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Biophysical Reviews

, Volume 10, Issue 2, pp 641–658 | Cite as

Artificial bio-nanomachines based on protein needles derived from bacteriophage T4

  • Hiroshi Inaba
  • Takafumi Ueno
Review

Abstract

Bacteriophage T4 is a natural bio-nanomachine which achieves efficient infection of host cells via cooperative motion of specific three-dimensional protein architectures. The relationships between the protein structures and their dynamic functions have recently been clarified. In this review we summarize the design principles for fabrication of nanomachines using the component proteins of bacteriophage T4 based on these recent advances. We focus on the protein needle known as gp5, which is located at the center of the baseplate at the end of the contractile tail of bacteriophage T4. This protein needle plays a critical role in directly puncturing host cells, and analysis has revealed that it contains a common motif used for cell puncture in other known injection systems, such as T6SS. Our artificial needle based on the β-helical domain of gp5 retains the ability to penetrate cells and can be engineered to deliver various cargos into living cells. Thus, the unique components of bacteriophage T4 and other natural nanomachines have great potential for use as molecular scaffolds in efforts to fabricate new bio-nanomachines.

Keywords

Bacteriophage T4 Gp5 β-Helix Protein needle Cell penetration 

Notes

Acknowledgements

This work was supported by a Research Fellowship for Young Scientists of JSPS for H.I. (No. 4240) and by JSPS KAKENHI grant nos. JP13F03343, JP16H04177, JP16K13095, JP23350080, and JP26102513 and from Mochida Memorial Foundation for Medical and Pharmaceutical Research for T.U.

Compliance with ethical standards

Conflict of interest

Hiroshi Inaba declares that he has no conflict of interest. Takafumi Ueno declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by the authors.

