Springer Protocols: Abstract: Protein-Ligand Interaction Probed by Time-Resolved Crystallography

Protein-Ligand Interaction Probed by Time-Resolved Crystallography

By: Marius Schmidt², Hyotcherl Ihee³, Reinhard Pahl⁴, Vukica Šrajer⁵

Abstract

Full Text

Download PDF (476K)

Time-resolved (TR) crystallography is a unique method for determining the structures of intermediates in biomolecular reactions. The technique reached its mature stage with the development of the powerful third-generation synchrotron X-ray sources, and the advances in data processing and analysis of timeresolved Laue crystallographic data. A time resolution of 100 ps has been achieved and relatively small structural changes can be detected even from only partial reaction initiation. The remaining challenge facing the application of this technique to a broad range of biological systems is to find an efficient and rapid, system-specific method for the reaction initiation in the crystal. Other frontiers for the technique involve the continued improvement in time resolution and further advances in methods for determining intermediate structures and reaction mechanisms. The time-resolved technique, combined with trapping methods and computational approaches, holds the promise for a complete structure-based description of biomolecular reactions.

Affiliation(s): (2) Department of Physics, Technical University of Munich, Garching, Germany
(3) Department of Chemistry and School of Molecular Science, KAIST, Daejeon, South Korea
(4) Consortium for Advanced Radiation Sources, The University of Chicago, Chicago, IL
(5) Consortium for Advanced Radiation Sources and Department of Biochemistry and Molecular Biology, Chicago, IL

Book Title: Protein-Ligand Interactions: Methods and Applications

Series: Methods in Molecular Biology | Volume: 305 | Pub. Date: Mar-21-2005 | Page Range: 115-154 | DOI: 10.1385/1-59259-912-5:115

Subject: Protein Science

Key Words: Time-resolved macromolecular crystallography - Laue diffraction - intermediate states - reaction mechanism - SVD

References

Download References

1.	Moffat K. and Henderson R. (1995) Freeze trapping of reaction intermediates. Curr. Opin. Struct. Biol. 5, 656–663.

2.	Schlichting I. and Chu K. (2000) Trapping intermediates in the crystal: ligand binding to myoglobin. Curr. Opin. Struct. Biol. 10, 744–752.

3.	Stoddard B. L. (2001) Trapping reaction intermediates in macromolecular crystals for structural Analysis. Methods in Enzymology 24, 125–138.

4.	Ursby T., Weik M., Fioravanti E., Delarue M., Goeldner M., and Bourgeois D. (2002) Cryophotolysis of caged compounds: a technique for trapping interme-diate states in protein crystals. Acta Cryst. D58, 607–614.

5.	Hellingwerf K., Hendriks J., and Gensch T. (2003) On the configurational and conformational changes in photoactive yellow protein that leads to signal generation in Ectothiorhodospira halophila.J Biol. Phys. 28, 295–412.

6.	Brudler R., Rammelsberg R., Woo T. T., Getzoff E. D., and Gerwert K. (2001) Structure of the I₁ early intermediate of photoactive yellow protein by FTIR spectroscopy. Nature Struct. Biol. 8, 265–270.

7.	Ujj L., Devanathan S., Meyer T. E., Cusanovich M. A., Tollin G., and Atkinson G. H. (1998) New photocycle intermediates in the photoactive yellow protein from Ecothiorhodospira halophila: picosecond transient absorption spectroscopy. Biophys. J. 75, 406–412.

8.	Haupts U., Tittor J., and Oesterhelt D. (1999) Closing in on bacteriorhodopsin: progress in understanding the molecule. Annu. Rev. Biophys. Biomol. Struct. 283, 67–99.

9.	Mizutani Y. and Kitagawa T. (2001) Ultrafast structural relaxation of myoglobin following photodissociation of carbon monoxide probed by time-resolved resonance Raman cpectroscopy. J. Phys. Chem. B 105, 10,992–10,999.

10.	Jackson T. A., Lim M., and Anfinrud P. (1994) Complex nonexponential relaxation in myoglobin after photodissociation of MbCO: measurement and analysis from 2 ps to 56 Âµs. Chem. Phys 180, 131–140.

11.	Ansari A., Jones C. M., Henry E. R., Hofrichter J., and Eaton W. A. (1994) Conformational relaxation and ligand binding in myoglobin. Biochemistry 33, 5128–5145.

12.	Xie X. and Simon J. D. (1991) Protein conformational relaxation following photodissociation of co from carbonmonoxymyoglobin-picosecond circular-dichroism and absorption studies. Biochemistry 30, 3682–3692.

