Journal of Protein Chemistry

, Volume 7, Issue 1, pp 1–34 | Cite as

Entropic elastic processes in protein mechanisms. I. Elastic structure due to an inverse temperature transition and elasticity due to internal chain dynamics

  • Dan W. Urry
Review

Abstract

Numerous physical characterizations clearly demonstrate that the polypentapeptide of elastin (Val1-Pro2-Gly3-Val4-Gly5)u in water undergoes an inverse temperature transition. Increase in order occurs both intermolecularly and intramolecularly on raising the temperature from 20 to 40°C. The physical characterizations used to demonstrate the inverse temperature transition include microscopy, light scattering, circular dichroism, the nuclear Overhauser effect, temperature dependence of composition, nuclear magnetic resonance (NMR) relaxation, dielectric relaxation, and temperature dependence of elastomer length. At fixed extension of the cross-linked polypentapeptide elastomer, the development of elastomeric force is seen to correlate with increase in intramolecular order, that is, with the inverse temperature transition. Reversible thermal denaturation of the ordered polypentapeptide is observed with composition and circular dichroism studies, and thermal denaturation of the crosslinked elastomer is also observed with loss of elastomeric force and elastic modulus. Thus, elastomeric force is lost when the polypeptide chains are randomized due to heating at high temperature. Clearly, elastomeric force is due to nonrandom polypeptide structure. In spite of this, elastomeric force is demonstrated to be dominantly entropic in origin. The source of the entropic elastomeric force is demonstrated to be the result of internal chain dynamics, and the mechanism is called the librational entropy mechanism of elasticity. There is significant application to the finding that elastomeric force develops due to an inverse temperature transition. By changing the hydrophobicity of the polypeptide, the temperature range for the inverse temperature transition can be changed in a predictable way, and the temperature range for the development of elastomeric force follows. Thus, elastomers have been prepared where the development of elastomeric force is shifted over a 40°C temperature range from a midpoint temperature of 30°C for the polypentapeptide to 10°C by increasing hydrophobicity with addition of a single CH2 moiety per pentamer and to 50°C by decreasing hydrophobicity. The implications of these findings to elastic processes in protein mechanisms are (1) When elastic processes are observed in proteins, it is unnecessary, and possibly incorrect, to attempt description in terms of random chain networks and random coils; (2) rather than requiring a random chain network characterized by a random distribution of end-to-end chain lengths, entropic elastomeric force can be exhibited by a single, short peptide segment; (3) perhaps of greatest significance, whether occurring in a short peptide segment or in a fibrillar protein, it should be possible reversibly to turn elastomeric force on and off by reversibly changing the hydrophobicity of the polypeptide. Phosphorylation and dephosphorylation would be the most obvious means of changing the hydrophobicity of a polypeptide. These considerations are treated in Part 2: Simple (Passive) and Coupled (Active) Development of Elastic Forces (see Urry, 1988).

