Molecular genetics of bacteriophage P22 scaffolding protein's functional domains

Journal of Molecular Biology

Volumn 348, Issue 4, 2005, Pages 831-844

  Weigele, Peter R ^a,b   Sampson, Laura ^a   Winn Stapley, Danella ^a,b   Casjens, Sherwood R ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bacteriophage P22; Procapsid; Scaffolding protein; Virus assembly

Indexed keywords

BACTERIAL PROTEIN; COAT PROTEIN; DNA; SCAFFOLD PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; GENETIC COMPLEMENTATION; GENOME; MOLECULAR GENETICS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRION; VIRUS CAPSID;

EID: 17444370140     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.03.004     Document Type: Article

References (63)

1. D. Caspar, and A. Klug Physical principles in the construction of regular viruses Cold Spring Harbor Symp. Quant. Biol. 27 1962 1 27
2. W. Earnshaw, and S. Casjens DNA packaging by the double-stranded DNA bacteriophages Cell 21 1980 319 331
3. T. Dokland Scaffolding proteins and their role in virus assembly Cell. Mol. Life Sci. 56 1999 580 603
4. Z. Hong, M. Beaudet-Miller, J. Durkin, R. Zhang, and A.D. Kwong Identification of a minimal hydrophobic domain in the herpes simplex virus type 1 scaffolding protein which is required for interaction with the major capsid protein J. Virol. 70 1996 533 540
5. W.W. Newcomb, F.L. Homa, D.R. Thomsen, and J.C. Brown In vitro assembly of the herpes simplex virus procapsid: formation of small procapsids at reduced scaffolding protein concentration J. Struct. Biol. 133 2001 23 31
6. N.L. Oien, D.R. Thomsen, M.W. Wathen, W.W. Newcomb, J.C. Brown, and F.L. Homa Assembly of herpes simplex virus capsids using the human cytomegalovirus scaffold protein: critical role of the C terminus J. Virol. 71 1997 1281 1291
7. A.D. Burch, J. Ta, and B.A. Fane Cross-functional analysis of the Microviridae internal scaffolding protein J. Mol. Biol. 286 1999 95 104
8. J. King, and S. Casjens Catalytic head assembling protein in virus morphogenesis Nature 251 1974 112 119
9. S. Casjens Molecular organization of the bacteriophage P22 coat protein shell J. Mol. Biol. 131 1979 1 14
10. B.V. Prasad, P.E. Prevelige, E. Marietta, R.O. Chen, D. Thomas, J. King, and W. Chiu Three-dimensional transformation of capsids associated with genome packaging in a bacterial virus J. Mol. Biol. 231 1993 65 74
11. S. Casjens, and J. King P22 morphogenesis I: Catalytic scaffolding protein in capsid assembly J. Supramol. Struct. 2 1974 202 224
12. W. Earnshaw, S. Casjens, and S. Harrison Assembly of the head of bacteriophage P22, X-ray diffraction from heads, proheads and related structures J. Mol. Biol. 104 1976 387 410
13. K. Eppler, E. Wyckoff, J. Goates, R. Parr, and S. Casjens Nucleotide sequence of the bacteriophage P22 genes required for DNA packaging Virology 183 1991 519 538
14. C. Bazinet, J. Benbasat, J. King, J.M. Carazo, and J.L. Carrascosa Purification and organization of the gene 1 portal protein required for phage P22 DNA packaging Biochemistry 27 1988 1849 1856
15. D. Botstein, C.H. Waddell, and J. King Mechanism of head assembly and DNA encapsulation in Salmonella phage P22. I. Genes, proteins, structures and DNA maturation J. Mol. Biol. 80 1973 669 695
16. C. Bazinet, and J. King Initiation of P22 procapsid assembly in vivo J. Mol. Biol. 202 1988 77 86
17. B. Greene, and J. King Scaffolding mutants identifying domains required for P22 procapsid assembly and maturation Virology 225 1996 82 96
18. M.H. Parker, W.F. Stafford III, and P.E. Prevelige Jr Bacteriophage P22 scaffolding protein forms oligomers in solution J. Mol. Biol. 268 1997 655 665
19. M.L. Galisteo, and J. King Conformational transformations in the protein lattice of phage P22 procapsids Biophys. J. 65 1993 227 235
