boege, U., Rossmann, M. G. & Wengler, G. (1991). Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354, 3743.
Cockburn, J. J. B., Abrescia, N. G. A., Grimes, J. M., Sutton, G. C., Diprose, J. M., Benevides, J. M., Thomas, G. J. Jr, Bamford, J. K. H., Bamford, D. H. & Stuart, D. I. (2004). Membrane structure and interactions with protein and DNA in bacteriophage PRD1. Nature 432, 122125.
Cohen, D. N., Sham, Y. Y., Haugstad, G. D., Xiang, Y., Rossmann, M. G., Anderson, D. L. & Popham, D. L. (2009). Shared catalysis in virus entry and bacterial cell wall depolymerization. Journal of Molecular Biology 387, 607618.
Colman, P. M., Varghese, J. N. & Laver, W. G. (1983). Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303, 4144.
Coombs, D. H. & Arisaka, F. (1994). T4 tail structure and function. In Molecular Biology of Bacteriophage T4 (ed. Karam, J. D.), pp. 259281. Washington, DC: American Society for Microbiology.
Crick, F. H. C. & Watson, J. D. (1956). Structure of small viruses. Nature 177, 473475.
Crick, F. H. C. & Watson, J. D. (1957). Virus structure: general principles. In Ciba Foundation Symposium on the Nature of Viruses (eds. Wolstenholme, G. E. W., Millar, E. C. P. and Ciba Foundation), pp. 513. London: J. & A. Churchill.
Crowfoot, D. & Schmidt, G. M. J. (1945). X-ray crystallographic measurements on a single crystal of a tobacco necrosis virus derivative. Nature 155, 504505.
Crowther, R. A., Amos, L. A., Finch, J. T., DeRosier, D. J. & Klug, A. (1970). Three-dimensional reconstructions of spherical viruses by Fourier synthesis from electron micrographs. Nature 226, 421425.
Crowther, R. A., Lenk, E. V., Kikuchi, Y. & King, J. (1977). Molecular reorganization in the hexagon to star transition of the baseplate of bacteriophage T4. Journal of Molecular Biology 116, 489523.
Davis, C. W., Nguyen, H. Y., Hanna, S. L., Sánchez, M. D., Doms, R. W. & Pierson, T. C. (2006). West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. Journal of Virology 80, 12901301.
Dessen, A., Volchkov, V., Dolnik, O., Klenk, H.-D. & Weissenhorn, W. (2000). Crystal structure of the matrix protein VP40 from Ebola virus. EMBO Journal 19, 42284236.
DiMattia, M. A., Nam, H. J., Van Vliet, K., Mitchell, M., Bennett, A., Gurda, B. L., McKenna, R., Olson, N. H., Sinkovits, R. S., Potter, M., Byrne, B. J., Aslanidi, G., Zolotukhin, S., Muzyczka, N., Baker, T. S. & Agbandje-McKenna, M. (2012). Structural insight into the unique properties of adeno-associated virus serotype 9. Journal of Virology 86, 69476958.
Diprose, J. M., Grimes, J. M., Sutton, G. C., Burroughs, J. N., Meyer, A., Maan, S., Mertens, P. P. & Stuart, D. I. (2002). The core of bluetongue virus binds double-stranded RNA. Journal of Virology 76, 95339536.
Dokland, T., McKenna, R., Ilag, L. L., Bowman, B. R., Incardona, N. L., Fane, B. A. & Rossmann, M. G. (1997). Structure of a viral procapsid with molecular scaffolding. Nature 389, 308313.
Dokland, T., Walsh, M., Mackenzie, J. M., Khromykh, A. A., Ee, K.-H. & Wang, S. (2004). West Nile virus core protein: tetramer structure and ribbon formation. Structure 12, 11571163.
Dorsch, S., Liebisch, G., Kaufmann, B., von Landenberg, P., Hoffmann, J. H., Drobnik, W. & Modrow, S. (2002). The VP1 unique region of parvovirus B19 and its constituent phospholipase A2-like activity. Journal of Virology 76, 20142018.
Dubochet, J., Adrian, M., Chang, J. J., Homo, J. C., Lepault, J., McDowall, A. W. & Schultz, P. (1988). Cryo-electron microscopy of vitrified specimens. Quarterly Reviews of Biophysics 21, 129228.
Eiserling, F. A. & Black, L. W. (1994). Pathways in T4 morphogenesis. In Molecular Biology of Bacteriophage T4 (eds. Karam, J. D., Drake, J. W., Kreuzer, K. N., Mosig, G., Hall, D. H., Eiserling, F. A., Black, L. W., Spicer, E. K., Kutter, E., Carlson, C. & Miller, E. S.), pp. 209212. Washington, DC: American Society for Microbiology.
Elshuber, S., Allison, S. L., Heinz, F. X. & Mandl, C. W. (2003). Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. Journal of General Virology 84, 183191.
Ferlenghi, I., Clarke, M., Ruttan, T., Allison, S. L., Schalich, J., Heinz, F. X., Harrison, S. C., Rey, F. A. & Fuller, S. D. (2001). Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Molecular Cell 7, 593602.
Filman, D. J., Syed, R., Chow, M., Macadam, A. J., Minor, P. D. & Hogle, J. M. (1989). Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO Journal 18, 15671579.
Finch, J. T. & Klug, A. (1959). Structure of poliomyelitis virus. Nature 183, 17091714.
Fokine, A., Battisti, A. J., Kostyuchenko, V. A., Black, L. W. & Rossmann, M. G. (2006). Cryo-EM structure of a bacteriophage T4 gp24 bypass mutant: the evolution of pentameric vertex proteins in icosahedral viruses. Journal of Structural Biology 154, 255259.
Fokine, A., Chipman, P. R., Leiman, P. G., Mesyanzhinov, V. V., Rao, V. B. & Rossmann, M. G. (2004). Molecular architecture of the prolate head of bacteriophage T4. Proceedings of the National Academy of Sciences of the United States of America 101, 60036008.
Fokine, A., Miroshnikov, K. A., Shneider, M. M., Mesyanzhinov, V. V. & Rossmann, M. G. (2008). Structure of the bacteriophage phiKZ lytic transglycosylase, gp144. Journal of Biological Chemistry 283, 72427250.
Fokine, A., Zhang, Z., Kanamaru, S., Bowman, V. D., Aksyuk, A. A., Arisaka, F., Rao, V. B. & Rossmann, M. G. (2013). The molecular architecture of the bacteriophage T4 neck. Journal of Molecular Biology 425, 17311744.
Franklin, R. E. & Holmes, K. C. (1958). Tobacco mosaic virus: application of the method of isomorphous replacement to the determination of the helical parameters and radial density distribution. Acta Crystallographica 11, 213220.
Franklin, R. E., Klug, A. & Holmes, K. C. (1957). X-ray diffraction studies of the structure and morphology of tobacco mosaic virus. In Ciba Foundation Symposium on the Nature of Viruses (eds. Wolstenholme, G. E. W., Millar, E. C. P. and Ciba Foundation), pp. 3955. London: J. & A. Churchill.
Fu, C. Y. & Johnson, J. E. (2012). Structure and cell biology of archaeal virus STIV. Current Opinion in Virology 2, 122127.
Fuller, D. N., Raymer, D. M., Kottadiel, V. I., Rao, V. B. & Smith, D. E. (2007). Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proceedings of the National Academy of Sciences of the United States of America 104, 1686816873.
