Skip to main content
SpringerLink
Log in

Single-stranded DNA binding protein encoded by the filamentous bacteriophage M13: structural and functional characteristics

  • Review
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The single-stranded DNA binding protein, or gene V protein (gVp), encoded by gene V of the filamentous bacteriophage M13 is a multifunctional protein that not only regulates viral DNA replication but also gene expression at the level of mRNA translation. It furthermore is implicated as a scaffolding and/or chaperone protein during the phage assembly process at the hostcell membrane. The protein is 87 amino acids long and its biological functional entity is a homodimer. In this manuscript a short description of the life cycle of filamentous phages is presented and our current knowledge of the major functional and structural properties and characteristics of gene V protein are reviewed. In addition models of the superhelical complexes gVp forms with ssDNA are described and their (possible) biological meaning in the infection process are discussed. Finally it is described that the ‘DNA binding loop’ of gVp is a recurring motif in many ssDNA binding proteins and that the fold of gVp is shared by a large family of evolutionarily conserved gene regulatory proteins.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

dsDNA:

double-stranded DNA

ssDNA:

single-stranded DNA

dsDBP:

double-stranded DNA binding protein

ssDBP:

single-stranded DNA binding protein

CSD:

cold-shock domain

NMR:

nuclear magnetic resonance

g‘X’p:

gene ‘X’ protein

References

  1. Freemont PS, Lane AN & Sanderson MR (1991) Biochem. J. 278: 1–23

    PubMed  Google Scholar 

  2. Brändén C & Tooze J (1991) Introduction to Protein Structure. Garland Publishing Company, Inc., New York

    Google Scholar 

  3. Pabo CO & Sauer RT (1992) Ann. Rev. Biochem. 61: 1053–1095

    PubMed  Google Scholar 

  4. Travers A (1993) DNA-Protein Interactions. Chapman & Hall, London

    Google Scholar 

  5. Kornberg A & Baker TA (1992) DNA Replication WH Freeman & Company, New York

    Google Scholar 

  6. Lindberg G, Kowalczykowski SC, Rist JK, Sugino A & Rothman-Denes LB (1989) J. Biol. Chem. 264: 12700–12708

    PubMed  Google Scholar 

  7. Martín G, Lázaro JM, Méndez E & Salas M (1989) Nucl. Acids Res. 17: 3663–3672

    PubMed  Google Scholar 

  8. Chase JW & Williams KR (1986) Ann. Rev. Biochem. 55: 103–136

    PubMed  Google Scholar 

  9. Gutierrez C, Martin G, Sogo JM & Salas M (1991) J. Biol. Chem. 266: 2104–2111

    PubMed  Google Scholar 

  10. Meyer RR & Laine PS (1990) Microbiol. Rev. 54: 342–380

    PubMed  Google Scholar 

  11. Heyer W-D & Kolodner RD (1989) Biochemistry 28: 2856–2861

    PubMed  Google Scholar 

  12. Tucker PA, Tsernoglou D, Tucker AD, Coenjaerts FEJ, Leenders H & Van der Vliet PC (1994) EMBO J. 13: 2994–3002

    PubMed  Google Scholar 

  13. Model P & Russel M (1988) In: Calender R (Ed) The Bacteriophages, Vol 2, Filamentous Bacteriophage (pp 375–456) Plenum Publishing Corp., New York

    Google Scholar 

  14. Marvin DA (1990) Int. J. Biol. Macromol. 12: 125–138

    PubMed  Google Scholar 

  15. Russel M (1991) Mol. Microbiol. 5: 1607–1613

    PubMed  Google Scholar 

  16. Makowski L (1984) In: Jurnak FA & McPherson A (Eds) Biological Macromolecules & Assemblies, Vol 1, Virus Structures (pp 203–253) John Wiley and Sons, New York