Key words

inverse temperature transition entropic elasticity thermomechanical transduction mechanochemical coupling polypentapeptide of elastin librational entropy mechanism of elasticity internal chain dynamics 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aaron, B. B., and Gosline, J. M. (1980).Nature (Lond.) 287, 865–867.Google Scholar
  2. Aaron, B. B., and Gosline, J. M. (1981).Biopolymers 20, 1247–1260.Google Scholar
  3. Andrady, A. L., and Mark, J. E. (1980).Biopolymers 19, 849–855.Google Scholar
  4. Barnes, C., Evans, J. A., and Lewis, T. J. (1985).J. Acoust. Soc. Am. 78(1), 6–11.Google Scholar
  5. Buchet, R., Luan, C.-H., Prasad, K. U., Harris, R. D., and Urry, D. W. (1988).J. Phys. Chem. (in press).Google Scholar
  6. Bungenberg de Jong, H. G. (1949). InColloid Science, Vol. 2 (Kruyt, H. R., ed.), Elsevier/North-Holland Publisher, Amsterdam, pp. 232–258.Google Scholar
  7. Bungenberg de Jong, H. G., and Kruyt, H. R. (1929).Proc. Kon. Ned. Akad. Wet. 32, 849–856.Google Scholar
  8. Bungenberg de Jong, H. G., and Kruyt, H. R. (1930).Kolloid Z. 50, 39–48.Google Scholar
  9. Cerf, R. (1985).Biophys. J. 47, 751–756,Google Scholar
  10. Cho, K. C., Leung, W. P., Mok, H. Y., and Cjoy, C. L. (1985).Biochim. Biophys. Acta 830, 36–44.Google Scholar
  11. Cleary, E. G., and Moont, M. (1977).Adv. Exp. Med. Biol. 79, 477–490.Google Scholar
  12. Cook, W. J., Einspahr, H. M., Trapane, T. L., Urry, D. W., and Bugg, C. W. (1980).J. Am. Chem. Soc. 102, 5502–5505.Google Scholar
  13. Dauber, P., Goodman, M., Hagler, A. T., Osguthorpe, D., Sharon, R., and Stern, P. (1981). InACS Symposium Series, No. 173.Supercomputers in Chemistry (Lykos, P., and Shavitt, I., eds.), American Chemical Society, Washington, D.C., pp. 161–191.Google Scholar
  14. Dorrington, K. L., and McCrum, N. G. (1977).Biopolymers 16, 1201–1222.Google Scholar
  15. Eyring, H. (1932).Phys. Rev. 39, 746–748.Google Scholar
  16. Eyring, H., Henderson, D., Stover, B. J., and Eyring, E. M. (1964).Statistical Mechanics and Dynamics, John Wiley & Sons, New York, p. 90.Google Scholar
  17. Fleming, W. W., Sullivan, C. E., and Torchia, D. A. (1980).Biopolymers 19, 597–618.Google Scholar
  18. Flory, P. J. (1953).Principles of Polymer Chemistry, Cornell University Press, Ithaca, New York.Google Scholar
  19. Flory, P. J., Ciferri, A., and Hoeve, C. A. J. (1960).J. Polymer Sci. 45, 235–236.Google Scholar
  20. Frank, H. S., and Evans, M. W. (1945).J. Chem. Phys. 13, 493–407.Google Scholar
  21. Franzblau, C., and Lent, R. W. (1969). InBrookhaven Symposium in Biology: Structure, Function and Evolution in Proteins, Vol. 2, Associated Universities, Inc., Upton, N.Y., pp. 358–377.Google Scholar
  22. Gosline, J. M. (1978).Biopolymers 17, 677–695.Google Scholar
  23. Gosline, J. M. (1980). InThe Mechanical Properties of Biological Materials (Vincent, J. F. V., and Currey, J. D., eds.), Cambridge University Press, London, pp. 331–357.Google Scholar
  24. Gosline, J. M., and Rosenbloom, J. (1984). InExtracellular Matrix Biochemistry (Piez, K. A., and Reddi, A. H., eds.), Elsevier/North-Holland Publishers, Amsterdam, pp. 191–227.Google Scholar
  25. Gray, W. R., Sandberg, L. B., and Foster, J. A. (1973).Nature (Lond.) 246, 461–466.Google Scholar
  26. Henze, R., and Urry, D. W. (1985).J. Am. Chem. Soc. 107, 2991–2993.Google Scholar
  27. Hoeve, C. A. J., and Flory, P. J. (1958).J. Am. Chem. Soc. 80, 6523–6526.Google Scholar
