Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics
Abstract
:1. Introduction
2. Endogenous Production of H2S
2.1. Non-Enzymatic Production of H2S
2.2. Enzymatic Production of H2S
3. S-Sulfhydration of ATP Synthase
4. S-Sulfhydration of Lactate Dehydrogenase (LDH)
5. H2S Donates Electrons to the Mitochondrial Respiratory Chain via Sulfide Quinone Oxidoreductase (SQOR)
6. H2S at Toxic Concentrations Inhibits Mitochondrial Cytochrome c Oxidase
7. H2S at Low Concentrations Serves as Electron Donor for Mitochondrial Cytochrome c Oxidase
8. Effect of H2S on the Operation of the Branched Respiratory Chain of E. coli and Bacterial Growth
9. Concluding Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Abe, K.; Kimura, H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 1996, 16, 1066–1071. [Google Scholar] [CrossRef] [Green Version]
- Yang, G.; Wu, L.; Jiang, B.; Yang, W.; Qi, J.; Cao, K.; Meng, Q.; Mustafa, A.K.; Mu, W.; Zhang, S.; et al. H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine gamma-lyase. Science 2008, 322, 587–590. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bakalarz, D.; Korbut, E.; Yuan, Z.; Yu, B.; Wojcik, D.; Danielak, A.; Magierowska, K.; Kwiecien, S.; Brzozowski, T.; Marcinkowska, M.; et al. Novel hydrogen sulfide (H2S)-releasing BW-HS-101 and its non-H2S releasing derivative in modulation of microscopic and molecular parameters of gastric mucosal barrier. Int. J. Mol. Sci. 2021, 22, 5211. [Google Scholar] [CrossRef] [PubMed]
- Nowaczyk, A.; Kowalska, M.; Nowaczyk, J.; Grzesk, G. Carbon monoxide and nitric oxide as examples of the youngest class of transmitters. Int. J. Mol. Sci. 2021, 22, 6029. [Google Scholar] [CrossRef]
- Kimura, H. Production and physiological effects of hydrogen sulfide. Antioxid. Redox Signal. 2014, 20, 783–793. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wareham, L.K.; Southam, H.M.; Poole, R.K. Do nitric oxide, carbon monoxide and hydrogen sulfide really qualify as ’gasotransmitters’ in bacteria? Biochem. Soc. Trans. 2018, 46, 1107–1118. [Google Scholar] [CrossRef] [Green Version]
- Randi, E.B.; Zuhra, K.; Pecze, L.; Panagaki, T.; Szabo, C. Physiological concentrations of cyanide stimulate mitochondrial Complex IV and enhance cellular bioenergetics. Proc. Natl. Acad. Sci. USA 2021, 118, e2026245118. [Google Scholar] [CrossRef]
- Giamogante, F.; Cali, T.; Malatesta, F. Physiological cyanide concentrations do not stimulate mitochondrial cytochrome c oxidase activity. Proc. Natl. Acad. Sci. USA 2021, 118, e2112373118. [Google Scholar] [CrossRef]
- Zhao, W.; Zhang, J.; Lu, Y.; Wang, R. The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. Embo J. 2001, 20, 6008–6016. [Google Scholar] [CrossRef] [Green Version]
- Papapetropoulos, A.; Pyriochou, A.; Altaany, Z.; Yang, G.; Marazioti, A.; Zhou, Z.; Jeschke, M.G.; Branski, L.K.; Herndon, D.N.; Wang, R.; et al. Hydrogen sulfide is an endogenous stimulator of angiogenesis. Proc. Natl. Acad. Sci. USA 2009, 106, 21972–21977. [Google Scholar] [CrossRef] [Green Version]
- Yang, G.; Sun, X.; Wang, R. Hydrogen sulfide-induced apoptosis of human aorta smooth muscle cells via the activation of mitogen-activated protein kinases and caspase-3. FASEB J. 2004, 18, 1782–1784. [Google Scholar] [CrossRef] [PubMed]
- Murphy, B.; Bhattacharya, R.; Mukherjee, P. Hydrogen sulfide signaling in mitochondria and disease. FASEB J. 2019, 33, 13098–13125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cao, X.; Ding, L.; Xie, Z.Z.; Yang, Y.; Whiteman, M.; Moore, P.K.; Bian, J.S. A review of hydrogen sulfide synthesis, metabolism, and measurement: Is modulation of hydrogen sulfide a novel therapeutic for cancer? Antioxid. Redox Signal. 2019, 31, 1–38. [Google Scholar] [CrossRef] [PubMed]
- Corpas, F.J.; Palma, J.M. H2S signaling in plants and applications in agriculture. J. Adv. Res. 2020, 24, 131–137. [Google Scholar] [CrossRef]
- Shatalin, K.; Shatalina, E.; Mironov, A.; Nudler, E. H2S: A universal defense against antibiotics in bacteria. Science 2011, 334, 986–990. [Google Scholar] [CrossRef]
- Borisov, V.B.; Siletsky, S.A.; Nastasi, M.R.; Forte, E. ROS defense systems and terminal oxidases in bacteria. Antioxidants 2021, 10, 839. [Google Scholar] [CrossRef]
- Calhoun, D.B.; Englander, S.W.; Wright, W.W.; Vanderkooi, J.M. Quenching of room temperature protein phosphorescence by added small molecules. Biochemistry 1988, 27, 8466–8474. [Google Scholar] [CrossRef]
- Riahi, S.; Rowley, C.N. Why can hydrogen sulfide permeate cell membranes? J. Am. Chem. Soc. 2014, 136, 15111–15113. [Google Scholar] [CrossRef]
- Li, Q.; Lancaster, J.R., Jr. Chemical foundations of hydrogen sulfide biology. Nitric Oxide 2013, 35, 21–34. [Google Scholar] [CrossRef] [Green Version]
- Llopis, J.; McCaffery, J.M.; Miyawaki, A.; Farquhar, M.G.; Tsien, R.Y. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. USA 1998, 95, 6803–6808. [Google Scholar] [CrossRef] [Green Version]
- Abad, M.F.; Di Benedetto, G.; Magalhaes, P.J.; Filippin, L.; Pozzan, T. Mitochondrial pH monitored by a new engineered green fluorescent protein mutant. J. Biol. Chem. 2004, 279, 11521–11529. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohkuma, S.; Poole, B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. USA 1978, 75, 3327–3331. [Google Scholar] [CrossRef] [Green Version]
- Powell, C.R.; Dillon, K.M.; Matson, J.B. A review of hydrogen sulfide (H2S) donors: Chemistry and potential therapeutic applications. Biochem. Pharmacol. 2018, 149, 110–123. [Google Scholar] [CrossRef]
- Yang, J.; Minkler, P.; Grove, D.; Wang, R.; Willard, B.; Dweik, R.; Hine, C. Non-enzymatic hydrogen sulfide production from cysteine in blood is catalyzed by iron and vitamin B6. Commun. Biol. 2019, 2, 194. [Google Scholar] [CrossRef] [Green Version]