    Google Scholar 

  17. Marvin DA, Hale, RD & Nave C (1994) J. Mol. Biol. 235: 260–286

    PubMed  Google Scholar 

  18. Watson JD, Gilman M, Wikowski J & Zoller M (1992) Recombinant DNA (2nd Ed). W.H. Freeman and Company, New York

    Google Scholar 

  19. Rasched I & Oberer E (1986) Micriobiol. Rev. 50: 401–427

    Google Scholar 

  20. Russel M (1994) Science 265: 612–614

    PubMed  Google Scholar 

  21. Hagishitani N, Hagashitani A & Horiuchi K (1993) J. Virol. 67: 2175–2181

    PubMed  Google Scholar 

  22. Kazmierzak BI, Mieike DL, Russel M & Model P (1994) J. Mol. Biol. 238, 187–198

    PubMed  Google Scholar 

  23. Kokoska RJ, Blumer KJ & Steege DA (1990) Biochimie 72: 803–811

    PubMed  Google Scholar 

  24. Michel B & Zinder ND (1989) Proc. Natl. Acad. Sci. USA 86: 4002–4006

    PubMed  Google Scholar 

  25. Michel B & Zinder ND (1989) Nucl. Acids Res. 17: 7333–7344

    PubMed  Google Scholar 

  26. Zaman GJR, Schoenmakers JGG & Konings RNH (1990) Eur. J. Biochem. 189: 119–124

    PubMed  Google Scholar 

  27. Zaman GJR, Smetsers A, Kaan AM, Schoenmakers JGG & Konings RNH (1991) Biochim. Biophys. Acta. 1089: 183–192

    PubMed  Google Scholar 

  28. Fulford W & Model P (1988) J. Mol. Biol. 203: 39–48

    PubMed  Google Scholar 

  29. Fulford W & Model P (1988) J. Mol. Biol. 203: 49–62, Acta 607: 361–371

    PubMed  Google Scholar 

  30. Alberts B & Herrick G (1971) Methods Enzymol. 21: 198–217

    Google Scholar 

  31. Alberts B, Frey L & Delius H (1972) J. Mol. Biol. 68: 139–152

    PubMed  Google Scholar 

  32. Oey JL & Knippers R (1972) J. Mol. Biol. 68: 125–138

    PubMed  Google Scholar 

  33. Holwitt E & Krasna AI (1982) Arch. Biochem. Biophys. 214: 792–805

    PubMed  Google Scholar 

  34. Pratt D, Laws P & Griffith J (1974) J. Mol. Biol. 82: 425–439

    PubMed  Google Scholar 

  35. De Jong EAM, Van Duynhoven JPM, Harmsen BJM, Konings RNH & Hilbers CW (1989) J. Mol. Biol. 206: 119–132

    PubMed  Google Scholar 

  36. De Jong EAM, Van Duynhoven JPM, Harmsen BJM, Tesser GI, Konings RNH & Hilbers CW (1989) J. Mol. Biol. 206: 133–152

    PubMed  Google Scholar 

  37. Kneale GG (1992) Curr. Opinion Structural Biol. 2: 124–130

    Google Scholar 

  38. Powell MD & Gray DM (1993) Biochemistry 32: 12538–12547

    PubMed  Google Scholar 

  39. Folmer RHA, Folkers PJM, Kaan A, Jonker, AJ, Aelen JMA, Konings RNH & Hilbers CW (1994) Eur. J. Biochem. 224: 663–676

