Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-24T00:49:18.984Z Has data issue: false hasContentIssue false
  • English
  • Français

Biophysics of viral infectivity: matching genome length with capsid size

Published online by Cambridge University Press:  21 April 2008

Elmar Nurmemmedov ,
Martin Castelnovo ,
Carlos Enrique Catalano  and
Alex Evilevitch
Elmar Nurmemmedov
Affiliation:
Department of Biochemistry, Center for Chemistry and Chemical Engineering, Lund University, Lund, Sweden
Martin Castelnovo
Affiliation:
Laboratoire Joliot-Curie – Laboratoire de Physique, Ecole Normale Superieure de Lyon, Lyon, France
Carlos Enrique Catalano
Affiliation:
Department of Medicinal Chemistry, University of Washington School of Pharmacy, Seattle, WA, USA
Alex Evilevitch*
Affiliation:
Department of Biochemistry, Center for Chemistry and Chemical Engineering, Lund University, Lund, Sweden
*
*Author for correspondence: Dr A. Evilevitch, Department of Biochemistry, Center for Chemistry and Chemical Engineering, Lund University, Box 124, S-221 00, Lund, Sweden.  Tel.: +46 46 222 3291; Fax: +46 46 222 4116; Email: Alex.Evilevitch@biochemistry.lu.se
Get access Rights & Permissions [Opens in a new window]

Abstract

In this review, we discuss recent advances in biophysical virology, presenting experimental and theoretical studies on the physical properties of viruses. We focus on the double-stranded (ds) DNA bacteriophages as model systems for all of the dsDNA viruses both prokaryotic and eukaryotic. Recent studies demonstrate that the DNA packaged into a viral capsid is highly pressurized, which provides a force for the first step of passive injection of viral DNA into a bacterial cell. Moreover, specific studies on capsid strength show a strong correlation between genome length, and capsid size and robustness. The implications of these newly appreciated physical properties of a viral particle with respect to the infection process are discussed.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 40 , Issue 4 , November 2007 , pp. 327 - 356
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

6. References

Alcorlo, M., Gonzalez-Huici, V., Hermoso, J. M., Meijer, W. J. & Salas, M. (2007). The phage phi29 membrane protein p16·7, involved in DNA replication, is required for efficient ejection of the viral genome. Journal of Bacteriology 189, 5542–5549.CrossRefGoogle ScholarPubMed
Ali, I., Marenduzzo, D. & Yeomans, J. M. (2006). Polymer packaging and ejection in viral capsids: shape matters. Physical Review Letters 96, 208102.CrossRefGoogle ScholarPubMed
Amalfitano, A. & Parks, R. J. (2002). Separating fact from fiction: assessing the potential of modified adenovirus vectors for use in human gene therapy. Current Gene Therapy 2, 111–133.CrossRefGoogle ScholarPubMed
Anderson, D. L. & Grimes, S. (2005). The phi29 DNA packaging motor: seeking the mechanism. In Viral Genome Packaging Machines: Genetics, Structure and Mechanism (ed. Catalano, C. E.), pp. 102–113. Georgetown, TX: Landes Bioscience/Eurekah.com.CrossRefGoogle Scholar
Anderson, T. F. (1950). Destruction of bacterial viruses by osmotic shock. Journal of Applied Physics 21, 70.Google Scholar
Anderson, T. F., Rappaport, C. & Muscatine, N. A. (1953). On the structure and osmotic properties of phage particles. Annales de l'Institut Pasteur (Paris) 84, 5–14.Google ScholarPubMed
Arscott, P. G., Li, A. Z. & Bloomfield, V. A. (1990). Condensation of DNA by trivalent cations. 1. Effects of DNA length and topology on the size and shape of condensed particles. Biopolymers 30, 619–630.CrossRefGoogle ScholarPubMed
Arsuaga, J., Tan, R. K., Vazquez, M., Sumners, D. W. & Harvey, S. C. (2002). Investigation of viral DNA packaging using molecular mechanics models. Biophysical Chemistry 101–102, 475–484.CrossRefGoogle ScholarPubMed
Baines, J. D. & Weller, S. K. (2005). Cleavage and packaging of herpes simplex virus 1 DNA. In Viral Genome Packaging Machines: Genetics, Structure and Mechanism (ed. Catalano, C. E.), pp. 135–150. Georgetown, TX, USA: Landes Bioscience/Eurekah.com.CrossRefGoogle Scholar
Bancroft, J. B., Hiebert, E., Rees, M. W. & Markham, R. (1968a). Properties of cowpea chlorotic mottle virus, its protein and nucleic acid. Virology 34, 224–239.CrossRefGoogle ScholarPubMed
Bancroft, J. B., Wagner, G. W. & Bracker, C. E. (1968b). The self-assembly of a nucleic-acid free pseudo-top component for a small spherical virus. Virology 36, 146–149.CrossRefGoogle ScholarPubMed