- Kabil, O.; Vitvitsky, V.; Xie, P.; Banerjee, R. The quantitative significance of the transsulfuration enzymes for H2S production in murine tissues. Antioxid. Redox Signal. 2011, 15, 363–372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giuffre, A.; Vicente, J.B. Hydrogen sulfide biochemistry and interplay with other gaseous mediators in mammalian physiology. Oxid. Med. Cell. Longev. 2018, 2018, 6290931. [Google Scholar] [CrossRef] [PubMed]
- Shatalin, K.; Nuthanakanti, A.; Kaushik, A.; Shishov, D.; Peselis, A.; Shamovsky, I.; Pani, B.; Lechpammer, M.; Vasilyev, N.; Shatalina, E.; et al. Inhibitors of bacterial H2S biogenesis targeting antibiotic resistance and tolerance. Science 2021, 372, 1169–1175. [Google Scholar] [CrossRef]
- Caruana, N.J.; Stroud, D.A. The road to the structure of the mitochondrial respiratory chain supercomplex. Biochem. Soc. Trans. 2020, 48, 621–629. [Google Scholar] [CrossRef] [Green Version]
- Cogliati, S.; Cabrera-Alarcon, J.L.; Enriquez, J.A. Regulation and functional role of the electron transport chain supercomplexes. Biochem. Soc. Trans. 2021, BST20210460. [Google Scholar] [CrossRef]
- Modis, K.; Ju, Y.; Ahmad, A.; Untereiner, A.A.; Altaany, Z.; Wu, L.; Szabo, C.; Wang, R. S-Sulfhydration of ATP synthase by hydrogen sulfide stimulates mitochondrial bioenergetics. Pharmacol. Res. 2016, 113, 116–124. [Google Scholar] [CrossRef] [Green Version]
- Untereiner, A.A.; Olah, G.; Modis, K.; Hellmich, M.R.; Szabo, C. H2S-induced S-sulfhydration of lactate dehydrogenase a (LDHA) stimulates cellular bioenergetics in HCT116 colon cancer cells. Biochem. Pharmacol. 2017, 136, 86–98. [Google Scholar] [CrossRef] [PubMed]
- Goubern, M.; Andriamihaja, M.; Nubel, T.; Blachier, F.; Bouillaud, F. Sulfide, the first inorganic substrate for human cells. FASEB J. 2007, 21, 1699–1706. [Google Scholar] [CrossRef] [PubMed]
- Nicholls, P. The effect of sulphide on cytochrome aa3. Isosteric and allosteric shifts of the reduced α-peak. Biochim. Biophys. Acta 1975, 396, 24–35. [Google Scholar] [CrossRef]
- Petersen, L.C. The effect of inhibitors on the oxygen kinetics of cytochrome c oxidase. Biochim. Biophys. Acta 1977, 460, 299–307. [Google Scholar] [CrossRef]
- Szabo, C.; Ransy, C.; Modis, K.; Andriamihaja, M.; Murghes, B.; Coletta, C.; Olah, G.; Yanagi, K.; Bouillaud, F. Regulation of mitochondrial bioenergetic function by hydrogen sulfide. Part I. Biochemical and physiological mechanisms. Br. J. Pharmacol. 2014, 171, 2099–2122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nicholls, P.; Kim, J.K. Oxidation of sulphide by cytochrome aa3. Biochim. Biophys. Acta 1981, 637, 312–320. [Google Scholar] [CrossRef]
- Nicholls, P.; Kim, J.K. Sulphide as an inhibitor and electron donor for the cytochrome c oxidase system. Can. J. Biochem. 1982, 60, 613–623. [Google Scholar] [CrossRef] [PubMed]
- Nicholls, P.; Marshall, D.C.; Cooper, C.E.; Wilson, M.T. Sulfide inhibition of and metabolism by cytochrome c oxidase. Biochem. Soc. Trans. 2013, 41, 1312–1316. [Google Scholar] [CrossRef] [Green Version]
- Vitvitsky, V.; Miljkovic, J.L.; Bostelaar, T.; Adhikari, B.; Yadav, P.K.; Steiger, A.K.; Torregrossa, R.; Pluth, M.D.; Whiteman, M.; Banerjee, R.; et al. Cytochrome c reduction by H2S potentiates sulfide signaling. ACS Chem. Biol. 2018, 13, 2300–2307. [Google Scholar] [CrossRef]
- Doherty, J.R.; Cleveland, J.L. Targeting lactate metabolism for cancer therapeutics. J. Clin. Invest. 2013, 123, 3685–3692. [Google Scholar] [CrossRef]
- Powell, M.A.; Somero, G.N. Hydrogen sulfide oxidation Is coupled to oxidative phosphorylation in mitochondria of Solemya reidi. Science 1986, 233, 563–566. [Google Scholar] [CrossRef]
- Landry, A.P.; Ballou, D.P.; Banerjee, R. Hydrogen sulfide oxidation by sulfide quinone oxidoreductase. Chembiochem 2021, 22, 949–960. [Google Scholar] [CrossRef] [PubMed]
- Landry, A.P.; Moon, S.; Kim, H.; Yadav, P.K.; Guha, A.; Cho, U.S.; Banerjee, R. A catalytic trisulfide in human sulfide quinone oxidoreductase catalyzes Coenzyme A persulfide synthesis and inhibits butyrate oxidation. Cell Chem. Biol. 2019, 26, 1515–1525.e1514. [Google Scholar] [CrossRef] [PubMed]
- Malatesta, F.; Antonini, G.; Sarti, P.; Brunori, M. Structure and function of a molecular machine: Cytochrome c oxidase. Biophys. Chem. 1995, 54, 1–33. [Google Scholar] [CrossRef]
- Melo, A.M.; Teixeira, M. Supramolecular organization of bacterial aerobic respiratory chains: From cells and back. Biochim. Biophys. Acta 2016, 1857, 190–197. [Google Scholar] [CrossRef]
- Siletsky, S.A.; Borisov, V.B.; Mamedov, M.D. Photosystem II and terminal respiratory oxidases: Molecular machines operating in opposite directions. Front. Biosci. 2017, 22, 1379–1426. [Google Scholar] [CrossRef] [Green Version]
- Pereira, M.M.; Sousa, F.L.; Verissimo, A.F.; Teixeira, M. Looking for the minimum common denominator in haem-copper oxygen reductases: Towards a unified catalytic mechanism. Biochim. Biophys. Acta 2008, 1777, 929–934. [Google Scholar] [CrossRef] [Green Version]
- Pereira, M.M.; Santana, M.; Teixeira, M. A novel scenario for the evolution of haem-copper oxygen reductases. Biochim. Biophys. Acta 2001, 1505, 185–208. [Google Scholar] [CrossRef] [Green Version]
- Pereira, M.M.; Gomes, C.M.; Teixeira, M. Plasticity of proton pathways in haem-copper oxygen reductases. FEBS Lett. 2002, 522, 14–18. [Google Scholar] [CrossRef] [Green Version]
- Pereira, M.M.; Teixeira, M. Proton pathways, ligand binding and dynamics of the catalytic site in haem-copper oxygen reductases: A comparison between the three families. Biochim. Biophys. Acta 2004, 1655, 340–346. [Google Scholar] [CrossRef] [Green Version]
- Papa, S.; Capitanio, N.; Capitanio, G.; Palese, L.L. Protonmotive cooperativity in cytochrome c oxidase. Biochim. Biophys. Acta 2004, 1658, 95–105. [Google Scholar] [CrossRef] [Green Version]
