Polymorphism of DNA conformation inside the bacteriophage capsid

Journal of Biological Physics

Volumn 39, Issue 2, 2013, Pages 201-213

  Leforestier, Amélie ^a  

^a CNRS   (France)

Author keywords

Bacteriophage; Cryo electron microscopy; DNA ejection; DNA packaging

Indexed keywords

DOUBLE STRANDED DNA;

ARTICLE; BACTERIOPHAGE; CRYSTAL STRUCTURE; DNA CONFORMATION; DNA PACKAGING; DNA POLYMORPHISM; NONHUMAN; OSMOTIC PRESSURE; OSMOTIC STRESS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; TEMPERATURE; TRANSMISSION ELECTRON MICROSCOPY; VIRUS CAPSID;

BACTERIOPHAGES; CAPSID; CATIONS; DNA PACKAGING; DNA, VIRAL; NUCLEIC ACID CONFORMATION; OSMOTIC PRESSURE;

MIRIDAE;

EID: 84878731494     PISSN: 00920606     EISSN: 15730689     Source Type: Journal    
DOI: 10.1007/s10867-013-9315-y     Document Type: Article

References (70)

1. North, A.C.T.; Rich, A.: X-ray diffraction studies of bacterial viruses. Nature 191, 1242-1245 (1961)
2. Earnshaw, W.C.; Harrison, S.C.: DNA arrangement in isometric phage heads. Nature 268, 598-602 (1977)
3. Lepault, J.; Dubochet, J.; Baschong, W.; Kellenberger, E.: Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. EMBO J. 6, 1507-1512 (1987)
4. Booy, F.P.; Newcomb, W.W.; Trus, B.L.; Brown, J.C.; Baker, T.S.; Steven, A.C.: Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell 64, 1007-1015 (1991)
5. Black, L.W.; Thomas, J.A.: Condensed genome structure. In: Rosmann, M.G.; Rao, V.B. (eds.) Viral Molecular Machines, Advances in Exeprimental Medecine and Biology 726. Springer (2012)
6. Richards, K.E.; Williams, R.C.; Calendar, R.: Mode of DNA packing within bacteriophage heads. J. Mol. Biol. 78, 255-259 (1973)
7. Earnshaw, W.C.; Casjens, S.R.: DNA packaging by the double-standed DNA bacteriophages. Cell 21, 319-331 (1980)
8. Cerritelli, M.E.; Cheng, N.Q.; Rosenberg, A.H.; McPherson, C.E.; Booy, F.P.; Steven, A.C.: Ecapsidated conformation of bacteriophage T7 DNA. Cell 91, 271-280 (1997)
9. Jiang, W.; Chang, J.; Jakana, J.; Weigele, P.; King, J.; Chiu, W.: Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439, 612-216 (2006)
10. Chang, J.; Weigele, P.; King, J.; Chiu, W.; Jiang, W.: Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14, 1073-1082 (2006)
11. Leiman, P.G.; Battisti, A.J.; Bowman, V.D.; Stummeyer, K.; Mühlenhoff, Garady-Schahn, R.; Scholl D.; Molineux I.J.: The structure of bacteriophages K1E and K1-5 expleain processive degradation of polysaccharide capsules and evolution of new host specificities. J. Mol. Biol. 371, 836-849 (2007)
12. Liu, X.; Zhang, Q.; Murata, K.; Baker, M.L.; Sullivan, M.B.; Fu, C.; Dougherty, M.T.; Schmid, M.F.; Osburne, M.S.; Chisholm, S.W.; Chiu, W.: Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat. Struct. Mol. Biol. 17, 830-837 (2010)
13. Odijk, T.: Hexagonally packed DNA within bacteriopahge T7 stabilised by curvature stress. Biophys. J. 75, 1223-1227 (1998)
14. Odijk, T.; Slok, F.: Nonuniform Donnan equilibrium within bacteriophage packed with DNA. J. Phys. Chem. B 107, 8074-8077 (2003)