Fuller, S. D. (1987). The T=4 envelope of Sindbis virus is organized by interactions with a complementary T=3 capsid. Cell 48, 923934.
Gaykema, W. P., Volbeda, A. & Hol, W. G. (1986). Structure determination of Panulirus interruptus haemocyanin at 3·2 Å resolution. Successful phase extension by sixfold density averaging. Journal of Molecular Biology 187, 255275.
Gibbons, D. L. & Kielian, M. (2002). Molecular dissection of the Semliki Forest virus homotrimer reveals two functionally distinct regions of the fusion protein. Journal of Virology 76, 11941205.
Greve, J. M., Davis, G., Meyer, A. M., Forte, C. P., Yost, S. C., Marlor, C. W., Kamarck, M. E. & McClelland, A. (1989). The major human rhinovirus receptor is ICAM-1. Cell 56, 839847.
Grimes, J. M., Burroughs, J. N., Gouet, P., Diprose, J. M., Malby, R., Ziéntara, S., Mertens, P. P. C. & Stuart, D. I. (1998). The atomic structure of the bluetongue virus core. Nature 395, 470478.
Gubler, D. J. (1988). Dengue. In Epidemiology of Arthropod-Borne Viral Diseases (ed. Monath, T. P.), pp. 223260. Boca Raton, FL: CRC Press.
Guirakhoo, F., Bolin, R. A. & Roehrig, J. T. (1992). The Murray Valley encephalitis virus prM protein confers acid resistance to virus particles and alters the expression of epitopes within the R2 domain of E glycoprotein. Virology 191, 921931.
Guirakhoo, F., Heinz, F. X., Mandl, C. W., Holzmann, H. & Kunz, C. (1991). Fusion activity of flaviviruses: comparison of mature and immature (prM-containing) tick-borne encephalitis virions. Journal of General Virology 72, 13231329.
Hafenstein, S., Bowman, V. D., Sun, T., Nelson, C. D. S., Palermo, L., Chipman, P. R., Battisti, A. J., Parrish, C. R. & Rossmann, M. G. (2009). The structural analysis of eight different FAb interacting with parvovirus capsids reveals alternative mechanisms of neutralization and binding to host range variant capsids. Journal of Virology 83, 55565566.
Hafenstein, S., Palermo, L. M., Kostyuchenko, V. A., Xiao, C., Morais, M. C., Nelson, C. D. S., Bowman, V. D., Battisti, A. J., Chipman, P. R., Parrish, C. R. & Rossmann, M. G. (2007). Asymmetric binding of transferrin receptor to parvovirus capsids. Proceedings of the National Academy of Sciences of the United States of America 104, 65856589.
Harris, A., Forouhar, F., Qiu, S., Sha, B. & Luo, M. (2001). The crystal structure of the influenza matrix protein M1 at neutral pH: M1-M1 protein interfaces can rotate in the oligomeric structures of M1. Virology 289, 3444.
Harrison, S. C. (1968). A point-focusing camera for single-crystal diffraction. Journal of Applied Crystallography 1, 8490.
Harrison, S. C. (2008). Viral membrane fusion. Nature Structural and Molecular Biology 15, 690698.
Harrison, S. C. (2010). Virology. Looking inside adenovirus. Science 329, 10261027.
Harrison, S. C., Olson, A. J., Schutt, C. E., Winkler, F. K. & Bricogne, G. (1978). Tomato bushy stunt virus at 2·9 Å resolution. Nature 276, 368373.
Harrison, S. C., Strong, R. K., Schlesinger, S. & Schlesinger, M. J. (1992). Crystallization of Sindbis virus and its nucleocapsid. Journal of Molecular Biology 226, 277280.
Hatfull, G. F., Pedulla, M. L., Jacobs-Sera, D., Cichon, P. M., Foley, A., Ford, M. E., Gonda, R. M., Houtz, J. M., Hryckowian, A. J., Kelchner, V. A., Namburi, S., Pajcini, K. V., Popovich, M. G., Schleicher, D. T., Simanek, B. Z., Smith, A. L., Zdanowicz, G. M., Kumar, V., Peebles, C. L., Jacobs, W. R. Jr, Lawrence, J. G. & Hendrix, R. W. (2006). Exploring the mycobacteriophage metaproteome: phage genomics as an educational platform. PLoS Genetics 2, e92.
Hayashi, M. A. (1978). Morphogenesis of the isometric phages. In Cold Spring Harbor Monograph: The Single-Stranded DNA Phages, vol. 8 (eds. Denhardt, D. T., Dressler, D. & Ray, D. S.), pp. 531547. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Hayden, F. G., Herrington, D. T., Coats, T. L., Kim, K. H., Cooper, E. C., Villano, S. A., Liu, S., Hudson, S., Pevear, D. C., Collett, M. & McKinlay, M. A. (2003). Efficacy and safety of oral pleconaril for treatment of picornavirus colds in adults: results of two double-blind, randomized, placebo-controlled trials. Clinical Infectious Diseases 36, 15231532.
He, Y., Bowman, V. D., Mueller, S., Bator, C. M., Bella, J., Peng, X., Baker, T. S., Wimmer, E., Kuhn, R. J. & Rossmann, M. G. (2000). Interaction of the poliovirus receptor with poliovirus. Proceedings of the National Academy of Sciences of the United States of America 97, 7984.
He, Y., Chipman, P. R., Howitt, J., Bator, C. M., Whitt, M. A., Baker, T. S., Kuhn, R. J., Anderson, C. W., Freimuth, P. & Rossmann, M. G. (2001). Interaction of coxsackievirus B3 with the full-length coxsackievirus-adenovirus receptor. Nature Structural Biology 8, 874878.
Heinz, F. X., Stiasny, K., Püschner-Auer, G., Holzmann, H., Allison, S. L., Mandl, C. W. & Kunz, C. (1994). Structural changes and functional control of the tick-borne encephalitis virus glycoprotein E by the heterodimeric association with protein prM. Virology 198, 109117.
Hermodson, M. A., Abad-Zapatero, C., Abdel-Meguid, S. S., Pundak, S., Rossmann, M. G. & Tremaine, J. H. (1982). Amino acid sequence of southern bean mosaic virus coat protein and its relation to the three-dimensional structure of the virus. Virology 119, 133149.
Hogle, J. M. (2002). Poliovirus cell entry: common structural themes in viral cell entry pathways. Annual Review of Microbiology 56, 677702.
Hogle, J. M., Chow, M. & Filman, D. J. (1985). Three-dimensional structure of poliovirus at 2·9 Å resolution. Science 229, 13581365.
Holmes, K. C., Stubbs, G. J., Mandelkow, E. & Gallwitz, U. (1975). Structure of tobacco mosaic virus at 6·7 Å resolution. Nature 254, 192196.
Horne, R. W., Brenner, S., Waterson, A. P. & Wildy, P. (1959). The icosahedral form of an adenovirus. Journal of Molecular Biology 1, 8486.
Hueffer, K., Govindasamy, L., Agbandje-McKenna, M. & Parrish, C. R. (2003). Combinations of two capsid regions controlling canine host range determine canine transferrin receptor binding by canine and feline parvoviruses. Journal of Virology 77, 1009910105.
