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Mechanism of Superoxide and Hydrogen Peroxide Formation by Fumarate Reductase, Succinate Dehydrogenase, and Aspartate Oxidase
Open accessAbstract
Oxidative stress is created in aerobic organisms when molecular oxygen chemically oxidizes redox enzymes, forming superoxide (O2*-) and hydrogen peroxide (H2O2). Prior work identified several flavoenzymes from Escherichia coli that tend to autoxidize. Of these, fumarate reductase (Frd) is notable both for its high turnover number and for its production of substantial O2*- in addition to H2O2. We have sought to identify characteristics of Frd that predispose it to this behavior. The ability of excess succinate to block autoxidation and the inhibitory effect of lowering the flavin potential indicate that all detectable autoxidation occurs from its FAD site, rather than from iron-sulfur clusters or bound quinones. The flavin adenine dinucleotide (FAD) moiety of Frd is unusually solvent-exposed, as evidenced by its ability to bind sulfite, and this may make it more likely to react adventitiously with O2*-. The autoxidizing species is apparently fully reduced flavin rather than flavosemiquinone, since treatments that more fully reduce the enzyme do not slow its turnover number. They do, however, switch the major product from O2*- to H2O2. A similar effect is achieved by lowering the potential of the proximal [2Fe-2S] cluster. These data suggest that Frd releases O2*- into bulk solution if this cluster is available to sequester the semiquinone electron; otherwise, that electron is rapidly transferred to the nascent superoxide, and H2O2 is the product that leaves the active site. This model is supported by the behavior of "aspartate oxidase" (aspartate:fumarate oxidoreductase), an Frd homologue that lacks Fe-S clusters. Its dihydroflavin also reacts avidly with oxygen, and H2O2 is the predominant product. In contrast, succinate dehydrogenase, with high potential clusters, generates O2*- exclusively. The identities of enzyme autoxidation products are significant because O2*- and H2O2 damage cells in different ways.
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In the citing paper
“Both enzymes produced ROS with a linear dependence on the dissolved oxygen concentration, although SQR produced ROS at a much lower rate.”
From Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning (2013) · cites this paper as [101]
In the citing paper
“E. coli SQR exclusively produces superoxide.In contrast, E. coli QFR produces mainly superoxide at lower succinate concentrations and comparably more hydrogen peroxide at higher substrate concentrations [101].”
From Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning (2013) · cites this paper as [101]
In the citing paper
“While a contribution of the Q site might occur in the respective mutants, the most likely source of ROS in wild-type complex II is the fully reduced FAD [37,101].”
From Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning (2013) · cites this paper as [101]
In the citing paper
“Messner and Imlay concluded that QFR releases superoxide from the fully reduced flavin if the [2Fe-2S] cluster is available to sequester the semiquinone electron; otherwise this electron is rapidly transferred to the nascent superoxide and hydrogen peroxide is released [101].”
From Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning (2013) · cites this paper as [101]
In the citing paper
“In principle, fully reduced FAD can either transfer one electron onto molecular oxygen which leads to the formation of superoxide (probably the major reaction in complex II, but only confirmed for E. coli SQR [101]) or it may also transfer both electrons onto O 2 which leads to the formation of H 2 O 2 (as shown for E. coli QFR [101]) (Fig. 2B).”
From Differential effects of complex II on mitochondrial ROS production and their relation to cardioprotective pre- and postconditioning (2013) · cites this paper as [101]
In the citing paper
“An impairment in the normal removal of electrons from the flavin group in SdhA could promote superoxide generation through the autoxidation of the reduced flavin group by O 2 in the matrix (34, 38, 46, 51).”
From Loss of the SdhB, but Not the SdhA, Subunit of Complex II Triggers Reactive Oxygen Species-Dependent Hypoxia-Inducible Factor Activation and Tumorigenesis (2008) · cites this paper as [34]
In the citing paper
“Some evidence suggests that the flavin adenine dinucleotide site in SdhA is the principal source of superoxide generation, due to the exposure of that moiety to the aqueous environment and the high electron density that develops when the electron flux downstream from that site is obstructed (34, 51).”
From Loss of the SdhB, but Not the SdhA, Subunit of Complex II Triggers Reactive Oxygen Species-Dependent Hypoxia-Inducible Factor Activation and Tumorigenesis (2008) · cites this paper as [34]
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Targeting Mitochondria for Cancer Treatment
Zorova, L. D., Abramicheva, P. A., Andrianova, N. V., Babenko, V. A., Zorov, S. D., Pevzner, I. B., Popkov, V. A., Semenovich, D. S., Yakupova, E. I., Silachev, D. N., et al. (2024) · Pharmaceutics · doi:10.3390/pharmaceutics16040444 · Cited by 23
“…yields an increase in the probability of one-electron leakage from the reduced ubiquinone to available O 2 , the concentration of which, although small under conditions of physical hypoxia, is insufficient to obtain four electrons from cytochrome oxidase with subsequent formation of water [53–56].”
