Skip to main content

Genome Gating in Tailed Bacteriophage Capsids

  • Chapter
  • First Online:
Viral Molecular Machines

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 726))

Abstract

Tailed bacteriophages use a portal system for genome entry and exit from viral capsids. Here, we review the mechanisms how these movements are controlled by the genome gatekeeper that assembles at the portal structure. Phage DNA is packaged at high pressure inside the viral capsid by a powerful motor. The viral genome is translocated through the central channel of the portal protein found at a single vertex of the capsid. Packaging is normally terminated by endonucleolytic cleavage of the substrate DNA followed by disassembly of the packaging motor and closure of the portal system, preventing leakage of the viral genome. This can be achieved either by conformational changes in the portal protein or by sequential addition of proteins that extend the portal channel (adaptors) and physically close it preventing DNA exit (stoppers). The resulting connector structure provides the interface for assembly of short tails (podoviruses) or for attachment of preformed long tails (siphoviruses and myoviruses). The connector maintains the viral DNA correctly positioned for ejection that is triggered by interaction of the phage particle with bacterial receptors. Recent exciting advances are providing new molecular insights on the mechanisms that ensure precise coordination of these critical steps required both for stable viral genome packaging and for its efficient release to initiate infection.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    Please note that some authors use the term “connector” to designate exclusively the portal protein.

References

  • Abuladze NK, Gingery M, Tsai J, Eiserling FA (1994) Tail length determination in bacteriophage T4. Virology 199:301–310

    Article  PubMed  CAS  Google Scholar 

  • Adams MB, Hayden M, Casjens S (1983) On the sequential packaging of bacteriophage P22 DNA. J Virol 46:673–677

    PubMed  CAS  Google Scholar 

  • 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 24:3820–3829

    Article  PubMed  CAS  Google Scholar 

  • Andres D, Hanke C, Baxa U, Seul A, Barbirz S, Seckler R (2010) Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro. J Biol Chem 285:36768–36775

    Article  PubMed  CAS  Google Scholar 

  • Bamford DH, Grimes JM, Stuart DI (2005) What does structure tell us about virus evolution? Curr Opin Struct Biol 15:655–663

    Article  PubMed  CAS  Google Scholar 

  • Bazinet C, King J (1985) The DNA translocating vertex of dsDNA bacteriophage. Annu Rev Microbiol 39:109–129

    Article  PubMed  CAS  Google Scholar 

  • 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 371:374–387

    Article  PubMed  CAS  Google Scholar 

  • 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 391:227–245

    Article  PubMed  CAS  Google Scholar 

  • Black LW (1989) DNA packaging in dsDNA bacteriophages. Annu Rev Microbiol 43:267–292

    Article  PubMed  CAS  Google Scholar 

  • Böhm J, Lambert O, Frangakis AS, Letellier L, Baumeister W, Rigaud JL (2001) FhuA-mediated phage genome transfer into liposomes: a cryo-electron tomography study. Curr Biol 11:1168–1175

    Article  PubMed  Google Scholar 

  • Boulanger P, le Maire M, Bonhivers M, Dubois S, Desmadril M, Letellier L (1996) Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry 35:14216–14224

    Article  PubMed  CAS  Google Scholar 

  • Camacho AC, Gual A, Lurz R, Tavares P, Alonso JC (2003) Bacillus subtilis bacteriophage SPP1 DNA packaging motor requires terminase and portal proteins. J Biol Chem 278:23251–23259

    Article  PubMed  CAS  Google Scholar 

  • 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 395:754–768

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 107:14384–14389

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 108(25):10168–10173

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Hayden M (1988) Analysis in vivo of the bacteriophage P22 headful nuclease. J Mol Biol 199:467–474

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Hendrix R (1988) Control mechanisms in dsDNA bacteriophage assembly. In: Calendar R (ed) The bacteriophages, vol 1. Plenum Press, New York

    Google Scholar 

  • Casjens S, Horn T, Kaiser AD (1972) Head assembly steps controlled by genes F and W in bacteriophage lambda. J Mol Biol 64:551–563

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Wyckoff E, Hayden M, Sampson L, Eppler K, Randall S, Moreno E, Serwer P (1992) Bacteriophage P22 portal protein is part of the gauge that regulates packing density of intravirion DNA. J Mol Biol 224:1055–1074

