DNA bending-induced phase transition of encapsidated genome in phage λ

Nucleic Acids Research

Volumn 41, Issue 8, 2013, Pages 4518-4524

  Lander, Gabriel C ^a   Johnson, John E ^a   Rau, Donald C ^b   Potter, Clinton S ^a   Carragher, Bridget ^a   Evilevitch, Alex ^c,d  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c CARNEGIE MELLON UNIVERSITY   (United States)

^d LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CURVED DNA; DOUBLE STRANDED DNA; SPERMINE; VIRUS DNA;

ARTICLE; BACTERIOPHAGE LAMBDA; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; DNA BINDING; DNA PACKAGING; DNA STRAND; DNA STRUCTURE; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; VIRUS CAPSID; VIRUS GENOME;

BACTERIOPHAGE LAMBDA; CAPSID; CRYOELECTRON MICROSCOPY; DNA PACKAGING; DNA, VIRAL; GENOME, VIRAL; NUCLEIC ACID CONFORMATION; VIRUS ASSEMBLY;

EID: 84877302870     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt137     Document Type: Article

References (47)

1. Flint, S.J., Enquist, L.W., Krug, R.M., Skalka, A.M. and Racaniello, V.R. (2000) Principles of Virology: Molecular Biology, Pathogenesis and Control. American Society for Microbiology, Washington, DC.
2. Rau, D.C. and Parsegian, V.A. (1992) Direct measurement of temperature-dependent solvation forces between DNA double helices. Biophys. J., 61, 260-271.
3. Rodriguez, M., Rau, D., O'Sullivan, D., Brown, A.H., Papa, R. and Attene, G. (2012) Genetic structure and linkage disequilibrium in landrace populations of barley in Sardinia. Theor. Appl. Genet., 125, 171-184.
4. Strey, H.H., Podgornik, R., Rau, D.C. and Parsegian, V.A. (1998) DNA-DNA interactions. Curr. Opin. Struct. Biol., 8, 309-313.
5. Leikin, S., Parsegian, V.A., Rau, D.C. and Rand, R.P. (1993) Hydration forces. Ann. Rev. Phys. Chem., 44, 369-395.
6. Stanley, C. and Rau, D.C. (2011) Evidence for water structuring forces between surfaces. Curr. Opin. Colloid Interface Sci., 16, 551-556.
7. Earnshaw, W.C. and Casjens, S.R. (1980) DNA packaging by the double-stranded DNA bacteriophages. Cell, 21, 319-331.
8. Qiu, X., Rau, D.C., Parsegian, V.A., Fang, L.T., Knobler, C.M. and Gelbart, W.M. (2011) Salt-dependent DNA-DNA spacings in intact bacteriophage lambda reflect relative importance of DNA self-repulsion and bending energies. Phys. Rev. Lett., 106, 028102.
9. Parsegian, V.A., Rand, R.P., Fuller, N.L. and Rau, D.C. (1986) Osmotic stress for the direct measurement of intermolecular forces. Methods Enzymol., 127, 400-416.
10. Rau, D.C., Lee, B. and Parsegian, V.A. (1984) Measurement of the repulsive force between polyelectrolyte molecules in ionic solution: hydration forces between parallel DNA double helices. Proc. Natl Acad. Sci. USA, 81, 2621-2625.
11. Todd, B.A. and Rau, D.C. (2008) Interplay of ion binding and attraction in DNA condensed by multivalent cations. Nucleic Acids Res., 36, 501-510.
12. Todd, B.A., Parsegian, V.A., Shirahata, A., Thomas, T.J. and Rau, D.C. (2008) Attractive forces between cation condensed DNA double helices. Biophys. J., 94, 4775-4782.
13. Rau, D.C. and Parsegian, V.A. (1992) Direct measurement of the intermolecular forces between counterion-condensed DNA double helices. Evidence for long range attractive hydration forces. Biophys. J., 61, 246-259.
14. Raspaud, E., Durand, D. and Livolant, F. (2005) Interhelical spacing in liquid crystalline spermine and spermidine-DNA precipitates. Biophys. J., 88, 392-403.
15. Hud, N.V. and Downing, K.H. (2001) Cryoelectron microscopy of lambda phage DNA condensates in vitreous ice: the fine structure of DNA toroids. Proc. Natl Acad. Sci. USA, 98, 14925-14930.
16. Evilevitch, A., Fang, L.T., Yoffe, A.M., Castelnovo, M., Rau, D.C., Parsegian, V.A., Gelbart, W.M. and Knobler, C.M. (2008) Effects of salt concentrations and bending energy on the extent of ejection of phage genomes. Biophys. J., 94, 1110-1120.
17. Tzlil, S., Kindt, J.T., Gelbart, W.M. and Ben-Shaul, A. (2003) Forces and pressures in DNA packaging and release from viral capsids. Biophys. J., 84, 1616-1627.
18. Kindt, J., Tzlil, S., Ben-Shaul, A. and Gelbart, W.M. (2001) DNA packaging and ejection forces in bacteriophage. Proc. Natl Acad. Sci. USA, 98, 13671-13674.
19. Silhavy, T.J. (1984) Experiments with gene fusions. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
20. Graff, A., Sauer, M., Van Gelder, P. and Meier, W. (2002) Virus-assisted loading of polymer nanocontainer. Proc. Natl Acad. Sci. USA, 99, 5064-5068.