Baumann, R. G., Mullaney, J. & Black, L. W. (2006). Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Molecular Microbiology 61, 16–32.CrossRefGoogle ScholarPubMed
Becker, A. & Murialdo, H. (1990). Bacteriophage lambda DNA: the beginning of the end. Journal of Bacteriology 172, 2819–2824.CrossRefGoogle ScholarPubMed
Becker, A., Murialdo, H. & Gold, M. (1977). Studies on an in vitro system for the packaging and maturation of phage lambda DNA. Virology 78, 277–290.CrossRefGoogle Scholar
Berk, A. J. (2007). Adenoviridae: the viruses and their replication. In Fields Virology (ed. Knipe, D. M. and Howley, P. M.), pp. 2355–2394. Philadelphia, PA, USA: Lippincott, Williams and Wilkins.Google Scholar
Black, L. W. (1989). DNA packaging in dsDNA bacteriophages. Annual Review of Microbiology 43, 267–292.CrossRefGoogle ScholarPubMed
Black, L. W., Newcomb, W. W., Boring, J. W. & Brown, J. C. (1985). Ion etching bacteriophage T4: support for a spiral-fold model of packaged DNA. Proceedings of the National Academy of Sciences USA 82, 7960–7964.CrossRefGoogle ScholarPubMed
Bloomfield, V. A. (1991). Condensation of DNA by multivalent cations: considerations on mechanism. Biopolymers 31, 1471–1481.CrossRefGoogle ScholarPubMed
Bloomfield, V. A. (1997). DNA condensation by multivalent cations. Biopolymers 44, 269–282.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Boulanger, P., Le Maire, M., Bonhivers, M., Dubois, S., Desmadril, M. & Letellier, L. (1996). Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry 35, 14216–14224.CrossRefGoogle ScholarPubMed
Brockmann, D., Hufnagel, L. & Geisel, T. (2006). The scaling laws of human travel. Nature 439, 462–465.CrossRefGoogle ScholarPubMed
Buenemann, M. & Lenz, P. (2007). Mechanical limits of viral capsids. Proceedings of the National Academy of Sciences USA 104, 9925–9930.CrossRefGoogle ScholarPubMed
Calendar, R. (2006). The Bacteriophages, 2nd edn. New York: Oxford University Press.Google Scholar
Cardone, G., Winkler, D. C., Trus, B. L., Cheng, N., Heuser, J. E., Newcomb, W. W., Brown, J. C. & Steven, A. C. (2007). Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361, 426–434.CrossRefGoogle ScholarPubMed
Carrasco, C., Carreira, A., Schaap, I. A., Serena, P. A., Gomez-Herrero, J., Mateu, M. G. & De Pablo, P. J. (2006). DNA-mediated anisotropic mechanical reinforcement of a virus. Proceedings of the National Academy of Sciences USA 103, 13706–13711.CrossRefGoogle ScholarPubMed
Casjens, S. & Weigele, P. (2005). DNA packaging by bacteriophage P22. In Viral Genome Packaging Machines: Genetics, Structure and Mechanism (ed. Catalano, C. E.), pp. 80–88. Georgetown, TX, USA: Landes Bioscience/Eurekah.com.CrossRefGoogle Scholar
Caspar, D. L. & Klug, A. (1962). Physical principles in the construction of regular viruses. Cold Spring Harbor Symposium on Quantitative Biology 27, 1–24.CrossRefGoogle ScholarPubMed
Castelnovo, M., Bowles, R. K., Reiss, H. & Gelbart, W. M. (2003). Osmotic force resisting chain insertion in a colloidal suspension. European Physical Journal E. Soft Matter 10, 191–197.CrossRefGoogle Scholar
Castelnovo, M. & Evilevitch, A. (2007). DNA ejection from bacteriophage: towards a general behavior for osmotic-suppression experiments. European Physical Journal E. Soft Matter 24, 9–18.CrossRefGoogle ScholarPubMed
Catalano, C. E. (2005a). Viral genome packaging machines: an overview. In Viral Genome Packaging Machines: Genetics, Structure and Mechanism (ed. Catalano, C. E.), pp. 1–4. Georgetown, TX, USA: Landes Bioscience/Eurekah.com.CrossRefGoogle Scholar
Catalano, C. E. (2005b). Viral Genome Packaging Machines: Genetics, Structure and Mechanism. Georgetown, TX, USA: Landes Bioscience/Eurekah.com. New York, NY, USA: Kluwer Academic/Plenum Publishers.CrossRefGoogle Scholar
Cerritelli, M. E., Cheng, N., Rosenberg, A. H., McPherson, C. E., Booy, F. P. & Steven, A. C. (1997). Encapsidated conformation of bacteriophage T7 DNA. Cell 91, 271–280.CrossRefGoogle ScholarPubMed
Chai, S., Lurz, R. & Alonso, J. C. (1995). The small subunit of the terminase enzyme of Bacillus subtilis bacteriophage SPP1 forms a specialized nucleoprotein complex with the packaging initiation region. Journal of Molecular Biology 252, 386–398.CrossRefGoogle ScholarPubMed
Conway, J. F., Cheng, N., Ross, P. D., Hendrix, R. W., Duda, R. L. & Steven, A. C. (2007). A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged. Journal of Structural Biology 158, 224–232.CrossRefGoogle Scholar
