Structural changes of bacteriophage φ29 upon DNA packaging and release

EMBO Journal

Volumn 25, Issue 21, 2006, Pages 5229-5239

  Xiang, Ye ^a   Morais, Marc C ^a   Battisti, Anthony J ^a   Grimes, Shelley ^b   Jardine, Paul J ^b   Anderson, Dwight L ^b   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

29 structure; Cryo electron microscopy; DNA ejection; DNA packaging

Indexed keywords

PROTEIN P22;

ARTICLE; BACTERIOPHAGE; CRYOELECTRON MICROSCOPY; DNA PACKAGING; DNA STRUCTURE; GENE ORDER; INFECTION; NONHUMAN; PRIORITY JOURNAL;

BACILLUS PHAGES; CRYOELECTRON MICROSCOPY; DNA PACKAGING; DNA, VIRAL; GENOME, VIRAL; MODELS, BIOLOGICAL; VIRAL PROTEINS; VIRUS ASSEMBLY;

BACILLUS PHAGE PHI29;

EID: 33750450852     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601386     Document Type: Article

References (76)

1. Ackermann HW (2003) Bacteriophage observations and evolution. Res Microbiol 154: 245-251
2. Agirrezabala X, Martin-Benito J, Castón JR, Miranda R, Valpuesta JM, Carrascosa JL (2005) Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J 24: 3820-3829
3. Anderson D, Reilly B (1993) Morphogenesis of bacteriophage φ29. In Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics, Sonenshein AL, Hoch JA, Losick R (eds), pp 859-867. Washington, DC: American Society for Microbiology
4. Anderson DL, Hickman DD, Reilly BE (1966) Structure of Bacillus subtilis bacteriophage f29 and the length of φ29 deoxyribonucleic acid. J Bacteriol 91: 2081-2089
5. Baumann RG, Mullaney J, Black LW (2006) Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol 61: 16-32
6. Benson SD, Bamford JKH, Bamford DH, Burnett RM (2004) Does common architecture reveal a viral lineage spanning all three domains of life? Mol Cell 16: 673-685
7. Bjornsti MA, Reilly BE, Anderson DL (1983) Morphogenesis of bacteriophage φ29 of Bacillus subtilis: oriented and quantized in vitro packaging of DNA-protein gp3. J Virol 45: 383-396
8. Black LW, Newcomb WW, Boring JW, Brown JC (1985) Ion etching of bacteriophage T4: support for a spiral-fold model of packaged DNA. Proc Natl Acad Sci USA 82: 7960-7964
9. Black LW, Showe MK, Steven AC (1994) Morphogenesis of the T4 head. In Molecular Biology of Bacteriophage T4, Karam JD (ed), pp 218-258. Washington, DC: American Society for Microbiology
10. Camacho A, Jiménez F, Viñuela E, Salas M (1979) Order of assembly of the lower collar and the tail proteins of Bacillus subtilis bacteriophage phi 29. J Virol 29: 540-545
11. Carazo JM, Santisteban A, Carrascosa JL (1985) Three-dimensional reconstruction of bacteriophage φ29 neck particles at 2.2nm resolution. J Mol Biol 183: 79-88
12. Carrascosa JL, Valpuesta JM (1999) Bacteriophage connectors: structural features of a DNA translocating motor. Recent Res Devel Virol 1: 449-465
13. Cerritelli ME, Cheng N, Rosenberg AH, McPherson CE, Booy FP, Steven AC (1997) Encapsidated conformation of bacteriophage T7 DNA. Cell 91: 271-280
14. Chang J, Weigele P, King J, Chiu W, Jiang W (2006) Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14: 1073-1082
15. Cuff JA, Barton GJ (2000) Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins: Struct Funct Genet 40: 502-511
16. Earnshaw WC, King J, Harrison SC, Eiserling FA (1978) The structural organization of the DNA packaged within the heads of T4 wild type, isometric and giant bacteriophages. Cell 14: 559-568
17. Fokine A, Chipman PR, Leiman PG, Mesyanzhinov VV, Rao VB, Rossmann MG (2004) Molecular architecture of the prolate head of bacteriophage T4. Proc Natl Acad Sci USA 101: 6003-6008
18. Fokine A, Leiman PG, Shneider MM, Ahvaze B, Boeshans KM, Steven AC, Black LW, Mesyanzhinov VV, Rossmann MG (2005) Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc Natl Acad Sci USA 102: 7163-7168
19. Garcia JA, Carrascosa JL, Salas M (1983) Assembly of the tail protein of the Bacillus subtilis phage φ29. Virology 125: 18-30
20. Grimes S, Anderson D (1990) RNA dependence of the bacteriophage φ29 DNA packaging ATPase. J Mol Biol 215: 559-566
21. Grimes S, Jardine PJ, Anderson DL (2002) Bacteriophage φ29 DNA packaging. Adv Virus Res 58: 255-294
22. Guo P, Grimes S, Anderson D (1986) A defined system for in vitro packaging of DNA-gp3 of the Bacillus subtilis bacteriophage φ29. Proc Natl Acad Sci USA 83: 3505-3509