13.	Schotte F., Lim M., Jackson T. A., Smirnov A. V., Soman J., Olson J. S., Phillips G. N. J., Wulff M., and Anfinrud P. (2003) Watching a protein as it functions with 150ps time-resolved X-ray crystallography. Science 300, 1944–1947.

14.	Krinsky S., Fundamentals of Hard X-ray Synchrotron Radiation Sources, in Third-Generation HardX-ray Synchrotron Radiation Sources, Mills D., Ed., John Wiley & Sons, Inc., New York (2002).

15.	Ren Z., Bourgeois D., Helliwell J. R., Moffat K., Šrajer V., and Stoddard B. L. (1999) Laue crystallography: coming of age. J. Synchrotron Rad. 6, 891–917.

16.	Šrajer V., Ren Z., Teng T.-Y., Schmidt M., Ursby T., Bourgeois D., Pradervand C., Schildkamp W., Wulff M., and Moffat K. (2001) Protein conformational relaxation and ligand migration in myoglobin: a nanosecond to millisecond molecular movie from time-resolved Laue X-ray diffraction. Biochemistry 40, 13,802–13,815.

17.	Bourgeois D., Vallone B., Schotte F., Arcovito A., Miele A. E., Sciara G., Wulff M., Anfinrud P., and Brunori M. (2003) Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography. Proc. Natl. Acad. Sci. 100, 8704–8709.

18.	Srajer V., Teng T.-Y., Ursby T., Pradervand C., Ren Z., Adachi S., Schildkamp W., Bourgeois D., Wulff M., and Moffat K. (1996) Photolysis of the carbon monoxide complex of myoglobin: nanosecond time-resolved crystallography. Science 274, 1726–1729.

19.	Neutze R., Pebay-Peyroula E., Edman K., Royant A., Navarro J., and Landau E. M. (2002) Bacteriorhodopsin: a high resolution structural view of vectorial proton transport. Biochim. Biophys. Acta 1565, 144–167.

20.	Ren Z., Perman B., Šrajer V., Teng T.-Y., Pradervand C., Bourgeois D., Schotte F., Ursby T., Kort R., Wulff Mand Moffat K. (2001) A molecularmovie at 1.8 A resolution displays the photocycle of photoactive yellow protein, a eubacterial blue-light receptor, from nanoseconds to seconds. Biochemistry 40, 13,788–13,801.

21.	Genick U. K., Borgstahl G. E., Ng K., Ren Z., Pradervand C., Burke P. M., Šrajer V., Teng T.-Y., Schildkamp W., McRee D. E., Moffat K., and Getzoff E. D. (1997) Structure of a protein photocycle intermediate by millisecond time-resolved crystallography. Science 275, 1471–1475.

22.	Perman B., Šrajer V., Ren Z., Teng T-.Y., Pradervand C., Ursby T., Bourgeois D., Schotte F., Wulff M., Kort R., Hellingwerf K., and Moffat K. (1998) Energy transduction on the nanosecond time scale: early structural events in a xanthopsin photocycle. Science 279, 1946–1950.

23.	Crosson S. and Moffat K. (2002) Photoexcited structure of a plant photoreceptor domain reveals a light-driven molecular switch. Plant Cell 14, 1067–1075.

24.	Karplus M. (1999) In Simplicity and Complexity in Proteins and Nucleic Acids, (Frauenfelder H., Deisenhofer J., and Wolynes P., eds.). Dahlem University Press, Belin, 139.

25.	Moffat K. (2001) Time-resolved biochemical crystallography: a mechanistic perspective. Chem. Rev. 101, 1569–1581.

25a.	Steinfeld J. I., Francisco J. S., and Haase W. L. (1989) Chemical Kinetics and Dynamics. Prentice Hall, Englewood Cliffs, NJ.

26.	Moffat K. (1989) Time-Resolved Macromolecular Crystallography. Annu. Rev.Biophys. Biophys. Chem. 18, 309–332.

27.	Schmidt M., Rajagopal S., Ren Z., and Moffat K. (2003) Application of singular value decomposition to the analysis of time-resolved macromolecular x-ray data. Biophys. J. 84, 2112–2129.

28.	Schmidt M., Pahl R., Šrajer V., Anderson S., Ren Z., Ihee H., and Moffat K. (2004) Protein kinetics: structures of intermediates and reaction mechanism from time-resolved x-ray data. Proc. Natl. Acad. Sci. 101, 4799–4804.

29.	Rajagopal S., Schmidt M., Anderson S., Ihee H., and Moffat K. (2004) Analysis of experimental time-resolved crystallographic data by singular value decomposition. Acta Cryst. D 60, 860–871.