Huxley, H. E. & Zubay, G. (1960). The structure of the protein shell of turnip yellow mosaic virus. Journal of Molecular Biology 2, 189196.
Jiang, W., Chang, J., Jakana, J., Weigele, P., King, J. & Chiu, W. (2006). Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439, 612616.
Jiang, W., Li, Z., Zhang, Z., Baker, M. L., Prevelige, P. E. Jr & Chiu, W. (2003). Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nature Structural Biology 10, 131135.
Kanamaru, S., Kondabagil, K., Rossmann, M. G. & Rao, V. B. (2004). The functional domains of bacteriophage T4 terminase. Journal of Biological Chemistry 279, 4079540801.
Kanamaru, S., Leiman, P. G., Kostyuchenko, V. A., Chipman, P. R., Mesyanzhinov, V. V., Arisaka, F. & Rossmann, M. G. (2002). Structure of the cell-puncturing device of bacteriophage T4. Nature 415, 553557.
Kaufmann, B., Baxa, U., Chipman, P. R., Rossmann, M. G., Modrow, S. & Seckler, R. (2005). Parvovirus B19 does not bind to membrane-associated globoside in vitro. Virology 332, 189198.
Kaufmann, B., Bowman, V. D., Li, Y., Szelei, J., Waddell, P. J., Tijssen, P. & Rossmann, M. G. (2010a). Structure of Penaeus stylirostris densovirus, a shrimp pathogen. Journal of Virology 84, 1128911296.
Kaufmann, B., Chipman, P. R., Holdaway, H. A., Johnson, S., Fremont, D. H., Kuhn, R. J., Diamond, M. S. & Rossmann, M. G. (2009). Capturing a flavivirus pre-fusion intermediate. PLoS Pathogens 5, e1000672.
Kaufmann, B., Chipman, P. R., Kostyuchenko, V. A., Modrow, S. & Rossmann, M. G. (2008). Visualization of the externalized VP2 N-termini of infectious human parvovirus B19. Journal of Virology 82, 73067312.
Kaufmann, B., El-Far, M., Plevka, P., Bowman, V. D., Li, Y., Tijssen, P. & Rossmann, M. G. (2011). Structure of Bombyx mori densovirus 1, a silkworm pathogen. Journal of Virology 85, 46914697.
Kaufmann, B., Nybakken, G. E., Chipman, P. R., Zhang, W., Diamond, M. S., Fremont, D. H., Kuhn, R. J. & Rossmann, M. G. (2006). West Nile virus in complex with the Fab fragment of a neutralizing monoclonal antibody. Proceedings of the National Academy of Sciences of the United States of America 103, 1240012404.
Kaufmann, B., Plevka, P., Kuhn, R. J. & Rossmann, M. G. (2010b). Crystallization and preliminary X-ray diffraction analysis of West Nile virus. Acta Crystallographica Section F 66, 558562.
Kaufmann, B. & Rossmann, M. G. (2011). Molecular mechanisms involved in the early steps of flavivirus cell entry. Microbes and Infection 13, 19.
Kaufmann, B., Simpson, A. A. & Rossmann, M. G. (2004). The structure of human parvovirus B19. Proceedings of the National Academy of Sciences of the United States of America 101, 1162811633.
Kay, L. E. (1986). W. M. Stanley's crystallization of the tobacco mosaic virus, 1930–1940. Isis 77, 450472.
Kellenberger, E. (1976). DNA viruses: cooperativity and regulation through conformational changes as features of phage assembly. Philosophical Transactions of the Royal Society of London B: Biological Sciences 276, 313.
Kendrew, J. C., Bodo, G., Dintzis, H. M., Parrish, R. G., Wyckoff, H. & Phillips, D. C. (1958). A three-dimensional model of the myoglobin molecule obtained by X-ray analysis. Nature 181, 662666.
Kendrew, J. C., Dickerson, R. E., Strandberg, B. E., Hart, R. G., Davies, D. R., Phillips, D. C. & Shore, V. C. (1960). Structure of myoglobin. A three-dimensional Fourier synthesis at 2 Å resolution. Nature 185, 422427.
Khayat, R., Tang, L., Larson, E. T., Lawrence, C. M., Young, M. & Johnson, J. E. (2005). Structure of an archaeal virus capsid protein reveals a common ancestry to eukaryotic and bacterial viruses. Proceedings of the National Academy of Sciences of the United States of America 102, 1894418949.
Kielian, M. (1995). Membrane fusion and the alphavirus life cycle. Advances in Virus Research 45, 113151.
Kielian, M. & Rey, F. A. (2006). Virus membrane-fusion proteins: more than one way to make a hairpin. Nature Reviews Microbiology 4, 6776.
Kikuchi, Y. & King, J. (1975). Assembly of the tail of bacteriophage T4. Journal of Supramolecular Structure 3, 2438.
Klose, T., Kuznetsov, Y. G., Xiao, C., Sun, S., McPherson, A. & Rossmann, M. G. (2010). The three-dimensional structure of Mimivirus. Intervirology 53, 268273.
Klug, A. (1972). Interpretation of the rotation function map of satellite tobacco necrosis virus: octahedral packing of icosahedral particles. Cold Spring Harbor Symposia on Quantitative Biology 36, 483487.
Klug, A., Finch, J. T. & Franklin, R. E. (1957). The structure of turnip yellow mosaic virus: X-ray diffraction studies. Biochimica et Biophysica Acta 25, 242252.
Kolatkar, P. R., Bella, J., Olson, N. H., Bator, C. M., Baker, T. S. & Rossmann, M. G. (1999). Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO Journal 18, 62496259.
Kostyuchenko, V. A., Chipman, P. R., Leiman, P. G., Arisaka, F., Mesyanzhinov, V. V. & Rossmann, M. G. (2005). The tail structure of bacteriophage T4 and its mechanism of contraction. Nature Structural and Molecular Biology 12, 810813.
Kostyuchenko, V. A., Leiman, P. G., Chipman, P. R., Kanamaru, S., van Raaij, M. J., Arisaka, F., Mesyanzhinov, V. V. & Rossmann, M. G. (2003). Three-dimensional structure of bacteriophage T4 baseplate. Nature Structural Biology 10, 688693.
Kuhn, R. J. (2007). Chapter 30: Togaviridae: the viruses and their replication. In Fields Virology (eds. Knipe, D. M. & Howley, P. M.), pp. 10011021. Philadelphia, PA: Lippincott Williams & Wilkins.
Kuhn, R. J., Zhang, W., Rossmann, M. G., Pletnev, S. V., Corver, J., Lenches, E., Jones, C. T., Mukhopadhyay, S., Chipman, P. R., Strauss, E. G., Baker, T. S. & Strauss, J. H. (2002). Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108, 717725.
Kuznetsov, Y. G., Xiao, C., Sun, S., Raoult, D., Rossmann, M. G. & McPherson, A. (2010). Atomic force microscopy investigation of the giant mimivirus. Virology 404, 127137.
La Scola, B., Audic, S., Robert, C., Jungang, L., de Lamballerie, X., Drancourt, M., Birtles, R., Claverie, J. M. & Raoult, D. (2003). A giant virus in amoebae. Science 299, 2033.
Lamb, R. A. & Jardetzky, T. S. (2007). Structural basis of viral invasion: lessons from paramyxovirus F. Current Opinion in Structural Biology 17, 427436.
