The dsDNA Packaging Motor in Bacteriophage ø29

  • Marc C. Morais
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 726)


The tailed dsDNA bacteriophage ø29 packages its 19.3-kb genome into a preassembled prolate icosahedral procapsid structure using a phage-encoded macromolecular motor. This process is remarkable considering that compaction of DNA to near crystalline densities within the confined space of the capsid requires that the motor work against considerable entropic, enthalpic, and DNA bending energies. The heart of the bacteriophage ø29 packaging motor consists of three macromolecular components: the connector protein, an RNA molecule known as the pRNA, and an ATPase. The pRNA is thus far unique to ø29, but the connector and ATPase are homologous to portal and terminase proteins, respectively, in other tailed dsDNA bacteriophages. Despite decades of effort and a wealth of genetic, biochemical, biophysical, structural, and single particle data, the mechanism of DNA packaging in bacteriophage ø29 remains elusive. In this chapter, we describe the development of a highly efficient in vitro DNA packaging system for ø29, review the data available for each individual macromolecular component in the packaging motor, and present and evaluate various packaging mechanisms that have been proposed to explain the available data.


Power Stroke Packaging Activity dsDNA Virus Genome Packaging Pair Step 
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.



I am indebted to Dr. Michael Rossmann, who first introduced me to ø29, mentored much of my own research on the DNA packaging motor, and always graciously shared his considerable wisdom. I would also like to thank my collaborators: Drs. Dwight Anderson, Paul Jardine, Dr. Jaya Koti and Shelley Grimes for many thoughtful discussions regarding the mechanism of genome packaging in ø29, as well as for their invaluable contributions to the field of DNA packaging by dsDNA bacteriophages.


  1. Aathavan K, Politzer AT, Kaplan A, Moffitt JR, Chemla YR, Grimes S, Jardine PJ, Anderson DL, Bustamante C (2009) Substrate interactions and promiscuity in a viral DNA packaging motor. Nature 461(7264):669–673PubMedCrossRefGoogle Scholar
  2. Abrahams JP, Leslie AG, Lutter R, Walker JE (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370(6491):621–628PubMedCrossRefGoogle Scholar
  3. Agirrezabala X, Velazquez-Muriel JA, Gomez-Puertas P, Scheres SH, Carazo JM, Carrascosa JL (2007) Quasi-atomic model of bacteriophage t7 procapsid shell: insights into the structure and evolution of a basic fold. Structure 15(4):461–472PubMedCrossRefGoogle Scholar
  4. Anderson DL, Reilly BE (1993) Morphogenesis of bacteriophage phi29. In: Hoch JA, Losick R, Sonenshein AL (eds) Bacillus subtilis and other gram positive bacteria: physiology, biochemistry and molecular genetics. ASM Press, Washington, DC, pp 859–867Google Scholar
  5. Atz R, Ma S, Gao J, Anderson DL, Grimes S (2007) Alanine scanning and Fe-BABE probing of the bacteriophage ø29 prohead RNA-connector interaction. J Mol Biol 369(1):239–248PubMedCrossRefGoogle Scholar
  6. Bailey S, Wichitwechkarn J, Johnson D, Reilly BE, Anderson DL, Bodley JW (1990) Phylogenetic analysis and secondary structure of the Bacillus subtilis bacteriophage RNA required for DNA packaging. J Biol Chem 265(36):22365–22370PubMedGoogle Scholar
  7. Baker TS, Olson NH, Fuller SD (1999) Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol Mol Biol Rev 63(4):862–922, table of contentsPubMedGoogle Scholar
  8. Baumann RG, Mullaney J, Black LW (2006) Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol 61(1):16–32PubMedCrossRefGoogle Scholar
