Coordination chemistry controls the thiol oxidase activity of the B12-trafficking protein CblC

Li, Zhu; Shanmuganathan, Aranganathan; Ruetz, Markus; Yamada, Kazuhiro; Lesniak, Nicholas A.; Kräutler, Bernhard; Brunold, Thomas C.; Koutmos, Markos; Banerjee, Ruma

doi:10.1074/jbc.m117.788554

Coordination chemistry controls the thiol oxidase activity of the B₁₂-trafficking protein CblC

Journal Article · Sat Jul 01 00:00:00 EDT 2017 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.m117.788554· OSTI ID:1839713

Li, Zhu ^[1]; Shanmuganathan, Aranganathan ^[2]; Ruetz, Markus ^[1]; Yamada, Kazuhiro ^[2]; Lesniak, Nicholas A. ^[1]; Kräutler, Bernhard ^[3]; Brunold, Thomas C. ^[4]; Koutmos, Markos ^[2]; Banerjee, Ruma ^[1]

Univ. of Michigan Medical Center, Ann Arbor, MI (United States)
Uniformed Services Univ. of the Health Sciences, Bethesda, MD (United States)
Univ. of Innsbruck (Austria). Centre of Molecular Biosciences
Univ. of Wisconsin, Madison, WI (United States)

The cobalamin or B₁₂ cofactor supports sulfur and one-carbon metabolism and the catabolism of odd-chain fatty acids, branched-chain amino acids, and cholesterol. CblC is a B₁₂-processing enzyme involved in an early cytoplasmic step in the cofactor-trafficking pathway. It catalyzes the glutathione (GSH)-dependent dealkylation of alkylcobalamins and the reductive decyanation of cyanocobalamin. CblC from Caenorhabditis elegans (ceCblC) also exhibits a robust thiol oxidase activity, converting reduced GSH to oxidized GSSG with concomitant scrubbing of ambient dissolved O2. The mechanism of thiol oxidation catalyzed by ceCblC is not known. In this study, we demonstrate that novel coordination chemistry accessible to ceCblC-bound cobalamin supports its thiol oxidase activity via a glutathionyl-cobalamin intermediate. Deglutathionylation of glutathionyl-cobalamin by a second molecule of GSH yields GSSG. The crystal structure of ceCblC provides insights into how architectural differences at the α- and β-faces of cobalamin promote the thiol oxidase activity of ceCblC but mute it in wild-type human CblC. The R161G and R161Q mutations in human CblC unmask its latent thiol oxidase activity and are correlated with increased cellular oxidative stress disease. In summary, we have uncovered key architectural features in the cobalamin-binding pocket that support unusual cob(II)alamin coordination chemistry and enable the thiol oxidase activity of ceCblC.

View Accepted Manuscript (DOE)

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1839713

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 23 Vol. 292; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
adenosylcobalamin (AdoCbl)
enzyme
glutathione
oxidation-reduction (redox)
spectroscopy
thiol