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The Bacteriophage DNA Packaging Machine

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Viral Molecular Machines

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

Abstract

Large dsDNA bacteriophages and herpesviruses encode a powerful ATP-driven DNA-translocating machine that encapsidates a viral genome into a preformed capsid shell or prohead. The key components of the packaging machine are the packaging enzyme (terminase, motor) and the portal protein that forms the unique DNA entrance vertex of prohead. The terminase complex, comprised of a recognition subunit (small terminase) and an endonuclease/translocase subunit (large terminase), cuts viral genome concatemers. The terminase–viral DNA complex docks on the portal vertex, assembling a motor complex containing five large terminase subunits. The pentameric motor processively translocates DNA until the head shell is full with one viral genome. The motor cuts the DNA again and dissociates from the full head, allowing head-finishing proteins to assemble on the portal, sealing the portal, and constructing a platform for tail attachment. A body of evidence from molecular genetics and biochemical, structural, and biophysical approaches suggests that ATP hydrolysis–driven conformational changes in the packaging motor (large terminase) power DNA motion. Various parts of the motor subunit, such as the ATPase, arginine finger, transmission domain, hinge, and DNA groove, work in concert to translocate about 2 bp of DNA per ATP hydrolyzed. Powerful single-molecule approaches are providing precise delineation of steps during each translocation event in a motor that has a speed as high as a millisecond/step. The phage packaging machine has emerged as an excellent model for understanding the molecular machines, given the mechanistic parallels between terminases, helicases, and numerous motor proteins.

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References

  • 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 461:669–673

    Article  PubMed  CAS  Google Scholar 

  • Alam TI, Draper B, Kondabagil K, Rentas FJ, Ghosh-Kumar M, Sun S, Rossmann MG, Rao VB (2008) The headful packaging nuclease of bacteriophage T4. Mol Microbiol 69:1180–1190

    PubMed  CAS  Google Scholar 

  • Al-Zahrani AS, Kondabagil K, Gao S, Kelly N, Ghosh-Kumar M, Rao VB (2009) The small terminase, gp16, of bacteriophage T4 is a regulator of the DNA packaging motor. J Biol Chem 284:24490–24500

    Article  PubMed  CAS  Google Scholar 

  • Arens JS, Hang Q, Hwang Y, Tuma B, Max S (1999) Mutations that extend the specificity of the endonuclease activity of lambda terminase. J Bacteriol 181:218–224

    PubMed  CAS  Google Scholar 

  • Baumann RG, Mullaney J, Black LW (2006) Portal fusion protein constraints on function in DNA packaging of bacteriophage T4. Mol Microbiol 61:16–32

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Hendrix R (1988) Control mechanisms in dsDNA bacteriophage assembly. In: Calendar R (ed) The bacteriophages, 1st edn. Plenum, New York, pp 15–91

    Google Scholar 

  • Casjens S, Huang WM, Hayden M, Parr R (1987) Initiation of bacteriophage P22 DNA packaging series. Analysis of a mutant that alters the DNA target specificity of the packaging apparatus. J Mol Biol 194:411–422

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Sampson L, Randall S, Eppler K, Wu H, Petri JB, Schmieger H (1992a) Molecular genetic analysis of bacteriophage P22 gene 3 product, a protein involved in the initiation of headful DNA packaging. J Mol Biol 227:1086–1099

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Wyckoff E, Hayden M, Sampson L, Eppler K, Randall S, Moreno ET, Serwer P (1992b) 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 

  • Catalano CE, Cue D, Feiss M (1995) Virus DNA packaging: the strategy used by phage lambda. Mol Microbiol 16:1075–1086

    Article  PubMed  CAS  Google Scholar 

  • Chai S, Lurz R, Alonso JC (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 252:386–398

    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 

  • Comolli LR, Spakowitz AJ, Siegerist CE, Jardine PJ, Grimes S, Anderson DL, Bustamante C, Downing KH (2008) Three-dimensional architecture of the bacteriophage phi29 packaged genome and elucidation of its packaging process. Virology 371:267–277

    Article  PubMed  CAS  Google Scholar 

  • Cordin O, Tanner NK, Doere M, Linder P, Banroques J (2004) The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. EMBO J 23:2478–2487

    Article  PubMed  CAS  Google Scholar 

  • Cordin O, Banroques J, Tanner NK, Linder P (2006) The DEAD-box protein family of RNA helicases. Gene 367:17–37

    Article  PubMed  CAS  Google Scholar 

  • Davidson A, Gold M (1992) Mutations abolishing the endonuclease activity of bacteriophage lambda terminase lie in two distinct regions of the A gene, one of which may encode a leucine zipper DNA binding domain. Virology 161:305–315