  9. Bjornsti MA, Reilly BE, Anderson DL (1983) Morphogenesis of bacteriophage phi 29 of Bacillus subtilis: oriented and quantized in vitro packaging of DNA protein gp3. J Virol 45(1):383–396PubMedGoogle Scholar
  10. Bjornsti MA, Reilly BE, Anderson DL (1984) Bacteriophage phi 29 proteins required for in vitro DNA-gp3 packaging. J Virol 50(3):766–772PubMedGoogle Scholar
  11. Blanco L, Salas M (1996) Relating structure to function in phi29 DNA polymerase. J Biol Chem 271(15):8509–8512PubMedCrossRefGoogle Scholar
  12. Braig K, Menz RI, Montgomery MG, Leslie AG, Walker JE (2000) Structure of bovine mitochondrial F(1)-ATPase inhibited by Mg(2+) ADP and aluminium fluoride. Structure 8(6):567–573PubMedCrossRefGoogle Scholar
  13. Burroughs AM, Iyer LM, Aravind L (2007) Comparative genomics and evolutionary trajectories of viral ATP dependent DNA-packaging systems. Genome Dyn 3:48–65PubMedCrossRefGoogle Scholar
  14. Camacho A, Jimenez F, De La Torre J, Carrascosa JL, Mellado RP, Vasquez C, Vinuela E, Salas M (1977) Assembly of Bacillus subtilis phage phi29. 1. Mutants in the cistrons coding for the structural proteins. Eur J Biochem 73(1):39–55PubMedCrossRefGoogle Scholar
  15. Chemla YR, Aathavan K, Michaelis J, Grimes S, Jardine PJ, Anderson DL, Bustamante C (2005) Mechanism of force generation of a viral DNA packaging motor. Cell 122(5):683–692PubMedCrossRefGoogle Scholar
  16. Chen C, Zhang C, Guo P (1999) Sequence requirement for hand-in-hand interaction in formation of RNA dimers and hexamers to gear phi29 DNA translocation motor. RNA 5(6):805–818PubMedCrossRefGoogle Scholar
  17. Chen C, Sheng S, Shao Z, Guo P (2000) A dimer as a building block in assembling RNA. A hexamer that gears bacterial virus phi29 DNA-translocating machinery. J Biol Chem 275(23):17510–17516PubMedCrossRefGoogle Scholar
  18. Chen DH, Baker ML, Hryc CF, DiMaio F, Jakana J, Wu W, Dougherty M, Haase-Pettingell C, Schmid MF, Jiang W, Baker D, King JA, Chiu W (2011) Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc Natl Acad Sci USA 108(4):1355–1360PubMedCrossRefGoogle Scholar
  19. Cohen DN, Sham YY, Haugstad GD, Xiang Y, Rossmann MG, Anderson DL, Popham DL (2009) Shared catalysis in virus entry and bacterial cell wall depolymerization. J Mol Biol 387(3):607–618PubMedCrossRefGoogle Scholar
  20. Dai W, Hodes A, Hui WH, Gingery M, Miller JF, Zhou ZH (2010) Three-dimensional structure of tropism-switching Bordetella bacteriophage. Proc Natl Acad Sci USA 107(9):4347–4352PubMedCrossRefGoogle Scholar
  21. Ding F, Lu C, Zhao W, Rajashankar KR, Anderson DL, Jardine PJ, Grimes S, Ke A (2011) Structure and assembly of the essential RNA ring component of a viral DNA packaging motor. Proc Natl Acad Sci USA 108:7357–7362PubMedCrossRefGoogle Scholar
  22. Draper B, Rao VB (2007) An ATP hydrolysis sensor in the DNA packaging motor from bacteriophage T4 suggests an inchworm-type translocation mechanism. J Mol Biol 369(1):79–94PubMedCrossRefGoogle Scholar
  23. Earnshaw WC, Casjens SR (1980) DNA packaging by the double-stranded DNA bacteriophages. Cell 21(2):319–331PubMedCrossRefGoogle Scholar
  24. Fokine A, Leiman PG, Shneider MM, Ahvazi 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(20):7163–7168PubMedCrossRefGoogle Scholar
  25. Frank J, Wagenknecht T, McEwen BF, Marko M, Hsieh CE, Mannella CA (2002) Three-dimensional imaging of biological complexity. J Struct Biol 138(1–2):85–91PubMedCrossRefGoogle Scholar
  26. Fu CY, Prevelige PE Jr (2009) In vitro incorporation of the phage Phi29 connector complex. Virology 394(1):149–153PubMedCrossRefGoogle Scholar
