Structural and Kinetic Characterization of Active-Site Histidine as a Proton Shuttle in Catalysis by Human Carbonic Anhydrase II†,‡
- Zoë Fisher
- ,
- Jose A. Hernandez Prada
- ,
- Chingkuang Tu
- ,
- David Duda
- ,
- Craig Yoshioka
- ,
- Haiqian An
- ,
- Lakshmanan Govindasamy
- ,
- David N. Silverman
- , and
- Robert McKenna
Abstract
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.
†
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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- Deryanur KILIÇ, Orhan ERDOĞAN, Ömer İrfan KÜFREVİOĞLU. Effect of mutation in active site residue Trp209 to Val, Leu, Ile and Pro on the catalytic activity and affinity for some benzenesulfonamides of human carbonic anhydrase II. TURKISH JOURNAL OF BIOLOGY 2017, 41 , 835-842. https://doi.org/10.3906/biy-1705-37
- Sina Ibne Noor, Jacques Pouyssegur, Joachim W. Deitmer, Holger M. Becker. Integration of a ‘proton antenna’ facilitates transport activity of the monocarboxylate transporter MCT4. The FEBS Journal 2017, 284 (1) , 149-162. https://doi.org/10.1111/febs.13964
- Vijayakumar Somalinga, Greg Buhrman, Ashikha Arun, Robert B. Rose, Amy M. Grunden, . A High-Resolution Crystal Structure of a Psychrohalophilic α–Carbonic Anhydrase from Photobacterium profundum Reveals a Unique Dimer Interface. PLOS ONE 2016, 11 (12) , e0168022. https://doi.org/10.1371/journal.pone.0168022
- Carrie Lomelino, Robert McKenna. Carbonic anhydrase inhibitors: a review on the progress of patent literature (2011–2016). Expert Opinion on Therapeutic Patents 2016, 26 (8) , 947-956. https://doi.org/10.1080/13543776.2016.1203904
- Wilson Galvão de Morais, Eliana Setsuko Kamimura, Eloízio Júlio Ribeiro, Benevides Costa Pessela, Vicelma Luiz Cardoso, Miriam Maria de Resende. Optimization of the production and characterization of lipase from Candida rugosa and Geotrichum candidum in soybean molasses by submerged fermentation. Protein Expression and Purification 2016, 123 , 26-34. https://doi.org/10.1016/j.pep.2016.04.001
- Carrie Lomelino, Claudiu Supuran, Robert McKenna. Non-Classical Inhibition of Carbonic Anhydrase. International Journal of Molecular Sciences 2016, 17 (7) , 1150. https://doi.org/10.3390/ijms17071150
- Sopheavy Siek, Natalie A. Dixon, Mukesh Kumar, Jodi S. Kraus, Kirsten R. Wells, Brittany W. Rowe, Steven P. Kelley, Matthias Zeller, Glenn P. A. Yap, Elizabeth T. Papish. Synthesis of Biomimetic Zinc Complexes for CO2 Activation and the Influence of Steric Changes in the Ttz Ligands [Ttz = Tris(triazolyl)borate]. European Journal of Inorganic Chemistry 2016, 2016 (15-16) , 2495-2507. https://doi.org/10.1002/ejic.201500819
- Chae Un Kim, HyoJin Song, Balendu Sankara Avvaru, Sol M. Gruner, SangYoun Park, Robert McKenna. Tracking solvent and protein movement during CO 2 release in carbonic anhydrase II crystals. Proceedings of the National Academy of Sciences 2016, 113 (19) , 5257-5262. https://doi.org/10.1073/pnas.1520786113
- Ryszard Michalczyk, Clifford J. Unkefer, John-Paul Bacik, Tobias E. Schrader, Andreas Ostermann, Andrey Y. Kovalevsky, Robert McKenna, Suzanne Zoë Fisher. Joint neutron crystallographic and NMR solution studies of Tyr residue ionization and hydrogen bonding: Implications for enzyme-mediated proton transfer. Proceedings of the National Academy of Sciences 2015, 112 (18) , 5673-5678. https://doi.org/10.1073/pnas.1502255112
