Distribution of DNA-condensing protein complexes in the adenovirus core

Nucleic Acids Research

Volumn 43, Issue 8, 2015, Pages 4274-4283

  Pérez Berná, Ana J ^a,e   Marion, Sanjin ^b   Chichón, F Javier ^a   Fernández, José J ^a   Winkler, Dennis C ^c   Carrascosa, José L ^a   Steven, Alasdair C ^c   Šiber, Antonio ^b,d   San Martín, Carmen ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b INSTITUTE OF PHYSICS   (Croatia)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^d JO EF STEFAN INSTITUTE   (Slovenia)

^e ALBA SYNCHROTRON LIGHT SOURCE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOPROTEIN; DNA BINDING PROTEIN; DOUBLE STRANDED DNA; VIRUS DNA; CORE PROTEIN;

ADENOVIRIDAE; ARTICLE; CHROMOSOME CONDENSATION; CONTROLLED STUDY; DNA BINDING; DNA PROTEIN COMPLEX; DNA SUPERCOILING; ELECTRON TOMOGRAPHY; MOLECULAR CROWDING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; VIRION; VIRUS CAPSID; ULTRASTRUCTURE;

ADENOVIRIDAE; HUMAN ADENOVIRUS; MIRIDAE;

ADENOVIRIDAE; DNA, VIRAL; ELECTRON MICROSCOPE TOMOGRAPHY; MOLECULAR DYNAMICS SIMULATION; VIRAL CORE PROTEINS; VIRION;

EID: 84930225771     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv187     Document Type: Article

References (73)

