The Bacteriophage Head-to-Tail Interface

  • Paulo Tavares
Part of the Subcellular Biochemistry book series (SCBI, volume 88)


Many icosahedral viruses use a specialized portal vertex for genome encapsidation in the viral capsid (or head). This structure then controls release of the viral genetic information to the host cell at the beginning of infection. In tailed bacteriophages, the portal system is connected to a tail device that delivers their genome to the bacterial cytoplasm. The head-to-tail interface is a multiprotein complex that locks the viral DNA inside the phage capsid correctly positioned for egress and that controls its ejection when the viral particle interacts with the host cell receptor. Here we review the molecular mechanisms how this interface is assembled and how it carries out those two critical steps in the life cycle of tailed phages.


Bacteriophage Head-to-tail interface Portal system Capsid DNA packaging DNA ejection 



Marie-Christine Vaney (Institut Pasteur, Paris) is acknowledged for insightful discussions on structure analysis and for invaluable help to prepare manuscript figures.

I thank present and past members of our team and collaborators for their insightful research that established present knowledge on the SPP1 head-to-tail interface.

Work in our laboratory on SPP1 phage assembly is supported by institutional funding from CNRS.


  1. Abrescia NG, Bamford DH, Grimes JM, Stuart DI (2012) Structure unifies the viral universe. Annu Rev Biochem 81:795–822PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ackermann HW (2012) Bacteriophage electron microscopy. Adv Virus Res 82:1–32PubMedCrossRefPubMedCentralGoogle Scholar
  3. Agirrezabala X, Martín-Benito J, Castón JR, Miranda R, Valpuesta JM, Carrascosa JL (2005) Maturation of phage T7 involves structural modification of both shell and inner core components. EMBO J 24:3820–3829PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aksyuk AA, Rossmann MG (2011) Bacteriophage assembly. Virus 3:172–203CrossRefGoogle Scholar
  5. Arnaud CA, Effantin G, Vivès C, Engilberge S, Bacia M, Boulanger P, Girard E, Schoehn G, Breyton C (2017) Bacteriophage T5 tail tube structure suggests a trigger mechanism for Siphoviridae DNA ejection. Nat Commun 8:1953PubMedPubMedCentralCrossRefGoogle Scholar
  6. Auzat I, Petitpas I, Lurz R, Weise F, Tavares P (2014) A touch of glue to complete bacteriophage assembly: the tail-to-head joining protein (THJP) family. Mol Microbiol 91:1164–1178PubMedCrossRefGoogle Scholar
  7. Bazinet C, King J (1985) The DNA translocating vertex of dsDNA bacteriophage. Annu Rev Microbiol 39:109–129PubMedCrossRefGoogle Scholar
  8. Bhardwaj A, Olia AS, Walker-Kopp N, Cingolani G (2007) Domain organization and polarity of tail needle GP26 in the portal vertex structure of bacteriophage P22. J Mol Biol 371:374–387PubMedCrossRefGoogle Scholar
  9. Bhardwaj A, Walker-Kopp N, Casjens SR, Cingolani G (2009) An evolutionarily conserved family of virion tail needles related to bacteriophage P22 gp26: correlation between structural stability and length of the alpha-helical trimeric coiled coil. J Mol Biol 391:227–245PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bhardwaj A, Sankhala RS, Olia AS, Brooke D, Casjens SR, Taylor DJ, Prevelige PE Jr, Cingolani G (2016) Structural Plasticity of the Protein Plug That Traps Newly Packaged Genomes in Podoviridae Virions. J Biol Chem 291:215–226PubMedCrossRefGoogle Scholar
  11. Bowman BR, Welschhans RL, Jayaram H, Stow ND, Preston VG, Quiocho FA (2006) Structural characterization of the UL25 DNA-packaging protein from herpes simplex virus type 1. J Virol 80:2309–2317PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cardarelli L, Lam R, Tuite A, Baker LA, Sadowski PD, Radford DR, Rubinstein JL, Battaile KP, Chirgadze N, Maxwell KL, Davidson AR (2010a) The crystal structure of bacteriophage HK97 gp6: defining a large family of head-tail connector proteins. J Mol Biol 395:754–368PubMedCrossRefGoogle Scholar