References

  1. Aksyuk AA, Leiman PG, Kurochkina LP, Shneider MM, Kostyuchenko VA, Mesyanzhinov VV, Rossmann MG (2009) The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO J 28:821–829.  https://doi.org/10.1038/emboj.2009.36 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aksyuk AA, Bowman VD, Kaufmann B, Fields C, Klose T, Holdaway HA, Fischetti VA, Rossmann MG (2012) Structural investigations of a Podoviridae streptococcus phage C1, implications for the mechanism of viral entry. Proc Natl Acad Sci USA 109:14001–14006.  https://doi.org/10.1073/pnas.1207730109 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Archer MJ, Liu JL (2009) Bacteriophage T4 nanoparticles as materials in sensor applications: variables that influence their organization and assembly on surfaces. Sensors 9:6298–6311.  https://doi.org/10.3390/s90806298 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arisaka F, Yap ML, Kanamaru S, Rossmann MG (2016) Molecular assembly and structure of the bacteriophage T4 tail. Biophys Rev 8:385–396.  https://doi.org/10.1007/s12551-016-0230-x CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bartual SG, Otero JM, Garcia-Doval C, Llamas-Saiz AL, Kahn R, Fox GC, van Raaij MJ (2010) Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc Natl Acad Sci USA 107:20287–20292.  https://doi.org/10.1073/pnas.1011218107 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bebeacua C, Bron P, Lai L, Vegge CS, Brøndsted L, Spinelli S, Campanacci V, Veesler D, van Heel M, Cambillau C (2010) Structure and molecular assignment of lactococcal phage TP901-1 baseplate. J Biol Chem 285:39079–39086.  https://doi.org/10.1074/jbc.M110.175646 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bhardwaj A, Molineux IJ, Casjens SR, Cingolani G (2011) Atomic structure of bacteriophage Sf6 tail needle knob. J Biol Chem 286:30867–30877.  https://doi.org/10.1074/jbc.M111.260877 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bönemann G, Pietrosiuk A, Mogk A (2010) Tubules and donuts: a type VI secretion story. Mol Microbiol 76:815–821.  https://doi.org/10.1111/j.1365-2958.2010.07171.x CrossRefPubMedGoogle Scholar
  9. Brackmann M, Nazarov S, Wang J, Basler M (2017) Using force to punch holes: mechanics of contractile nanomachines. Trends Cell Biol 27:623–632.  https://doi.org/10.1016/j.tcb.2017.05.003 CrossRefPubMedGoogle Scholar
  10. Browning C, Shneider MM, Bowman VD, Schwarzer D, Leiman PG (2012) Phage pierces the host cell membrane with the iron-loaded spike. Structure 20:326–339.  https://doi.org/10.1016/j.str.2011.12.009 CrossRefPubMedGoogle Scholar
  11. Buth SA, Menin L, Shneider MM, Engel J, Boudko SP, Leiman PG (2015) Structure and biophysical properties of a triple-stranded beta-helix comprising the central spike of bacteriophage T4. Viruses 7:4676–4706.  https://doi.org/10.3390/v7082839 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Costa TRD, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G (2015) Secretion systems in gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13:343–359.  https://doi.org/10.1038/nrmicro3456 CrossRefPubMedGoogle Scholar
  13. Daube SS, Arad T, Bar-Ziv R (2007) Cell-free co-synthesis of protein nanoassemblies: tubes, rings, and doughnuts. Nano Lett 7:638–641.  https://doi.org/10.1021/nl062560n CrossRefPubMedGoogle Scholar
  14. Efimov AV, Kurochkina LP, Mesyanzhinov VV (2002) Engineering of bacteriophage T4 tail sheath protein. Biochemistry (Mosc) 67:1366–1370.  https://doi.org/10.1023/A:1021857926152. CrossRefGoogle Scholar
  15. Fokine A, Rossmann MG (2014) Molecular architecture of tailed double-stranded DNA phages. Bacteriophage 4:e28281.  https://doi.org/10.4161/bact.28281 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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.  https://doi.org/10.1073/pnas.0400444101 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fujita K, Tanaka Y, Sho T, Ozeki S, Abe S, Hikage T, Kuchimaru T, Kizaka-Kondoh S, Ueno T (2014) Intracellular CO release from composite of ferritin and ruthenium carbonyl complexes. J Am Chem Soc 136:16902–16908.  https://doi.org/10.1021/ja508938f CrossRefPubMedGoogle Scholar