Cordova, A., Deserno, M., Gelbart, W. M. & Ben-Shaul, A. (2003). Osmotic shock and the strength of viral capsids. Biophysical Journal 85, 70–74.CrossRefGoogle ScholarPubMed
Cue, D. & Feiss, M. (1997). Genetic evidence that recognition of cosQ, the signal for termination of phage lambda DNA packaging, depends on the extent of head filling. Genetics 147, 7–17.CrossRefGoogle ScholarPubMed
Daniels, D. L., Schroeder, J. L., Szybalski, W., Sanger, F., Coulson, A. R., Hong, G. F., Hill, D. F., Petersen, G. B. & Blattner, F. R. (1983). Complete annotated lambda sequence. In Lambda II (ed. Hendrix, R. W., Roberts, J. W., Stahl, F. W. and Weisberg, R. A.), pp. 522–523. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory.Google Scholar
De Frutos, M., Brasiles, S., Tavares, P. & Raspaud, E. (2005a). Effect of spermine and DNase on DNA release from bacteriophage T5. European Physical Journal E. Soft Matter 17, 429–434.CrossRefGoogle ScholarPubMed
De Frutos, M., Letellier, L. & Raspaud, E. (2005b). DNA ejection from bacteriophage T5: analysis of the kinetics and energetics. Biophysical Journal 88, 1364–1370.CrossRefGoogle ScholarPubMed
De Paepe, M. & Taddei, F. (2006). Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biology 4, e193.CrossRefGoogle ScholarPubMed
Dokland, T. (1999). Scaffolding proteins and their role in viral assembly. Cellular and Molecular Life Sciences 56, 580–603.CrossRefGoogle ScholarPubMed
Dokland, T. & Murialdo, H. (1993). Structural transitions during maturation of bacteriophage lambda capsids. Journal of Molecular Biology 233, 682–694.CrossRefGoogle ScholarPubMed
Droge, A. & Tavares, P. (2000). In vitro packaging of DNA of the Bacillus subtilis bacteriophage SPP1. Journal of Molecular Biology 296, 103–115.CrossRefGoogle ScholarPubMed
Droge, A. & Tavares, P. (2005). Bacteriophage SPP1 DNA packaging. In Viral Genome Packaging Machines: Genetics, Structure and Mechanism (ed. Catalano, C. E.), pp. 89–101. Georgetown, TX, USA: Landes Bioscience/Eurekah.com.CrossRefGoogle Scholar
Duda, R. L. (1998). Protein chainmail: catenated protein in viral capsids. Cell 94, 55–60.CrossRefGoogle ScholarPubMed
Earnshaw, W., Casjens, S. & Harrison, S. C. (1976). Assembly of the head of bacteriophage P22: x-ray diffraction from heads, proheads and related structures. Journal of Molecular Biology 104, 387–410.CrossRefGoogle ScholarPubMed
Earnshaw, W. C. & Casjens, S. R. (1980). DNA packaging by the double-stranded DNA bacteriophages. Cell 21, 319–331.CrossRefGoogle ScholarPubMed
Earnshaw, W. C. & Harrison, S. C. (1977). DNA arrangement in isometric phage heads. Nature 268, 598–602.CrossRefGoogle ScholarPubMed
Earnshaw, W. C., King, J., Harrison, S. C. & Eiserling, F. A. (1978). The structural organization of DNA packaged within the heads of T4 wild-type, isometric and giant bacteriophages. Cell 14, 559–568.CrossRefGoogle ScholarPubMed
Echols, H. (2001). Operators and Promoters: The Story of Molecular Biology and its Creators. Berkeley, CA: University of California Press.CrossRefGoogle Scholar
Enemark, E. J. & Joshua-Tor, L. (2006). Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442, 270–275.CrossRefGoogle Scholar
Evilevitch, A. (2006). Effects of condensing agent and nuclease on the extent of ejection from phage lambda. Journal of Physical Chemistry B, 110, 22261–22265.CrossRefGoogle ScholarPubMed
Evilevitch, A., Castelnovo, M., Knobler, C. M. & Gelbart, W. M. (2004). Measuring the force ejecting DNA from phage. Journal of Physical Chemistry B 108, 6838–6843.CrossRefGoogle Scholar
Evilevitch, A., Fang, L. T., Yoffe, A. M., Castelnovo, M., Rau, D. C., Parsegian, V. A., Gelbart, W. M. & Knobler, C. M. (2008). Effects of salt concentrations and bending energy on the extent of ejection of phage genomes. Biophysical Journal 94, 1110–1120.CrossRefGoogle ScholarPubMed
Evilevitch, A., Gober, J. W., Phillips, M., Knobler, C. M. & Gelbart, W. M. (2005). Measurements of DNA lengths remaining in a viral capsid after osmotically suppressed partial ejection. Biophysical Journal 88, 751–756.CrossRefGoogle Scholar
Evilevitch, A., Lavelle, L., Knobler, C. M., Raspaud, E. & Gelbart, W. M. (2003). Osmotic pressure inhibition of DNA ejection from phage. Proceedings of the National Academy of Sciences USA 100, 9292–9295.CrossRefGoogle ScholarPubMed
Feiss, M. & Catalano, C. E. (2005). Bacteriophage lambda terminase and the mechanism of viral DNA packaging. In Viral Genome Packaging Machines: Genetics, Structure, and Mechanism (ed. Catalano, C. E.), pp. 5–39. New York, NY, USA: Landes Bioscience/Eurekah.com.CrossRefGoogle Scholar
