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Alternate substrate binding modes to two mutant (D98N and H255N) forms of nitrite reductase from Alcaligenes faecalis S-6: structural model of a transient catalytic intermediate.

Boulanger MJ, Murphy ME
Biochemistry 40 9132-41 (2001)
Related entries: 1j9q, 1j9s, 1j9t

Cited: 25 times
EuropePMC logo PMID: 11478880

Abstract

High-resolution nitrite soaked oxidized and reduced crystal structures of two active site mutants, D98N and H255N, of nitrite reductase (NIR) from Alcaligenes faecalis S-6 were determined to better than 2.0 A resolution. In the oxidized D98N nitrite-soaked structures, nitrite is coordinated to the type II copper via its oxygen atoms in an asymmetric bidentate manner; however, elevated B-factors and weak electron density indicate that both nitrite and Asn98 are less ordered than in the native enzyme. This disorder likely results from the inability of the N delta 2 atom of Asn98 to form a hydrogen bond with the bound protonated nitrite, indicating that the hydrogen bond between Asp98 and nitrite in the native NIR structure is essential in anchoring nitrite in the active site for catalysis. In the oxidized nitrite soaked H255N crystal structure, nitrite does not displace the ligand water and is instead coordinated in an alternative mode via a single oxygen to the type II copper. His255 is clearly essential in defining the nitrite binding site despite the lack of direct interaction with the substrate in the native enzyme. The resulting pentacoordinate copper site in the H255N structure also serves as a model for a proposed transient intermediate in the catalytic mechanism consisting of a hydroxyl and nitric oxide molecule coordinated to the copper. The formation of an unusual dinuclear type I copper site in the reduced nitrite soaked D98N and H255N crystal structures may represent an evolutionary link between the mononuclear type I copper centers and dinuclear Cu(A) sites.

Reviews citing this publication (4)

  1. Copper active sites in biology. Solomon EI, Heppner DE, Johnston EM, Ginsbach JW, Cirera J, Qayyum M, Kieber-Emmons MT, Kjaergaard CH, Hadt RG, Tian L. Chem Rev 114 3659-3853 (2014)
  2. Binding and activation of nitrite and nitric oxide by copper nitrite reductase and corresponding model complexes. Merkle AC, Lehnert N. Dalton Trans 41 3355-3368 (2012)
  3. Recent structural insights into the function of copper nitrite reductases. Horrell S, Kekilli D, Strange RW, Hough MA. Metallomics 9 1470-1482 (2017)
  4. Serial femtosecond crystallography at the SACLA: breakthrough to dynamic structural biology. Mizohata E, Nakane T, Fukuda Y, Nango E, Iwata S. Biophys Rev 10 209-218 (2018)

Articles citing this publication (21)