15. Tzlil, S.; Kindt, J.T.; Gelbart, W.M.; Ben-Shaul, A.: Forces and pressures in DNA packaging and release from viral capsids. Biophys. J. 84, 1616-1627 (2003)
16. Purohit, P.K.; Kondev, J.; Phillips, R.: Mechanics of DNA packaging in viruses. Proc. Natl. Acad. Sci. U. S. A. 100, 3173-3178 (2003)
17. Petrov, A.S.; Boz, M.B.; Harvey, S.C.: The conformation of double-stranded DNA inside bacteriophages depends on capsid size and shape. J. Struct. Biol. 160, 241-248 (2007)
18. Leforestier, A.; Livolant, F.: The bacteriophage genome undergoes a succession of intracapsid phase transitions upon DNA ejection. J. Mol. Biol. 396, 384-395 (2010)
19. Smith, D.E.; Tans, S.J.; Smith, S.B.; Grimes, S.; Anderson, D.L.; Bustamante, C.: The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 413, 748-752 (2001)
20. Gaussier, H.; Yang, Q.; Catalano, C.E.: Building a virus from scratch assembly of an infectious virus using purified components in a rigourously defined biochemical assay. J. Mol. Biol. 357, 1154-1166 (2006)
21. Kondabagil, K.R.; Zhang, Z.H.; Rao, V.B.: The DNA translocating ATPase of bacteriophage T4 packaging motor. J. Mol. Biol. 363, 786-799 (2006)
22. Roa, M.: Receptor-triggered ejection of DNA and protein in phage lambda. FEMS Microbiol. Lett. 11, 257-252 (1981)
23. Boulanger, P.; Le Maire, M.; Bonhivers, M.; Dubois, S.; Desmadril, M.; Letellier, L.: Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry 35, 14216-14224 (1996)
24. São-José, C.; de Frutos, M.; Raspaud, E.; Santos, M.A.; Tavares, P.: 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 (2007)
25. Evilevitch, A.; Lavelle, C.; Knobler, C.; Raspaud, E.; Gelbart, W.M.: Osmotic pressure inhibition of DNA from phage. Proc. Natl. Acad. Sci. U.S.A. 100, 9292-9295 (2003)
26. Knobler, C.M.; Gelbart, W.M.: Physical chemistry of DNA viruses. Ann. Rev. Phys. Chem. 60, 367-383 (2009)
27. Gelbart, W.M.; Knobler, C.M.: The physics of phages. Phys. Today 61, 42-44 (2008)
28. Smith, D.E.: Single molecule studies of viral DNA packaging. Curr. Opin. Virol. 1, 134-141 (2011)
29. Wu, D.; Van Valen, D.; Hu, Q.; Phillips, R.: Ion-dependent dynamics of DNA ejections for bacteriophage lambda. Biophys. J. 99, 1101-1119 (2010)
30. Evilevitch, A.; Fang, L.T.; Yoffe, A.M.; Castelnovo, M.; Rau, D.C.; Parsegian, V.A.; Gelbart, W.M.; Knobler, C.M.: Effects of salt concentrations and bending energy on the extent of ejection of phage genomes. Biophys. J. 94, 1110-1120 (2008)
31. Fuller, D.N.; Rickgauer, J.P.; Jardine, P.J.; Grimes, S.; Anderson, D.L.; Smith, D.E.: Ionic effects on viral DNA packaging and portal motor function in bactériophage phi29. Proc. Natl. Acad. Sci. U.S.A. 104, 11245-11250 (2007)
32. Leforestier, A.; Siber, A.; Livolant, F.; Podgornik, R.: Protein-DNA interactions determine the shapes of DNA toroids condensed in virus capsids. Biophys. J. 100, 2209-2216 (2011)
