Skip to main content
SpringerLink
Log in

Dipoles of the α-helix and β-sheet: their role in protein folding

  • Article
  • Published:

From Nature

View current issue Submit your manuscript

Abstract

As a result of the regular arrangement of peptide dipoles in secondary structure segments and the low effective dielectric constant in Hydrophobic cores, the electrostatic energy of a protein is very sensitive to the relative orientation of the segments. We provide here evidence that the alignment of secondary structure dipoles is significant in determining the three-dimensional structure of globular 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

References

  1. Wada, A. Adv. Biophys. 9, 1–63 (1976).

    MathSciNet  CAS  Google Scholar 

  2. Hol, W. G. J., Van Duijnen, P. Th. & Berendsen, H. J. C. Nature 273, 443–446 (1978).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Van Duijnen, P. Th., Thole, B. T. & Hol, W. G. J. Biophys. Chem. 9, 273–280 (1979).

    Article  CAS  PubMed  Google Scholar 

  4. Drenth, J., Swen, H. M., Hoogenstraaten, W. & Sluyterman, L. A. Æ. Proc. K. ned. Akad. Wet. C78, 104–110 (1975).

    CAS  Google Scholar 

  5. Jernigan, R. L., Miyazawa, S. & Szu, S. C. Macromolecules 13, 518–525 (1980).

    Article  ADS  CAS  Google Scholar 

  6. Blagdon, D. E. & Goodman, M. Biopolymers 14, 241–245 (1975).

    Article  CAS  PubMed  Google Scholar 

  7. Levitt, M. & Chothia, C. Nature 261, 552–558 (1976).

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Bloomer, A. C., Champness, J. N., Bricogne, G., Staden, R. & Klug, R. Nature 276, 362–368 (1978).

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Stubbs, G., Warren, S. & Holmes, K. Nature 267, 216–221 (1977).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Kendrew, J. C. et al. Nature 185, 422–427 (1960).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Kretsinger, R. H. & Nockolds, C. E. J. biol Chem. 248, 3313–3326 (1973).

    CAS  PubMed  Google Scholar 

  12. Hendrickson, W. A. & Ward, K. B. J. biol. Chem. 252, 3012–3018 (1977).

    CAS  PubMed  Google Scholar 

  13. Banyard, S. H., Stammers, D. K. & Harrison, P. M. Nature 271, 282–284 (1978).

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Mathews, F. S., Bethge, P. H. & Czerwinski, E. W. J. biol. Chem. 254, 1699–1706 (1979).

    CAS  PubMed  Google Scholar 

  15. Weber, P. C. et al. Nature 286, 302–304 (1980).

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Weber, P. C. & Salemme, R. Nature 287, 82–84 (1980).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Mornon, J. P., Fridlansky, F., Bally, R. & Milgrom, E. J. molec. Biol. 137, 415–429 (1980).

    Article  CAS  PubMed  Google Scholar 

  18. Poulos, Th. L. et al. J. biol. Chem. 255, 575–580 (1980).

    CAS  PubMed  Google Scholar 

  19. Imoto, T., Johnson, L. N., North, A. C. T., Phillips, D. C. & Rupley, J. A. in The Enzymes Vol. 7 (ed. Boyer, P. D.) 666–868 (Academic, New York, 1972).

    Google Scholar 

  20. Remington, S. J. et al. J. molec. Biol. 118, 81–98 (1978).

    Article  CAS  PubMed  Google Scholar 

  21. Colman, P. M., Jansonius, J. N. & Matthews, B. W. J. molec. Biol. 70, 701–724 (1972).

    Article  CAS  PubMed  Google Scholar 

  22. Mathews, F. S., Levine, M. & Argos, P. J. molec. Biol. 64, 449–464 (1972).

    Article  CAS  PubMed  Google Scholar 

  23. Chothia, C. J. Molec. Biol. 75, 295–302 (1973).

    Article  CAS  PubMed  Google Scholar 

  24. Janin, J. & Chothia, C. J. molec. Biol. 143, 95–128 (1980).

    Article  CAS  PubMed  Google Scholar 

  25. Arnott, S., Dover, S. D. & Elliot, A. J. molec. Biol. 30, 201–208 (1967).

    Article  CAS  PubMed  Google Scholar 

  26. Fraser, R. D. B. & MacRae, T. P. Conformation in Fibrous Proteins (Academic, New York, 1973).

  27. Leijonmarck, M., Eriksson, S. & Liljas, A. Nature 286, 824–826 (1980).

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Wierenga, R. K., De Jong, R. J., Kalk, K. H., Hol, W. G. J. & Drenth, J. J. molec. Biol. 131, 55–73 (1979).

