Near-IR MCD of the Nonheme Ferrous Active Site in Naphthalene 1,2-Dioxygenase: Correlation to Crystallography and Structural Insight into the Mechanism of Rieske Dioxygenases
- 12 January 2008
- journal article
- research article
- Published by American Chemical Society (ACS) in Journal of the American Chemical Society
- Vol. 130 (5), 1601-1610
- https://doi.org/10.1021/ja074769o
Abstract
Near-IR MCD and variable temperature, variable field (VTVH) MCD have been applied to naphthalene 1,2-dioxygenase (NDO) to describe the coordination geometry and electronic structure of the mononuclear nonheme ferrous catalytic site in the resting and substrate-bound forms with the Rieske 2Fe2S cluster oxidized and reduced. The structural results are correlated with the crystallographic studies of NDO and other related Rieske nonheme iron oxygenases to develop molecular level insights into the structure/function correlation for this class of enzymes. The MCD data for resting NDO with the Rieske center oxidized indicate the presence of a six-coordinate high-spin ferrous site with a weak axial ligand which becomes more tightly coordinated when the Rieske center is reduced. Binding of naphthalene to resting NDO (Rieske oxidized and reduced) converts the six-coordinate sites into five-coordinate (5c) sites with elimination of a water ligand. In the Rieske oxidized form the 5c sites are square pyramidal but transform to a 1:2 mixture of trigonal bipyramial/square pyramidal sites when the Rieske center is reduced. Thus the geometric and electronic structure of the catalytic site in the presence of substrate can be significantly affected by the redox state of the Rieske center. The catalytic ferrous site is primed for the O2 reaction when substrate is bound in the active site in the presence of the reduced Rieske site. These structural changes ensure that two electrons and the substrate are present before the binding and activation of O2, which avoids the uncontrolled formation and release of reactive oxygen species.Keywords
This publication has 55 references indexed in Scilit:
- Structural investigations of the ferredoxin and terminal oxygenase components of the biphenyl 2,3-dioxygenase from Sphingobium yanoikuyae B1BMC Structural Biology, 2007
- Radical Intermediates in Monooxygenase Reactions of Rieske DioxygenasesJournal of the American Chemical Society, 2007
- Structural Basis for Regioselectivity and Stereoselectivity of Product Formation by Naphthalene 1,2-DioxygenaseJournal of Bacteriology, 2006
- Spectroscopic and electronic structure studies of aromatic electrophilic attack and hydrogen-atom abstraction by non-heme iron enzymesProceedings of the National Academy of Sciences of the United States of America, 2006
- The “Bridging” Aspartate 178 in Phthalate Dioxygenase Facilitates Interactions between the Rieske Center and the Iron(II)−Mononuclear CenterBiochemistry, 2006
- Rieske business: Structure–function of Rieske non-heme oxygenasesBiochemical and Biophysical Research Communications, 2005
- Structure of the Terminal Oxygenase Component of Angular Dioxygenase, Carbazole 1,9a-DioxygenaseJournal of Molecular Biology, 2005
- Structural Insight into the Dioxygenation of Nitroarene Compounds: the Crystal Structure of Nitrobenzene DioxygenaseJournal of Molecular Biology, 2005
- The 2-His-1-carboxylate facial triad: a versatile platform for dioxygen activation by mononuclear non-heme iron(II) enzymesJBIC Journal of Biological Inorganic Chemistry, 2005
- Crystal Structure of the Terminal Oxygenase Component of Biphenyl Dioxygenase Derived from Rhodococcus sp. Strain RHA1Journal of Molecular Biology, 2004