30.	Abdel-Meguid S. S., Jeruzalmi D., and Sanderson M. R. (1996) Preliminary characterization of crystals. In Crystallographic methods and Protocols, Vol. 56 (Jones C., Mulloy B., and Sanderson M. R., eds.). Humana Press, Totowa, NJ, 55–86.

31.	Carrell H. L. and Glusker J. P. (2001) Crystallography of Biological Macromolecules, Kluwer Academic Publishers, Dordrecht, The Netherlands.

32.	Ren Z. and Moffat K. (1995) Quantitative analysis of synchrotron laue diffraction patterns in macromolecular crystallography. J. Appl. Cryst. 10, 461–481.

33.	Ren Z. and Moffat K. (1995) Deconvolution of energy overlaps in laue diffraction. J. Appl. Cryst. 28, 482–493.

34.	Campbell J. W. (1995) LAUEGEN, an X-windows-based program for the processing of Laue diffraction data. J. Appl. Cryst. 28, 228–236.

35.	Arzt S., Campbell J. W., Harding M. M., Hao Q., and Helliwell J. R. (1999) LSCALE-the new normalization, scaling and absorption correction program in the Daresbury Laue software suite. J. Appl. Cryst. 32, 554–562.

36.	Wakatsuki S. (1993) LEAP, Laue evaluation analysis package, for time-resolved protein crystallography, in CCP4 Study Weekend Proceedings: Data Collectionand Processing, Sawyer L., Isaacs N. W., and Bailey S., eds., CLRC Daresbury, Warrington, UK, 71–79.

37.	Bourgeois D., Nurizzo D., Kahn R., and Cambillau C. (1998) An integration routine based on profile fitting with optimized fitting area for the evaluation of weak and/or overlapped two-dimensional Laue or monochromatic patterns. J. Appl. Cryst. 31, 22–35.

39.	Scott W. G., Murray J. B., Arnold J. R. P., Stoddard B. L., and Klug A. (1996) Capturing the structure of a catalytic RNA intermediate: the hammerhead ribozyme. Science 274, 2065–2069.

40.	Singer P. T., Smalas A., Carty R. P., Mangel W. F., and Sweet R. M. (1993) The hydrolytic water molecule in trypsin revealed by time-resolved Laue crystallography. Science 259, 669–673.

41.	Fulop V., Phizackerley R. P., Soltis S. M., Clifton I. J., Wakatsuki S., Erman J., Hajdu J., and Edwards S. L. (1994) Laue diffraction study on the structure of cytochrome c peroxidase compound I. Structure 2, 201–208.

42.	Bolduc J. M., Dyer D. H., Scott W. G., Singer P., Sweet R. M., Koshland D. E. J., and Stoddard B. L. (1995) Mutagenesis and Laue structures of enzyme intermediates: isocitrate dehydrogenase. Science 268, 1312–1318.

43.	Gouet P., Jouve H. M., Williams P. A., Andersson I., Andreoletti P., Nussaume L., and Hajdu J. (1996) Ferryl intermediates of catalase captured by time-resolved Weisenberg crystallography and UV-VIS spectroscopy. Nature Struct. Biol. 3, 951–956.

44.	Helliwell J. R., Nieh Y. P., Raftery J., Cassetta A., Habash J., Carr P. D., Ursby T., Wulff M., Thompson A. W., C., N. A., and Hadener A. (1998) Time resolved structures of hydroxymethylbilane synthase (Lys59Gln mutant) as it is loaded with substrate determined by Laue diffraction. J. Chem. Soc. Faraday Trans. 94, 2615–2622.

45.	Schlichting I. and Goody R. S. (1997) Triggering methods in crystallographic enzyme kinetics. Methods in Enzymology 277, 467–490.

47.	Hori T., Moriyama H., Kawaguchi J., Hayashi-Iwasaki Y., Oshima T., and Tanaka N. (2000) The initial step of the thermal unfolding of 3-isopropylmalate dehydrogenase detected by the temperature-jump Laue method. Protein Engineering 13, 527–533.

48.	McCray J. A. and Trentham D. R. (1989) Properties and uses of photoreactive caged compounds. Annu. Rev. Biophys. Biophys. Chem. 18, 239–270.

49.	Corrie J. E. T., and Trenhtam D. R. (1993) Biological Applications of Photochemical Switches, Vol. 2, Wiley, New York, NY.

50.	Schlichting I., Almo S. C., Rupp G., Wilson K., Petratos K., Lentfer A., Wittinghofer A., Kabash W., Pai E. F., Petsko G. A., and Goody R. S. (1990) Time-resolved X-ray crystallographic study of the conformational change in Ha-ras p21 protein on GTP hydrolysis. Nature 345, 309–315.

