Biological X-ray absorption spectroscopy (BioXAS): a valuable tool for the study of trace elements in the life sciences

Current Opinion in Structural Biology

Volumn 18, Issue 5, 2008, Pages 609-616

  Strange, Richard W ^a   Feiters, Martin C ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMIUM; HALOGEN; METAL; METALLOPROTEIN; TRACE ELEMENT;

ABSORPTION SPECTROSCOPY; BIOLOGY; BIOMEDICINE; COMPUTATIONAL FLUID DYNAMICS; CRYSTAL STRUCTURE; DEGENERATIVE DISEASE; OXIDATION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; RADIATION INJURY; REVIEW; X RAY; X RAY CRYSTALLOGRAPHY;

ABSORPTIOMETRY, PHOTON; ANIMALS; BIOLOGICAL SCIENCE DISCIPLINES; CHROMIUM; ELECTRONS; HALOGENS; HUMANS; METALS; MODELS, MOLECULAR; NEURODEGENERATIVE DISEASES; NITRITE REDUCTASES; OXIDATION-REDUCTION; PROTEIN CONFORMATION; SPECTRUM ANALYSIS; SPECTRUM ANALYSIS, RAMAN; SUPEROXIDE DISMUTASE; TRACE ELEMENTS; X-RAYS;

EID: 53249119007     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2008.06.002     Document Type: Review

References (58)