- Borisov, V.B. Defects in mitochondrial respiratory complexes III and IV, and human pathologies. Mol. Aspects Med. 2002, 23, 385–412. [Google Scholar] [CrossRef]
- Borisov, V.B. Mutations in respiratory chain complexes and human diseases. Ital. J. Biochem. 2004, 53, 34–40. [Google Scholar]
- Borisov, V.B.; Siletsky, S.A. Features of organization and mechanism of catalysis of two families of terminal oxidases: Heme-copper and bd-type. Biochemistry 2019, 84, 1390–1402. [Google Scholar] [CrossRef] [PubMed]
- Hederstedt, L. Molecular biology of Bacillus subtilis cytochromes anno 2020. Biochemistry 2021, 86, 8–21. [Google Scholar] [CrossRef]
- Sousa, F.L.; Alves, R.J.; Ribeiro, M.A.; Pereira-Leal, J.B.; Teixeira, M.; Pereira, M.M. The superfamily of heme-copper oxygen reductases: Types and evolutionary considerations. Biochim. Biophys. Acta 2012, 1817, 629–637. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wikstrom, M.; Krab, K.; Sharma, V. Oxygen activation and energy conservation by cytochrome c oxidase. Chem. Rev. 2018, 118, 2469–2490. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Capitanio, N.; Palese, L.L.; Capitanio, G.; Martino, P.L.; Richter, O.M.; Ludwig, B.; Papa, S. Allosteric interactions and proton conducting pathways in proton pumping aa3 oxidases: Heme a as a key coupling element. Biochim. Biophys. Acta 2012, 1817, 558–566. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maneg, O.; Malatesta, F.; Ludwig, B.; Drosou, V. Interaction of cytochrome c with cytochrome oxidase: Two different docking scenarios. Biochim. Biophys. Acta 2004, 1655, 274–281. [Google Scholar] [CrossRef] [Green Version]
- Gavrikova, E.V.; Grivennikova, V.G.; Borisov, V.B.; Cecchini, G.; Vinogradov, A.D. Assembly of a chimeric respiratory chain from bovine heart submitochondrial particles and cytochrome bd terminal oxidase of Escherichia coli. FEBS Lett. 2009, 583, 1287–1291. [Google Scholar] [CrossRef] [Green Version]
- von Ballmoos, C.; Adelroth, P.; Gennis, R.B.; Brzezinski, P. Proton transfer in ba3 cytochrome c oxidase from Thermus thermophilus. Biochim. Biophys. Acta 2012, 1817, 650–657. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rich, P.R. Mitochondrial cytochrome c oxidase: Catalysis, coupling and controversies. Biochem. Soc. Trans. 2017, 45, 813–829. [Google Scholar] [CrossRef]
- Yoshikawa, S.; Shimada, A. Reaction mechanism of cytochrome c oxidase. Chem. Rev. 2015, 115, 1936–1989. [Google Scholar] [CrossRef]
- Forte, E.; Giuffre, A.; Huang, L.S.; Berry, E.A.; Borisov, V.B. Nitric oxide does not inhibit but is metabolized by the cytochrome bcc-aa3 supercomplex. Int. J. Mol. Sci. 2020, 21, 8521. [Google Scholar] [CrossRef] [PubMed]
- Siletsky, S.A.; Borisov, V.B. Proton pumping and non-pumping terminal respiratory oxidases: Active sites intermediates of these molecular machines and their derivatives. Int. J. Mol. Sci. 2021, 22, 10852. [Google Scholar] [CrossRef]
- Tsukihara, T.; Aoyama, H.; Yamashita, E.; Tomizaki, T.; Yamaguchi, H.; Shinzawa-Itoh, K.; Nakashima, R.; Yaono, R.; Yoshikawa, S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 1996, 272, 1136–1144. [Google Scholar] [CrossRef] [PubMed]
- Yano, N.; Muramoto, K.; Shimada, A.; Takemura, S.; Baba, J.; Fujisawa, H.; Mochizuki, M.; Shinzawa-Itoh, K.; Yamashita, E.; Tsukihara, T.; et al. The Mg2+-containing water cluster of mammalian cytochrome c oxidase collects four pumping proton equivalents in each catalytic cycle. J. Biol. Chem. 2016, 291, 23882–23894. [Google Scholar] [CrossRef] [Green Version]
- Shimada, A.; Etoh, Y.; Kitoh-Fujisawa, R.; Sasaki, A.; Shinzawa-Itoh, K.; Hiromoto, T.; Yamashita, E.; Muramoto, K.; Tsukihara, T.; Yoshikawa, S. X-ray structures of catalytic intermediates of cytochrome c oxidase provide insights into its O2 activation and unidirectional proton-pump mechanisms. J. Biol. Chem. 2020, 295, 5818–5833. [Google Scholar] [CrossRef] [Green Version]
- Shimada, A.; Hara, F.; Shinzawa-Itoh, K.; Kanehisa, N.; Yamashita, E.; Muramoto, K.; Tsukihara, T.; Yoshikawa, S. Critical roles of the CuB site in efficient proton pumping as revealed by crystal structures of mammalian cytochrome c oxidase catalytic intermediates. J. Biol. Chem. 2021, 297, 100967. [Google Scholar] [CrossRef]
- Antonini, E.; Brunori, M.; Colosimo, A.; Greenwood, C.; Wilson, M.T. Oxygen “pulsed” cytochrome c oxidase: Functional properties and catalytic relevance. Proc. Natl. Acad. Sci. USA 1977, 74, 3128–3132. [Google Scholar] [CrossRef] [Green Version]
- Moody, A.J. “As prepared” forms of fully oxidised haem/Cu terminal oxidases. Biochim. Biophys. Acta 1996, 1276, 6–20. [Google Scholar] [CrossRef] [Green Version]
- Moody, A.J.; Cooper, C.E.; Rich, P.R. Characterisation of ‘fast’ and ‘slow’ forms of bovine heart cytochrome-c oxidase. Biochim. Biophys. Acta 1991, 1059, 189–207. [Google Scholar] [CrossRef]
- Cooper, C.E.; Brown, G.C. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: Chemical mechanism and physiological significance. J. Bioenerg. Biomembr. 2008, 40, 533–539. [Google Scholar] [CrossRef] [PubMed]
- Khan, A.A.; Schuler, M.M.; Prior, M.G.; Yong, S.; Coppock, R.W.; Florence, L.Z.; Lillie, L.E. Effects of hydrogen sulfide exposure on lung mitochondrial respiratory chain enzymes in rats. Toxicol. Appl. Pharmacol. 1990, 103, 482–490. [Google Scholar] [CrossRef]
- Khan, A.A.; Yong, S.; Prior, M.G.; Lillie, L.E. Cytotoxic effects of hydrogen sulfide on pulmonary alveolar macrophages in rats. J. Toxicol. Environ. Health 1991, 33, 57–64. [Google Scholar] [CrossRef]
- Struve, M.F.; Brisbois, J.N.; James, R.A.; Marshall, M.W.; Dorman, D.C. Neurotoxicological effects associated with short-term exposure of Sprague-Dawley rats to hydrogen sulfide. Neurotoxicology 2001, 22, 375–385. [Google Scholar] [CrossRef]