Larson, S. B., Koszelak, S., Day, J., Greenwood, A., Dodds, J. A. & McPherson, A. (1993). Double-helical RNA in satellite tobacco mosaic virus. Nature 361, 179182.
Lebedev, A. A., Krause, M. H., Isidro, A. L., Vagin, A. A., Orlova, E. V., Turner, J., Dodson, E. J., Tavares, P. & Antson, A. A. (2007). Structural framework for DNA translocation via the viral portal protein. EMBO Journal 26, 19841994.
Lee, K. K. & Johnson, J. E. (2003). Complementary approaches to structure determination of icosahedral viruses. Current Opinion in Structural Biology 13, 558569.
Leiman, P. G., Arisaka, F., van Raaij, M. J., Kostyuchenko, V. A., Aksyuk, A. A., Kanamaru, S. & Rossmann, M. G. (2010). Morphogenesis of the T4 tail and tail fibers. Virology Journal 7, 355.
Leiman, P. G., Chipman, P. R., Kostyuchenko, V. A., Mesyanzhinov, V. V. & Rossmann, M. G. (2004). Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118, 419429.
Leiman, P. G., Kanamaru, S., Mesyanzhinov, V. V., Arisaka, F. & Rossmann, M. G. (2003). Structure and morphogenesis of bacteriophage T4. Cellular and Molecular Life Sciences 60, 23562370.
Lerch, T. F., O'Donnell, J. K., Meyer, N. L., Xie, Q., Taylor, K. A., Stagg, S. M. & Chapman, M. S. (2012). Structure of AAV-DJ, a retargeted gene therapy vector: cryo-electron microscopy at 4·5 Å resolution. Structure 20, 13101320.
Lescar, J., Roussel, A., Wein, M. W., Navaza, J., Fuller, S. D., Wengler, G., Wengler, G. & Rey, F. A. (2001). The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105, 137148.
Li, L., Jose, J., Xiang, Y., Kuhn, R. J. & Rossmann, M. G. (2010). Structural changes of envelope proteins during alphavirus fusion. Nature 468, 705708.
Li, L., Lok, S.-M., Yu, I.-M., Zhang, Y., Kuhn, R. J., Chen, J. & Rossmann, M. G. (2008). The flavivirus precursor membrane-envelope protein complex: structure and maturation. Science 319, 18301834.
Liljas, L., Unge, T., Jones, T. A., Fridborg, K., Lövgren, S., Skoglund, U. & Strandberg, B. (1982). Structure of satellite tobacco necrosis virus at 3·0 Å resolution. Journal of Molecular Biology 159, 93108.
Lindenbach, B. D. & Rice, C. M. (2001). Flaviviridae: the viruses and their replication. In Fields Virology (eds. Knipe, D. M. & Howley, P. M.), pp. 9911041. Philadelphia: Lippincott Williams & Wilkins.
Lindenbach, B. D. & Rice, C. M. (2003). Molecular biology of flaviviruses. Advances in Virus Research 59, 2361.
Liu, H., Jin, L., Koh, S. B., Atanasov, I., Schein, S., Wu, L. & Zhou, Z. H. (2010). Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 329, 10381043.
Llamas-Saiz, A. L., Agbandje-McKenna, M., Wikoff, W. R., Bratton, J., Tattersall, P. & Rossmann, M. G. (1997). Structure determination of minute virus of mice. Acta Crystallographica Section D: Biological Crystallography 53, 93102.
Lorenz, I. C., Allison, S. L., Heinz, F. X. & Helenius, A. (2002). Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. Journal of Virology 76, 54805491.
Lozach, P. Y., Burleigh, L., Staropoli, I., Navarro-Sanchez, E., Harriague, J., Virelizier, J. L., Rey, F. A., Despres, P., Arenzana-Seisdedos, F. & Amara, A. (2005). Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. Journal of Biological Chemistry 280, 2369823708.
Lu, Y. E., Cassese, T. & Kielian, M. (1999). The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. Journal of Virology 73, 42724278.
Luo, M., Vriend, G., Kamer, G., Minor, I., Arnold, E., Rossmann, M. G., Boege, U., Scraba, D. G., Duke, G. M. & Palmenberg, A. C. (1987). The atomic structure of Mengo virus at 3·0 Å resolution. Science 235, 182191.
Ma, L., Jones, C. T., Groesch, T. D., Kuhn, R. J. & Post, C. B. (2004). Solution structure of dengue virus capsid protein reveals another fold. Proceedings of the National Academy of Sciences of the United States of America 101, 34143419.
Magdoff, B. S. (1960). Sub-units in southern bean mosaic virus. Nature 185, 673674.
Main, P. & Rossmann, M. G. (1966). Relationships among structure factors due to identical molecules in different crystallographic environments. Acta Crystallographica 21, 6772.
Mancini, E. J., Kainov, D. E., Grimes, J. M., Tuma, R., Bamford, D. H. & Stuart, D. I. (2004). Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 118, 743755.
Marsh, M. & Helenius, A. (1989). Virus entry into animal cells. Advances in Virus Research 36, 107151.
McKenna, R., Xia, D., Willingmann, P., Ilag, L. L., Krishnaswamy, S., Rossmann, M. G., Olson, N. H., Baker, T. S. & Incardona, N. L. (1992a). Atomic structure of single-stranded DNA bacteriophage ϕX174 and its functional implications. Nature 355, 137143.
McKenna, R., Xia, D., Willingmann, P., Ilag, L. L. & Rossmann, M. G. (1992b). Structure determination of the bacteriophage ϕX174. Acta Crystallographica Section B 48, 499511.
Modis, Y., Ogata, S., Clements, D. & Harrison, S. C. (2003). A ligand-binding pocket in the dengue virus envelope glycoprotein. Proceedings of the National Academy of Sciences of the United States of America 100, 69866991.
Modis, Y., Ogata, S., Clements, D. & Harrison, S. C. (2004). Structure of the dengue virus envelope protein after membrane fusion. Nature 427, 313319.
Modis, Y., Trus, B. L. & Harrison, S. C. (2002). Atomic model of the papillomavirus capsid. EMBO Journal 21, 47544762.
Moffitt, J. R., Chemla, Y. R., Aathavan, K., Grimes, S., Jardine, P. J., Anderson, D. L. & Bustamante, C. (2009). Intersubunit coordination in a homomeric ring ATPase. Nature 457, 446450.
Money, V. A., McPhee, H. K., Mosely, J. A., Sanderson, J. M. & Yeo, R. P. (2009). Surface features of a Mononegavirales matrix protein indicate sites of membrane interaction. Proceedings of the National Academy of Sciences of the United States of America 106, 44414446.
Morais, M. C., Choi, K. H., Koti, J. S., Chipman, P. R., Anderson, D. L. & Rossmann, M. G. (2005). Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudo-atomic structure of ϕ29. Molecular Cell 18, 149159.
Morais, M. C., Koti, J. S., Bowman, V. D., Reyes-Aldrete, E., Anderson, D. L. & Rossmann, M. G. (2008). Defining molecular and domain boundaries in the bacteriophage ϕ29 DNA packaging motor. Structure 16, 12671274.
Mosig, G. & Eiserling, F. (2006). T4 and related phages: structure and development. In The Bacteriophages (ed. Calendar, R.), pp. 225267. New York: Oxford University Press.