1. Marenduzzo, D., Finan, K. and Cook, P.R. (2006) The depletion attraction: an underappreciated force driving cellular organization. J. Cell Biol., 175, 681-686.
2. Richter, K., Nessling, M. and Lichter, P. (2007) Experimental evidence for the influence of molecular crowding on nuclear architecture. J. Cell Sci., 120, 1673-1680.
3. Hancock, R. (2012) Structure of metaphase chromosomes: a role for effects of macromolecular crowding. PLoS One, 7, e36045.
4. Luijsterburg, M.S., White, M.F., van Driel, R. and Dame, R.T. (2008) The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes. Crit. Rev. Biochem. Mol. Biol., 43, 393-418.
5. Carrivain, P., Cournac, A., Lavelle, C., Lesne, A., Mozziconacci, J., Paillusson, F., Signon, L., Victor, J.-M. and Barbi, M. (2012) Electrostatics of DNA compaction in viruses, bacteria and eukaryotes: functional insights and evolutionary perspective. Soft Matter, 8, 9285-9301.
6. Uhlmann, F. (2014) A silent revolution in chromosome biology. Nat. Rev. Mol. Cell Biol., 15, 431.
7. Maeshima, K., Hihara, S. and Eltsov, M. (2010) Chromatin structure: does the 30-nm fibre exist in vivo? Curr. Opin. Cell Biol., 22, 291-297.
8. Garcia, H.G., Grayson, P., Han, L., Inamdar, M., Kondev, J., Nelson, P.C., Phillips, R., Widom, J. and Wiggins, P.A. (2007) Biological consequences of tightly bent DNA: the other life of a macromolecular celebrity. Biopolymers, 85, 115-130.
9. Prasad, B.V.V. and Prevelige, P.E. Jr (2003) Viral genome organization. In: Richards, FM, Eisenberg, DS and Kuriyan, J (eds). Virus Structure. Advances in Protein Chemistry. Academic Press, San Diego, CA, Vol. 64, pp. 219-258.
10. Germond, J.E., Hirt, B., Oudet, P., Gross-Bellark, M. and Chambon, P. (1975) Folding of the DNA double helix in chromatin-like structures from simian virus 40. Proc. Natl Acad. Sci. U.S.A., 72, 1843-1847.
11. Wold, W.S.M. and Horwitz, M.S. (2007) Adenoviruses. In: Knipe, D, Howley, PM, Griffin, DE, Lamb, RA and Martin, MA (eds). Fields Virology. 5th edn. Lippincott Williams & Wilkins, Philadelphia, PA, pp. 2395-2436.
12. Thomas, C.E., Ehrhardt, A. and Kay, M.A. (2003) Progress and problems with the use of viral vectors for gene therapy. Nat. Rev. Genet., 4, 346-358.
13. Liu, H., Jin, L., Koh, S.B., Atanasov, I., Schein, S., Wu, L. and Zhou, Z.H. (2010) Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science, 329, 1038-1043.
14. Giberson, A.N., Davidson, A.R. and Parks, R.J. (2012) Chromatin structure of adenovirus DNA throughout infection. Nucleic Acids Res., 40, 2369-2376.
15. Chatterjee, P.K., Vayda, M.E. and Flint, S.J. (1986) Identification of proteins and protein domains that contact DNA within adenovirus nucleoprotein cores by ultraviolet light crosslinking of oligonucleotides 32P-labelled in vivo. J. Mol. Biol., 188, 23-37.
16. Pérez-Vargas, J., Vaughan, R.C., Houser, C., Hastie, K.M., Kao, C.C. and Nemerow, G.R. (2014) Isolation and characterization of the DNA and protein binding activities of adenovirus core protein V. J. Virol., 88, 9287-9296.
17. Chatterjee, P.K., Yang, U.C. and Flint, S.J. (1986) Comparison of the interactions of the adenovirus type 2 major core protein and its precursor with DNA. Nucleic Acids Res., 14, 2721-2735.
18. Johnson, J.S., Osheim, Y.N., Xue, Y., Emanuel, M.R., Lewis, P.W., Bankovich, A., Beyer, A.L. and Engel, D.A. (2004) Adenovirus protein VII condenses DNA, represses transcription, and associates with transcriptional activator E1A. J. Virol., 78, 6459-6468.
19. Anderson, C.W., Young, M.E. and Flint, S.J. (1989) Characterization of the adenovirus 2 virion protein, mu. Virology, 172, 506-512.
20. van Oostrum, J. and Burnett, R.M. (1985) Molecular Composition of the Adenovirus Type-2 Virion. J. Virol., 56, 439-448.
21. Benevento, M., Di Palma, S., Snijder, J., Moyer, C.L., Reddy, V.S., Nemerow, G.R. and Heck, A.J. (2014) Adenovirus composition, proteolysis, and disassembly studied by in-depth qualitative and quantitative proteomics. J. Biol. Chem., 289, 11421-11430.
22. Burg, J.L., Schweitzer, J. and Daniell, E. (1983) Introduction of superhelical turns into DNA by adenoviral core proteins and chromatin assembly factors. J. Virol., 46, 749-755.