  27. Fuller DN, Rickgauer JP, Jardine PJ, Grimes S, Anderson DL, Smith DE (2007) Ionic effects on viral DNA packaging and portal motor function in bacteriophage phi 29. Proc Natl Acad Sci USA 104(27):11245–11250PubMedCrossRefGoogle Scholar
  28. Garver K, Guo P (1997) Boundary of pRNA functional domains and minimum pRNA sequence requirement for specific connector binding and DNA packaging of phage phi29. RNA 3(9):1068–1079PubMedGoogle Scholar
  29. Geourjon C, Orelle C, Steinfels E, Blanchet C, Deleage G, Di Pietro A, Jault JM (2001) A common mechanism for ATP hydrolysis in ABC transporter and helicase superfamilies. Trends Biochem Sci 26(9):539–544PubMedCrossRefGoogle Scholar
  30. Grimes S, Anderson D (1989) In vitro packaging of bacteriophage phi 29 DNA restriction fragments and the role of the terminal protein gp3. J Mol Biol 209(1):91–100PubMedCrossRefGoogle Scholar
  31. Grimes S, Anderson D (1990) RNA dependence of the bacteriophage phi 29 DNA packaging ATPase. J Mol Biol 215(4):559–566PubMedCrossRefGoogle Scholar
  32. Grimes S, Jardine PJ, Anderson D (2002) Bacteriophage phi 29 DNA packaging. Adv Virus Res 58:255–294PubMedCrossRefGoogle Scholar
  33. Guasch A, Pous J, Ibarra B, Gomis-Ruth FX, Valpuesta JM, Sousa N, Carrascosa JL, Coll M (2002) Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle. J Mol Biol 315(4):663–676PubMedCrossRefGoogle Scholar
  34. Guo P, Grimes S, Anderson D (1986) A defined system for in vitro packaging of DNA-gp3 of the Bacillus subtilis bacteriophage phi 29. Proc Natl Acad Sci USA 83(10):3505–3509PubMedCrossRefGoogle Scholar
  35. Guo P, Peterson C, Anderson D (1987a) Initiation events in in-vitro packaging of bacteriophage phi 29 DNA-gp3. J Mol Biol 197(2):219–228PubMedCrossRefGoogle Scholar
  36. Guo P, Peterson C, Anderson D (1987b) Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi 29. J Mol Biol 197(2):229–236PubMedCrossRefGoogle Scholar
  37. Guo PX, Erickson S, Xu W, Olson N, Baker TS, Anderson D (1991a) Regulation of the phage phi 29 prohead shape and size by the portal vertex. Virology 183(1):366–373PubMedCrossRefGoogle Scholar
  38. Guo PX, Rajagopal BS, Anderson D, Erickson S, Lee CS (1991b) sRNA of phage phi 29 of Bacillus subtilis mediates DNA packaging of phi 29 proheads assembled in Escherichia coli. Virology 185(1):395–400PubMedCrossRefGoogle Scholar
  39. Guo P, Zhang C, Chen C, Garver K, Trottier M (1998) Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol Cell 2(1):149–155PubMedCrossRefGoogle Scholar
  40. Hagen EW, Reilly BE, Tosi ME, Anderson DL (1976) Analysis of gene function of bacteriophage phi 29 of Bacillus subtilis: identification of cistrons essential for viral assembly. J Virol 19(2):501–517PubMedGoogle Scholar
  41. Harding NE, Ito J, David GS (1978) Identification of the protein firmly bound to the ends of bacteriophage phi 29 DNA. Virology 84(2):279–292PubMedCrossRefGoogle Scholar
  42. Harris S, Schroeder SJ (2010) Nuclear magnetic resonance structure of the prohead RNA E-loop hairpin. Biochemistry 49(29):5989–5997PubMedCrossRefGoogle Scholar
  43. Hendrix RW (1978) Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci USA 75(10):4779–4783PubMedCrossRefGoogle Scholar
  44. Hendrix RW (2002) Bacteriophages: evolution of the majority. Theor Popul Biol 61(4):471–480PubMedCrossRefGoogle Scholar
  45. Hugel T, Michaelis J, Hetherington CL, Jardine PJ, Grimes S, Walter JM, Falk W, Anderson DL, Bustamante C (2007) Experimental test of connector rotation during DNA packaging into bacteriophage phi29 capsids. PLoS Biol 5(3):e59PubMedCrossRefGoogle Scholar
