1932

Abstract

Translocation of viral double-stranded DNA (dsDNA) into the icosahedral prohead shell is catalyzed by TerL, a motor protein that has ATPase, endonuclease, and translocase activities. TerL, following endonucleolytic cleavage of immature viral DNA concatemer recognized by TerS, assembles into a pentameric ring motor on the prohead's portal vertex and uses ATP hydrolysis energy for DNA translocation. TerL's N-terminal ATPase is connected by a hinge to the C-terminal endonuclease. Inchworm models propose that modest domain motions accompanying ATP hydrolysis are amplified, through changes in electrostatic interactions, into larger movements of the C-terminal domain bound to DNA. In phage ϕ29, four of the five TerL subunits sequentially hydrolyze ATP, each powering translocation of 2.5 bp. After one viral genome is encapsidated, the internal pressure signals termination of packaging and ejection of the motor. Current focus is on the structures of packaging complexes and the dynamics of TerL during DNA packaging, endonuclease regulation, and motor mechanics.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-100114-055212
2015-11-09
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/virology/2/1/annurev-virology-100114-055212.html?itemId=/content/journals/10.1146/annurev-virology-100114-055212&mimeType=html&fmt=ahah

Literature Cited

  1. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. 1.  1999. Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage. PNAS 96:2192–97 [Google Scholar]
  2. Rixon FJ, Schmidt MF. 2.  2014. Structural similarities in DNA packaging and delivery apparatuses in herpesviruses and dsDNA bacteriophages. Curr. Opin. Virol. 5:105–10 [Google Scholar]
  3. Rao VB, Feiss M. 3.  2008. The bacteriophage DNA packaging motor. Annu. Rev. Genet. 42:647–81 [Google Scholar]
  4. Feiss M, Rao VB. 4.  2012. The bacteriophage DNA packaging machine. Adv. Exp. Med. Biol. 726:489–509 [Google Scholar]
  5. Casjens SR. 5.  2011. The DNA-packaging nanomotor of tailed bacteriophages. Nat. Rev. Microbiol. 9:647–57 [Google Scholar]
  6. Chemla YR, Smith DE. 6.  2012. Single-molecule studies of viral DNA packaging. Adv. Exp. Med. Biol. 726:549–84 [Google Scholar]
  7. Black LW, Rao VB. 7.  2012. Structure, assembly, and DNA packaging of the bacteriophage T4 head. Adv. Virus Res. 82:119–53 [Google Scholar]
  8. Black LW. 8.  2015. Old, new, and widely true: the bacteriophage T4 DNA packaging mechanism. Virology 479–80:650–56 [Google Scholar]
  9. Morais MC. 9.  2012. The dsDNA packaging motor in bacteriophage ϕ29. Adv. Exp. Med. Biol. 726:511–47 [Google Scholar]
  10. Oliveira L, Tavares P, Alonso JC. 10.  2013. Headful DNA packaging: bacteriophage SPP1 as a model system. Virus Res. 173:247–59 [Google Scholar]
  11. Chelikani V, Ranjan T, Kondabagil K. 11.  2014. Revisiting the genome packaging in viruses with lessons from the “giants.”. Virology 466–67:15–26 [Google Scholar]
  12. Hendrix RW, Johnson JE. 12.  2012. Bacteriophage HK97 capsid assembly and maturation. Adv. Exp. Med. Biol. 726:351–63 [Google Scholar]
  13. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C. 13.  2001. The bacteriophage straight ϕ29 portal motor can package DNA against a large internal force. Nature 413:748–52 [Google Scholar]
  14. Berndsen ZT, Keller N, Smith DE. 14.  2015. Continuous allosteric regulation of a viral packaging motor by a sensor that detects the density and conformation of packaged DNA. Biophys. J. 108:315–24 [Google Scholar]
  15. Liu S, Chistol G, Hetherington CL, Tafoya S, Aathavan K. 15.  et al. 2014. A viral packaging motor varies its DNA rotation and step size to preserve subunit coordination as the capsid fills. Cell 157:702–13 [Google Scholar]
