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Structure determination of murine mitochondrial carbonic anhydrase V at 2.45-A resolution: implications for catalytic proton transfer and inhibitor design.

Boriack-Sjodin PA, Heck RW, Laipis PJ, Silverman DN, Christianson DW
Proc Natl Acad Sci U S A 92 10949-53 (1995)
Cited: 52 times
EuropePMC logo PMID: 7479916

Abstract

The three-dimensional structure of murine mitochondrial carbonic anhydrase V has been determined and refined at 2.45-A resolution (crystallographic R factor = 0.187). Significant structural differences unique to the active site of carbonic anhydrase V are responsible for differences in the mechanism of catalytic proton transfer as compared with other carbonic anhydrase isozymes. In the prototypical isozyme, carbonic anhydrase II, catalytic proton transfer occurs via the shuttle group His-64; carbonic anhydrase V has Tyr-64, which is not an efficient proton shuttle due in part to the bulky adjacent side chain of Phe-65. Based on analysis of the structure of carbonic anhydrase V, we speculate that Tyr-131 may participate in proton transfer due to its proximity to zinc-bound solvent, its solvent accessibility, and its electrostatic environment in the protein structure. Finally, the design of isozyme-specific inhibitors is discussed in view of the complex between carbonic anhydrase V and acetazolamide, a transition-state analogue. Such inhibitors may be physiologically important in the regulation of blood glucose levels.

Reviews - 1dmy mentioned but not cited (1)

  1. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Krishnamurthy VM, Kaufman GK, Urbach AR, Gitlin I, Gudiksen KL, Weibel DB, Whitesides GM. Chem Rev 108 946-1051 (2008)

Articles - 1dmy mentioned but not cited (3)

  1. Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Whittington DA, Waheed A, Ulmasov B, Shah GN, Grubb JH, Sly WS, Christianson DW. Proc Natl Acad Sci U S A 98 9545-9550 (2001)
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Reviews citing this publication (10)

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  9. Insights into the role of reactive sulfhydryl groups of Carbonic Anhydrase III and VII during oxidative damage. Monti DM, De Simone G, Langella E, Supuran CT, Di Fiore A, Monti SM. J Enzyme Inhib Med Chem 32 5-12 (2017)
  10. Carbonic Anhydrases as Potential Targets Against Neurovascular Unit Dysfunction in Alzheimer's Disease and Stroke. Lemon N, Canepa E, Ilies MA, Fossati S. Front Aging Neurosci 13 772278 (2021)

