Complex Interplay of Heme-Copper Oxidases with Nitrite and Nitric Oxide
<p>Redox cycle for nitrogen driven by prokaryotes. Shown are the major biological nitrogen transformation pathways, each of which are represented by lines in the same color, and the relative oxidation state at which they occur.</p> "> Figure 2
<p>Prosthetic group arrangements and proton pathways of typical bacterial HCOs (<b>A</b>) and bd QOs (<b>B</b>). (<b>A</b>) Representative structures of HCOs of A (divided into A1 and A2), B, and C subfamilies. Protein peptides, heme cofactors, and ions are shown as cartoons, sticks, and spheres, respectively. SUs I of families A and B, SU III of family A and CcoN of family C are colored in green; SUs II of families A and B, and CcoO of family C are colored in cyan; SU IV of family A, SU Iia of family B, and CcoO of family C are colored in magenta; the 30-mer peptide in family C HCO is colored in yellow. The blue dashed arrows indicate the proton pathways inside each HCO, with the amino acid residues at the entry point of each pathway marked with dashed cycles. (<b>B</b>) Structures of Cyt bd-I and bd-II QOs. Protein peptides and heme cofactors are shown as cartoons and sticks with subunits CydA and CydB colored in green and cyan, and CydX in bd-I QOs and CydS in bd-II QOs colored in magenta, respectively. The purple dashed arrow indicates the ‘water-molecule chain’ observed between residues Asp119 (subunit A) and Asp58 (subunit B) in bd-I QOs. The blue dashed arrows indicate two proposed proton pathways in bd-II QOs. Figures are prepared with PyMOL (Molecular Graphics System, LLC) <a href="https://www.pymol.org" target="_blank">https://www.pymol.org</a> (accessed on 20 December 2021).</p> "> Figure 3
<p>The catalytic cycle of HCO and the interplay with NO through the two pathways. The catalytic cycle of HCO is schematically reported with the indication of the redox and the oxygen ligation state of the BNC (heme a3-CuB active site). In the reductive phase, the oxidized species O is fully reduced to R by two single-electron donations via formation of the half-reduced intermediate E. In the oxidative phase, upon reaction with O<sub>2</sub>, R converts to P and F, and O is regenerated eventually through further electron transfer. The nitrite-bound derivative (Fe<sup>3+</sup> CuB<sup>2+</sup> NO<sub>2</sub><sup>−</sup>) and the nitrosylated adduct (Fe<sup>2+</sup> CuB<sup>+</sup> NO) are generated by the reactions of these intermediates with NO. Tyr, CuB-interacting residue Y244, with an asterisk representing the radical form.</p> "> Figure 4
<p>Scheme of a heme-copper assembly mediated oxidation of NO to nitrite and structures of ligand-absent and NO-binding BNCs of CcOs. (<b>A</b>) A μ-oxo heme-FeIII-O-CuII complex facilitates NO oxidation to nitrite, forming reduced heme and CuII-nitrito complexes. This scheme is modified from the figure in reference [<a href="#B26-ijms-23-00979" class="html-bibr">26</a>] with ChemDraw. (<b>B</b>) Spatial structure of the BNC of Cyt caa3 oxidase from <span class="html-italic">T. thermophilus</span> HB8. The copper atom (CuB) is coordinated by three histidine residues. The distance between CuB and heme-iron is less than 5 Å. (<b>C</b>) X-ray structure of the NO-bound CcO from bovine CcO. The distances between CuB and oxygen atom from NO, heme-Fe, and nitrogen atom from NO are 2.5 Å and 1.8 Å, respectively. Figures of B and C are prepared with PyMOL (Molecular Graphics System, LLC) <a href="https://www.pymol.org" target="_blank">https://www.pymol.org</a> (accessed on 20 December 2021).</p> "> Figure 5
<p>Bacterial targets of NO and nitrite revealed by in vivo analyses. Shown is the scenario that bacteria are confronted with NO from exogenous sources. The proteins sensitive to NO primarily include: (i) Fe-S containing dehydratases such as LpdA, IIvD, and AcnB that can form DNIC with NO; (ii) hemoproteins such as cyts c, HCOs, and cyt bd quinol oxidase that can form Fe<sup>2+</sup>-NO complex. Unlike NO, the targets of nitrite are more specific. HCOs are the most crucial targets of nitrite. Besides, housekeeping aconitase AcnB rapidly loses activity upon nitrite exposure. Dashline arrow for the transport of nitrite represents that the molecules, unlike NO, could not diffuse into the cytoplasm easily. OM and IM represent outer- and inner-membrane of Gram-negative bacteria, respectively. Solid and dash line arrows represent crossing the membranes freely and in a transporter-dependent manner respectively.</p> ">
Abstract
:1. Introduction
2. Bacterial Terminal Oxidases for pmf Generation
2.1. HCOs
2.2. bd QO
3. Roles of HCOs in the Transformation of Nitrogen Oxides
4. Inhibition of HCOs by Nitrite and NO
5. HCOs Are Primary Targets of Nitrite but Not NO In Vivo
6. Concluding Remarks
Funding
Conflicts of Interest
References
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Chen, J.; Xie, P.; Huang, Y.; Gao, H. Complex Interplay of Heme-Copper Oxidases with Nitrite and Nitric Oxide. Int. J. Mol. Sci. 2022, 23, 979. https://doi.org/10.3390/ijms23020979
Chen J, Xie P, Huang Y, Gao H. Complex Interplay of Heme-Copper Oxidases with Nitrite and Nitric Oxide. International Journal of Molecular Sciences. 2022; 23(2):979. https://doi.org/10.3390/ijms23020979
Chicago/Turabian StyleChen, Jinghua, Peilu Xie, Yujia Huang, and Haichun Gao. 2022. "Complex Interplay of Heme-Copper Oxidases with Nitrite and Nitric Oxide" International Journal of Molecular Sciences 23, no. 2: 979. https://doi.org/10.3390/ijms23020979