  16. Sao-Jose C, de Frutos M, Raspaud E, Santos MA, Tavares P. 16.  2007. Pressure built by DNA packing inside virions: enough to drive DNA ejection in vitro, largely insufficient for delivery into the bacterial cytoplasm. J. Mol. Biol. 374:346–55 [Google Scholar]
  17. Evilevitch A, Fang LT, Yoffe AM, Castelnovo M, Rau DC. 17.  et al. 2008. Effects of salt concentrations and bending energy on the extent of ejection of phage genomes. Biophys. J. 94:1110–20 [Google Scholar]
  18. de Beer T, Fang J, Ortega M, Yang Q, Maes L. 18.  et al. 2002. Insights into specific DNA recognition during the assembly of a viral genome packaging machine. Mol. Cell 9:981–91 [Google Scholar]
  19. Roy A, Bhardwaj A, Datta P, Lander GC, Cingolani G. 19.  2012. Small terminase couples viral DNA binding to genome-packaging ATPase activity. Structure 20:1403–13 [Google Scholar]
  20. Zhao H, Finch CJ, Sequeira RD, Johnson BA, Johnson JE. 20.  et al. 2010. Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine. PNAS 107:1971–76 [Google Scholar]
  21. Buttner CR, Chechik M, Ortiz-Lombardia M, Smits C, Ebong IO. 21.  et al. 2012. Structural basis for DNA recognition and loading into a viral packaging motor. PNAS 109:811–16 [Google Scholar]
  22. Sun S, Gao S, Kondabagil K, Xiang Y, Rossmann MG, Rao VB. 22.  2012. Structure and function of the small terminase component of the DNA packaging machine in T4-like bacteriophages. PNAS 109:817–22 [Google Scholar]
  23. Bhardwaj A, Casjens SR, Cingolani G. 23.  2014. Exploring the atomic structure and conformational flexibility of a 320 Å long engineered viral fiber using X-ray crystallography. Acta Crystallogr. D 70:342–53 [Google Scholar]
  24. Gao S, Rao VB. 24.  2011. Specificity of interactions among the DNA-packaging machine components of T4-related bacteriophages. J. Biol. Chem. 286:3944–56 [Google Scholar]
  25. Zhao H, Kamau YN, Christensen TE, Tang L. 25.  2012. Structural and functional studies of the phage Sf6 terminase small subunit reveal a DNA-spooling device facilitated by structural plasticity. J. Mol. Biol. 423:413–26 [Google Scholar]
  26. Chai S, Lurz R, Alonso JC. 26.  1995. 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 252:386–98 [Google Scholar]
  27. Higgins RR, Becker A. 27.  1995. Interaction of terminase, the DNA packaging enzyme of phage λ, with its cos DNA substrate. J. Mol. Biol 252:31–46 [Google Scholar]
  28. Kanamaru S, Kondabagil K, Rossmann MG, Rao VB. 28.  2004. The functional domains of bacteriophage T4 terminase. J. Biol. Chem. 279:40795–801 [Google Scholar]
  29. Alam TI, Draper B, Kondabagil K, Rentas FJ, Ghosh-Kumar M. 29.  et al. 2008. The headful packaging nuclease of bacteriophage T4. Mol. Microbiol. 69:1180–90 [Google Scholar]
  30. Smits C, Chechik M, Kovalevskiy OV, Shevtsov MB, Foster AW. 30.  et al. 2009. Structural basis for the nuclease activity of a bacteriophage large terminase. EMBO Rep. 10:592–98 [Google Scholar]
  31. Zhao H, Christensen TE, Kamau YN, Tang L. 31.  2013. Structures of the phage Sf6 large terminase provide new insights into DNA translocation and cleavage. PNAS 110:8075–80 [Google Scholar]
  32. Roy A, Cingolani G. 32.  2012. Structure of P22 headful packaging nuclease. J. Biol. Chem. 287:28196–205 [Google Scholar]
  33. Nadal M, Mas PJ, Blanco AG, Arnan C, Sola M. 33.  et al. 2010. Structure and inhibition of herpesvirus DNA packaging terminase nuclease domain. PNAS 107:16078–83 [Google Scholar]
  34. Selvarajan Sigamani S, Zhao H, Kamau YN, Baines JD, Tang L. 34.  2013. The structure of the herpes simplex virus DNA-packaging terminase pUL15 nuclease domain suggests an evolutionary lineage among eukaryotic and prokaryotic viruses. J. Virol. 87:7140–48 [Google Scholar]