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  5. A plant-type (beta-class) carbonic anhydrase in the thermophilic methanoarchaeon Methanobacterium thermoautotrophicum. Smith KS, Ferry JG. J Bacteriol 181 6247-6253 (1999)
  6. Gamma carbonic anhydrases in plant mitochondria. Parisi G, Perales M, Fornasari MS, Colaneri A, González-Schain N, Gómez-Casati D, Zimmermann S, Brennicke A, Araya A, Ferry JG, Echave J, Zabaleta E. Plant Mol Biol 55 193-207 (2004)
  7. Insights towards sulfonamide drug specificity in α-carbonic anhydrases. Aggarwal M, Kondeti B, McKenna R. Bioorg Med Chem 21 1526-1533 (2013)
  8. Crystal structure of human carbonic anhydrase XIII and its complex with the inhibitor acetazolamide. Di Fiore A, Monti SM, Hilvo M, Parkkila S, Romano V, Scaloni A, Pedone C, Scozzafava A, Supuran CT, De Simone G. Proteins 74 164-175 (2009)
  9. Crystal structure of carbonic anhydrase from Neisseria gonorrhoeae and its complex with the inhibitor acetazolamide. Huang S, Xue Y, Sauer-Eriksson E, Chirica L, Lindskog S, Jonsson BH. J Mol Biol 283 301-310 (1998)
  10. Structures of murine carbonic anhydrase IV and human carbonic anhydrase II complexed with brinzolamide: molecular basis of isozyme-drug discrimination. Stams T, Chen Y, Boriack-Sjodin PA, Hurt JD, Liao J, May JA, Dean T, Laipis P, Silverman DN, Christianson DW. Protein Sci 7 556-563 (1998)
  11. Mitochondrial carbonic anhydrase in the nervous system: expression in neuronal and glial cells. Ghandour MS, Parkkila AK, Parkkila S, Waheed A, Sly WS. J Neurochem 75 2212-2220 (2000)
  12. Carbonic anhydrase inhibitors: aromatic sulfonamides and disulfonamides act as efficient tumor growth inhibitors. Supuran CT, Scozzafava A. J Enzyme Inhib 15 597-610 (2000)
  13. Characterization of heterologously produced carbonic anhydrase from Methanosarcina thermophila. Alber BE, Ferry JG. J Bacteriol 178 3270-3274 (1996)
  14. Carbonic anhydrase in Acetobacterium woodii and other acetogenic bacteria. Braus-Stromeyer SA, Schnappauf G, Braus GH, Gössner AS, Drake HL. J Bacteriol 179 7197-7200 (1997)
  15. Structural analysis of charge discrimination in the binding of inhibitors to human carbonic anhydrases I and II. Srivastava DK, Jude KM, Banerjee AL, Haldar M, Manokaran S, Kooren J, Mallik S, Christianson DW. J Am Chem Soc 129 5528-5537 (2007)
  16. Probing the energetics of dissociation of carbonic anhydrase-ligand complexes in the gas phase. Gao J, Wu Q, Carbeck J, Lei QP, Smith RD, Whitesides GM. Biophys J 76 3253-3260 (1999)
  17. Roles of the conserved aspartate and arginine in the catalytic mechanism of an archaeal beta-class carbonic anhydrase. Smith KS, Ingram-Smith C, Ferry JG. J Bacteriol 184 4240-4245 (2002)
  18. Carbonic anhydrase inhibitors: the X-ray crystal structure of ethoxzolamide complexed to human isoform II reveals the importance of thr200 and gln92 for obtaining tight-binding inhibitors. Di Fiore A, Pedone C, Antel J, Waldeck H, Witte A, Wurl M, Scozzafava A, Supuran CT, De Simone G. Bioorg Med Chem Lett 18 2669-2674 (2008)
  19. Molecular modeling study for the binding of zonisamide and topiramate to the human mitochondrial carbonic anhydrase isoform VA. Vitale RM, Pedone C, Amodeo P, Antel J, Wurl M, Scozzafava A, Supuran CT, De Simone G. Bioorg Med Chem 15 4152-4158 (2007)
  20. Structural and kinetic characterization of an archaeal beta-class carbonic anhydrase. Smith KS, Cosper NJ, Stalhandske C, Scott RA, Ferry JG. J Bacteriol 182 6605-6613 (2000)
  21. Intracellular beta-carbonic anhydrase of the unicellular green alga Coccomyxa. Cloning of the cdna and characterization of the functional enzyme overexpressed in Escherichia coli. Hiltonen T, Björkbacka H, Forsman C, Clarke AK, Samuelsson G. Plant Physiol 117 1341-1349 (1998)
  22. X-ray crystallographic and kinetic investigations of 6-sulfamoyl-saccharin as a carbonic anhydrase inhibitor. Alterio V, Tanc M, Ivanova J, Zalubovskis R, Vozny I, Monti SM, Di Fiore A, De Simone G, Supuran CT. Org Biomol Chem 13 4064-4069 (2015)
