DNA Packaging in Bacteriophage T4

  • Venigalla B. Rao
  • Lindsay W. Black
Part of the Molecular Biology Intelligence Unit book series (MBIU)


Portal Protein Packaging Machine ATPase Motor Terminase Subunit Large Terminase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Earnshaw WC, Casjens SR. DNA packaging by the double-stranded DNA bacteriophages. Cell 1980; 21:319–331.PubMedCrossRefGoogle Scholar
  2. 2.
    Black LW. DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 1989; 43:267–292.PubMedCrossRefGoogle Scholar
  3. 3.
    Catalano CE, Cue D, Feiss M. Virus DNA packaging: The strategy used by phage lambda. Mol Microbiol 1995; 16:1075–1086.PubMedCrossRefGoogle Scholar
  4. 4.
    Black LW, Showe MK, Steven AC. Morphogenesis of the T4 head. In: Karam JD, ed. Molecular biology of bacteriophage T4. Washington, DC: ASM Press, 1994:218–258.Google Scholar
  5. 5.
    Mitchell M, Matsuzaki S, Imai S et al. Sequence analysis of bacteriophage T4 DNA-packaging/terminase genes 16 and 17 reveals a common ATPase center in the large subunit of viral terminases. Nucleic Acids Res 2002; 30:4009–4021.PubMedCrossRefGoogle Scholar
  6. 6.
    Smith MCM, Burns RN, Wilson SE et al. The complete genome sequence of the streptomyces temperate phage φC31: Evolutionary relationships to other viruses. Nucleic Acids Res 1999; 27(No. 10):2145–2155.PubMedCrossRefGoogle Scholar
  7. 7.
    Davison AJ. Channel catfish virus: A new type of herpesvirus. Virology 1992; 186:9–14.PubMedCrossRefGoogle Scholar
  8. 8.
    Rao VB, Black LW. Cloning, overexpression and purification of the terminase proteins gpl6 and gpl7 of bacteriophage T4: Construction of a defined in vitro packaging system using purified terminase proteins. J Mol Biol 1988; 200:475–488.PubMedCrossRefGoogle Scholar
  9. 9.
    Powell D, Franklin J, Arisaka F et al. Bacteriophage T4 DNA packaging genes 16 and 17. Nucl Acids Res 1990; 18:4005.PubMedCrossRefGoogle Scholar
  10. 10.
    Wunderli H, van den Brock J, Kellenberger E. Studies related to the head-maturation pathway of bacteriophage T4 and T2. I. Morphology and kinetics of intracellular particles produced by mutants in the maturation genes. J Supramol Struct 1977; 7:135–161.PubMedCrossRefGoogle Scholar
  11. 11.
    Lin H, Simon MN, Black LW. Purification and characterization of the small subunit of phage T4 terminase, gpl6, required for DNA packaging. J Biol Chem 1997; 272:3495–3501.PubMedCrossRefGoogle Scholar
  12. 12.
    Leffers G, Rao VB. Biochemical characterization of an ATPase activity associated with the large DNA packaging unit gpl7 from bacteriophage T4. J Biol Chem 2000; 275:37127–37136.PubMedCrossRefGoogle Scholar
  13. 13.
    Yang Q, Berton N, Manning MC et al. Domain structure of gpNuI, a phage lambda DNA pack aging protein. Biochemistry 1999; 38:14238–14247.PubMedCrossRefGoogle Scholar
  14. 14.
    Franklin J, Mosig G. Expression of the bacteriophage T4 DNA terminase genes 16 and 17 yields multiple proteins. Gene 1996; 177:179–189.PubMedCrossRefGoogle Scholar
  15. 15.
    Becker A, Gold M. Prediction of an ATP reactive center in the small subunit, gpNuI, of the phage lambda terminase enzyme. J Mol Biol 1988; 199:219–222.PubMedCrossRefGoogle Scholar
  16. 16.
    de Beer T, Fang J, Ortega M et al. Insights into specific DNA recognition during the assembly of a viral genome packaging machine. Molecular Cell 2002; 9:981–991.PubMedCrossRefGoogle Scholar
  17. 17.
    Via A, Ferre F, Brannetti B et al. Three-dimensional view of the surface motif associated with the P-loop structure: Cis and trans cases of convergent evolution. J Mol Biol 2000; 303:455–465.PubMedCrossRefGoogle Scholar
  18. 18.
    Guo P, Peterson C, Anderson D. The DNA packaging protein gpl6 of bacteriophage φ29 is a prohead-and DNA-gp3-dependent ATPase. J Mol Biol 1987; 197:229–236.PubMedCrossRefGoogle Scholar