  35. Sun S, Kondabagil K, Draper B, Alam TI, Bowman VD. 35.  et al. 2008. The structure of the phage T4 DNA packaging motor suggests a mechanism dependent on electrostatic forces. Cell 135:1251 [Google Scholar]
  36. Rychlik MP, Chon H, Cerritelli SM, Klimek P, Crouch RJ, Nowotny M. 36.  2010. Crystal structures of RNase H2 in complex with nucleic acid reveal the mechanism of RNA-DNA junction recognition and cleavage. Mol. Cell 40:658–70 [Google Scholar]
  37. Yang W, Lee JY, Nowotny M. 37.  2006. Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol. Cell 22:5–13 [Google Scholar]
  38. Cornilleau C, Atmane N, Jacquet E, Smits C, Alonso JC. 38.  et al. 2013. The nuclease domain of the SPP1 packaging motor coordinates DNA cleavage and encapsidation. Nucleic Acids Res. 41:340–54 [Google Scholar]
  39. Ghosh-Kumar M, Alam TI, Draper B, Stack JD, Rao VB. 39.  2011. Regulation by interdomain communication of a headful packaging nuclease from bacteriophage T4. Nucleic Acids Res. 39:2742–55 [Google Scholar]
  40. Camacho AG, Gual A, Lurz R, Tavares P, Alonso JC. 40.  2003. Bacillus subtilis bacteriophage SPP1 DNA packaging motor requires terminase and portal proteins. J. Biol. Chem. 278:23251–59 [Google Scholar]
  41. Kala S, Cumby N, Sadowski PD, Hyder BZ, Kanelis V. 41.  et al. 2014. HNH proteins are a widespread component of phage DNA packaging machines. PNAS 111:6022–27 [Google Scholar]
  42. Quiles-Puchalt N, Carpena N, Alonso JC, Novick RP, Marina A, Penades JR. 42.  2014. Staphylococcal pathogenicity island DNA packaging system involving cos-site packaging and phage-encoded HNH endonucleases. PNAS 111:6016–21 [Google Scholar]
  43. Heming JD, Huffman JB, Jones LM, Homa FL. 43.  2014. Isolation and characterization of the herpes simplex virus 1 terminase complex. J. Virol. 88:225–36 [Google Scholar]
  44. Borst EM, Kleine-Albers J, Gabaev I, Babic M, Wagner K. 44.  et al. 2013. The human cytomegalovirus UL51 protein is essential for viral genome cleavage-packaging and interacts with the terminase subunits pUL56 and pUL89. J. Virol. 87:1720–32 [Google Scholar]
  45. Maluf N, Gaussier H, Bogner E, Feiss M, Catalano C. 45.  2006. Assembly of bacteriophage λ terminase into a viral DNA maturation and packaging machine. Biochemistry 45:15259–68 [Google Scholar]
  46. Andrews BT, Catalano CE. 46.  2013. Strong subunit coordination drives a powerful viral DNA packaging motor. PNAS 110:5909–14 [Google Scholar]
  47. Moffitt JR, Chemla YR, Aathavan K, Grimes S, Jardine PJ. 47.  et al. 2009. Intersubunit coordination in a homomeric ring ATPase. Nature 457:446–50 [Google Scholar]
  48. Cao S, Saha M, Zhao W, Jardine PJ, Zhang W. 48.  et al. 2014. Insights into the structure and assembly of the bacteriophage 29 double-stranded DNA packaging motor. J. Virol. 88:3986–96 [Google Scholar]
  49. Huang H, Masters M. 49.  2014. Bacteriophage P1 pac sites inserted into the chromosome greatly increase packaging and transduction of Escherichia coli genomic DNA. Virology 468–70:274–82 [Google Scholar]
  50. Furth ME, Wickner SH. 50.  1983. Lambda DNA replication. Lambda II RW Hendrix, JW Roberts, FW Stahl, RA Weisberg 145–73 Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press [Google Scholar]
  51. Sternberg N, Coulby J. 51.  1987. Recognition and cleavage of the bacteriophage P1 packaging site (pac). I. Differential processing of the cleaved ends in vivo. J. Mol. Biol. 194:453–68 [Google Scholar]
  52. Vafabakhsh R, Kondabagil K, Earnest T, Lee KS, Zhang Z. 52.  et al. 2014. Single-molecule packaging initiation in real time by a viral DNA packaging machine from bacteriophage T4. PNAS 111:15096–101 [Google Scholar]
  53. Rao VB, Black LW. 53.  1988. 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 200:475–85 [Google Scholar]