51.	Stoddard B. L., Koenigs P., Porter N., Petratos K., Petsko G. A., and Ringe D. (1991) Observation of the light-triggered binding of pyrone to chymotrypsin by Laue X-ray crystallography. Proc. Natl. Acad. Sci. 88, 5503–5507.

52.	Duke E. M. H., Wakatsuki W., Hadfield A., and Johnson L. N. (1994) Laue and monochromatic diffraction studies on catalysis in phosphorylase b crystals. Protein Sci. 3, 1178–1196.

53.	Stoddard B. L., Cohen B. E., Brubaker M., Mesecar A. D., and Koshland D. E. J. (1998) Millisecond Laue structures of an enzyme-product complex using photocaged substrate analogs. Nature Struct. Biol. 5, 891–897.

54.	Chen Y., Šrajer V., Ng K., LeGrand A., and Moffat K. (1994) Optical monitoring of protein crystals in time-resolved x-ray experiments— microspectrophotometer design and performance. Rev. Sci. Instrum. 65, 1506–1511.

55.	Hadfield A. and Hajdu J. (1993) A fast and portable microspectrophotometer for protein crystallography. J. Appl. Cryst. 26, 839–842.

56.	Sakai K., Matsui Y., Kouyama T., Shiro Y., and Adachi S.-I. (2002) Optical monitoring of freeze trapped reaction intermediates in protein crystals: A microspectrophotometer for cryogenic protein crystallography. J. Appl. Cryst. 35, 270–273.

57.	Bourgeois D., Vernede X., Adam V., Fioravanti E., and Ursby T. (2002) A microspectrophotometer for UV-visible absorption and fluorescence studies of protein crystals. J. Appl. Cryst. 35, 319–326.

58.	Anderson S., Šrajer V., Pahl R., Rajagopal S., Schotte F., Anfinrud P., Wulff M., and Moffat K. (2004) Chromophore conformation and the evolution of tertiary structural changes in photoactive yellow protein. Structure 12, 1039–1045.

59.	Bourgeois D., Ursby T., Wulff M., Pradervand C., LeGrand A., Schildkamp W., Laboure S., Šrajer V., Teng T.-Y., Roth M., and Moffat K. (1996) Feasibility and realization of single-pulse laue diffraction on macromolecular crystals at ESRF. J. Synchrotron Rad. 3, 65–74.

60.	Schotte F., Techert S., Anfinrud P., Šrajer V., Moffat K., and Wulff M. (2002) Picosecond structural studies using pulsed synchrotron radiation. In Third-Generation HardX-Ray Synchrotron Radiation Sources. (Mills D., ed.). John Wiley & Sons, Inc., New York, NY, 345–401.

61.	Knapp J. E., Šrajer V., Pahl R., and Royer W. E. J. (2004) Immobilization of Scapharca HbI crystals improves data quality of a time-resolved crystallographic experiment. Micron. 35, 107–108.

62.	Šrajer V., Crosson S., Schmidt M., Key J., Schotte F., Anderson S., Perman B., Ren Z., Teng T.-Y., Bourgeois D., Wulff M., and Moffat K. (2000) Extraction of accurate structure factor amplitudes from Laue data: wavelength normalization with wiggler and undulator X-ray sources. J. Synchrotron Rad. 7,236–244.

63.	Bourgeois D., Wagner U., and Wulff M. (2000) Towards automated Laue data processing: application to the choice of optimal X-ray spectrum. Acta Cryst. D56, 973–985.

64.	Helliwell J. R. (1992) Macromolecular Crystallography With Synchrotron Radiation. Cambridge University Press, Cambridge, UK.

65.	Drenth J. (1999) Principles of Protein X-Ray Crystallography, Springer, New York, NY.

66.	Henderson R., and Moffat J. K. (1971) The difference Fourier technique in protein crystallography: errors and their treatment. Acta Cryst. B 27, 1414–1420.

67.	Ursby T., and Bourgeois D. (1997) Improved estimation of structure-factor difference amplitudes from poorly accurate data. Acta Cryst. A 53, 564–575.

68.	McRee D. E. (1999) Practical Protein Crystallography, Academic Press, San Diego, CA.

69.	Jones T. A., Bergdoll M., and Kjeldgaard MO. (1990) A macromolecular modeling environment. In Crystallographic and Modeling Methods in Molecular Design. (Bugg C. and Ealick S., eds.). Springer-Verlag Press, New York, NY, 189–195.