Feiss, M., Fisher, R. A., Crayton, M. A. & Egner, C. (1977). Packaging of the bacteriophage lambda chromosome: effect of chromosome length. Virology 77, 281–293.CrossRefGoogle ScholarPubMed
Finch, J. T. & Bancroft, J. B. (1968). Structure of the reaggregted protein shells of 2 spherical viruses. Nature 220, 815–816.CrossRefGoogle ScholarPubMed
Flint, S. J., Enquist, L. W., Racaniello, V. R. & Skalka, A. M. (2004a). Assembly, exit, and maturation. In Principles of Virology: Molecular Biology, Pathogenesis, and Control of Animal Viruses (ed. Flint, S. J.), pp. 451–491. Washington, DC, USA: ASM Press.Google Scholar
Flint, S. J., Enquist, L. W., Racaniello, V. R. & Skalka, A. M. (2004b). Attachment and entry. In Principles of Virology: Molecular Biology, Pathogenesis, and Control of Animal Viruses (ed. Flint, S. J.), pp. 127–180. Washington, DC, USA: ASM Press.Google Scholar
Flint, S. J., Enquist, L. W., Racaniello, V. R. & Skalka, A. M. (2004c). Prevention and control of viral diseases. In Principles of Virology: Molecular Biology, Pathogenesis, and Control of Animal Viruses (ed. Flint, S. J.), pp. 703–757. Washington, DC, USA: ASM Press.Google Scholar
Forrey, C. & Muthukumar, M. (2006). Langevin dynamics simulations of genome packing in bacteriophage. Biophysical Journal 91, 25–41.CrossRefGoogle ScholarPubMed
Fujisawa, H. & Morita, M. (1997). Phage DNA packaging. Genes Cells 2, 537–545.CrossRefGoogle ScholarPubMed
Fuller, D. N., Raymer, D. M., Kottadiel, V. I., Rao, V. B. & Smith, D. E. (2007a). Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proceedings of the National Academy of Sciences USA 104, 16868–16873.CrossRefGoogle ScholarPubMed
Fuller, D. N., Raymer, D. M., Rickgauer, J. P., Robertson, R. M., Catalano, C. E., Anderson, D. L., Grimes, S. & Smith, D. E. (2007b). Measurements of single DNA molecule packaging dynamics in bacteriophage lambda reveal high forces, high motor processivity, and capsid transformations. Journal of Molecular Biology 373, 1113–1122.CrossRefGoogle ScholarPubMed
Gabashvili, I. S. & Grosberg, A. (1991). Bacteriophage DNA reptation. Biofizika 36, 788–793.Google ScholarPubMed
Gabashvili, I. S. & Grosberg, A. (1992). Dynamics of double stranded DNA reptation from bacteriophage. Journal of Biomolcular Structure and Dynamics 9, 911–920.CrossRefGoogle ScholarPubMed
Gan, L., Conway, J. F., Firek, B. A., Cheng, N., Hendrix, R. W., Steven, A. C., Johnson, J. E. & Duda, R. L. (2004). Control of crosslinking by quaternary structure changes during bacteriophage HK97 maturation. Molecular Cell 14, 559–569.CrossRefGoogle ScholarPubMed
Gan, L., Speir, J. A., Conway, J. F., Lander, G., Cheng, N., Firek, B. A., Hendrix, R. W., Duda, R. L., Liljas, L. & Johnson, J. E. (2006). Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM. Structure 14, 1655–1665.CrossRefGoogle ScholarPubMed
Gaussier, H., Yang, Q. & Catalano, C. E. (2006). Building a virus from scratch: assembly of an infectious virus using purified components in a rigorously defined biochemical assay system. Journal of Molecular Biology 357, 1154–1166.CrossRefGoogle Scholar
Gibbons, M. M. & Klug, W. S. (2007a). Mechanical modeling of viral capsids. Journal of Materials Science 42, 8995–9004.CrossRefGoogle Scholar
Gibbons, M. M. & Klug, W. S. (2007b). Nonlinear finite-element analysis of nanoindentation of viral capsids. Physical Review E 75, 031901.CrossRefGoogle ScholarPubMed
Gonzalez-Huici, V., Salas, M. & Hermoso, J. M. (2004). The push-pull mechanism of bacteriophage O29 DNA injection. Molecular Microbiology 52, 529–540.CrossRefGoogle ScholarPubMed
Grayson, P., Evilevitch, A., Inamdar, M. M., Purohit, P. K., Gelbart, W. M., Knobler, C. M. & Phillips, R. (2006). The effect of genome length on ejection forces in bacteriophage lambda. Virology 348, 430–436.CrossRefGoogle ScholarPubMed
Grayson, P., Han, L., Winther, T. & Phillips, R. (2007). Real-time observations of single bacteriophage lambda DNA ejections in vitro. Proceedings of the National Academy of Sciences USA 104, 14652–14657.CrossRefGoogle ScholarPubMed
Guo, P., Grimes, S. & Anderson, D. (1986). A defined system for in vitro packaging of DNA-gp3 of the Bacillus subtilis bacteriophage phi 29. Proceedings of the National Academy of Sciences USA 83, 3505–3509.CrossRefGoogle ScholarPubMed
Hamada, K., Fujisawa, H. & Minagawa, T. (1986). A defined in vitro system for packaging of bacteriophage T3 DNA. Virology 151, 119–123.CrossRefGoogle ScholarPubMed