  28. Hoeve, C. A. J., and Flory, P. J. (1974).Biopolymers 13, 677–686.Google Scholar
  29. Karplus, M., and McCammon, J. A. (1981).CRC Crit. Rev. Biochem. 9, 293–349.Google Scholar
  30. Kauzmann, W. (1959).Adv. Protein Chem. 14, 1–63.Google Scholar
  31. Lyerla, J. R., and Torchia, D. A. (1975).Biochemistry 13, 5175–5183.Google Scholar
  32. Mandelkern, L. (1983).An Introduction to Macromolecules, 2nd ed., Springer-Verlag, New York.Google Scholar
  33. Momany, F. A., Carruthers, L. M., McGuire, R. F., and Scheraga, H. A. (1974).J. Phys. Chem. 78, 1595–1620.Google Scholar
  34. Momany, F. A., McGuire, R. F., Burgess, A. W., and Scheraga, H. A. (1975).J. Phys. Chem. 7, 2361–2381.Google Scholar
  35. Onsager, L. (1931).Phys. Rev. 37, 405–426.Google Scholar
  36. Partridge, S. M. (1962).Adv. Protein Chem. 17, 227–302.Google Scholar
  37. Pethig, R. (1979). InDielectric and Electronic Properties of Biological Materials, John Wiley & Sons, New York, pp. 100–149.Google Scholar
  38. Petruska, J. A., and Sandberg, L. B. (1968).Biochem. Biophys. Res. Commun. 33, 222–228.Google Scholar
  39. Queslel, J. P., and Mark, J. E. (1986). InEncyclopedia of Polymer Science and Engineering, Vol. 5, 2nd ed., John Wiley & Sons, pp. 365–408.Google Scholar
  40. Sandberg, L. B., Gray, W. R., and Franzblau, C. (1977).Adv. Exp. Med. Biol. 79, 259–261.Google Scholar
  41. Sandberg, L. B., Soskel, N. T., and Leslie, J. B. (1981).N. Engl. J. Med. 304, 566–579.Google Scholar
  42. Schneider, F., Müller-Landau, F., and Mayer, A. (1969).Biopolymers 8, 537–544.Google Scholar
  43. Swaminathan, S., Harrison, S. W., and Beveridge, D. L. (1978).J. Am. Chem. Soc. 100, 5705.Google Scholar
  44. Tanford, C. (1973).The Hydrophobic Effect: Formation of Micelles and Biological Membranes, John Wiley & Sons, New York.Google Scholar
  45. Thomas, G. J., Jr., Prescott, B., and Urry, D. W. (1987).Biopolymers 26, 921–934.Google Scholar
  46. Torchia, D. A., Batchelder, L. S., Fleming, W. W., Jelinski, L. W., Sarkar, S. K., and Sullivan, C. E. (1983). InMobility and Function in Proteins and Nucleic Acids (Porter, R., O'Connor, M., and Whelan, J., eds.), Pitman Publishers, London, pp. 98–115.Google Scholar
  47. Torchia, D. A., and Piez, K. A. (1973).J. Mol. Biol. 76, 419–424.Google Scholar
  48. Urry, D. W. (1972).Proc. Natl. Acad. Sci. USA 69, 1610–1614.Google Scholar
  49. Urry, D. W. (1974). InArterial Mesenchyme and Arteriosclerosis (Wagner, W. D., and Clarkson, T. B., eds.), Plenum Publishing Corporation, New York,Adv. Exp. Med. Biol. 43, pp. 211–243.Google Scholar
  50. Urry, D. W. (1982).Methods Enzymol. 82, 673–716.Google Scholar
  51. Urry, D. W. (1983).Ultrastruct. Pathol. 4, 227–251.Google Scholar
  52. Urry, D. W. (1984).J. Protein Chem. 3, 403–436.Google Scholar
  53. Urry, D. W. (1985). InBiomolecular Stereodynamics. Vol. III (Sarma, R. H., and Sarma, M. H., eds.), Adenine Press, Guilderland, New York, pp. 173–196.Google Scholar
  54. Urry, D. W. (1987).Advances in the Molecular Biology of Connective Tissue Fibrous Proteins, Professor S. M. Partridge Festschrift Volume, (L. Gotte, ed.), Scottish Academic Press, Edinburgh, pp. 25–50.Google Scholar
  55. Urry, D. W. (1988).J. Protein Chem. 7, 81–114.Google Scholar
  56. Urry, D. W., and Long, M. M. (1976).CRC Crit. Rev. Biochem. 4, 1–45.Google Scholar
  57. Urry, D. W., and Prasad, K. U. (1985). InBiocompatibility of Tissue Analogues (Williams, D. F., ed.), CRC Press, Boca Raton, Florida, pp. 89–116.Google Scholar