    Article  CAS  PubMed  Google Scholar 

  29. Cohen, L. A. in The Enzymes Vol. l (ed. Boyer, P. D.) 147–211 (Academic, New York, 1970).

    Google Scholar 

  30. Ottesen, M., Johansen, J. T. & Swendsen, I. in Structure–Function Relationships of Proteolytic Enzymes (eds Desnuelle, P. Neurath, H. & Ottesen, M.) 175–187 (Munksgaard, Copenhagen, 1970).

    Book  Google Scholar 

  31. Glazer, A. N. in The Proteins Vol. 2 (eds Neurath, H. & Hill, R. L.) 1–103 (1976).

    Book  Google Scholar 

  32. Ploegman, J. H., Drent, G., Kalk, K. H. & Hol, W. G. J. J. molec. Biol. 123, 557–594 (1978).

    Article  CAS  PubMed  Google Scholar 

  33. Delbaere, L. T. J., Hatcheon, W. L. B., James, M. N. G. & Thiessen, W. E. Nature 257, 758–763 (1975).

    Article  ADS  CAS  PubMed  Google Scholar 

  34. Ehrenson, S. J. Am. chem. Soc. 98, 7510–7514 (1976).

    Article  CAS  Google Scholar 

  35. Rees, D. C. J. molec. Biol. 141, 323–326 (1980).

    Article  CAS  PubMed  Google Scholar 

  36. Burnett, R. M. et al. J. biol. Chem. 249, 4383–4392 (1974).

    CAS  PubMed  Google Scholar 

  37. McLachlan, A. D. & Stewart, M. J. molec. Biol. 103, 271–298 (1976).

    Article  CAS  PubMed  Google Scholar 

  38. Arnott, S. & Wonacott, A. J. J. molec. Biol. 21, 371–383 (1966).

    Article  CAS  PubMed  Google Scholar 

  39. Privalov, P. L. Adv. Protein Chem. 33, 167–241 (1979).

    Article  CAS  PubMed  Google Scholar 

  40. Kauzmann, W. Adv. Protein Chem. 14, 1–63 (1959).

    Article  CAS  PubMed  Google Scholar 

  41. Dijkstra, B. W., Drenth, J., Kalk, K. H. & Vandermaelen, P. J. J. molec. Biol. 124, 53–60 (1978).

    Article  CAS  PubMed  Google Scholar 

  42. Takano, T. et al. J. biol. Chem. 252, 776–785 (1977).

    CAS  PubMed  Google Scholar 

  43. Holbrook, J. J., Liljas, A., Steindel, S. J. & Rossmann, M. G. in The Enzymes Vol. 11 (ed. Boyer, P. D.) 191–292 (Academic, New York, 1975).

    Google Scholar 

  44. Brändén, C.-I., Jörnvall, H., Eklund, H. & Furugren, B. in The Enzymes Vol. 11 (ed. Boyer, P. D.) 103–190 (Academic, New York, 1975).

    Google Scholar 

  45. Buehner, M., Ford, G. C., Moras, D., Olsen, K. W. & Rossmann, M. G. J. molec. Biol. 82, 563–585 (1974).

    Article  CAS  PubMed  Google Scholar 

  46. Schulz, G. E., Elzinga, M., Marx, F. & Schirmer, R. H. Nature 250, 120–123 (1974).

    Article  ADS  CAS  PubMed  Google Scholar 

  47. Wright, C. S., Alden, R. A. & Kraut, J. Nature 221, 235–242 (1969).

    Article  ADS  CAS  PubMed  Google Scholar 

  48. Matthews, D. et al. J. biol. Chem. 253, 6946–6954 (1978).

    CAS  PubMed  Google Scholar 

  49. Banner, D. W. et al. Nature 255, 609–614 (1975).

    Article  ADS  CAS  PubMed  Google Scholar 

  50. Hartsuck, J. A. & Lipscomb, W. N. in The Enzymes Vol. 3 (ed. Boyer, P. D.) 1–56 (Academic, New York, 1971).

    Google Scholar 

  51. Drenth, J., Jansonius, J. N., Koekoek, R. & Wolthers, B. G. in The Enzymes Vol. 3 (ed. Boyer, P. D.) 485–499 (Academic, New York, 1971).