    PubMed  Google Scholar 

  40. Gray CW (1989) J. Mol. Biol. 208: 57–64

    PubMed  Google Scholar 

  41. Alma NCM, Harmsen BJM, Van Boom JH, Van der Marel G & Hilbers CW (1982) Eur. J. Biochem. 122: 319–326

    PubMed  Google Scholar 

  42. Gray DM, Sherry AD, Teherani J & Kansy JW (1984) J. Biomol. Struct. Dynam. 2: 77–91

    Google Scholar 

  43. Kansy JW, Clack BA & Gray DM (1986) J. Biomol. Struct. Dynam. 3: 1079–1110

    Google Scholar 

  44. Bulsink H, Wijnaendts van Resandt RW, Harmsen BJM & Hilbers CW (1986) Eur. J. Biochem. 157: 329–334

    PubMed  Google Scholar 

  45. Bulsink H, Harmsen BJM & Hilbers CW (1988) Eur. J. Biochem. 176: 597–608

    PubMed  Google Scholar 

  46. Alma NCM, Harmsen BJM, Van Boom JH, Van der Marel G & Hilbers CW (1983) Biochemistry 22: 2104–2115

    PubMed  Google Scholar 

  47. Day LA (1973) Biochemistry 12: 5329–5339

    PubMed  Google Scholar 

  48. Anderson RA, Nakashima Y & Coleman JE (1975) Biochemistry 14: 907–917

    PubMed  Google Scholar 

  49. Pretorius HT, Klein M & Day LA (1975) J. Biol. Chem. 250: 9262–9269

    PubMed  Google Scholar 

  50. Bobst AM, Langemeier PW, Warwick-Koochaki PE, Bobst EV & Ireland JC (1982) J. Biol. Chem. 257: 6184–6193

    PubMed  Google Scholar 

  51. Bobst AM, Ireland JC & Bobst EV (1984) J. Biol. Chem. 259: 2130–2134

    PubMed  Google Scholar 

  52. Cavalieri SJ, Neet KE & Goldthwait DA (1976) J. Mol. Biol. 102: 697–711

    PubMed  Google Scholar 

  53. Alma NCM, Harmsen BJM, De Jong EAM, Van de Ven J & Hilbers CW (1983) J Mol Biol 163: 47–62

    PubMed  Google Scholar 

  54. Stassen APM, Harmsen BJM, Schoenmakers JGG, Hilbers CW & Konings RNH (1992) Eur. J. Biochem. 206: 605–612

    PubMed  Google Scholar 

  55. Dunker AK & Anderson EA (1975) Biochim. Biophys. Acta. 402: 31–34

    PubMed  Google Scholar 

  56. Pörschke D & Rauh H (1983) Biochemistry 22: 4737–4745

    PubMed  Google Scholar 

  57. Bulsink H, Harmsen BJM & Hilbers CW (1985) J. Biomol. Struct. Dynam. 3: 227–247

    Google Scholar 

  58. Peeters BPH, Konings RNH & Schoenmakers JGG (1983) J. Mol. Biol. 169: 197–215

    PubMed  Google Scholar 

  59. Kneale GG, Freeman R & Marvin DA (1982) J. Mol. Biol. 156: 279–292

    PubMed  Google Scholar 

  60. Kneale GG (1983) Biochim. Biophys. Acta 739: 216–224

    PubMed  Google Scholar 

  61. De Jong EAM, Harmsen BJM, Konings RNH & Hilbers CW (1987) Biochemistry 26: 2039–2046

    PubMed  Google Scholar 

  62. Kneale GG & Wijnaendts van Resandt RW (1985) Eur. J. Biochem. 149: 85–93

    PubMed  Google Scholar 

  63. Carpenter ML & Kneale GG (1991) J. Mol. Biol. 217: 681–689

    PubMed  Google Scholar 

  64. Rasched I & Pohl FM (1974) FEBS Lett. 46: 115–118

    PubMed  Google Scholar 

  65. Sang B-C & Gray DM (1989) J. Biomol. Struct. Dynam. 7: 693–706

    Google Scholar 

  66. Zaman GJR (1991) Translational Regulation by the Single-Stranded DNA Binding Protein of the Filamentous Bacteriophage M13. PhD Thesis, University of Nijmegen, The Netherlands.

    Google Scholar 

  67. Record MT, Lohman TM & De Haseth P (1976) J. Mol. Biol. 107: 145–158

    PubMed  Google Scholar 

  68. Record MT, Anderson CF & Lohman TM (1978) Quart. Rev. Biophys. 11: 103–178

    Google Scholar 

  69. Russel M (1992) J. Mol. Biol. 227: 453–462

    PubMed  Google Scholar 

  70. McPherson A, Jurnak FA, Wang AHJ, Molineux I & Rich A (1979) J. Mol. Biol. 134: 379–400

    PubMed  Google Scholar 

  71. Brayer GD & McPherson A (1983) J. Mol. Biol. 169: 565–596

    PubMed  Google Scholar 

  72. Van Duynhoven JPM, Folkers PJM, Stassen APM, Harmsen BJM, Konings RNH & Hilbers CW (1990) FEBS Lett. 261: 1–4

    PubMed  Google Scholar 

  73. Folkers PJM, Nilges M, Folmer RHA, Konings RNH & Hilbers CW (1994) J. Mol. Biol. 236: 229–246

    PubMed  Google Scholar 

  74. Skinner MM, Zhang H, Leschnitzer DH, Guan Y, Bellamy H, Sweet RM, Gray CW, Konings RNH, Wang AHJ & Terwilliger TC (1994) Proc. Natl. Acad. Sci. USA 91: 2071–2075

    PubMed  Google Scholar 

  75. Konings RNH, Folmer RHA, Folkers PJM, Nilges M & Hilbers CW (1995) FEMS Reviews, in press

  76. Van Duynhoven JPM, Folkers PJM, Prinse CWJM, Harmsen BJM, Konings RNH & Hilbers CW (1992) Biochemistry 31: 1254–1262

    PubMed  Google Scholar 

  77. Van Duynhoven JPM, Nooren IMA, Swinkels DW, Folkers PJM, Harmsen BJM, Konings RNH, Tesser GI & Hilbers CW (1993) Eur. J. Biochem. 216: 507–517

    PubMed  Google Scholar 

  78. Folkers PJM, Van Duynhoven JPM, Jonker AJ, Harmsen BJM, Konings RNH & Hilbers CW (1991) Eur. J. Biochem. 202: 349–360

    PubMed  Google Scholar 

  79. Folkers PJM, Stassen APM, Van Duynhoven JPM, Harmsen BJM, Konings RNH & Hilbers CW (1991) Eur. J. Biochem. 200: 139–148