  18. Fuller DN, Raymer DM, Kottadiel VI, Rao VB, Smith DE (2007) Single phage T4 DNA packaging motors exhibit large force generation, high velocity, and dynamic variability. Proc Natl Acad Sci USA 104:16868–16873.  https://doi.org/10.1073/pnas.0704008104 CrossRefPubMedPubMedCentralGoogle Scholar
  19. García-Gallego S, Bernardes GJL (2014) Carbon-monoxide-releasing molecules for the delivery of therapeutic CO in vivo. Angew Chem Int Ed 53:9712–9721.  https://doi.org/10.1002/anie.201311225 CrossRefGoogle Scholar
  20. Ge P, Scholl D, Leiman PG, Yu X, Miller JF, Zhou ZH (2015) Atomic structures of a bactericidal contractile nanotube in its pre- and postcontraction states. Nat Struct Mol Biol 22:377–382.  https://doi.org/10.1038/nsmb.2995 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Granell M, Namura M, Alvira S, Kanamaru S, van Raaij MJ (2017) Crystal structure of the carboxy-terminal region of the bacteriophage T4 proximal long tail fiber protein gp34. Viruses.  https://doi.org/10.3390/v9070168
  22. Harada K, Yamashita E, Nakagawa A, Miyafusa T, Tsumoto K, Ueno T, Toyama Y, Takeda S (2013) Crystal structure of the C-terminal domain of mu phage central spike and functions of bound calcium ion. Biochim Biophys Acta 1834:284–291.  https://doi.org/10.1016/j.bbapap.2012.08.015 CrossRefPubMedGoogle Scholar
  23. Heinemann SH, Hoshi T, Westerhausen M, Schiller A (2014) Carbon monoxide—physiology, detection and controlled release. Chem Commun 50:3644–3617.  https://doi.org/10.1039/c3cc49196j CrossRefGoogle Scholar
  24. Heymann JB, Bartho JD, Rybakova D, Venugopal HP, Winkler DC, Sen A, Hurst MR, Mitra AK (2013) Three-dimensional structure of the toxin-delivery particle antifeeding prophage of Serratia entomophila. J Biol Chem 288:25276–25284.  https://doi.org/10.1074/jbc.M113.456145 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ho BT, Dong TG, Mekalanos JJ (2014) A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15:9–21.  https://doi.org/10.1016/j.chom.2013.11.008 CrossRefPubMedGoogle Scholar
  26. Hou L, Gao F, Li N (2010) T4 virus-based toolkit for the direct synthesis and 3D organization of metal quantum particles. Chem Eur J 16:14397–14403.  https://doi.org/10.1002/chem.201000393 CrossRefPubMedGoogle Scholar
  27. Hu B, Margolin W, Molineux IJ, Liu J (2015) Structural remodeling of bacteriophage T4 and host membranes during infection initiation. Proc Natl Acad Sci USA 112:E4919–E4928.  https://doi.org/10.1073/pnas.1501064112 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hurst MRH, Glare TR, Jackson TA (2004) Cloning Serratia entomophila antifeeding genes–a putative defective prophage active against the grass grub Costelytra zealandica. J Bacteriol 186:5116–5128.  https://doi.org/10.1128/JB.186.15.5116-5128.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hurst MRH, Beard SS, Jackson TA, Jones SM (2007) Isolation and characterization of the Serratia entomophila antifeeding prophage. FEMS Microbiol Lett 270:42–48.  https://doi.org/10.1111/j.1574-6968.2007.00645.x CrossRefPubMedGoogle Scholar
  30. Hyman P, Valluzzi R, Goldberg E (2002) Design of protein struts for self-assembling nanoconstructs. Proc Natl Acad Sci USA 99:8488–8493.  https://doi.org/10.1073/pnas.132544299 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Inaba H, Kanamaru S, Arisaka F, Kitagawa S, Ueno T (2012) Semi-synthesis of an artificial scandium(III) enzyme with a b-helical bio-nanotube. Dalton Trans 41:11424–11427.  https://doi.org/10.1039/c2dt31030a CrossRefPubMedGoogle Scholar
  32. Inaba H, Kitagawa S, Ueno T (2014a) Protein needles as molecular templates for artificial metalloenzymes. Isr J Chem 55:40–50.  https://doi.org/10.1002/ijch.201400097 CrossRefGoogle Scholar
  33. Inaba H, Sanghamitra NJM, Fukai T, Matsumoto T, Nishijo K, Kanamaru S, Arisaka F, Kitagawa S, Ueno T (2014b) Intracellular protein delivery system with protein needle–GFP construct. Chem Lett 43:1505–1507.  https://doi.org/10.1246/cl.140481 CrossRefGoogle Scholar
