Skip to main content
PMC home page
Protein Science : A Publication of the Protein Society logoLink to Protein Science : A Publication of the Protein Society
. 1995 Feb;4(2):149–158. doi: 10.1002/pro.5560040202

Structure and dynamics of the water around myoglobin.

G N Phillips Jr 1, B M Pettitt 1
PMCID: PMC2143067  PMID: 7757005

Abstract

The interplay between simulations at various levels of hydration and experimental observables has led to a picture of the role of solvent in thermodynamics and dynamics of protein systems. One of the most studied protein-solvent systems is myoglobin, which serves as a paradigm for the development of structure-function relationships in many biophysical studies. We review here some aspects of the solvation of myoglobin and the resulting implications. In particular, recent theoretical and simulation studies unify much of the diverse set of experimental results on water near proteins.

Full Text

The Full Text of this article is available as a PDF (2.9 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ansari A., Berendzen J., Braunstein D., Cowen B. R., Frauenfelder H., Hong M. K., Iben I. E., Johnson J. B., Ormos P., Sauke T. B. Rebinding and relaxation in the myoglobin pocket. Biophys Chem. 1987 May 9;26(2-3):337–355. doi: 10.1016/0301-4622(87)80034-0. [DOI] [PubMed] [Google Scholar]
  2. Badger J. Multiple hydration layers in cubic insulin crystals. Biophys J. 1993 Oct;65(4):1656–1659. doi: 10.1016/S0006-3495(93)81220-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bauminger E. R., Cohen S. G., Nowik I., Ofer S., Yariv J. Dynamics of heme iron in crystals of metmyoglobin and deoxymyoglobin. Proc Natl Acad Sci U S A. 1983 Feb;80(3):736–740. doi: 10.1073/pnas.80.3.736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berendsen H. J., Van Gunsteren W. F., Zwinderman H. R., Geurtsen R. G. Simulations of proteins in water. Ann N Y Acad Sci. 1986;482:269–286. doi: 10.1111/j.1749-6632.1986.tb20961.x. [DOI] [PubMed] [Google Scholar]
  5. Brooks C. L., 3rd, Karplus M. Solvent effects on protein motion and protein effects on solvent motion. Dynamics of the active site region of lysozyme. J Mol Biol. 1989 Jul 5;208(1):159–181. doi: 10.1016/0022-2836(89)90093-4. [DOI] [PubMed] [Google Scholar]
  6. Cheng X. D., Schoenborn B. P. Neutron diffraction study of carbonmonoxymyoglobin. J Mol Biol. 1991 Jul 20;220(2):381–399. doi: 10.1016/0022-2836(91)90020-7. [DOI] [PubMed] [Google Scholar]
  7. Doster W., Bachleitner A., Dunau R., Hiebl M., Lüscher E. Thermal properties of water in myoglobin crystals and solutions at subzero temperatures. Biophys J. 1986 Aug;50(2):213–219. doi: 10.1016/S0006-3495(86)83455-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Doster W., Cusack S., Petry W. Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature. 1989 Feb 23;337(6209):754–756. doi: 10.1038/337754a0. [DOI] [PubMed] [Google Scholar]
  9. Eisenstadt M. NMR relaxation of protein and water protons in diamagnetic hemoglobin solutions. Biochemistry. 1985 Jul 2;24(14):3407–3421. doi: 10.1021/bi00335a004. [DOI] [PubMed] [Google Scholar]
  10. Fullerton G. D., Ord V. A., Cameron I. L. An evaluation of the hydration of lysozyme by an NMR titration method. Biochim Biophys Acta. 1986 Feb 14;869(3):230–246. doi: 10.1016/0167-4838(86)90063-4. [DOI] [PubMed] [Google Scholar]
  11. Fung B. M. Nuclear magnetic resonance study of water interactions with proteins, biomolecules, membranes, and tissues. Methods Enzymol. 1986;127:151–161. doi: 10.1016/0076-6879(86)27013-5. [DOI] [PubMed] [Google Scholar]
  12. Furois-Corbin S., Smith J. C., Kneller G. R. Picosecond timescale rigid-helix and side-chain motions in deoxymyoglobin. Proteins. 1993 Jun;16(2):141–154. doi: 10.1002/prot.340160203. [DOI] [PubMed] [Google Scholar]