  54. Mitchell MS, Matsuzaki S, Imai S, Rao VB. 54.  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. 30:4009–21 [Google Scholar]
  55. Kondabagil K, Dai L, Vafabakhsh R, Ha T, Draper B, Rao VB. 55.  2014. Designing a nine cysteine-less DNA packaging motor from bacteriophage T4 reveals new insights into ATPase structure and function. Virology 468–70:660–68 [Google Scholar]
  56. Tsay JM, Sippy J, DelToro D, Andrews BT, Draper B. 56.  et al. 2010. Mutations altering a structurally conserved loop-helix-loop region of a viral packaging motor change DNA translocation velocity and processivity. J. Biol. Chem. 285:24282–89 [Google Scholar]
  57. Tanner NK, Cordin O, Banroques J, Doere M, Linder P. 57.  2003. The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell 11:127–38 [Google Scholar]
  58. Kondabagil K, Draper B, Rao VB. 58.  2012. Adenine recognition is a key checkpoint in the energy release mechanism of phage T4 DNA packaging motor. J. Mol. Biol. 415:329–42 [Google Scholar]
  59. Mitchell MS, Rao VB. 59.  2006. Functional analysis of the bacteriophage T4 DNA-packaging ATPase motor. J. Biol. Chem. 281:518–27 [Google Scholar]
  60. Tsay JM, Sippy J, Feiss M, Smith DE. 60.  2009. The Q motif of a viral packaging motor governs its force generation and communicates ATP recognition to DNA interaction. PNAS 106:14355–60 [Google Scholar]
  61. Simpson A, Tao Y, Leiman P, Badasso M, He Y. 61.  et al. 2000. Structure of the bacteriophage ϕ29 DNA packaging motor. Nature 408:745–50 [Google Scholar]
  62. Lebedev AA, Krause MH, Isidro AL, Vagin AA, Orlova EV. 62.  et al. 2007. Structural framework for DNA translocation via the viral portal protein. EMBO J. 26:1984–94 [Google Scholar]
  63. Padilla-Sanchez V, Gao S, Kim HR, Kihara D, Sun L. 63.  et al. 2014. Structure-function analysis of the DNA translocating portal of the bacteriophage T4 packaging machine. J. Mol. Biol. 426:1019–38 [Google Scholar]
  64. Olia AS, Prevelige PE Jr, Johnson JE, Cingolani G. 64.  2011. Three-dimensional structure of a viral genome-delivery portal vertex. Nat. Struct. Mol. Biol. 18:597 [Google Scholar]
  65. Sun L, Zhang X, Gao S, Rao PA, Padilla-Sanchez V. 65.  et al. 2015. Cryo-EM structure of the bacteriophage T4 portal protein assembly at near-atomic resolution. Nat. Commun 6:7548 [Google Scholar]
  66. Tang J, Lander GC, Olia A, Li R, Casjens S. 66.  et al. 2011. Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in P22. Structure 19:496–502 [Google Scholar]
  67. Isidro A, Henriques AO, Tavares P. 67.  2004. The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology 322:253–63 [Google Scholar]
  68. Casjens S, Wyckoff E, Hayden M, Sampson L, Eppler K. 68.  et al. 1992. Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA. J. Mol. Biol. 224:1055–74 [Google Scholar]
  69. Cue D, Feiss M. 69.  1997. Genetic evidence that recognition of cosQ, the signal for termination of phage λ DNA packaging, depends on the extent of head filling. Genetics 147:7–17 [Google Scholar]
  70. Hugel T, Michaelis J, Hetherington CL, Jardine PJ, Grimes S. 70.  et al. 2007. Experimental test of connector rotation during DNA packaging into bacteriophage ϕ29 capsids. PLOS Biol. 5:e59 [Google Scholar]
  71. Baumann RG, Mullaney J, Black LW. 71.  2006. Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol. Microbiol. 61:16–32 [Google Scholar]
  72. Cuervo A, Vaney MC, Antson AA, Tavares P, Oliveira L. 72.  2007. Structural rearrangements between portal protein subunits are essential for viral DNA translocation. J. Biol. Chem. 282:18907–13 [Google Scholar]
  73. Grimes S, Ma S, Gao J, Atz R, Jardine PJ. 73.  2011. Role of ϕ29 connector channel loops in late-stage DNA packaging. J. Mol. Biol. 410:50–59 [Google Scholar]