  34. Inaba H, Sanghamitra NJM, Fujita K, Sho T, Kuchimaru T, Kitagawa S, Kizaka-Kondoh S, Ueno T (2015a) A metal carbonyl-protein needle composite designed for intracellular CO delivery to modulate NF-kB activity. Mol BioSyst 11:3111–3118.  https://doi.org/10.1039/c5mb00327j CrossRefPubMedGoogle Scholar
  35. Inaba H, Fujita K, Ueno T (2015b) Design of biomaterials for intracellular delivery of carbon monoxide. Biomater Sci 3:1423–1438.  https://doi.org/10.1039/C5BM00210A CrossRefPubMedGoogle Scholar
  36. Kageyama Y, Murayama M, Onodera T, Yamada S, Fukada H, Kudou M, Tsumoto K, Toyama Y, Kado S, Kubota K, Takeda S (2009) Observation of the membrane binding activity and domain structure of gpV, which comprises the tail spike of bacteriophage P2. Biochemistry 48:10129–10135.  https://doi.org/10.1021/bi900928n CrossRefPubMedGoogle Scholar
  37. Kanamaru S (2009) Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc Natl Acad Sci USA 106:4067–4068.  https://doi.org/10.1073/pnas.0901205106 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kanamaru S, Leiman PG, Kostyuchenko VA, Chipman PR, Mesyanzhinov VV, Arisaka F, Rossmann MG (2002) Structure of the cell-puncturing device of bacteriophage T4. Nature 415:553–557.  https://doi.org/10.1038/415553a CrossRefPubMedGoogle Scholar
  39. Kanamaru S, Ishiwata Y, Suzuki T, Rossmann MG, Arisaka F (2005) Control of bacteriophage T4 tail lysozyme activity during the infection process. J Mol Biol 346:1013–1020.  https://doi.org/10.1016/j.jmb.2004.12.042 CrossRefPubMedGoogle Scholar
  40. Karam JD, Drake JW, Kreuzer KN, Mosig G, Hall DH, Eiserling FA, Black LW, Spicer EK, Kutter E, Carlson K, Miller ES (eds) (1994) Molecular biology of bacteriophage T4. American Society for Microbiology, Washington D.C.Google Scholar
  41. Karimi M, Mirshekari H, Basri SMM, Bahrami S, Moghoofei M, Hamblin MR (2016) Bacteriophages and phage-inspired nanocarriers for targeted delivery of therapeutic cargos. Adv Drug Deliv Rev 106:45–62.  https://doi.org/10.1016/j.addr.2016.03.003 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Keten S, Alvarado JFR, Müftü S, Buehler MJ (2009) Nanomechanical characterization of the triple b-helix domain in the cell puncture needle of bacteriophage T4 virus. Cell Mol Bioeng 2:66–74.  https://doi.org/10.1007/s12195-009-0047-9 CrossRefGoogle Scholar
  43. Keten S, Xu Z, Buehler MJ (2011) Triangular core as a universal strategy for stiff nanostructures in biology and biologically inspired materials. Mater Sci Eng C 31:775–780.  https://doi.org/10.1016/j.msec.2011.01.004 CrossRefGoogle Scholar
  44. Kondabagil K, Dai L, Vafabakhsh R, Ha T, Draper B, Rao VB (2014) Designing a nine cysteine-less DNA packaging motor from bacteriophage T4 reveals new insights into ATPase structure and function. Virology 468:660–668.  https://doi.org/10.1016/j.virol.2014.08.033 CrossRefPubMedGoogle Scholar
  45. Koshiyama T, Yokoi N, Ueno T, Kanamaru S, Nagano S, Shiro Y, Arisaka F, Watanabe Y (2008) Molecular design of heteroprotein assemblies providing a bionanocup as a chemical reactor. Small 4:50–54.  https://doi.org/10.1002/smll.200700855 CrossRefPubMedGoogle Scholar
  46. Koshiyama T, Ueno T, Kanamaru S, Arisaka F, Watanabe Y (2009) Construction of an energy transfer system in the bio-nanocup space by heteromeric assembly of gp27 and gp5 proteins isolated from bacteriophage T4. Org Biomol Chem 7:2649–2654.  https://doi.org/10.1039/b904297k CrossRefPubMedGoogle Scholar
  47. Kostyuchenko VA, Leiman PG, Chipman PR, Kanamaru S, van Raaij MJ, Arisaka F, Mesyanzhinov VV, Rossmann MG (2003) Three-dimensional structure of bacteriophage T4 baseplate. Nat Struct Biol 10:688–693.  https://doi.org/10.1038/nsb970 CrossRefPubMedGoogle Scholar