  19. 19.
    Rao VB, Mitchell MS. The N-terminal ATPase site in the large terminase protein gpl7 is critically required for DNA packaging in bacteriophage T4. J Mol Biol 2001; 314:401–411.PubMedCrossRefGoogle Scholar
  20. 20.
    Franklin J, Haseltine D, Davenport L et al. The largest (70 kDa) product of the bacteriophage T4 DNA terminase gene 17 binds to single stranded DNA segments and digests them towards junctions with double-stranded DNA. J Mol Biol 1998; 277:541–557.PubMedCrossRefGoogle Scholar
  21. 21.
    Kuebler D, Rao VB. Functional analysis of the DNA-packaging/terminase protein gpl7 from bacteriophage T4. J Mol Biol 1998; 281:803–814.PubMedCrossRefGoogle Scholar
  22. 22.
    Rentas F. Molecular genetic and biochemical analysis of a putative terminase cutting site in the large DNA packaging protein gpl7 from bacteriophage T4. PhD thesis. Washington, DC: The Catholic University of America, 2001.Google Scholar
  23. 23.
    Gerit JA. Mechanistic principles of enzyme catalyzed cleavage of phosphodiester bonds in nucleases. 2nd ed. NY: Cold Spring Harbor Press, 1993:1–34.Google Scholar
  24. 24.
    Lin H, Rao VB, Black LW. Analysis of capsid portal protein and terminase functional domains: Interaction Sites Required for DNA Packaging in Bacteriophage T4. J Mol Biol 1999; 289:249–260.PubMedCrossRefGoogle Scholar
  25. 25.
    Marys N, Chang D-Y, Baumann RG et al. A bipartite bacteriophage T4 SOC and HOC randomized peptide display library: Detection and analysis of phage T4 terminase (gpl7) and late σ factor (gp55) interaction. J Mol Biol 2002; 319:289–304.CrossRefGoogle Scholar
  26. 26.
    Zhang Z, Sumbilla C, Lewis D et al. Mutational analysis of the peptide segment linking phosphorylation and Ca(2+)-binding domains in the sarcoplasmic reticulum Ca(2+)-ATPase. J Biol Chem 1995; 270:16283–16290.PubMedGoogle Scholar
  27. 27.
    Louie D, Serwer P. Blunt-ended ligation can be used to produce DNA ladders with rung spacing as large as 0.17 Mb, Nucleic Acids Res 1990; 18:3090.PubMedCrossRefGoogle Scholar
  28. 28.
    Bhattacharyya SP, Rao VB. A novel terminase activity associated with the DNA packaging protein gpl7 of bacteriophage T4. Virology 1993; 196:34–44.PubMedCrossRefGoogle Scholar
  29. 29.
    Bhattacharyya SP, Rao VB. Structural analysis of DNA cleaved in vivo by bacteriophage T4 terminase. Gene 1994; 146:67–72.PubMedCrossRefGoogle Scholar
  30. 30.
    Baumann RG. The role of portal and terminase proteins in the mechanism of DNA packaging in the dsDNA bacteriophage T4. PhD thesis. Baltimore, Md: University of Maryland Med Sch, 2002.Google Scholar
  31. 31.
    Hsiao CL, Black LW. Head morphogenesis of bacteriophage T4. III. The role of gene 20 in DNA packaging. Virology 1978; 91:26–38.PubMedCrossRefGoogle Scholar
  32. 32.
    Hsiao CL, Black LW. DNA packaging and the pathway of bacteriophage T4 head assembly. Proc Natl Acad Sci USA 1977; 74:3652–3656.PubMedCrossRefGoogle Scholar
  33. 33.
    Driedonks RA, Engel A, ten Heggeler B et al. Gene 20 product of bacteriophage T4 its purification and structure. J Mol Biol 1981; 152:641–662.PubMedCrossRefGoogle Scholar
  34. 34.
    Valpuesta JM, Carrascosa JL. Structure of viral connectors and their function in bacteriphage assembly and DNA packaging. Q Rev Biophys 1994; 27:107–155.PubMedGoogle Scholar
  35. 35.
    Hsiao CL, Black LW. Head morphogenesis of bacteriophage T4. II. The role of gene 40 in initiating prehead assembly. Virology 1978; 91:15–25.PubMedCrossRefGoogle Scholar
  36. 36.
    Michaud G, Zachary A, Rao VB et al. Membrane associated assembly of a phage T4 DNA entrance vertex structure studied with expression vectors. J Mol Biol 1989; 209:667–681.PubMedCrossRefGoogle Scholar
  37. 37.