- Dorman, D.C.; Moulin, F.J.; McManus, B.E.; Mahle, K.C.; James, R.A.; Struve, M.F. Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: Correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol. Sci. 2002, 65, 18–25. [Google Scholar] [CrossRef]
- Dorman, D.C.; Struve, M.F.; Gross, E.A.; Brenneman, K.A. Respiratory tract toxicity of inhaled hydrogen sulfide in Fischer-344 rats, Sprague-Dawley rats, and B6C3F1 mice following subchronic (90-day) exposure. Toxicol. Appl. Pharmacol. 2004, 198, 29–39. [Google Scholar] [CrossRef]
- Wu, N.; Du, X.; Wang, D.; Hao, F. Myocardial and lung injuries induced by hydrogen sulfide and the effectiveness of oxygen therapy in rats. Clin. Toxicol. 2011, 49, 161–166. [Google Scholar] [CrossRef]
- Thompson, R.W.; Valentine, H.L.; Valentine, W.M. Cytotoxic mechanisms of hydrosulfide anion and cyanide anion in primary rat hepatocyte cultures. Toxicology 2003, 188, 149–159. [Google Scholar] [CrossRef]
- Leschelle, X.; Goubern, M.; Andriamihaja, M.; Blottiere, H.M.; Couplan, E.; Gonzalez-Barroso, M.D.; Petit, C.; Pagniez, A.; Chaumontet, C.; Mignotte, B.; et al. Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide. Biochim. Biophys. Acta 2005, 1725, 201–212. [Google Scholar] [CrossRef]
- Truong, D.H.; Eghbal, M.A.; Hindmarsh, W.; Roth, S.H.; O’Brien, P.J. Molecular mechanisms of hydrogen sulfide toxicity. Drug Metab. Rev. 2006, 38, 733–744. [Google Scholar] [CrossRef]
- Sun, W.H.; Liu, F.; Chen, Y.; Zhu, Y.C. Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion. Biochem. Biophys. Res. Commun. 2012, 421, 164–169. [Google Scholar] [CrossRef] [PubMed]
- Groeger, M.; Matallo, J.; McCook, O.; Wagner, F.; Wachter, U.; Bastian, O.; Gierer, S.; Reich, V.; Stahl, B.; Huber-Lang, M.; et al. Temperature and cell-type dependency of sulfide effects on mitochondrial respiration. Shock 2012, 38, 367–374. [Google Scholar] [CrossRef] [PubMed]
- Buckler, K.J. Effects of exogenous hydrogen sulphide on calcium signalling, background (TASK) K channel activity and mitochondrial function in chemoreceptor cells. Pflugers Arch. 2012, 463, 743–754. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Meo, I.; Fagiolari, G.; Prelle, A.; Viscomi, C.; Zeviani, M.; Tiranti, V. Chronic exposure to sulfide causes accelerated degradation of cytochrome c oxidase in ethylmalonic encephalopathy. Antioxid. Redox Signal. 2011, 15, 353–362. [Google Scholar] [CrossRef] [PubMed]
- Nicholls, P.; Petersen, L.C.; Miller, M.; Hansen, F.B. Ligand-induced spectral changes in cytochrome c oxidase and their possible significance. Biochim. Biophys. Acta 1976, 449, 188–196. [Google Scholar] [CrossRef]
- Hill, B.C.; Woon, T.C.; Nicholls, P.; Peterson, J.; Greenwood, C.; Thomson, A.J. Interactions of sulphide and other ligands with cytochrome c oxidase. An electron-paramagnetic-resonance study. Biochem. J. 1984, 224, 591–600. [Google Scholar] [CrossRef]
- Furne, J.; Saeed, A.; Levitt, M.D. Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295, R1479–R1485. [Google Scholar] [CrossRef] [Green Version]
- Dordevic, D.; Jancikova, S.; Vitezova, M.; Kushkevych, I. Hydrogen sulfide toxicity in the gut environment: Meta-analysis of sulfate-reducing and lactic acid bacteria in inflammatory processes. J. Adv. Res. 2020, 27, 55–69. [Google Scholar] [CrossRef]
- Carbonero, F.; Benefiel, A.C.; Alizadeh-Ghamsari, A.H.; Gaskins, H.R. Microbial pathways in colonic sulfur metabolism and links with health and disease. Front. Physiol. 2012, 3, 448. [Google Scholar] [CrossRef] [Green Version]
- Forte, E.; Borisov, V.B.; Falabella, M.; Colaco, H.G.; Tinajero-Trejo, M.; Poole, R.K.; Vicente, J.B.; Sarti, P.; Giuffre, A. The terminal oxidase cytochrome bd promotes sulfide-resistant bacterial respiration and growth. Sci. Rep. 2016, 6, 23788. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Korshunov, S.; Imlay, K.R.; Imlay, J.A. The cytochrome bd oxidase of Escherichia coli prevents respiratory inhibition by endogenous and exogenous hydrogen sulfide. Mol. Microbiol. 2016, 101, 62–77. [Google Scholar] [CrossRef] [Green Version]
- Forte, E.; Giuffre, A. How bacteria breathe in hydrogen sulphide-rich environments. Biochemist 2016, 38, 8–11. [Google Scholar] [CrossRef]
- Borisov, V.B.; Forte, E. Terminal oxidase cytochrome bd protects bacteria against hydrogen sulfide toxicity. Biochemistry 2021, 86, 22–32. [Google Scholar] [CrossRef] [PubMed]
- Karami, N.; Nowrouzian, F.; Adlerberth, I.; Wold, A.E. Tetracycline resistance in Escherichia coli and persistence in the infantile colonic microbiota. Antimicrob. Agents Chemother. 2006, 50, 156–161. [Google Scholar] [CrossRef] [Green Version]
- Poole, R.K.; Cook, G.M. Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv. Microb. Physiol. 2000, 43, 165–224. [Google Scholar] [CrossRef]
- Ingledew, W.J.; Poole, R.K. The respiratory chains of Escherichia coli. Microbiol. Rev. 1984, 48, 222–271. [Google Scholar] [CrossRef]
- Azarkina, N.; Borisov, V.; Konstantinov, A.A. Spontaneous spectral changes of the reduced cytochrome bd. FEBS Lett. 1997, 416, 171–174. [Google Scholar] [CrossRef] [Green Version]
- Erhardt, H.; Dempwolff, F.; Pfreundschuh, M.; Riehle, M.; Schafer, C.; Pohl, T.; Graumann, P.; Friedrich, T. Organization of the Escherichia coli aerobic enzyme complexes of oxidative phosphorylation in dynamic domains within the cytoplasmic membrane. Microbiologyopen 2014, 3, 316–326. [Google Scholar] [CrossRef]
- Borisov, V.B.; Verkhovsky, M.I. Oxygen as Acceptor. EcoSal Plus 2015, 6. [Google Scholar] [CrossRef] [PubMed]
