Protein-DNA interactions determine the shapes of DNA toroids condensed in virus capsids

Biophysical Journal

Volumn 100, Issue 9, 2011, Pages 2209-2216

  Leforestier, Amélie ^a   Šiber, Antonio ^b   Livolant, Françoise ^a   Podgornik, Rudolf ^c,d  

^a UNIVERSITÉ PARIS SUD   (France)

^b INSTITUTE OF PHYSICS   (Croatia)

^c JO EF STEFAN INSTITUTE   (Slovenia)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

MIRIDAE;

EID: 79959721686     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.03.012     Document Type: Article

References (48)

1. Wolffe, A. P. 1998. Chromatin structure. Advances in Genome Biology. 5:363-414.
2. Cerritelli, M. E., N. Cheng,..., A. C. Steven. 1997. Encapsidated conformation of bacteriophage T7 DNA. Cell. 91:271-280. (Pubitemid 27456394)
3. Bloomfield, V. A. 1996. DNA condensation. Curr. Opin. Struct. Biol. 6:334-341. (Pubitemid 26197433)
4. Hud, N. V., and I. D. Vilfan. 2005. Toroidal DNA condensates: unraveling the fine structure and the role of nucleation in determining size. Annu. Rev. Biophys. Biomol. Struct. 34:295-318. (Pubitemid 40847727)
5. Evdokimov, Y. M., A. L. Platonov,..., Y. M. Varshavsky. 1972. A compact form of double-stranded DNA in solution. FEBS Lett. 23:180-184.
6. Evdokimov, Y. M., T. L. Pyatigorskaya,..., Y. M. Varshavsky. 1976. A comparative X-ray diffraction and circular dichroism study of DNA compact particles formed in water-salt solutions, containing poly (ethylene glycol). Nucleic Acids Res. 3:2353-2366.
7. Laemmli, U. K. 1975. Characterization of DNA condensates induced by poly (ethylene oxide) and polylysine. Proc. Natl. Acad. Sci. USA. 72:4288-4292.
8. Grosberg, A. Yu, and A. V. Zhestkov. 1986. On the compact form of linear duplex DNA: globular states of the uniform elastic (persistent) macromolecule. J. Biomol. Struct. Dyn. 3:859-872.
9. Ubbink, J., and T. Odijk. 1996. Deformation of toroidal DNA condensates under surface stress. Europhys. Lett. 33:353-358. (Pubitemid 126340187)
10. Hud, N. V., and K. H. Downing. 2001. Cryoelectron microscopy of phage λ condensates in vitreous ice: the fine structure of DNA toroids. Proc. Natl. Acad. Sci. USA. 98:14925-14930. (Pubitemid 34013946)
11. Zhang, C, P. G. Shao,..., R. C. van der Maarel. 2009. Macromolecular crowding induced elongation and compaction in a naochannel. Biophys. J. 97:1678-1686.
12. Hou, X.-M., W. Li,..., P. Y. Wang. 2009. Formation of DNA toroids inside confined droplets adsorbed on mica surfaces. Phys. Rev. EStat. Nonlin. Soft Matter Phys. 79:051912.
13. Lambert, O., L. Letellier,..., J.-L. Rigaud. 2000. DNA delivery by phage as a strategy for encapsulating toroidal condensates of arbitrary size into liposomes. Proc. Natl. Acad. Sci. USA. 97:7248-7253. (Pubitemid 30431449)
14. Evilevitch, A. 2006. Effect of condensing agents and nuclease on the extent of ejection from phage λ. J. Phys. Chem. B. 110:22261-22265. (Pubitemid 44806950)
15. Leforestier, A., and F. Livolant. 2009. Structure of toroidal DNA collapsed inside the phage capsid. Proc. Natl. Acad. Sci. USA. 106:9157-9162.
16. Jeembaeva, M., M. Castelnovo, F Larsson, and A. Evilevitch. 2008. Osmotic pressure: resisting of promoting DNA ejection from phage λ. J. Mol. Biol. 381:310-323.
17. Cremer, T., and C. Cremer. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2:292-301. (Pubitemid 33674777)
18. Cunha, S., T. Odijk, E. Süleymanoglu, and C. L. Woldringh. 2001. Isolation of the Escherichia coli nucleoid. Biochimie. 83:149-154. (Pubitemid 32243558)
19. Marenduzzo, D., C. Micheletti, and E. Orlandini. 2010. Biopolymer organization upon confinement. J. Phys. Condens. Matter. 22:283102.
20. Boulanger, P., M. le Maire,..., L. Letellier. 1996. Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry. 35:14216-14224. (Pubitemid 26384416)
21. Leforestier, A., and F Livolant. 2010. The bacteriophage genome undergoes a succession of intracapsid phase transitions upon DNA ejection. J. Mol. Biol. 396:384-395.
22. Leforestier, A., S. Brasilès,..., F Livolant. 2008. Bacteriophage T5 DNA ejection under pressure. J. Mol. Biol. 384:730-739.