70.	Henry E. R. and Hofrichter J. (1992) Singular value decomposition: Application to analysis of experimental data. Methods in Enzymology 210, 129–192.

71.	Carson M. (1997) Ribbons. In Methods in En., zymology, Vol. 277. (Sweet R. M., and Carter C. W., eds.) Academic Press, 493–505.

72.	Hajdu J., Neutze R., Sjogren T., Edman K., Szoke H., Wilmouth R. C., and Wilmot C. M. (2000) Analyzing protein functions in four dimensions. Nature Struct. Biol. 7, 1006–1012.

73.	Moffat K. (1998) Time-Resolved Crystallography. Acta Cryst. A 54, 833–841.

74.	Schlichting I., Berendzen J., Chu K., Stock A. M., Maves S. A., Benson D. E., Sweet R. M., Ringe D., Petsko G. A., and Sligar S. G. (2000) The catalytic pathway of cytochrome P450_cam at atomic resolution. Science 287, 1615–1622.

75.	Berglund G. I., Carlsson G. H., Smith A. T., Szoke H., Henriksen A., and Hajdu J. (2002) The catalysis pathway of horseradish peroxidase at high resolution. Nature 417, 463–468.

76.	Schlichting I., Berendzen J., Phillips G. N., and Sweet R. M. (1994) Crystal structure of photolyzed carbonmonoxy-myoglobin. Nature 371, 808–812.

77.	Teng T. Y., Šrajer V., and Moffat K. (1994) Photolysis-induced structural changes in single crystals of carbonmonoxymyoglobin at 40K. Nature Struct. Biol. 1, 701–705.

78.	Teng T. Y., Šrajer V., and Moffat K. (1997) Initial trajectory of carbon monoxide after photodissociation from myoglobin at cryogenic temperatures. Biochemistry 36, 12,087–12,100.

79.	Chu K., Vojtechovsky J., McMahon B. H., Sweet R. M., Berendzen J., and Schlichting I. (2000) Structure of a ligand-binding intermediate in wild-type carbonmonoxy myoglobin. Nature 403, 921–923.

80.	Ostermann A., Waschipky R., Parak F. G., and Nienhaus G. U. (2000) Ligand binding and conformational motions in myoglobin. Nature 404, 205–208.

81.	Genick U. K., Soltis S. M., Kuhn P., Canestrelli I. L., and Getzoff E. D. (1998) Structure at 0.85 angstrom resolution of an early protein photocycle intermediate. Nature 392, 206–209.

82.	Kendrew J. C., Dickerson R. E., Strandberg B. E., Hart R. G., Davies D. R., Phillps D. C. and Shore V. C. (1960) Structure of myoglobin. A three-dimensional Fourier synthesis at 2 A resolution. Nature 185.

83.	Ansari A., Berendzen J., Bowne S. F., Frauenfelder H., T., I. I. E., Sauke T. B., Shyamsunder E., and Young R. D. (1985) Protein states and protein quakes. Proc. Natl. Acad. Sci. 82, 5000–5004.

84.	Kachalova G. S., Popov A. N., and Bartunik H. D. (1999) A steric mechanism for inhibition of CO binding to heme proteins. Science 284, 473–476.

85.	Meyer T. E. (1985) Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophile phototrophic bacterium Ectothiorhodospira halophila. Biochim. Biophys. Acta. 806, 175–183.

86.	Sprenger W. W., Hoff W. D., Armitage J. P., and Hellingwerf K. J. (1993) The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein. J. Bacteriol. 175, 3096–3104.

87.	Cusanovich M. A. and Meyer T. E. (2003) Photactive yellow protein: a prototypic PAS domain sensory protein and development of a common signaling mechanism. Biochemistry 42, 4759–4770.

88.	Winick H. (1995) The linac coherent light source (LCLS): A fourth generation light source using the SLAC linac. J. Elec. Spec. Rel. Phenom. 75, 1–8.

89.	Wiik B. H. (1997) The TESLA project: an accelerator facility for basic science. Nucl. Inst. Meth. Phys. Res. B 398, 1–17.

90.	Rossi G., Renzi M., Eikenberry E. F., Tate M. W., Bilderback D. H., Fontes E., Wixted R., Barna S., and Gruner S. M. (1999) Tests of a prototype pixel array detector for microsecond time-resolved X-ray diffraction. J. Synchrotron Rad. 6, 1096–1105.

91.	Rajagopal S., Kostov K., and Moffat K. (2004) Analytical trapping: Extraction of time-independent structures from time-dependent crystallographic data. J. Struct. Biol., in press.