- Azarkina, N.; Siletsky, S.; Borisov, V.; von Wachenfeldt, C.; Hederstedt, L.; Konstantinov, A.A. A cytochrome bb′-type quinol oxidase in Bacillus subtilis strain 168. J. Biol. Chem. 1999, 274, 32810–32817. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Melin, F.; Sabuncu, S.; Choi, S.K.; Leprince, A.; Gennis, R.B.; Hellwig, P. Role of the tightly bound quinone for the oxygen reaction of cytochrome bo3 oxidase from Escherichia coli. FEBS Lett. 2018, 592, 3380–3387. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szundi, I.; Kittredge, C.; Choi, S.K.; McDonald, W.; Ray, J.; Gennis, R.B.; Einarsdottir, O. Kinetics and intermediates of the reaction of fully reduced Escherichia coli bo3 ubiquinol oxidase with O2. Biochemistry 2014, 53, 5393–5404. [Google Scholar] [CrossRef]
- Mogi, T.; Tsubaki, M.; Hori, H.; Miyoshi, H.; Nakamura, H.; Anraku, Y. Two terminal quinol oxidase families in Escherichia coli: Variations on molecular machinery for dioxygen reduction. J. Biochem. Mol. Biol. Biophys. 1998, 2, 79–110. [Google Scholar]
- Svensson Ek, M.; Brzezinski, P. Oxidation of ubiquinol by cytochrome bo3 from Escherichia coli: Kinetics of electron and proton transfer. Biochemistry 1997, 36, 5425–5431. [Google Scholar] [CrossRef]
- Yang, K.; Borisov, V.B.; Konstantinov, A.A.; Gennis, R.B. The fully oxidized form of the cytochrome bd quinol oxidase from E. coli does not participate in the catalytic cycle: Direct evidence from rapid kinetics studies. FEBS Lett. 2008, 582, 3705–3709. [Google Scholar] [CrossRef] [Green Version]
- Junemann, S. Cytochrome bd terminal oxidase. Biochim. Biophys. Acta 1997, 1321, 107–127. [Google Scholar] [CrossRef] [Green Version]
- Borisov, V.B.; Forte, E.; Sarti, P.; Giuffre, A. Catalytic intermediates of cytochrome bd terminal oxidase at steady-state: Ferryl and oxy-ferrous species dominate. Biochim. Biophys. Acta 2011, 1807, 503–509. [Google Scholar] [CrossRef]
- Li, M.; Jorgensen, S.K.; McMillan, D.G.; Krzeminski, L.; Daskalakis, N.N.; Partanen, R.H.; Tutkus, M.; Tuma, R.; Stamou, D.; Hatzakis, N.S.; et al. Single enzyme experiments reveal a long-lifetime proton leak state in a heme-copper oxidase. J. Am. Chem. Soc. 2015, 137, 16055–16063. [Google Scholar] [CrossRef]
- Asseri, A.H.; Godoy-Hernandez, A.; Goojani, H.G.; Lill, H.; Sakamoto, J.; McMillan, D.G.G.; Bald, D. Cardiolipin enhances the enzymatic activity of cytochrome bd and cytochrome bo3 solubilized in dodecyl-maltoside. Sci. Rep. 2021, 11, 8006. [Google Scholar] [CrossRef] [PubMed]
- Nikolaev, A.; Safarian, S.; Thesseling, A.; Wohlwend, D.; Friedrich, T.; Michel, H.; Kusumoto, T.; Sakamoto, J.; Melin, F.; Hellwig, P. Electrocatalytic evidence of the diversity of the oxygen reaction in the bacterial bd oxidase from different organisms. Biochim. Biophys. Acta Bioenerg. 2021, 1862, 148436. [Google Scholar] [CrossRef] [PubMed]
- Nakanishi-Matsui, M.; Sekiya, M.; Futai, M. ATP synthase from Escherichia coli: Mechanism of rotational catalysis, and inhibition with the epsilon subunit and phytopolyphenols. Biochim. Biophys. Acta 2016, 1857, 129–140. [Google Scholar] [CrossRef] [PubMed]
- Deckers-Hebestreit, G.; Greie, J.; Stalz, W.; Altendorf, K. The ATP synthase of Escherichia coli: Structure and function of F0 subunits. Biochim. Biophys. Acta 2000, 1458, 364–373. [Google Scholar] [CrossRef] [Green Version]
- Sobti, M.; Walshe, J.L.; Wu, D.; Ishmukhametov, R.; Zeng, Y.C.; Robinson, C.V.; Berry, R.M.; Stewart, A.G. Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch. Nat. Commun. 2020, 11, 2615. [Google Scholar] [CrossRef]
- Puustinen, A.; Finel, M.; Haltia, T.; Gennis, R.B.; Wikstrom, M. Properties of the two terminal oxidases of Escherichia coli. Biochemistry 1991, 30, 3936–3942. [Google Scholar] [CrossRef]
- Jasaitis, A.; Borisov, V.B.; Belevich, N.P.; Morgan, J.E.; Konstantinov, A.A.; Verkhovsky, M.I. Electrogenic reactions of cytochrome bd. Biochemistry 2000, 39, 13800–13809. [Google Scholar] [CrossRef]
- Belevich, I.; Borisov, V.B.; Zhang, J.; Yang, K.; Konstantinov, A.A.; Gennis, R.B.; Verkhovsky, M.I. Time-resolved electrometric and optical studies on cytochrome bd suggest a mechanism of electron-proton coupling in the di-heme active site. Proc. Natl. Acad. Sci. USA 2005, 102, 3657–3662. [Google Scholar] [CrossRef] [Green Version]
- Belevich, I.; Borisov, V.B.; Verkhovsky, M.I. Discovery of the true peroxy intermediate in the catalytic cycle of terminal oxidases by real-time measurement. J. Biol. Chem. 2007, 282, 28514–28519. [Google Scholar] [CrossRef] [Green Version]
- Borisov, V.B.; Belevich, I.; Bloch, D.A.; Mogi, T.; Verkhovsky, M.I. Glutamate 107 in subunit I of cytochrome bd from Escherichia coli is part of a transmembrane intraprotein pathway conducting protons from the cytoplasm to the heme b595/heme d active site. Biochemistry 2008, 47, 7907–7914. [Google Scholar] [CrossRef]
- Borisov, V.B.; Murali, R.; Verkhovskaya, M.L.; Bloch, D.A.; Han, H.; Gennis, R.B.; Verkhovsky, M.I. Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode. Proc. Natl. Acad. Sci. USA 2011, 108, 17320–17324. [Google Scholar] [CrossRef] [Green Version]
- Abramson, J.; Riistama, S.; Larsson, G.; Jasaitis, A.; Svensson-Ek, M.; Laakkonen, L.; Puustinen, A.; Iwata, S.; Wikstrom, M. The structure of the ubiquinol oxidase from Escherichia coli and its ubiquinone binding site. Nat. Struct. Biol. 2000, 7, 910–917. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Han, L.; Vallese, F.; Ding, Z.; Choi, S.K.; Hong, S.; Luo, Y.; Liu, B.; Chan, C.K.; Tajkhorshid, E.; et al. Cryo-EM structures of Escherichia coli cytochrome bo3 reveal bound phospholipids and ubiquinone-8 in a dynamic substrate binding site. Proc. Natl. Acad. Sci. USA 2021, 118, e2106750118. [Google Scholar] [CrossRef] [PubMed]
- Safarian, S.; Hahn, A.; Mills, D.J.; Radloff, M.; Eisinger, M.L.; Nikolaev, A.; Meier-Credo, J.; Melin, F.; Miyoshi, H.; Gennis, R.B.; et al. Active site rearrangement and structural divergence in prokaryotic respiratory oxidases. Science 2019, 366, 100–104. [Google Scholar] [CrossRef]