33. Mangenot, S, Hochrein, M.; Rädler, J. Letellier, L.: Real-time imaging of DNA éjection from single phage particles. Curr. Biol. 15, 430-435 (2005)
34. Chiaruttini, N.; de Frutos, M.; Augarde, E.; Boulanger, P.; Letellier, L.; Viasno, V.: Is the in vitro ejection of bacteriophage dna quasistatic? A bulk to single virus study. Biophys. J. 99, 447-455 (2010)
35. Leforestier, A.; Brasiles, S.; de Frutos M.; Raspaud E.; Letellier, L.; Tavares, P.; Livolant, F.: Bacteriophage T5 DNA ejection under pressure. J. Mol. Biol. 384, 730-739 (2008)
36. Comolli, L.R.; Spakowitz, A.J.; Siegerist, C.E.; Jardine, P.J.; Grimes, S.; Anderson, D.L.; Bustamante, C.; Downing, K.H.: Three-dimensional architecture of the bacteriophage phi29 packaged genome and elucidation of its packaging process. Virology 371, 267-277 (2008)
37. Fang, P.A.; Wright, E.T.; Weintraub, S.T.; Hakala, K.; Wu, W.; Serwer, P.; Jiang, W.: Visualization of bacteriophage T3 capsids with DNA incompletely packaged in vivo. J. Mol. Biol. 384, 1384-1399 (2008)
38. Durand, D.; Doucet, J.; Livolant, F.: A study of the structure of highly concentrated phases of DNA by X-ray diffraction. J. Phys. II. 2, 1769-1783 (1992)
39. Livolant, F.; Leforestier, A.: Condensed phases of DNA: structure and phase transitions. Prog. Polym. Sci. 21, 1115-1164 (1996)
40. Petrov, A.S.; Harvey, S.C.: Structural and thermodynamic principles of viral packaging. Structure 15, 21-27 (2007)
41. Petrov, A.S.; Harvey S.C.: Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys. J. 95, 497-502 (2008)
42. Forrey, C.; Muthukumar, M.: Langevin dynamics simulations of genome packing in bacteriophage. Biophys. J. 91, 25-41 (2006)
43. Qiu, X.; Rau, D.C.; Parsegian, V.A.; Fang, L.T.; Knobler, C.M.; Gelbart, W.M.: Salt-dependent DNA-DNA spacings in intact bacteriophage λ reflect relative importance of DNA self-repulsion and bending energies. Phys. Rev. Lett. 106, 028102 (2011)
44. Geggier, S.; Kotlyar, A.; Vologodskii, A.: Temperature dependence of DNA persistence length. Nucleic Acid. Res. 39, 1419-1426 (2011)
45. Forties, R.; Bundschuh, R.; Poirier, M.G.: The flexibility of locally melted DNA. Nucleic Acid. Res. 37, 4580-4586 (2009)
46. de Frutos, M.; Letellier, L.; Raspaud, E.: DNA ejection from bacteriophage T5: analysis of the kinetics and energetics. Biophys. J. 88, 1364-1370 (2005)
47. Gosule, L.C.; Schellman, J.A.: Compact form of DNA induced by spermidine. Nature 259, 333-335 (1976)
48. Bloomfield, V.A.: DNA condensation by multivalent cations. Biopolymers 44, 269-282 (1997)
49. 6. J. Mol. Biol. 144, 431-453 (1980)
50. Raspaud, E.; Olvera de la Cruz, M.; Sikorav, J.L.; Livolant, F.: Precipitation of DNA by polyamines: a polyelectrolyte behavior. Biophys. J. 74, 381-393 (1998)
51. Raspaud, E.; Durand, D.; Livolant, F.: Interhelical spacing in liquid crystalline spermine and spermidine-DNA precipitates. Biophys. J. 88, 392-403 (2005)
52. Leforestier, A.; Livolant, F.: Structure of toroidal DNA collapsed inside the phage capsid. Proc. Natl. Acad. Sci. 106, 9157-9162 (2009)