1. Crichton R.R. Biological Inorganic Chemistry, An Introduction (2008), Elsevier
2. Banci L., Bertini I., and Mangani S. Integration of XAS and NMR techniques for the structure determination of metalloproteins. Examples from the study of copper transport proteins. J Synchrotron Radiat 12 (2005) 94-97
3. Wirth C., Meyer-Klaucke W., Pattus F., and Cobessi D. From the periplasmic signalling domain to the extracellular face of an outer membrane signal transducer of Pseudomonas aeruginosa: crystal structure of the ferric pyoverdine outer membrane receptor. J Mol Biol 368 (2007) 398-406. The complex of the siderophore pyoverdin with Ga(III) was used for structure elucidation by NMR because of the paramagnetism of the complex with Fe(III). EXAFS shows that the Ga(III) and Fe(III) coordination in the complexes are identical except for slightly longer ligand distances to Fe(III).
4. -.
5. De la Mora-Rey T., and Wilmot C.M. Synergy within structural biology of single crystal optical spectroscopy and X-ray crystallography. Curr Opin Struct Biol 17 (2007) 580-586
6. Royant A., Carpentier P., Ohana J., McGeehan J., Paetzold B., Noirclerc-Savoye M., Vernede X., Adam V., and Bourgeois D. Advances in spectroscopic methods for biological crystals. 1. Fluorescence lifetime measurements. J Appl Crystallogr 40 (2007) 1105-1112
7. Beitlich T., Kuhnel K., Schulze-Briese C., Shoeman R.L., and Schlichting I. Cryoradiolytic reduction of crystalline heme proteins: analysis by UV-vis spectroscopy and X-ray crystallography. J Synchrotron Radiat 14 (2006) 11-23
8. Pearson A.R., Pahl R., Kovoleva E.G., Davidson V.L., and Wilmot C.M. Tracking X-ray-derived redox changes in crystals of a methylamine dehydrogenase/amicyanin complex using single-crystal UV/Vis microspectrophotometry. J Synchrotron Radiat 14 (2007) 92-98
9. Hough M.A., Antonyuk S.V., Strange R.W., Eady R.R., and Hasnain S.S. Crystallography with online optical and X-ray absorption spectroscopies demonstrates an ordered mechanism in copper nitrite reductase. J Mol Biol 378 (2008) 353-361. On-line multiple spectroscopic techniques were used to assess radiation-induced redox changes at different metal sites, demonstrating the importance of ensuring the correct status of redox centres in crystal structure determinations. In copper nitrite reductase, an electron is delivered from the type-1 copper (T1Cu) centre to the type-2 copper (T2Cu) centre where catalysis occurs. PX, XAS and optical spectroscopy were used in situ to show that X-rays rapidly and selectively photoreduce the T1Cu centre, that the T2Cu centre does not photoreduce during PX data collection and that internal electron transfer between the T1Cu and T2Cu centres does not occur. These data unambiguously demonstrate an 'ordered' mechanism in which electron transfer is gated by binding nitrite to the T2Cu.
10. Carpentier P., Royant A., Ohana J., and Bourgeois D. Advances in spectroscopic methods for biological crystals. 2. Raman spectroscopy. J Appl Crystallogr 40 (2007) 1113-1122. Combined on-line methods are increasingly important to interpretation of protein structures and this paper shows the advantages of combining Raman measurements with PX on beamlines to study proteins in situ, focussing on the benefits to crystallographic structure determination. With metalloprotein crystals, this method can also be allied with XAS measurements, in particular to examine ligand binding or radiation damage to metal sites.
11. Katona G., Carpentier P., Niviere V., Amara P., Adam V., Ohana J., Tsanov N., and Bourgeois D. Raman-assisted crystallography reveals end-on peroxide intermediates in a nonheme iron enzyme. Science 316 (2007) 449-453. A nice example of what can be achieved by on-line Raman with PX.
12. Einsle O., Andrade S.L.A., Dobbek H., Meyer J., and Rees D.C. Assignment of individual metal redox states in a metalloprotein by crystallographic refinement at multiple X-ray wavelengths. J Am Chem Soc 129 (2007) 2210-2211. This paper shows how redox states in individual metals in metal clusters and multi-metal proteins can be accurately assigned and separated on the basis of the energy and shape of XANES spectra. By collecting complete PX data sets at several absorption edge energies and refining the energy-dependent f″ and f′ anomalous scattering factors for each atom, the XANES spectra for each metal site can be reconstructed. The experiments are relatively straightforward on SAD/MAD beamlines. With rapid data collection possible using the latest generation of X-ray detectors (e.g. Pilatus), radiation damage to metal sites should also be minimised sufficiently even in the worst cases.
13. Holton J.M. XANES measurements of the rate of radiation damage to selenomethionine side chains. J Synchrotron Radiat 14 (2007) 51-72
14. Olieric V., Ennifar E., Meents A., Fleurant M., Besnard C., Pattison P., Schiltz M., Schulze-Briese C., and Dumas P. Using X-ray absorption spectra to monitor specific radiation damage to anomalously scattering atoms in macromolecular crystallography. Acta Crystallogr D 63 (2007) 759-768
15. Ferreira K.N., Iverson T.M., Maghlaoui K., Barber J., and Iwata S. Architecture of photosynthetic oxygen-evolving center. Science 303 (2004) 1831-1838
16. Loll B., Kern J., Saenger W., Zouni A., and Biesiadka J. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438 (2005) 1040-1044
