1et5 › Citations

Catalytic roles for two water bridged residues (Asp-98 and His-255) in the active site of copper-containing nitrite reductase.

Boulanger MJ, Kukimoto M, Nishiyama M, Horinouchi S, Murphy ME
J Biol Chem 275 23957-64 (2000)
Related entries: 1et7, 1et8

Cited: 57 times
EuropePMC logo PMID: 10811642

Abstract

Two active site residues, Asp-98 and His-255, of copper-containing nitrite reductase (NIR) from Alcaligenes faecalis have been mutated to probe the catalytic mechanism. Three mutations at these two sites (D98N, H255D, and H255N) result in large reductions in activity relative to native NIR, suggesting that both residues are involved intimately in the reaction mechanism. Crystal structures of these mutants have been determined using data collected to better than 1. 9-A resolution. In the native structure, His-255 Nepsilon2 forms a hydrogen bond through a bridging water molecule to the side chain of Asp-98, which also forms a hydrogen bond to a water or nitrite oxygen ligated to the active site copper. In the D98N mutant, reorientation of the Asn-98 side chain results in the loss of the hydrogen bond to the copper ligand water, consistent with a negatively charged Asp-98 directing the binding and protonation of nitrite in the native enzyme. An additional solvent molecule is situated between residues 255 and the bridging water in the H255N and H255D mutants and likely inhibits nitrite binding. The interaction of His-255 with the bridging water appears to be necessary for catalysis and may donate a proton to reaction intermediates in addition to Asp-98.

Articles - 1et5 mentioned but not cited (1)

  1. BION-2: Predicting Positions of Non-Specifically Bound Ions on Protein Surface by a Gaussian-Based Treatment of Electrostatics. Shashikala HBM, Chakravorty A, Panday SK, Alexov E. Int J Mol Sci 22 E272 (2020)


Reviews citing this publication (6)

  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. Catalysis and Electron Transfer in De Novo Designed Helical Scaffolds. Pinter TBJ, Koebke KJ, Pecoraro VL. Angew Chem Int Ed Engl 59 7678-7699 (2020)
  3. Catalysis and Electron Transfer in De Novo Designed Metalloproteins. Koebke KJ, Pinter TBJ, Pitts WC, Pecoraro VL. Chem Rev 122 12046-12109 (2022)
  4. Metalloprotein catalysis: structural and mechanistic insights into oxidoreductases from neutron protein crystallography. Schröder GC, Meilleur F. Acta Crystallogr D Struct Biol 77 1251-1269 (2021)
  5. 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)
  6. Tracking electrons in biological macromolecules: from ensemble to single molecule. Tabares LC, Gupta A, Aartsma TJ, Canters GW. Molecules 19 11660-11678 (2014)

Articles citing this publication (50)