  46. Hung LW, Wang IX, Nikaido K, Liu PQ, Ames GF, Kim SH (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396(6712):703–707PubMedCrossRefGoogle Scholar
  47. Iyer LM, Leipe DD, Koonin EV, Aravind L (2004a) Evolutionary history and higher order classification of AAA  +  ATPases. J Struct Biol 146(1–2):11–31PubMedCrossRefGoogle Scholar
  48. Iyer LM, Makarova KS, Koonin EV, Aravind L (2004b) Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 32(17):5260–5279PubMedCrossRefGoogle Scholar
  49. Jiang W, Li Z, Zhang Z, Baker ML, Prevelige PE Jr, Chiu W (2003) Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10(2):131–135PubMedCrossRefGoogle Scholar
  50. Jiang W, Baker ML, Jakana J, Weigele PR, King J, Chiu W (2008) Backbone structure of the infectious epsilon 15 virus capsid revealed by electron cryomicroscopy. Nature 451(7182):1130–1134PubMedCrossRefGoogle Scholar
  51. Kabaleeswaran V, Puri N, Walker JE, Leslie AG, Mueller DM (2006) Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase. EMBO J 25(22):5433–5442PubMedCrossRefGoogle Scholar
  52. Kainov DE, Mancini EJ, Telenius J, Lisal J, Grimes JM, Bamford DH, Stuart DI, Tuma R (2008) Structural basis of mechanochemical coupling in a hexameric molecular motor. J Biol Chem 283(6):3607–3617PubMedCrossRefGoogle Scholar
  53. Kamtekar S, Berman AJ, Wang J, Lazaro JM, de Vega M, Blanco L, Salas M, Steitz TA (2006) The phi29 DNA polymerase: protein-primer structure suggests a model for the initiation to elongation transition. EMBO J 25(6):1335–1343PubMedCrossRefGoogle Scholar
  54. Kellenberger E, Sechaud J, Ryter A (1959) Electron microscopical studies of phage multiplication. IV. The establishment of the DNA pool of vegetative phage and the maturation of phage particles. Virology 8:478–498PubMedCrossRefGoogle Scholar
  55. Koti JS, Morais MC, Rajagopal R, Owen BA, McMurray CT, Anderson DL (2008) DNA packaging motor assembly intermediate of bacteriophage phi29. J Mol Biol 381(5):1114–1132PubMedCrossRefGoogle Scholar
  56. Lander GC, Khayat R, Li R, Prevelige PE, Potter CS, Carragher B, Johnson JE (2009) The P22 tail machine at subnanometer resolution reveals the architecture of an infection conduit. Structure 17(6):789–799PubMedCrossRefGoogle Scholar
  57. Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26(7):1984–1994PubMedCrossRefGoogle Scholar
  58. Lee TJ, Guo P (2006) Interaction of gp16 with pRNA and DNA for genome packaging by the motor of bacterial virus phi29. J Mol Biol 356(3):589–599PubMedCrossRefGoogle Scholar
  59. Lee JY, Yang W (2006) UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127(7):1349–1360PubMedCrossRefGoogle Scholar
  60. Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317(1):41–72PubMedCrossRefGoogle Scholar
  61. Leschziner AE, Nogales E (2007) Visualizing flexibility at molecular resolution: analysis of heterogeneity in single-particle electron microscopy reconstructions. Annu Rev Biophys Biomol Struct 36:43–62PubMedCrossRefGoogle Scholar
  62. Lisal J, Tuma R (2005) Cooperative mechanism of RNA packaging motor. J Biol Chem 280(24):23157–23164PubMedCrossRefGoogle Scholar
  63. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128(1):82–97PubMedCrossRefGoogle Scholar
  64. Mancini EJ, Kainov DE, Grimes JM, Tuma R, Bamford DH, Stuart DI (2004) Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 118(6):743–755PubMedCrossRefGoogle Scholar
  65. Mitchell MS, Matsuzaki S, Imai S, Rao VB (2002) 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 30(18):4009–4021PubMedCrossRefGoogle Scholar