    Article  PubMed  CAS  Google Scholar 

  • 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 14:1073–1082

    Article  PubMed  CAS  Google Scholar 

  • Chang JT, Schmid MF, Haase-Pettingell C, Weigele PR, King JA, Chiu W (2010) Visualizing the structural changes of bacteriophage epsilon 15 and its Salmonella host during infection. J Mol Biol 402:731–740

    Article  PubMed  CAS  Google Scholar 

  • Chattoraj DK, Inman RB (1974) Location of DNA ends in P2, 186, P4 and lambda bacteriophage heads. J Mol Biol 87:11–22

    Article  PubMed  CAS  Google Scholar 

  • Cingolani G, Moore SD, Prevelige PE Jr, Johnson JE (2002) Preliminary crystallographic analysis of the bacteriophage P22 portal protein. J Struct Biol 139:46–54

    Article  PubMed  CAS  Google Scholar 

  • 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 201:91–100

    Article  PubMed  CAS  Google Scholar 

  • Dube P, Tavares P, Lurz R, van Heel M (1993) Bacteriophage SPP1 portal protein: a DNA pump with 13-fold symmetry. EMBO J 12:1303–1309

    PubMed  CAS  Google Scholar 

  • 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 365:175–186

    Article  PubMed  CAS  Google Scholar 

  • Effantin G, Boulanger P, Neumann E, Letellier L, Conway JF (2006) Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J Mol Biol 361:993–1002

    Article  PubMed  CAS  Google Scholar 

  • Evilevitch A, Lavelle L, Knobler CM, Raspaud E, Gelbart WM (2003) Osmotic pressure inhibition of DNA ejection from phage. Proc Natl Acad Sci USA 100:9292–9295

    Article  PubMed  CAS  Google Scholar 

  • Feiss M, Catalano CE (2005) Bacteriophage lambda terminase and the mechanism of viral DNA packaging. In: Catalano CE (ed) Viral genome packaging machines: genetics, structure, and mechanism. Landes Bioscience, Georgetown, TX

    Google Scholar 

  • Feiss M, Siegele DA (1979) Packaging of the bacteriophage lambda chromosome: dependence of cos cleavage on chromosome length. Virology 92:190–200

    Article  PubMed  CAS  Google Scholar 

  • Feiss M, Sippy J, Miller G (1985) Processive action of terminase during sequential packaging of bacteriophage λ chromosomes. J Mol Biol 186:759–771

    Article  PubMed  CAS  Google Scholar 

  • Fokine A, Chipman PR, Leiman PG, Mesyanzhinov VV, Rao VB, Rossmann MG (2004) Molecular architecture of the prolate head of bacteriophage T4. Proc Natl Acad Sci USA 101:6003–6008

    Article  PubMed  CAS  Google Scholar 

  • Fujisawa H, Morita M (1997) Phage DNA packaging. Genes Cells 2:537–545

    Article  PubMed  CAS  Google Scholar 

  • 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 357:1154–1166

    Article  PubMed  CAS  Google Scholar 

  • 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 315:663–676

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto C, Fujisawa H (1992) DNA sequences necessary for packaging bacteriophage T3 DNA. Virology 187:788–795

    Article  PubMed  CAS  Google Scholar 

  • Hoffman B, Levine M (1975) Bacteriophage P22 virion protein which performs an essential early function. II. Characterization of the gene 16 function. J Virol 16:1547–1559

    PubMed  CAS  Google Scholar 

  • Isidro A, Henriques AO, Tavares P (2004a) The portal protein plays essential roles at different steps of the SPP1 DNA packaging process. Virology 322:253–263

    Article  PubMed  CAS  Google Scholar 

  • Isidro A, Santos MA, Henriques AO, Tavares P (2004b) The high-resolution functional map of bacteriophage SPP1 portal protein. Mol Microbiol 51:949–962

    Article  PubMed  CAS  Google Scholar 

  • Jiang W, Chang J, Jakana J, Weigele P, King J, Chiu W (2006) Structure of epsilon 15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439:612–661

    Article  PubMed  CAS  Google Scholar 

  • Johnson JE, Chiu W (2007) DNA packaging and delivery machines in tailed bacteriophages. Curr Opin Struct Biol 17:237–243

    Article  PubMed  CAS  Google Scholar 

  • Katsura I (1987) Determination of bacteriophage lambda tail length by a protein ruler. Nature 327:73–75

    Article  PubMed  CAS  Google Scholar 

  • Kostyuchenko VA, Chipman PR, Leiman PG, Arisaka F, Mesyanzhinov VV, Rossmann MG (2005) The tail structure of bacteriophage T4 and its mechanism of contraction. Nat Struct Mol Biol 12:810–813