  74. Jing P, Haque F, Shu D, Montemagno C, Guo P. 74.  2010. One-way traffic of a viral motor channel for double-stranded DNA translocation. Nano Lett. 10:3620–27 [Google Scholar]
  75. Wieczorek D, Didion L, Feiss M. 75.  2002. Alterations of the portal protein of bacteriophage λ suppress mutations in cosQ, the site required for termination of DNA packaging. Genetics 161:21–31 [Google Scholar]
  76. Tavares P, Santos MA, Lurz R, Morelli G, de Lencastre H, Trautner TA. 76.  1992. Identification of a gene in Bacillus subtilis bacteriophage SPP1 determining the amount of packaged DNA. J. Mol. Biol. 225:81–92 [Google Scholar]
  77. Morais MC, Koti JS, Bowman VD, Reyes-Aldrete E, Anderson DL, Rossmann MG. 77.  2008. Defining molecular and domain boundaries in the bacteriophage ϕ29 DNA packaging motor. Structure 16:1267–74 [Google Scholar]
  78. Dauden MI, Martin-Benito J, Sanchez-Ferrero JC, Pulido-Cid M, Valpuesta JM, Carrascosa JL. 78.  2013. Large terminase conformational change induced by connector binding in bacteriophage T7. J. Biol. Chem. 288:16998–7007 [Google Scholar]
  79. Schwartz C, De Donatis GM, Fang H, Guo P. 79.  2013. The ATPase of the phi29 DNA packaging motor is a member of the hexameric AAA+ superfamily. Virology 443:20–27 [Google Scholar]
  80. Oliveira L, Cuervo A, Tavares P. 80.  2010. Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. J. Biol. Chem. 285:7366–73 [Google Scholar]
  81. Lin H, Rao VB, Black LW. 81.  1999. Analysis of capsid portal protein and terminase functional domains: interaction sites required for DNA packaging in bacteriophage T4. J. Mol. Biol. 289:249–60 [Google Scholar]
  82. Hegde S, Padilla-Sanchez V, Draper B, Rao VB. 82.  2012. Portal-large terminase interactions of the bacteriophage T4 DNA packaging machine implicate a molecular lever mechanism for coupling ATPase to DNA translocation. J. Virol. 86:4046–57 [Google Scholar]
  83. Dixit AB, Ray K, Thomas JA, Black LW. 83.  2013. The C-terminal domain of the bacteriophage T4 terminase docks on the prohead portal clip region during DNA packaging. Virology 446:293–302 [Google Scholar]
  84. Fuller DN, Raymer DM, Rickgauer JP, Robertson RM, Catalano CE. 84.  et al. 2007. Measurements of single DNA molecule packaging dynamics in bacteriophage λ reveal high forces, high motor processivity, and capsid transformations. J. Mol. Biol. 373:1113–22 [Google Scholar]
  85. Fuller DN, Raymer DM, Kottadiel VI, Rao VB, Smith DE. 85.  2007. Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. PNAS 104:16868–73 [Google Scholar]
  86. Duffy C, Feiss M. 86.  2002. The large subunit of bacteriophage λ's terminase plays a role in DNA translocation and packaging termination. J. Mol. Biol. 316:547–61 [Google Scholar]
  87. Morita M, Tasaka M, Fujisawa H. 87.  1993. DNA packaging ATPase of bacteriophage T3. Virology 193:748–52 [Google Scholar]
  88. Guo P, Peterson C, Anderson D. 88.  1987. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage ϕ29. J. Mol. Biol. 197:229–36 [Google Scholar]
  89. Chemla YR, Aathavan K, Michaelis J, Grimes S, Jardine PJ. 89.  et al. 2005. Mechanism of force generation of a viral DNA packaging motor. Cell 122:683–92 [Google Scholar]
  90. Aathavan K, Politzer AT, Kaplan A, Moffitt JR, Chemla YR. 90.  et al. 2009. Substrate interactions and promiscuity in a viral DNA packaging motor. Nature 461:669–73 [Google Scholar]
  91. Chistol G, Liu S, Hetherington CL, Moffitt JR, Grimes S. 91.  et al. 2012. High degree of coordination and division of labor among subunits in a homomeric ring ATPase. Cell 151:1017–28 [Google Scholar]