Harrison, D. P. & Bode, V. C. (1975). Putrescine and certain polyamines can inhibit DNA injection from bacteriophage lambda. Journal of Molecular Biology 96, 461–470.CrossRefGoogle ScholarPubMed
Harrison, S. C. (1983). Packaging of DNA into bacteriophage heads: a model. Journal of Molecular Biology 171, 577–580.CrossRefGoogle ScholarPubMed
Hendrix, R. W. (1978). Symmetry mismatch and DNA packaging in large bacteriophages. Proceedings of the National Academy of Sciences USA 75, 4779–4783.CrossRefGoogle ScholarPubMed
Hendrix, R. X., Roberts, J. W., Stahl, F. W. & Weisberg, R. A. (1983). Lambda II. New York: Cold Spring Harbor Laboratory.Google Scholar
Hershey, A. D. & Chase, M. (1952). Independent functions of viral protein and nucleic acid in growth of bacteriophage. Journal of General Physiology 36, 39–56.CrossRefGoogle ScholarPubMed
Hiebert, E., Bancroft, J. B. & Bracker, C. E. (1968). The assembly in vitro of some small spherical viruses, hybrid viruses, and other nucleoproteins. Virology 34, 492–508.CrossRefGoogle ScholarPubMed
Hwang, Y. & Feiss, M. (1995). A defined system for in vitro lambda DNA packaging. Virology 211, 367–376.CrossRefGoogle ScholarPubMed
Inamdar, M. M., Gelbart, W. M. & Phillips, R. (2006). Dynamics of DNA ejection from bacteriophage. Biophysical Journal 91, 411–420.CrossRefGoogle ScholarPubMed
Ivanovska, I., Wuite, G., Jonsson, B. & Evilevitch, A. (2007). Internal DNA pressure modifies stability of WT phage. Proceedings of the National Academy of Sciences USA 104, 9603–9608.CrossRefGoogle ScholarPubMed
Ivanovska, I. L., De Pablo, P. J., Ibarra, B., Sgalari, G., Mackintosh, F. C., Carrascosa, J. L., Schmidt, C. F. & Wuite, G. J. (2004). Bacteriophage capsids: tough nanoshells with complex elastic properties. Proceedings of the National Academy of Sciences USA 101, 7600–7605.CrossRefGoogle ScholarPubMed
Jeruzalmi, D., O'Donnell, M. & Kuriyan, J. (2002). Clamp loaders and sliding clamps. Current Opinion in Structural Biology 12, 217–224.CrossRefGoogle ScholarPubMed
Kainov, D. E., Mancini, E. J., Telenius, J., Lisal, J., Grimes, J. M., Bamford, D. H., Stuart, D. I. & Tuma, R. (2008). Structural basis of mechanochemical coupling in a hexameric molecular motor. Journal of Biological Chemistry 283, 3607–3617.CrossRefGoogle Scholar
Kegel, W. K. & van der Schoot, P. (2004). Competing hydrophobic and screened-coulomb interactions in hepatitis B virus capsid assembly. Biophysical Journal 86, 3905–3913.CrossRefGoogle ScholarPubMed
Kemp, P., Gupta, M. & Molineux, I. J. (2004). Bacteriophage T7 DNA ejection into cells is initiated by an enzyme-like mechanism. Molecular Microbiology 53, 1251–1265.CrossRefGoogle ScholarPubMed
Kindt, J., Tzlil, S., Ben-Shaul, A. & Gelbart, W. M. (2001). DNA packaging and ejection forces in bacteriophage. Proceedings of the National Academy of Sciences USA 98, 13671–13674.CrossRefGoogle ScholarPubMed
Klug, W. S., Bruinsma, R. F., Michel, J. P., Knobler, C. M., Ivanovska, I. L., Schmidt, C. F. & Wuite, G. J. (2006). Failure of viral shells. Physical Review Letters 97, 228101.CrossRefGoogle ScholarPubMed
Klug, W. S. & Ortiz, M. (2003). A director field model of DNA packaging in viral capsids. Journal of the Mechanics and Physics of Solids 51, 1815–1847.CrossRefGoogle Scholar
Knipe, D. M. & Howley, P. M. (2007). Fields Virology, 5th edn. Philadelphia, PA, USA: Lippincott, Williams and Wilkins.Google Scholar
Kol, N., Gladnikoff, M., Barlam, D., Shneck, R. Z., Rein, A. & Rousso, I. (2006). Mechanical properties of murine leukemia virus particles: effect of maturation. Biophysical Journal 91, 767–774.CrossRefGoogle ScholarPubMed
Kol, N., Shi, Y., Tsvitov, M., Barlam, D., Shneck, R. Z., Kay, M. S. & Rousso, I. (2007). A stiffness switch in human immunodeficiency virus. Biophysical Journal 92, 1777–1783.CrossRefGoogle ScholarPubMed
Kushner, D. J. (1969). Self-assembly of biological structures. Bacteriology Reviews 33, 302–345.CrossRefGoogle ScholarPubMed
Lamarque, J. C., Le, T. V. & Harvey, S. C. (2004). Packaging double-helical DNA into viral capsids. Biopolymers 73, 348–355.CrossRefGoogle ScholarPubMed
Lander, G. C., Tang, L., Casjens, S. R., Gilcrease, E. B., Prevelige, P., Poliakov, A., Potter, C. S., Carragher, B. & Johnson, J. E. (2006). The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312, 1791–1795.CrossRefGoogle ScholarPubMed