  13. Cardarelli L, Pell LG, Neudecker P, Pirani N, Liu A, Baker LA, Rubinstein JL, Maxwell KL, Davidson AR (2010b) Phages have adapted the same protein fold to fulfill multiple functions in virion assembly. Proc Natl Acad Sci U S A 107:14384–14389PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cardarelli L, Maxwell KL, Davidson AR (2011) Assembly mechanism is the key determinant of the dosage sensitivity of a phage structural protein. Proc Natl Acad Sci U S A 108:10168–10173PubMedPubMedCentralCrossRefGoogle Scholar
  15. Casjens S, Hendrix R (1988) Control mechanisms in dsDNA bacteriophage assembly. In: Calendar R (ed) The bacteriophages, vol 1. Plenum Press, New YorkGoogle Scholar
  16. Casjens S, Molineux I (2012) Short noncontractile tail machines: adsorption and DNA delivery by podoviruses. Adv Exp Med Biol 726:143–179PubMedCrossRefGoogle Scholar
  17. Casjens S, Horn T, Kaiser AD (1972) Head assembly steps controlled by genes F and W in bacteriophage lambda. J Mol Biol 64:551–563PubMedCrossRefGoogle Scholar
  18. Chaban Y, Lurz R, Brasilès S, Cornilleau C, Karreman M, Zinn-Justin S, Tavares P, Orlova EV (2015) Structural rearrangements in the phage head-to-tail Interface during assembly and infection. Proc Natl Acad Sci U S A 112:7009–7014PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chagot B, Auzat I, Gallopin M, Petitpas I, Gilquin B, Tavares P, Zinn-Justin S (2012) Solution structure of gp17 from the Siphoviridae bacteriophage SPP1: insights into its role in virion assembly. Proteins: Struct Funct Bioinf 80:319–326CrossRefGoogle Scholar
  20. Chang J, Weigele P, King J, Chiu W, Jiang W (2006) Cryo-EM asymmetric reconstruction of bacteriophage P22 reveals organization of its DNA packaging and infecting machinery. Structure 14:1073–1082PubMedCrossRefGoogle Scholar
  21. Chang JT, Schmid MF, Haase-Pettingell C, Weigele PR, King JA, Chiu W (2010) Visualizing the structural changes of bacteriophage Epsilon15 and its Salmonella host during infection. J Mol Biol 402:731–740PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chattoraj DK, Inman RB (1974) Location of DNA ends in P2, 186, P4 and lambda bacteriophage heads. J Mol Biol 87:11–22PubMedCrossRefGoogle Scholar
  23. Chemla YR, Smith DE (2012) Single-molecule studies of viral DNA packaging. Adv Exp Med Biol 726:549–584PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 U S A 108:1355–1360PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cressiot B, Greive SJ, Si W, Pascoa TC, Mojtabavi M, Chechik M, Jenkins HT, Lu X, Zhang K, Aksimentiev A, Antson AA, Wanunu M (2017) Porphyrin-Assisted Docking of a Thermophage Portal Protein into Lipid Bilayers: Nanopore Engineering and Characterization. ACS Nano. in press 11:11931. Scholar
  26. Cuervo A, Carrascosa JL (2011) Viral connectors for DNA encapsulation. Curr Opin Biotechnol 23:529–536PubMedCrossRefGoogle Scholar
  27. Davidson AR, Cardarelli L, Pell LG, Radford DR, Maxwell KL (2012) Long noncontractile tail machines of bacteriophages. Adv Exp Med Biol 726:115–142PubMedCrossRefPubMedCentralGoogle Scholar
  28. Donate LE, Herranz L, Secilla JP, Carazo JM, Fujisawa H, Carrascosa JL (1988) Bacteriophage T3 connector: three-dimensional structure and comparison with other viral head-tail connecting regions. J Mol Biol 201:91–100PubMedCrossRefPubMedCentralGoogle Scholar
  29. Dröge A, Santos MA, Stiege A, Alonso JC, Lurz R, Trautner TA, Tavares P (2000) Shape and DNA packaging activity of bacteriophage SPP1 procapsid: protein components and interactions during assembly. J Mol Biol 296:117–132PubMedCrossRefGoogle Scholar
  30. Dube P, Tavares P, Lurz R, van Heel M (1993) Bacteriophage SPP1 portal protein: a DNA pump with 13-fold symmetry. EMBO J 12:1303–1309PubMedPubMedCentralCrossRefGoogle Scholar
