X-Ray-Radiation-Induced Cooperative Atomic Movements in Protein

Journal of Molecular Biology

Volumn 387, Issue 5, 2009, Pages 1092-1105

  Petrova, Tatiana ^a,b   Lunin, Vladimir Y ^b   Ginell, Stephan ^a   Hazemann, Isabelle ^c   Lazarski, Krzysztof ^a   Mitschler, André ^c   Podjarny, Alberto ^c   Joachimiak, Andrzej ^a  

^a ARGONNE NATIONAL LABORATORY   (United States)

^b INSTITUTE OF MATHEMATICAL PROBLEMS OF BIOLOGY   (Russian Federation)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

crystal disorder; protein molecule; radiation damage; structural changes

Indexed keywords

ASPARTIC ACID; GLUTAMIC ACID; WATER;

ANISOTROPY; ARTICLE; ATOM; CONFORMATIONAL TRANSITION; DECARBOXYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RADIATION INJURY; X RAY; X RAY DIFFRACTION;

EID: 63649094988     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.02.030     Document Type: Article

References (54)

1. Carugo O., and Carugo K.D. When X-rays modify the protein structure: radiation damage at work. Trends Biochem. Sci. 30 (2005) 213-219
2. Ravelli R.B., and McSweeney S.M. The "fingerprint" that X-rays can leave on structures. Structure 8 (2000) 315-328
3. Weik M., Ravelli B.G., Kryger G., McSeeney S., Raves M.L., Harel M., et al. Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc. Natl Acad. Sci. USA 97 (2000) 623-628
4. Burmeister W.P. Structural changes in cryo-cooled protein crystal owing to radiation damage. Acta Crystallogr., Sect. D: Biol. Crystallogr. 56 (2000) 328-341
5. Fioravanti E., Vellieux F.M.D., Amara P., Madern D., and Weik M. Specific radiation damage to acidic residues and its relation to their chemical and structural environment. J. Synchrotron Radiat. 14 (2007) 84-97
6. Adam V., Royant A., Niviere V., Molina-Heredia F.P., and Bourgeois D. Structure of superoxide reductase bound to ferrocyanide and active site expansion upon X-ray-induced photo-reduction. Structure 12 (2004) 1729-1740
7. 4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc. Natl Acad. Sci. USA 102 (2005) 12047-12052
8. Rice L.M., Earnest T.N., and Brunger A.T. Single-wavelength anomalous diffraction phasing revisited. Acta Crystallogr., Sect. D: Biol. Crystallogr. 56 (2000) 1413-1420
9. Evans G., Polentarutti M., Carugu K.D., and Bricogne G. SAD phasing with triiodide, softer X-rays and some help from radiation damage. Acta Crystallogr., Sect. D: Biol. Crystallogr. 59 (2003) 1429-1443
10. Ramagopal U.A., Dauter Z., Thirumuruhan R., Fedorov E., and Almo S.C. Radiation-induced site-specific damage of mercury derivatives: phasing and implications. Acta Crystallogr., Sect. D: Biol. Crystallogr. 61 (2005) 1289-1298
11. Oliéric V., Ennifar E., Meents A., Fleurant M., Besnard C., Pattison P., et al. Using X-ray absorption spectra to monitor specific radiation damage to anomalously scattering atoms in macromolecular crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 63 (2007) 759-768
12. Sliz P., Harrison S.C., and Rosenbaum G. How does radiation damage in protein crystals depend on X-ray dose?. Structure 11 (2003) 13-19
13. Shimizu N., Hirata K., Hasegawa K., Ueno G., and Yamamoto M. Dose dependence of radiation damage for protein crystals studied at various X-ray energies. J. Synchrotron Radiat. 14 (2007) 4-10
14. Teng T., and Moffat K. Primary radiation damage of protein crystals by an intense synchrotron X-ray beam. J. Synchrotron Radiat. 7 (2000) 313-317
15. Kmetko J., Husseini N.S., Naides M., Kalinin Y., and Thorne R.E. Quantifying X-ray radiation damage in protein crystals at cryogenic temperatures. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 (2006) 1030-1038