Muckelbauer, J. K., Kremer, M., Minor, I., Tong, L., Zlotnick, A., Johnson, J. E. & Rossmann, M. G. (1995). Structure determination of coxsackievirus B3 to 3·5 Å resolution. Acta Crystallographica Section D: Biological Crystallography 51, 871887.
Mukhopadhyay, S., Kim, B.-S., Chipman, P. R., Rossmann, M. G. & Kuhn, R. J. (2003). Structure of West Nile virus. Science 302, 248.
Mukhopadhyay, S., Zhang, W., Gabler, S., Chipman, P. R., Strauss, E. G., Strauss, J. H., Baker, T. S., Kuhn, R. J. & Rossmann, M. G. (2006). Mapping the structure and function of the E1 and E2 glycoproteins in alphaviruses. Structure 14, 6373.
Nagai, Y., Klenk, H.-D. & Rott, R. (1976). Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology 72, 494508.
Nandhagopal, N., Simpson, A. A., Gurnon, J. R., Yan, X., Baker, T. S., Graves, M. V., Van Etten, J. L. & Rossmann, M. G. (2002). The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proceedings of the National Academy of Sciences of the United States of America 99, 1475814763.
Neumann, P., Lieber, D., Meyer, S., Dautel, P., Kerth, A., Kraus, I., Garten, W. & Stubbs, M. T. (2009). Crystal structure of the Borna disease virus matrix protein (BDV-M) reveals ssRNA binding properties. Proceedings of the National Academy of Sciences of the United States of America 106, 37103715.
Nixon, H. L. & Gibbs, A. J. (1960). Electron microscope observations on the structure of turnip yellow mosaic virus. Journal of Molecular Biology 2, 197200.
Olia, A. S., Prevelige, P. E. Jr, Johnson, J. E. & Cingolani, G. (2011). Three-dimensional structure of a viral genome-delivery portal vertex. Nature Structural and Molecular Biology 18, 597603.
Oliveira, M. A., Zhao, R., Lee, W., Kremer, M. J., Minor, I., Rueckert, R. R., Diana, G. D., Pevear, D. C., Dutko, F. J., McKinlay, M. A. & Rossmann, M. G. (1993). The structure of human rhinovirus 16. Structure 1, 5168.
Olson, N. H., Kolatkar, P. R., Oliveira, M. A., Cheng, R. H., Greve, J. M., McClelland, A., Baker, T. S. & Rossmann, M. G. (1993). Structure of a human rhinovirus complexed with its receptor molecule. Proceedings of the National Academy of Sciences of the United States of America 90, 507511.
Padron, E., Bowman, V., Kaludov, N., Govindasamy, L., Levy, H., Nick, P., McKenna, R., Muzyczka, N., Chiorini, J. A., Baker, T. S. & Agbandje-McKenna, M. (2005). Structure of adeno-associated virus type 4. Journal of Virology 79, 50475058.
Perutz, M. F., Rossmann, M. G., Cullis, A. F., Muirhead, H., Will, G. & North, A. C. T. (1960). Structure of haemoglobin. A three-dimensional Fourier synthesis at 5·5-Å resolution, obtained by X-ray analysis. Nature 185, 416422.
Pletnev, S. V., Zhang, W., Mukhopadhyay, S., Fisher, B. R., Hernandez, R., Brown, D. T., Baker, T. S., Rossmann, M. G. & Kuhn, R. J. (2001). Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold. Cell 105, 127136.
Plevka, P., Battisti, A. J., Winkler, D. C., Tars, K., Holdaway, H. A., Bator, C. M. & Rossmann, M. G. (2012a). Sample preparation induced artifacts in cryo-electron tomographs. Microscopy and Microanalysis 18, 10431048.
Plevka, P., Hafenstein, S., Li, L., D'Abrgamo, A. Jr, Cotmore, S. F., Rossmann, M. G. & Tattersall, P. (2011a). Structure of a packaging-defective mutant of minute virus of mice indicates that the genome is packaged via a pore at a 5-fold axis. Journal of Virology 85, 48224827.
Plevka, P., Kaufmann, B. & Rossmann, M. G. (2011b). Analysis of phases in the structure determination of an icosahedral virus. Acta Crystallographica Section D: Biological Crystallography 67, 568577.
Plevka, P., Perera, R., Cardosa, J., Kuhn, R. J. & Rossmann, M. G. (2012b). Crystal structure of human enterovirus 71. Science 336, 1274.
Plevka, P., Perera, R., Cardosa, J., Kuhn, R. J. & Rossmann, M. G. (2012c). Structure determination of enterovirus 71. Acta Crystallographica Section D: Biological Crystallography 68, 12171222.
Plevka, P., Tars, K. & Liljas, L. (2009). Structure and stability of icosahedral particles of a covalent coat protein dimer of bacteriophage MS2. Protein Science 18, 1653–61.
Pokidysheva, E., Zhang, Y., Battisti, A. J., Bator-Kelly, C. M., Chipman, P. R., Xiao, C., Gregorio, G. G., Hendrickson, W. A., Kuhn, R. J. & Rossmann, M. G. (2006). Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124, 485493.
Rao, V. B. & Feiss, M. (2008). The bacteriophage DNA packaging motor. Annual Review of Genetics 42, 647681.
Rao, Z., Belyaev, A. S., Fry, E., Roy, P., Jones, I. M. & Stuart, D. I. (1995). Crystal structure of SIV matrix antigen and implications for virus assembly. Nature 378, 743747.
Rayment, I., Baker, T. S., Caspar, D. L. & Murakami, W. T. (1982). Polyoma virus capsid structure at 22·5 Å resolution. Nature 295, 110115 (issue cover).
Reddy, V. S., Natchiar, S. K., Stewart, P. L. & Nemerow, G. R. (2010). Crystal structure of human adenovirus at 3·5 Å resolution. Science 329, 10711075.
Rey, F. A., Heinz, F. X., Mandl, C., Kunz, C. & Harrison, S. C. (1995). The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375, 291298.
Roberts, M. M., White, J. L., Grütter, M. G. & Burnett, R. M. (1986). Three-dimensional structure of the adenovirus major coat protein hexon. Science 232, 11481151.
Rossmann, M. G. (1972). The Molecular Replacement Method: A Collection of Papers on the Use of Non-crystallographic Symmetry. New York: Gordon & Breach.
Rossmann, M. G. (1979). Processing oscillation diffraction data for very large unit cells with an automatic convolution technique and profile fitting. Journal of Applied Crystallography 12, 225238.
Rossmann, M. G. (1984). Synchrotron radiation studies of large proteins and supramolecular structures. In Biological Systems: Structure and Analysis (ed. Diakun, G. P. G., C. D., ), pp. 2840. Daresbury: Science and Engineering Research Council.
Rossmann, M. G. (1989a). The canyon hypothesis. Hiding the host cell receptor attachment site on a viral surface from immune surveillance. Journal of Biological Chemistry 264, 1458714590.
Rossmann, M. G. (1989b). Determination of virus structures by the use of molecular replacement density averaging. In Improving Protein Phases. Proceedings of the Study Weekend held at Daresbury, 1988 (eds. Bailey, S., Dodson, E. & Phillips, S.), pp. 4956. Daresbury: Science and Engineering Research Council.
Rossmann, M. G. (1994). Viral cell recognition and entry. Protein Science 3, 17121725.