17. 2+ cluster of photosystem II and its protein environment as revealed by X-ray crystallography. Philos Trans R Soc B 363 (2008) 1129-1137
18. 4Ca cluster. Science 314 (2006) 821-825
19. Kern J., Biesiadka J., Loll B., Saenger W., and Zouni A. Structure of the Mn-4-Ca cluster as derived from X-ray diffraction. Photosynth Res 92 (2007) 389-405
20. Grabolle M., Haumann M., Muller C., Liebisch P., and Dau H. Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10-300 K. J Biol Chem 281 (2006) 4580-4588
21. 4Ca redox active site in single crystals of photosystem II, studied as a function of the dose and energy of X-rays, temperature and time. It was shown that conditions previously used for PX data collection do cause serious damage to the metal cluster.
22. Corbett M.C., Latimer M.J., Poulos T.L., Sevrioukova I.F., Hodgson K.O., and Hedman B. Photoreduction of the active site of the metalloprotein putidaredoxin by synchrotron radiation. Acta Crystallogr D 63 (2007) 951-960
23. Dubois L., Jacquamet L., Pecaut J., and Latour J.-M. X-ray photoreduction of a di(mu-oxo)Mn(III)Mn(IV) complex occurs at temperatures as low as 20 K. Chem Commun 43 (2006) 4521-4523
24. Ryde U. Accurate metal-site structures in proteins obtained by combining experimental data and quantum chemistry. Dalton Trans 6 (2007) 607-625
25. Senn H.M., and Thiel W. QM/MM studies of enzymes. Curr Opin Chem Biol 11 (2007) 182-187
26. Barrett M.L., Harvey I., Sundararajan M., Surendran R., Hall J.F., Ellis M.J., Hough M.A., Strange R.W., Hillier I.H., and Hasnain S.S. Atomic resolution crystal structures, EXAFS, and quantum chemical studies of rusticyanin and its two mutants provide insight into its unusual properties. Biochemistry 45 (2006) 2927-2939
27. Basumallick L., Sarangi R., George S.D., Elmore B., Hooper A.B., Hedman B., Hodgson K.O., and Solomon E.I. Spectroscopic and density functional studies of the red copper site in nitrosocyanin: role of the protein in determining active site geometric and electronic structure. J Am Chem Soc 127 (2005) 3531-3544
28. Loscher S., Schwartz L., Stein M., Ott S., and Haumann M. Facilitated hydride binding in an Fe-Fe hydrogenase active-site biomimic revealed by X-ray absorption spectroscopy and DFT calculations. Inorg Chem 46 (2007) 11094-11105
29. Yano J., Robblee J., Pushkar Y., Marcus M.A., Bendix J., Workman J.M., Collins T.J., Solomon E.I., George S.D., and Yachandra V.K. Polarized X-ray absorption spectroscopy of single-crystal Mn(V) complexes relevant to the oxygen-evolving complex of photosystem II. J Am Chem Soc 129 (2007) 12989-13000
30. Sepulcre F., Cordomi A., Proietti M.G., Perez J.J., Garcia J., Querol E., and Padros E. X-ray absorption and molecular dynamics study of cation binding sites in the purple membrane. Proteins Struct Func Bioinform 67 (2007) 360-374
31. Dey A., Okamura T., Ueyama N., Hedman B., Hodgson K.O., and Solomon E.I. Sulfur K-edge XAS and DFT calculations on P450 model complexes: effects of hydrogen bonding on electronic structure and redox potentials. J Am Chem Soc 127 (2005) 12046-12053. A series of carefully designed model compounds featuring Fe in a porphyrin with a single sulfur ligand allows the effect of H-bonding to sulfur to be established by sulfur K-edge XAS combined with DFT. The results are of relevance to the catalytic mechanism of cytochrome P450. It is shown that the redox potential depends on ligand-metal bond covalency, which can be probed by sulfur K-edge XAS, and in turn depends on H-bonding to S.
32. 2+) clusters: effects of H-bonding and structural distortion on covalency and spin topology. Inorg Chem 44 (2005) 8349-8354
33. Dey A., Jenney F.E., Adams M.W.W., Johnson M.K., Hodgson K.O., Hedman B., and Solomon E.I. Sulfur K-edge X-ray absorption spectroscopy and density functional theory calculations on superoxide reductase: role of the axial thiolate in reactivity. J Am Chem Soc 129 (2007) 12418-12431
34. Hsiao Y.W., Tao Y., Shokes J.E., Scott R.A., and Ryde U. EXAFS structure refinement supplemented by computational chemistry. Phys Rev B 74 (2006) 214101
35. Ryde U., Hsiao Y.W., Rulisek L., and Solomon E.I. Identification of the peroxy adduct in multicopper oxidases by a combination of computational chemistry and extended X-ray absorption fine-structure measurements. J Am Chem Soc 129 (2007) 726-727
36. Arcovito A., Benfatto M., Cianci M., Hasnain S.S., Nienhaus K., Nienhaus G.U., Savino C., Strange R.W., Vallone B., and Della Longa S. X-ray structure analysis of a metalloprotein with enhanced active-site resolution using in situ X-ray absorption near edge structure spectroscopy. Proc Natl Acad Sci U S A 104 (2007) 6211-6216. A combination of PX (at 1.4 Å resolution) and polarised XANES experiments were carried out on the same single crystal of cyanomet sperm whale myoglobin (MbCN). The XANES yielded Fe-haem structural parameters with ±(0.02-0.07) Å accuracy on the atomic distances and ±7° on the Fe-CN angle. These parameters were subsequently used as restraints in the crystal structure refinement to obtain a structural model with a higher precision of the bond lengths and angles at the active site than would have been possible with the crystallographic data alone.
37. Strange R.W., Ellis M., and Hasnain S.S. Atomic resolution crystallography and XAFS. Coord Chem Rev 249 (2005) 197-208
