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Conformational Flexibility in Protein Molecules from Robert Huber

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Conformational Flexibility in Protein Molecules from Robert Huber 538 Nature Vol. 280 16 August 1979 Conformational flexibility in protein molecules from Robert Huber IN describing protein molecules the term in providing us with an overall view of the Several examples of protein crystal flexibility is used with quite different molecule in contrast to the spectroscopic structures are now known where disorder meanings. A precise definition for a techniques which focus on a particular (either dynamic or static) is a dominating particular protein molecule would require label. However, there are a number of aspect: antibody molecules 14. 15, the determination of the number, energy theoretical and experimental problems. As trypsinogen 16, citrate synthase17, tobacco and geometry of the various stable the physical diffraction process is mosaic virus protein 18• 19 and tomato bushy conformational states the molecule might instantaneous compared with lattice stunt virus20 • In these molecules substantial have, the kinetic parameters of vibrations, the 'temperature' factor parts show no significant electron density interconversion and the thermal motion of determined crystallographically does not indicating disorder in the crystalline state. all the atoms in each conformer: a differentiate between thermal motion and In some of the molecular species rigid states considerable task, requiring a great variety static disorder. Static disorder may have are known with different functions, of experimental techniques, if feasible at components from conformational micro­ providing evidence for the functional all. Several rather different experimental heterogeneity of the protein molecules significance of large scale disorder 21 • approaches have provided evidence that (substates or microscopic states) and from Except in the case of TMV protein, where protein molecules are indeed flexible: lattice defects. The interesting parameters, NMR experiments have demonstrated deuterium-hydrogen exchange under non­ thermal motion and substates are difficult increased thermal mobility of the denaturing conditions 1, fluorescence to determine accurately and still more disordered segments 22 , it is unclear which quenching of internal tryptophan residues difficult to separate from one another. The type of disorder (conformational by oxygen diffusing into the protein experimental problem has been partly heterogeneity or thermal motion) prevails molecule2, ESR, NMR, and fluorescence overcome since the development of in these examples. Lattice defects involving depolarisation. These last spectroscopic techniques for refinement of protein the molecule as a whole are excluded, of techniques allow one to determine the crystal structures, some five years ago. course, as most parts of the molecules are mobility as a function of temperature of Protein structures were successfully well ordered. certain residues whose spectroscopic signal refined t0-!2 using principles borrowed from Two reports in this issue of Nature are can be identified. The power of these small molecule crystallography, centred on the question of conformational methods is clearly demonstrated by recent extensively modified and adapted to the disorder and its static and dynamic experiments, using NMR techniques, much larger problem 13 • From these studies components determined by crystal­ which show that the aromatic rings of it was obvious that the 'temperature' lographic methods in two different tyrosyl and phenylalanyl residues in factors of individual atoms were important systems: lysozyme (Artymiuk et a/. page pancreatic trypsin inhibitor (PTI) flip 3-5 _ variables for the correct description of the 563) and myoglobin (Frauenfelder et a/. Model calculations show that aromatic protein structure. However, the values page 558). Two different lysozyme species ring flipping is a consequence of were regarded with some suspicion, as they crystallising in different crystal forms have substantial breathing motions of the changed from atom to atom in a rather been carefully refined and atomic protein, which include movement of the erratic way due to the limited resolution of 'temperature' factors determined. When polypeptide backbone6• 7• The mobility of the diffraction data. But, when the these were averaged for the main chain tryptophanyl residues has been probed, 'temperature' factors were averaged for atoms of each residue a close using very short and intense light pulses to rigid groups and smoothed along the main correspondence between the two crystal 8 measure fluorescence depolarisation • and side chains, physically reasonable structures was obvious, suggesting that the Motions in the picosecond time range are features were obvious: 'temperature' variation in 'temperature' factor along the found, but the degree of flexibility is factors increased in external polypeptide chain is a molecular property and not different for different protein species, loops and external side chains were more seriously influenced by crystal packing. A some being rather rigid, some soft. Recent mobile than internal ones. detailed mathematical analysis indicates a molecular dynamics calculations on PTI9 rigid body translation and Iibration of the show structural fluctuations in the molecule as a whole, overlaid with picosecond range of a size in rough additional flexibility of some external 1. Woodward& Hilton A. Rev. Biophys. Bioeng. 