  1. Atomic resolution structures of resting-state, substrate- and product-complexed Cu-nitrite reductase provide insight into catalytic mechanism. Antonyuk SV, Strange RW, Sawers G, Eady RR, Hasnain SS. Proc Natl Acad Sci U S A 102 12041-12046 (2005)
  2. Crystal structure of the soluble domain of the major anaerobically induced outer membrane protein (AniA) from pathogenic Neisseria: a new class of copper-containing nitrite reductases. Boulanger MJ, Murphy ME. J Mol Biol 315 1111-1127 (2002)
  3. Redox-coupled proton transfer mechanism in nitrite reductase revealed by femtosecond crystallography. Fukuda Y, Tse KM, Nakane T, Nakatsu T, Suzuki M, Sugahara M, Inoue S, Masuda T, Yumoto F, Matsugaki N, Nango E, Tono K, Joti Y, Kameshima T, Song C, Hatsui T, Yabashi M, Nureki O, Murphy ME, Inoue T, Iwata S, Mizohata E. Proc Natl Acad Sci U S A 113 2928-2933 (2016)
  4. Atomic resolution structures of native copper nitrite reductase from Alcaligenes xylosoxidans and the active site mutant Asp92Glu. Ellis MJ, Dodd FE, Sawers G, Eady RR, Hasnain SS. J Mol Biol 328 429-438 (2003)
  5. A survey of left-handed helices in protein structures. Novotny M, Kleywegt GJ. J Mol Biol 347 231-241 (2005)
  6. Directing the mode of nitrite binding to a copper-containing nitrite reductase from Alcaligenes faecalis S-6: characterization of an active site isoleucine. Boulanger MJ, Murphy ME. Protein Sci 12 248-256 (2003)
  7. Directed evolution of copper nitrite reductase to a chromogenic reductant. MacPherson IS, Rosell FI, Scofield M, Mauk AG, Murphy ME. Protein Eng Des Sel 23 137-145 (2010)
  8. Enzyme catalysis captured using multiple structures from one crystal at varying temperatures. Horrell S, Kekilli D, Sen K, Owen RL, Dworkowski FSN, Antonyuk SV, Keal TW, Yong CW, Eady RR, Hasnain SS, Strange RW, Hough MA. IUCrJ 5 283-292 (2018)
  9. Structural insights into the function of a thermostable copper-containing nitrite reductase. Fukuda Y, Tse KM, Lintuluoto M, Fukunishi Y, Mizohata E, Matsumura H, Takami H, Nojiri M, Inoue T. J Biochem 155 123-135 (2014)
  10. Sensing nitrite through a pseudoazurin-nitrite reductase electron transfer relay. Astier Y, Canters GW, Davis JJ, Hill HA, Verbeet MP, Wijma HJ. Chemphyschem 6 1114-1120 (2005)
  11. Elucidating the mechanism for the reduction of nitrite by copper nitrite reductase--a contribution from quantum chemical studies. De Marothy SA, Blomberg MR, Siegbahn PE. J Comput Chem 28 528-539 (2007)
  12. Comparative analysis of amino acid composition in the active site of nirk gene encoding copper-containing nitrite reductase (CuNiR) in bacterial spp. Adhikari UK, Rahman MM. Comput Biol Chem 67 102-113 (2017)
  13. The binding of nitric oxide at the Cu(i) site of copper nitrite reductase and of inorganic models: DFT calculations of the energetics and EPR parameters of side-on and end-on structures. Periyasamy G, Sundararajan M, Hillier IH, Burton NA, McDouall JJ. Phys Chem Chem Phys 9 2498-2506 (2007)
  14. A rearranging ligand enables allosteric control of catalytic activity in copper-containing nitrite reductase. Wijma HJ, Macpherson I, Alexandre M, Diederix RE, Canters GW, Murphy ME, Verbeet MP. J Mol Biol 358 1081-1093 (2006)
  15. Intra-electron transfer induced by protonation in copper-containing nitrite reductase. Lintuluoto M, Lintuluoto JM. Metallomics 10 565-578 (2018)
  16. Copper-Containing Nitrite Reductase Employing Proton-Coupled Spin-Exchanged Electron-Transfer and Multiproton Synchronized Transfer to Reduce Nitrite. Qin X, Deng L, Hu C, Li L, Chen X. Chemistry 23 14900-14910 (2017)
  17. Crystal structure of C-terminal desundecapeptide nitrite reductase from Achromobacter cycloclastes. Li HT, Chang T, Chang WC, Chen CJ, Liu MY, Gui LL, Zhang JP, An XM, Chang WR. Biochem Biophys Res Commun 338 1935-1942 (2005)
  18. pH-profile crystal structure studies of C-terminal despentapeptide nitrite reductase from Achromobacter cycloclastes. Li HT, Wang C, Chang T, Chang WC, Liu MY, Le Gall J, Gui LL, Zhang JP, An XM, Chang WR. Biochem Biophys Res Commun 316 107-113 (2004)
  19. Crystal structure of a NO-forming nitrite reductase mutant: an analog of a transition state in enzymatic reaction. Liu SQ, Chang T, Liu MY, LeGall J, Chang WC, Zhang JP, Liang DC, Chang WR. Biochem Biophys Res Commun 302 568-574 (2003)
  20. Crystallographic study of dioxygen chemistry in a copper-containing nitrite reductase from Geobacillus thermodenitrificans. Fukuda Y, Matsusaki T, Tse KM, Mizohata E, Murphy MEP, Inoue T. Acta Crystallogr D Struct Biol 74 769-777 (2018)
  21. Quantitative elemental imaging in eukaryotic algae. Schmollinger S, Chen S, Merchant SS. Metallomics 15 mfad025 (2023)


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