  23. The first example of a significant active site conformational rearrangement in a carbonic anhydrase-inhibitor adduct: the carbonic anhydrase I-topiramate complex. Alterio V, Monti SM, Truppo E, Pedone C, Supuran CT, De Simone G. Org Biomol Chem 8 3528-3533 (2010)
  24. BRAF, KRAS and PIK3CA Mutation and Sensitivity to Trastuzumab in Breast Cancer Cell Line Model Patra S, Young V, Llewellyn L, Senapati JN, Mathew J. Asian Pac J Cancer Prev 18 2209-2213 (2017)
  25. Spectroscopic and MD simulation studies on unfolding processes of mitochondrial carbonic anhydrase VA induced by urea. Idrees D, Prakash A, Haque MA, Islam A, Ahmad F, Hassan MI. J Biomol Struct Dyn 34 1987-1997 (2016)
  26. Cell-specific expression of mitochondrial carbonic anhydrase in the human and rat gastrointestinal tract. Saarnio J, Parkkila S, Parkkila AK, Waheed A, Karttunen T, Sly WS. J Histochem Cytochem 47 517-524 (1999)
  27. Carbonic anhydrase inhibitors: novel compounds containing S-NH moieties: sulfenamido-sulfonamides, sulfenimido-sulfonamides and their interaction with isozymes I, II and IV. Scozzafava A, Supuran CT. J Enzyme Inhib 13 419-442 (1998)
  28. Introduction of histidine analogs leads to enhanced proton transfer in carbonic anhydrase V. Earnhardt JN, Wright SK, Qian M, Tu C, Laipis PJ, Viola RE, Silverman DN. Arch Biochem Biophys 361 264-270 (1999)
  29. Cloning, expression, purification and characterization of human mitochondrial carbonic anhydrase VA. Idrees D, Kumar S, Rehman SAA, Gourinath S, Islam A, Ahmad F, Imtaiyaz Hassan M. 3 Biotech 6 16 (2016)
  30. Carbonic anhydrase inhibitors, interaction of boron derivatives with isozymes I and II: a new binding site for hydrophobic inhibitors at the entrance of the active site as shown by docking studies. Chazalette C, Riviere-Baudet M, Scozzafava A, Abbate F, Ben Maarouf Z, Supuran CT. J Enzyme Inhib 16 125-133 (2001)
  31. Examination of the role of Gln-158 in the mechanism of CO(2) hydration catalyzed by beta-carbonic anhydrase from Arabidopsis thaliana. Rowlett RS, Tu C, Murray PS, Chamberlin JE. Arch Biochem Biophys 425 25-32 (2004)
  32. Proton uptake by bacterial reaction centers: the protein complex responds in a similar manner to the reduction of either quinone acceptor. Miksovska J, Schiffer M, Hanson DK, Sebban P. Proc Natl Acad Sci U S A 96 14348-14353 (1999)
  33. Structural study of the location of the phenyl tail of benzene sulfonamides and the effect on human carbonic anhydrase inhibition. Güzel-Akdemir O, Biswas S, Lastra K, McKenna R, Supuran CT. Bioorg Med Chem 21 6674-6680 (2013)
  34. Exploration of the residues modulating the catalytic features of human carbonic anhydrase XIII by a site-specific mutagenesis approach. De Simone G, Di Fiore A, Truppo E, Langella E, Vullo D, Supuran CT, Monti SM. J Enzyme Inhib Med Chem 34 1506-1510 (2019)
  35. Isolation and expression of murine carbonic anhydrase IV. Hurt JD, Tu C, Laipis PJ. Protein Expr Purif 12 7-16 (1998)
  36. FDA-approved carbonic anhydrase inhibitors reduce amyloid β pathology and improve cognition, by ameliorating cerebrovascular health and glial fitness. Canepa E, Parodi-Rullan R, Vazquez-Torres R, Gamallo-Lana B, Guzman-Hernandez R, Lemon NL, Angiulli F, Debure L, Ilies MA, Østergaard L, Wisniewski T, Gutiérrez-Jiménez E, Mar AC, Fossati S. Alzheimers Dement 19 5048-5073 (2023)
  37. From Homology Modeling to the Hit Identification and Drug Repurposing: A Structure-Based Approach in the Discovery of Novel Potential Anti-Obesity Compounds. Costa G, Artese A, Ortuso F, Alcaro S. Methods Mol Biol 2266 263-277 (2021)
  38. Stabilization of anionic and neutral forms of a fluorophoric ligand at the active site of human carbonic anhydrase I. Manokaran S, Banerjee J, Mallik S, Srivastava DK. Biochim Biophys Acta 1804 1965-1973 (2010)


Related citations provided by authors (1)

  1. Catalytic Properties of Mouse Carbonic Anhydrase V. Heck RW, Tanhauser SM, Manda R, TU C, Laipis PJ, Silverman DN J. Biol. Chem. 269 24742- (1994)

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