Lanni, Y. T. (1968). First-step-transfer deoxyribonucleic acid of bacteriophage T5. Bacteriology Reviews 32, 227–242.CrossRefGoogle ScholarPubMed
Lata, R., Conway, J. F., Cheng, N., Duda, R. L., Hendrix, R. W., Wikoff, W. R., Johnson, J. E., Tsuruta, H. & Steven, A. C. (2000). Maturation dynamics of a viral capsid: visualization of transitional intermediate states. Cell 100, 253–263.CrossRefGoogle ScholarPubMed
Lee, K. K., Gan, L., Tsuruta, H., Hendrix, R. W., Duda, R. L. & Johnson, J. E. (2004). Evidence that a local refolding event triggers maturation of HK97 bacteriophage capsid. Journal of Molecular Biology 340, 419–433.CrossRefGoogle ScholarPubMed
Lidmar, J., Mirny, L. & Nelson, D. R. (2003). Virus shapes and buckling transitions in spherical shells. Physical Review E 68, 051910.CrossRefGoogle ScholarPubMed
Lin, H., Simon, M. N. & Black, L. W. (1997). Purification and characterization of the small subunit of phage T4 terminase, gp16, required for DNA packaging. Journal of Biological Chemistry 272, 3495–3501.CrossRefGoogle ScholarPubMed
Locker, C. R. & Harvey, S. C. (2006). A model for viral genome packing. Multiscale Modeling and Simulation 5, 1264–1279.CrossRefGoogle Scholar
Lof, D., Schillen, K., Jonsson, B. & Evilevitch, A. (2007a). Dynamic and static light scattering analysis of DNA ejection from the phage lambda. Physical Review E. Statistical, Nonlinear and Soft Matter Physics 76, 011914.CrossRefGoogle ScholarPubMed
Lof, D., Schillen, K., Jonsson, B. & Evilevitch, A. (2007b). Forces controlling the rate of DNA ejection from phage lambda. Journal of Molecular Biology 368, 55–65.CrossRefGoogle ScholarPubMed
Maluf, N. K., Gaussier, H., Bogner, E., Feiss, M. & Catalano, C. E. (2006). Assembly of bacteriophage lambda terminase into a viral DNA maturation and packaging machine. Biochemistry 45, 15259–15268.CrossRefGoogle ScholarPubMed
Mangenot, S., Hochrein, M., Radler, J. & Letellier, L. (2005). Real-time imaging of DNA ejection from single phage particles. Current Biology 15, 430–435.CrossRefGoogle ScholarPubMed
Michel, J. P., Ivanovska, I. L., Gibbons, M. M., Klug, W. S., Knobler, C. M., Wuite, G. J. & Schmidt, C. F. (2006). Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proceedings of the National Academy of Sciences USA 103, 6184–6189.CrossRefGoogle ScholarPubMed
Mitchell, M. S., Matsuzaki, S., Imai, S. & Rao, V. B. (2002). Sequence analysis of bacteriophage T4 DNA packaging/terminase genes 16 and 17 reveals a common ATPase center in the large subunit of viral terminases. Nucleic Acids Research 30, 4009–4021.CrossRefGoogle ScholarPubMed
Molineux, I. J. (2001). No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Molecular Microbiology 40, 1–8.CrossRefGoogle ScholarPubMed
Morais, M. C., Tao, Y., Olson, N. H., Grimes, S., Jardine, P. J., Anderson, D. L., Baker, T. S. & Rossmann, M. G. (2001). Cryoelectron-microscopy image reconstruction of symmetry mismatches in bacteriophage phi29. Journal of Structural Biology 135, 38–46.CrossRefGoogle ScholarPubMed
Neidhardt, F. (1996). Escherichia coli and Salmonella typhimirium, p. 1211. Washington, DC, USA: ASM Press.Google Scholar
Newcomb, W. W., Booy, F. P. & Brown, J. C. (2007). Uncoating the herpes simplex virus genome. Journal of Molecular Biology 370, 633–642.CrossRefGoogle ScholarPubMed
Nguyen, T. T., Bruinsma, R. F. & Gelbart, W. M. (2005). Elasticity theory and shape transitions of viral shells. Physical Review E 72, 051923.CrossRefGoogle ScholarPubMed
Odijk, T. (1998). Hexagonally packed DNA within bacteriophage T7 stabilized by curvature stress. Biophysical Journal 75, 1223–1227.CrossRefGoogle ScholarPubMed
Ojala, P. M., Sodeik, B., Ebersold, M. W., Kutay, U. & Helenius, A. (2000). Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Molecular Cell Biology 20, 4922–4931.CrossRefGoogle ScholarPubMed
Oliveira, L., Alonso, J. C. & Tavares, P. (2005). A defined in vitro system for DNA packaging by the bacteriophage SPP1: insights into the headful packaging mechanism. Journal of Molecular Biology 353, 529–539.CrossRefGoogle ScholarPubMed
Oppenheim, A. & Peleg, A. (1989). Helpers for efficient encapsidation of SV40 pseudovirions. Gene 77, 79–86.CrossRefGoogle ScholarPubMed
Parsegian, V. A., Rand, R. P., Fuller, N. L. & Rau, D. C. (1986). Osmotic stress for the direct measurement of intermolecular forces. Methods in Enzymology 127, 400–416.CrossRefGoogle ScholarPubMed
Patel, S. S. & Donmez, I. (2006). Mechanisms of helicases. Journal of Biological Chemistry 281, 18265–18268.CrossRefGoogle ScholarPubMed
