An extended N-H bond, driven by a conserved second-order interaction, orients the flavin N5 orbital in cholesterol oxidase

Golden, Emily; Yu, Li-Juan; Meilleur, Flora; Blakeley, Matthew P.; Duff, Anthony P.; Karton, Amir; Vrielink, Alice

doi:10.1038/srep40517

An extended N-H bond, driven by a conserved second-order interaction, orients the flavin N5 orbital in cholesterol oxidase

Journal Article · Tue Jan 17 23:00:00 EST 2017 · Scientific Reports

DOI:https://doi.org/10.1038/srep40517· OSTI ID:1624882

Golden, Emily ^[1]; Yu, Li-Juan ^[2]; Meilleur, Flora ^[3]; Blakeley, Matthew P. ^[4]; Duff, Anthony P. ^[5]; Karton, Amir ^[2]; Vrielink, Alice ^[2]

Univ. of Western Australia, Crawley, WA (Australia). School of Chemistry and Biochemistry; DOE/OSTI
Univ. of Western Australia, Crawley, WA (Australia). School of Chemistry and Biochemistry
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS); North Carolina State Univ., Raleigh, NC (United States). Structural and Molecular Biochmistry
Inst. Laue-Langevin (ILL), Grenoble (France)
Australian Nuclear Science and Technology Organisation (ANSTO), Lucas Heights, NSW (Australia). Bragg Inst.

The protein microenvironment surrounding the flavin cofactor in flavoenzymes is key to the efficiency and diversity of reactions catalysed by this class of enzymes. X-ray diffraction structures of oxidoreductase flavoenzymes have revealed recurrent features which facilitate catalysis, such as a hydrogen bond between a main chain nitrogen atom and the flavin redox center (N5). A neutron diffraction study of cholesterol oxidase has revealed an unusual elongated main chain nitrogen to hydrogen bond distance positioning the hydrogen atom towards the flavin N5 reactive center. Investigation of the structural features which could cause such an unusual occurrence revealed a positively charged lysine side chain, conserved in other flavin mediated oxidoreductases, in a second shell away from the FAD cofactor acting to polarize the peptide bond through interaction with the carbonyl oxygen atom. Double-hybrid density functional theory calculations confirm that this electrostatic arrangement affects the N-H bond length in the region of the flavin reactive center. We propose a novel second-order partial-charge interaction network which enables the correct orientation of the hydride receiving orbital of N5. The implications of these observations for flavin mediated redox chemistry are discussed.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Science Foundation (NSF)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1624882

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 7; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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