  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. Biochemical and genomic analysis of the denitrification pathway within the genus Neisseria. Barth KR, Isabella VM, Clark VL. Microbiology (Reading) 155 4093-4103 (2009)
  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. 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)
  6. Structures of protein-protein complexes involved in electron transfer. Antonyuk SV, Han C, Eady RR, Hasnain SS. Nature 496 123-126 (2013)
  7. Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion? Kim SW, Fushinobu S, Zhou S, Wakagi T, Shoun H. Appl Environ Microbiol 75 2652-2658 (2009)
  8. Comparative Genomics of Candidatus Methylomirabilis Species and Description of Ca. Methylomirabilis Lanthanidiphila. Versantvoort W, Guerrero-Cruz S, Speth DR, Frank J, Gambelli L, Cremers G, van Alen T, Jetten MSM, Kartal B, Op den Camp HJM, Reimann J. Front Microbiol 9 1672 (2018)
  9. Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers. Helen D, Kim H, Tytgat B, Anne W. BMC Genomics 17 155 (2016)
  10. Biochemical and crystallographic studies of the Met144Ala, Asp92Asn and His254Phe mutants of the nitrite reductase from Alcaligenes xylosoxidans provide insight into the enzyme mechanism. Ellis MJ, Prudêncio M, Dodd FE, Strange RW, Sawers G, Eady RR, Hasnain SS. J Mol Biol 316 51-64 (2002)
  11. 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)
  12. 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)
  13. Impact of residues remote from the catalytic centre on enzyme catalysis of copper nitrite reductase. Leferink NG, Antonyuk SV, Houwman JA, Scrutton NS, Eady RR, Hasnain SS. Nat Commun 5 4395 (2014)
  14. Redox-coupled structural changes in nitrite reductase revealed by serial femtosecond and microfocus crystallography. Fukuda Y, Tse KM, Suzuki M, Diederichs K, Hirata K, Nakane T, Sugahara M, Nango E, Tono K, Joti Y, Kameshima T, Song C, Hatsui T, Yabashi M, Nureki O, Matsumura H, Inoue T, Iwata S, Mizohata E. J Biochem 159 527-538 (2016)
  15. Copper-containing nitrite reductase from Pseudomonas chlororaphis DSM 50135. Pinho D, Besson S, Brondino CD, de Castro B, Moura I. Eur J Biochem 271 2361-2369 (2004)
  16. Effect of self-alkalization on nitrite accumulation in a high-rate denitrification system: Performance, microflora and enzymatic activities. Li W, Shan XY, Wang ZY, Lin XY, Li CX, Cai CY, Abbas G, Zhang M, Shen LD, Hu ZQ, Zhao HP, Zheng P. Water Res 88 758-765 (2016)
  17. 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)
  18. Spectroscopic characterization of reaction intermediates in a model for copper nitrite reductase. Kujime M, Fujii H. Angew Chem Int Ed Engl 45 1089-1092 (2006)
  19. 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)
  20. An unprecedented insight into the catalytic mechanism of copper nitrite reductase from atomic-resolution and damage-free structures. Rose SL, Antonyuk SV, Sasaki D, Yamashita K, Hirata K, Ueno G, Ago H, Eady RR, Tosha T, Yamamoto M, Hasnain SS. Sci Adv 7 eabd8523 (2021)
  21. Catalytic and spectroscopic analysis of blue copper-containing nitrite reductase mutants altered in the environment of the type 2 copper centre: implications for substrate interaction. Prudêncio M, Eady RR, Sawers G. Biochem J 353 259-266 (2001)
  22. Fluorescence lifetime analysis of nitrite reductase from Alcaligenes xylosoxidans at the single-molecule level reveals the enzyme mechanism. Tabares LC, Kostrz D, Elmalk A, Andreoni A, Dennison C, Aartsma TJ, Canters GW. Chemistry 17 12015-12019 (2011)
  23. Orientational control over nitrite reductase on modified gold electrode and its effects on the interfacial electron transfer. Krzemiński L, Cronin S, Ndamba L, Canters GW, Aartsma TJ, Evans SD, Jeuken LJ. J Phys Chem B 115 12607-12614 (2011)
  24. 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)
  25. Development of de Novo Copper Nitrite Reductases: Where We Are and Where We Need To Go. Koebke KJ, Pecoraro VL. ACS Catal 8 8046-8057 (2018)
  26. 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)
  27. First example of a Cu(I)-(η2-O,O)nitrite complex derived from Cu(II)-nitrosyl. Kalita A, Kumar P, Deka RC, Mondal B. Chem Commun (Camb) 48 1251-1253 (2012)
