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A short, strong hydrogen bond in the active site of human carbonic anhydrase II.

Avvaru BS, Kim CU, Sippel KH, Gruner SM, Agbandje-McKenna M, Silverman DN, McKenna R
Biochemistry 49 249-51 (2010)
Cited: 90 times
EuropePMC logo PMID: 20000378

Abstract

The crystal structure of human carbonic anhydrase II (HCA II) obtained at 0.9 A resolution reveals that a water molecule, termed deep water, Dw, and bound in a hydrophobic pocket of the active site forms a short, strong hydrogen bond with the zinc-bound solvent molecule, a conclusion based on the observed oxygen-oxygen distance of 2.45 A. This water structure has similarities with hydrated hydroxide found in crystals of certain inorganic complexes. The energy required to displace Dw contributes in significant part to the weak binding of CO(2) in the enzyme-substrate complex, a weak binding that enhances k(cat) for the conversion of CO(2) into bicarbonate. In addition, this short, strong hydrogen bond is expected to contribute to the low pK(a) of the zinc-bound water and to promote proton transfer in catalysis.

Reviews - 3ks3 mentioned but not cited (6)

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Articles - 3ks3 mentioned but not cited (52)

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  28. Structural and biophysical characterization of the α-carbonic anhydrase from the gammaproteobacterium Thiomicrospira crunogena XCL-2: insights into engineering thermostable enzymes for CO2 sequestration. Díaz-Torres NA, Mahon BP, Boone CD, Pinard MA, Tu C, Ng R, Agbandje-McKenna M, Silverman D, Scott K, McKenna R. Acta Crystallogr. D Biol. Crystallogr. 71 1745-1756 (2015)
  29. Structural elucidation of the hormonal inhibition mechanism of the bile acid cholate on human carbonic anhydrase II. Boone CD, Tu C, McKenna R. Acta Crystallogr. D Biol. Crystallogr. 70 1758-1763 (2014)
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  31. Aspirin: A Suicide Inhibitor of Carbonic Anhydrase II. Andring J, Combs J, McKenna R. Biomolecules 10 (2020)
  32. Effect of donor atom identity on metal-binding pharmacophore coordination. Dick BL, Patel A, McCammon JA, Cohen SM. J. Biol. Inorg. Chem. 22 605-613 (2017)
  33. Sculpting Metal-binding Environments in De Novo Designed Three-helix Bundles. Plegaria JS, Pecoraro VL. Isr. J. Chem. 55 85-95 (2015)
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  35. Structure and mechanism of copper-carbonic anhydrase II: a nitrite reductase. Andring JT, Kim CU, McKenna R. IUCrJ 7 287-293 (2020)
  36. The Crystal Structure of a hCA VII Variant Provides Insights into the Molecular Determinants Responsible for Its Catalytic Behavior. Buonanno M, Di Fiore A, Langella E, D'Ambrosio K, Supuran CT, Monti SM, De Simone G. Int J Mol Sci 19 (2018)
  37. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
  38. Advances in Anti-Cancer Drug Development Targeting Carbonic Anhydrase IX and XII. Mboge MY, McKenna R, Frost SC. Top Anticancer Res 5 3-42 (2015)
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  42. Visualizing drug binding interactions using microcrystal electron diffraction. Clabbers MTB, Fisher SZ, Coinçon M, Zou X, Xu H. Commun Biol 3 417 (2020)
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  46. Engineered Carbonic Anhydrase VI-Mimic Enzyme Switched the Structure and Affinities of Inhibitors. Kazokaitė J, Kairys V, Smirnovienė J, Smirnov A, Manakova E, Tolvanen M, Parkkila S, Matulis D. Sci Rep 9 12710 (2019)
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  48. Network of Conformational Transitions Revealed by Molecular Dynamics Simulations of the Carbonic Anhydrase II Apo-Enzyme. Ma H, Li A, Gao K. ACS Omega 2 8414-8420 (2017)
  49. Preliminary X-ray crystallographic analysis of α-carbonic anhydrase from Thiomicrospira crunogena XCL-2. Díaz Torres N, González G, Biswas S, Scott KM, McKenna R. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68 1064-1066 (2012)
  50. The Influence of Varying Fluorination Patterns on the Thermodynamics and Kinetics of Benzenesulfonamide Binding to Human Carbonic Anhydrase II. Glöckner S, Ngo K, Wagner B, Heine A, Klebe G. Biomolecules 10 (2020)
  51. The oxygen-oxygen distance of water in crystallographic data sets. Palese LL. Data Brief 28 105076 (2020)
  52. Vanillin enones as selective inhibitors of the cancer associated carbonic anhydrase isoforms IX and XII. The out of the active site pocket for the design of selective inhibitors? Riafrecha LE, Le Pors MS, Lavecchia MJ, Bua S, Supuran CT, Colinas PA. J Enzyme Inhib Med Chem 36 2118-2127 (2021)


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  3. Update on carbonic anhydrase inhibitors: a patent review (2008 - 2011). Aggarwal M, McKenna R. Expert Opin Ther Pat 22 903-915 (2012)
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  5. Thermodynamic, kinetic, and structural parameterization of human carbonic anhydrase interactions toward enhanced inhibitor design. Linkuvienė V, Zubrienė A, Manakova E, Petrauskas V, Baranauskienė L, Zakšauskas A, Smirnov A, Gražulis S, Ladbury JE, Matulis D. Q Rev Biophys 51 e10 (2018)