- M. Ghiasi, S. Kamalinahad, M. Zahedi. Complexation of nanoscale enzyme inhibitor with carbonic anhydrase active center: A quantum mechanical approach. Journal of Structural Chemistry 2014, 55 (8) , 1574-1586. https://doi.org/10.1134/S0022476614080277
- Christopher D. Boone, Melissa Pinard, Rob McKenna, David Silverman. Catalytic Mechanism of α-Class Carbonic Anhydrases: CO2 Hydration and Proton Transfer. 2014, 31-52. https://doi.org/10.1007/978-94-007-7359-2_3
- Deri Morgan, Boris Musset, Kethika Kulleperuma, Susan M.E. Smith, Sindhu Rajan, Vladimir V. Cherny, Régis Pomès, Thomas E. DeCoursey. Peregrination of the selectivity filter delineates the pore of the human voltage-gated proton channel hHV1. Journal of General Physiology 2013, 142 (6) , 625-640. https://doi.org/10.1085/jgp.201311045
- Weitai Wu, Shuiqin Zhou. Responsive Materials for Self‐ R egulated Insulin Delivery. Macromolecular Bioscience 2013, 13 (11) , 1464-1477. https://doi.org/10.1002/mabi.201300120
- Thomas E. DeCoursey. Voltage-Gated Proton Channels: Molecular Biology, Physiology, and Pathophysiology of the H V Family. Physiological Reviews 2013, 93 (2) , 599-652. https://doi.org/10.1152/physrev.00011.2012
- Mayank Aggarwal, Christopher D. Boone, Bhargav Kondeti, Robert McKenna. Structural annotation of human carbonic anhydrases. Journal of Enzyme Inhibition and Medicinal Chemistry 2013, 28 (2) , 267-277. https://doi.org/10.3109/14756366.2012.737323
- Mayank Aggarwal, Bhargav Kondeti, Robert McKenna. Insights towards sulfonamide drug specificity in α-carbonic anhydrases. Bioorganic & Medicinal Chemistry 2013, 21 (6) , 1526-1533. https://doi.org/10.1016/j.bmc.2012.08.019
- Luciana Gavernet, José L. Gonzalez Funes, Pablo H. Palestro, Luis E. Bruno Blanch, Guillermina L. Estiu, Alfonso Maresca, Ivana Barrios, Claudiu T. Supuran. Inhibition pattern of sulfamide-related compounds in binding to carbonic anhydrase isoforms I, II, VII, XII and XIV. Bioorganic & Medicinal Chemistry 2013, 21 (6) , 1410-1418. https://doi.org/10.1016/j.bmc.2012.10.048
- Puspita Halder, Srabani Taraphder. Modeling the structure and proton transfer pathways of the mutant His-107-Tyr of human carbonic anhydrase II. Journal of Molecular Modeling 2013, 19 (1) , 289-298. https://doi.org/10.1007/s00894-012-1549-2
- Z. Fisher, C. D. Boone, S. M. Biswas, B. Venkatakrishnan, M. Aggarwal, C. Tu, M. Agbandje-McKenna, D. Silverman, R. McKenna. Kinetic and structural characterization of thermostabilized mutants of human carbonic anhydrase II. Protein Engineering Design and Selection 2012, 25 (7) , 347-355. https://doi.org/10.1093/protein/gzs027
- Valentina G. Zobnina, Marina V. Kosevich, Vitaliy V. Chagovets, Oleg A. Boryak, Károly Vékey, Ágnes Gömöry, Anna N. Kulyk. Interactions of oligomers of organic polyethers with histidine amino acid. Rapid Communications in Mass Spectrometry 2012, 26 (5) , 532-540. https://doi.org/10.1002/rcm.5342
- Sudaratana R Krungkrai, Jerapan Krungkrai. Malaria parasite carbonic anhydrase: inhibition of aromatic/heterocyclic sulfonamides and its therapeutic potential. Asian Pacific Journal of Tropical Biomedicine 2011, 1 (3) , 233-242. https://doi.org/10.1016/S2221-1691(11)60034-8
- Balendu Sankara Avvaru, Daniel J. Arenas, Chingkuang Tu, D.B. Tanner, Robert McKenna, David N. Silverman. Comparison of solution and crystal properties of Co(II)–substituted human carbonic anhydrase II. Archives of Biochemistry and Biophysics 2010, 502 (1) , 53-59. https://doi.org/10.1016/j.abb.2010.07.010