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X-ray absorption spectroscopic characterization of the diferric-peroxo intermediate of human deoxyhypusine hydroxylase in the presence of its substrate eIF5a

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Abstract

Human deoxyhypusine hydroxylase (hDOHH) is an enzyme that is involved in the critical post-translational modification of the eukaryotic translation initiation factor 5A (eIF5A). Following the conversion of a lysine residue on eIF5A to deoxyhypusine (Dhp) by deoxyhypusine synthase, hDOHH hydroxylates Dhp to yield the unusual amino acid residue hypusine (Hpu), a modification that is essential for eIF5A to promote peptide synthesis at the ribosome, among other functions. Purification of hDOHH overexpressed in E. coli affords enzyme that is blue in color, a feature that has been associated with the presence of a peroxo-bridged diiron(III) active site. To gain further insight into the nature of the diiron site and how it may change as hDOHH goes through the catalytic cycle, we have conducted X-ray absorption spectroscopic studies of hDOHH on five samples that represent different species along its reaction pathway. Structural analysis of each species has been carried out, starting with the reduced diferrous state, proceeding through its O2 adduct, and ending with a diferric decay product. Our results show that the Fe⋯Fe distances found for the five samples fall within a narrow range of 3.4–3.5 Å, suggesting that hDOHH has a fairly constrained active site. This pattern differs significantly from what has been associated with canonical dioxygen activating nonheme diiron enzymes, such as soluble methane monooxygenase and Class 1A ribonucleotide reductases, for which the Fe⋯Fe distance can change by as much as 1 Å during the redox cycle. These results suggest that the O2 activation mechanism for hDOHH deviates somewhat from that associated with the canonical nonheme diiron enzymes, opening the door to new mechanistic possibilities for this intriguing family of enzymes.

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Scheme 1

Reproduced with permission from Ref. [20]

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Acknowledgments

This work was supported by the National Institutes of Health grant GM-38767 to L. Q. and postdoctoral fellowship 5F32GM106612-02 to L. M. E. and by the Intramural Research Program of the National Institute of Dental and Craniofacial Research. V. V. V. is grateful to the Vietnam Education Foundation for providing him with a predoctoral fellowship. XAS data were collected on Beamline 7–3 at the Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory and at Beamline X3B of the National Synchrotron Light Source (NSLS). SLAC is supported by the US Department of Energy (DOE), Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. Use of Beamline 7–3 is supported by the DOE Office of Biological and Environmental Research, and by the National Institutes of Health, National Institute of General Medical Sciences (including P41GM103393). NSLS is a DOE Office of Science User Facility operated for the DOE Office of Science by Brookhaven National Laboratory under Contract No. DE-AC02-98CH10886. We thank Dr. Caleb Allpress for helpful discussions.

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  1. Van V. Vu

    Present address: NTT Hi-Tech Institute, Nguyen Tat Thanh University, 298-300A Nguyen Tat Thanh Street, Ward 13, District 4, Ho Chi Minh City, Vietnam

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  1. Department of Chemistry and Center for Metals in Biocatalysis, University of Minnesota, 207 Pleasant St. SE, Minneapolis, MN, 55455, USA

    Andrew J. Jasniewski, Lisa M. Engstrom, Van V. Vu & Lawrence Que Jr.

  2. National Institute of Dental and Craniofacial Research, National Institutes of Health, 9000 Rockville Pike, Bethesda, MD, 20892, USA

    Myung Hee Park

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Jasniewski, A.J., Engstrom, L.M., Vu, V.V. et al. X-ray absorption spectroscopic characterization of the diferric-peroxo intermediate of human deoxyhypusine hydroxylase in the presence of its substrate eIF5a. J Biol Inorg Chem 21, 605–618 (2016). https://doi.org/10.1007/s00775-016-1373-8

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