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Phage DNA Transport Across Membranes

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Structure and Dynamics of Confined Polymers

Part of the book series: NATO Science Series ((ASHT,volume 87))

Abstract

Phage nucleic acid transport is atypical among membrane transport and thus poses a fascinating problem: transport is unidirectional, and it concerns a unique molecule the size of which may represent 50 times that of the bacterium. The rate of DNA transport can reach values as high as 3,000 to 4,000 base pairs s-1. This raises many questions which will be addressed in this review. Is there a single mechanism of transport for all types of phage? How does the phage genome overcome the hydrophobic barrier of the host envelope? Is DNA transported as a free molecule or in association with proteins? Is such transport dependent on phage and/or host cell components? What is the driving force for transport? Data will be presented on tailed phage which are the most common type of phage, occurring in over 100 genera of bacteria and for which DNA transport has been the most extensively studied. We will show that it is possible to analyse these mechanisms both in vivo and in vitro by using biochemical as well as biophysical approaches.

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Reference

  1. Dubnau, D.(1999), DNA uptake in bacteria. Ann. Rev. Biochem. 53, 217–244.

    Google Scholar 

  2. Mitchell, P. (1968), Chemiosmotic coupling and energy transduction L. Glynn Research, Bodmin and Cornwall (eds).

    Google Scholar 

  3. Goldberg, E., Grinius, L. and Letellier, L. (1994), Recognition, attachment and injection, in The Molecular Biology of Bacteriophage T4, Karam, A. et al. (eds). American Society for Microbiology, Washington DC, pp. 347–357.

    Google Scholar 

  4. Reanney, D., and Ackermann, H.W. (1982), Comparative biology and evolution of bacteriophages, Adv. lrr. Res. 27, 205–280.

    Google Scholar 

  5. Dreisekelman, B. (1994), Translocation of DNA across bacterial membranes, Microbiol. Rev. 58, 293–316.

    Google Scholar 

  6. Palmen, R., Driessen, A.J. and Hellingwerf, K.J. (1994), Bioenergetic aspects of the translocation of macromolecules across bacterial membranes, Biochem. Biophys. Acta, 1183, 417–451.

    Article  Google Scholar 

  7. Letellier, L. and Bonhivers, M. (1996), Intrinsic and extrinsic channels in bacteria in Transport Processes in Eukaryotic and Prokaryotic Organisms, Handbook of Biological Physics, 2, Konings, W., Kaback, H.R. and Lolkema, J.S. (eds.), Elsevier, NY, pp. 615–637.

    Google Scholar 

  8. Zillig, W., Prangishvilli, D., Schleper, C., Elferink M., Holz, I., Albers, S., Janekovic, D. and Götz, D. (1996), Viruses, plasmids and other genetic elements of thermophilic and hyperthermophilic Archae, FEMS Microbiol. Rev. 18, 225–236.

    Article  Google Scholar 

  9. Hendrix, R., Smith, M., Burns, R., Ford, M. and Hatfull, G.(1999), Evolutionary relationships among diverse bacteriophage and prophage: all the world’s a phage. Proc.Natl.Acad.Sci. (USA) 96, 2192–2197.

    Article  ADS  Google Scholar 

  10. Bloomfield, V. (1996), DNA condensation, Curr. Opin. Struct. Biol. 6, 334–341.

    Article  Google Scholar 

  11. Earnshaw, W. and Casjens, S. (1980), DNA packaging by the double-stranded DNA bacteriophage, Cell 21, 319–331.

    Article  Google Scholar 

  12. Black, L.W. (1989), DNA packaging in ds DNA bacteriophage, Ann. Rev.Microbiol. 43,267–292.

    Article  Google Scholar 

  13. Black, L.W., Showe, M. and Steven, A. (1994), Morphogenesis of the T4 head in Molecular Biology of Bacteriophage T4; Karam A., et al. (eds). Washington DC; American Society for Microbiology; pp. 218–248.

    Google Scholar 

  14. Hendrix, R. (1998) Bacteriophage DNA packaging, RNA gears in a DNA transport machine, Cell 94, 147–150.

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  17. Casjens, S., Wyckoff, E., Hayden, M., Sampson, L., Eppler, K., Randall, S., Moreno, E. and 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  Google Scholar 

  18. Lepault, K., Dubochet, J., Baschong, W. and Kellenberger, W. (1987)¡ Organization of double stranded DNA in bacteriophages: a study by cry-electron microscopy of vitrified samples, EMBO J. 6, 1507–1512.