23. Everitt, E., Lutter, L. and Philipson, L. (1975) Structural proteins of adenoviruses. XII. Location and neighbor relationship among proteins of adenovirion type 2 as revealed by enzymatic iodination, immunoprecipitation and chemical cross-linking. Virology, 67, 197-208.
24. Blainey, P.C., Graziano, V., Pérez-Berná, A.J., McGrath, W.J., Flint, S.J., Martín, C., Xie, X.S. and Mangel, W.F. (2013) Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space: IV. Viral proteinase slides along DNA to locate and process its substrates. J. Biol. Chem., 288, 2092-2102.
25. Chatterjee, P.K., Vayda, M.E. and Flint, S.J. (1985) Interactions among the three adenovirus core proteins. J. Virol., 55, 379-386.
26. Brown, D.T., Westphal, M., Burlingham, B.T., Winterhoff, U. and Doerfler, W. (1975) Structure and composition of the adenovirus type 2 core. J. Virol., 16, 366-387.
27. Newcomb, W.W., Boring, J.W. and Brown, J.C. (1984) Ion etching of human adenovirus 2: structure of the core. J. Virol., 51, 52-56.
28. Wong, M.L. and Hsu, M.T. (1989) Linear adenovirus DNA is organized into supercoiled domains in virus particles. Nucleic Acids Res., 17, 3535-3550.
29. Corden, J., Engelking, H.M. and Pearson, G.D. (1976) Chromatin-like organization of the adenovirus chromosome. Proc. Natl Acad. Sci. U.S.A., 73, 401-404.
30. Mirza, M.A. and Weber, J. (1982) Structure of adenovirus chromatin. Biochim. Biophys. Acta, 696, 76-86.
31. Vayda, M.E., Rogers, A.E. and Flint, S.J. (1983) The structure of nucleoprotein cores released from adenovirions. Nucleic Acids Res., 11, 441-460.
32. Pérez-Berná, A.J., Marabini, R., Scheres, S.H.W., Menéndez-Conejero, R., Dmitriev, I.P., Curiel, D.T., Mangel, W.F., Flint, S.J. and San Martín, C. (2009) Structure and uncoating of immature adenovirus. J. Mol. Biol., 392, 547-557.
33. Devaux, C., Timmins, P.A. and Berthet-Colominas, C. (1983) Structural studies of adenovirus type 2 by neutron and X-ray scattering. J. Mol. Biol., 167, 119-132.
34. Le, L.P., Le, H.N., Nelson, A.R., Matthews, D.A., Yamamoto, M. and Curiel, D.T. (2006) Core labeling of adenovirus with EGFP. Virology, 351, 291-302.
35. Puntener, D., Engelke, M.F., Ruzsics, Z., Strunze, S., Wilhelm, C. and Greber, U.F. (2011) Stepwise loss of fluorescent core protein V from human adenovirus during entry into cells. J. Virol., 85, 481-496.
36. Ugai, H., Borovjagin, A.V., Le, L.P., Wang, M. and Curiel, D.T. (2007) Thermostability/infectivity defect caused by deletion of the core protein V gene in human adenovirus type 5 is rescued by thermo-selectable mutations in the core protein X precursor. J. Mol. Biol., 366, 1142-1160.
37. Bett, A.J., Prevec, L. and Graham, F.L. (1993) Packaging capacity and stability of human adenovirus type 5 vectors. J. Virol., 67, 5911-5921.
38. Smith, A.C., Poulin, K.L. and Parks, R.J. (2009) DNA genome size affects the stability of the adenovirus virion. J. Virol., 83, 2025-2028.
39. San Martín, C. (2012) Latest Insights on Adenovirus Structure and Assembly. Viruses, 4, 847-877.
40. 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.
41. San Martín, C., Burnett, R.M., de Haas, F., Heinkel, R., Rutten, T., Fuller, S.D., Butcher, S.J. and Bamford, D.H. (2001) Combined EM/X-ray imaging yields a quasi-atomic model of the adenovirus-related bacteriophage PRD1, and shows key capsid and membrane interactions. Structure, 9, 917-930.
42. De Frutos, M., Leforestier, A. and Livolant, F. (2014) Relationship between the genome packaging in the bacteriophage capsid and the kinetics of DNA ejection. Biophys. Rev. Lett., 9, 81-104.
43. Seki, T., Dmitriev, I., Kashentseva, E., Takayama, K., Rots, M., Suzuki, K. and Curiel, D.T. (2002) Artificial extension of the adenovirus fiber shaft inhibits infectivity in coxsackievirus and adenovirus receptor-positive cell lines. J. Virol., 76, 1100-1108.
44. Maizel, J.V. Jr, White, D.O. and Scharff, M.D. (1968) The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology, 36, 115-125.
45. Harris, A., Cardone, G., Winkler, D.C., Heymann, J.B., Brecher, M., White, J.M. and Steven, A.C. (2006) Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl Acad. Sci. U.S.A., 103, 19123-19127.
46. Mastronarde, D.N. (2005) Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol., 152, 36-51.