BackgroundJaiswal, P. K., Srivastava, S., Gupta, J., & Thakur, I. S. (2012) · Toxicology Letters · doi:10.1016/j.toxlet.2012.08.014 · Cited by 20
“After undergoing metabolism, PAHs produces ROS in high quantity by redox cycling (Imlay, 2003; Messner and Imlay, 2002).”
BackgroundEffect of Telmisartan in the Oxidative Stress Components Induced by Ischemia Reperfusion in Rats
Rodríguez-Lara, S. Q., Trujillo-Rangel, W. Á., Castillo‐Romero, A., Totsuka-Sutto, S. E., García-Cobián, T. A., Cardona-Muñóz, E. G., Miranda‐Díaz, A. G., Ramírez-Lizardo, E. J., & García‐Benavides, L. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/1302985 · Cited by 21
Norambuena, J., Hanson, T. E., Barkay, T., & Boyd, J. M. (2019) · mBio · doi:10.1128/mbio.00183-19 · Cited by 18
Mounkoro, P., Michel, T., Golinelli‐Cohen, M., Blandin, S. A., Davioud–Charvet, E., & Meunier, B. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.11.010 · Cited by 18
Zhao, Z., Rothery, R. A., & Weiner, J. H. (2006) · Biochemistry and Cell Biology · doi:10.1139/o06-188 · Cited by 18
“Moreover, when we used an enzyme fraction with limited ubiquinone in the membrane (a result of microaerobic expression) and without exogenous ubiquinone, we observed a succinate-concentration dependent profile of superoxide production (data not shown) that was very similar to that reported previously (Messner and Imla…”
BackgroundMethodResultInfluentialDíaz-Vásquez, W. A., Abarca-Lagunas, M. J., Cornejo, F. A., Pinto, C. A., Arenas, F., & Vásquez, C. C. (2014) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2014.10.011 · Cited by 17
Zhang, Z., Pan, B., Wang, L., & Sun, G. Z. (2021) · ACS Applied Bio Materials · doi:10.1021/acsabm.1c01042 · Cited by 16
Hypothesis: Why Different Types of SDH Gene Variants Cause Divergent Tumor Phenotypes
Bayley, J., & Devilee, P. (2022) · Genes · doi:10.3390/genes13061025 · Cited by 18
Huang, X., Harmer, J. R., Schenk, G., & Southam, G. (2024) · Frontiers in Chemistry · doi:10.3389/fchem.2024.1349020 · Cited by 18
“In these reactions, hydrogen atoms are used to form water or H 2 O 2 by enzymes such as sul fi te oxidase (SOE), glucose oxidase (GOX), or alcohol oxidase (AOX) (Messner and Imlay, 2002; Leskovac et al., 2005; Jancura et al., 2014; Kappler and Enemark, 2015).”
Kassem, I. I., Khatri, M., Sanad, Y. M., Wolboldt, M., Saif, Y. Μ., Olson, J. W., & Rajashekara, G. (2014) · MicrobiologyOpen · doi:10.1002/mbo3.158 · Cited by 16
“Since chemically oxidized redox-enzymes, including fumarate reductase and Sdh, contribute to the generation of oxidative stress in Escherichia coli, we assessed the role of Mfr in C. jejuni after exposure to hydrogen peroxide (H2O2).”
BackgroundLin, C., Huang, F.-P., Ling, Y. S., Liang, H., Lee, S.-H., Hu, M.-Y., & Tsao, P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0120429 · Cited by 16
“Moreover, the literature suggests that succinate plays a role in antioxidant-based prevention of autoxidation [38] and reduces injuries due to oxidative stress.”
BackgroundDong, R., Liang, Y., He, S., Cui, Y., Shi, C., He, Y., & Shi, X. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01522-21 · Cited by 15
“vins or iron-sulfur clusters for univalent redox reactions (7, 9).”
BackgroundHow an assembly factor enhances covalent FAD attachment to the flavoprotein subunit of complex II
Maklashina, E., Iverson, T. M., & Cecchini, G. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102472 · Cited by 15
“Similarly, high fumarate or succinate concentrations inhibit hydrogen peroxide production in mature complex II (39, 40).”
BackgroundTargeting Oxidative Stress in Stroke
Bach, A. (2017) · Springer series in translational stroke research · doi:10.1007/978-3-319-45345-3_8 · Cited by 15
Selivanov, V. A., Zagubnaya, O. A., Nartsissov, Y. R., & Cascante, M. (2021) · PLoS ONE · doi:10.1371/journal.pone.0255164 · Cited by 15
“Our simulation of ROS production in the flavin site of complex II (according to Messner and Imlay [41]) with inhibited electron transport through complexes I and III reproduced such a bell-shaped peak at low succinate concentrations (~50 μM).”
