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Structural and Kinetic Characterization of Active-Site Histidine as a Proton Shuttle in Catalysis by Human Carbonic Anhydrase II,

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Departments of Biochemistry and Molecular Biology and of Pharmacology and Therapeutics, College of Medicine, University of Florida, Gainesville, Florida 32610
Cite this: Biochemistry 2005, 44, 4, 1097–1105
Publication Date (Web):January 5, 2005
https://doi.org/10.1021/bi0480279
Copyright © 2005 American Chemical Society

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    Abstract

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    In the catalysis of the hydration of carbon dioxide and dehydration of bicarbonate by human carbonic anhydrase II (HCA II), a histidine residue (His64) shuttles protons between the zinc-bound solvent molecule and the bulk solution. To evaluate the effect of the position of the shuttle histidine and pH on proton shuttling, we have examined the catalysis and crystal structures of wild-type HCA II and two double mutants:  H64A/N62H and H64A/N67H HCA II. His62 and His67 both have their side chains extending into the active-site cavity with distances from the zinc approximately equivalent to that of His64. Crystal structures were determined at pH 5.1−10.0, and the catalysis of the exchange of 18O between CO2 and water was assessed by mass spectrometry. Efficient proton shuttle exceeding a rate of 105 s-1 was observed for histidine at positions 64 and 67; in contrast, relatively inefficient proton transfer at a rate near 103 s-1 was observed for His62. The observation, in the crystal structures, of a completed hydrogen-bonded water chain between the histidine shuttle residue and the zinc-bound solvent does not appear to be required for efficient proton transfer. The data suggest that the number of intervening water molecules between the donor and acceptor supporting efficient proton transfer in HCA II is important, and furthermore suggest that a water bridge consisting of two intervening water molecules is consistent with efficient proton transfer.

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     This work was supported in part by the University of Florida, College of Medicine, start-up funds (R.M.), the Thomas Maren Foundation (R.M.), and National Institutes of Health Grant GM25154 (D.N.S.).

     The atomic coordinates have been deposited in the Protein Data Bank (entries 1T9N, 1TBO, 1TBT, 1TE3, 1TEQ, 1TEU, 1TG3, 1TG9, 1TH9, and 1THK).

    §

     Department of Biochemistry and Molecular Biology.

     Department of Pharmacology and Therapeutics.

    *

     To whom correspondence should be addressed. R.M.:  Department of Biochemistry and Molecular Biology, College of Medicine, University of Florida, Box 100245, Gainesville, FL 32610; phone, (352) 392-5696; fax, (352) 392-3422; e-mail, [email protected]. D.N.S.:  Department of Pharmacology, College of Medicine, University of Florida, Box 100267, Gainesville, FL 32610; phone, (352) 392-3556; fax, (352) 392-9696; e-mail, [email protected].

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