  48. Kottadiel VI, Rao VB, Chemla YR (2012) The dynamic pause-unpackaging state, an off-translocation recovery state of a DNA packaging motor from bacteriophage T4. Proc Natl Acad Sci USA 109:20000–20005.  https://doi.org/10.1073/pnas.1209214109 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Koudelka KJ, Manchester M (2010) Chemically modified viruses: principles and applications. Curr Opin Chem Biol 14:810–817.  https://doi.org/10.1016/j.cbpa.2010.10.005 CrossRefPubMedGoogle Scholar
  50. Kube S, Wendler P (2015) Structural comparison of contractile nanomachines. AIMS Biophys 2:88–115.  https://doi.org/10.3934/biophy.2015.2.88 CrossRefGoogle Scholar
  51. Leiman PG, Kanamaru S, Mesyanzhinov VV, Arisaka F, Rossmann MG (2003) Structure and morphogenesis of bacteriophage T4. Cell Mol Life Sci 60:2356–2370.  https://doi.org/10.1007/s00018-003-3072-1 CrossRefPubMedGoogle Scholar
  52. 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 USA 106:4154–4159.  https://doi.org/10.1073/pnas.0813360106 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Leiman PG, Arisaka F, van Raaij MJ, Kostyuchenko VA, Aksyuk AA, Kanamaru S, Rossmann MG (2010) Morphogenesis of the T4 tail and tail fibers. Virol J 7:355.  https://doi.org/10.1186/1743-422X-7-355 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Li F, Wang Q (2014) Fabrication of nanoarchitectures templated by virus-based nanoparticles: strategies and applications. Small 10:230–245.  https://doi.org/10.1002/smll.201301393 CrossRefPubMedGoogle Scholar
  55. Liu Z, Qiao J, Niu Z, Wang Q (2012) Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles. Chem Soc Rev 41:6178–6194.  https://doi.org/10.1039/c2cs35108k CrossRefPubMedGoogle Scholar
  56. Liu JL, Dixit AB, Robertson KL, Qiao E, Black LW (2014) Viral nanoparticle-encapsidated enzyme and restructured DNA for cell delivery and gene expression. Proc Natl Acad Sci USA 111:13319–13324.  https://doi.org/10.1073/pnas.1321940111 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Ma Y, Nolte RJM, Cornelissen JJLM (2012) Virus-based nanocarriers for drug delivery. Adv Drug Deliv Rev 64:811–825.  https://doi.org/10.1016/j.addr.2012.01.005 CrossRefPubMedGoogle Scholar
  58. Migliori AD, Keller N, Alam TI, Mahalingam M, Rao VB, Arya G, Smith DE (2014) Evidence for an electrostatic mechanism of force generation by the bacteriophage T4 DNA packaging motor. Nat Commun 5:4173.  https://doi.org/10.1038/ncomms5173 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Moody MF (1967) Structure of the sheath of bacteriophage T4: I. Structure of the contracted sheath and polysheath. J Mol Biol 25:167–200.  https://doi.org/10.1016/0022-2836(67)90136-2 CrossRefPubMedGoogle Scholar
  60. Motterlini R, Otterbein LE (2010) The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 9:728–743.  https://doi.org/10.1038/nrd3228 CrossRefPubMedGoogle Scholar
  61. Nakayama K, Takashima K, Ishihara H, Shinomiya T, Kageyama M, Kanaya S, Ohnishi M, Murata T, Mori H, Hayashi T (2000) The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol Microbiol 38:213–231.  https://doi.org/10.1046/j.1365-2958.2000.02135.x CrossRefPubMedGoogle Scholar
  62. Nishima W, Kanamaru S, Arisaka F, Kitao A (2011) Screw motion regulates multiple functions of T4 phage protein gene product 5 during cell puncturing. J Am Chem Soc 133:13571–13576.  https://doi.org/10.1021/ja204451g CrossRefPubMedGoogle Scholar
  63. Olia AS, Casjens S, Cingolani G (2007) Structure of phage P22 cell envelope–penetrating needle. Nat Struct Mol Biol 14:1221–1226.  https://doi.org/10.1038/nsmb1317 CrossRefPubMedGoogle Scholar
  64. Olia AS, Casjens S, Cingolani G (2009) Structural plasticity of the phage P22 tail needle gp26 probed with xenon gas. Protein Sci 18:537–548.  https://doi.org/10.1002/pro.53 PubMedPubMedCentralGoogle Scholar
  65. 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.  https://doi.org/10.1038/nsmb.2023 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 26:3720–3728.  https://doi.org/10.1038/sj.emboj.7601786 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 104:15508–15513.  https://doi.org/10.1073/pnas.0706532104 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rao VB, Black LW (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 200:475–488.  https://doi.org/10.1016/0022-2836(88)90537-2 CrossRefPubMedGoogle Scholar