    Google Scholar 

  52. Baker, E. N. J. molec. Biol. 141, 441–484 (1980).

    Article  CAS  PubMed  Google Scholar 

  53. Pollock, E. L., Aider, B. J. & Pratt, L. R. Proc. natn. Acad. Sci. U.S.A. 77, 49–51 (1980).

    Article  ADS  CAS  Google Scholar 

  54. Pethig, T. Dielectric and Electronic Properties of Biological Materials (Wiley, New York, 1979).

    Google Scholar 

  55. Applequist, J. & Mahr, T. G. J. Am. chem. Soc. 88, 5419 (1966).

    Article  CAS  PubMed  Google Scholar 

  56. Kirkwood, J. G. & Westheimer, F. H. J. chem. Phys. 6, 5419–5429 (1938); 7, 437 (1939).

    Google Scholar 

  57. Bernstein, F. C. et al. J. molec. Biol. 112, 535–542 (1977).

    Article  CAS  PubMed  Google Scholar 

  58. Levitt, M. & Greer, J. J. molec. Biol. 114, 181–239 (1977).

    Article  CAS  PubMed  Google Scholar 

  59. Sawyer, L. et al. J. molec. Biol. 118, 137–208 (1978).

    Article  CAS  PubMed  Google Scholar 

  60. Wyckoff, H. W. et al. J. biol. Chem. 245, 305–328 (1970).

    CAS  PubMed  Google Scholar 

  61. Hardman, K. D. & Ainsworth, C. F. Biochemistry 11, 4910–4919 (1972).

    Article  CAS  PubMed  Google Scholar 

  62. Reeke, G. N., Becker, J. W. & Edelman, G. M. J. biol Chem. 250, 1525–1547 (1975).

    CAS  PubMed  Google Scholar 

  63. Watenpaugh, K. D., Sieker, L. C., Herriott, J. C. & Jensen, L. H. Acta crystallogr. B29, 943–956 (1973).

    Article  CAS  Google Scholar 

  64. Carter, C. W. et al. J. biol. Chem. 249, 4212–4225 (1974).

    CAS  PubMed  Google Scholar 

  65. Poljak, R. J., Amzel, L. M., Chen, B. L., Phizackerley, R. P. & Saul, F. Proc. natn. Acad. Sci. U.S.A. 71, 3440–3444 (1974).

    Article  ADS  CAS  Google Scholar 

  66. Blake, C. C. F., Geisow, M., Oatley, S. J., Rérat, B. & Rérat, C. J. molec. Biol. 121, 339–356 (1978).

    Article  CAS  PubMed  Google Scholar 

  67. Tsernoglou, D. & Petsko, G. A. Proc. natn. Acad. Sci. U.S.A. 74, 971–974 (1977).

    Article  ADS  CAS  Google Scholar 

  68. Low, B. W. et al. Proc. natn. Acad. Sci. U.S.A. 73, 2991–2994 (1976).

    Article  ADS  CAS  Google Scholar 

  69. Richardson, J. S., Thomas, K. A., Rubin, B. H. & Richardson, D. C. Proc. natn. Acad. Sci. U.S.A. 72, 1349–1353 (1975).

    Article  ADS  CAS  Google Scholar 

  70. Matthews, B. W., Fenna, R. A., Bolognesi, M. C., Schmid, M. F. & Olson, J. M. J. molec. Biol. 131, 259–285 (1979).

    Article  CAS  PubMed  Google Scholar 

  71. Mitsui, Y., Satow, Y., Watanabe, Y. & litaka, Y. J. molec. Biol. 131, 697–724 (1979).

    Article  CAS  PubMed  Google Scholar 

  72. Sweet, R. M., Wright, H. T., Janin, J., Chothia, C. H. & Blow, D. M. Biochemistry 13, 4212–4228 (1974).

    Article  CAS  PubMed  Google Scholar 

  73. Harrison, S. C., Olson, A. J., Schutt, C. E. & Winkler, F. K. Nature 276, 368–378 (1978).

    Article  ADS  CAS  PubMed  Google Scholar 

  74. Tang, J., James, M. N. G., Hsu, I. N., Jenkins, J. A. & Blundell, T. L. Nature 271, 618–621 (1978).

    Article  ADS  CAS  PubMed  Google Scholar 

  75. Hermans, J. & McQueen, J. E. Acta crystallogr. A30, 730–739 (1974).

    Article  Google Scholar 

  76. Pauling, L. & Corey, R. B. Proc. natn. Acad. Sci. U.S.A. 39, 253–256 (1953).

    Article  ADS  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Chemical Physics, Department of Chemistry, University of Groningen, Nijenborgh 16, 9747 AG, Groningen, The Netherlands

    Wim G. J. Hol & Louis M. Halie

  2. Biophysics Department, Max Planck Institute of Medical Research, Jahnstrasse 29, Heidelberg, FRG

    Christian Sander

Authors
  1. Wim G. J. Hol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Louis M. Halie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Sander
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hol, W., Halie, L. & Sander, C. Dipoles of the α-helix and β-sheet: their role in protein folding. Nature 294, 532–536 (1981). https://doi.org/10.1038/294532a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/294532a0

  • Springer Nature Limited

This article is cited by

Search

Navigation