  28. High-resolution neutron crystallography visualizes an OH-bound resting state of a copper-containing nitrite reductase. Fukuda Y, Hirano Y, Kusaka K, Inoue T, Tamada T. Proc Natl Acad Sci U S A 117 4071-4077 (2020)
  29. Methylated Histidines Alter Tautomeric Preferences that Influence the Rates of Cu Nitrite Reductase Catalysis in Designed Peptides. Koebke KJ, Yu F, Van Stappen C, Pinter TBJ, Deb A, Penner-Hahn JE, Pecoraro VL. J Am Chem Soc 141 7765-7775 (2019)
  30. 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)
  31. Electroreduction of nitrite on gold electrode modified with Cu-containing nitrite reductase model complex. Hiratsu T, Suzuki S, Yamaguchi K. Chem Commun (Camb) 4534-4535 (2005)
  32. Models of noncoupled dinuclear copper centers in azurin. Berry SM, Mayers JR, Zehm NA. J Biol Inorg Chem 14 143-149 (2009)
  33. Structure and nitrite reduction reactivity study of bio-inspired copper(i)-nitro complexes in steric and electronic considerations of tridentate nitrogen ligands. Chang YL, Lin YF, Chuang WJ, Kao CL, Narwane M, Chen HY, Chiang MY, Hsu SCN. Dalton Trans 47 5335-5341 (2018)
  34. The first example of photochemical reduction of nitrite into nitrogen monoxide by a dinuclear Ru(II)-Cu(II) complex and photoinduced intramolecular electron transfer reaction between Ru(II) and Cu(II) moieties. Isoda N, Torii Y, Okada T, Misoo M, Yokoyama H, Ikeda N, Nojiri M, Suzuki S, Yamaguchi K. Dalton Trans 10175-10177 (2009)
  35. 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)
  36. Copper nitrite reductase from Sinorhizobium meliloti 2011: Crystal structure and interaction with the physiological versus a nonmetabolically related cupredoxin-like mediator. Ramírez CS, Tolmie C, Opperman DJ, González PJ, Rivas MG, Brondino CD, Ferroni FM. Protein Sci 30 2310-2323 (2021)
  37. 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)
  38. In Silico Analysis of the Enzymes Involved in Haloarchaeal Denitrification. Bernabeu E, Miralles-Robledillo JM, Giani M, Valdés E, Martínez-Espinosa RM, Pire C. Biomolecules 11 1043 (2021)
  39. Nitrite Reductase Activity in Engineered Azurin Variants. Berry SM, Strange JN, Bladholm EL, Khatiwada B, Hedstrom CG, Sauer AM. Inorg Chem 55 4233-4247 (2016)
  40. 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)
  41. 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)
  42. 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)
  43. Structures of substrate- and product-bound forms of a multi-domain copper nitrite reductase shed light on the role of domain tethering in protein complexes. Sasaki D, Watanabe TF, Eady RR, Garratt RC, Antonyuk SV, Hasnain SS. IUCrJ 7 557-565 (2020)
  44. The structure of the Met144Leu mutant of copper nitrite reductase from Alcaligenes xylosoxidans provides the first glimpse of a protein-protein complex with azurin II. Paraskevopoulos K, Hough MA, Sawers RG, Eady RR, Hasnain SS. J Biol Inorg Chem 12 789-796 (2007)
  45. Thermal stability effects of removing the type-2 copper ligand His306 at the interface of nitrite reductase subunits. Stirpe A, Sportelli L, Wijma H, Verbeet MP, Guzzi R. Eur Biophys J 36 805-813 (2007)
  46. A QM/MM Study of Nitrite Binding Modes in a Three-Domain Heme-Cu Nitrite Reductase. Sen K, Hough MA, Strange RW, Yong CW, Keal TW. Molecules 23 E2997 (2018)
  47. Acid-induced nitrite reduction of nonheme iron(ii)-nitrite: mimicking biological Fe-NiR reactions. Kulbir, Das S, Devi T, Ghosh S, Chandra Sahoo S, Kumar P. Chem Sci 14 2935-2942 (2023)
  48. Biochemical Characterization of the Copper Nitrite Reductase from Neisseria gonorrhoeae. Barreiro DS, Oliveira RNS, Pauleta SR. Biomolecules 13 1215 (2023)
  49. Nitric oxide-release study of a bio-inspired copper(i)-nitrito complex under chemical and biological conditions. Chuang WJ, Narwane M, Chen HY, Kao CL, Huang B, Hsu KM, Wang YM, Hsu SCN. Dalton Trans 47 13151-13157 (2018)
  50. Nitrite reductase activity within an antiparallel de novo scaffold. Koebke KJ, Tebo AG, Manickas EC, Deb A, Penner-Hahn JE, Pecoraro VL. J Biol Inorg Chem 26 855-862 (2021)


Quick links