  69. Rao VB, Black LW (2010) Structure and assembly of bacteriophage T4 head. Virol J 7:356.  https://doi.org/10.1186/1743-422X-7-356 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Robertson KL, Soto CM, Archer MJ, Odoemene O, Liu JL (2011) Engineered T4 viral nanoparticles for cellular imaging and flow cytometry. Bioconjug Chem 22:595–604.  https://doi.org/10.1021/bc100365j CrossRefPubMedGoogle Scholar
  71. Rossmann MG, Rao VB (eds) (2012) Viral molecular machines. Springer, New YorkGoogle Scholar
  72. Rossmann MG, Mesyanzhinov VV, Arisaka F, Leiman PG (2004) The bacteriophage T4 DNA injection machine. Curr Opin Struct Biol 14:171–180.  https://doi.org/10.1016/j.sbi.2004.02.001 CrossRefPubMedGoogle Scholar
  73. Sanghamitra NJM, Inaba H, Arisaka F, Wang DO, Kanamaru S, Kitagawa S, Ueno T (2014) Plasma membrane translocation of a protein needle based on a triple-stranded b-helix motif. Mol BioSyst 10:2677–2683.  https://doi.org/10.1039/C4MB00293H CrossRefPubMedGoogle Scholar
  74. Sarris PF, Ladoukakis ED, Panopoulos NJ, Scoulica EV (2014) A phage tail-derived element with wide distribution among both prokaryotic domains: a comparative genomic and phylogenetic study. Genome Biol Evol 6:1739–1747.  https://doi.org/10.1093/gbe/evu136 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 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.  https://doi.org/10.1073/pnas.1000232107 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Shikuma NJ, Pilhofer M, Weiss GL, Hadfield MG, Jensen GJ, Newman DK (2014) Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 343:529–533.  https://doi.org/10.1126/science.1246794 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500:350–353.  https://doi.org/10.1038/nature12453 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Spínola-Amilibia M, Davó-Siguero I, Ruiz FM, Santillana E, Medrano FJ, Romero A (2016) The structure of VgrG1 from Pseudomonas aeruginosa, the needle tip of the bacterial type VI secretion system. Acta Crystallogr D Struct Biol 72:22–33.  https://doi.org/10.1107/S2059798315021142 CrossRefPubMedGoogle Scholar
  79. Sugimoto K, Kanamaru S, Iwasaki K, Arisaka F, Yamashita I (2006) Construction of a ball-and-spike protein supramolecule. Angew Chem Int Ed 45:2725–2728.  https://doi.org/10.1002/anie.200504018 CrossRefGoogle Scholar
  80. 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.  https://doi.org/10.1016/j.molcel.2007.02.013 CrossRefPubMedGoogle Scholar
  81. 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.  https://doi.org/10.1016/j.cell.2008.11.015 CrossRefPubMedGoogle Scholar
  82. 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 6:7548.  https://doi.org/10.1038/ncomms8548 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Suzuki H, Yamada S, Toyama Y, Takeda S (2010) The C-terminal domain is sufficient for host-binding activity of the mu phage tail-spike protein. Biochim Biophys Acta 1804:1738–1742.  https://doi.org/10.1016/j.bbapap.2010.05.003 CrossRefPubMedGoogle Scholar
  84. Takeda S, Arisaka F, Ishii S, Kyogoku Y (1990) Structural studies of the contractile tail sheath protein of bacteriophage T4. 1. Conformational change of the tail sheath upon contraction as probed by differential chemical modification. Biochemistry 29:5050–5056.  https://doi.org/10.1021/bi00473a008 CrossRefPubMedGoogle Scholar
  85. Tao P, Mahalingam M, Marasa BS, Zhang Z, Chopra AK, Rao VB (2013) In vitro and in vivo delivery of genes and proteins using the bacteriophage T4 DNA packaging machine. Proc Natl Acad Sci USA 110:5846–5851.  https://doi.org/10.1073/pnas.1300867110 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Taylor NMI, Prokhorov NS, Guerrero-Ferreira RC, Shneider MM, Browning C, Goldie KN, Stahlberg H, Leiman PG (2016) Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 533:346–352.  https://doi.org/10.1038/nature17971 CrossRefPubMedGoogle Scholar