    Google Scholar 

  19. Tao,Y., Olson, N., Xu, W., Anderson, D., Rossmann, M. and Baker T. (1998), Assembly of a tailed bacterial virus and its genome release studied in three dimensions, Cell 95, 431–437.

    Article  Google Scholar 

  20. Cerritelli, M.E., Cheng, N., Rosenberg, A., McPherson, C., Booy, F. and Steven, A. (1997), Encapsidated conformation of bacteriophage T7 DNA, Cell, 91, 271–280.

    Article  Google Scholar 

  21. Harrison, S. (1983), Packaging of DNA into bacterial heads: a model. J. Mol. Biol. 171, 577–580.

    Article  Google Scholar 

  22. Odijk, T. (1998), Hexagonally packed DNA within bacteriophage T7 stabilized by curvature stress, Biophys. J. 75, 1223–1227.

    Article  ADS  Google Scholar 

  23. Cohen S.S. (1998), in A Guide to the Polyamines, Oxford Press, pp. 366–395.

    Google Scholar 

  24. Heller, K.J. (1992), Molecular interaction between bacteriophage and the Gram-negative cell envelope. Arch. Microbial. 158, 235–248.

    Article  Google Scholar 

  25. Boulanger, P. and Letellier, L. (1988), Characterization of ion channels involved in the penetration of phage T4 DNA into E. coli cells, J.Biol.Chem. 263, 9767–9775.

    Google Scholar 

  26. Boulanger, P. and Letellier, L. (1992), Ion channels are likely to be involved in the two steps of phage T5 DNA penetration into E. coli cells, J. Biol. Chem. 267, 3168–3172.

    Google Scholar 

  27. René Garcia, L.R. and Molineux, I. (1996), Transcription-independent DNA translocation of bacteriophage T7DNA into Escherichia coli, J. Bacteriol. 178, 6921–6929.

    Google Scholar 

  28. Bonhivers, M. (1996), Thesis, University of Paris VI, France.

    Google Scholar 

  29. Lanni, Y. (1968), First step transfer DNA of bacteriophage T5, Bacteriol. Rev. 32, 227–242.

    Google Scholar 

  30. Guihard, G., Boulanger, P. and Letellier, L. (1992), Involvement of phage T5 tail proteins and contact sites between the outer and inner membrane of Escherichia coli in phage T5 DNA injection, J. Biol. Chem. 267, 3173–3178.

    Google Scholar 

  31. Boulanger, et al., In preparation.

    Google Scholar 

  32. Lambert, O., Plançon, L., Rigaud, J-L- and Letellier, L. (1998), Protein-mediated DNA transfer into liposomes, Mol. Microbiol. 30: 761–765.

    Article  Google Scholar 

  33. Gabashvili, I. and Grosberg, A. (1992), Dynamics of double-stranded DNA reptation from bacteriophage, J. Biomol. Struct. and Dynamics 9, 911–920.

    Article  Google Scholar 

  34. Rau, D., Lee, B. and Parsegian, V. (1984), Measurement of the repulsive force between polyelectrolyte molecules in ionic solution: hydration forces between parallel double helices, Proc. Natl. Acad. Sci. (USA) 81, 2621–2625.

    Article  ADS  Google Scholar 

  35. Grinius, L. (1980), Nucleic acid transport driven by ion gradient across cell membranes, FEBSLett., 113, 1–10.

    Article  Google Scholar 

  36. Labedan, B. and Goldberg, E. (1979), Requirement for a membrane potential in injection of phage T4 DNA, Proc. Natl. Acad. Sci. (USA) 76, 4669–4673.

    Article  ADS  Google Scholar 

  37. Filali Maltouf, K. and Labedan, B. (1983), Host metabolic energy is not required for injection of bacteriophage T5 DNA, J. Bacteriol. 153, 124–133.

    Google Scholar 

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

    Google Scholar 

  39. Carlsson, C. Jonsson, M. and Akerman, B. (1995), Double bands in DNA gel electrophoresis caused by bis-intercalating dyes, Nucleic Acid Res. 23, 2413–2420.

    Article  Google Scholar 

  40. Nikaido, H. and Saier, M.II. (1992), Transport proteins in bacteria: common themes in their design, Science 258, 936–942.

    Article  ADS  Google Scholar 

  41. Moeck, G.S. and Coulton, J.W. (1998), TonB-dependent iron acquisition: mechanisms of siderophore -mediated active transport, Mol. Microbiol. 28, 675–681.

