Sulfur K-Edge XAS Studies of the Effect of DNA Binding on the [Fe 4 S 4 ] Site in EndoIII and MutY
Abstract
S K-edge X-ray absorption spectroscopy (XAS) was used to study the [Fe4S4] clusters in the DNA repair glycosylases EndoIII and MutY to evaluate the effects of DNA binding and solvation on Fe–S bond covalencies (i.e., the amount of S 3p character mixed into the Fe 3d valence orbitals). Increased covalencies in both iron–thiolate and iron–sulfide bonds would stabilize the oxidized state of the [Fe4S4] clusters. Our results are compared to those on previously studied [Fe4S4] model complexes, ferredoxin (Fd), and to new data on high-potential iron–sulfur protein (HiPIP). A limited decrease in covalency is observed upon removal of solvent water from EndoIII and MutY, opposite to the significant increase observed for Fd, where the [Fe4S4] cluster is solvent exposed. Importantly, in EndoIII and MutY, a large increase in covalency is observed upon DNA binding, which is due to the effect of its negative charge on the iron–sulfur bonds. Furthermore, in EndoIII, this change in covalency can be quantified and makes a significant contribution to the observed decrease in reduction potential found experimentally in DNA repair proteins, enabling their HiPIP-like redox behavior.
- Authors:
-
- Stanford Univ., CA (United States). Dept. of Chemistry; SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource
- California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Chemistry
- Univ. of California, Davis, CA (United States). Dept. of Chemistry
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
- OSTI Identifier:
- 1394069
- Grant/Contract Number:
- AC02-76SF00515; CA069875; F31 AG040954; GM040392; GM103393; GM120087
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of the American Chemical Society
- Additional Journal Information:
- Journal Volume: 139; Journal Issue: 33; Journal ID: ISSN 0002-7863
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Ha, Yang, Arnold, Anna R., Nuñez, Nicole N., Bartels, Phillip L., Zhou, Andy, David, Sheila S., Barton, Jacqueline K., Hedman, Britt, Hodgson, Keith O., and Solomon, Edward I. Sulfur K-Edge XAS Studies of the Effect of DNA Binding on the [Fe 4 S 4 ] Site in EndoIII and MutY. United States: N. p., 2017.
Web. doi:10.1021/jacs.7b03966.
Ha, Yang, Arnold, Anna R., Nuñez, Nicole N., Bartels, Phillip L., Zhou, Andy, David, Sheila S., Barton, Jacqueline K., Hedman, Britt, Hodgson, Keith O., & Solomon, Edward I. Sulfur K-Edge XAS Studies of the Effect of DNA Binding on the [Fe 4 S 4 ] Site in EndoIII and MutY. United States. https://doi.org/10.1021/jacs.7b03966
Ha, Yang, Arnold, Anna R., Nuñez, Nicole N., Bartels, Phillip L., Zhou, Andy, David, Sheila S., Barton, Jacqueline K., Hedman, Britt, Hodgson, Keith O., and Solomon, Edward I. Tue .
"Sulfur K-Edge XAS Studies of the Effect of DNA Binding on the [Fe 4 S 4 ] Site in EndoIII and MutY". United States. https://doi.org/10.1021/jacs.7b03966. https://www.osti.gov/servlets/purl/1394069.