    Article  Google Scholar 

  • de Beer T, Ortega M, Berton N, Yang Q, Overduin M, Catalano CE (2000) Assignment of the 1H, 13C, and 15N resonances of the DNA binding domain of gpNu1, a genome packaging protein from bacteriophage lambda. J Biomol NMR 18:69–70

    Article  PubMed  Google Scholar 

  • de Beer T, Fang J, Ortega M, Yang Q, Maes L, Duffy C, Berton N, Sippy J, Overduin M, Feiss M, Catalano CE (2002) Insights into specific DNA recognition during the assembly of a viral genome packaging machine. Mol Cell 9:981–991

    Article  PubMed  Google Scholar 

  • Dhar A, Feiss M (2005) Bacteriophage lambda terminase: alterations of the high-affinity ATPase affect viral DNA packaging. J Mol Biol 347:71–80

    Article  PubMed  CAS  Google Scholar 

  • 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(18):7357–7362

    Article  PubMed  CAS  Google Scholar 

  • 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 369:79–94

    Article  PubMed  CAS  Google Scholar 

  • Duffy C, Feiss M (2002) The large subunit of bacteriophage lambda’s terminase plays a role in DNA translocation and packaging termination. J Mol Biol 316:547–561

    Article  PubMed  CAS  Google Scholar 

  • Earnshaw WC, Casjens SR (1980) DNA packaging by the double-stranded DNA bacteriophages. Cell 21:319–331

    Article  PubMed  CAS  Google Scholar 

  • Evilevitch A, Fang LT, Yoffe AM, Castelnovo M, Rau DC, Parsegian VA, Gelbart WM, Knobler CM (2008) Effects of salt concentrations and bending energy on the extent of ejection of phage genomes. Biophys J 94:1110–1120

    Article  PubMed  CAS  Google Scholar 

  • Feiss M, Bublitz A (1975) Polarized packaging of bacteriophage lambda chromosomes. J Mol Biol 94:583–594

    Article  PubMed  CAS  Google Scholar 

  • Feiss M, Reynolds E, Schrock M, Sippy J (2010) DNA packaging by lambda-like bacteriophages: mutations broadening the packaging specificity of terminase, the lambda-packaging enzyme. Genetics 184:43–52

    Article  PubMed  CAS  Google Scholar 

  • Frackman S, Siegele DA, Feiss M (1985) The terminase of bacteriophage lambda. Functional domains for cosB binding and multimer assembly. J Mol Biol 183:225–238

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fuller DN, Raymer DM, Kottadiel VI, Rao VB, Smith DE (2007a) Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc Natl Acad Sci USA 104:16868–16873

    Article  PubMed  CAS  Google Scholar 

  • Fuller DN, Raymer DM, Rickgauer JP, Robertson RM, Catalano CE, Anderson DL, Grimes S, Smith DE (2007b) Measurements of single DNA molecule packaging dynamics in bacteriophage lambda reveal high forces, high motor processivity, and capsid transformations. J Mol Biol 373:1113–1122

    Article  PubMed  CAS  Google Scholar 

  • Gao S, Rao VB (2011) Specificity of interactions among the DNA-packaging machine components of T4-related bacteriophages. J Biol Chem 286:3944–3956

    Article  PubMed  CAS  Google Scholar 

  • Ghosh-Kumar M, Alam TI, Draper B, Stack JD, Rao VB (2011) Regulation by interdomain communication of a headful packaging nuclease from bacteriophage T4. Nucleic Acids Res 39:2742–2755

    Article  PubMed  CAS  Google Scholar 

  • Goetzinger K, Rao V (2003) Defining the ATPase center of bacteriophage T4 DNA packaging machine: requirement for a catalytic glutamate residue in the large terminase protein gp17. J Mol Biol 331:139–154

    Article  PubMed  CAS  Google Scholar 

  • Grimes S, Jardine PJ, Anderson D (2002) Bacteriophage phi 29 DNA packaging. Adv Virus Res 58:255–294

    Article  PubMed  CAS  Google Scholar 

  • Grimes S, Ma, S, Gao J, Atz R, Jardine P (2011) Role of the ø29 connector channel loops in late-stage DNA packaging. J Mol Biol 410:50–59

    Google Scholar 

  • Gual A, Alonso JC (1998) Characterization of the small subunit of the terminase enzyme of the Bacillus subtilis bacteriophage SPP1. Virology 242:279–287