  66. Moffitt JR, Chemla YR, Aathavan K, Grimes S, Jardine PJ, Anderson DL, Bustamante C (2009) Intersubunit coordination in a homomeric ring ATPase. Nature 457(7228):446–450PubMedCrossRefGoogle Scholar
  67. Morais MC, Baker AS, Dunaway-Mariano D, Allen KN (2000) Crystallization and preliminary crystallographic analysis of phosphonoacetaldehyde hydrolase. Acta Crystallogr D Biol Crystallogr 56(Pt 2):206–209PubMedCrossRefGoogle Scholar
  68. 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 phi29. J Struct Biol 135(1):38–46PubMedCrossRefGoogle Scholar
  69. Morais MC, Kanamaru S, Badasso MO, Koti JS, Owen BA, McMurray CT, Anderson DL, Rossmann MG (2003) Bacteriophage phi29 scaffolding protein gp7 before and after prohead assembly. Nat Struct Biol 10(7):572–576PubMedCrossRefGoogle Scholar
  70. 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 phi29. Mol Cell 18(2):149–159PubMedCrossRefGoogle Scholar
  71. Morais MC, Koti JS, Bowman VD, Reyes-Aldrete E, Anderson DL, Rossmann MG (2008) Defining molecular and domain boundaries in the bacteriophage phi29 DNA packaging motor. Structure 16(8):1267–1274PubMedCrossRefGoogle Scholar
  72. Mosharrafa ET, Schachtele CF, Reilly BE, Anderson DL (1970) Complementary Strands of Bacteriophage phi29 Deoxyribonucleic Acid: Preparative Separation and Transcription Studies. J Virol 6(6):855–864PubMedGoogle Scholar
  73. Muller DJ, Engel A, Carrascosa JL, Velez M (1997) The bacteriophage phi29 head-tail connector imaged at high resolution with the atomic force microscope in buffer solution. EMBO J 16(10):2547–2553PubMedCrossRefGoogle Scholar
  74. Nadanaciva S, Weber J, Wilke-Mounts S, Senior AE (1999) Importance of F1-ATPase residue alpha-Arg-376 for catalytic transition state stabilization. Biochemistry 38(47):15493–15499PubMedCrossRefGoogle Scholar
  75. Ogura T, Whiteheart SW, Wilkinson AJ (2004) Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA  +  ATPases. J Struct Biol 146(1–2):106–112PubMedCrossRefGoogle Scholar
  76. Orlova EV, Gowen B, Droge A, Stiege A, Weise F, Lurz R, van Heel M, Tavares P (2003) Structure of a viral DNA gatekeeper at 10 A resolution by cryo-electron microscopy. EMBO J 22(6):1255–1262PubMedCrossRefGoogle Scholar
  77. Petrov AS, Harvey SC (2008) Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys J 95(2):497–502PubMedCrossRefGoogle Scholar
  78. Reid RJ, Bodley JW, Anderson D (1994a) Characterization of the prohead-pRNA interaction of bacteriophage phi 29. J Biol Chem 269(7):5157–5162PubMedGoogle Scholar
  79. Reid RJ, Bodley JW, Anderson D (1994b) Identification of bacteriophage phi 29 prohead RNA domains necessary for in vitro DNA-gp3 packaging. J Biol Chem 269(12):9084–9089PubMedGoogle Scholar
  80. Reid RJ, Zhang F, Benson S, Anderson D (1994c) Probing the structure of bacteriophage phi 29 prohead RNA with specific mutations. J Biol Chem 269(28):18656–18661PubMedGoogle Scholar
  81. Rickgauer JP, Fuller DN, Grimes S, Jardine PJ, Anderson DL, Smith DE (2008) Portal motor velocity and internal force resisting viral DNA packaging in bacteriophage phi29. Biophys J 94(1):159–167PubMedCrossRefGoogle Scholar
  82. Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of nucleotide-binding protein. Nature 250(463):194–199PubMedCrossRefGoogle Scholar
  83. Rossmann MG, Morais MC, Leiman PG, Zhang W (2005) Combining X-ray crystallography and electron microscopy. Structure 13(3):355–362PubMedCrossRefGoogle Scholar
  84. Salas M, Mellado RP, Vinuela E (1978) Characterization of a protein covalently linked to the 5′ termini of the DNA of Bacillus subtilis phage phi29. J Mol Biol 119(2):269–291PubMedCrossRefGoogle Scholar