    Yap N, Rao VB. Novel mutants in the 5′-upstream region of the portal protein gene 20 overcome a gp40-dependent prohead assembly block in bacteriophage T4. J Mol Biol 1996; 263:539–550.PubMedCrossRefGoogle Scholar
  38. 38.
    Simpson AA, Tao Y, Leiman PG et al. Structure of the bacteriophage φ29 DNA packaging motor. Nature 2000; 408:745–750.PubMedCrossRefGoogle Scholar
  39. 39.
    Wu DG, Black LW. Gene amplification mechanism for the hyperproduction of T4 bacteriophage 17 and 18 proteins. J Mol Biol 1987; 195:769–783.PubMedCrossRefGoogle Scholar
  40. 40.
    Wu DG, Wu CH, Black LW. Reiterated gene amplifications at specific short homology sequences in phage T4 produce Hpl7 mutants. J Mol Biol 1991; 218:705–721.PubMedCrossRefGoogle Scholar
  41. 41.
    Wu CHH, Lin H, Black LW. Bacteriophage T4 gene 17 amplification mutants: Evidence for initiation by the T4 terminase subunit gpl6. J Mol Biol 1995; 247:523–528.PubMedCrossRefGoogle Scholar
  42. 42.
    Lin H, Black LW. DNA requirements in vivo for phage T4 packaging. Virology 1998; 242:118–127.PubMedCrossRefGoogle Scholar
  43. 43.
    Wu CHH, Black LW. Mutational analysis of the sequence-specific recombination box for amplification of gene 17 of bacteriophage T4. J Mol Biol 1995; 247:604–617.PubMedCrossRefGoogle Scholar
  44. 44.
    Black LW. DNA packaging and cutting by phage terminases: Control in phage T4 by a synaptic mechanism. Bioessays 1995; 17:1052–1060.CrossRefGoogle Scholar
  45. 45.
    Grossi GF, Macchiato MF, Gialanella G. Circular permutation analysis of phage T4 DNA by electron microscopy. Z Naturforsch 1983; 38:294–296.Google Scholar
  46. 46.
    Carrascosa JL. Head maturation pathway of bacteriophage T4 and T2. IV. In vitro transformation of T4 head-related particles produced by mutants in gene 17 to capsid-like structures. J Virol 1978; 26:420–428.PubMedGoogle Scholar
  47. 47.
    Steven AC, Greenstone H, Bauer AC et al. The maturation-dependent conformational change of the major capsid protein of bacteriophage T4 involves a substantial change in secondary structure. Biochemistry 1990; 29:5556–5561.PubMedCrossRefGoogle Scholar
  48. 48.
    Rao VB, Black LW. Evidence that a phage T4 DNA packaging enzyme is a processed form of the major capsid gene product. Cell 1985; 185:565–578.Google Scholar
  49. 49.
    Xue MQ, Black LW. Role of the major capsid protein of phage T4 in DNA packaging from structure-function and site-directed mutagenesis studies. J Struct Biol 1990; 104:75–83.PubMedCrossRefGoogle Scholar
  50. 50.
    Galisteo ML, King J. Conformational transitions in the protein lattice of phage P22 capsids. Biophys J 1993; 65:227–235.PubMedGoogle Scholar
  51. 51.
    Steven AC. Conformational change-an alternative energy source? Exothermic phase transition in phage capsid maturation. Biophys J 1993; 65:5–6.PubMedGoogle Scholar
  52. 52.
    Rao VB, Black LW. DNA packaging of bacteriophage T4 proheads in vitro: Evidence that prohead expansion is not coupled to DNA packaging. J Mol Biol 1985; 185:565–578.PubMedCrossRefGoogle Scholar
  53. 53.
    Jardine PJ, McCormick MC, Lutze-Wallace C et al. The bacteriophage T4 DNA packaging apparatus targets the unexpanded prohead. J Mol Biol 1998; 284:647–659.PubMedCrossRefGoogle Scholar
  54. 54.
    Jardine PJ, Coombs DH. Capsid expansion follows the initiation of DNA packaging in bacteriophage T4. J Mol Biol 1998; 284:661–672.PubMedCrossRefGoogle Scholar
  55. 55.
    Hohn B. DNA sequences necessary for packaging of bacteriophage lambda DNA. Proc Natl Acad Sci USA 1983; 80:7456–7460.PubMedCrossRefGoogle Scholar
  56. 56.
    Shibata H, Fujisawa H, Minagawa T. Characterization of the bacteriophage T3 DNA packaging reaction in vitro in a defined system. J Mol Biol 1987; 196:845–51.PubMedCrossRefGoogle Scholar
  57. 57.
    Son, Watson RH, Serwer P. The direction and rate of bacteriophage T7 DNA packaging in vitro. Virology 1993; 196:282–289.PubMedCrossRefGoogle Scholar
