A critical coiled coil motif in the small terminase, gp16, from bacteriophage T4: Insights into DNA packaging initiation and assembly of packaging motor

Journal of Molecular Biology

Volumn 358, Issue 1, 2006, Pages 67-82

  Kondabagil, Kiran R ^a   Rao, Venigalla B ^a  

^a CATHOLIC UNIVERSITY OF AMERICA   (United States)

Author keywords

Coiled coil motif; DNA packaging; Phage T4; Terminase; Virus assembly

Indexed keywords

PROTEIN GP16; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE; DNA PACKAGING; GEL FILTRATION; HYDROPHOBICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PH; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

DNA VIRUSES;

EID: 33645101691     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.01.078     Document Type: Article

References (47)

1. W.C. Earnshaw, and S.R. Casjens DNA packaging by the double-stranded DNA bacteriophages Cell 21 1980 319 331
2. L.W. Black DNA packaging in dsDNA bacteriophage R. Calender The Bacteriophages 1988 Plenum Press New York 321 363
3. M. Feiss, and C.E. Catalano Bacteriophage lambda terminase and the mechanisms of viral DNA packaging C.E. Catalano Viral Genome Packaging Machines: Genetics, Structure, and Mechanism 2005 Landes Bioscience Georgetown, TX 5 39
4. D.E. Smith, S.J. Tans, S.B. Smith, S. Grimes, D.L. Anderson, and C. Bustamante The bacteriophage straight phi29 portal motor can package DNA against a large internal force Nature 413 2001 748 752
5. V.B. Rao, and L.W. Black DNA packaging in bacteriophage T4 C.E. Catalano In Viral Genome Packaging Machines: Genetics, Structure, and Mechanism 2005 Landes Bioscience Georgetown, TX 40 58
6. V.B. Rao, and L.W. Black Cloning, overexpression and purification of the terminase proteins gp16 and gp17 of bacteriophage T4. Construction of a defined in vitro DNA packaging system using purified terminase proteins J. Mol. Biol. 200 1988 475 488
7. A. Guasch, J. Pous, A. Parraga, J.M. Valpuesta, J.L. Carrascosa, and M. Coll Crystallographic analysis reveals the 12-fold symmetry of the bacteriophage phi29 connector particle J. Mol. Biol. 281 1998 219 225
8. R.W. Roger Symmetry mismatch and DNA packaging in large bacteriophages Proc. Natl Acad. Sci. USA 75 1978 4779 47783
9. A.A. Simpson, Y. Tao, P.G. Leiman, M.O. Badasso, Y. He, and P.J. Jardine Structure of the bacteriophage phi29 DNA packaging motor Nature 408 2000 745 750
10. G. Leffers, and V.B. Rao Biochemical characterization of an ATPase activity associated with the large packaging subunit gp17 from bacteriophage T4 J. Biol. Chem. 275 2000 37127 37136
11. S.P. Bhattacharyya, and V.B. Rao Structural analysis of DNA cleaved in vivo by bacteriophage T4 terminase Gene 146 1994 67 72
12. H. Lin, M.N. Simon, and L.W. Black Purification and characterization of the small subunit of phage T4 terminase, gp16, required for DNA packaging J. Biol. Chem. 272 1997 3495 3501
13. M.S. Mitchell, S. Matsuzaki, S. Imai, and V.B. Rao Sequence analysis of bacteriophage T4 DNA packaging/terminase genes 16 and 17 reveals a common ATPase center in the large subunit of viral terminases Nucl. Acids Res. 30 2002 4009 4021
14. V.B. Rao, and M.S. Mitchell The N-terminal ATPase site in the large terminase protein gp17 is critically required for DNA packaging in bacteriophage T4 J. Mol. Biol. 314 2001 401 411
15. K.R. Goetzinger, and V.B. Rao Defining the ATPase center of bacteriophage T4 DNA packaging machine: requirement for a catalytic glutamate residue in the large terminase protein gp17 J. Mol. Biol. 331 2003 139 154
16. F. Rentas, and V.B. Rao Defining the bacteriophage T4 DNA packaging machine: evidence for a C-terminal DNA cleavage domain in the large terminase/packaging protein gp17 J. Mol. Biol. 334 2003 37 52
17. S. Kanamaru, K. Kondabagil, M.G. Rossmann, and V.B. Rao The functional domains of bacteriophage t4 terminase J. Biol. Chem. 279 2004 40795 40801
18. G. Shinder, and M. Gold The Nul subunit of bacteriophage lambda terminase binds to specific sites in cos J. Virol. 62 1988 387 392
19. S. Chai, R. Lurz, and J.C. Alonso The small subunit of the terminase enzyme of Bacillus subtilis bacteriophage SPP1 forms a specialized nucleoprotein complex with the packaging initiation region J. Mol. Biol. 252 1995 386 398
20. A.G. Camacho, A. Gual, R. Lurz, P. Tavares, and J.C. Alonso Bacillus subtilis bacteriophage SPP1 DNA packaging motor requires terminase and portal proteins J. Biol. Chem. 278 2003 23251 23259
21. H. Shibata, H. Fujisawa, and T. Minagawa Characterization of the bacteriophage T3 DNA packaging reaction in vitro in a defined system J. Mol. Biol. 196 1987 845 851