23. Purohit, P. K., J. Kondev, and R. Phillips. 2003. Mechanics of DNA packaging in viruses. Proc. Natl. Acad. Sci. USA. 100:3173-3178. (Pubitemid 36356558)
24. Šiber, A., M. Dragar,..., R. Podgornik. 2008. Packing nanomechanics of viral genome. Eur. Phys. J. E. 26:317-325.
25. Petrov, A. S., and S. C. Harvey. 2008. Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys. J. 95:497-502.
26. Raspaud, E., D. Durand, and F Livolant. 2005. Interhelical spacing in liquid crystalline spermine and spermidine-DNA precipitates. Biophys. J. 88:392-403. (Pubitemid 40070685)
27. Strey, H. H., R. Podgornik,..., V. A. Parsegian. 1998. DNA-DNA interactions. Curr. Op. Struct. Biol. 8:309-313. (Pubitemid 28321357)
28. Kanduč, M., A. Naji,..., R. Podgornik. 2010. Dressed counterions: strong electrostatic coupling in the presence of salt. J. Chem. Phys. 132:124701-124715.
29. Lerman, L. S. 1971. A transition to a compact form of DNA in polymer solutions. Proc. Natl. Acad. Sci. USA. 68:1886-1890.
30. Maniatis, T., J. H. Venable, and L. S. Lerman. 1974. The structure of ψ DNA. J. Mol. Biol. 84:37-64.
31. Cohen, J. A., R. Podgornik,..., V. A. Parsegian. 2009. A phenomenological one-parameter equation of state for osmotic pressures of PEG and other neutral flexible polymers in good solvents. J. Phys. Chem. B. 113:3709-3714.
32. Bealle, G., J. Jestinc, and D. Carrière. 2011. Osmotically induced deformation of capsid-like icosahedral vesicles. Soft Matter. 7:1084-1089.
33. Šiber, A., and R. Podgornik. 2009. Stability of elastic icosadeltahedral shells under uniform external pressure: application to viruses under osmotic pressure. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 79:011919.
34. Evilevitch, A., J. W. Gober,..., W. M. Gelbart. 2005. Measurements of DNA lengths remaining in a viral capsid after osmotically suppressed partial ejection. Biophys. J. 88:751-756. (Pubitemid 40070716)
35. São-José, C, M. de Frutos,..., P. Tavares. 2007. Pressure built by DNA packing inside virions: enough to drive DNA ejection in vitro, largely insufficient for delivery into the bacterial cytoplasm. J. Mol. Biol. 374:346-355. (Pubitemid 350007657)
36. Ubbink, J., and T Odijk. 1996. Deformation of toroidal DNA condensates under surface stress. Europhys. Lett. 33:353-358. (Pubitemid 126340187)
37. Landau, L. D., and E. M. Lifshitz. 1980. Statistical Physics., Vol. 1. Pergamon Press, Oxford.
38. Tzlil, S., J. T Kindt,..., A. Ben-Shaul. 2003. Forces and pressures in DNA packaging and release from viral capsids. Biophys. J. 84:1616-1627. (Pubitemid 36322926)
39. Kanduč, M., A. Naji,..., R. Podgornik. 2010. Dressed counterions: strong electrostatic coupling in the presence of salt. J. Chem. Phys. 132:124701-124715.
40. Rau, D. C, and V. A. Parsegian. 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.
41. Rau, D. C, and V. A. Parsegian. 1992. Direct measurement of temperature-dependent solvation forces between DNA double helices. Biophys. J. 61:260-271.
42. Ben-Yaakov, D., D. Andelman,..., R. Podgornik. 2009. Beyond standard Poisson-Boltzmann theory: ion-specific interactions in aqueous solutions. J. Phys. Condens. Matter. 21:424106.
43. Kanduč, M., A. Naji,..., R. Podgornik. 2009. The role of multipoles in counterion-mediated interactions between charged surfaces: strong and weak coupling. J. Phys. Condens. Matter. 21:424103.
44. Fang, Y, and J. H. Hoh. 1998. Surface-directed DNA condensation in the absence of soluble multivalent cations. Nucleic Acids Res. 26:588-593. (Pubitemid 28291589)
45. Kato, A., E. Shindo,..., K. Yoshikawa. 2009. Conformational transition of giant DNA in a confined space surrounded by a phospholipid membrane. Biophys. J. 97:1678-1686.
46. Parsegian, V. A., R. P. Rand, and D. C. Rau. 1995. Macromolecules and water: probing with osmotic stress. Methods Enzymol. 259:43-94.
47. Helgstrand, C, W. R. Wikoff, R. L. Duda, R. W. Hendreix, J. E. Johnson, and L. Liljas. 2003. The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 A resolution. J. Mol. Biol. 334:885-899. (Pubitemid 37485678)
48. Effantin, G., P. Boulanger,..., J. F Conway. 2006. Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J. Mol. Biol. 361:993-1002. (Pubitemid 44189441)