Unsolved problems in biology
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1 Unsolved problems in biology What can advanced x-ray spectroscopy contribute? James Penner-Hahn Biophysics Research Division and Department of Chemistry The University of Michigan
2 Metalloproteins 30-50% of all proteins are estimated to be metalloproteins J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 2
3 Metals in Biology Trace elements known to be required V, Cr, Mn, Fe, Co, Ni, Cu, Zn, Se, Mo Trace elements suggested to be required Ti, Sn, As, Br Important toxins Hg, Cd, As, Pb Important therapeutics Pt, V, Au, Tc J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 3
4 Bioinorganic Chemistry What is the structure of the metal site? Metric details Geometry Electronic structure Bonding/covalency How does this structure change during the reaction? What is the role of the metal in controlling reactivity? J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 4
5 Techniques for studying metal sites in proteins UV-visible spectroscopy EPR spectroscopy Magnetic susceptibility MCD NMR spectroscopy Require open d shell Requires I=1/2 nucleus X-ray crystallography Requires crystals J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 5
6 Roles for EXAFS and XANES in Bioinorganic Chemistry De novo structure determination Comparison with crystallography Bond length Geometry Determination of oxidation state Determination of electronic structure J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 6
7 Limitations of XAS Resolution limited ability to: distinguish sites in multi-site systems determine detailed bond-length distribution resolve closely spaced transitions Sensitivity limited ability to: distinguish N vs. O ligands probe electronic structure of closed shell (e.g., d 10 ) ions J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 7
8 Potential applications of highresolution x-ray spectroscopy Site-specific measurements of XAS Edge sharpening Determination of electronic structure for problem metals Ligand identification J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 8
9 Site-specific EXAFS Prussian blue: Fe 4 (Fe(CN) 6 ) 3 Low spin Fe(II) high spin Fe(III) Glatzel, et al., Inorg. Chem., 2002, 41, J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 9
10 By monitoring different Kβ 1,3 emission energies, can measure siteselective EXAFS. J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 10
11 Possible applications of site-specific EXAFS Fe 2Methane mono-oxygenase (MMO) Mn 2 Arginase, catalase Zn 2Phosphatases, Esterases, Hydrolases J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 11
12 Possible applications of site-specific EXAFS, continued Fe 4Anaerobic ribonucleotide reductase Mn 4 Photosynthetic oxygen evolving complex Zn 3, Zn 4 Metallothionein Cu nparticulate MMO J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 12
13 Challenges for site-specific EXAFS Ability to resolve emission from different sites L.S. Fe(II) vs. H.S. Fe(III) may be best possible case Need to know something about site in order to assign transitions J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 13
14 What is needed? Model studies (especially molecular complexes) Exploration of alternative emission lines that may give better ability to resolve different sites Ability to study a wider range of elements at high energy J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 14
15 Electronic structure from XANES X-ray absorption (both metal and ligand edges) gives electronic structure information for open-shell complexes. Direct 1s 4p 1s 4p + LMCT 4p 3d 3p 4p 3d 3p 4p 3d 3p 1s 1s 1s J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 15
16 Polarized XANES for CuCl 4 2 Shake-down Direct Shadle et al., J. Am. Chem. Soc. 1993, 115, J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 16
17 Ligand K-edge spectra for MCl 4 give covalency 4p 3d 3p Fe(III) Fe(II) Co Ni 1s Cu M Cl Shadle et al., J. Am. Chem. Soc. 1995,117, J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 17
18 Cl & S are very common elements Same effects observed for Br & Se CuBr KBr But with lower resolution J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 18
19 Available energy resolution is often insufficient J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 19
20 Highresolution emission effectively removes corehole broadening Hämäläinen et al., Phys. Rev. Lett, , 2850 J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 20
21 Edge sharpening for transition metals using HR-XES detection Hayashi et al., Chem. Phys. Lett J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 21
22 Possible applications of edge sharpening 3d transition metals Se Sub ev resolution of 3d energy levels Improved resolution of 1s-4p (+shakedown) transitions Analog of sulfur, but can be substituted uniquely J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 22
23 What is needed? Model studies (especially molecular complexes) Exploration of alternative emission lines that may give better resolution Ability to study a wider range of elements at high energy J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 23
24 K-edge electronic spectroscopy Metal 1s-3d transitions d-orbital splitting (electronic structure) geometry Shake-down transitions covalency Ligand K-edge transitions covalency Not available for closed shell systems J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 24
25 XES should (in principle) probe filled molecular orbitals giving information comparable to XPS/UPS 3d 3p 3s 2p 2s 1s J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 25
26 Highest energy emission lines probe occupied valence orbitals Bergmann et al., J. Synchr. Rad., J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 26
27 Electronic structure from high-resolution MnN(CN) 5 4 XES MnO 2 Mn Bergmann et al., J. Chem. Phys. 2002, 116, 2011 J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 27
28 Mn Kβ (3p 1s) emission Taguchi et al., Phys. Rev. B., 2000, 61, 2558 J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 28
29 XES and RIXS as a probe of electronic structure Should give same information as XPS or UPS Probe larger volume of sample Less sensitive to radiation damage Not susceptible to charging artifacts May provide a solution for electronic studies of problem metals J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 29
30 Zn Problem metals Most common trace element Required for all classes of enzymes Typically probed using Co(II) substitution Cu(I) Storage form of Cu in cells Critical for understanding metal chaperones As, Pb, Cd Important toxins J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 30
31 Problem metals (continued) Mg Critical in DNA binding, ribozyme function Typically probed using Mn(II) substitution Ca Important structural element Important in signalling Ligands Cl, Br, Se, S important for a complete understanding of metal active sites J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 31
32 Challenges for studies of closedshell elements Model studies (especially molecular complexes) Theoretical description of emission spectra Ability to study a wider range of elements at high energy J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 32
33 Ligand identification Cross-over bands (Kβ'') are due to ligand-metal charge transfer Bergmann et al., Chem. Phys. Lett J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 33
34 Possible applications of ligand identification Distinguish O vs. N ligands Distinguish OH vs. OH 2 ligands J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 34
35 Mechanism of homocysteine methylation involves both Co and Zn R N N N N Zn is required for both methionine synthases Me Co Co and seems to play a similar role N N Me N N HOOC H C CH2 CH2 SH Zn HOOC H C CH 2 CH 2 S Zn NH 2 NH 2 J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 35
36 Combination of Zn + Se EXAFS consistent with small distortions from tetrahedral geometry in substrate-bound enzyme J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 36
37 Carbonic Anhydrase Zn-bound water or Zn-bound hydroxide? J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 37
38 Challenges for ligand identification Model studies Theoretical description of cross-over bands Wider availability of energies J. Penner-Hahn - SSRL Advanced Spectroscopy Workshop 38
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