- Thesseling, A.; Rasmussen, T.; Burschel, S.; Wohlwend, D.; Kagi, J.; Muller, R.; Bottcher, B.; Friedrich, T. Homologous bd oxidases share the same architecture but differ in mechanism. Nat. Commun. 2019, 10, 5138. [Google Scholar] [CrossRef] [Green Version]
- Choi, S.K.; Schurig-Briccio, L.; Ding, Z.; Hong, S.; Sun, C.; Gennis, R.B. Location of the substrate binding site of the cytochrome bo3 ubiquinol oxidase from Escherichia coli. J. Am. Chem. Soc. 2017, 139, 8346–8354. [Google Scholar] [CrossRef] [PubMed]
- Borisov, V.B.; Gennis, R.B.; Hemp, J.; Verkhovsky, M.I. The cytochrome bd respiratory oxygen reductases. Biochim. Biophys. Acta 2011, 1807, 1398–1413. [Google Scholar] [CrossRef] [Green Version]
- Arutyunyan, A.M.; Sakamoto, J.; Inadome, M.; Kabashima, Y.; Borisov, V.B. Optical and magneto-optical activity of cytochrome bd from Geobacillus thermodenitrificans. Biochim. Biophys. Acta 2012, 1817, 2087–2094. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murali, R.; Gennis, R.B.; Hemp, J. Evolution of the cytochrome bd oxygen reductase superfamily and the function of CydAA’ in Archaea. ISME J. 2021. [Google Scholar] [CrossRef]
- Borisov, V.B. Cytochrome bd: Structure and properties. Biochemistry 1996, 61, 565–574. [Google Scholar]
- Forte, E.; Borisov, V.B.; Vicente, J.B.; Giuffre, A. Cytochrome bd and gaseous ligands in bacterial physiology. Adv. Microb. Physiol. 2017, 71, 171–234. [Google Scholar] [CrossRef] [PubMed]
- Borisov, V.B. Effect of membrane environment on ligand-binding properties of the terminal oxidase cytochrome bd-I from Escherichia coli. Biochemistry 2020, 85, 1603–1612. [Google Scholar] [CrossRef] [PubMed]
- Borisov, V.B.; Siletsky, S.A.; Paiardini, A.; Hoogewijs, D.; Forte, E.; Giuffre, A.; Poole, R.K. Bacterial oxidases of the cytochrome bd family: Redox enzymes of unique structure, function and utility as drug targets. Antioxid. Redox Signal. 2021, 34, 1280–1318. [Google Scholar] [CrossRef] [PubMed]
- Hill, J.J.; Alben, J.O.; Gennis, R.B. Spectroscopic evidence for a heme-heme binuclear center in the cytochrome bd ubiquinol oxidase from Escherichia coli. Proc. Natl. Acad. Sci. USA 1993, 90, 5863–5867. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsubaki, M.; Hori, H.; Mogi, T.; Anraku, Y. Cyanide-binding site of bd-type ubiquinol oxidase from Escherichia coli. J. Biol. Chem. 1995, 270, 28565–28569. [Google Scholar] [CrossRef] [Green Version]
- Borisov, V.; Arutyunyan, A.M.; Osborne, J.P.; Gennis, R.B.; Konstantinov, A.A. Magnetic circular dichroism used to examine the interaction of Escherichia coli cytochrome bd with ligands. Biochemistry 1999, 38, 740–750. [Google Scholar] [CrossRef]
- Vos, M.H.; Borisov, V.B.; Liebl, U.; Martin, J.L.; Konstantinov, A.A. Femtosecond resolution of ligand-heme interactions in the high-affinity quinol oxidase bd: A di-heme active site? Proc. Natl. Acad. Sci. USA 2000, 97, 1554–1559. [Google Scholar] [CrossRef] [Green Version]
- Borisov, V.B.; Sedelnikova, S.E.; Poole, R.K.; Konstantinov, A.A. Interaction of cytochrome bd with carbon monoxide at low and room temperatures: Evidence that only a small fraction of heme b595 reacts with CO. J. Biol. Chem. 2001, 276, 22095–22099. [Google Scholar] [CrossRef] [Green Version]
- Borisov, V.B.; Liebl, U.; Rappaport, F.; Martin, J.L.; Zhang, J.; Gennis, R.B.; Konstantinov, A.A.; Vos, M.H. Interactions between heme d and heme b595 in quinol oxidase bd from Escherichia coli: A photoselection study using femtosecond spectroscopy. Biochemistry 2002, 41, 1654–1662. [Google Scholar] [CrossRef] [Green Version]
- Arutyunyan, A.M.; Borisov, V.B.; Novoderezhkin, V.I.; Ghaim, J.; Zhang, J.; Gennis, R.B.; Konstantinov, A.A. Strong excitonic interactions in the oxygen-reducing site of bd-type oxidase: The Fe-to-Fe distance between hemes d and b595 is 10 A. Biochemistry 2008, 47, 1752–1759. [Google Scholar] [CrossRef]
- Borisov, V.B. Interaction of bd-type quinol oxidase from Escherichia coli and carbon monoxide: Heme d binds CO with high affinity. Biochemistry 2008, 73, 14–22. [Google Scholar] [CrossRef] [PubMed]
- Bloch, D.A.; Borisov, V.B.; Mogi, T.; Verkhovsky, M.I. Heme/heme redox interaction and resolution of individual optical absorption spectra of the hemes in cytochrome bd from Escherichia coli. Biochim. Biophys. Acta 2009, 1787, 1246–1253. [Google Scholar] [CrossRef] [Green Version]
- Rappaport, F.; Zhang, J.; Vos, M.H.; Gennis, R.B.; Borisov, V.B. Heme-heme and heme-ligand interactions in the di-heme oxygen-reducing site of cytochrome bd from Escherichia coli revealed by nanosecond absorption spectroscopy. Biochim. Biophys. Acta 2010, 1797, 1657–1664. [Google Scholar] [CrossRef] [PubMed]
- Borisov, V.B.; Verkhovsky, M.I. Accommodation of CO in the di-heme active site of cytochrome bd terminal oxidase from Escherichia coli. J. Inorg. Biochem. 2013, 118, 65–67. [Google Scholar] [CrossRef] [PubMed]
- Siletsky, S.A.; Zaspa, A.A.; Poole, R.K.; Borisov, V.B. Microsecond time-resolved absorption spectroscopy used to study CO compounds of cytochrome bd from Escherichia coli. PLoS ONE 2014, 9, e95617. [Google Scholar] [CrossRef]
- Siletsky, S.A.; Rappaport, F.; Poole, R.K.; Borisov, V.B. Evidence for fast electron transfer between the high-spin haems in cytochrome bd-I from Escherichia coli. PLoS ONE 2016, 11, e0155186. [Google Scholar] [CrossRef]
- Siletsky, S.A.; Dyuba, A.V.; Elkina, D.A.; Monakhova, M.V.; Borisov, V.B. Spectral-kinetic analysis of recombination reaction of heme centers of bd-type quinol oxidase from Escherichia coli with carbon monoxide. Biochemistry 2017, 82, 1354–1366. [Google Scholar] [CrossRef]
- Svensson, M.; Nilsson, T. Flow-flash study of the reaction between cytochrome bo and oxygen. Biochemistry 1993, 32, 5442–5447. [Google Scholar] [CrossRef]
- Borisov, V.B.; Smirnova, I.A.; Krasnosel’skaya, I.A.; Konstantinov, A.A. Oxygenated cytochrome bd from Escherichia coli can be converted into the oxidized form by lipophilic electron acceptors. Biochemistry 1994, 59, 437–443. [Google Scholar]
