Structure of 3-mercaptopropionic acid dioxygenase with a substrate analog reveals bidentate substrate binding at the iron center
Abstract
Thiol dioxygenases are a subset of nonheme iron oxygenases that catalyze the formation of sulfinic acids from sulfhydryl-containing substrates and dioxygen. Among this class, cysteine dioxygenases (CDOs) and 3-mercaptopropionic acid dioxygenases (3MDOs) are the best characterized, and the mode of substrate binding for CDOs is well understood. However, the manner in which 3-mercaptopropionic acid (3MPA) coordinates to the nonheme iron site in 3MDO remains a matter of debate. A model for bidentate 3MPA coordination at the 3MDO Fe-site has been proposed on the basis of computational docking, whereas steady-state kinetics and EPR spectroscopic measurements suggest a thiolate-only coordination of the substrate. To address this gap in knowledge, we determined the structure of Azobacter vinelandii 3MDO (Av3MDO) in complex with the substrate analog and competitive inhibitor, 3-hydroxypropionic acid (3HPA). The structure together with DFT computational modeling demonstrates that 3HPA and 3MPA associate with iron as chelate complexes with the substrate-carboxylate group forming an additional interaction with Arg168 and the thiol bound at the same position as in CDO. A chloride ligand was bound to iron in the coordination site assigned as the O2-binding site. Supporting HYSCORE spectroscopic experiments were performed on the (3MPA/NO)-bound Av3MDO iron nitrosyl (S = 3/2) site. Inmore »
- Authors:
-
- Univ. of Alabama, Birmingham, AL (United States). Dept. of Chemistry and Biochemistry
- Univ. of Texas, Arlington, TX (United States). Dept. of Chemistry and Biochemistry
- Case Western Reserve Univ., Cleveland, OH (United States). Dept. of Pharmacology
- Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)
- Univ. of Washington, Seattle, WA (United States). Depts. of Biological Structure and Biochemistry
- Univ. of California, Irvine, CA (United States). School of Medicine, Dept. of Ophthalmology
- Univ. of California, Irvine, CA (United States). School of Medicine, Dept. of Ophthalmology; Univ. of California, Irvine, CA (United States). School of Medicine, Dept. of Physiology and Biophysics; VA Long Beach Healthcare System, CA (United States). Research Service
- Publication Date:
- Research Org.:
- Brookhaven National Lab. (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1778798
- Report Number(s):
- BNL-221309-2021-JAAM
Journal ID: ISSN 0021-9258
- Grant/Contract Number:
- SC0012704
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 296; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE
Citation Formats
York, Nicholas J., Lockart, Molly M., Sardar, Sinjinee, Khadka, Nimesh, Shi, Wuxian, Stenkamp, Ronald E., Zhang, Jianye, Kiser, Philip D., and Pierce, Brad S. Structure of 3-mercaptopropionic acid dioxygenase with a substrate analog reveals bidentate substrate binding at the iron center. United States: N. p., 2021.
Web. doi:10.1016/j.jbc.2021.100492.
York, Nicholas J., Lockart, Molly M., Sardar, Sinjinee, Khadka, Nimesh, Shi, Wuxian, Stenkamp, Ronald E., Zhang, Jianye, Kiser, Philip D., & Pierce, Brad S. Structure of 3-mercaptopropionic acid dioxygenase with a substrate analog reveals bidentate substrate binding at the iron center. United States. https://doi.org/10.1016/j.jbc.2021.100492
York, Nicholas J., Lockart, Molly M., Sardar, Sinjinee, Khadka, Nimesh, Shi, Wuxian, Stenkamp, Ronald E., Zhang, Jianye, Kiser, Philip D., and Pierce, Brad S. Fri .
"Structure of 3-mercaptopropionic acid dioxygenase with a substrate analog reveals bidentate substrate binding at the iron center". United States. https://doi.org/10.1016/j.jbc.2021.100492. https://www.osti.gov/servlets/purl/1778798.
@article{osti_1778798,
title = {Structure of 3-mercaptopropionic acid dioxygenase with a substrate analog reveals bidentate substrate binding at the iron center},
author = {York, Nicholas J. and Lockart, Molly M. and Sardar, Sinjinee and Khadka, Nimesh and Shi, Wuxian and Stenkamp, Ronald E. and Zhang, Jianye and Kiser, Philip D. and Pierce, Brad S.},
abstractNote = {Thiol dioxygenases are a subset of nonheme iron oxygenases that catalyze the formation of sulfinic acids from sulfhydryl-containing substrates and dioxygen. Among this class, cysteine dioxygenases (CDOs) and 3-mercaptopropionic acid dioxygenases (3MDOs) are the best characterized, and the mode of substrate binding for CDOs is well understood. However, the manner in which 3-mercaptopropionic acid (3MPA) coordinates to the nonheme iron site in 3MDO remains a matter of debate. A model for bidentate 3MPA coordination at the 3MDO Fe-site has been proposed on the basis of computational docking, whereas steady-state kinetics and EPR spectroscopic measurements suggest a thiolate-only coordination of the substrate. To address this gap in knowledge, we determined the structure of Azobacter vinelandii 3MDO (Av3MDO) in complex with the substrate analog and competitive inhibitor, 3-hydroxypropionic acid (3HPA). The structure together with DFT computational modeling demonstrates that 3HPA and 3MPA associate with iron as chelate complexes with the substrate-carboxylate group forming an additional interaction with Arg168 and the thiol bound at the same position as in CDO. A chloride ligand was bound to iron in the coordination site assigned as the O2-binding site. Supporting HYSCORE spectroscopic experiments were performed on the (3MPA/NO)-bound Av3MDO iron nitrosyl (S = 3/2) site. In combination with spectroscopic simulations and optimized DFT models, this work provides an experimentally verified model of the Av3MDO enzyme–substrate complex, effectively resolving a debate in the literature regarding the preferred substrate-binding denticity. These results elegantly explain the observed 3MDO substrate specificity, but leave unanswered questions regarding the mechanism of substrate-gated reactivity with dioxygen.},
doi = {10.1016/j.jbc.2021.100492},
journal = {Journal of Biological Chemistry},
number = ,
volume = 296,
place = {United States},
year = {Fri Jan 01 00:00:00 EST 2021},
month = {Fri Jan 01 00:00:00 EST 2021}
}
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