  31. Edmonds L, Liu A, Kwan JJ, Avanessy A, Caracoglia M, Yang I, Maxwell KL, Rubenstein J, Davidson AR, Donaldson LW (2007) The NMR structure of the gpU tail-terminator protein from bacteriophage lambda: identification of sites contributing to Mg(II)-mediated oligomerization and biological function. J Mol Biol 365:175–186PubMedCrossRefPubMedCentralGoogle Scholar
  32. Evilevitch A, Lavelle L, Knobler CM, Raspaud E, Gelbart WM (2003) Osmotic pressure inhibition of DNA ejection from phage. Proc Natl Acad Sci U S A 100:9292–9295PubMedPubMedCentralCrossRefGoogle Scholar
  33. Farley MM, Tu J, Kearns DB, Molineux IJ, Liu J (2017) Ultrastructural analysis of bacteriophage Φ29 during infection of Bacillus subtilis. J Struct Biol 197:163–171PubMedCrossRefPubMedCentralGoogle Scholar
  34. Fokine A, Rossmann MG (2014) Molecular architecture of tailed double-stranded DNA phages. Bacteriophage 4:e28281PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fokine A, Zhang Z, Kanamaru S, Bowman VD, Aksyuk AA, Arisaka F, Rao VB, Rossmann MG (2013) The molecular architecture of the bacteriophage T4 neck. J Mol Biol 425:1731–1744PubMedPubMedCentralCrossRefGoogle Scholar
  36. Fu CY, Prevelige PE Jr (2009) In vitro incorporation of the phage Phi29 connector complex. Virology 394:149–153PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gaussier H, Yang Q, Catalano CE (2006) Building a virus from scratch: assembly of an infectious virus using purified components in a rigorously defined biochemical assay system. J Mol Biol 357:1154–1166PubMedCrossRefPubMedCentralGoogle Scholar
  38. Grundy FJ, Howe MM (1985) Morphogenetic structures present in lysates of amber mutants of bacteriophage Mu. Virology 143:485–504PubMedCrossRefPubMedCentralGoogle Scholar
  39. Guasch A, Pous J, Ibarra B, Gomis-Rüth FX, Valpuesta JM, Sousa N, Carrascosa JL, Coll M (2002) Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophages phi29 connector particle. J Mol Biol 315:663–676PubMedCrossRefPubMedCentralGoogle Scholar
  40. van Heel M, Orlova EV, Dube P, Tavares P (1996) Intrinsic versus imposed curvature in cyclical oligomers: the portal protein of bacteriophage SPP1. EMBO J 15:4785–4788PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hu B, Margolin W, Molineux IJ, Liu J (2013) The bacteriophage T7 virion undergoes extensive structural remodeling during infection. Science 339:576–579PubMedCrossRefPubMedCentralGoogle Scholar
  42. Hu B, Margolin W, Molineux IJ, Liu J (2015) Structural remodeling of bacteriophage T4 and host membranes during infection initiation. Proc Natl Acad Sci U S A 112:E4919–E4928PubMedPubMedCentralCrossRefGoogle Scholar
  43. Isidro A, Henriques AO, Tavares P (2004a) The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology 322:253–263PubMedCrossRefPubMedCentralGoogle Scholar
  44. Isidro A, Santos MA, Henriques AO, Tavares P (2004b) The high-resolution functional map of bacteriophage SPP1 portal protein. Mol Microbiol 51:949–962PubMedCrossRefPubMedCentralGoogle Scholar
  45. Jiang W, Chang J, Jakana J, Weigele P, King J, Chiu W (2006) Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439:612–661PubMedPubMedCentralCrossRefGoogle Scholar
  46. Johnson JE, Chiu W (2007) DNA packaging and delivery machines in tailed bacteriophages. Curr Opin Struct Biol 17:237–243PubMedCrossRefPubMedCentralGoogle Scholar
  47. Katsura I (1987) Determination of bacteriophage lambda tail length by a protein ruler. Nature 327:73–75PubMedCrossRefPubMedCentralGoogle Scholar
  48. Katsura I, Tsugita A (1977) Purification and characterization of the major protein and the terminator protein of the bacteriophage lambda tail. Virology 76:129–145PubMedCrossRefPubMedCentralGoogle Scholar
  49. Krupovic M, Bamford DH (2011) Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr Opin Virol 1:118–124PubMedCrossRefPubMedCentralGoogle Scholar
  50. Lander GC, Tang L, Casjens SR, Gilcrease EB, Prevelige P, Poliakov A, Potter CS, Carragher B, Johnson JE (2006) The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312:1791–1795PubMedCrossRefPubMedCentralGoogle Scholar
