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The hand of the filamentous bacteriophage helix

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Abstract

Filamentous bacteriophage (Inovirus) is a widely studied model system in molecular biophysics. The structure of the virion has been analysed by various methods, but the methods have seldom questioned the hand of the virion helix. The hand of the helix relating the protein subunits in the class II virus strain Pf1 was chosen by calculating an electron-density distribution from X-ray fibre diffraction data, using a maximum-entropy method, but to our knowledge this method has not been used for a similar purpose in any other system. Moreover, this same hand was extended only by analogy, with no direct analysis of the corresponding data, to the class I virus strain Ff (fd, f1, M13), which has a different helix symmetry. Here we use published solid-state NMR data to confirm the validity of the hand of Pf1 chosen by the maximum-entropy method, and to confirm the extension to Ff.

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Abbreviations

PDB:

Protein Data Bank

PISA:

Polarity index slant angle

PISEMA:

Polarisation inversion spin exchange at the magic angle

rmsd:

Root-mean-square deviation

References

  • Bryan RK (1987) Maximum entropy in structural molecular biology: the fiber diffraction phase problem. In: Smith CR, Erickson GJ (eds) Maximum-entropy and Baysian spectral analysis and estimation problems. Reidel, Dordrecht, pp 207–228

    Google Scholar 

  • Bryan RK, Bansal M, Folkhard W, Nave C, Marvin DA (1983) Maximum-entropy calculation of the electron density at 4 Å resolution of Pf1 filamentous bacteriophage. Proc Natl Acad Sci USA 80:4728–4731

    Article  ADS  Google Scholar 

  • Crick FHC (1953) The packing of α-helices: simple coiled-coils. Acta Crystallogr 6:689–697

    Article  Google Scholar 

  • Denny JK, Wang J, Cross TA, Quine JR (2001) PISEMA powder patterns and PISA wheels. J Magn Reson 152:217–226

    Article  ADS  Google Scholar 

  • Goldbourt A, Gross BJ, Day LA, McDermott AE (2007) Filamentous phage studied by magic-angle spinning NMR: resonance assignment and secondary structure of the coat protein in Pf1. J Am Chem Soc 129:2338–2344

    Article  Google Scholar 

  • Gonzalez A, Nave C, Marvin DA (1995) Pf1 filamentous bacteriophage: Refinement of a molecular model by simulated annealing using 3.3Å resolution X-ray fibre diffraction data. Acta Crystallogr Sect D 51:792–804

    Article  Google Scholar 

  • Guex N, Peitsch MC (1997) Swiss-model and the Swiss-PDB viewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723

    Article  Google Scholar 

  • Hansen MR, Hanson P, Pardi A (2000) Filamentous bacteriophage for aligning RNA, DNA, and proteins for measurement of nuclear magnetic resonance dipolar coupling interactions. Methods Enzymol. 317:220–240

    Article  Google Scholar 

  • Khalil AS, Ferrer JM, Brau RR, Kottmann ST, Noren CJ, Lang MJ, Belcher AM (2007) Single M13 bacteriophage tethering and stretching. Proc Natl Acad Sci USA 104:4892–4897

    Article  ADS  Google Scholar 

  • Kleywegt GJ (1997) Validation of protein models from Cα coordinates alone. J Mol Biol 273:371–376

    Article  Google Scholar 

  • Makowski L, Caspar DLD, Marvin DA (1980) Filamentous bacteriophage Pf1 structure determined at 7 Å resolution by refinement of models for the α-helical subunit. J Mol Biol 140:149–181

    Article  Google Scholar 

  • Marassi FM, Opella SJ (2000) A solid-state NMR index of helical membrane protein structure and topology. J Magn Reson 144:150–155

    Article  ADS  Google Scholar 

  • Marassi FM, Opella SJ (2002) Using Pisa pies to resolve ambiguities in angular constraints from PISEMA spectra of aligned proteins. J Biomol NMR 23:239–242

    Article  Google Scholar 

  • Marassi FM, Opella SJ (2003) Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints. Protein Sci 12:403–411

    Article  Google Scholar 

  • Marvin DA, Wachtel EJ (1976) Structure and assembly of filamentous bacterial viruses. Philos Trans R Soc Lond Ser B 276:81–98

    Article  ADS  Google Scholar 

  • Marvin DA, Nave C, Ladner JE, Fowler AG, Brown RS, Wachtel EJ (1981) Macromolecular structural transitions in Pf1 filamentous bacterial virus. In: Balaban M, Sussman JL, Traub W, Yonath A (eds) Structural aspects of recognition and assembly in biological macromolecules. Balaban ISS, Rehovot, pp 891–910