  85. Schachtele CF, De Sain CV, Anderson DL (1973) Transcription during the development of bacteriophage phi29: definition of “early” and “late” phi29 ribonucleic acid. J Virol 11(1):9–16PubMedGoogle Scholar
  86. Shu D, Zhang H, Jin J, Guo P (2007) Counting of six pRNAs of phi29 DNA-packaging motor with customized single-molecule dual-view system. EMBO J 26(2):527–537PubMedCrossRefGoogle Scholar
  87. 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 phi29 DNA packaging motor. Nature 408(6813):745–750PubMedCrossRefGoogle Scholar
  88. 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 phi29. Acta Crystallogr D Biol Crystallogr 57(Pt 9):1260–1269PubMedCrossRefGoogle Scholar
  89. Singleton MR, Sawaya MR, Ellenberger T, Wigley DB (2000) Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101(6):589–600PubMedCrossRefGoogle Scholar
  90. Singleton MR, Dillingham MS, Wigley DB (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem 76:23–50PubMedCrossRefGoogle Scholar
  91. Skordalakes E, Berger JM (2003) Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell 114(1):135–146PubMedCrossRefGoogle Scholar
  92. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C (2001) The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 413(6857):748–752PubMedCrossRefGoogle Scholar
  93. Story RM, Steitz TA (1992) Structure of the recA protein-ADP complex. Nature 355(6358):374–376PubMedCrossRefGoogle Scholar
  94. Story RM, Weber IT, Steitz TA (1992) The structure of the E. coli recA protein monomer and polymer. Nature 355(6358):318–325PubMedCrossRefGoogle Scholar
  95. Subramanya HS, Bird LE, Brannigan JA, Wigley DB (1996) Crystal structure of a DExx box DNA helicase. Nature 384(6607):379–383PubMedCrossRefGoogle Scholar
  96. Sun S, Kondabagil K, Gentz PM, Rossmann MG, Rao VB (2007) The structure of the ATPase that powers DNA packaging into bacteriophage T4 procapsids. Mol Cell 25(6):943–949PubMedCrossRefGoogle Scholar
  97. Sun S, Kondabagil K, Draper B, Alam TI, Bowman VD, Zhang Z, Hegde S, Fokine A, Rossmann MG, Rao VB (2008) The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 135(7):1251–1262PubMedCrossRefGoogle Scholar
  98. Tang J, Olson N, Jardine PJ, Grimes S, Anderson DL, Baker TS (2008) DNA poised for release in bacteriophage phi29. Structure 16(6):935–943PubMedCrossRefGoogle Scholar
  99. 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(3):431–437PubMedCrossRefGoogle Scholar
  100. Thomsen ND, Berger JM (2008) Structural frameworks for considering microbial protein- and nucleic acid-dependent motor ATPases. Mol Microbiol 69(5):1071–1090PubMedCrossRefGoogle Scholar
  101. Trottier M, Guo P (1997) Approaches to determine stoichiometry of viral assembly components. J Virol 71(1):487–494PubMedGoogle Scholar
  102. Tsuprun V, Anderson D, Egelman EH (1994) The bacteriophage phi 29 head-tail connector shows 13-fold symmetry in both hexagonally packed arrays and as single particles. Biophys J 66(6):2139–2150PubMedCrossRefGoogle Scholar
  103. Valle M, Kremer L, Martinez AC, Roncal F, Valpuesta JM, Albar JP, Carrascosa JL (1999) Domain architecture of the bacteriophage phi29 connector protein. J Mol Biol 288(5):899–909PubMedCrossRefGoogle Scholar
  104. Valpuesta JM, Carrascosa JL (1994) Structure of viral connectors and their function in bacteriophage assembly and DNA packaging. Q Rev Biophys 27(2):107–155PubMedCrossRefGoogle Scholar
  105. Valpuesta JM, Fernandez JJ, Carazo JM, Carrascosa JL (1999) The three-dimensional structure of a DNA translocating machine at 10 A resolution. Structure 7(3):289–296PubMedCrossRefGoogle Scholar