22. Y. Hwang, and M. Feiss A defined system for in vitro lambda DNA packaging Virology 211 1995 367 376
23. L. Oliveira, J.C. Alonso, and P. Tavares A defined in vitro system for DNA packaging by the bacteriophage SPP1: insights into the headful packaging mechanism J. Mol. Biol. 353 2005 529 539
24. A.N. Lupas, and M. Gruber The structure of alpha-helical coiled coils Advan. Protein Chem. 70 2005 37 78
25. A. Lupas Coiled coils: new structures and new functions Trends Biochem. Sci. 21 1996 375 382
26. A. Lupas Predicting coiled-coil regions in proteins Curr. Opin. Struct. Biol. 7 1997 388 393
27. M. Delorenzi, T. Speed, and H.M.M. An model for coiled-coil domains and a comparison with PSSM-based predictions Bioinformatics 18 2002 617 625
28. V.A. Fischetti, G.M. Landau, J.P. Schmidt, and P. Sellers Identifying periodic occurrences of a template with applications to protein structure Inf. Proc. Letters 45 1993 11 18
29. V.A. Fischetti, V. Pancholi, P. Sellers, J. Schmidt, G. Landau, X. Xu, and O. Schneewind Streptococcal M protein: a common structural motif used by Gram-positive bacteria for biologically active surface molecules T.K. Korhonen T. Hovi P.H. Makela FEMS: Molecular Recognition in Host-Parasite Interactions 1992 Plenum Press New York 31 38
30. B. Berger, D.B. Wilson, E. Wolf, T. Tonchev, M. Milla, and P.S. Kim Predicting coiled coils by use of pairwise residue correlations Proc. Natl Acad. Sci. USA 92 1995 8259 8263
31. E. Wolf, P.S. Kim, and B. Berger MultiCoil: a program for predicting two- and three-stranded coiled coils Protein Sci. 6 1997 1179 1189
32. Q. Yang, T. de Beer, L. Woods, J.D. Meyer, M.C. Manning, M. Overduin, and C.E. Catalano Cloning, expression, and characterization of a DNA binding domain of gpNu1, a phage lambda DNA packaging protein Biochemistry 38 1999 465 477
33. J.H. White, and C.C. Richardson Gene 18 protein of bacteriophage T7. Overproduction, purification, and characterization J. Biol. Chem. 262 1987 8845 8850
34. R.M. Delahay, and G. Frankel Coiled-coil proteins associated with type III secretion systems: a versatile domain revisited Mol. Microbiol. 45 2002 905 916
35. P. Burkhard, J. Stetefeld, and S.V. Strelkov Coiled coils: a highly versatile protein folding motif Trends Cell Biol. 11 2001 82 88
36. Q. Yang, N. Berton, M.C. Manning, and C.E. Catalano Domain structure of gpNu1, a phage lambda DNA packaging protein Biochemistry 38 1999 14238 14247
37. D.L. Bain, N. Berton, M. Ortega, J. Baran, Q. Yang, and C.E. Catalano Biophysical characterization of the DNA binding domain of gpNu1, a viral DNA packaging protein J. Biol. Chem. 276 2001 20175 20181
38. H. Gaussier, M.E. Ortega, N.K. Maluf, and C.E. Catalano Nucleotides regulate the conformational state of the small terminase subunit from bacteriophage lambda: implications for the assembly of a viral genome-packaging motor Biochemistry 44 2005 9645 9656
39. T. de Beer, J. Fang, M. Ortega, Q. Yang, L. Maes, and C. Duffy Insights into specific DNA recognition during the assembly of a viral genome packaging machine Mol. Cell. 9 2002 981 991
40. R.G. Baumann, and L.W. Black Isolation and characterization of T4 bacteriophage gp17 terminase, a large subunit multimer with enhanced ATPase activity J. Biol. Chem. 278 2003 4618 4627
41. A. Gual, A.G. Camacho, and J.C. Alonso Functional analysis of the terminase large subunit, G2P, of Bacillus subtilis bacteriophage SPP1 J. Biol. Chem. 275 2000 35311 35319
42. Q. Yang, T. de Beer, L. Woods, J.D. Meyer, M.C. Manning, M. Overduin, and C.E. Catalano Cloning, expression, and characterization of a DNA binding domain of gpNu1, a phage lambda DNA packaging protein Biochemistry 38 1999 465 477
43. C. Duffy, and M. Feiss The large subunit of bacteriophage lambda's terminase plays a role in DNA translocation and packaging termination J. Mol Biol. 316 2002 547 561
44. J. Walshaw, and D.N. Woolfson Socket: a program for identifying and analysing coiled-coil motifs within protein structures J. Mol Biol. 307 2001 1427 1450
45. S. Golz, and B. Kemper Association of Holliday-structure resolving endonuclease VII with gp20 from the packaging machine of phage T4 J. Mol. Biol. 285 1999 1131 1144
46. F.W. Studier, A.H. Rosenberg, J.J. Dunn, and J.W. Dubendorff Use of T7 RNA polymerase to direct expression of cloned genes Methods Enzymol. 185 1990 60 89
47. R.M. Horton, H.D. Hunt, S.N. Ho, J.K. Pullen, and L.R. Pease Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension Gene 77 1989 61 68