    Article  PubMed  CAS  Google Scholar 

  • 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 312:1791–1795

    Article  PubMed  CAS  Google Scholar 

  • 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 26:1984–1994

    Article  PubMed  CAS  Google Scholar 

  • 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 118:419–429

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 106:8507–8512

    Article  PubMed  CAS  Google Scholar 

  • 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 17:830–836

    Article  PubMed  CAS  Google Scholar 

  • 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 310:1027–1037

    Article  PubMed  CAS  Google Scholar 

  • Mangenot S, Hochrein M, Radler J, Letellier L (2005) Real-time imaging of DNA ejection from single phage particles. Curr Biol 15:430–435

    Article  PubMed  CAS  Google Scholar 

  • 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 275:18879–18886

    Article  PubMed  CAS  Google Scholar 

  • 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 308:9–14

    Article  PubMed  CAS  Google Scholar 

  • 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 318:1395–1404

    Article  PubMed  CAS  Google Scholar 

  • Moore SD, Prevelige PE Jr (2001) Structural transformations accompanying the assembly of bacteriophage P22 portal protein rings in vitro. J Biol Chem 276:6779–6788

    Article  PubMed  CAS  Google Scholar 

  • Moore SD, Prevelige PE Jr (2002) Bacteriophage P22 portal vertex formation in vivo. J Mol Biol 315:975–994

    Article  PubMed  CAS  Google Scholar 

  • Murata K, Liu X, Danev R, Jakana J, Schmid MF, King J, Nagayama K, Chiu W (2010) Zernike phase contrast cryo-electron microscopy and tomography for structure determination at nanometer and subnanometer resolutions. Structure 18:903–912

    Article  PubMed  CAS  Google Scholar 

  • Newcomb WW, Juhas RM, Thomsen DR, Homa FL, Burch AD, Weller SK, Brown JC (2001) The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J Virol 75:10923–10932

    Article  PubMed  CAS  Google Scholar 

  • 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 363:558–576

    Article  PubMed  CAS  Google Scholar 

  • 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 46:8776–8784

    Article  PubMed  CAS  Google Scholar 

  • Olia AS, Casjens S, Cingolani G (2007b) Structure of phage P22 cell envelope-penetrating needle. Nat Struct Mol Biol 14:1221–1226

    Article  PubMed  CAS  Google Scholar 

  • Olia AS, Prevelige PE Jr, Johnson JE, Cingolani G (2011) Three-dimensional structure of a viral genome-delivery portal vertex. Nat Struct Mol Biol 18:597–603

    Article  PubMed  CAS  Google Scholar 

  • 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 281:21914–21923

    Article  PubMed  CAS  Google Scholar 

  • Oliveira L, Cuervo A, Tavares P (2010) Direct interaction of the bacteriophage SPP1 packaging ATPase with the portal protein. J Biol Chem 285:7366–7373

    Article  PubMed  CAS  Google Scholar 

  • 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. Nat Struct Biol 6:842–846

    Article  PubMed  CAS  Google Scholar 

  • 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 22:1255–1262

    Article  PubMed  CAS  Google Scholar 

  • Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR (2009) 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 USA 106:4160–4165

    Article  PubMed  CAS  Google Scholar 

  • 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 165:103–114

    Article  PubMed  CAS  Google Scholar 

  • 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 26:2728–3720

    Article  Google Scholar 

  • Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. Annu Rev Genet 42:647–681

    Article  PubMed  CAS  Google Scholar 

  • Roessner CA, Struck DK, Ihler GM (1983) Injection of DNA into liposomes by bacteriophage lambda. J Biol Chem 258:643–648

    PubMed  CAS  Google Scholar 

  • Rossmann MG, Mesyanzhinov VV, Arisaka F, Leiman PG (2004) The bacteriophage T4 DNA injection machine. Curr Opin Struct Biol 14:171–180

    Article  PubMed  CAS  Google Scholar 

  • Salas M (2006) Phage φ29 and its relatives. In: Calendar R (ed) The bacteriophages, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • 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 281:11464–11470

    Article  PubMed  Google Scholar 

  • 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 374:346–355

    Article  PubMed  Google Scholar 

  • Sciara G, Bebeacua C, Bron P, Tremblay D, Ortiz-Lombardia M, Lichière J, van Heel M, Campanacci V, Moineau S, Cambillau C (2010) Structure of lactococcal phage p2 baseplate and its mechanism of activation. Proc Natl Acad Sci USA 107:6852–6857