  58. 58.
    Steven AC, Bauer AC, Bisher ME et al. The maturation-dependent conformational change of phage T4 capsid involves the translocation of specific epitopes between the inner and outer capsid surfaces. J Struct Biol 1991; 106:221–236.PubMedCrossRefGoogle Scholar
  59. 59.
    Mullaney J, Black LW. Activity of foreign proteins targeted within the bacteriophage T4 head and prohead: Implications for packaged DNA structure. J Mol Biol 1998; 283:913–929.PubMedCrossRefGoogle Scholar
  60. 60.
    Morita M, Tasaka M, Fujisawa H. DNA packaging ATPase of bacteriophage T3. Virology 1993;193:748–752.PubMedCrossRefGoogle Scholar
  61. 61.
    Guo P, Peterson C, Anderson D. Initiation events in in-vitro packaging of bacteriophage phi 29 DNA-gp3. J Mol Biol 1987; 197:219–228.PubMedCrossRefGoogle Scholar
  62. 62.
    Duffy C, Feiss M. The large subunit of bacteriophage lambda’s terminase plays a role in DNA translocation and packaging termination. J Mol Biol 2002; 316:547–561.PubMedCrossRefGoogle Scholar
  63. 63.
    Luftig RB, Wood WB, Okinaka R. Bacteriophage T4 head morphogenesis. On the nature of gene 49 defective heads and their role as intermediates. J Mol Biol 1971; 57:555–573.PubMedCrossRefGoogle Scholar
  64. 64.
    Kemper B, Brown DT. Function of gene 49 of bacteriophage T4. II. Analysis of intracellular development and the structure of very fast-sedimenting DNA. J Virol 1976; 18:1000–1015.PubMedGoogle Scholar
  65. 65.
    Golz S, Kemper B. Association of holliday-structure resolving endonuclease VII with gp20 from the packaging machine of phage T4. J Mol Biol 1999; 285:1131–1144.PubMedCrossRefGoogle Scholar
  66. 66.
    Zachary A, Black LW. DNA ligase is required for encapsidation of bacteriophage T4 DNA. J Mol Biol 1981; 149:641–658.PubMedCrossRefGoogle Scholar
  67. 67.
    Zachary A, Black LW. Topoisomerase II and other DNA-delay and DNA-arrest mutations impair bactreriophage T4 DNA packaging in vivo and in vitro. J Virol 1986; 60:97–104.PubMedGoogle Scholar
  68. 68.
    Pearson RK, Fox MS. Effects of DNA heterologies on bacteriophage λ packaging. Genetics 1988;118:5–12.PubMedGoogle Scholar
  69. 69.
    Coren J, Pierce J, Sternberg N. Headful packaging revisited: The packaging of more than one DNA molecule into a bacteriophage Pl head. J Mol Biol 1995; 249:176–184.PubMedCrossRefGoogle Scholar
  70. 70.
    Leffers G, Rao V. A discontinuous headful packaging model for packaging of less than headful length DNA molecules by bacteriophage T4. J Mol Biol 1996; 258:839–850.PubMedCrossRefGoogle Scholar
  71. 71.
    Hang JQ, Tack BF, Feiss M. ATPase center of bacteriophage lambda terminase involved in post-cleavage stages of DNA packaging: Identification of ATP-interacting amino acids. J Mol Biol 2000; 302:777–795.PubMedCrossRefGoogle Scholar
  72. 72.
    Morita M, Tasaka M, Fujisawa H. Analysis of functional domains of the packaging proteins of bacteriophage T3 by site-directed mutagenesis. J Mol Biol 1994; 235:248–259.PubMedCrossRefGoogle Scholar
  73. 73.
    Koonin EV, Tatusov RL, Rudd KE. Sequence similarity analysis of Escherichia coli proteins: Functional and evolutionary implications. Proc Natl Acad Sci USA 1995; 92:11921–11925.PubMedCrossRefGoogle Scholar
  74. 74.
    Baumann RG, Black LW. Isolation and characterization of T4 bacteriophage gpl7 terminase: A large subunit multimer with enhanced ATPase activity. J Biol Chem 2003; 278:4618–4627.PubMedCrossRefGoogle Scholar

Copyright information

© and Kluwer Academic/Plenum Publishers 2005

Authors and Affiliations

  • Venigalla B. Rao
    • 1
  • Lindsay W. Black
    • 2
  1. 1.Department of BiologyThe Catholic University of AmericaWashington, District of ColumbiaUSA
  2. 2.Department of Biochemistry and Molecular BiologyUniversity of Maryland School of MedicineBaltimoreUSA

Personalised recommendations