    Article  PubMed  CAS  Google Scholar 

  • 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 83:3505–3509

    Article  PubMed  CAS  Google Scholar 

  • Guo PX, Erickson S, Anderson D (1987) A small viral RNA is required for in vitro packaging of bacteriophage phi 29 DNA. Science (New York, NY) 236:690–694

    Article  CAS  Google Scholar 

  • Hang Q, Tack B, Feiss M (2000) An ATPase center of bacteriophage lambda terminase involved in post-cleavage stages of DNA packaging: identification of ATP-interactive amino acids. J Mol Biol 302:777–795

    Article  PubMed  CAS  Google Scholar 

  • Huang RK, Khayat R, Lee KK, Gertsman I, Duda RL, Hendrix RW, Johnson JE (2011) The Prohead-I structure of bacteriophage HK97: implications for scaffold-mediated control of particle assembly and maturation. J Mol Biol 408:541–554

    Article  PubMed  CAS  Google Scholar 

  • Hwang Y, Feiss M (1996) Mutations affecting the high affinity ATPase center of gpA, the large subunit of bacteriophage lambda terminase, inactivate the endonuclease activity of terminase. J Mol Biol 261:524–535

    Article  PubMed  CAS  Google Scholar 

  • Hwang Y, Feiss M (2000) The endonuclease and helicase activities of bacteriophage lambda terminase: changing nearby residue 515 restores activity to the gpA K497D mutant enzyme. Virology 277:204–214

    Article  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 

  • Iyer LM, Makarova KS, Koonin EV, Aravind L (2004) 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 32:5260–5279

    Article  PubMed  CAS  Google Scholar 

  • Jing P, Haque F, Shu D, Guo P (2010) One-way traffic of a viral motor channel for double-stranded DNA translocation. Nano Lett 10(9):3620–3627

    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 

  • Kanamaru S, Kondabagil K, Rossmann MG, Rao VB (2004) The functional domains of bacteriophage T4 terminase. J Biol Chem 279:40795–40801

    Article  PubMed  CAS  Google Scholar 

  • Katsura I (1989) Structure and inherent properties of the bacteriophage lambda head shell. VI. DNA-packaging-defective mutants in the major capsid protein. J Mol Biol 205:397–405

    Article  PubMed  CAS  Google Scholar 

  • Kondabagil KR, Rao VB (2006) A critical coiled coil motif in the small terminase, gp16, from bacteriophage T4: insights into DNA packaging initiation and assembly of packaging motor. J Mol Biol 358:67–82

    Article  PubMed  CAS  Google Scholar 

  • Kuebler D, Rao VB (1998) Functional analysis of the DNA-packaging/terminase protein gp17 from bacteriophage T4. J Mol Biol 281:803–814

    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 AA, Orlova EV, Turner J, Dodson EJ, Tavares P, Antson AA (2007) Structural framework for DNA translocation via the viral portal protein. EMBO J 26:1984–1994

    Article  PubMed  CAS  Google Scholar 

  • Lee KK, Gan L, Tsuruta H, Moyer C, Conway JF, Duda RL, Hendrix RW, Steven AC, Johnson JE (2008) Virus capsid expansion driven by the capture of mobile surface loops. Structure 16:1491–1502

    Article  PubMed  CAS  Google Scholar 

  • Lin H, Black LW (1998) DNA requirements in vivo for phage T4 packaging. Virology 242:118–127

    Article  PubMed  CAS  Google Scholar 

  • Lin H, Simon MN, Black LW (1997) Purification and characterization of the small subunit of phage T4 terminase, gp16, required for DNA packaging. J Biol Chem 272:3495–3501

    Article  PubMed  CAS  Google Scholar 

  • Maluf N, Yang Q, Catalano C (2005) Self-association properties of the bacteriophage lambda terminase holoenzyme: implications for the DNA packaging motor. J Mol Biol 347:523–542

    Article  PubMed  CAS  Google Scholar 

  • Maluf N, Gaussier H, Bogner E, Feiss M, Catalano C (2006) Assembly of bacteriophage lambda terminase into a viral DNA maturation and packaging machine. Biochemistry 45:15259–15268

    Article  PubMed  CAS  Google Scholar 

  • Mitchell MS, Rao VB (2004) Novel and deviant Walker A ATP-binding motifs in bacteriophage large terminase-DNA packaging proteins. Virology 321:217–221

    Article  PubMed  CAS  Google Scholar 

  • Mitchell MS, Rao VB (2006) Functional analysis of the bacteriophage T4 DNA-packaging ATPase motor. J Biol Chem 281:518–527

