DNA Poised for Release in Bacteriophage ø29

Structure

Volumn 16, Issue 6, 2008, Pages 935-943

  Tang, Jinghua ^a   Olson, Norman ^a   Jardine, Paul J ^b   Grimes, Shelley ^b   Anderson, Dwight L ^b,c   Baker, Timothy S ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

DNA; MICROBIO; PROTEINS

Indexed keywords

DOUBLE STRANDED DNA;

ARTICLE; BACILLUS PHAGE; BACTERIUM; DNA CONFORMATION; DNA DENATURATION; DNA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DNA INTERACTION; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID;

BACILLUS PHAGES; CAPSID PROTEINS; DNA, VIRAL; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; VIRION; VIRUS ASSEMBLY;

BACTERIA (MICROORGANISMS); MIRIDAE;

EID: 44649135211     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2008.02.024     Document Type: Article

References (56)

1. Aebi U., Bijlenga R., v d Broek J., v d Broek H., Eiserling F., Kellenberger C., Kellenberger E., Mesyanzhinov V., Muller L., Showe M., et al. The transformation of tau particles into T4 heads. II. Transformations of the surface lattice and related observations on form determination. J. Supramol. Struct. 2 (1974) 253-275
2. Agirrezabala X., Martín-Benito J., Castón J.R., Miranda R., Valpuesta J.M., and Carrascosa J.L. Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J. 24 (2005) 3820-3829
3. Allen G.S., and Frank J. Structural insights on the translation initiation complex: ghosts of a universal initiation complex. Mol. Microbiol. 63 (2007) 941-950
4. Anderson D., and Reilly B. Bacteriophage φ29 morphogenesis. In: Hoch J.A., Losick R., and Sonenshein A.L. (Eds). Bacillus subtilis and Other Gram Positive Bacteria: Physiology, Biochemistry, and Molecular Genetics (1993), ASM Publications, Washington, DC 859-867
5. Baker M.L., Jiang W., Rixon F.J., and Chiu W. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79 (2005) 14967-14970
6. Baker T.S., and Cheng R.H. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116 (1996) 120-130
7. Baker T.S., Olson N.H., and Fuller S.D. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol. Mol. Biol. Rev. 63 (1999) 862-922
8. Berk V., and Cate J.H. Insights into protein biosynthesis from structures of bacterial ribosomes. Curr. Opin. Struct. Biol. 17 (2007) 302-309
9. Bottcher B., Wynne S.A., and Crowther R.A. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386 (1997) 88-91
10. Carrascosa J.L., Carazo J.M., and Garcia N. Structural localization of the proteins of the head to tail connecting region of bacteriophage φ29. Virology 124 (1983) 133-143
11. Chang J., Weigele P., King J., Chiu W., and Jiang W. Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14 (2006) 1073-1082
12. Chemla Y.R., Aathavan K., Michaelis J., Grimes S., Jardine P.J., Anderson D.L., and Bustamante C. Mechanism of force generation of a viral DNA packaging motor. Cell 122 (2005) 683-692
13. Comolli L.R., Spakowitz A.J., Siegerist C.E., Jardine P.J., Grimes S., Anderson D.L., Bustamante C., and Downing K.H. Three-dimensional architecture of the bacteriophage φ29 packaged genome and elucidation of its packaging process. Virology 371 (2008) 267-277
14. Conway J.F., Cheng N., Zlotnick A., Wingfield P.T., Stahl S.J., and Steven A.C. Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature 386 (1997) 91-94
15. Garcia H.G., Grayson P., Han L., Inamdar M., Kondev J., Nelson P.C., Phillips R., Widom J., and Wiggins P.A. Biological consequences of tightly bent DNA: the other life of a macromolecular celebrity. Biopolymers 85 (2007) 115-130