- D’Mello, R.; Hill, S.; Poole, R.K. The oxygen affinity of cytochrome bo′ in Escherichia coli determined by the deoxygenation of oxyleghemoglobin and oxymyoglobin: Km values for oxygen are in the submicromolar range. J. Bacteriol. 1995, 177, 867–870. [Google Scholar] [CrossRef] [Green Version]
- D’mello, R.; Hill, S.; Poole, R.K. The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two-oxygen-binding haems: Implicaitons for regulation of activity in vivo by oxygen inihibition. Microbiology 1996, 142, 755–763. [Google Scholar] [CrossRef] [Green Version]
- Belevich, I.; Borisov, V.B.; Konstantinov, A.A.; Verkhovsky, M.I. Oxygenated complex of cytochrome bd from Escherichia coli: Stability and photolability. FEBS Lett. 2005, 579, 4567–4570. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Belevich, I.; Borisov, V.B.; Bloch, D.A.; Konstantinov, A.A.; Verkhovsky, M.I. Cytochrome bd from Azotobacter vinelandii: Evidence for high-affinity oxygen binding. Biochemistry 2007, 46, 11177–11184. [Google Scholar] [CrossRef]
- Cotter, P.A.; Chepuri, V.; Gennis, R.B.; Gunsalus, R.P. Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J. Bacteriol. 1990, 172, 6333–6338. [Google Scholar] [CrossRef] [Green Version]
- Alexeeva, S.; Hellingwerf, K.; Teixeira de Mattos, M.J. Quantitative assessment of oxygen availability: Perceived aerobiosis and its effect on flux distribution in the respiratory chain of Escherichia coli. J. Bacteriol. 2002, 184, 1402–1406. [Google Scholar] [CrossRef] [Green Version]
- Rolfe, M.D.; Ter Beek, A.; Graham, A.I.; Trotter, E.W.; Asif, H.M.; Sanguinetti, G.; de Mattos, J.T.; Poole, R.K.; Green, J. Transcript profiling and inference of Escherichia coli K-12 ArcA activity across the range of physiologically relevant oxygen concentrations. J. Biol. Chem. 2011, 286, 10147–10154. [Google Scholar] [CrossRef] [Green Version]
- Ederer, M.; Steinsiek, S.; Stagge, S.; Rolfe, M.D.; Ter Beek, A.; Knies, D.; Teixeira de Mattos, M.J.; Sauter, T.; Green, J.; Poole, R.K.; et al. A mathematical model of metabolism and regulation provides a systems-level view of how Escherichia coli responds to oxygen. Front. Microbiol. 2014, 5, 124. [Google Scholar] [CrossRef] [PubMed]
- Bettenbrock, K.; Bai, H.; Ederer, M.; Green, J.; Hellingwerf, K.J.; Holcombe, M.; Kunz, S.; Rolfe, M.D.; Sanguinetti, G.; Sawodny, O.; et al. Towards a systems level understanding of the oxygen response of Escherichia coli. Adv. Microb. Physiol. 2014, 64, 65–114. [Google Scholar] [CrossRef] [PubMed]
- Forte, E.; Borisov, V.B.; Konstantinov, A.A.; Brunori, M.; Giuffre, A.; Sarti, P. Cytochrome bd, a key oxidase in bacterial survival and tolerance to nitrosative stress. Ital. J. Biochem. 2007, 56, 265–269. [Google Scholar]
- Borisov, V.B.; Forte, E.; Siletsky, S.A.; Arese, M.; Davletshin, A.I.; Sarti, P.; Giuffre, A. Cytochrome bd protects bacteria against oxidative and nitrosative stress: A potential target for next-generation antimicrobial agents. Biochemistry 2015, 80, 565–575. [Google Scholar] [CrossRef]
- Giuffre, A.; Borisov, V.B.; Mastronicola, D.; Sarti, P.; Forte, E. Cytochrome bd oxidase and nitric oxide: From reaction mechanisms to bacterial physiology. FEBS Lett. 2012, 586, 622–629. [Google Scholar] [CrossRef] [PubMed]
- Giuffre, A.; Borisov, V.B.; Arese, M.; Sarti, P.; Forte, E. Cytochrome bd oxidase and bacterial tolerance to oxidative and nitrosative stress. Biochim. Biophys. Acta 2014, 1837, 1178–1187. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Forte, E.; Borisov, V.B.; Siletsky, S.A.; Petrosino, M.; Giuffre, A. In the respiratory chain of Escherichia coli cytochromes bd-I and bd-II are more sensitive to carbon monoxide inhibition than cytochrome bo3. Biochim. Biophys. Acta Bioenerg. 2019, 1860, 148088. [Google Scholar] [CrossRef]
- Borisov, V.B.; Forte, E.; Konstantinov, A.A.; Poole, R.K.; Sarti, P.; Giuffre, A. Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide. FEBS Lett. 2004, 576, 201–204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Borisov, V.B.; Forte, E.; Sarti, P.; Brunori, M.; Konstantinov, A.A.; Giuffre, A. Nitric oxide reacts with the ferryl-oxo catalytic intermediate of the CuB-lacking cytochrome bd terminal oxidase. FEBS Lett. 2006, 580, 4823–4826. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Borisov, V.B.; Forte, E.; Sarti, P.; Brunori, M.; Konstantinov, A.A.; Giuffre, A. Redox control of fast ligand dissociation from Escherichia coli cytochrome bd. Biochem. Biophys. Res. Commun. 2007, 355, 97–102. [Google Scholar] [CrossRef]
- Mason, M.G.; Shepherd, M.; Nicholls, P.; Dobbin, P.S.; Dodsworth, K.S.; Poole, R.K.; Cooper, C.E. Cytochrome bd confers nitric oxide resistance to Escherichia coli. Nat. Chem. Biol. 2009, 5, 94–96. [Google Scholar] [CrossRef] [PubMed]
- Borisov, V.B.; Forte, E.; Giuffre, A.; Konstantinov, A.; Sarti, P. Reaction of nitric oxide with the oxidized di-heme and heme-copper oxygen-reducing centers of terminal oxidases: Different reaction pathways and end-products. J. Inorg. Biochem. 2009, 103, 1185–1187. [Google Scholar] [CrossRef]
- Shepherd, M.; Achard, M.E.; Idris, A.; Totsika, M.; Phan, M.D.; Peters, K.M.; Sarkar, S.; Ribeiro, C.A.; Holyoake, L.V.; Ladakis, D.; et al. The cytochrome bd-I respiratory oxidase augments survival of multidrug-resistant Escherichia coli during infection. Sci. Rep. 2016, 6, 35285. [Google Scholar] [CrossRef]
- Holyoake, L.V.; Hunt, S.; Sanguinetti, G.; Cook, G.M.; Howard, M.J.; Rowe, M.L.; Poole, R.K.; Shepherd, M. CydDC-mediated reductant export in Escherichia coli controls the transcriptional wiring of energy metabolism and combats nitrosative stress. Biochem. J. 2016, 473, 693–701. [Google Scholar] [CrossRef] [Green Version]