  92. Kottadiel VI, Rao VB, Chemla YR. 92.  2012. The dynamic pause-unpackaging state, an off-translocation recovery state of a DNA packaging motor from bacteriophage T4. PNAS 109:20000–5 [Google Scholar]
  93. Burroughs AM, Iyer LM, Aravind L. 93.  2007. Comparative genomics and evolutionary trajectories of viral ATP dependent DNA-packaging systems. Genome Dyn. 3:48–65 [Google Scholar]
  94. Migliori AD, Keller N, Alam TI, Mahalingam M, Rao VB. 94.  et al. 2014. Evidence for an electrostatic mechanism of force generation by the bacteriophage T4 DNA packaging motor. Nat. Commun. 5:4173 [Google Scholar]
  95. Draper B, Rao VB. 95.  2007. An ATP hydrolysis sensor in the DNA packaging motor from bacteriophage T4 suggests an inchworm-type translocation mechanism. J. Mol. Biol. 369:79–94 [Google Scholar]
  96. Migliori AD, Smith DE, Arya G. 96.  2014. Molecular interactions and residues involved in force generation in the T4 viral DNA packaging motor. J. Mol. Biol. 426:4002–17 [Google Scholar]
  97. Mancini EJ, Kainov DE, Grimes JM, Tuma R, Bamford DH, Stuart DI. 97.  2004. Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 118:743–55 [Google Scholar]
  98. Ray K, Sabanayagam CR, Lakowicz JR, Black LW. 98.  2010. DNA crunching by a viral packaging motor: compression of a procapsid-portal stalled Y-DNA substrate. Virology 398:224–32 [Google Scholar]
  99. Oram M, Sabanayagam C, Black LW. 99.  2008. Modulation of the packaging reaction of bacteriophage T4 terminase by DNA structure. J. Mol. Biol. 381:61–72 [Google Scholar]
  100. Harvey SC. 100.  2015. The scrunchworm hypothesis: Transitions between A-DNA and B-DNA provide the driving force for genome packaging in double-stranded DNA bacteriophages. J. Struct. Biol. 189:1–8 [Google Scholar]
  101. Feiss M, Siegele DA. 101.  1979. Packaging of the bacteriophage lambda chromosome: dependence of cos cleavage on chromosome length. Virology 92:190–200 [Google Scholar]
  102. Cue D, Feiss M. 102.  2001. Bacteriophage λ DNA packaging: DNA site requirements for termination and processivity. J. Mol. Biol. 311:233–40 [Google Scholar]
  103. Cue D, Feiss M. 103.  1993. A site required for termination of packaging of the phage λ chromosome. PNAS 90:9290–94 [Google Scholar]
  104. Cue D, Feiss M. 104.  1998. Termination of packaging of the bacteriophage λ chromosome: cosQ is required for nicking the bottom strand of cosN. J. Mol. Biol. 280:11–29 [Google Scholar]
  105. Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige P. 105.  et al. 2006. The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312:1791–95 [Google Scholar]
  106. Lhuillier S, Gallopin M, Gilquin B, Brasiles S, Lancelot N. 106.  et al. 2009. Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. PNAS 106:8507–12 [Google Scholar]
  107. White HE, Sherman MB, Brasiles S, Jacquet E, Seavers P. 107.  et al. 2012. Capsid structure and its stability at the late stages of bacteriophage SPP1 assembly. J. Virol. 86:6768–77 [Google Scholar]
  108. Maxwell KL, Yee AA, Booth V, Arrowsmith CH, Gold M, Davidson AR. 108.  2001. The solution structure of bacteriophage λ protein W, a small morphogenetic protein possessing a novel fold. J. Mol. Biol. 308:9–14 [Google Scholar]
  109. Maxwell KL, Davidson AR, Murialdo H, Gold M. 109.  2000. Thermodynamic and functional characterization of protein W from bacteriophage λ: The three C-terminal residues are critical for activity. J. Biol. Chem. 275:18879–86 [Google Scholar]
  110. Strauss H, King J. 110.  1984. Steps in the stabilization of newly packaged DNA during phage P22 morphogenesis. J. Mol. Biol. 172:523–43 [Google Scholar]
/content/journals/10.1146/annurev-virology-100114-055212
Loading
/content/journals/10.1146/annurev-virology-100114-055212
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error