    Article  PubMed  CAS  Google Scholar 

  • Mitchell M, Matsuzaki S, Imai S, Rao V (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 30:4009–4021

    Article  PubMed  CAS  Google Scholar 

  • Moll WD, Guo P (2005) Translocation of nicked but not gapped DNA by the packaging motor of bacteriophage phi29. J Mol Biol 351:100–107

    Article  PubMed  CAS  Google Scholar 

  • 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 16:1267–1274

    Article  PubMed  CAS  Google Scholar 

  • Morita M, Tasaka M, Fujisawa H (1993) DNA packaging ATPase of bacteriophage T3. Virology 193:748–752

    Article  PubMed  CAS  Google Scholar 

  • Nadal M, Mas PJ, Blanco AG, Arnan C, Sola M, Hart DJ, Coll M (2010) Structure and inhibition of herpesvirus DNA packaging terminase nuclease domain. Proc Natl Acad Sci USA 107:16078–16083

    Article  PubMed  CAS  Google Scholar 

  • Nemecek D, Gilcrease EB, Kang S, Preveilige PE Jr, Casjens S, Thomas GJ Jr (2007) Subunit conformations and assembly states of a DNA-translocating motor: the terminase of bacteriophage P22. J Mol Biol 374:817–836

    Article  PubMed  CAS  Google Scholar 

  • Newcomb WW, Cockrell SK, Homa FL, Brown JC (2009) Polarized DNA ejection from the herpesvirus capsid. J Mol Biol 392:885–894

    Article  PubMed  CAS  Google Scholar 

  • Nowotny M, Yang W (2006) Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J 25:1924–1933

    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, 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, 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 

  • Oram M, Sabanayagam C, Black LW (2008) Modulation of the packaging reaction of bacteriophage T4 terminase by DNA structure. J Mol Biol 381:61–72

    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 

  • Ortega ME, Gaussier H, Catalano CE (2007) The DNA maturation domain of gpA, the DNA packaging motor protein of bacteriophage lambda, contains an ATPase site associated with endonuclease activity. J Mol Biol 373:851–865

    Article  PubMed  CAS  Google Scholar 

  • Ponchon L, Boulanger P, Labesse G, Letellier L (2006) The endonuclease domain of bacteriophage terminases belongs to the resolvase/integrase/ribonuclease H superfamily: a bioinformatics analysis validated by a functional study on bacteriophage T5. J Biol Chem 281:5829–5836

    Article  PubMed  CAS  Google Scholar 

  • Qiu X, Rau DC, Parsegian VA, Fang LT, Knobler CM, Gelbart WM (2011) Salt-Dependent DNA-DNA Spacings in Intact Bacteriophage lambda Reflect Relative Importance of DNA Self-Repulsion and Bending Energies. Phys Rev Lett 106:028102

    Article  PubMed  Google Scholar 

  • Rao VB, Black LW (1985) DNA packaging of bacteriophage T4 proheads in vitro. Evidence that prohead expansion is not coupled to DNA packaging. J Mol Biol 185:565–578

    Article  PubMed  CAS  Google Scholar 

  • Rao VB, Feiss M (2008) The bacteriophage DNA packaging motor. In: Annual review of genetics, Annual Reviews, Palo Alto, CA, pp 647–681

    Google Scholar 

  • Ray K, Sabanayagam CR, Lakowicz JR, Black LW (2010) DNA crunching by a viral packaging motor: compression of a procapsid-portal stalled Y-DNA substrate. Virology 398:224–232

    Article  PubMed  CAS  Google Scholar 

  • Rentas FJ, Rao VB (2003) Defining the bacteriophage T4 DNA packaging machine: evidence for a C-terminal DNA cleavage domain in the large terminase/packaging protein gp17. J Mol Biol 334:37–52

    Article  PubMed  CAS  Google Scholar 

  • Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of nucleotide-binding protein. Nature 250:194–199

    Article  PubMed  CAS  Google Scholar 

  • 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 26:527–537

    Article  PubMed  CAS  Google Scholar 

  • Simpson A, Tao Y, Leiman P, Badasso M, He Y, Jardine P, Olson N, Morais M, Grimes S, Anderson D, Baker T, Rossmann M (2000) Structure of the bacteriophage phi29 DNA packaging motor. Nature 408:745–750

    Article  PubMed  CAS  Google Scholar 

  • Smith D, Tans S, Smith S, Grimes S, Anderson D, Bustamante C (2001) The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature 413:748–752