21. Roa, M. and Scandella, D. (1976) Multiple steps during interaction between coliphage-lambda and its receptor protein Invitro. Virology, 72, 182-194.
22. Suloway, C., Pulokas, J., Fellmann, D., Cheng, A., Guerra, F., Quispe, J., Stagg, S., Potter, C.S. and Carragher, B. (2005) Automated molecular microscopy: the new Leginon system. J. Struct. Biol., 151, 41-60.
23. Lander, G.C., Stagg, S.M., Voss, N.R., Cheng, A., Fellmann, D., Pulokas, J., Yoshioka, C., Irving, C., Mulder, A., Lau, P.W. et al. (2009) Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol., 166, 95-102.
24. Roseman, A.M. (2004) FindEM-a fast, efficient program for automatic selection of particles from electron micrographs. J. Struct. Biol., 145, 91-99.
25. Mallick, S.P., Carragher, B., Potter, C.S. and Kriegman, D.J. (2005) ACE: automated CTF estimation. Ultramicroscopy, 104, 8-29.
26. Ludtke, S.J., Baldwin, P.R. and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol., 128, 82-97.
27. Booy, F.P., Newcomb, W.W., Trus, B.L., Brown, J.C., Baker, T.S. and Steven, A.C. (1991) Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell, 64, 1007-1015.
28. Jiang, W., Chang, J., Jakana, J., Weigele, P., King, J. and Chiu, W. (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature, 439, 612-616.
29. Cerritelli, M.E., Cheng, N., Rosenberg, A.H., McPherson, C.E., Booy, F.P. and Steven, A.C. (1997) Encapsidated conformation of bacteriophage T7 DNA. Cell, 91, 271-280.
30. Huet, A., Conway, J.F., Letellier, L. and Boulanger, P. (2010) In vitro assembly of the T=13 procapsid of bacteriophage T5 with its scaffolding domain. J. Virol., 84, 9350-9358.
31. Comolli, L.R., Spakowitz, A.J., Siegerist, C.E., Jardine, P.J., Grimes, S., Anderson, D.L., Bustamante, C. and Downing, K.H. (2008) Three-dimensional architecture of the bacteriophage phi29 packaged genome and elucidation of its packaging process. Virology, 371, 267-277.
32. Lander, G.C., Evilevitch, A., Jeembaeva, M., Potter, C.S., Carragher, B. and Johnson, J.E. (2008) Bacteriophage lambda stabilization by auxiliary protein gpD: timing, location, and mechanism of attachment determined by cryo-EM. Structure, 16, 1399-1406.
33. Earnshaw, W.C. and Harrison, S.C. (1977) DNA arrangement in isometric phage heads. Nature, 268, 598-602.
34. Yang, J. and Rau, D.C. (2005) Incomplete ion dissociation underlies the weakened attraction between DNA helices at high spermidine concentrations. Biophys. J., 89, 1932-1940.
35. Nurmemmedov, E., Castelnovo, M., Medina, E., Catalano, C.E. and Evilevitch, A. (2012) Challenging packaging limits and infectivity of phage lambda. J. Mol. Biol., 415, 263-273.
36. Park, S.Y., Harries, D. and Gelbart, W.M. (1998) Topological defects and the optimum size of DNA condensates. Biophys. J., 75, 714-720.
37. Evilevitch, A. (2006) Effects of condensing agent and nuclease on the extent of ejection from phage lambda. J. Phys. Chem. B, 110, 22261-22265.
38. Evilevitch, A., Lavelle, L., Knobler, C.M., Raspaud, E. and Gelbart, W.M. (2003) Osmotic pressure inhibition of DNA ejection from phage. Proc. Natl Acad. Sci. USA, 100, 9292-9295.
39. Evilevitch, A., Gober, J.W., Phillips, M., Knobler, C.K. and Gelbart, W.M. (2005) Measurements of DNA lengths remaining in a viral capsid after osmotically suppressed partial ejection. Biophys. J., 88, 751-756.
40. Kornyshev, A.A., Leikin, S. and Malinin, S.V. (2002) Chiral electrostatic interaction and cholesteric liquid crystals of DNA. Eur. Phys. J. E, 7, 83-93.
41. Cherstvy, A.G., Kornyshev, A.A. and Leikin, S. (2002) Temperature-dependent DNA condensation triggered by rearrangement of adsorbed cations. J. Phys. Chem. B, 106, 13362-13369.
42. Leforestier, A. and Livolant, F. (1993) Supramolecular ordering of DNA in the cholesteric liquid crystalline phase: an ultrastructural study. Biophys. J., 65, 56-72.
43. Leforestier, A. and Livolant, F. (1991) Cholesteric liquid crystalline DNA; a comparative analysis of cryofixation methods. Biol. Cell, 71, 115-122.
44. Livolant, F., Levelut, A.M., Doucet, J. and Benoit, J.P. (1989) The highly concentrated liquid-crystalline phase of DNA is columnar hexagonal. Nature, 339, 724-726.
45. Livolant, F. (1984) Cholesteric organization of DNA in the stallion sperm head. Tissue Cell, 16, 535-555.
46. Livolant, F. (1984) Cholesteric organization of DNA in vivo and in vitro. Eur. J. Cell Biol., 33, 300-311.
47. Lepault, J., Dubochet, J., Baschong, W. and Kellenberger, E. (1987) Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. EMBO J., 6, 1507-1512.