    Article  Google Scholar 

  42. Schirmer, T., Keller, T.A., Wang, Y.F. and Rosenbusch, J.P. (1995), Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science, 267, 512–514.

    Article  ADS  Google Scholar 

  43. Bonhivers, M., Ghazi, A., Boulanger, P. and Letellier, L. (1996), FhuA, a transporter of the Escherichia coli outer membrane, is converted into a channel upon binding of bacteriophage T5, EMBO J. 15, 1850–1856.

    Google Scholar 

  44. Rutz, J.M., Liu, J., Lyons, J.A., Goranson, J., Armstrong, S.K., McIntosh, M.A., Feix, J.B. and Klebba, P.E. (1992), Formation of a gated channel by a ligand-specific transport protein in the bacterial outer membrane, Science 258, 471–475.

    Article  ADS  Google Scholar 

  45. Kasianowicz, J.J., Brandin, E., Branton, D. and Deamer, D.W. (1996), Characterization of individual polynucleotide molecules using a membrane channel, Proc. Natl. Acad Sci. (USA) 93, 13770–13773.

    Article  ADS  Google Scholar 

  46. Akeson, M., Branton, D. Kasianowicz, J.J. Brandin, E. and Deamer, D.W. (1999), Microsecond time-scale discrimination between polycytidylic acid and polyadenylic acid segments within single RNA molecules, Biophys. J. 77, 3227–3233.

    Article  Google Scholar 

  47. Henrickson, S.E, Misakian, M., Robertson, B. and Kasianowicz, J.J. (2000), Asymmetric driven DNA transport in a nanometer-scale pore. Phys. Rev. Lett. 85, 3057–3060.

    Article  ADS  Google Scholar 

  48. Lambert, O., Moeck, G., Levy, D., Planton, L., Letellier, L and Rigaud J.-L. (1999), An 8A projected structure of FhuA, a ligand gated channel of the E. coli outer membrane, J Structural Biol., 126, 145–155.

    Article  Google Scholar 

  49. Löcher, K., Rees, B., Koebnick, R., Mitschler, A., Moulinier, L., Rosenbusch, J. and Moras, D. (1998), Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome bound states reveal allosteric changes. Cell 95, 771–778.

    Article  Google Scholar 

  50. Ferguson, A., Hofman, E., Coulton, J., Diederichs, K. and Welte, W. (1998), Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide, Science 282, 2215–2220.

    Article  ADS  Google Scholar 

  51. Buchanan, S., Smith, B., Venkatramani, L., Xia, D., Esser, L., Palnitkar, M., Chakraborty, R., van der Helm, D. and Deisenhofer, J. (1999), Crystal structure of the outer membrane active transporter FepA from E. coli. Nat. Struct. Biol. 6, 56–63.

    Article  Google Scholar 

  52. Plançon, L., Chami, M. and Letellier, L. (1997), Reconstitution of FhuA, an E. coli outer membrane protein into liposomes. Binding of phage T5 to FhuA triggers the transfer of DNA into the proteoliposomes, J. Biol. Chem. 272, 16868–16872.

    Article  Google Scholar 

  53. Lambert, O., Letellier, L., Gelbart, W. and Rigaud, J.-L. (2000), DNA delivery by phage as a new strategy for encapsulating toroidal condensates of arbitrary size into liposomes. Proc. Natl. Acad. Sci. (USA), in press.

    Google Scholar 

  54. Behr, J.P. (1994), Gene transfer with synthetic cationic amphiphiles; prospects for gene therapy. Bioconj. Chem. 5, 382–389.

    Article  Google Scholar 

  55. Pelta, J., Livolant, F., Sikorav, J.L. (1996a), DNA aggregation induced by polyamines and cobalt-hexamine. J. Biol. Chem. 271, 5656–5662.

    Article  Google Scholar 

  56. Pelta, J., Durand, D., Doucet, J. and Livolant, F. (1996b), DNA mesophases induced by spermidine: Structural properties and biological implications. Biophys. J 71, 48–63.

    Article  Google Scholar 

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Letellier, L. (2002). Phage DNA Transport Across Membranes. In: Kasianowicz, J.J., Kellermayer, M.S.Z., Deamer, D.W. (eds) Structure and Dynamics of Confined Polymers. NATO Science Series, vol 87. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0401-5_2

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  • DOI: https://doi.org/10.1007/978-94-010-0401-5_2

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-1-4020-0698-2

  • Online ISBN: 978-94-010-0401-5

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