  51. 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 17:789–799PubMedPubMedCentralCrossRefGoogle Scholar
  52. Lebedev AA, Krause MH, Isidro AL, Vagin A, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26:1984–1994PubMedPubMedCentralCrossRefGoogle Scholar
  53. Leiman PG, Shneider MM (2012) Contractile tail machines of bacteriophages. Adv Exp Med Biol 726:93–114PubMedCrossRefPubMedCentralGoogle Scholar
  54. Leiman PG, Chipman PR, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2004) Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host. Cell 118:419–429PubMedCrossRefPubMedCentralGoogle Scholar
  55. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, Pukatzki S, Burley SK, Almo SC, Mekalanos JJ (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci U S A 106:4154–4159PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lengyel JA, Goldstein RN, Marsh M, Calendar R (1974) Structure of the bacteriophage P2 tail. Virology 62:161–174PubMedCrossRefPubMedCentralGoogle Scholar
  57. Lhuillier S, Gallopin M, Gilquin B, Brasilès S, Lancelot N, Letellier G, Gilles M, Dethan G, Orlova EV, Couprie J, Tavares P, Zinn-Justin S (2009) Structure of bacteriophage SPP1 head-to-tail connection reveals mechanism for viral DNA gating. Proc Natl Acad Sci U S A 106:8507–8512PubMedPubMedCentralCrossRefGoogle Scholar
  58. Liu X, Zhang Q, Murata K, Baker ML, Sullivan MB, Fu C, Dougherty MT, Schmid MF, Osburne MS, Chisholm SW, Chiu W (2010) Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 17:830–836PubMedPubMedCentralCrossRefGoogle Scholar
  59. Loessner MJ, Inman RB, Lauer P, Calendar R (2000) Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol Microbiol 35:324–340PubMedCrossRefPubMedCentralGoogle Scholar
  60. Lokareddy RK, Sankhala RS, Roy A, Afonine PV, Motwani T, Teschke CM, Parent KN, Cingolani G (2017) Portal protein functions akin to a DNA-sensor that couples genome-packaging to icosahedral capsid maturation. Nat Commun 8:14310PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lopes A, Tavares P, Petit MA, Guérois R, Zinn-Justin S (2014) Automated classification of tailed bacteriophages according to their neck organization. BMC Genomics 15:1027PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lurz R, Orlova EV, Günther D, Dube P, Dröge A, Weise F, van Heel M, Tavares P (2001) Structural organisation of the head-to-tail interface of a bacterial virus. J Mol Biol 310:1027–1037PubMedCrossRefGoogle Scholar
  63. Maxwell KL, Davidson AR, Murialdo H, Gold M (2000) Thermodynamic and functional characterization of protein W from bacteriophage lambda. The three C-terminal residues are critical for activity. J Biol Chem 275:18879–18886PubMedCrossRefGoogle Scholar
  64. Maxwell KL, Yee AA, Booth V, Arrowsmith CH, Gold M, Davidson AR (2001) The solution structure of bacteriophage lambda protein W, a small morphogenetic protein possessing a novel fold. J Mol Biol 308:9–14PubMedCrossRefGoogle Scholar
  65. Maxwell KL, Yee AA, Arrowsmith CH, Gold M, Davidson AR (2002) The solution structure of the bacteriophage lambda head-tail joining protein, gpFII. J Mol Biol 318:1395–1404PubMedCrossRefGoogle Scholar
  66. Moore SD, Prevelige PE Jr (2001) Structural transformations accompanying the assembly of bacteriophage P22 portal protein rings in vitro. J Biol Chem 276:6779–6788PubMedCrossRefGoogle Scholar
  67. Morais MC (2012) The dsDNA packaging motor in bacteriophage ϕ29. Adv Exp Med Biol 726:511–547PubMedCrossRefGoogle Scholar
  68. Motwani T, Lokareddy RK, Dunbar CA, Cortines JR, Jarrold MF, Cingolani G, Teschke CM (2017) A viral scaffolding protein triggers portal ring oligomerization and incorporation during procapsid assembly. Sci Adv 3:e1700423PubMedPubMedCentralCrossRefGoogle Scholar