    Google Scholar 

  • Marvin DA, Bryan RK, Nave C (1987) Pf1 Inovirus: electron density distribution calculated by a maximum entropy algorithm from native fibre diffraction data to 3 Å resolution and single isomorphous replacement data to 5 Å resolution. J Mol Biol 193:315–343

    Article  Google Scholar 

  • Marvin DA, Hale RD, Nave C, Helmer-Citterich M (1994) Molecular models and structural comparisons of native and mutant class I filamentous bacteriophages Ff (fd, f1, M13), If1 and IKe. J Mol Biol 235:260–286

    Article  Google Scholar 

  • Marvin DA, Welsh LC, Symmons MF, Scott WRP, Straus SK (2006) Molecular structure of fd (f1, M13) filamentous bacteriophage refined with respect to X-ray fibre diffraction and solid-state NMR data supports specific models of phage assembly at the bacterial membrane. J Mol Biol 355:294–309

    Article  Google Scholar 

  • Melo F, Feytmans E (1998) Assessing protein structures with a non-local atomic interaction energy. J Mol Biol 277:1141–1152

    Article  Google Scholar 

  • Russel M, Model P (2006) Filamentous phage. In: Calendar R (ed) The bacteriophages, 2nd edn. Oxford University Press, USA, pp 146–160

    Google Scholar 

  • Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160:65–73

    Article  ADS  Google Scholar 

  • Schwieters CD, Kuszewski JJ, Clore GM (2006) Using Xplor-NIH for NMR molecular structure determination. Prog NMR Spectrosc 48:47–62

    Article  Google Scholar 

  • Thiriot DS, Nevzorov AA, Zagyanskiy L, Wu CH, Opella SJ (2004) Structure of the coat protein in Pf1 bacteriophage determined by solid-state NMR spectroscopy. J Mol Biol 341:869–879

    Article  Google Scholar 

  • Tombolato F, Ferrarini A, Grelet E (2006) Chiral nematic phase of suspensions of rodlike viruses: left-handed phase helicity from a right-handed molecular helix. Phys Rev Lett 96:258302(4)

    Article  ADS  Google Scholar 

  • Wang H, Stubbs G (1993) Molecular dynamics in refinement against fiber diffraction data. Acta Crystallog Sect A 49:504–513

    Article  Google Scholar 

  • Wang J, Denny J, Tian C, Kim S, Mo Y, Kovacs F, Song Z, Nishimura K, Gan Z, Fu R, Quine JR, Cross TA (2000) Imaging membrane protein helical wheels. J Magn Reson 144:162–167

    Article  ADS  Google Scholar 

  • Webster RE (2001) Filamentous phage biology. In: Barbas CF III, Burton DR, Scott JK, Silverman GJ (eds) Phage display: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 1.1–1.37

    Google Scholar 

  • Welsh LC, Symmons MF, Marvin DA (2000) The molecular structure and structural transition of the α-helical capsid in filamentous bacteriophage Pf1. Acta Crystallogr Sect D 56:137–150

    Article  Google Scholar 

  • Zeri AC, Mesleh MF, Nevzorov AA, Opella SJ (2003) Structure of the coat protein in fd filamentous bacteriophage particles determined by solid-state NMR spectroscopy. Proc Natl Acad Sci USA 100:6458–6463

    Article  ADS  Google Scholar 

Download references

Acknowledgments

WRPS acknowledges support from the Canada Foundation for Innovation. SKS acknowledges support from the Natural Sciences and Engineering Research Council of Canada (University Faculty Award and Discovery Grant) and from the University of British Columbia. DAM acknowledges support from the Department of Biochemistry, University of Cambridge.

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Authors and Affiliations

  1. Department of Chemistry, University of British Columbia, V6T 1Z1, BC, Canada

    S. K. Straus & W. R. P. Scott

  2. Department of Biochemistry, University of Cambridge, Cambridge, CB2 1GA, UK

    D. A. Marvin

Authors
  1. S. K. Straus
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  2. W. R. P. Scott
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  3. D. A. Marvin
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Correspondence to D. A. Marvin.

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Straus, S.K., Scott, W.R.P. & Marvin, D.A. The hand of the filamentous bacteriophage helix. Eur Biophys J 37, 1077–1082 (2008). https://doi.org/10.1007/s00249-008-0327-7

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  • DOI: https://doi.org/10.1007/s00249-008-0327-7

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