16. Garman E.F., and Owen R.L. Cryocooling and radiation damage in macromolecular crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 (2006) 32-47
17. Nukagara M., Mayama K., Hujer A.M., Bomolo R.A., and Knox J.R. Ultrahigh resolution structure of a Class A β-lactamase: on the mechanism and specificity of the extended-spectrum SHV-2 enzyme. J. Mol. Biol. 328 (2003) 289-301
18. Fuhrmann C.N., Kelch B.A., Ota N., and Agard D.A. The 0.83 Ǻ resolution structure of α-lytic protease reveals the detailed structure of the active site and identifies a source of conformational strain. J. Mol. Biol. 338 (2004) 999-1013
19. Banumathi S., Zwart P.H., Ramagopal U.A., Dauter M., and Dauter Z. Structural effects of radiation damage and its potential for phasing. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 1085-1093
20. Horovitz A., Serrano L., Avron B., Bycroft M., and Fersht A.R. Strength and co-operativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216 (1990) 1031-1044
21. Anashkina A., Kuznetsov E., Esipova N., and Tumanyan V. Comprehensive statistical analysis of residues interaction specificity at protein-protein interfaces. Proteins 67 (2007) 1060-1077
22. Borek D., Ginell S.L., Cymborowski M., Minor W., and Otwinowski Z. Many faces of radiation-induced changes. J. Synchrotron Radiat. 14 (2007) 24-33
23. Berglund G.I., Carlsson G.H., Smith A.T., Szoke H., Henriksen A., and Hajdu J. The catalytic pathway of horseradish peroxidase at high resolution. Nature 417 (2002) 463-468
24. Dubnovitsky A.P., Ravelli R.B.G., Popov A.N., and Papageorgiou A.C. Strain relief at the active site of phosphoserine aminotransferase induced by radiation damage. Protein Sci. 14 (2005) 1498-1507
25. Rosenbaum G., Alkire R.W., Evans G., Rotella F.J., Lazarski K., Zhang R.G., et al. The Structural Biology Center 19ID undulator beamline: facility specifications and protein crystallographic results. J. Synchrotron Radiat. 13 (2006) 30-45
26. Murray J.W., Garman E.F., and Ravelli R.B.G. X-ray absorption by macromolecular crystals: the effect of wavelength and crystal composition on absorbed dose. J. Appl. Crystallogr. 37 (2004) 513-522
27. Henderson R. Cryo-protection of protein crystals against radiation damage in electron and X-ray diffraction. Proc. R. Soc. London, Ser. B. 241 (1990) 6-8
28. Owen R.L., Rudiño-Piñera E., and Garman E.F. Experimental determination of the radiation dose limit for cryocooled protein crystals. Proc. Natl Acad. Sci. USA 103 (2006) 4912-4917
29. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2256-2268
30. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography Collaborative Computational Project, Number 4. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
31. Schneider T.R. Domain identification by iterative analysis of error-scaled difference distance matrices. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2269-2275
32. Mosca R., and Schneider T.R. RAPIDO: a web server for the alignment of protein structures in the presence of conformational changes. Nucleic Acids Res. 36 (2008) W42-W46
33. Mosca R., Branetti B., and Schneider T.R. Alignment of protein structures in the presence of domain motions. BMC Bioinformatics 9 (2008) 352-368
34. Trueblood K.N., Bürgi H.-B., Burzlaff H., Dunitz J.D., Gramaccioli C.M., Schulz H.H., et al. Atomic displacement parameter nomenclature. Report of a subcommittee on atomic displacement parameter nomenclature. Acta Crystallogr., Sect. A: Found Crystallogr. 52 (1996) 770-781
35. Petrova T., Ginell S., Mitschler A., Hazemann I., Schneider T., Cousido A., et al. Ultra-high resolution study of protein atomic displacement parameters at cryotemperatures obtained with helium cryostat. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 (2006) 1535-1544
