Poster abstracts

Poster number 19 submitted by Effie Miller

Investigating molecular determinants of cofactor assembly and metal specificity in R2lox, a cambialistic Mn/Fe metalloprotein

Effie K. Miller (Ohio State Biochemistry Program), Zachary R. Smith (Chemistry and Biochemistry), Hannah S. Shafaat (Chemistry and Biochemistry)

Abstract:
As one of only two redox-active Mn/Fe proteins, the R2-like ligand-binding oxidase (R2lox) spontaneously and selectively forms a Mn/Fe cofactor in vitro, contradicting the Irving-Williams series for metal-binding affinities.1 R2lox is capable of executing multi-electron chemistry, performing C-H bond oxidation upon O2 activation to generate an unprecedented tyrosine-valine crosslink within its scaffold, achieving this reaction with impressive control and selectivity.1,2 As such, R2lox presents a unique opportunity for investigating the molecular elements contributing to metal specificity, cofactor assembly, and chemical reactivity within a single protein scaffold.
In this work, we have utilized various biophysical spectroscopies along with molecular biology and protein engineering methods to address many of the questions surrounding the Mn/Fe protein systems. Initial examination of the WT Mn/Fe R2lox assembly mechanism using time-resolved spectroscopies, combined with global kinetic modeling, resulted in identification of two reaction intermediates with distinct kinetic profiles and spectral signatures.3 Further characterization using advanced pulsed electron paramagnetic resonance (EPR) has revealed two spin-coupled, EPR-active species with unique spectral and relaxation profiles. To further examine metal binding and reactivity, point mutations in the primary and secondary metal coordination spheres have been introduced into the R2lox scaffold. Data indicate different relative binding affinities for MnII and FeII along with an influence of the hydrogen bonding network on the R2lox reaction mechanism. Taken together, this work provides characterization of the Mn/Fe R2lox assembly mechanism and reaction intermediates and sets the stage for using the R2lox scaffold to probe molecular determinants of heterobimetallic protein reactivity.

References:
(1) Griese, J. J.; Roos, K.; Cox, N.; Shafaat, H. S.; Branca, R. M. M.; Lehtio, J.; Graslund, A.; Lubitz, W.; Siegbahn, P. E. M.; Hogbom, M. Direct Observation of Structurally Encoded Metal Discrimination and Ether Bond Formation in a Heterodinuclear Metalloprotein. Proc. Natl. Acad. Sci. 2013, 110 (43), 17189–17194.
(2) Maugeri, P. T.; Griese, J. J.; Branca, R. M.; Miller, E. K.; Smith, Z. R.; Eirich, J.; Högbom, M.; Shafaat, H. S. Driving Protein Conformational Changes with Light: Photoinduced Structural Rearrangement in a Heterobimetallic Oxidase. J. Am. Chem. Soc. 2018, 140 (4), 1471–1480.
(3) Miller, E. K.; Trivelas, N. E.; Maugeri, P. T.; Blaesi, E. J.; Shafaat, H. S. Time-Resolved Investigations of Heterobimetallic Cofactor Assembly in R2lox Reveal Distinct Mn/Fe Intermediates. Biochemistry 2017, 56 (26), 3369–3379.

Keywords: Heterobimetallic, EPR, oxidase