  13. Genberg L., Richard L., McLendon G., Miller R. J. Direct observation of global protein motion in hemoglobin and myoglobin on picosecond time scales. Science. 1991 Mar 1;251(4997):1051–1054. doi: 10.1126/science.1998121. [DOI] [PubMed] [Google Scholar]
  14. Goldanskii V. I., Krupyanskii Y. F. Protein and protein-bound water dynamics studied by Rayleigh scattering of Mössbauer radiation (RSMR). Q Rev Biophys. 1989 Feb;22(1):39–92. doi: 10.1017/s003358350000336x. [DOI] [PubMed] [Google Scholar]
  15. Jiang J. S., Brünger A. T. Protein hydration observed by X-ray diffraction. Solvation properties of penicillopepsin and neuraminidase crystal structures. J Mol Biol. 1994 Oct 14;243(1):100–115. doi: 10.1006/jmbi.1994.1633. [DOI] [PubMed] [Google Scholar]
  16. Johnson K. A., Olson J. S., Phillips G. N., Jr Structure of myoglobin-ethyl isocyanide. Histidine as a swinging door for ligand entry. J Mol Biol. 1989 May 20;207(2):459–463. doi: 10.1016/0022-2836(89)90269-6. [DOI] [PubMed] [Google Scholar]
  17. Kossiakoff A. A. Neutron protein crystallography: advances in methods and applications. Annu Rev Biophys Bioeng. 1983;12:159–182. doi: 10.1146/annurev.bb.12.060183.001111. [DOI] [PubMed] [Google Scholar]
  18. Kuntz I. D., Jr, Kauzmann W. Hydration of proteins and polypeptides. Adv Protein Chem. 1974;28:239–345. doi: 10.1016/s0065-3233(08)60232-6. [DOI] [PubMed] [Google Scholar]
  19. Kurinov I. V., Krupianskii Iu F., Suzdalev I. P., Gol'danskii V. I. Izuchenie vliianiia gidratatsii na dinamiku nekotorykh globuliarnykh belkov metodom réleevskogo rasseianiia messbauérovskogo izlucheniia. Biofizika. 1987 Mar-Apr;32(2):210–214. [PubMed] [Google Scholar]
  20. Kuriyan J., Wilz S., Karplus M., Petsko G. A. X-ray structure and refinement of carbon-monoxy (Fe II)-myoglobin at 1.5 A resolution. J Mol Biol. 1986 Nov 5;192(1):133–154. doi: 10.1016/0022-2836(86)90470-5. [DOI] [PubMed] [Google Scholar]
  21. Lee B., Richards F. M. The interpretation of protein structures: estimation of static accessibility. J Mol Biol. 1971 Feb 14;55(3):379–400. doi: 10.1016/0022-2836(71)90324-x. [DOI] [PubMed] [Google Scholar]
  22. Lounnas V., Pettitt B. M., Phillips G. N., Jr A global model of the protein-solvent interface. Biophys J. 1994 Mar;66(3 Pt 1):601–614. doi: 10.1016/s0006-3495(94)80835-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morris A. S., Thanki N., Goodfellow J. M. Hydration of amino acid side chains: dependence on secondary structure. Protein Eng. 1992 Dec;5(8):717–728. doi: 10.1093/protein/5.8.717. [DOI] [PubMed] [Google Scholar]
  24. Olson J. S., Mathews A. J., Rohlfs R. J., Springer B. A., Egeberg K. D., Sligar S. G., Tame J., Renaud J. P., Nagai K. The role of the distal histidine in myoglobin and haemoglobin. Nature. 1988 Nov 17;336(6196):265–266. doi: 10.1038/336265a0. [DOI] [PubMed] [Google Scholar]
  25. Parak F. Correlation of protein dynamics with water mobility: Mössbauer spectroscopy and microwave absorption methods. Methods Enzymol. 1986;127:196–206. doi: 10.1016/0076-6879(86)27016-0. [DOI] [PubMed] [Google Scholar]
  26. Parak F., Knapp E. W. A consistent picture of protein dynamics. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7088–7092. doi: 10.1073/pnas.81.22.7088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Parak F., Knapp E. W., Kucheida D. Protein dynamics. Mössbauer spectroscopy on deoxymyoglobin crystals. J Mol Biol. 1982 Oct 15;161(1):177–194. doi: 10.1016/0022-2836(82)90285-6. [DOI] [PubMed] [Google Scholar]
  28. Pethig R., Kell D. B. The passive electrical properties of biological systems: their significance in physiology, biophysics and biotechnology. Phys Med Biol. 1987 Aug;32(8):933–970. doi: 10.1088/0031-9155/32/8/001. [DOI] [PubMed] [Google Scholar]
  29. Phillips G. N., Jr, Arduini R. M., Springer B. A., Sligar S. G. Crystal structure of myoglobin from a synthetic gene. Proteins. 1990;7(4):358–365. doi: 10.1002/prot.340070407. [DOI] [PubMed] [Google Scholar]
