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Proton-coupled electron transfer in the catalytic cycle of Alcaligenes xylosoxidans copper-dependent nitrite reductase.

Leferink NG, Han C, Antonyuk SV, Heyes DJ, Rigby SE, Hough MA, Eady RR, Scrutton NS, Hasnain SS
Biochemistry 50 4121-31 (2011)
Related entries: 2xwz, 2xx0, 2xxf

Cited: 34 times
EuropePMC logo PMID: 21469743

Abstract

We demonstrated recently that two protons are involved in reduction of nitrite to nitric oxide through a proton-coupled electron transfer (ET) reaction catalyzed by the blue Cu-dependent nitrite reductase (Cu NiR) of Alcaligenes xylosoxidans (AxNiR). Here, the functionality of two putative proton channels, one involving Asn90 and the other His254, is studied using single (N90S, H254F) and double (N90S--H254F) mutants. All mutants studied are active, indicating that protons are still able to reach the active site. The H254F mutation has no effect on the catalytic activity, while the N90S mutation results in ~70% decrease in activity. Laser flash-photolysis experiments show that in H254F and wild-type enzyme electrons enter at the level of the T1Cu and then redistribute between the two Cu sites. Complete ET from T1Cu to T2Cu occurs only when nitrite binds at the T2Cu site. This indicates that substrate binding to T2Cu promotes ET from T1Cu, suggesting that the enzyme operates an ordered mechanism. In fact, in the N90S and N90S--H254F variants, where the T1Cu site redox potential is elevated by ∼60 mV, inter-Cu ET is only observed in the presence of nitrite. From these results it is evident that the Asn90 channel is the main proton channel in AxNiR, though protons can still reach the active site if this channel is disrupted. Crystallographic structures provide a clear structural rationale for these observations, including restoration of the proton delivery via a significant movement of the loop connecting the T1Cu ligands Cys130 and His139 that occurs on binding of nitrite. Notably, a role for this loop in facilitating interaction of cytochrome c(551) with Cu NiR has been suggested previously based on a crystal structure of the binary complex.

Reviews - 2xx1 mentioned but not cited (1)

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Reviews citing this publication (8)

  1. 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)
  2. Gating mechanisms for biological electron transfer: integrating structure with biophysics reveals the nature of redox control in cytochrome P450 reductase and copper-dependent nitrite reductase. Leferink NG, Pudney CR, Brenner S, Heyes DJ, Eady RR, Samar Hasnain S, Hay S, Rigby SE, Scrutton NS. FEBS Lett 586 578-584 (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. Kinetic and spectroscopic probes of motions and catalysis in the cytochrome P450 reductase family of enzymes. Pudney CR, Heyes DJ, Khara B, Hay S, Rigby SE, Scrutton NS. FEBS J 279 1534-1544 (2012)
  5. Designing Artificial Metalloenzymes by Tuning of the Environment beyond the Primary Coordination Sphere. Van Stappen C, Deng Y, Liu Y, Heidari H, Wang JX, Zhou Y, Ledray AP, Lu Y. Chem Rev 122 11974-12045 (2022)
  6. 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)
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  2. 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)
  3. Redox cycling and kinetic analysis of single molecules of solution-phase nitrite reductase. Goldsmith RH, Tabares LC, Kostrz D, Dennison C, Aartsma TJ, Canters GW, Moerner WE. Proc Natl Acad Sci U S A 108 17269-17274 (2011)
  4. Characterization of a nitrite reductase involved in nitrifier denitrification. Lawton TJ, Bowen KE, Sayavedra-Soto LA, Arp DJ, Rosenzweig AC. J Biol Chem 288 25575-25583 (2013)
  5. 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)
  6. 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)
  7. 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)
  8. 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)
  9. Laser-flash photolysis indicates that internal electron transfer is triggered by proton uptake by Alcaligenes xylosoxidans copper-dependent nitrite reductase. Leferink NG, Eady RR, Hasnain SS, Scrutton NS. FEBS J 279 2174-2181 (2012)
  10. 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)
  11. Unexpected Roles of a Tether Harboring a Tyrosine Gatekeeper Residue in Modular Nitrite Reductase Catalysis. Hedison TM, Shenoy RT, Iorgu AI, Heyes DJ, Fisher K, Wright GSA, Hay S, Eady RR, Antonyuk SV, Hasnain SS, Scrutton NS. ACS Catal 9 6087-6099 (2019)
  12. Catalytically important damage-free structures of a copper nitrite reductase obtained by femtosecond X-ray laser and room-temperature neutron crystallography. Halsted TP, Yamashita K, Gopalasingam CC, Shenoy RT, Hirata K, Ago H, Ueno G, Blakeley MP, Eady RR, Antonyuk SV, Yamamoto M, Hasnain SS. IUCrJ 6 761-772 (2019)
  13. High-temperature and high-resolution crystallography of thermostable copper nitrite reductase. Fukuda Y, Inoue T. Chem Commun (Camb) 51 6532-6535 (2015)
  14. 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)
  15. 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)
  16. Solvent-slaved protein motions accompany proton coupled electron transfer reactions catalysed by copper nitrite reductase. Hedison TM, Heyes DJ, Shanmugam M, Iorgu AI, Scrutton NS. Chem Commun (Camb) 55 5863-5866 (2019)
  17. Active Intermediates in Copper Nitrite Reductase Reactions Probed by a Cryotrapping-Electron Paramagnetic Resonance Approach. Hedison TM, Shanmugam M, Heyes DJ, Edge R, Scrutton NS. Angew Chem Int Ed Engl 59 13936-13940 (2020)
  18. Intra-electron transfer induced by protonation in copper-containing nitrite reductase. Lintuluoto M, Lintuluoto JM. Metallomics 10 565-578 (2018)
  19. 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)
  20. Dynamic mechanism of proton transfer in mannitol 2-dehydrogenase from Pseudomonas fluorescens: mobile GLU292 controls proton relay through a water channel that connects the active site with bulk solvent. Klimacek M, Brunsteiner M, Nidetzky B. J Biol Chem 287 6655-6667 (2012)
  21. 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)
  22. Nature of the copper-nitrosyl intermediates of copper nitrite reductases during catalysis. Hough MA, Conradie J, Strange RW, Antonyuk SV, Eady RR, Ghosh A, Hasnain SS. Chem Sci 11 12485-12492 (2020)
  23. Biochemical Characterization of the Copper Nitrite Reductase from Neisseria gonorrhoeae. Barreiro DS, Oliveira RNS, Pauleta SR. Biomolecules 13 1215 (2023)
  24. Elucidation of the Electrocatalytic Nitrite Reduction Mechanism by Bio-Inspired Copper Complexes. van Langevelde PH, Engbers S, Buda F, Hetterscheid DGH. ACS Catal 13 10094-10103 (2023)
  25. Investigation of the proton relay system operative in human cystosolic aminopeptidase P. Chang HC, Kung CC, Chang TT, Jao SC, Hsu YT, Li WS, Li WS. PLoS One 13 e0190816 (2018)


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