36. Ramirez U.D., and Freymann D.M. Analysis of protein hydration in ultra-high resolution structures of the SRP GTPase Ffh. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 (2006) 1520-1534
37. Weik M., Kryger G., Schreurs A.M.M., Bouma B., Silman I., Sussman J.L., et al. Solvent behavior in flash-cooled protein crystals at cryogenic temperatures. Acta Crystallogr., Sect. A: Found Crystallogr. 57 (2001) 566-573
38. Weik M. Low temperature behavior of water confined by biological macromolecules and its relation to protein dynamics. Eur. Phys. J. E 12 (2003) 153-158
39. Tilton Jr. R.F., Dewan J.C., and Petsko G.A. Effects of temperature on protein structure and dynamics: x-ray crystallographic studies of the protein ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry 31 (1992) 2469-2481
40. Kurinov I.V., and Harrison R.W. The influence of temperature on lysozyme crystals. Structure and dynamics of protein and water. Acta Crystallogr., Sect. D: Biol. Crystallogr. 51 (1995) 98-109
41. Mhaisekar A., Kazmierczak M.J., and Banerjee R. Three-dimensional numerical analysis of convection and conduction cooling of spherical biocrystals with localized heating from synchrotron X-ray beams. J. Synchrotron Radiat. 12 (2005) 318-328
42. Snell E.H., Bellamy H.D., Rosenbaum G., and van der Woerd M.J. Non-invasive measurement of X-ray beam heating on a surrogate crystal sample. J. Synchrotron Radiat. 14 (2006) 109-115
43. Yonath A., Harms J., Hansen H.A., Bashan A., Schlunzen F., Levin I., et al. Crystallographic studies on the ribosome, a large macromolecular assembly exhibiting severe nonisomorphism, extreme beam sensitivity and no internal symmetry. Acta Crystallogr., Sect. A: Found Crystallogr. 54 (1998) 945-955
44. Ravelli R.B.G., Theveneau P., McSweeney S., and Caffrey M. Unit-cell volume change as a metric of radiation damage in crystals of macromolecules. J. Synchrotron Radiat. 9 (2002) 355-360
45. Murray J., and Garman E. Investigation of possible free-radical scavengers and metrics for radiation damage in protein crystallography. J. Synchrotron Radiat. 9 (2002) 347-354
46. Weik M., Ravelli R.B.G., Silman I., Sussman J.L., Gros P., and Kroon J. Specific protein dynamics near solvent glass transition assayed by radiation-induced structural changes. Protein Sci. 10 (2001) 1953-1961
47. Meents A., Wagner A., Schneider R., Pradervand C., Pohl E., and Schulze-Briese C. Reduction of X-ray-induced radiation damage of macromolecular crystal by data collection at 15 K: a systematic study. Acta Crystallogr., Sect. D: Biol. Crystallogr. 63 (2007) 302-309
48. Murray J.W., Rudiño-Piñera E., Owen R.L., Grininger M., Ravelli R.B.G., and Garman E.F. Parameters affecting the X-ray dose absorbed by macromolecular crystals. J. Synchrotron Radiat. 12 (2005) 268-275
49. Holton G.M. XANES measurements of the rate of radiation damage to selenomethionine side chains. J. Synchrotron Radiat. 14 (2007) 1-3
50. Lamour V., Barth P., Rogniaux H., Poterszman A., Howard E., Mitschler A., et al. Production of crystals of human aldose reductase with very high resolution diffraction. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 (1999) 721-723
51. Howard E.I., Sanishvili R., Cachau R.E., Mitschler A., Chevrier B., Barth P., et al. Proteins 55 (2004) 792-804
52. Minor W., Cymborowski M., Otwinowski Z., and Chruszez M. HKL-3000: the integration of the data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 (2006) 859-866
53. Sheldrick G.M., and Schneider T.R. SHELXL: high-resolution refinement. Methods Enzymol. 277 (1997) 319-343
54. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132