  58. Urry, D. W., and Venkatachalam, C. M. (1983).Int. J. Quant. Chem. Quant. Biol. Symp. 10, 81–93.Google Scholar
  59. Urry, D. W., Okamoto, K., Harris, R. D., Hendrix, C. F. and Long, M. M. (1976).Biochemistry 15, 4083–4089.Google Scholar
  60. Urry, D. W., Khaled, M. A., Rapaka, R. S., and Okamoto, K. (1977).Biochem. Biophys. Res. Commun. 79, 700–706.Google Scholar
  61. Urry, D. W., Venkatachalam, C. V., Long, M. M., and Prasad, K. U. (1982). InConformation in Biology (Srinivasan, R., and Sarma, R. H., eds.), G. N. Ramachandran Festschrift Volume, Adenine Press, Guilderland, New York, pp. 11–27.Google Scholar
  62. Urry, D. W., Trapane, T. L., Long, M. M., and Prasad, K. U. (1983a).J. Chem. Soc. Farad. Trans. 179, 853–868.Google Scholar
  63. Urry, D. W., Trapane, T. L., Wood, S. A., Walker, J. T., Harris, R. D., and Prasad, K. U. (1983b).Int. J. Peptide Protein Res. 22, 164–175.Google Scholar
  64. Urry, D. W., Henze, R., Harris, R. D., and Prasad, K. U. (1984).Biochem. Biophys. Res. Commun. 125, 1082–1088.Google Scholar
  65. Urry, D. W., Henze, R., Redington, P., Long, M. M., and Prasad, K. U. (1985a).Biochem. Biophys. Res. Commun. 128, 1000–1006.Google Scholar
  66. Urry, D. W., Prasad, K. U., Trapane, T. L., Iqbal, M. Harris, R. D., and Henze, R. (1985b).Polymer. Mater. Sci. Eng. 53, 241–245.Google Scholar
  67. Urry, D. W., Shaw, R. G., and Prasad, K. U. (1985c).Biochem. Biophys. Res. Commun. 130, 50–57.Google Scholar
  68. Urry, D. W., Trapane, T. L., Iqbal, M. Venkatachalam, C. M., and Prasad, K. U. (1985d).Biochemistry 24, 5182–5189.Google Scholar
  69. Urry, D. W., Trapane, T. L., and Prasad, K. U. (1985e).Biopolymers 24, 2345–2356.Google Scholar
  70. Urry, D. W., Venkatachalam, C. M., Wood, S. A., and Prasad, K. U. (1985f). InStructure and Motion: Membranes, Nucleis Acids and Proteins (Clementi, E., Corongiu, G., Sarma, M. H., and Sarma, R. H., eds.), Adenine Press, Guilderland, New York, pp. 185–203.Google Scholar
  71. Urry, D. W., Harris, R. D., Long, M. M., and Prasad, K. U. (1986a).Int. J. Peptide Protein Res. 28, 649–660.Google Scholar
  72. Urry, D. W., Haynes, B., and Harris, R. D. (1986b).Biochem. Biophys. Res. Commun. 141, 749–755.Google Scholar
  73. Urry, D. W., Long, M. M., Harris, R. D., and Prasad, K. U. (1986c).Biopolymers 25, 1939–1953.Google Scholar
  74. Urry, D. W., Trapane, T. L., McMichens, R. B., Iqbal, M., Harris, R. D., and Prasad, K. U. (1986d).Biopolymers 25, S209-S228.Google Scholar
  75. Urry, D. W., Prasad, K. U., Trapane, T. L., Iqbal, M., Harris, R. D., Okamoto, K., and Henze, R. (1987a).Peptide Chem. (in press).Google Scholar
  76. Venkatachalam, C. M., and Urry, D. W. (1981).Macromolecules 14, 1225–1229.Google Scholar
  77. Venkatachalam, C. M., and Urry, D. W. (1986).Int. J. Quant. Chem. Quant. Biol. Symp. 12, 15–24.Google Scholar
  78. Volpin, D., Urry, D. W., Pasquali-Ronchetti, I., and Gotte, L. (1976).Micron 7, 193–198.Google Scholar
  79. Weis-Fogh, T., and Andersen, S. A. (1970).Nature (Lond.) 227, 718–721.Google Scholar
  80. Zana, R., and Tondre, C. (1972).J. Phys. Chem. 76, 1737–1743.Google Scholar

Copyright information

© Plenum Publishing Corporation 1988

Authors and Affiliations

  • Dan W. Urry
    • 1
  1. 1.Laboratory of Molecular BiophysicsThe University of Alabama at BirminghamBirmingham

Personalised recommendations