Dynamic Hydrogen-Bonding Network in the Distal Pocket of the Nitrosyl Complex of Pseudomonas aeruginosa cd Nitrite Reductase.

cd nitrite reductase (NIR) is a key enzyme in the denitrification process that reduces nitrite to nitric oxide (NO). It contains a specialized d-heme cofactor, found only in this class of enzymes, where the substrate, nitrite, binds and is converted to NO. For a long time, it was believed that NO mu...

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Published in:Journal of the American Chemical Society Vol. 133; no. 9; pp. 3043 - 3056
Main Authors: Radoul, Marina, Bykov, Dmytro, Rinaldo, Serena, Cutruzzolà, Francesca, Neese, Frank, Goldfarb, Daniella
Format: Article
Published: American Chemical Society 3/9/2011
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Online Access:View this record in EBSCOhost
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      dt: 3/9/2011
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      pub: American Chemical Society
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        10.1021/ja109688w
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        atl: Dynamic Hydrogen-Bonding Network in the Distal Pocket of the Nitrosyl Complex of Pseudomonas aeruginosa cd Nitrite Reductase.
      aug:
        au:
          Radoul, Marina
          Bykov, Dmytro
          Rinaldo, Serena
          Cutruzzolà, Francesca
          Neese, Frank
          Goldfarb, Daniella
        affil:
          Department of Chemical Physics, Weizmann Institute of Science, Rehovot 76100, Israel
          Dipartimento di Scienze Biochimiche "A. Rossi Fanelli", Universit di Roma "La Sapienza", Rome, Italy
          Institute for Physical and Theoretical Chemistry, University of Bonn, Wegelerstrasse 12, Bonn -53115, Germany
      su:
        Hydrogen bonding
        Molecular association
        Pseudomonas aeruginosa
        Density functionals
        Nitrogen compounds
        Scission (Chemistry)
      sug:
        subj:
          Hydrogen bonding
          Molecular association
          Pseudomonas aeruginosa
          Density functionals
          Nitrogen compounds
          Scission (Chemistry)
      ab: cd nitrite reductase (NIR) is a key enzyme in the denitrification process that reduces nitrite to nitric oxide (NO). It contains a specialized d-heme cofactor, found only in this class of enzymes, where the substrate, nitrite, binds and is converted to NO. For a long time, it was believed that NO must be released from the ferric d-heme to avoid enzyme inhibition by the formation of ferrous-nitroso complex, which was considered as a dead-end product. However, recently an enhanced rate of NO dissociation from the ferrous form, not observed in standard b-type hemes, has been reported and attributed to the unique d-heme structure (Rinaldo, S.; Arcovito, A.; Brunori, M.; Cutruzzol, F. J. Biol. Chem. 2007, 282, 14761-14767). Here, we report on a detailed study of the spatial and electronic structure of the ferrous d-heme NO complex from Pseudomonas aeruginosa cd NIR and two mutants Y10F and H369A/H327A in solution, searching for the unique properties that are responsible for the relatively fast release. There are three residues at the "distal" side of the heme (Tyr, His, and His), and in this work we focus on the identification and characterization of possible H-bonds they can form with the NO, thereby affecting the stability of the complex. For this purpose, we have used high field pulse electron-nuclear double resonance (ENDOR) combined with density functional theory (DFT) calculations. The DFT calculations were essential for assigning and interpreting the ENDOR spectra in terms of geometric structure. We have shown that the NO in the nitrosyl d-heme complex of cd NIR forms H-bonds with Tyr and His, whereas the second conserved histidine, His, appears to be less involved in NO H-bonding. This is in contrast to the crystal structure that shows that Tyr is removed from the NO. We have also observed a larger solvent accessibility to the distal pocket in the mutants as compared to the wild-type. Moreover, it was shown that the H-bonding network within the active site is dynamic and that a change in the protonation state of one of the residues does affect the strength and position of the H-bonds formed by the others. In the Y10F mutant, His is closer to the NO, whereas mutation of both distal histidines displaces Tyr, removing its H-bond. The implications of the H-bonding network found in terms of the complex stability and catalysis are discussed.
      pubtype: Academic Journal
      doctype: Article
      src: R
    language: English
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          year: 2011
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