23. Hagen EW, Reilly BE, Tosi ME, Anderson DL (1976) Analysis of gene function of bacteriophage φ29 of Bacillus subtilis: identification of cistrons essential for viral assembly. J Virol 19: 501-517
24. Harrison SC (1983) Packaging of DNA into bacteriophage heads: a model. J Mol Biol 171: 577-580
25. Hendrix RW (1978) Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci USA 75: 4779-4783
26. Hendrix RW (2002) Bacteriophages: evolution of the majority. Theor Popul Biol 61: 471-480
27. Holm L, Sander C (1993) Protein structure comparison by alignment of distance matrices. J Mol Biol 233: 123-138
28. Holm L, Sander C (1998) Touring protein fold space with Dali/FSSP. Nucl Acids Res 26: 316-319
29. Hud NV (1995) Double-stranded DNA organization in bacteriophage heads: an alternative toroid-based model. Biophysics J 69: 1355-1362
30. Jenkins J, Mayans O, Pickersgill R (1998) Structure and evolution of parallel β-helix proteins. J Struct Biol 122: 236-246
31. Jiang W, Chang J, Jakana J, Weigele P, King J, Chiu W (2006) Structure of epsilon 15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature (London) 439: 612-616
32. Jiang W, Li Z, Zhang Z, Baker ML, Prevelige Jr PE, Chiu W (2003) Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10: 131-135
33. Kamtekar S, Berman AJ, Wang J, Lázaro JM, de Vega M, Blanco L, Salas M, Steitz TA (2006) The φ29 DNA polymerase: protein-primer structure suggests a model for the initiation to elongation transition. EMBO J 25: 1335-1343
34. Kostyuchenko VA, Leiman PG, Chipman PR, Kanamaru S, van Raaij MJ, Arisaka F, Mesyanzhinov VV, Rossmann MG (2003) Three-dimensional structure of bacteriophage T4 baseplate. Nat Struct Biol 10: 688-693
35. Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige Jr. PE, Poliakov A, Potter CS, Carragher B, Johnson JE (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312: 1791-1795
36. Lata R, Conway JF, Cheng N, Duda RL, Hendrix RW, Wikoff WR, Johnson JE, Tsuruta H, Steven AC (2000) Maturation dynamics of a viral capsid: visualization of transitional intermediate states. Cell 100: 253-263
37. Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118: 419-429
38. Lepault J, Dubochet J, Baschong W, Kellenberger E (1987) Organization of double-stranded DNA in bacteriophages: a study by cryo-electron microscopy of vitrified samples. EMBO J 6: 1507-1512
39. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97
40. McConnell M, Reznick A, Wright A (1979) Studies on the initial interactions of bacteriophage ε15 with its host cell, Salmonella anatum. Virology 94: 10-23
41. Méndez E, Ramírez G, Salas M, Viñuela E (1971) Structural proteins of bacteriophage φ29. Virology 45: 567-576
42. Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51: 1169-1183
43. Morais MC, Choi KH, Koti JS, Chipman PR, Anderson DL, Rossmann MG (2005) Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudoatomic structure of φ29. Mol Cell 18: 149-159
44. Morais MC, Kanamaru S, Badasso MO, Koti JS, Owen BAL, McMurray CT, Anderson DL, Rossmann MG (2003) Bacteriophage φ29 scaffolding protein gp7 before and after pro-head assembly. Nat Struct Biol 10: 572-576
45. Morais MC, Tao Y, Olson NH, Grimes S, Jardine PJ, Anderson DL, Baker TS, Rossmann MG (2001) Cryoelectron-microscopy image reconstruction of symmetry mismatches in bacteriophage φ29. J Struct Biol 135: 38-46
46. Murzin AG, Brenner SE, Hubbard T, Chothia C (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247: 536-540
47. Nandhagopal N, Simpson AA, Gurnon JR, Yan X, Baker TS, Graves MV, Van Etten JL, Rossmann MG (2002) The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc Natl Acad Sci USA 99: 14758-14763
48. Nelson RA, Reilly BE, Anderson DL (1976) Morphogenesis of bacteriophage φ29 of Bacillus subtilis: preliminary isolation and characterization of intermediate particles of the assembly pathway. J Virol 19: 518-532
49. Orlova EV, Dube P, Beckmann E, Zemlin F, Lurz R, Trautner TA, Tavares P, van Heel M (1999) Structure of the 13-fold symmetric portal protein of bacteriophage SPP1. Nat Struct Biol 6: 842-846
50. Orlova EV, Gowen B, Dröge A, Stiege A, Weise F, Lurz R, van Heel M, Tavares P (2003) Structure of a viral DNA gatekeeper at 10 Å resolution by cryo-electron microscopy. EMBO J 22: 1255-1262
51. Petersen TN, Kauppinen S, Larsen S (1997) The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: a right-handed parallel β helix. Structure 5: 533-544