Rossmann, M. G. (1999). Synchrotron radiation as a tool for investigating virus structures. Journal of Synchrotron Radiation 6, 816821.
Rossmann, M. G. (2001). Molecular replacement – historical background. Acta Crystallographica Section D: Biological Crystallography 57, 13601366.
Rossmann, M. G., Arnold, E., Erickson, J. W., Frankenberger, E. A., Griffith, J. P., Hecht, H. J., Johnson, J. E., Kamer, G., Luo, M., Mosser, A. G., Rueckert, R. R., Sherry, B. & Vriend, G. (1985). Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317, 145153.
Rossmann, M. G., Battisti, A. J. & Plevka, P. (2011). Future prospects. In Advances in Protein Chemistry and Structural Biology, Volume 82: Recent Advances in Electron Cryomicroscopy, Part B (eds. Ludtke, S. J. & Prasad, B. V. V.), pp. 101121. San Diego, CA: Academic Press.
Rossmann, M. G., Bella, J., Kolatkar, P. R., He, Y., Wimmer, E., Kuhn, R. J. & Baker, T. S. (2000). Minireview: cell recognition and entry by rhino- and enteroviruses. Virology 269, 239247.
Rossmann, M. G. & Blow, D. M. (1962). The detection of sub-units within the crystallographic asymmetric unit. Acta Crystallographica 15, 2431.
Rossmann, M. G. & Erickson, J. W. (1983). Oscillation photography of radiation-sensitive crystals using a synchrotron source. Journal of Applied Crystallography 16, 629636.
Rossmann, M. G., Ford, G. C., Watson, H. C. & Banaszak, L. J. (1972). Molecular symmetry of glyceraldehyde-3-phosphate dehydrogenase. Journal of Molecular Biology 64, 237249.
Rossmann, M. G., He, Y. & Kuhn, R. J. (2002). Picornavirus-receptor interactions. Trends in Microbiology 10, 324331.
Rossmann, M. G. & Johnson, J. E. (1989). Icosahedral RNA virus structure. Annual Review of Biochemistry 58, 533573.
Rossmann, M. G., Leslie, A. G. W., Abdel-Meguid, S. S. & Tsukihara, T. (1979). Processing and post-refinement of oscillation camera data. Journal of Applied Crystallography 12, 570581.
Rossmann, M. G., McKenna, R., Tong, L., Xia, D., Dai, J., Wu, H., Choi, H. K., Marinescu, D. & Lynch, R. E. (1992). Molecular replacement real space averaging. In Molecular Replacement. Proceedings of the CCP4 Study Weekend, 31 January – 1 February 1992 (eds. Dodson, E., Gover, S. & Wolf, W.), pp. 3348. Daresbury: Science and Engineering Research Council.
Rossmann, M. G., Moras, D. & Olsen, K. W. (1974). Chemical and biological evolution of a nucleotide-binding protein. Nature 250, 194199.
Rossmann, M. G. & Palmenberg, A. C. (1988). Conservation of the putative receptor attachment site in picornaviruses. Virology 164, 373382.
Roussel, A., Lescar, J., Vaney, M. C., Wengler, G. & Rey, F. A. (2006). Structure and interactions at the viral surface of the envelope protein E1 of Semliki Forest virus. Structure 14, 7586.
Roy, A., Bhardwaj, A., Datta, P., Lander, G. C. & Cingolani, G. (2012). Small terminase couples viral DNA binding to genome-packaging ATPase activity. Structure 20, 14031413.
Scheid, A., Caliguiri, L. A., Compans, R. W. & Choppin, P. W. (1972). Isolation of paramyxovirus glycoproteins. Association of both hemagglutinating and neuraminidase activities with the larger SV5 glycoprotein. Virology 50, 640652.
Sherry, B., Mosser, A. G., Colonno, R. J. & Rueckert, R. R. (1986). Use of monoclonal antibodies to identify four neutralization immunogens on a common cold picornavirus, human rhinovirus 14. Journal of Virology 57, 246257.
Sherry, B. & Rueckert, R. (1985). Evidence for at least two dominant neutralization antigens on human rhinovirus 14. Journal of Virology 53, 137143.
Shnyrova, A. V., Ayllon, J., Mikhalyov, I. I., Villar, E., Zimmerberg, J. & Frolov, V. A. (2007). Vesicle formation by self-assembly of membrane-bound matrix proteins into a fluidlike budding domain. Journal of Cell Biology 179, 627633.
Simpson, A. A., Chandrasekar, V., Hébert, B., Sullivan, G. M., Rossmann, M. G. & Parrish, C. R. (2000a). Host range and variability of calcium binding by surface loops in the capsids of canine and feline parvoviruses. Journal of Molecular Biology 300, 597610.
Simpson, A. A., Chipman, P. R., Baker, T. S., Tijssen, P. & Rossmann, M. G. (1998). The structure of an insect parvovirus (Galleria mellonella densovirus) at 3·7 Å resolution. Structure 6, 13551367.
Simpson, A. A., Hebert, B., Sullivan, G. M., Parrish, C. R., Zadori, Z., Tijssen, P. & Rossmann, M. G. (2002). The structure of porcine parvovirus: comparison with related viruses. Journal of Molecular Biology 315, 11891198.
Simpson, A. A., Nandhagopal, N., Van Etten, J. L. & Rossmann, M. G. (2003). Structural analyses of Phycodnaviridae and Iridoviridae. Acta Crystallographica Section D: Biological Crystallography 59, 20532059.
Simpson, A. A., Tao, Y., Leiman, P. G., Badasso, M. O., He, Y., Jardine, P. J., Olson, N. H., Morais, M. C., Grimes, S., Anderson, D. L., Baker, T. S. & Rossmann, M. G. (2000b). Structure of the bacteriophage ϕ29 DNA packaging motor. Nature 408, 745750.
Smith, D. E., Tans, S. J., Smith, S. B., Grimes, S., Anderson, D. L. & Bustamante, C. (2001). The bacteriophage ϕ29 portal motor can package DNA against a large internal force. Nature 413, 748752.
Smith, T. J., Chase, E. S., Schmidt, T. J., Olson, N. H. & Baker, T. S. (1996). Neutralizing antibody to human rhinovirus 14 penetrates the receptor-binding canyon. Nature 383, 350354.
Smith, T. J., Kremer, M. J., Luo, M., Vriend, G., Arnold, E., Kamer, G., Rossmann, M. G., McKinlay, M. A., Diana, G. D. & Otto, M. J. (1986). The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science 233, 12861293.
Smyth, M., Tate, J., Hoey, E., Lyons, C., Martin, S. & Stuart, D. (1995). Implications for viral uncoating from the structure of bovine enterovirus. Nature Structural Biology 2, 224231.
Stadler, K., Allison, S. L., Schalich, J. & Heinz, F. X. (1997). Proteolytic activation of tick-borne encephalitis virus by furin. Journal of Virology 71, 84758481.
Staunton, D. E., Merluzzi, V. J., Rothlein, R., Barton, R., Marlin, S. D. & Springer, T. A. (1989). A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56, 849853.
Stehle, T., Gamblin, S. J., Yan, Y. & Harrison, S. C. (1996). The structure of simian virus 40 refined at 3·1 Å resolution. Structure 4, 165182.
Stiasny, K., Allison, S. L., Marchler-Bauer, A., Kunz, C. & Heinz, F. X. (1996). Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tick-borne encephalitis virus. Journal of Virology 70, 81428147.