16. Goddard T.D., Huang C.C., and Ferrin T.E. Software extensions to UCSF chimera for interactive visualization of large molecular assemblies. Structure 13 (2005) 473-482
17. Gonzalez-Huici V., Salas M., and Hermoso J.M. The push-pull mechanism of bacteriophage φ29 DNA injection. Mol. Microbiol. 52 (2004) 529-540
18. Grigorieff N. FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 157 (2007) 117-125
19. Grimes S., Jardine P.J., and Anderson D. Bacteriophage φ29 DNA packaging. Adv. Virus Res. 58 (2002) 255-294
20. Guasch A., Pous J., Ibarra B., Gomis-Ruth F.X., Valpuesta J.M., Sousa N., Carrascosa J.L., and Coll M. Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage φ29 connector particle. J. Mol. Biol. 315 (2002) 663-676
21. Hagen E.W., Reilly B.E., Tosi M.E., and Anderson D.L. Analysis of gene function of bacteriophage φ29 of Bacillus subtilis: identification of cistrons essential for viral assembly. J. Virol. 19 (1976) 501-517
22. Hendrix R.W. Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl. Acad. Sci. USA 75 (1978) 4779-4783
23. Isidro A., Santos M.A., Henriques A.O., and Tavares P. The high-resolution functional map of bacteriophage SPP1 portal protein. Mol. Microbiol. 51 (2004) 949-962
24. Jäälinoja H.T., Huiskonen J.T., and Butcher S.J. Electron cryomicroscopy comparison of the architectures of the enveloped bacteriophages Φ6 and Φ8. Structure 15 (2007) 157-167
25. Ji Y., Marinescu D.C., Zhang W., Zhang X., Yan X., and Baker T.S. A model-based parallel origin and orientation refinement algorithm for cryoTEM and its application to the study of virus structures. J. Struct. Biol. 154 (2006) 1-19
26. Jiang W., and Ludtke S.J. Electron cryomicroscopy of single particles at subnanometer resolution. Curr. Opin. Struct. Biol. 15 (2005) 571-577
27. Jiang W., Chang J., Jakana J., Weigele P., King J., and Chiu W. Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439 (2006) 612-616
28. Johnson J.E., and Chiu W. DNA packaging and delivery machines in tailed bacteriophages. Curr. Opin. Struct. Biol. 17 (2007) 237-243
29. Kamtekar S., Berman A.J., Wang J., Lazaro J.M., de Vega M., Blanco L., Salas M., and Steitz T.A. Insights into strand displacement and processivity from the crystal structure of the protein-primed DNA polymerase of bacteriophage Φ29. Mol. Cell 16 (2004) 609-618
30. Lander G.C., Tang L., Casjens S.R., Gilcrease E.B., Prevelige P., Poliakov A., Potter C.S., Carragher B., and Johnson J.E. The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312 (2006) 1791-1795
31. Lebedev A.A., Krause M.H., Isidro A.L., Vagin A.A., Orlova E.V., Turner J., Dodson E.J., Tavares P., and Antson A.A. Structural framework for DNA translocation via the viral portal protein. EMBO J. 26 (2007) 1984-1994
32. Ludtke S.J., Chen D.H., Song J.L., Chuang D.T., and Chiu W. Seeing GroEL at 6 Å resolution by single particle electron cryomicroscopy. Structure 12 (2004) 1129-1136
33. Marinescu D.C., and Ji Y. A computational framework for the 3D structure determination of viruses with unknown symmetry. J. Parallel Distrib. Comput. 63 (2003) 738-758
34. Meijer W.J., Horcajadas J.A., and Salas M. Phi29 family of phages. Microbiol. Mol. Biol. Rev. 65 (2001) 261-287
35. Mitra K., and Frank J. Ribosome dynamics: insights from atomic structure modeling into cryo-electron microscopy maps. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 299-317
36. Morais M.C., Tao Y., Olson N.H., Grimes S., Jardine P.J., Anderson D.L., Baker T.S., and Rossmann M.G. Cryoelectron-microscopy image reconstruction of symmetry mismatches in bacteriophage φ29. J. Struct. Biol. 135 (2001) 38-46