- Jones-Carson, J.; Husain, M.; Liu, L.; Orlicky, D.J.; Vazquez-Torres, A. Cytochrome bd-dependent bioenergetics and antinitrosative defenses in Salmonella pathogenesis. mBio 2016, 7, e02052-16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meng, Q.; Yin, J.; Jin, M.; Gao, H. Distinct nitrite and nitric oxide physiologies in Escherichia coli and Shewanella oneidensis. Appl. Environ. Microbiol. 2018, 84, e00559-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beebout, C.J.; Eberly, A.R.; Werby, S.H.; Reasoner, S.A.; Brannon, J.R.; De, S.; Fitzgerald, M.J.; Huggins, M.M.; Clayton, D.B.; Cegelski, L.; et al. Respiratory heterogeneity shapes biofilm formation and host colonization in uropathogenic Escherichia coli. mBio 2019, 10, e02400-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Borisov, V.B.; Forte, E.; Siletsky, S.A.; Sarti, P.; Giuffre, A. Cytochrome bd from Escherichia coli catalyzes peroxynitrite decomposition. Biochim. Biophys. Acta 2015, 1847, 182–188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Borisov, V.; Gennis, R.; Konstantinov, A.A. Peroxide complex of cytochrome bd: Kinetics of generation and stability. Biochem. Mol. Biol. Int. 1995, 37, 975–982. [Google Scholar]
- Borisov, V.B.; Gennis, R.B.; Konstantinov, A.A. Interaction of cytochrome bd from Escherichia coli with hydrogen peroxide. Biochemistry 1995, 60, 231–239. [Google Scholar]
- Borisov, V.B.; Davletshin, A.I.; Konstantinov, A.A. Peroxidase activity of cytochrome bd from Escherichia coli. Biochemistry 2010, 75, 428–436. [Google Scholar] [CrossRef]
- Borisov, V.B.; Forte, E.; Davletshin, A.; Mastronicola, D.; Sarti, P.; Giuffre, A. Cytochrome bd oxidase from Escherichia coli displays high catalase activity: An additional defense against oxidative stress. FEBS Lett. 2013, 587, 2214–2218. [Google Scholar] [CrossRef]
- Forte, E.; Borisov, V.B.; Davletshin, A.; Mastronicola, D.; Sarti, P.; Giuffre, A. Cytochrome bd oxidase and hydrogen peroxide resistance in Mycobacterium tuberculosis. mBio 2013, 4, e01006-13. [Google Scholar] [CrossRef] [Green Version]
- Al-Attar, S.; Yu, Y.; Pinkse, M.; Hoeser, J.; Friedrich, T.; Bald, D.; de Vries, S. Cytochrome bd displays significant quinol peroxidase activity. Sci. Rep. 2016, 6, 27631. [Google Scholar] [CrossRef] [Green Version]
- Kita, K.; Konishi, K.; Anraku, Y. Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. J. Biol. Chem. 1984, 259, 3375–3381. [Google Scholar] [CrossRef]
- Sakamoto, J.; Koga, E.; Mizuta, T.; Sato, C.; Noguchi, S.; Sone, N. Gene structure and quinol oxidase activity of a cytochrome bd-type oxidase from Bacillus stearothermophilus. Biochim. Biophys. Acta 1999, 1411, 147–158. [Google Scholar] [CrossRef] [Green Version]
- Forte, E.; Siletsky, S.A.; Borisov, V.B. In Escherichia coli ammonia inhibits cytochrome bo3 but activates cytochrome bd-I. Antioxidants 2021, 10, 13. [Google Scholar] [CrossRef] [PubMed]
- Mascolo, L.; Bald, D. Cytochrome bd in Mycobacterium tuberculosis: A respiratory chain protein involved in the defense against antibacterials. Prog. Biophys. Mol. Biol. 2020, 152, 55–63. [Google Scholar] [CrossRef] [PubMed]
- Lee, B.S.; Sviriaeva, E.; Pethe, K. Targeting the cytochrome oxidases for drug development in mycobacteria. Prog. Biophys. Mol. Biol. 2020, 152, 45–54. [Google Scholar] [CrossRef]
- Cook, G.M.; Hards, K.; Dunn, E.; Heikal, A.; Nakatani, Y.; Greening, C.; Crick, D.C.; Fontes, F.L.; Pethe, K.; Hasenoehrl, E.; et al. Oxidative phosphorylation as a target space for tuberculosis: Success, caution, and future directions. Microbiol. Spectr. 2017, 5. [Google Scholar] [CrossRef] [Green Version]
- Bald, D.; Villellas, C.; Lu, P.; Koul, A. Targeting energy metabolism in Mycobacterium tuberculosis, a new paradigm in antimycobacterial drug discovery. mBio 2017, 8, e00272-17. [Google Scholar] [CrossRef] [Green Version]
- Hards, K.; Cook, G.M. Targeting bacterial energetics to produce new antimicrobials. Drug Resist. Updat. 2018, 36, 1–12. [Google Scholar] [CrossRef]
- Winstedt, L.; Frankenberg, L.; Hederstedt, L.; von Wachenfeldt, C. Enterococcus faecalis V583 contains a cytochrome bd-type respiratory oxidase. J. Bacteriol. 2000, 182, 3863–3866. [Google Scholar] [CrossRef] [Green Version]
- Lee, B.S.; Hards, K.; Engelhart, C.A.; Hasenoehrl, E.J.; Kalia, N.P.; Mackenzie, J.S.; Sviriaeva, E.; Chong, S.M.S.; Manimekalai, M.S.S.; Koh, V.H.; et al. Dual inhibition of the terminal oxidases eradicates antibiotic-tolerant Mycobacterium tuberculosis. EMBO Mol. Med. 2021, 13, e13207. [Google Scholar] [CrossRef]
- Saini, V.; Chinta, K.C.; Reddy, V.P.; Glasgow, J.N.; Stein, A.; Lamprecht, D.A.; Rahman, M.A.; Mackenzie, J.S.; Truebody, B.E.; Adamson, J.H.; et al. Hydrogen sulfide stimulates Mycobacterium tuberculosis respiration, growth and pathogenesis. Nat. Commun. 2020, 11, 557. [Google Scholar] [CrossRef] [PubMed]
- Kunota, T.T.R.; Rahman, M.A.; Truebody, B.E.; Mackenzie, J.S.; Saini, V.; Lamprecht, D.A.; Adamson, J.H.; Sevalkar, R.R.; Lancaster, J.R., Jr.; Berney, M.; et al. Mycobacterium tuberculosis H2S functions as a sink to modulate central metabolism, bioenergetics, and drug susceptibility. Antioxidants 2021, 10, 1285. [Google Scholar] [CrossRef] [PubMed]
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Borisov, V.B.; Forte, E. Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics. Int. J. Mol. Sci. 2021, 22, 12688. https://doi.org/10.3390/ijms222312688
Borisov VB, Forte E. Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics. International Journal of Molecular Sciences. 2021; 22(23):12688. https://doi.org/10.3390/ijms222312688
Chicago/Turabian StyleBorisov, Vitaliy B., and Elena Forte. 2021. "Impact of Hydrogen Sulfide on Mitochondrial and Bacterial Bioenergetics" International Journal of Molecular Sciences 22, no. 23: 12688. https://doi.org/10.3390/ijms222312688