47. Kremer, J.R., Mastronarde, D.N. and McIntosh, J.R. (1996) Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol., 116, 71-76.
48. Agulleiro, J.I. and Fernandez, J.J. (2011) Fast tomographic reconstruction on multicore computers. Bioinformatics, 27, 582-583.
49. Frangakis, A.S. and Hegerl, R. (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol., 135, 239-250.
50. Heymann, J.B., Cardone, G., Winkler, D.C. and Steven, A.C. (2008) Computational resources for cryo-electron tomography in Bsoft. J. Struct. Biol., 161, 232-242.
51. Scheres, S.H., Núñez-Ramírez, R., Sorzano, C.O., Carazo, J.M. and Marabini, R. (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc., 3, 977-990.
52. Scheres, S.H., Melero, R., Valle, M. and Carazo, J.-M. (2009) Averaging of electron subtomograms and random conical tilt reconstructions through likelihood optimization. Structure, 17, 1563-1572.
53. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
54. Likos, C.N. (2001) Effective interactions in soft condensed matter physics. Phys. Rep., 348, 267-439.
55. Lei, M., de Graff, A.M.R., Thorpe, M.F., Wells, S.A. and Sartbaeva, A. (2009) Uncovering the intrinsic geometry from the atomic pair distribution function of nanomaterials. Phys. Rev. B, 80, 24118.
56. Plimpton, S. (1995) Fast parallel algorithms for short-range molecular dynamics. J. Comput. Phys., 117, 1-19.
57. Schneider, T. and Stoll, E. (1978) Molecular-dynamics study of a three-dimensional one-component model for distortive phase transitions. Phys. Rev. B, 17, 1302-1322.
58. Weeks, J., Chandler, D. and Andersen, H. (1971) Role of Repulsive Forces in Determining the Equilibrium Structure of Simple Liquids. J. Chem. Phys., 54, 5237-5247.
59. Locker, C.R. and Harvey, S.C. (2006) A model for viral genome packing. Multiscale Model. Simul., 5, 1264-1279.
60. Schiessel, H. (2003) The physics of chromatin. J. Phys., 15, R699.
61. Jun, S., Arnold, A. and Ha, B.-Y. (2007) Confined space and effective interactions of multiple self-avoiding chains. Phys. Rev. Lett., 98, 128303.
62. Cuervo, A., Dauden, M.I. and Carrascosa, J.L. (2013) Nucleic acid packaging in viruses. Subcell. Biochem., 68, 361-394.
63. Baker, T.S., Drak, J. and Bina, M. (1988) Reconstruction of the three-dimensional structure of simian virus 40 and visualization of the chromatin core. Proc. Natl Acad. Sci. U.S.A., 85, 422-426.
64. Saper, G., Kler, S., Asor, R., Oppenheim, A., Raviv, U. and Harries, D. (2013) Effect of capsid confinement on the chromatin organization of the SV40 minichromosome. Nucleic Acids Res., 41, 1569-1580.
65. Bauer, D.W., Huffman, J.B., Homa, F.L. and Evilevitch, A. (2013) Herpes virus genome, the pressure is on. J. Am. Chem. Soc., 135, 11216-11221.
66. Pérez-Berná, A.J., Ortega-Esteban, A., Menéndez-Conejero, R., Winkler, D.C., Menéndez, M., Steven, A.C., Flint, S.J., de Pablo, P.J. and San Martín, C. (2012) The role of capsid maturation on adenovirus priming for sequential uncoating. J. Biol. Chem., 287, 31582-31595.
67. Šiber, A., Božič, A.L. and Podgornik, R. (2012) Energies and pressures in viruses: contribution of nonspecific electrostatic interactions. Phys. Chem. Chem. Phys., 14, 3746-3765.
68. Minton, A.P. (1997) Influence of excluded volume upon macromolecular structure and associations in 'crowded' media. Curr. Opin. Biotechnol., 8, 65-69.
69. Nakano, S., Miyoshi, D. and Sugimoto, N. (2014) Effects of molecular crowding on the structures, interactions, and functions of nucleic acids. Chem. Rev., 114, 2733-2758.
70. Zimmerman, S.B. (1993) Macromolecular crowding effects on macromolecular interactions: some implications for genome structure and function. Biochim. Biophys. Acta, 1216, 175-185.
71. Thomas, V., Bertelli, C., Collyn, F., Casson, N., Telenti, A., Goesmann, A., Croxatto, A. and Greub, G. (2011) Lausannevirus, a giant amoebal virus encoding histone doublets. Environ. Microbiol., 13, 1454-1466.
72. Krupovic, M. and Bamford, D.H. (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nat. Rev. Microbiol., 6, 941-948.
73. Gornik, S.G., Ford, K.L., Mulhern, T.D., Bacic, A., McFadden, G.I. and Waller, R.F. (2012) Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Curr. Biol., 22, 2303-2312.