20. R. Tuma, M.H. Parker, P. Weigele, L. Sampson, Y. Sun, and N.R. Krishna A helical coat protein recognition domain of the bacteriophage P22 scaffolding protein J. Mol. Biol. 281 1998 81 94
21. R. Tuma, P.E. Prevelige Jr, and G.J. Thomas Jr Structural transitions in the scaffolding and coat proteins of P22 virus during assembly and disassembly Biochemistry 35 1996 4619 4627
22. M.H. Parker, M. Jablonsky, S. Casjens, L. Sampson, N.R. Krishna, and P.E. Prevelige Jr Cloning, purification, and preliminary characterization by circular dichroism and NMR of a carboxyl-terminal domain of the bacteriophage P22 scaffolding protein Protein Sci. 6 1997 1583 1586
23. Y. Sun, M.H. Parker, P. Weigele, S. Casjens, P.E. Prevelige Jr, and N.R. Krishna Structure of the coat protein-binding domain of the scaffolding protein from a double-stranded DNA virus J. Mol. Biol. 297 2000 1195 1202
24. M.H. Parker, S. Casjens, and P.E. Prevelige Jr Functional domains of bacteriophage P22 scaffolding protein J. Mol. Biol. 281 1998 69 79
25. B. Greene, and J. King In vitro unfolding/refolding of wild type phage P22 scaffolding protein reveals capsid-binding domain J. Biol. Chem. 274 1999 16135 16140
26. Weigele, P. (2003). The role of scaffolding protein in bacteriophage P22 morphogenesis. PhD dissertation, University of Utah.
27. W. Earnshaw, and J. King Structure of phage P22 coat protein aggregates formed in the absence of the scaffolding protein J. Mol. Biol. 126 1978 721 747
28. J. King, E.V. Lenk, and D. Botstein Mechanism of head assembly and DNA encapsulation in Salmonella phage P22. II. Morphogenetic pathway J. Mol. Biol. 80 1973 697 731
29. B. Hoffman, and M. Levine Bacteriophage P22 virion protein which performs an essential early function. II. Characterization of the gene 16 function J. Virol. 16 1975 1547 1559
30. B. Hoffman, and M. Levine Bacteriophage P22 virion protein which performs an essential early function. I. Analysis of 16-ts mutants J. Virol. 16 1975 1536 1546
31. S. Casjens, E. Wyckoff, M. Hayden, L. Sampson, K. Eppler, and S. Randall Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA J. Mol. Biol. 224 1992 1055 1074
32. S. Casjens, and M. Hayden Analysis in vivo of the bacteriophage P22 headful nuclease J. Mol. Biol. 199 1988 467 474
33. M.L. Pedulla, M.E. Ford, T. Karthikeyan, J.M. Houtz, R.W. Hendrix, and G.F. Hatfull Corrected sequence of the bacteriophage P22 genome J. Bacteriol. 185 2003 1475 1477
34. T. Dokland, R.A. Bernal, A. Burch, S. Pletnev, B.A. Fane, and M.G. Rossmann The role of scaffolding proteins in the assembly of the small, single-stranded DNA virus phiX174 J. Mol. Biol. 288 1999 595 608
35. D.R. Thomsen, W.W. Newcomb, J.C. Brown, and F.L. Homa Assembly of the herpes simplex virus capsid: requirement for the carboxyl-terminal twenty-five amino acids of the proteins encoded by the UL26 and UL26.5 genes J. Virol. 69 1995 3690 3703
36. J. Kennard, F.J. Rixon, I.M. McDougall, J.D. Tatman, and V.G. Preston The 25 amino acid residues at the carboxy terminus of the herpes simplex virus type 1 UL26.5 protein are required for the formation of the capsid shell around the scaffold J. Gen. Virol. 76 1995 1611 1621
37. P.A. Thuman-Commike, B. Greene, J.A. Malinski, M. Burbea, A. McGough, W. Chiu, and P.E. Prevelige Jr Mechanism of scaffolding-directed virus assembly suggested by comparison of scaffolding-containing and scaffolding-lacking P22 procapsids Biophys. J. 76 1999 3267 3277
38. P.A. Thuman-Commike, B. Greene, J. Jakana, A. McGough, P.E. Prevelige, and W. Chiu Identification of additional coat-scaffolding interactions in a bacteriophage P22 mutant defective in maturation J. Virol. 74 2000 3871 3873
39. Z. Zhang, B. Greene, P.A. Thuman-Commike, J. Jakana, P.E. Prevelige Jr, J. King, and W. Chiu Visualization of the maturation transition in bacteriophage P22 by electron cryomicroscopy J. Mol. Biol. 297 2000 615 626