53. Leforestier, A.; Bertin, A.; Dubochet, J.; Richter, K. Sartori Blanc, N.; Livolant, F.: Expression of chirality in columnar hexagonal phases or DNA and nucleosomes. C.R.A.S Chimie 11, 229-244 (2008)
54. Evdokimov, Yu. M.; Platonov, A.L.; Tikhonenko, A.S.; Varshavsky, Ya. M.: A compact form of double stranded DNA in solution. FEBS Lett. 23, 180-184 (1972)
55. Lerman, L.S.: A transition to a compact form of DNA in polymer solutions. PNAS 68, 1886-1890 (1971)
56. Pelta, J.; Livolant, F.; Sikorav, J.L.: DNA aggregation induced by polyamines and cobalthexamine. J. Biol. Chem. 271, 5656-5662 (1996)
57. Lee, S.; Tran, C.V.; Nguyen, T.T.: Inhibition of DNA ejection from bacteriophage by Mg(+2) counterions. J. Chem. Phys. 134, 125104 (2011)
58. Li, Z.D.; Wu, J.Z.; Wang, Z.G.: Osmotic pressure and packaging structure of caged DNA. Biophys. J. 94, 737-746 (2007)
59. Jeembaeva, M.; Castelnovo, M.; Larsson, F.; Evilevitch, A.: Osmotic pressure: resisting of promoting DNA ejection from phage λ. J. Mol. Biol. 381, 310-323 (2008)
60. Evilevitch, A.: Effects of condensing agent and nuclease on the extent of ejection from phage lambda. J. Phys. Chem. B. 110(44), 22261-22265 (2006)
61. Hagerman, P.J.: Flexibility of DNA. Ann. Rev. Biophys. Biophys. Chem. 17, 265-286 (1988)
62. Baumann, C.G.; Smith, S.B.; Bloomfield, V.A.; Bustamante, C.: Ionic effects on the elasticity of single DNA molecules. Proc. Natl. Acad. Sci. U.S.A. 94, 6185-6190 (2000)
63. Wiggins, P.A.; van der Heijden, T.; Moreno-Herrero, F.; Spakowitz, A.; Phillips, R.; Widom, J.; Dekker, C.; Nelson, P.C.: High flexibility of DNA on short length scales probed by atomic force microscopy. Nat. Nanotechnol. 1, 137-141 (2006)
64. Yuan, C.L.; Chen, H.M.; Xion, W.L.; Archer, L.A.: DNA bending stiffness on small length scales. Phys. Rev. Lett. 100, 018102 (2008)
65. Guerrero-Ferreira, R.C.; Wright, E.R.: Cryo-electron tomography of bacterial viruses. Virology 435, 179-186 (2013)
66. Liu, J.; Chen, C.Y.; Shiomi, D.; Niki, H.; Margolin, W.: Visualization of bacteriophage P1 infection by cryo-electron tomography of tiny Escherichia coli. Virology 417, 304-311 (2011)
67. Hu, B.; Margolin, W.; Molineux, I.J.; Liu, J.: The bacteriophage t7 virion undergoes extensive structural remodeling during infection. Science 339, 576-579 (2013)
68. Gautier, A.; Salamin, L.; Tosi-Couture, E.; Mc Dowall, A.; Dubochet, J.: Electron microscopy of the chromosome of dinoflagellates in situ: confirmation of Bouligand's liquid crystal hypothesis. J. Ultrastr. Mol. Struct. Res. 97, 10-30 (1986)
69. Sartori Blanc, N.; Senn, A.; Leforestier, A.; Livolant, F.; Dubochet, J.: DNA in Human and Stallion spermatozoa forms local hexagonal packing with twist and many defects. J. Struct. Biol. 134, 76-81 (2001)
70. Virrankoski-Castrodeza, V.N.; Parish, J.H.: Evidence for supercoiling in the DNA of bacteriophages heads. Arch. Microbiol. 126, 277-283 (1980)