    Article  PubMed  CAS  Google Scholar 

  • Smits C, Chechik M, Kovalevskiy OV, Shevtsov MB, Foster AW, Alonso JC, Antson AA (2009) Structural basis for the nuclease activity of a bacteriophage large terminase. EMBO Rep 10:592–598

    Article  PubMed  CAS  Google Scholar 

  • Sternberg N, Weisberg R (1977) Packaging of coliphage lambda DNA. II. The role of the gene D protein. J Mol Biol 117:733–759

    Article  PubMed  CAS  Google Scholar 

  • 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 25:943–949

    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 

  • Sun S, Rao VB, Rossmann MG (2010) Genome packaging in viruses. Curr Opin Struct Biol 20:114–120

    Article  PubMed  CAS  Google Scholar 

  • Tanner NK, Cordin O, Banroques J, Doere M, Linder P (2003) The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol Cell 11:127–138

    Article  PubMed  CAS  Google Scholar 

  • Tsay JM, Sippy J, Feiss M, Smith DE (2009) The Q motif of a viral packaging motor governs its force generation and communicates ATP recognition to DNA interaction. Proc Natl Acad Sci USA 106:14355–14360

    Article  PubMed  CAS  Google Scholar 

  • Tsay JM, Sippy J, Deltoro D, Andrews BT, Draper B, Rao V, Catalano CE, Feiss M, Smith DE (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(31):24282–24289

    Article  PubMed  CAS  Google Scholar 

  • Wendt J, Feiss M (2004) A fragile lattice: replacing bacteriophage l’s head stability gene D with the shp gene of phage 21 generates the Mg++-dependent virus, lambda shp. Virology 326:41–46

    Article  PubMed  CAS  Google Scholar 

  • Wu H, Sampson L, Parr R, Casjens S (2002) The DNA site utilized by bacteriophage P22 for initiation of DNA packaging. Mol Microbiol 45:1631–1646

    Article  PubMed  CAS  Google Scholar 

  • Yang K, Poon AP, Roizman B, Baines JD (2008a) Temperature-sensitive mutations in the putative herpes simplex virus type 1 terminase subunits pUL15 and pUL33 preclude viral DNA cleavage/packaging and interaction with pUL28 at the nonpermissive temperature. J Virol 82:487–494

    Article  PubMed  CAS  Google Scholar 

  • Yang Q, Maluf NK, Catalano CE (2008b) Packaging of a unit length viral genome: the role of nucleotides and the gpD decoration protein in stable nucleocapsid assembly in bacteriophage lambda. J Mol Biol 383:1037–1048

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Kottadiel VI, Vafabakhsh R, Dai L, Chemla YR, Ha T, Rao VB (2011) A promiscuous DNA packaging machine from bacteriophage T4. PLoS Biol 9:e1000592

    Article  PubMed  CAS  Google Scholar 

  • Zhao W, Morais MC, Anderson DL, Jardine PJ, Grimes S (2008) Role of the CCA bulge of prohead RNA of bacteriophage Ď•29 in DNA packaging. J Mol Biol 383:520–528

    Article  PubMed  CAS  Google Scholar 

  • Zhao H, Finch CJ, Sequeira RD, Johnson BA, Johnson JE, Casjens SR, Tang L (2010) Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine. Proc Natl Acad Sci USA 107:1971–1976

    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 

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Acknowledgments

The authors thank Bonnie Draper and Vishal Kottadiel for their assistance in preparing the figures. VBR thanks Michael Rossmann and Siyang Sun for many thoughtful discussions over the years. Special thanks for our present and former lab members for their contributions, and our apologies to colleagues whose work could not be cited due to space limitations. The research in the authors’ laboratories has been funded by National Science Foundation (M.F. MCB-0717620 and VBR MCB-0110574, 423528, 0923873) and National Institutes of Health (MF GM-51611 and VBR NIAID-R56AI081726, NIBIB-EB009869).

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Authors and Affiliations

  1. Department of Microbiology, Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, IA, 52242, USA

    Michael Feiss

  2. Department of Biology, The Catholic University of America, Washington, DC, 20064, USA

    Venigalla B. Rao

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  1. Michael Feiss
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  2. Venigalla B. Rao
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Correspondence to Michael Feiss or Venigalla B. Rao .

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Editors and Affiliations

  1. Dept. Biological Sciences, Purdue University, W. State St. 915, West Lafayette, 47907-2054, Indiana, USA

    Michael G. Rossmann

  2. Dept. Biology, Catholic University of America, Washington, 20064, District of Columbia, USA

    Venigalla B. Rao

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Feiss, M., Rao, V.B. (2012). The Bacteriophage DNA Packaging Machine. 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_22

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