  87. Ueno T (2008) Functionalization of viral protein assemblies by self-assembly reactions. J Mater Chem 18:3741–3745.  https://doi.org/10.1039/b806296j CrossRefGoogle Scholar
  88. Ueno T, Koshiyama T, Tsuruga T, Goto T, Kanamaru S, Arisaka F, Watanabe Y (2006) Bionanotube tetrapod assembly by in situ synthesis of a gold nanocluster with (gp5–His6)3 from bacteriophage T4. Angew Chem Int Ed 45:4508–4512.  https://doi.org/10.1002/anie.200504588 CrossRefGoogle Scholar
  89. Vafabakhsh R, Kondabagil K, Earnest T, Lee KS, Zhang Z, Dai L, Dahmen KA, Rao VB, Ha T (2014) Single-molecule packaging initiation in real time by a viral DNA packaging machine from bacteriophage T4. Proc Natl Acad Sci USA 111:15096–15101.  https://doi.org/10.1073/pnas.1407235111 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Veesler D, Cambillau C (2011) A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol Mol Biol Rev 75:423–433.  https://doi.org/10.1128/MMBR.00014-11 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Wen AM, Steinmetz NF (2016) Design of virus-based nanomaterials for medicine, biotechnology, and energy. Chem Soc Rev 45:4074–4126.  https://doi.org/10.1039/C5CS00287G CrossRefPubMedPubMedCentralGoogle Scholar
  92. Wendell D, Jing P, Geng J, Subramaniam V, Lee TJ, Montemagno C, Guo P (2009) Translocation of double-stranded DNA through membrane-adapted phi29 motor protein nanopores. Nat Nanotechnol 4:765–772.  https://doi.org/10.1038/nnano.2009.259 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Xu J, Xiang Y (2017) Membrane penetration by bacterial viruses. J Virol 91:e00162–17.  https://doi.org/10.1128/JVI.00162-17
  94. Xu J, Gui M, Wang D, Xiang Y (2016) The bacteriophage f29 tail possesses a pore-forming loop for cell membrane penetration. Nature 534:544–547.  https://doi.org/10.1038/nature18017 CrossRefPubMedGoogle Scholar
  95. Yamashita E, Nakagawa A, Takahashi J, Tsunoda K, Yamada S, Takeda S (2011) The host-binding domain of the P2 phage tail spike reveals a trimeric iron-binding structure. Acta Crystallogr Sect F Struct Biol Cryst Commun 67:837–841.  https://doi.org/10.1107/S1744309111005999 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Yang G, Dowling AJ, Gerike U, ffrench-Constant RH, Waterfield NR (2006) Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth. J Bacteriol 188:2254–2261.  https://doi.org/10.1128/JB.188.6.2254-2261.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Yap ML, Klose T, Arisaka F, Speir JA, Veesler D, Fokine A, Rossmann MG (2016) Role of bacteriophage T4 baseplate in regulating assembly and infection. Proc Natl Acad Sci USA 113:2654–2659.  https://doi.org/10.1073/pnas.1601654113 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Yokoi N, Inaba H, Terauchi M, Stieg AZ, Sanghamitra NJM, Koshiyama T, Yutani K, Kanamaru S, Arisaka F, Hikage T, Suzuki A, Yamane T, Gimzewski JK, Watanabe Y, Kitagawa S, Ueno T (2010) Construction of robust bio-nanotubes using the controlled self-assembly of component proteins of bacteriophage T4. Small 6:1873–1879.  https://doi.org/10.1002/smll.201000772 CrossRefPubMedGoogle Scholar
  99. Yokoi N, Miura Y, Huang C-Y, Takatani N, Inaba H, Koshiyama T, Kanamaru S, Arisaka F, Watanabe Y, Kitagawa S, Ueno T (2011) Dual modification of a triple-stranded b-helix nanotube with Ru and re metal complexes to promote photocatalytic reduction of CO2. Chem Commun 47:2074–2076.  https://doi.org/10.1039/c0cc03015e CrossRefGoogle Scholar
  100. Zoued A, Brunet YR, Durand E, Aschtgen M-S, Logger L, Douzi B, Journet L, Cambillau C, Cascales E (2014) Architecture and assembly of the type VI secretion system. Biochim Biophys Acta 1843:1664–1673.  https://doi.org/10.1016/j.bbamcr.2014.03.018 CrossRefPubMedGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Chemistry and Biotechnology, Graduate School of EngineeringTottori UniversityTottoriJapan
  2. 2.School of Life Science and TechnologyTokyo Institute of TechnologyYokohamaJapan

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