  106. van Heel M, Gowen B, Matadeen R, Orlova EV, Finn R, Pape T, Cohen D, Stark H, Schmidt R, Schatz M, Patwardhan A (2000) Single-particle electron cryo-microscopy: towards atomic resolution. Q Rev Biophys 33(4):307–369PubMedCrossRefGoogle Scholar
  107. Velankar SS, Soultanas P, Dillingham MS, Subramanya HS, Wigley DB (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97(1):75–84PubMedCrossRefGoogle Scholar
  108. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1(8):945–951PubMedGoogle Scholar
  109. Wichitwechkarn J, Bailey S, Bodley JW, Anderson D (1989) Prohead RNA of bacteriophage phi 29: size, stoichiometry and biological activity. Nucleic Acids Res 17(9):3459–3468PubMedCrossRefGoogle Scholar
  110. Wikoff WR, Liljas L, Duda RL, Tsuruta H, Hendrix RW, Johnson JE (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289(5487):2129–2133PubMedCrossRefGoogle Scholar
  111. Wittinghofer A, Scheffzek K, Ahmadian MR (1997) The interaction of Ras with GTPase-activating proteins. FEBS Lett 410(1):63–67PubMedCrossRefGoogle Scholar
  112. Xiang Y, Morais MC, Battisti AJ, Grimes S, Jardine PJ, Anderson DL, Rossmann MG (2006) Structural changes of bacteriophage phi29 upon DNA packaging and release. EMBO J 25(21):5229–5239PubMedCrossRefGoogle Scholar
  113. Xiang Y, Morais MC, Cohen DN, Bowman VD, Anderson DL, Rossmann MG (2008) Crystal and cryoEM structural studies of a cell wall degrading enzyme in the bacteriophage phi29 tail. Proc Natl Acad Sci USA 105(28):9552–9557PubMedCrossRefGoogle Scholar
  114. Xiao F, Moll WD, Guo S, Guo P (2005) Binding of pRNA to the N-terminal 14 amino acids of connector protein of bacteriophage phi29. Nucleic Acids Res 33(8):2640–2649PubMedCrossRefGoogle Scholar
  115. Yehle CO (1978) Genome-linked protein associated with the 5′ termini of bacteriophage phi29 DNA. J Virol 27(3):776–783PubMedGoogle Scholar
  116. Yoshida M, Amano T (1995) A common topology of proteins catalyzing ATP-triggered reactions. FEBS Lett 359(1):1–5PubMedCrossRefGoogle Scholar
  117. Yu J, Moffitt J, Hetherington CL, Bustamante C, Oster G (2010) Mechanochemistry of a viral DNA packaging motor. J Mol Biol 400(2):186–203PubMedCrossRefGoogle Scholar
  118. Zhang C, Lee CS, Guo P (1994) The proximate 5′ and 3′ ends of the 120-base viral RNA (pRNA) are crucial for the packaging of bacteriophage phi 29 DNA. Virology 201(1):77–85PubMedCrossRefGoogle Scholar
  119. Zhang C, Tellinghuisen T, Guo P (1995) Confirmation of the helical structure of the 5′/3′ termini of the essential DNA packaging pRNA of phage phi 29. RNA 1(10):1041–1050PubMedGoogle Scholar
  120. Zhang F, Lemieux S, Wu X, St-Arnaud D, McMurray CT, Major F, Anderson D (1998) Function of hexameric RNA in packaging of bacteriophage phi 29 DNA in vitro. Mol Cell 2(1):141–147PubMedCrossRefGoogle Scholar
  121. Zhao W, Morais MC, Anderson DL, Jardine PJ, Grimes S (2008) Role of the CCA bulge of prohead RNA of bacteriophage ø29 in DNA packaging. J Mol Biol 383(3):520–528PubMedCrossRefGoogle Scholar
  122. Zheng H, Olia AS, Gonen M, Andrews S, Cingolani G, Gonen T (2008) A conformational switch in bacteriophage p22 portal protein primes genome injection. Mol Cell 29(3):376–383PubMedCrossRefGoogle Scholar
  123. Zhou ZH, Dougherty M, Jakana J, He J, Rixon FJ, Chiu W (2000) Seeing the herpesvirus capsid at 8.5 A. Science 288(5467):877–880PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular Biology, Sealy Center for Structural and Computational BiologyUniversity of Texas Medical Branch at GalvestonGalvestonUSA

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