37. Morais M.C., Kanamaru S., Badasso M.O., Koti J.S., Owen B.A., McMurray C.T., Anderson D.L., and Rossmann M.G. Bacteriophage φ29 scaffolding protein gp7 before and after prohead assembly. Nat. Struct. Biol. 10 (2003) 572-576
38. Morais M.C., Choi K.H., Koti J.S., Chipman P.R., Anderson D.L., and Rossmann M.G. Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudoatomic structure of φ29. Mol. Cell 18 (2005) 149-159
39. Peterson C., Simon M., Hodges J., Mertens P., Higgins L., Egelman E., and Anderson D. Composition and mass of the bacteriophage φ29 prohead and virion. J. Struct. Biol. 135 (2001) 18-25
40. Petrov A.S., and Harvey S.C. Structural and thermodynamic principles of viral packaging. Structure 15 (2007) 21-27
41. Petrov A.S., Lim-Hing K., and Harvey S.C. Packaging of DNA by bacteriophage ε15: structure, forces, and thermodynamics. Structure 15 (2007) 807-812
42. Purohit P.K., Inamdar M.M., Grayson P.D., Squires T.M., Kondev J., and Phillips R. Forces during bacteriophage DNA packaging and ejection. Biophys. J. 88 (2005) 851-866
43. Rice P.A., Yang S., Mizuuchi K., and Nash H.A. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87 (1996) 1295-1306
44. Rickgauer J.P., Fuller D.N., Grimes S., Jardine P.J., Anderson D.L., and Smith D.E. Portal motor velocity and capsid pressure during viral DNA packaging in bacteriophage φ29. Biophys. J. 94 (2008) 159-167
45. 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., et al. Structure of the bacteriophage φ29 DNA packaging motor. Nature 408 (2000) 745-750
46. Smith D.E., Tans S.J., Smith S.B., Grimes S., Anderson D.L., and Bustamante C. The bacteriophage straight Φ29 portal motor can package DNA against a large internal force. Nature 413 (2001) 748-752
47. Subirana J.A., Lloveras J., Lombardero M., and Vinuela E. X-ray scattering of the non-isometric Bacillus subtilis phage φ29. J. Mol. Biol. 128 (1979) 101-106
48. Tang J., Taylor D.W., and Taylor K.A. The three-dimensional structure of α-actinin obtained by cryoelectron microscopy suggests a model for Ca(2+)-dependent actin binding. J. Mol. Biol. 310 (2001) 845-858
49. Tao Y., Olson N.H., Xu W., Anderson D.L., Rossmann M.G., and Baker T.S. Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95 (1998) 431-437
50. Trus B.L., Roden R.B., Greenstone H.L., Vrhel M., Schiller J.T., and Booy F.P. Novel structural features of bovine papillomavirus capsid revealed by a three-dimensional reconstruction to 9 Å resolution. Nat. Struct. Biol. 4 (1997) 413-420
51. Van Heel M., and Harauz G. Resolution criteria for three dimensional reconstruction. Optik 73 (1986) 119-122
52. Wikoff W.R., Liljas L., Duda R.L., Tsuruta H., Hendrix R.W., and Johnson J.E. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289 (2000) 2129-2133
53. Xiang Y., Morais M.C., Battisti A.J., Grimes S., Jardine P.J., Anderson D.L., and Rossmann M.G. Structural changes of bacteriophage φ29 upon DNA packaging and release. EMBO J. 25 (2006) 5229-5239
54. Yu Z., and Bajaj C. Automatic ultrastructure segmentation of reconstructed cryoEM maps of icosahedral viruses. IEEE Trans. Image Process. 14 (2005) 1324-1337
55. Zhang X., Ji Y., Zhang L., Harrison S.C., Marinescu D.C., Nibert M.L., and Baker T.S. Features of reovirus outer capsid protein μ1 revealed by electron cryomicroscopy and image reconstruction of the virion at 7.0 Å resolution. Structure 13 (2005) 1545-1557
56. Zhou Z.H., Baker M.L., Jiang W., Dougherty M., Jakana J., Dong G., Lu G., and Chiu W. Electron cryomicroscopy and bioinformatics suggest protein fold models for rice dwarf virus. Nat. Struct. Biol. 8 (2001) 868-873