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  5. Inhibition of tumor-associated human carbonic anhydrase isozymes IX and XII by a new class of substituted-phenylacetamido aromatic sulfonamides. Akdemir A, Güzel-Akdemir O, Scozzafava A, Capasso C, Supuran CT. Bioorg. Med. Chem. 21 5228-5232 (2013)
  6. Structure of a dimeric fungal α-type carbonic anhydrase. Cuesta-Seijo JA, Borchert MS, Navarro-Poulsen JC, Schnorr KM, Mortensen SB, Lo Leggio L. FEBS Lett. 585 1042-1048 (2011)
  7. Joint neutron crystallographic and NMR solution studies of Tyr residue ionization and hydrogen bonding: Implications for enzyme-mediated proton transfer. Michalczyk R, Unkefer CJ, Bacik JP, Schrader TE, Ostermann A, Kovalevsky AY, McKenna R, Fisher SZ. Proc. Natl. Acad. Sci. U.S.A. 112 5673-5678 (2015)
  8. Carbonic anhydrases and their biotechnological applications. Boone CD, Habibzadegan A, Gill S, McKenna R. Biomolecules 3 553-562 (2013)
  9. The unique structure of carbonic anhydrase αCA1 from Chlamydomonas reinhardtii. Suzuki K, Yang SY, Shimizu S, Morishita EC, Jiang J, Zhang F, Hoque MM, Sato Y, Tsunoda M, Sekiguchi T, Takénaka A. Acta Crystallogr. D Biol. Crystallogr. 67 894-901 (2011)
  10. Appraisal of sildenafil binding on the structure and promiscuous esterase activity of native and histidine-modified forms of carbonic anhydrase II. Mahdiuni H, Bijari N, Varzandian M, Ghadami SA, Khazaei M, Nikbakht MR, Khodarahmi R. Biophys. Chem. 175-176 1-16 (2013)
  11. Complexes of CO₂ with the Azoles: Tetrel Bonds, Hydrogen Bonds and Other Secondary Interactions. Del Bene JE, Elguero J, Alkorta I. Molecules 23 (2018)
  12. Molecular dynamics study of human carbonic anhydrase II in complex with Zn(2+) and acetazolamide on the basis of all-atom force field simulations. Wambo TO, Chen LY, McHardy SF, Tsin AT. Biophys. Chem. 214-215 54-60 (2016)
  13. The pathway for serial proton supply to the active site of nitrogenase: enhanced density functional modeling of the Grotthuss mechanism. Dance I. Dalton Trans 44 18167-18186 (2015)
  14. Coupling Protein Dynamics with Proton Transport in Human Carbonic Anhydrase II. Taraphder S, Maupin CM, Swanson JM, Voth GA. J Phys Chem B 120 8389-8404 (2016)
  15. Bile Acid Conjugated DNA Chimera that Conditionally Inhibits Carbonic Anhydrase-II in the Presence of MicroRNA-21. Chu X, Battle CH, Zhang N, Aryal GH, Mottamal M, Jayawickramarajah J. Bioconjug. Chem. 26 1606-1612 (2015)
  16. Native mass spectrometry of human carbonic anhydrase I and its inhibitor complexes. Zoppi C, Nocentini A, Supuran CT, Pratesi A, Messori L. J Biol Inorg Chem 25 979-993 (2020)
  17. Conformational Change of H64 and Substrate Transportation: Insight Into a Full Picture of Enzymatic Hydration of CO2 by Carbonic Anhydrase. Fu Y, Fan F, Zhang Y, Wang B, Cao Z. Front Chem 9 706959 (2021)
  18. Conformationally locked lanthanide chelating tags for convenient pseudocontact shift protein nuclear magnetic resonance spectroscopy. Joss D, Walliser RM, Zimmermann K, Häussinger D. J. Biomol. NMR 72 29-38 (2018)
  19. Crystal Structure of Carbonic Anhydrase II in Complex with an Activating Ligand: Implications in Neuronal Function. Bhatt A, Mondal UK, Supuran CT, Ilies MA, McKenna R. Mol. Neurobiol. 55 7431-7437 (2018)
  20. Structural Characterization of Carbonic Anhydrase-Arylsulfonamide Complexes Using Ultraviolet Photodissociation Mass Spectrometry. Santos IC, Brodbelt JS. J Am Soc Mass Spectrom 32 1370-1379 (2021)
  21. Ibuprofen: a weak inhibitor of carbonic anhydrase II. Combs J, Andring J, McKenna R. Acta Crystallogr F Struct Biol Commun 78 395-402 (2022)
  22. Long-range paramagnetic NMR data can provide a closer look on metal coordination in metalloproteins. Cerofolini L, Staderini T, Giuntini S, Ravera E, Fragai M, Parigi G, Pierattelli R, Luchinat C. J. Biol. Inorg. Chem. 23 71-80 (2018)
  23. Membrane perturbations induced by the interactions of zinc ions with band 3 in human erythrocytes. Kiyoatake K, Nagadome S, Yamaguchi T. Biochem Biophys Rep 2 63-68 (2015)
  24. NMR studies of active-site properties of human carbonic anhydrase II by using (15) N-labeled 4-methylimidazole as a local probe and histidine hydrogen-bond correlations. Shenderovich IG, Lesnichin SB, Tu C, Silverman DN, Tolstoy PM, Denisov GS, Limbach HH. Chemistry 21 2915-2929 (2015)
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  26. Revisiting the concept of peptide bond planarity in an iron-sulfur protein by neutron structure analysis. Hanazono Y, Hirano Y, Takeda K, Kusaka K, Tamada T, Miki K. Sci Adv 8 eabn2276 (2022)
  27. The three-tails approach as a new strategy to improve selectivity of action of sulphonamide inhibitors against tumour-associated carbonic anhydrase IX and XII. Bonardi A, Bua S, Combs J, Lomelino C, Andring J, Osman SM, Toti A, Di Cesare Mannelli L, Gratteri P, Ghelardini C, McKenna R, Nocentini A, Supuran CT. J Enzyme Inhib Med Chem 37 930-939 (2022)


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