Petrov, A. S., Boz, M. B. & Harvey, S. C. (2007a). The conformation of double-stranded DNA inside bacteriophages depends on capsid size and shape. Journal of Structural Biology 160, 241–248.CrossRefGoogle ScholarPubMed
Petrov, A. S., Lim-Hing, K. & Harvey, S. C. (2007b). Packaging of DNA by bacteriophage epsilon15: structure, forces, and thermodynamics. Structure 15, 807–812.CrossRefGoogle ScholarPubMed
Ptashne, M. (2004). Genetic Switch: Phage Lambda Revisited. New York: Cold Spring Harbor Laboratory.Google Scholar
Purohit, P. K., Inamdar, M. M., Grayson, P. D., Squires, T. M., Kondev, J. & Phillips, R. (2005). Forces during bacteriophage DNA packaging and ejection. Biophysical Journal 88, 851–866.CrossRefGoogle ScholarPubMed
Purohit, P. K., Kondev, J. & Phillips, M. (2003a). Force steps during viral DNA packaging? Journal of the Mechanics and Physics of Solids 51, 2239–2257.CrossRefGoogle Scholar
Purohit, P. K., Kondev, J. & Phillips, R. (2003b). Mechanics of DNA packaging in viruses. Proceedings of the National Academy of Sciences USA 100, 3173–3178.CrossRefGoogle ScholarPubMed
Rao, V. B., Thaker, V. & Black, L. W. (1992). A phage T4 in vitro packaging system for cloning long DNA molecules. Gene 113, 25–33.CrossRefGoogle ScholarPubMed
Raspaud, E., Durand, D. & Livolant, F. (2005). Interhelical spacing in liquid crystalline spermine and spermidine-DNA precipitates. Biophysical Journal 88, 392–403.CrossRefGoogle ScholarPubMed
Raspaud, E., Olvera De La Cruz, M., Sikorav, J. L. & Livolant, F. (1998). Precipitation of DNA by polyamines: a polyelectrolyte behavior. Biophysical Journal 74, 381–393.CrossRefGoogle ScholarPubMed
Rau, D. C. & Parsegian, V. A. (1992). Direct measurement of the intermolecular forces between counterion-condensed DNA double helices. Evidence for long range attractive hydration forces. Biophysical Journal 61, 246–259.CrossRefGoogle ScholarPubMed
Rentas, F. J. & Rao, V. B. (2003). Defining the bacteriophage T4 DNA packaging machine: evidence for a C-terminal DNA cleavage domain in the large terminase/packaging protein gp17. Journal of Molecular Biology 334, 37–52.CrossRefGoogle ScholarPubMed
Richards, K. E., Williams, R. C. & Calendar, R. (1973). Mode of DNA packing within bacteriophage heads. Journal of Molecular Biology 78, 255–259.CrossRefGoogle ScholarPubMed
Rickgauer, J. P., Fuller, D. N., Grimes, S., Jardine, P. J., Anderson, D. L. & Smith, D. E. (2008). Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage ϕ29. Biophysical Journal 94, 159–167.CrossRefGoogle Scholar
Riemer, S. C. & Bloomfield, V. A. (1978). Packaging of DNA in bacteriophage heads: some considerations on energetics. Biopolymers 17, 785–794.CrossRefGoogle ScholarPubMed
Roa, M. & Scandella, D. (1976). Multiple steps during the interaction between coliphage lambda and its receptor protein in vitro. Virology 72, 182–194.CrossRefGoogle ScholarPubMed
Ross, P. D., Cheng, N., Conway, J. F., Firek, B. A., Hendrix, R. W., Duda, R. L. & Steven, A. C. (2005). Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization. EMBO Journal 24, 1352–1363.CrossRefGoogle ScholarPubMed
Ross, P. D., Conway, J. F., Cheng, N., Dierkes, L., Firek, B. A., Hendrix, R. W., Steven, A. C. & Duda, R. L. (2006). A free energy cascade with locks drives assembly and maturation of bacteriophage HK97 capsid. Journal of Molecular Biology 364, 512–525.CrossRefGoogle ScholarPubMed
Sao-Jose, C., Lhuillier, S., Lurz, R., Melki, R., Lepault, J., Santos, M. A. & Tavares, P. (2006). The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. Journal of Biological Chemistry 281, 11464–11470.CrossRefGoogle ScholarPubMed
Schellman, J. A. & Parthasarathy, N. (1984). X-ray diffraction studies on cation-collapsed DNA. Journal of Molecular Biology 175, 313–329.CrossRefGoogle ScholarPubMed
Serwer, P. (1986). Arrangement of double-stranded DNA packaged in bacteriophage capsids. An alternative model. Journal of Molecular Biology 190, 509–512.CrossRefGoogle ScholarPubMed
Shibata, H., Fujisawa, H. & Minagawa, T. (1987). Early events in DNA packaging in a defined in vitro system of bacteriophage T3. Virology 159, 250–258.CrossRefGoogle Scholar
Sikorav, J. L., Pelta, J. & Livolant, F. (1994). A liquid crystalline phase in spermidine-condensed DNA. Biophysical Journal 67, 1387–1392.CrossRefGoogle ScholarPubMed
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. (2000). Structure of the bacteriophage phi29 DNA packaging motor. Nature 408, 745–750.CrossRefGoogle ScholarPubMed