MethodKorshunov, S., & Imlay, J. A. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2516113122 · Cited by 14
Self-citationLiu, S., & Schäfer, A. I. (2026) · Chemical Reviews · doi:10.1021/acs.chemrev.5c01120 · Cited by 15
Identification of the YfgF MASE1 domain as a modulator of bacterial responses to aspartate
Lacey, M. M., Agasing, A. M., Lowry, R. C., & Green, J. D. (2013) · Open Biology · doi:10.1098/rsob.130046 · Cited by 14
“coli is transferred from anaerobic to aerobic conditions [22,23].”
Sommer, S.-P., Sommer, S., Sinha, B. N. M., Walter, D., Aleksić, I., Gohrbandt, B., Otto, C., & Leyh, R. G. (2011) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/j.ejcts.2011.02.081 · Cited by 14
“Catalysis at SQR contributes to mitochondrial superoxide generation [15].”
BackgroundPan, Y., Wang, Y., Fan, X., Wang, W., Yang, X., Cui, D., & Zhao, M. (2019) · Environmental Microbiology Reports · doi:10.1111/1758-2229.12733 · Cited by 14
“We speculated that the accumulated H2O2 was decomposed into O2 by BMNPs in the absence of POD; however, the increase in O2 concentration in the culture resulted in a decrease in BMNP production.”
BackgroundInfluentialReactive Oxygen Species in the Induction of Toxicity
Lenaz, G., & Strocchi, P. (2009) · Wiley eBooks · doi:10.1002/9780470744307.gat024 · Cited by 15
Salmonella Central Carbon Metabolism Enhances Bactericidal Killing by Fluoroquinolone Antibiotics
Braetz, S., Schwerk, P., Thompson, A., Tedin, K., & Fulde, M. (2022) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02344-21 · Cited by 13
Partipilo, M., Yang, G., Mascotti, M. L., Wijma, H. J., Slotboom, D. J., & Fraaije, M. W. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102304 · Cited by 13
“In recent years, a growing number of reports in the literature have shown how various flavoenzymes display side reactivity with molecular oxygen, forming ROS (19, 23).”
BackgroundGalván, A. E., Chalón, M. C., Schurig-Briccio, L. A., Salomón, R. A., Minahk, C. J., Gennis, R. B., & Bellomio, A. (2017) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2017.10.006 · Cited by 13
Out of plane distortions of the heme b of Escherichia coli succinate dehydrogenase
Tran, Q. M., Fong, C., Rothery, R. A., Maklashina, E., Cecchini, G., & Weiner, J. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032641 · Cited by 12
“Measurement of reactive oxygen species A cytochrome c reduction assay was used to quantitate the production of superoxide during enzyme turnover [9].”
MethodInfluentialThe Various Sources of Mitochondrial Oxygen Radicals: A Minireview
Bernacchia, A., Biondi, A., Genova, M. L., Lenaz, G., & Falasca, A. I. (2004) · Toxicology Mechanisms and Methods · doi:10.1080/15376520490257383 · Cited by 12
“Significantly, E. coli QFR is a potent source of H2O2, whereas SQR is not (Messner and Imlay 2002).”
Background
Metadata
- Authors
- Messner, K. R., & Imlay, J. A.
- Affiliations
- University of Illinois Urbana-Champaign (US)
- Corresponding author
- Imlay, James A.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2002-11
- Volume
- 277
- Issue
- 45
- Pages
- 42563-42571
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2044412059
- Cited by
- 301
- References
- 57
- Citations by year
- 2026: 9 · 2025: 4 · 2024: 12 · 2023: 11 · 2022: 15 · 2021: 14 · 2020: 18 · 2019: 13 · 2018: 17 · 2017: 14 · 2016: 8 · 2015: 12 · 2014: 16 · 2013: 21 · 2012: 18
- FWCI
- 3.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (GM49640)
- National Institute of General Medical Sciences (R01GM049640, GM 49640, T32 GM07283-20, T32GM007283)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
- Keywords
- fumarate reductase, succinate dehydrogenase, superoxide production, hydrogen peroxide production, FAD, flavin semiquinone, [2Fe-2S] cluster, oxidative stress, Escherichia coli
- MeSH terms
- Amino Acid Oxidoreductases, Cell Line, Cell Membrane, Escherichia coli, Flavin-Adenine Dinucleotide, Hydrogen Peroxide, Iron-Sulfur Proteins, Kinetics, Oxidation-Reduction, Solvents, Succinate Dehydrogenase, Superoxides, D-Aspartate Oxidase
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