Stiasny, K. & Heinz, F. X. (2006). Flavivirus membrane fusion. Journal of General Virology 87, 27552766.
Stockley, P. G., Stonehouse, N. J., Murray, J. B., Goodman, S. T., Talbot, S. J., Adams, C. J., Liljas, L. & Valegard, K. (1995). Probing sequence-specific RNA recognition by the bacteriophage MS2 coat protein. Nucleic Acids Research 23, 25122518.
Strauss, J. H. & Strauss, E. G. (2002). Viruses and Human Disease. San Diego: Academic Press.
Stubbs, G., Warren, S. & Holmes, K. (1977). Structure of RNA and RNA binding site in tobacco mosaic virus from 4 Å map calculated from X-ray fibre diagrams. Nature 267, 216221.
Sun, S., Gao, S., Kondabagil, K., Xiang, Y., Rossmann, M. G. & Rao, V. B. (2012). Structure and function of the small terminase component of the DNA packaging machine in T4-like bacteriophages. Proceedings of the National Academy of Sciences of the United States of America 109, 817822.
Sun, S., Kondabagil, K., Draper, B., Alam, T. I., Bowman, V. D., Zhang, Z., Hegde, S., Fokine, A., Rossmann, M. G. & Rao, V. B. (2008). The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 135, 12511262.
Sun, S., Kondabagil, K., Gentz, P. M., Rossmann, M. G. & Rao, V. B. (2007). The structure of the ATPase that powers DNA packaging into bacteriophage T4 procapsids. Molecular Cell 25, 943949.
Sun, S., Rao, V. B. & Rossmann, M. G. (2010). Genome packaging in viruses. Current Opinion in Structural Biology 20, 114120.
Sun, S., Xiang, Y., Wataru, A., Holdaway, H., Pal, P., Zhang, X., Diamond, M. S., Nabel, G. J. & Rossmann, M. G. (2013). Structural analyses at pseudo atomic resolution of Chikungunya virus and antibodies show mechanisms of neutralization. eLIFE, in press. doi: 10.7554/eLife.00435.
Tang, J., Jose, J., Chipman, P., Zhang, W., Kuhn, R. J. & Baker, T. S. (2011). Molecular links between the E2 envelope glycoprotein and nucleocapsid core in Sindbis virus. Journal of Molecular Biology 414, 442459.
Tao, Y., Olson, N. H., Xu, W., Anderson, D. L., Rossmann, M. G. & Baker, T. S. (1998). Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95, 431437.
Thomassen, E., Gielen, G., Schutz, M., Schoehn, G., Abrahams, J. P., Miller, S. & van Raaij, M. J. (2003). The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold. Journal of Molecular Biology 331, 361373.
Tong, L. & Rossmann, M. G. (1990). The locked rotation function. Acta Crystallographica Section A 46, 783792.
Tsao, J., Chapman, M. S., Agbandje, M., Keller, W., Smith, K., Wu, H., Luo, M., Smith, T. J., Rossmann, M. G., Compans, R. W. & Parrish, C. R. (1991). The three-dimensional structure of canine parvovirus and its functional implications. Science 251, 14561464.
Tsao, J., Chapman, M. S., Wu, H., Agbandje, M., Keller, W. & Rossmann, M. G. (1992). Structure determination of monoclinic canine parvovirus. Acta Crystallographica Section B 48, 7588.
Tuthill, T. J., Groppelli, E., Hogle, J. M. & Rowlands, D. J. (2010). Picornaviruses. Current Topical Microbiology Immunology 343, 4389.
Valegård, K., Liljas, L., Fridborg, K. & Unge, T. (1990). The three-dimensional structure of the bacterial virus MS2. Nature 345, 3641.
Valegård, K., Murray, J. B., Stockley, P. G., Stonehouse, N. J. & Liljas, L. (1994). Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature 371, 623626.
van Raaij, M. J., Schoehn, G., Burda, M. R. & Miller, S. (2001). Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre. Journal of Molecular Biology 314, 11371146.
von Bonsdorff, C. H. & Harrison, S. C. (1975). Sindbis virus glycoproteins form a regular icosahedral surface lattice. Journal of Virology 16, 141145.
von Bonsdorff, C. H. & Harrison, S. C. (1978). Hexagonal glycoprotein arrays from Sindbis virus membranes. Journal of Virology 28, 578583.
Voss, J. E., Vaney, M.-C., Duquerroy, S., Vonrhein, C., Girard-Blanc, C., Crublet, E., Thompson, A., Bricogne, G. & Rey, F. A. (2010). Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468, 709712.
Walters, R. W., Agbandje-McKenna, M., Bowman, V. D., Moninger, T. O., Olson, N. H., Seiler, M., Chiorini, J. A., Baker, T. S. & Zabner, J. (2004). Structure of adeno-associated virus serotype 5. Journal of Virology 78, 33613371.
Wang, X., Peng, W., Ren, J., Hu, Z., Xu, J., Lou, Z., Li, X., Yin, W., Shen, X., Porta, C., Walter, T. S., Evans, G., Axford, D., Owen, R., Rowlands, D. J., Wang, J., Stuart, D. I., Fry, E. E. & Rao, Z. (2012). A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nature Structural and Molecular Biology 19, 424429.
Watson, J. D. & Crick, F. H. C. (1953a). Genetical implications of the structure of deoxyribonucleic acid. Nature 171, 964967.
Watson, J. D. & Crick, F. H. C. (1953b). Molecular structure of nucleic acids: a structure for deoxyribose nucleic acid. Nature 171, 737738.
Wikoff, W. R., Liljas, L., Duda, R. L., Tsuruta, H., Hendrix, R. W. & Johnson, J. E. (2000). Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289, 21292133.
Wiley, D. C., Wilson, I. A. & Skehel, J. J. (1981). Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289, 373378.
Williams, R. C. & Smith, K. M. (1958). The polyhedral form of the Tipula iridescent virus. Biochimica et Biophysica Acta 28, 464469.
Wilson, H. R. (1966). Diffraction of X-rays by Proteins, Nucleic Acids and Viruses. London: Edward Arnold Publishers Ltd.
Wrigley, N. G. (1969). An electron microscope study of the structure of Sericesthis iridescent virus. Journal of General Virology 5, 123134.
Wu, H. & Rossmann, M. G. (1993). The canine parvovirus empty capsid structure. Journal of Molecular Biology 233, 231244.
Wu, S. J. L., Grouard-Vogel, G., Sun, W., Mascola, J. R., Brachtel, E., Putvatana, R., Louder, M. K., Filgueira, L., Marovich, M. A., Wong, H. K., Blauvelt, A., Murphy, G. S., Robb, M. L., Innes, B. L., Birx, D. L., Hayes, C. G. & Frankel, S. S. (2000). Human skin Langerhans cells are targets of dengue virus infection. Nature Medicine 6, 816820.
Xiang, Y., Morais, M. C., Cohen, D. N., Bowman, V. D., Anderson, D. L. & Rossmann, M. G. (2008). Crystal and cryoEM structural studies of a cell wall degrading enzyme in the bacteriophage ϕ29 tail. Proceedings of the National Academy of Sciences of the United States of America 105, 95529557.