8, 99(1979). agreement with the observed 2. Lakowicz & Weber Biochemistry 12,417 (1973). loops. Among these are the loops crystallographic temperature factor 10 and 3. Snyder eta/. Biochemistry 14, 3765 (1975). determining the substrate binding cleft in promise to provide the theoretical 4. Wagner eta/. Biophys. Struct. Mechanism 2, 139 (1976). lysozyme. A positive correlation between 5. Snyder eta/. Biochemistry 15, 2275 (1976). background to motions in proteins. 6. Gelin & Karplus Proc. natn. A cad. Sci. U.S.A. 71, 2002 ordered secondary structure and 'rigidity', However, the computational problems are (1975). and between shielding of amino acid side 7. Hetzel et al. Biophys. Struct. Mechanism l, 159 (1976). enormous and, so far, allow the analysis of 8. Munro eta/. Proc natn. Acad. Sci. U.S.A. 76,56 (1979). chains and their 'mobility' is obvious. The a small protein molecule such as PTI for a 9. Karplus & McCommon Naturel77, 578 (1979). slightly enhanced 'mobility' of the 10. Deisenhofer & Steigemann Acta Cryst. 831,238 (1975). few picoseconds only. This makes 11. Watenpaugh eta/. Acta Cryst. 829,943 (1973). substrate binding area is intriguing, in extrapolation to equilibrium properties 12. Huber et al. J. mo/ec.Bio/. 89, 73 (1974). particular, if it were to be found that these and comparison with the time-averaged 13. Diamond J. molec. Bioi. U, 371 (1974). segments 'rigidify' on substrate binding; 14. Colman eta/. J. mo/ec. Bioi. 100, 257 (1976). crystal structures problematic, as does the IS. Ely eta/. Biochemistry 17,820 (1978). one wonders why nature utilises such small neglect of solvent effects in calculations 16. Huber & Bode Ace. Chem. Res. 11, 114 (1978). effects, having in mind the drastic 17. Wiegand eta/. EurJ. Biochem. 93,41 (1978). performed to date. More refined dynamics 18. Bloomer eta/. Nature l76, 362 (1978). segmental flexibility in the examples calculations are currently being pursued. 19. Stubbs eta/. Nature 167,216 (1977). discussed before. Artymiuk et a/. do not 20. Harrison eta/. Nature 276, 368 (1978). Protein crystallography as a means to 21. Huber Trends in Biochem Sci. (in the press). and cannot dissect the 'temperature' gain information about flexibility is unique 22. Jardetzky era/. Nature 273, 564 (1978). factors observed into their static and 23. Parak eta/. Acta Cryst. Al7, 573 (1971). dynamic contributions. This problem is the 24. Epp eta/. Biochemistry 14,4943 (1975). Robert Huber is at the Max-Planck-lnstitut fiir 25. Steigemann&WeberJ. mo/ec. Bioi. ll7,309(1979). main object of the paper by Frauenfelder et Biochemie, Munich. 26. Richards J. molec. Bioi. 82, I (1974). a/. who analysed and carefully refined 0028-0836/79/330538-01 SOl.OO ©Macmillan Journals Ltd 1979 Nature Vol. 280 16August 1979 539 myoglobin crystals at various temperatures measurements are insensitive to static reach the satellite, by which time it will from 300 to 220 K, with the ultimate goal of disorder as long as the equilibration have spread out in space as a result of the differentiating static and dynamic disorder between different conformers is slow velocity dispersion. Reasonable by their low temperature limit. As protein compared with the life time of the excited assumptions show that it will take about 7 h crystals contain solvent which may not be Mtissbauer nucleus. The question of to sweep past the spacecraft. The allowed to freeze, the temperature range whether a protein molecule is to be experiment was working between 7 that is covered is small as is the regarded as a vibrating aperiodic February, 1972 and 2 August, 1974 and effect on the 'temperature' parameters crystalline solid or a 'semiliquid' 'glass', during this time 19 group bursts were seen, determined. characterised by a larger number of individual groups taking between 40 min The principal result of Frauenfelder et substates of similar energy, is a topic of and 13 h to pass the spacecraft. Fechtig, a/., that 'temperature' factors are increased lively discussion at present. Of course, Grtin and Morflll tried to correlate the in the peripheral parts of myoglobin and there is clear evidence for alternative side observation times of the groups with the correlate with the
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