52. Peterson C, Simon M, Hodges J, Mertens P, Higgins L, Egelman E, Anderson D (2001) Composition and mass of the bacteriophage φ29 prohead and virion. J Struct Biol 135: 18-25
53. Rao VB, Black LW (1985) DNA packaging of bacteriophage T4 proheads in vitro evidence that prohead expansion is not coupled to DNA packaging. J Mol Biol 185: 565-578
54. Reilly BE, Nelson RA, Anderson DL (1977) Morphogenesis of bacteriophage φ29 of Bacillus subtilis: mapping and functional analysis of the head fiber gene. J Virol 24: 363-377
55. Rossmann MG, Arnold E, Erickson JW, Frankenberger EA, Griffith JP, Hecht HJ, Johnson JE, Kamer G, Luo M, Mosser AG, Rueckert RR, Sherry B, Vriend G (1985) Structure of a human common cold virus and functional relationship to other picornaviruses. Nature (London) 317: 145-153
56. Rossmann MG, Bernal R, Pletnev SV (2001) Combining electron microscopic with X-ray crystallographic structures. J Struct Biol 136: 190-200
57. Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of a nucleotide-binding protein. Nature (London) 250: 194-199
58. Saigo K, Uchida H (1974) Connection of the right-hand terminus of DNA to the proximal end of the tail in bacteriophage lambda. Virology 61: 524-536
59. Simpson AA, Leiman PG, Tao Y, He Y, Badasso MO, Jardine PJ, Anderson DL, Rossmann MG (2001) Structure determination of the head-tail connector of bacteriophage φ29. Acta Crystallogr D 57: 1260-1269
60. Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, Jardine PJ, Olson NH, Morais MC, Grimes S, Anderson DL, Baker TS, Rossmann MG (2000) Structure of the bacteriophage φ29 DNA packaging motor. Nature (London) 408: 745-750
61. Spinelli S, Desmyter A, Verrips CT, de Haard HJW, Moineau S, Cambillau C (2006) Lactococcal bacteriophage p2 receptor-binding protein structure suggests a common ancestor gene with bacterial and mammalian viruses. Nat Struct Mol Biol 13: 85-89
62. Steinbacher S, Miller S, Baxa U, Budisa N, Weintraub A, Seckler R, Huber R (1997) Phage P22 tailspike protein: crystal structure of the head-binding domain at 2.3 Å, fully refined structure of the endorhamnosidase at 1.56 Å resolution, and the molecular basis of O-antigen recognition and cleavage. J Mol Biol 267: 865-880
63. Steinbacher S, Seckler R, Miller S, Steipe B, Huber R, Reinemer P (1994) Crystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer. Science 265: 383-386
64. Stummeyer K, Dickmanns A, Mühlenhoff M, Gerardy-Schahn R, Ficner R (2004) Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage K1F. Nat Struct Mol Biol 12: 90-96
65. Tang L, Marion WR, Cingolani G, Prevelige Jr PE, Johnson JE (2005) Three-dimensional structure of the bacteriophage P22 tail machine. EMBO J 24: 2087-2095
66. Tao Y, Olson NH, Xu W, Anderson DL, Rossmann MG, Baker TS (1998) Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95: 431-437
67. Thomas JO (1974) Chemical linkage of the tail to the right-hand end of bacteriophage lambda DNA. J Mol Biol 87: 1-9
68. Tosi M, Anderson DL (1973) Antigenic properties of bacteriophage φ29 structural proteins. J Virol 12: 1548-1559
69. Turnquist S, Simon M, Egelman E, Anderson D (1992) Supercoiled DNA wraps around the bacteriophage φ29 head-tail connector. Proc Natl Acad Sci USA 89: 10479-10483
70. van Heel M (1987) Similarity measures between images. Ultramicroscopy 21: 95-100
71. Vlcek C, Paces V (1986) Nucleotide sequence of the late region of Bacillus φ29 completes the 19285-bp sequence of φ29 genome. Comparison with the homologous sequence of phage PZA. Gene 46: 215-225
72. Wikoff WR, Liljas L, Duda RL, Tsuruta H, Hendrix RW, Johnson JE (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289: 2129-2133
73. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64: 69-114
74. Yasbin RE, Maino VC, Young FE (1976) Bacteriophage resistance in Bacillus subtilis 168, W23, and interstrain transformants. J Bacteriol 125: 1120-1126
75. Young FE (1967) Requirement of glucosylated teichoic acid for adsorption of phage in Bacillus subtilis 168. Proc Natl Acad Sci USA 58: 2377-2384
76. Zhang Z, Greene B, Thuman-Commike PA, Jakana J, Prevelige Jr PE, King J, Chiu W (2000) Visualization of the maturation transition in bacteriophage P22 by electron cryomicroscopy. J Mol Biol 297: 615-626