Xiao, C., Bator, C. M., Bowman, V. D., Rieder, E., He, Y., Hébert, B., Bella, J., Baker, T. S., Wimmer, E., Kuhn, R. J. & Rossmann, M. G. (2001). Interaction of coxsackievirus A21 with its cellular receptor, ICAM-1. Journal of Virology 75, 24442451.
Xiao, C., Chipman, P. R., Battisti, A. J., Bowman, V. D., Renesto, P., Raoult, D. & Rossmann, M. G. (2005). Cryo-electron microscopy of the giant Mimivirus. Journal of Molecular Biology 353, 493496.
Xiao, C., Kuznetsov, Y. G., Sun, S., Hafenstein, S. L., Kostyuchenko, V. A., Chipman, P. R., Suzan-Monti, M., Raoult, D., McPherson, A. & Rossmann, M. G. (2009). Structural studies of the giant Mimivirus. PLoS Biology 7, e1000092.
Xiao, C., McKinlay, M. A. & Rossmann, M. G. (2011). Design of capsid-binding antiviral agents against human rhinoviruses. In RSC Biomolecular Sciences Series, No. 21, Structural Virology (eds. Agbandje-McKenna, M. & McKenna, R.), pp. 321339. London, England: Royal Society of Chemistry.
Xiao, C. & Rossmann, M. G. (2011). Structures of giant icosahedral eukaryotic dsDNA viruses. Current Opinion in Virology 1, 101109.
Xie, Q., Bu, W., Bhatia, S., Hare, J., Somasundaram, T., Azzi, A. & Chapman, M. S. (2002). The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proceedings of the National Academy of Sciences of the United States of America 99, 1040510410.
Xie, Q. & Chapman, M. S. (1996). Canine parvovirus capsid structure, analyzed at 2·9 Å resolution. Journal of Molecular Biology 264, 497520.
Xu, L., Benson, S. D., Butcher, S. J., Bamford, D. H. & Burnett, R. M. (2003). The receptor binding protein P2 of PRD1, a virus targeting antibiotic-resistant bacteria, has a novel fold suggesting multiple functions. Structure 11, 309322.
Yan, X., Chipman, P. R., Castberg, T., Bratbak, G. & Baker, T. S. (2005). The marine algal virus PpV01 has an icosahedral capsid with T=219 quasi-symmetry. Journal of Virology 79, 92369243.
Yan, X., Olson, N. H., Van Etten, J. L., Bergoin, M., Rossmann, M. G. & Baker, T. S. (2000). Structure and assembly of large lipid-containing dsDNA viruses. Nature Structural Biology 7, 101103.
Yan, X., Yu, Z., Zhang, P., Battisti, A. J., Holdaway, H. A., Chipman, P. R., Bajaj, C., Bergoin, M., Rossmann, M. G. & Baker, T. S. (2009). The capsid proteins of a large, icosahedral dsDNA virus. Journal of Molecular Biology 385, 12871299.
Yin, H. S., Paterson, R. G., Wen, X., Lamb, R. A. & Jardetzky, T. S. (2005). Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proceedings of the National Academy of Sciences of the United States of America 102, 92889293.
Yin, H. S., Wen, X., Paterson, R. G., Lamb, R. A. & Jardetzky, T. S. (2006). Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439, 3844.
Yu, I.-M., Holdaway, H. A., Chipman, P. R., Kuhn, R. J., Rossmann, M. G. & Chen, J. (2009). Association of the pr peptides with dengue virus at acidic pH blocks membrane fusion. Journal of Virology 83, 1210112107.
Yu, I.-M., Zhang, W., Holdaway, H. A., Li, L., Kostyuchenko, V. A., Chipman, P. R., Kuhn, R. J., Rossmann, M. G. & Chen, J. (2008). Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 319, 18341837.
Yuan, P., Swanson, K. A., Leser, G. P., Paterson, R. G., Lamb, R. A. & Jardetzky, T. S. (2011). Structure of the Newcastle disease virus hemagglutinin-neuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proceedings of the National Academy of Sciences of the United States of America 108, 1492014925.
Zauberman, N., Mutsafi, Y., Halevy, D. B., Shimoni, E., Klein, E., Xiao, C., Sun, S. & Minsky, A. (2008). Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biology 6, e114.
Zhang, P., Mueller, S., Morais, M. C., Bator, C. M., Bowman, V. D., Hafenstein, S., Wimmer, E. & Rossmann, M. G. (2008). Crystal structure of CD155 and electron microscopic studies of its complexes with polioviruses. Proceedings of the National Academy of Sciences of the United States of America 105, 1828418289.
Zhang, R., Hryc, C. F., Cong, Y., Liu, X., Jakana, J., Gorchakov, R., Baker, M. L., Weaver, S. C. & Chiu, W. (2011a). 4·4 Å cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. EMBO Journal 30, 38543863.
Zhang, W., Chipman, P. R., Corver, J., Johnson, P. R., Zhang, Y., Mukhopadhyay, S., Baker, T. S., Strauss, J. H., Rossmann, M. G. & Kuhn, R. J. (2003a). Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nature Structural Biology 10, 907912.
Zhang, W., Mukhopadhyay, S., Pletnev, S. V., Baker, T. S., Kuhn, R. J. & Rossmann, M. G. (2002). Placement of the structural proteins in Sindbis virus. Journal of Virology 76, 1164511658.
Zhang, X., Sheng, J., Plevka, P., Kuhn, R. J., Diamond, M. S. & Rossmann, M. G. (2013). Dengue structure differs at the temperatures of its human and mosquito hosts. Proceedings of the National Academy of Sciences of the United States of America 110, 67956799.
Zhang, X., Sun, S., Xiang, Y., Wong, J., Klose, T., Raoult, D. & Rossmann, M. G. (2012). Structure of Sputnik, a virophage, at 3·5 Å resolution. Proceedings of the National Academy of Sciences of the United States of America 109, 1843118436.
Zhang, X., Walker, S. B., Chipman, P. R., Nibert, M. L. & Baker, T. S. (2003b). Reovirus polymerase l3 localized by cryo-electron microscopy of virions at a resolution of 7·6 Å. Nature Structural Biology 10, 10111018.
Zhang, X., Xiang, Y., Dunigan, D. D., Klose, T., Chipman, P. R., Van Etten, J. L. & Rossmann, M. G. (2011b). Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid. Proceedings of the National Academy of Sciences of the United States of America 108, 1483714842.
Zhang, Y., Corver, J., Chipman, P. R., Zhang, W., Pletnev, S. V., Sedlak, D., Baker, T. S., Strauss, J. H., Kuhn, R. J. & Rossmann, M. G. (2003c). Structures of immature flavivirus particles. EMBO Journal 22, 26042613.
Zhang, Y., Kaufmann, B., Chipman, P. R., Kuhn, R. J. & Rossmann, M. G. (2007). Structure of immature West Nile virus particles. Journal of Virology 81, 61416145.
Zhang, Y., Zhang, W., Ogata, S., Clements, D., Strauss, J. H., Baker, T. S., Kuhn, R. J. & Rossmann, M. G. (2004). Conformational changes of the flavivirus E glycoprotein. Structure 12, 16071618.
Zhang, Z., Kottadiel, V. I., Vafabakhsh, R., Dai, L., Chemla, Y. R., Ha, T. & Rao, V. B. (2011c). A promiscuous DNA packaging machine from bacteriophage T4. PLoS Biology 9, e1000592.