Smith, D. E., Tans, S. J., Smith, S. B., Grimes, S., Anderson, D. L. & Bustamante, C. (2001). The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 413, 748–752.CrossRefGoogle ScholarPubMed
Spakowitz, A. J. & Wang, Z. G. (2005). DNA packaging in bacteriophage: is twist important? Biophysical Journal 88, 3912–3923.CrossRefGoogle ScholarPubMed
Sternberg, N. & Weisberg, R. (1977). Packaging of coliphage lambda DNA. II. The role of the gene D protein. Journal of Molecular Biology 117, 733–759.CrossRefGoogle ScholarPubMed
Story, R. M., Li, H. & Abelson, J. N. (2001). Crystal structure of a DEAD box protein from the hyperthermophile Methanococcus jannaschii. Proceedings of the National Academy of Sciences USA 98, 1465–1470.CrossRefGoogle ScholarPubMed
Strey, H. H., Podgornik, R., Rau, D. C. & Parsegian, V. A. (1998). DNA–DNA interactions. Current Opinion in Structural Biology 8, 309–313.CrossRefGoogle ScholarPubMed
Sun, M., Louie, D. & Serwer, P. (1999). Single-event analysis of the packaging of bacteriophage T7 DNA concatemers in vitro. Biophysical Journal 77, 1627–1637.CrossRefGoogle ScholarPubMed
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, 943–949.CrossRefGoogle ScholarPubMed
Suwalsky, M., Traub, W., Shmueli, U. & Subirana, J. A. (1969). An X-ray study of the interaction of DNA with spermine. Journal of Molecular Biology 42, 363–373.CrossRefGoogle ScholarPubMed
Tama, F. & Brooks, C. L. 3rd. (2005). Diversity and identity of mechanical properties of icosahedral viral capsids studied with elastic network normal mode analysis. Journal of Molecular Biology 345, 299–314.CrossRefGoogle ScholarPubMed
Thomas, W. E., Trintchina, E., Forero, M., Vogel, V. & Sokurenko, E. V. (2002). Bacterial adhesion to target cells enhanced by shear force. Cell 109, 913–923.CrossRefGoogle ScholarPubMed
Tristram-Nagle, S. & Nagle, J. F. (2007). HIV-1 fusion peptide decreases bending energy and promotes curved fusion intermediates. Biophysical Journal 93, 2048–2055.CrossRefGoogle ScholarPubMed
Tzlil, S., Kindt, J. T., Gelbart, W. M. & Ben-Shaul, A. (2003). Forces and pressures in DNA packaging and release from viral capsids. Biophysical Journal 84, 1616–1627.CrossRefGoogle ScholarPubMed
Wagner, G. W. & Bancroft, J. B. (1968). The self-assembly of spherical viruses with mixed coat proteins. Virology 34, 748–756.CrossRefGoogle ScholarPubMed
WHO (2007). A safer future: global public health security in the 21st century. The World Health Report, 2007. Geneva: World Health Organization.Google Scholar
Widom, M., Lidmar, J. & Nelson, D. R. (2007). Soft modes near the buckling transition of icosahedral shells. Physical Review E 76, 031911.CrossRefGoogle ScholarPubMed
Wikoff, W. R., Che, Z., Duda, R. L., Hendrix, R. W. & Johnson, J. E. (2003). Crystallization and preliminary analysis of a dsDNA bacteriophage capsid intermediate: Prohead II of HK97. Acta Crystallographica D. Biological Crystallography 59, 2060–2064.CrossRefGoogle ScholarPubMed
Wikoff, W. R., Conway, J. F., Tang, J., Lee, K. K., Gan, L., Cheng, N., Duda, R. L., Hendrix, R. W., Steven, A. C. & Johnson, J. E. (2006). Time-resolved molecular dynamics of bacteriophage HK97 capsid maturation interpreted by electron cryo-microscopy and X-ray crystallography. Journal of Structural Biology 153, 300–306.CrossRefGoogle ScholarPubMed
Wikoff, W. R., Duda, R. L., Hendrix, R. W. & Johnson, J. E. (1998). Crystallization and preliminary X-ray analysis of the dsDNA bacteriophage HK97 mature empty capsid. Virology 243, 113–118.CrossRefGoogle ScholarPubMed
Wikoff, W. R., Duda, R. L., Hendrix, R. W. & Johnson, J. E. (1999). Crystallographic analysis of the dsDNA bacteriophage HK97 mature empty capsid. Acta Crystallographica D. Biological Crystallography 55, 763–771.CrossRefGoogle ScholarPubMed
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, 2129–2133.CrossRefGoogle ScholarPubMed
Yang, Q. & Catalano, C. E. (2003). Biochemical characterization of bacteriophage lambda genome packaging in vitro. Virology 305, 276–287.CrossRefGoogle ScholarPubMed
Zheng, H., Olia, A. S., Gonen, M., Andrews, S., Cingolani, G. & Gonen, T. (2008). A conformational switch in bacteriophage p22 portal protein primes genome injection. Molecular Cell 29, 376–383.CrossRefGoogle ScholarPubMed
Zimmerman, S. B. (1993). Macromolecular crowding effects on macromolecular interactions: some implications for genome structure and function. Biochimica et Biophysica Acta 1216, 175–185.CrossRefGoogle ScholarPubMed