  69. Newcomb WW, Homa FL, Brown JC (2005) Involvement of the portal at an early step in herpes simplex virus capsid assembly. J Virol 79:10540–10546PubMedPubMedCentralCrossRefGoogle Scholar
  70. Nováček J, Šiborová M, Benešík M, Pantůček R, Doškař J, Plevka P (2016) Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate. Proc Natl Acad Sci U S A 113:9351–9356PubMedPubMedCentralCrossRefGoogle Scholar
  71. Olia AS, Al-Bassam J, Winn-Stapley DA, Joss L, Casjens SR, Cingolani G (2006) Binding-induced stabilization and assembly of the phage P22 tail accessory factor gp4. J Mol Biol 363:558–576PubMedCrossRefPubMedCentralGoogle Scholar
  72. Olia AS, Bhardwaj A, Joss L, Casjens S, Cingolani G (2007a) Role of gene 10 protein in the hierarchical assembly of the bacteriophage P22 portal vertex structure. Biochemistry 46:8776–8784PubMedCrossRefGoogle Scholar
  73. Olia AS, Casjens S, Cingolani G (2007b) Structure of phage P22 cell envelope-penetrating needle. Nat Struct Mol Biol 14:1221–1226PubMedCrossRefPubMedCentralGoogle Scholar
  74. Olia AS, Prevelige PE Jr, Johnson JE, Cingolani G (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18:597–603PubMedPubMedCentralCrossRefGoogle Scholar
  75. Oliveira L, Henriques AO, Tavares P (2006) Modulation of the viral ATPase activity by the portal protein correlates with DNA packaging efficiency. J Biol Chem 281:21914–21923PubMedCrossRefGoogle Scholar
  76. Oliveira L, Cuervo A, Tavares P (2010) Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. J Biol Chem 285:7366–7373PubMedPubMedCentralCrossRefGoogle Scholar
  77. Orlova EV, Dube P, Beckmann E, Zemlin F, Lurz R, Trautner TA, Tavares P, van Heel M (1999) Structure of the 13-fold symmetric portal protein of bacteriophage SPP1. Nature Struct Biol 6:842–846PubMedCrossRefGoogle Scholar
  78. Orlova EV, Gowen B, Dröge A, Stiege A, Weise F, Lurz R, van Heel M, Tavares P (2003) Structure of a viral DNA gatekeeper at 10 Å resolution by cryo-electron microscopy. EMBO J 22:1255–1262PubMedPubMedCentralCrossRefGoogle Scholar
  79. Parker ML, Eiserling FA (1983) Bacteriophage SPO1 structure and morphogenesis. I. Tail structure and length regulation. J Virol 46:239–249PubMedPubMedCentralGoogle Scholar
  80. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR (2009a) The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci U S A 106:4160–4165PubMedPubMedCentralCrossRefGoogle Scholar
  81. Pell LG, Liu A, Edmonds L, Donaldson LW, Howell PL, Davidson AR (2009b) The X-ray crystal structure of the phage lambda tail terminator protein reveals the biologically relevant hexameric ring structure and demonstrates a conserved mechanism of tail termination among diverse long-tailed phages. J Mol Biol 389:938–951PubMedCrossRefGoogle Scholar
  82. Perucchetti R, Parris W, Becker A, Gold M (1988) Late stages in bacteriophage lambda head morphogenesis: in vitro studies on the action of the bacteriophage lambda D-gene and W-gene products. Virology 165:103–114PubMedCrossRefGoogle Scholar
  83. Plisson C, White HE, Auzat I, Zafarani A, São-José C, Lhuillier S, Tavares P, Orlova EV (2007) Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO J 26:2728–3720CrossRefGoogle Scholar
  84. Rao VB, Feiss M (2015) Mechanisms of DNA packaging by large double-stranded DNA viruses. Annu Rev Virol 2:351–378PubMedPubMedCentralCrossRefGoogle Scholar
  85. Saigo K (1975) Tail-DNA connection and chromosome structure in bacteriophage T5. Virology 68:154–165PubMedCrossRefGoogle Scholar
  86. São-José C, Lhuillier S, Lurz R, Melki R, Lepault J, Santos MA, Tavares P (2006) The ectodomain of the viral receptor YueB forms a fiber that triggers DNA ejection of bacteriophage SPP1 DNA. J Biol Chem 281:11464–11470PubMedCrossRefGoogle Scholar
  87. São-José C, de Frutos M, Raspaud E, Santos MA, Tavares P (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 374:346–355PubMedCrossRefGoogle Scholar