40. Casjens, S. & Weigele, P. (2004). Headful DNA packaging by bacteriophage P22. In Viral Genome Packaging (Catalano, C., ed.), pp. 80-88, Landes Publishing, USA.
41. D. Thomas, and P. Prevelige Jr A pilot protein participates in the initiation of P22 procapsid assembly Virology 182 1991 673 681
42. R. van Driel, and E. Couture Assembly of the scaffolding core of bacteriophage T4 preheads J. Mol. Biol. 123 1978 713 719
43. P. Ray, and H. Murialdo The role of gene Nu3 in bacteriophage lambda head morphogenesis Virology 64 1975 247 263
44. A. Droge, M.A. Santos, A.C. Stiege, J.C. Alonso, R. Lurz, T.A. Trautner, P. Tavares, and N.A. Shape packaging activity of bacteriophage SPP1 procapsid: protein components and interactions during assembly J. Mol. Biol. 296 2000 117 132
45. P.X. Guo, S. Erickson, W. Xu, N. Olson, T.S. Baker, and D. Anderson Regulation of the phage φ29 prohead shape and size by the portal vertex Virology 183 1991 366 373
46. S. Casjens, and R. Hendrix Control mechanisms in dsDNA bacteriophage assembly R. Calendar The Bacteriophages vol. 1 1988 Plenum Press New York City 15 91
47. B.K. Tye, J.A. Huberman, and D. Botstein Non-random circular permutation of phage P22 DNA J. Mol. Biol. 85 1974 501 528
48. B.K. Tye, R.K. Chan, and D. Botstein Packaging of an oversize transducing genome by Salmonella phage P22 J. Mol. Biol. 85 1974 485 500
49. S.D. Moore, and P.E. Prevelige Jr A P22 scaffold protein mutation increases the robustness of head assembly in the presence of excess portal protein J. Virol. 76 2002 10245 10255
50. E. Raleigh, N. Murray, H. Revel, R. Blumenthal, D. Westaway, and A. Reith McrA and McrB restriction phenotypes of some E. coli strains and impolcations for gene cloning Nucl. Acids Res. 16 1988 1563 1575
51. J. Schultz, T. Silhavy, M. Berman, N. Fiil, and S. Emr A previously unidentified gene in the spc operon of Escherichia coli K12 specifies a component of the protein export machinery Genetics 121 1982 635 649
52. S. Casjens, K. Eppler, L. Sampson, R. Parr, and E. Wyckoff Fine structure genetic and physical map of the gene 3 to 10 region of the bacteriophage P22 chromosome Genetics 127 1991 637 647
53. F. Winston, D. Botstein, and J.H. Miller Characterization of amber and ochre suppressors in Salmonella typhimurium J. Bacteriol. 137 1979 433 439
54. L.R. Bullas, and J.I. Ryu Salmonella typhimurium LT2 strains which are r- m+ for all three chromosomally located systems of DNA restriction and modification J. Bacteriol. 156 1983 471 474
55. W. Studier, A. Rosenberg, J. Dunn, and J. Dubendorff Use of T7 RNA polymerase to direct expression of cloned genes Methods Enzymol. 185 1990 60 89
56. D. Hanahan Studies on transformation of Escherichia coli with plasmids J. Mol. Biol. 166 1983 557 580
57. N.C. Franklin, and J.H. Doelling Overexpression of N antitermination proteins of bacteriophages lambda, 21, and P22: loss of N protein specificity J. Bacteriol. 171 1989 2513 2522
58. S. Tabor, and C.C. Richardson A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes Proc. Natl Acad. Sci. USA. 82 1985 1074 1078
59. R.L. Duda, J. Hempel, H. Michel, J. Shabanowitz, D. Hunt, and R.W. Hendrix Structural transitions during bacteriophage HK97 head assembly J. Mol. Biol. 247 1995 618 635
60. P.Z. O'Farrell, L.M. Gold, and W.M. Huang The identification of prereplicative bacteriophage T4 proteins J. Biol. Chem. 248 1973 5499 5501
61. T. Rabilloud, G. Carpentier, and P. Tarroux Improvement and simplification of low-background silver staining of proteins by using sodium dithionite Electrophoresis 9 1988 288 291
62. S. Casjens, D. Winn-Stapley, E. Gilcrease, R. Moreno, C. Kühlewein, and J.E. Chua The chromosome of Shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging J. Mol. Biol. 339 2004 379 394
63. S. Casjens, and W.M. Huang Linear chromosomal physical and genetic map of Borrelia burgdorferi, the Lyme disease agent Mol. Microbiol. 8 1993 967 980