@article{osti_1394069,
title = {Sulfur K-Edge XAS Studies of the Effect of DNA Binding on the [Fe 4 S 4 ] Site in EndoIII and MutY},
author = {Ha, Yang and Arnold, Anna R. and Nuñez, Nicole N. and Bartels, Phillip L. and Zhou, Andy and David, Sheila S. and Barton, Jacqueline K. and Hedman, Britt and Hodgson, Keith O. and Solomon, Edward I.},
abstractNote = {S K-edge X-ray absorption spectroscopy (XAS) was used to study the [Fe4S4] clusters in the DNA repair glycosylases EndoIII and MutY to evaluate the effects of DNA binding and solvation on Fe–S bond covalencies (i.e., the amount of S 3p character mixed into the Fe 3d valence orbitals). Increased covalencies in both iron–thiolate and iron–sulfide bonds would stabilize the oxidized state of the [Fe4S4] clusters. Our results are compared to those on previously studied [Fe4S4] model complexes, ferredoxin (Fd), and to new data on high-potential iron–sulfur protein (HiPIP). A limited decrease in covalency is observed upon removal of solvent water from EndoIII and MutY, opposite to the significant increase observed for Fd, where the [Fe4S4] cluster is solvent exposed. Importantly, in EndoIII and MutY, a large increase in covalency is observed upon DNA binding, which is due to the effect of its negative charge on the iron–sulfur bonds. Furthermore, in EndoIII, this change in covalency can be quantified and makes a significant contribution to the observed decrease in reduction potential found experimentally in DNA repair proteins, enabling their HiPIP-like redox behavior.},
doi = {10.1021/jacs.7b03966},
journal = {Journal of the American Chemical Society},
number = 33,
volume = 139,
place = {United States},
year = {Tue Jul 18 00:00:00 EDT 2017},
month = {Tue Jul 18 00:00:00 EDT 2017}
}
Web of Science
Works referenced in this record:
Structural and Functional Aspects of Metal Sites in Biology
journal, January 1996
- Holm, Richard H.; Kennepohl, Pierre; Solomon, Edward I.
- Chemical Reviews, Vol. 96, Issue 7
The environment of Fe4S4 clusters in ferredoxins and high-potential iron proteins. New information from x-ray crystallography and resonance Raman spectroscopy
journal, March 1991
- Backes, Gabriele; Mino, Yoshiki; Loehr, Thomas M.
- Journal of the American Chemical Society, Vol. 113, Issue 6
EXAFS studies of proteins and model compounds containing dimeric and tetrameric iron-sulfur clusters
journal, September 1979
- Teo, Boon-Keng; Shulman, R. G.; Brown, G. S.
- Journal of the American Chemical Society, Vol. 101, Issue 19
Vibrational mode structure and symmetry in proteins and analogs containing Fe4S4 clusters: resonance Raman evidence that HiPIP is tetrahedral while ferredoxin undergoes a D2d distortion
journal, November 1987
- Czernuszewicz, Roman S.; Macor, Kathleen A.; Johnson, Michael K.
- Journal of the American Chemical Society, Vol. 109, Issue 23
Ligand K-Edge X-ray Absorption Spectroscopy of [Fe 4 S 4 ] 1+,2+,3+ Clusters: Changes in Bonding and Electronic Relaxation upon Redox
journal, June 2004
- Dey, Abhishek; Glaser, Thorsten; Couture, Manon M. -J.
- Journal of the American Chemical Society, Vol. 126, Issue 26
Solvent Tuning of Electrochemical Potentials in the Active Sites of HiPIP Versus Ferredoxin
journal, November 2007
- Dey, A.; Jenney, F. E.; Adams, M. W. W.
- Science, Vol. 318, Issue 5855
DNA-Bound Redox Activity of DNA Repair Glycosylases Containing [4Fe-4S] Clusters †
journal, June 2005
- Boal, Amie K.; Yavin, Eylon; Lukianova, Olga A.
- Biochemistry, Vol. 44, Issue 23
A role for iron–sulfur clusters in DNA repair
journal, April 2005
- Lukianova, Olga A.; David, Sheila S.
- Current Opinion in Chemical Biology, Vol. 9, Issue 2
Endonuclease III is an iron-sulfur protein
journal, May 1989
- Cunningham, Richard P.; Asahara, Hitomi; Bank, Janet F.
- Biochemistry, Vol. 28, Issue 10
Direct Electrochemistry of Endonuclease III in the Presence and Absence of DNA
journal, September 2006
- Gorodetsky, Alon A.; Boal, Amie K.; Barton, Jacqueline K.
- Journal of the American Chemical Society, Vol. 128, Issue 37
DNA-mediated charge transport for DNA repair
journal, October 2003
- Boon, E. M.; Livingston, A. L.; Chmiel, N. H.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 22
DNA repair glycosylases with a [4Fe–4S] cluster: A redox cofactor for DNA-mediated charge transport?
journal, November 2007
- Boal, Amie K.; Yavin, Eylon; Barton, Jacqueline K.