38. Feiters M.C., Küpper F.C., and Meyer-Klaucke W. X-ray absorption spectroscopic studies on model compounds for biological iodine and bromine. J Synchrotron Radiat 12 (2005) 85-93
39. Küpper F.C., Carpenter L.J., McFiggans G.B., Palmer C.J., Waite T., Boneberg E.-M., Woitsch S., Weiller M., Abela R., Grolimund D., et al. Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. PNAS 105 (2008) 6954-6958
40. Feiters M.C., Leblanc C., Küpper F.C., Meyer-Klaucke W., Michel G., and Potin P. Bromine is an endogenous component of a vanadium bromoperoxidase. J Am Chem Soc (2005) 15340-15341. An Br-Br distance ∼6 Å, which is exceptionally long for BioXAS, is detected in A. nodosum (knotted wrack) haloperoxidase, and found, by comparison to model compounds and simulation, to be characteristic of a 3,5-dibromotyrosine residue. This discovery by EXAFS prompted complementary mass spectrometry studies, identifying the brominated tyrosine as a surface residue and re-refinement of the crystal structure.
41. Coker V.S., Gault A.G., Pearce C.I., van der Laan G., Telling N.D., Charnock J.M., Polya D.A., and Lloyd J.R. XAS and XMCD evidence for species-dependent partitioning of arsenic during microbial reduction of ferrihydrite to magnetite. Environ Sci Technol 40 (2006) 7745-7750
42. 3 to be quantified by deconvolution, and images representing the chemical environment of As to be reconstructed.
43. Manley S.A., George G.N., Pickering I.J., Glass R.S., Prenner E.J., Yamdagni R., Wu Q., and Gailer J. The seleno bis (S-glutathionyl) arsinium ion is assembled in erythrocyte lysate. Chem Res Technol 19 (2006) 601-607
44. George G.N., Johnson Nelson K., Harris H.H., Doonan C.J., and Rajagopalan K.V. Interaction of product analogues with the active site of Rhodobacter Sphaeroides dimethyl sulfoxide reductase. Inorg Chem 46 (2007) 3097-3104
45. Jacquamet L., Sun Y., Hatfield J., Gu W., Cramer S.P., Crowder M.W., Lorigan G.A., Vincent J.B., and Latour J.-M. Characterization of chromodulin by X-ray absorption and electron paramagnetic susceptibility measurements. J Am Chem Soc 125 (2003) 114-180
46. Levina A., Harris H.H., and Lay P.A. X-ray absorption and EPR spectroscopic studies of the biotransformations of chromium(VI) in mammalian cells. Is chromodulin an artifact of isolation methods?. J Am Chem Soc 129 (2007) 1065-1075 and correction 9832. A combined EPR (electron paramagnetic resonance) and XAS study of Cr in a large variety of model compounds and cell lines. XAS spectra of intact Cr(VI)-treated cells were found to be different from those of Cr(VI) combined with cell fractions, suggesting the existence of specific metabolic pathways for Cr(VI) in living cells.
47. Ektessabi A.I., and Rabionet M. The role of trace metallic elements in neurodegenerative disorders: quantitative analysis using XRD and XANES spectroscopy. Anal Sci 21 (2005) 885-892
48. Fahrni C.J. Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals. Curr Opin Chem Biol 11 (2007) 121-127
49. Paunesku T., Vogt S., Maser J., Lai B., and Woloschak G. X-ray fluorescence microprobe imaging in biology and medicine. J Cell Biochem 99 (2006) 1489-1502
50. Donnelly P.S., Xiao Z., and Wedd A.G. Copper and Alzheimer's disease. Curr Opin Chem Biol 11 (2007) 128-133
51. Kong G.K.W., Adams J.J., Harris H.H., Boas J.F., Curtain C.C., Galatis D., Masters C.L., Barnham K.J., McKinstry W.J., Cappai R., et al. Structural studies of the Alzheimer's amyloid precursor protein copper-binding domain reveal how it binds copper ions. J Mol Biol 367 (2007) 148-161
52. Noy D., Solomonov I., and Sinkevich O. Zinc-amyloid beta interactions on a millisecond time-scale stabilize non-fibbrillar Alzheimer-related species. J Am Chem Soc 130 (2008) 1376-1383. This was an interesting combination of kinetic and spectroscopic methods with time-resolved (stopped-flow freeze quench) EXAFS to study the interaction of Zn ions with the amyloid β peptide. Four key spectra (at 2.1, 10, 20 and 500 ms) were found to represent the complete data set. The variation of the EXAFS with time indicates the presence of different Zn-binding sites and/or structural transformations in the Zn-protein complex. Together with electron microscopy (EM) results, this showed that Zn ions specifically stabilise non-fibrillar aggregates implied in the pathology of Alzheimer's disease.
53. 2+-binding region in full-length human prion protein compared with the isolated octapeptide. Vet Microbiol 123 (2007) 358-366
54. Shearer J., and Soh P. The copper(II) adduct of the unstructured region of the amyloidogenic fragment derived from the human prion protein is redox-active at physiological pH. Inorg Chem 46 (2007) 710-719
55. 2+ complex. Eur Biophys J Biophys Lett 34 (2005) 97-112
56. Furlan S. Ab initio simulations of Cu binding sites on the N-terminal region of prion protein. J Biol Inorg Chem 12 (2007) 571-583
57. Shearer J., and Soh P. NiK-edge XAS suggests that coordination of Ni-II to the unstructured amyloidogenic region of the human prion protein produces a Ni-2 bis-mu-hydroxo dimer. J Inorg Biochem 101 (2007) 370-373
58. Strange R.W., Antonyuk S., Hough M.A., Doucette P.A., Valentine J.S., and Hasnain S.S. Variable metallation of human superoxide dismutase: atomic and high-resolution crystal structures of Cu-Zn, Zn-Zn and 'as isolated' wild-type enzymes. J Mol Biol 356 (2006) 1152-1162