    PubMed  Google Scholar 

  80. Stassen APM, Zaman GJR, Van Deursen JMA, Schoenmakers JGG & Konings RNH (1992) Eur. J. Biochem. 204: 1003–1014

    PubMed  Google Scholar 

  81. Alma NCM, Harmsen BJM, Hull WE, Van der Marel G, Van Boom JH & Hilbers CW (1981) Biochemistry 20: 4419–4428

    PubMed  Google Scholar 

  82. King GC & Coleman JE (1987) Biochemistry 26: 2929–2937

    PubMed  Google Scholar 

  83. Folkers PJM, Van Duynhoven JPM, Van Lieshout HTM, Harmsen BJM, Van Boom JH, Tesser GI, Konings RNH & Hilbers CW (1993) Biochemistry 32: 9407–9416

    PubMed  Google Scholar 

  84. Folmer RHA, Nilges M, Folkers PJM, Konings RNH & Hilbers CW (1994) J. Mol. Biol. 240: 341–357

    PubMed  Google Scholar 

  85. Guan Y, Zhang H, Konings RNH, Hilbers CW, Terwilliger TC & Wang AH-J (1994) Biochemistry 33: 7768–7778

    PubMed  Google Scholar 

  86. Terwilliger TC, Zabin HB, Horvath MP, Sandberg WS & Schlunk PM (1994) J. Mol. Biol. 236: 556–571

    PubMed  Google Scholar 

  87. Gray CW, Kneale GG, Leonard KR, Siegrist H & Marvin DA (1982) Virology 116: 40–52

    PubMed  Google Scholar 

  88. Dotto GP & Zinder ND (1983) Virology 130: 252–256

    PubMed  Google Scholar 

  89. Dotto GP & Zinder ND (1984) Proc. Natl. Acad. Sci. USA 81: 1336–1340

    PubMed  Google Scholar 

  90. Prasad BVV & Chiu W (1987) J. Mol. Biol. 193: 579–584

    PubMed  Google Scholar 

  91. Van Duynhoven JPM, Folkers PJM, Stassen APM, Harmsen BJM, Konings RNH & Hilbers CW (1990) FEBS Lett. 261: 1–4

    PubMed  Google Scholar 

  92. Stassen APM (1994) Studies on the Relationship between Structure and Funnction of the Single-Stranded DNA Binding Protein of the Filamentous Bacteriophage M13. PhD Thesis University of Nijmegen, The Netherlands

    Google Scholar 

  93. Plyte SE & Kneale GG (1991) Prot. Engineer. 4: 553–560

    Google Scholar 

  94. Schindelin H, Marahlel MA & Heineman U (1993) Nature (London) 364: 164–168

    PubMed  Google Scholar 

  95. Schindelin H, Jiang W, Inouye M & Heineman U (1994) Proc. Natl. Acad. Sci. USA 91: 5119–5123

    PubMed  Google Scholar 

  96. Newkirk, K, Feng W, Jiang W, Tejero R, Donald Emerson A, Inouye M & Montelione GT (1994) Proc. Natl. Acad. Sci. USA 91: 5114–51183

    PubMed  Google Scholar 

  97. Schnuchel A, Wiltscheck R, Czisch M, Herrier M, Willimsky G, Grauman P, Marahlel MA & Holak TA (1993) Nature (London) 364: 169–171

    PubMed  Google Scholar 

  98. Wolffe AP (1994) Bioessays 16: 245–251

    PubMed  Google Scholar 

  99. Brayer GD & McPherson A (1984) J. Biomol. Struct. Dynam. 2: 495–509

    Google Scholar 

  100. Brayer GD & McPherson A (1985) Eur. J. Biochem. 150: 287–296

    PubMed  Google Scholar 

  101. Hutchinson DL, Barnett BL & Bobst AM (1990) J. Biomol. Struct. Dynam. 8: 1–9

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Biology, University of Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands

    Alphons P. M. Stassen & Ruud N. H. Konings

  2. Department of Biophysical Chemistry, University of Nijmegen, Toernooiveld 1, 6525 ED, Nijmegen, The Netherlands

    Rutger H. A. Folmer, Cees W. Hilbers & Ruud N. H. Konings

Authors
  1. Alphons P. M. Stassen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rutger H. A. Folmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cees W. Hilbers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ruud N. H. Konings
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dedicated to the memory of our colleague Prof. Dr. John G.G. Schoenmakers

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stassen, A.P.M., Folmer, R.H.A., Hilbers, C.W. et al. Single-stranded DNA binding protein encoded by the filamentous bacteriophage M13: structural and functional characteristics. Mol Biol Rep 20, 109–127 (1994). https://doi.org/10.1007/BF00990543

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00990543

Key words

Search

Navigation