  30. Phillips S. E. Structure and refinement of oxymyoglobin at 1.6 A resolution. J Mol Biol. 1980 Oct 5;142(4):531–554. doi: 10.1016/0022-2836(80)90262-4. [DOI] [PubMed] [Google Scholar]
  31. Privalov P. L., Griko YuV, Venyaminov SYu, Kutyshenko V. P. Cold denaturation of myoglobin. J Mol Biol. 1986 Aug 5;190(3):487–498. doi: 10.1016/0022-2836(86)90017-3. [DOI] [PubMed] [Google Scholar]
  32. Privalov P. L., Makhatadze G. I. Contribution of hydration and non-covalent interactions to the heat capacity effect on protein unfolding. J Mol Biol. 1992 Apr 5;224(3):715–723. doi: 10.1016/0022-2836(92)90555-x. [DOI] [PubMed] [Google Scholar]
  33. Quillin M. L., Arduini R. M., Olson J. S., Phillips G. N., Jr High-resolution crystal structures of distal histidine mutants of sperm whale myoglobin. J Mol Biol. 1993 Nov 5;234(1):140–155. doi: 10.1006/jmbi.1993.1569. [DOI] [PubMed] [Google Scholar]
  34. Rohlfs R. J., Mathews A. J., Carver T. E., Olson J. S., Springer B. A., Egeberg K. D., Sligar S. G. The effects of amino acid substitution at position E7 (residue 64) on the kinetics of ligand binding to sperm whale myoglobin. J Biol Chem. 1990 Feb 25;265(6):3168–3176. [PubMed] [Google Scholar]
  35. Rupley J. A., Careri G. Protein hydration and function. Adv Protein Chem. 1991;41:37–172. doi: 10.1016/s0065-3233(08)60197-7. [DOI] [PubMed] [Google Scholar]
  36. Scanlon W. J., Eisenberg D. Solvation of crystalline proteins: theory and its application to available data. J Mol Biol. 1975 Nov 5;98(3):485–502. doi: 10.1016/s0022-2836(75)80082-9. [DOI] [PubMed] [Google Scholar]
  37. Schoenborn B. P. Solvent effect in protein crystals. A neutron diffraction analysis of solvent and ion density. J Mol Biol. 1988 Jun 20;201(4):741–749. doi: 10.1016/0022-2836(88)90470-6. [DOI] [PubMed] [Google Scholar]
  38. Steinbach P. J., Brooks B. R. Protein hydration elucidated by molecular dynamics simulation. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9135–9139. doi: 10.1073/pnas.90.19.9135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Teeter M. M. Water structure of a hydrophobic protein at atomic resolution: Pentagon rings of water molecules in crystals of crambin. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6014–6018. doi: 10.1073/pnas.81.19.6014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Teeter M. M. Water-protein interactions: theory and experiment. Annu Rev Biophys Biophys Chem. 1991;20:577–600. doi: 10.1146/annurev.bb.20.060191.003045. [DOI] [PubMed] [Google Scholar]
  41. Thanki N., Thornton J. M., Goodfellow J. M. Distributions of water around amino acid residues in proteins. J Mol Biol. 1988 Aug 5;202(3):637–657. doi: 10.1016/0022-2836(88)90292-6. [DOI] [PubMed] [Google Scholar]
  42. WATSON H. C., KENDREW J. C. The amino-acid sequence of sperm whale myoglobin. Comparison between the amino-acid sequences of sperm whale myoglobin and of human hemoglobin. Nature. 1961 May 20;190:670–672. doi: 10.1038/190670a0. [DOI] [PubMed] [Google Scholar]
  43. WEISS J. J. NATURE OF THE IRON-OXYGEN BOND IN OXYHAEMOGLOBIN. Nature. 1964 Jul 11;203:182–183. [PubMed] [Google Scholar]
  44. Wlodawer A. Neutron diffraction of crystalline proteins. Prog Biophys Mol Biol. 1982;40(1-2):115–159. doi: 10.1016/0079-6107(82)90012-8. [DOI] [PubMed] [Google Scholar]
  45. Yang P. H., Rupley J. A. Protein--water interactions. Heat capacity of the lysozyme--water system. Biochemistry. 1979 Jun 12;18(12):2654–2661. doi: 10.1021/bi00579a035. [DOI] [PubMed] [Google Scholar]
  46. Zipp A., Kauzmann W. Pressure denaturation of metmyoglobin. Biochemistry. 1973 Oct 9;12(21):4217–4228. doi: 10.1021/bi00745a028. [DOI] [PubMed] [Google Scholar]

Articles from Protein Science : A Publication of the Protein Society are provided here courtesy of The Protein Society

RESOURCES