  88. Sborgi L, Verma A, Muñoz V, de Alba E (2011) Revisiting the NMR structure of the ultrafast downhill folding protein gpW from bacteriophage λ. PLoS One 6:e26409PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 ϕ29 DNA packaging motor. Nature 408:745–750PubMedPubMedCentralCrossRefGoogle Scholar
  90. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C (2001) The bacteriophage ϕ29 portal motor can package DNA against a large internal force. Nature 413:748–752PubMedCrossRefGoogle Scholar
  91. Spinelli S, Veesler D, Bebeacua C, Cambillau C (2014) Structures and host-adhesion mechanisms of lactococcal siphophages. Front Microbiol 5:3PubMedPubMedCentralCrossRefGoogle Scholar
  92. Stockdale SR, Collins B, Spinelli S, Douillard FP, Mahony J, Cambillau C, van Sinderen D (2015) Structure and Assembly of TP901-1 Virion Unveiled by Mutagenesis. PLoS One 10:e0131676PubMedPubMedCentralCrossRefGoogle Scholar
  93. Strauss H, King J (1984) Steps in the stabilisation of newly packaged DNA during phage P22 morphogenesis. J Mol Biol 172:523–543PubMedCrossRefGoogle Scholar
  94. Sun L, Zhang X, Gao S, Rao PA, Padilla-Sanchez V, Chen Z, Sun S, Xiang Y, Subramaniam S, Rao VB, Rossmann MG (2015) Cryo-EM structure of the bacteriophage T4 portal protein assembly at near-atomic resolution. Nat Commun 6:7548PubMedPubMedCentralCrossRefGoogle Scholar
  95. Tang J, Olson N, Jardine PJ, Grimes S, Anderson DL, Baker TS (2008) DNA poised for release in bacteriophage phi29. Structure 16:935–943PubMedPubMedCentralCrossRefGoogle Scholar
  96. Tang J, Lander GC, Olia AS, Li R, Casjens S, Prevelige P Jr, Cingolani G, Baker TS, Johnson JE (2011) Peering down the barrel of a bacteriophage portal: the genome packaging and release valve in P22. Structure 19:496–502PubMedPubMedCentralCrossRefGoogle Scholar
  97. Tavares P, Lurz R, Stiege A, Rückert B, Trautner TA (1996) Sequential headful packaging and fate of the cleaved DNA ends in bacteriophage SPP1. J Mol Biol 264:954–967PubMedCrossRefPubMedCentralGoogle Scholar
  98. Tavares P, Zinn-Justin S, Orlova EV (2012) Genome gating in tailed bacteriophage capsids. Adv Exp Med Biol 726:585–600PubMedCrossRefPubMedCentralGoogle Scholar
  99. Thomas JO (1974) Chemical linkage of the tail to the right-hand end of bacteriophage lambda DNA. J Mol Biol 87:1–9PubMedCrossRefGoogle Scholar
  100. Thomas JO, Sternberg N, Weisberg R (1978) Altered arrangement of the DNA in injection-defective lambda bacteriophage. J Mol Biol 123:149–161PubMedCrossRefGoogle Scholar
  101. Trus BL, Cheng N, Newcomb WW, Homa FL, Brown JC, Steven AC (2004) Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J Virol 78:12668–12671PubMedPubMedCentralCrossRefGoogle Scholar
  102. Trus BL, Newcomb WW, Cheng N, Cardone G, Marekov L, Homa FL, Brown JC, Steven AC (2007) Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-Filled HSV-1 capsids. Mol Cell 26:479–489PubMedPubMedCentralCrossRefGoogle Scholar
  103. Veesler D, Cambillau C (2011) A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol Mol Biol Rev 75:423–433PubMedPubMedCentralCrossRefGoogle Scholar
  104. Vianelli A, Wang GR, Gingery M, Duda RL, Eiserling FA, Goldberg EB (2000) Bacteriophage T4 self-assembly: localization of gp3 and its role in determining tail length. J Bacteriol 182:680–688PubMedPubMedCentralCrossRefGoogle Scholar
  105. Vinga I, São-José C, Tavares P, Santos MA (2006) Bacteriophage entry in the host cell. In: Wegrzyn G (ed) Modern bacteriophage biology and biotechnology. Research Signpost, KeralaGoogle Scholar
  106. 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 25:5229–5239PubMedPubMedCentralCrossRefGoogle Scholar
  107. Zhao L, Kanamaru S, Chaidirek C, Arisaka F (2003) P15 and P3, the tail completion proteins of bacteriophage T4, both form hexameric rings. J Bacteriol 185:1693–1700PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Virology, Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ Paris-SudUniversité Paris-SaclayGif-sur-YvetteFrance

Personalised recommendations