- Journal of Inorganic Biochemistry, Vol. 101, Issue 11-12
DNA-Mediated Charge Transport as a Probe of MutY/DNA Interaction †
journal, July 2002
- Boon, Elizabeth M.; Pope, Mary Ann; Williams, Scott D.
- Biochemistry, Vol. 41, Issue 26
Ligand K-edge X-ray absorption spectroscopy: covalency of ligand–metal bonds
journal, January 2005
- Solomon, Edward I.; Hedman, Britt; Hodgson, Keith O.
- Coordination Chemistry Reviews, Vol. 249, Issue 1-2
Sulfur K-Edge X-ray Absorption Spectroscopy as a Probe of Ligand−Metal Bond Covalency: Metal vs Ligand Oxidation in Copper and Nickel Dithiolene Complexes
journal, February 2007
- Sarangi, Ritimukta; DeBeer George, Serena; Rudd, Deanne Jackson
- Journal of the American Chemical Society, Vol. 129, Issue 8
S K-edge X-ray Absorption Studies of Tetranuclear Iron−Sulfur Clusters: μ -Sulfide Bonding and Its Contribution to Electron Delocalization
journal, January 2001
- Glaser, Thorsten; Rose, Kendra; Shadle, Susan E.
- Journal of the American Chemical Society, Vol. 123, Issue 3
Multiplexed Electrochemistry of DNA-Bound Metalloproteins
journal, July 2013
- Pheeney, Catrina G.; Arnold, Anna R.; Grodick, Michael A.
- Journal of the American Chemical Society, Vol. 135, Issue 32
Ligand K-Edge X-ray Absorption Spectroscopy as a Probe of Ligand-Metal Bonding: Charge Donation and Covalency in Copper-Chloride Systems
journal, September 1994
- Shadle, Susan E.; Hedman, Britt; Hodgson, Keith O.
- Inorganic Chemistry, Vol. 33, Issue 19
Structure of a trapped endonuclease III-DNA covalent intermediate
journal, July 2003
- Fromme, J. C.
- The EMBO Journal, Vol. 22, Issue 13
Substrate recognition by Escherichia coli MutY using substrate analogs
journal, August 1999
- Chepanoske, C. L.; Porello, S. L.; Fujiwara, T.
- Nucleic Acids Research, Vol. 27, Issue 15
Efficient recognition of substrates and substrate analogs by the adenine glycosylase MutY requires the C-terminal domain
journal, January 2001
- Chmiel, N. H.
- Nucleic Acids Research, Vol. 29, Issue 2
Spectroscopic and DFT Studies of Second-Sphere Variants of the Type 1 Copper Site in Azurin: Covalent and Nonlocal Electrostatic Contributions to Reduction Potentials
journal, October 2012
- Hadt, Ryan G.; Sun, Ning; Marshall, Nicholas M.
- Journal of the American Chemical Society, Vol. 134, Issue 40
Positively Charged Residues within the Iron–Sulfur Cluster Loop of E. coli MutY Participate in Damage Recognition and Removal
journal, August 2000
- Chepanoske, Cindy Lou; Golinelli, Marie-Pierre; Williams, Scott D.
- Archives of Biochemistry and Biophysics, Vol. 380, Issue 1
Atomic structure of the DNA repair [4Fe-4S] enzyme endonuclease III
journal, October 1992
- Kuo, C.; McRee, D.; Fisher, C.
- Science, Vol. 258, Issue 5081
Works referencing / citing this record:
A combined Far-FTIR, FTIR Spectromicroscopy, and DFT Study of the Effect of DNA Binding on the [4Fe4S] Cluster Site in EndoIII
journal, February 2020
- Hassan, Ayaz; Macedo, Lucyano J. A.; Souza, João C. P. de
- Scientific Reports, Vol. 10, Issue 1
Direct experimental evaluation of ligand-induced backbonding in nickel metallacyclic complexes
journal, January 2019
- He, Weiying; Kennepohl, Pierre
- Faraday Discussions, Vol. 220
VMD: Visual molecular dynamics
journal, February 1996
- Humphrey, William; Dalke, Andrew; Schulten, Klaus
- Journal of Molecular Graphics, Vol. 14, Issue 1