Production of superoxide/hydrogen peroxide by the mitochondrial 2-oxoadipate dehydrogenase complex - PubMed (original) (raw)
Production of superoxide/hydrogen peroxide by the mitochondrial 2-oxoadipate dehydrogenase complex
Renata L S Goncalves et al. Free Radic Biol Med. 2016 Feb.
Free article
Abstract
In humans, mutations in dehydrogenase E1 and transketolase domain containing 1 (DHTKD1) are associated with neurological abnormalities and accumulation of 2-oxoadipate, 2-aminoadipate, and reactive oxygen species. The protein encoded by DHTKD1 has sequence and structural similarities to 2-oxoglutarate dehydrogenase, and the 2-oxoglutarate dehydrogenase complex can produce superoxide/H2O2 at high rates. The DHTKD1 enzyme is hypothesized to catalyze the oxidative decarboxylation of 2-oxoadipate, a shared intermediate of the degradative pathways for tryptophan, lysine and hydroxylysine. Here, we show that rat skeletal muscle mitochondria can produce superoxide/H2O2 at high rates when given 2-oxoadipate. We identify the putative mitochondrial 2-oxoadipate dehydrogenase complex as one of the sources and characterize the conditions that favor its superoxide/H2O2 production. Rates increased at higher NAD(P)H/NAD(P)(+) ratios and were higher at each NAD(P)H/NAD(P)(+) ratio when 2-oxoadipate was present, showing that superoxide/H2O2 was produced during the forward reaction from 2-oxoadipate, but not in the reverse reaction from NADH in the absence of 2-oxoadipate. The maximum capacity of the 2-oxoadipate dehydrogenase complex for production of superoxide/H2O2 is comparable to that of site IF of complex I, and seven, four and almost two-fold lower than the capacities of the 2-oxoglutarate, pyruvate and branched-chain 2-oxoacid dehydrogenase complexes, respectively. Regulation by ADP and ATP of H2O2 production driven by 2-oxoadipate was very different from that driven by 2-oxoglutarate, suggesting that site AF of the 2-oxoadipate dehydrogenase complex is a new source of superoxide/H2O2 associated with the NADH isopotential pool in mitochondria.
Keywords: 2-Oxoacid dehydrogenase complexes; 2-Oxoadipic acid dehydrogenase; DHTKD1; ROS; Reactive oxygen species; Skeletal muscle mitochondria.
Copyright © 2015 Elsevier Inc. All rights reserved.
Similar articles
- The 2-oxoacid dehydrogenase complexes in mitochondria can produce superoxide/hydrogen peroxide at much higher rates than complex I.
Quinlan CL, Goncalves RL, Hey-Mogensen M, Yadava N, Bunik VI, Brand MD. Quinlan CL, et al. J Biol Chem. 2014 Mar 21;289(12):8312-25. doi: 10.1074/jbc.M113.545301. Epub 2014 Feb 10. J Biol Chem. 2014. PMID: 24515115 Free PMC article. - The human Krebs cycle 2-oxoglutarate dehydrogenase complex creates an additional source of superoxide/hydrogen peroxide from 2-oxoadipate as alternative substrate.
Nemeria NS, Gerfen G, Guevara E, Nareddy PR, Szostak M, Jordan F. Nemeria NS, et al. Free Radic Biol Med. 2017 Jul;108:644-654. doi: 10.1016/j.freeradbiomed.2017.04.017. Epub 2017 Apr 21. Free Radic Biol Med. 2017. PMID: 28435050 - The mitochondrial 2-oxoadipate and 2-oxoglutarate dehydrogenase complexes share their E2 and E3 components for their function and both generate reactive oxygen species.
Nemeria NS, Gerfen G, Nareddy PR, Yang L, Zhang X, Szostak M, Jordan F. Nemeria NS, et al. Free Radic Biol Med. 2018 Feb 1;115:136-145. doi: 10.1016/j.freeradbiomed.2017.11.018. Epub 2017 Dec 1. Free Radic Biol Med. 2018. PMID: 29191460 - Human 2-Oxoglutarate Dehydrogenase and 2-Oxoadipate Dehydrogenase Both Generate Superoxide/H2O2 in a Side Reaction and Each Could Contribute to Oxidative Stress in Mitochondria.
Jordan F, Nemeria N, Gerfen G. Jordan F, et al. Neurochem Res. 2019 Oct;44(10):2325-2335. doi: 10.1007/s11064-019-02765-w. Epub 2019 Mar 7. Neurochem Res. 2019. PMID: 30847859 Review. - Generation of superoxide and hydrogen peroxide by side reactions of mitochondrial 2-oxoacid dehydrogenase complexes in isolation and in cells.
Bunik VI, Brand MD. Bunik VI, et al. Biol Chem. 2018 Apr 25;399(5):407-420. doi: 10.1515/hsz-2017-0284. Biol Chem. 2018. PMID: 29337692 Review.
Cited by
- Suppressors of Superoxide-H2O2 Production at Site IQ of Mitochondrial Complex I Protect against Stem Cell Hyperplasia and Ischemia-Reperfusion Injury.
Brand MD, Goncalves RL, Orr AL, Vargas L, Gerencser AA, Borch Jensen M, Wang YT, Melov S, Turk CN, Matzen JT, Dardov VJ, Petrassi HM, Meeusen SL, Perevoshchikova IV, Jasper H, Brookes PS, Ainscow EK. Brand MD, et al. Cell Metab. 2016 Oct 11;24(4):582-592. doi: 10.1016/j.cmet.2016.08.012. Epub 2016 Sep 22. Cell Metab. 2016. PMID: 27667666 Free PMC article. - Toward an Understanding of the Structural and Mechanistic Aspects of Protein-Protein Interactions in 2-Oxoacid Dehydrogenase Complexes.
Nemeria NS, Zhang X, Leandro J, Zhou J, Yang L, Houten SM, Jordan F. Nemeria NS, et al. Life (Basel). 2021 Apr 29;11(5):407. doi: 10.3390/life11050407. Life (Basel). 2021. PMID: 33946784 Free PMC article. Review. - Lipoic acid metabolism and mitochondrial redox regulation.
Solmonson A, DeBerardinis RJ. Solmonson A, et al. J Biol Chem. 2018 May 18;293(20):7522-7530. doi: 10.1074/jbc.TM117.000259. Epub 2017 Nov 30. J Biol Chem. 2018. PMID: 29191830 Free PMC article. Review. - Induction of mitochondrial reactive oxygen species production by GSH mediated S-glutathionylation of 2-oxoglutarate dehydrogenase.
Mailloux RJ, Craig Ayre D, Christian SL. Mailloux RJ, et al. Redox Biol. 2016 Aug;8:285-97. doi: 10.1016/j.redox.2016.02.002. Epub 2016 Feb 17. Redox Biol. 2016. PMID: 26928132 Free PMC article. - Crystal structure and interaction studies of human DHTKD1 provide insight into a mitochondrial megacomplex in lysine catabolism.
Bezerra GA, Foster WR, Bailey HJ, Hicks KG, Sauer SW, Dimitrov B, McCorvie TJ, Okun JG, Rutter J, Kölker S, Yue WW. Bezerra GA, et al. IUCrJ. 2020 Jun 10;7(Pt 4):693-706. doi: 10.1107/S205225252000696X. eCollection 2020 Jul 1. IUCrJ. 2020. PMID: 32695416 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Miscellaneous