    Article  PubMed  CAS  Google Scholar 

  • 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 408:745–750

    Article  PubMed  CAS  Google Scholar 

  • 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 413:748–752

    Article  PubMed  CAS  Google Scholar 

  • Strauss H, King J (1984) Steps in the stabilisation of newly packaged DNA during phage P22 morphogenesis. J Mol Biol 172:523–543

    Article  PubMed  CAS  Google Scholar 

  • Streisinger G, Emrich J, Stahl MM (1967) Chromosome structure in phage T4, iii. Terminal redundancy and length determination. Proc Natl Acad Sci USA 57:292–295

    Article  PubMed  CAS  Google Scholar 

  • 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 135:1251–1262

    Article  PubMed  CAS  Google Scholar 

  • Tang L, Marion WR, Cingolani G, Prevelige PE, Johnson JE (2005) Three-dimensional structure of the bacteriophage P22 tail machine. EMBO J 24:2087–2095

    Article  PubMed  CAS  Google Scholar 

  • Tang J, Olson N, Jardine PJ, Grimes S, Anderson DL, Baker TS (2008) DNA poised for release in bacteriophage phi29. Structure 16:935–943

    Article  PubMed  CAS  Google Scholar 

  • Tang J, Lander GC, Olia A, 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 19:496–502

    Article  PubMed  CAS  Google Scholar 

  • Tavares P, Santos MA, Lurz R, Morelli G, de Lencastre H, Trautner TA (1992) Identification of a gene in Bacillus subtilis bacteriophage SPP1 determining the amount of packaged DNA. J Mol Biol 225:81–92

    Article  PubMed  CAS  Google Scholar 

  • 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 264:954–967

    Article  PubMed  CAS  Google Scholar 

  • Thomas JO (1974) Chemical linkage of the tail to the right-hand end of bacteriophage lambda DNA. J Mol Biol 87:1–9

    Article  PubMed  CAS  Google Scholar 

  • Thomas JO, Sternberg N, Weisberg R (1978) Altered arrangement of the DNA in injection-defective lambda bacteriophage. J Mol Biol 123:149–161

    Article  PubMed  CAS  Google Scholar 

  • Tosi F, Labedan B, Legault-Démare J (1984) Analysis of the coliphage T5 DNA ejection process with free and liposome-associated TonA protein. J Virol 50:213–219

    PubMed  CAS  Google Scholar 

  • 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 78:12668–12671

    Article  PubMed  CAS  Google Scholar 

  • Tye BK, Huberman JA, Botstein D (1974) Non-random circular permutation of phage P22 DNA. J Mol Biol 85:501–532

    Article  PubMed  CAS  Google Scholar 

  • Valpuesta JM, Carrascosa JL (1994) Structure of viral connectors and their function in bacteriophage assembly and DNA packaging. Q Rev Biophys 27:107–155

    Article  PubMed  CAS  Google Scholar 

  • Valpuesta JM, Fujisawa H, Marco S, Carazo JM, Carrascosa JL (1992) Three-dimensional structure of T3 connector purified from overexpressing bacteria. J Mol Biol 224:103–112

    Article  PubMed  CAS  Google Scholar 

  • 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 15:4785–4788

    PubMed  Google Scholar 

  • Veesler D, Robin G, Lichière J, Auzat I, Tavares P, Bron P, Campanacci V, Cambillau C (2010) Crystal structure of bacteriophage SPP1 distal tail protein (gp 19.1): a baseplate hub paradigm in gram-positive infecting phages. J Biol Chem 285:36666–36673

    Article  PubMed  CAS  Google Scholar 

  • 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, Kerala, India

    Google Scholar 

  • 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 25:5229–5239

    Article  PubMed  CAS  Google Scholar 

  • 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 29:376–383

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are most thankful to Marie-Christine Vaney (Institut Pasteur, Paris) for the invaluable help to prepare Figs. 25.325.7. Work in our laboratories is supported by institutional funding from the CNRS (P.T and S.Z.-J.), the CEA (S.Z.-J.), the ANR grant “DNA Gating” (ANR-09-BLAN-0149-01), and the BBRSC (E.V.O.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paulo Tavares .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Tavares, P., Zinn-Justin, S., Orlova, E.V. (2012). Genome Gating in Tailed Bacteriophage Capsids. In: Rossmann, M., Rao, V. (eds) Viral Molecular Machines. Advances in Experimental Medicine and Biology, vol 726. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-0980-9_25

Download citation

Publish with us

Policies and ethics