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Structural study of X-ray induced activation of carbonic anhydrase.

Sjöblom B, Polentarutti M, Djinovic-Carugo K
Proc Natl Acad Sci U S A 106 10609-13 (2009)
Cited: 43 times
EuropePMC logo PMID: 19520834

Abstract

Carbonic anhydrase, a zinc metalloenzyme, catalyzes the reversible hydration of carbon dioxide to bicarbonate. It is involved in processes connected with acid-base homeostasis, respiration, and photosynthesis. More than 100 distinct human carbonic anhydrase II (HCAII) 3D structures have been generated in last 3 decades [Liljas A, et al. (1972) Nat New Biol 235:131-137], but a structure of an HCAII in complex with CO(2) or HCO(3)(-) has remained elusive. Here, we report previously undescribed structures of HCAII:CO(2) and HCAII:HCO(3)(-) complexes, together with a 3D molecular film of the enzymatic reaction observed successively in the same crystal after extended exposure to X-ray. We demonstrate that the unexpected enzyme activation was caused in an X-ray dose-dependent manner. Although X-ray damage to macromolecular samples has long been recognized [Ravelli RB, Garman EF (2006) Curr Opin Struct Biol 16:624-629], the detailed structural analysis reports on X-ray-driven reactions have been very rare in literature to date. Here, we report on enzyme activation and the associated chemical reaction in a crystal at 100 K. We propose mechanisms based on water photoradiolysis and/or electron radiolysis as the main cause of enzyme activation.

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  1. Structural study of X-ray induced activation of carbonic anhydrase. Sjöblom B, Polentarutti M, Djinovic-Carugo K. Proc Natl Acad Sci U S A 106 10609-10613 (2009)
  2. Structural mechanism of RuBisCO activation by carbamylation of the active site lysine. Stec B. Proc Natl Acad Sci U S A 109 18785-18790 (2012)
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  4. Mechanism of Action of Non-Synonymous Single Nucleotide Variations Associated with α-Carbonic Anhydrase II Deficiency. Sanyanga TA, Nizami B, Bishop ÖT. Molecules 24 E3987 (2019)
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  7. Plant carbonic anhydrase-like enzymes in neuroactive alkaloid biosynthesis. Nett RS, Dho Y, Tsai C, Passow D, Martinez Grundman J, Low YY, Sattely ES. Nature 624 182-191 (2023)


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  1. Frontiers, opportunities, and challenges in biochemical and chemical catalysis of CO2 fixation. Appel AM, Bercaw JE, Bocarsly AB, Dobbek H, DuBois DL, Dupuis M, Ferry JG, Fujita E, Hille R, Kenis PJ, Kerfeld CA, Morris RH, Peden CH, Portis AR, Ragsdale SW, Rauchfuss TB, Reek JN, Seefeldt LC, Thauer RK, Waldrop GL. Chem Rev 113 6621-6658 (2013)
  2. 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)
  3. Sequestration of carbon dioxide by the hydrophobic pocket of the carbonic anhydrases. Domsic JF, McKenna R. Biochim Biophys Acta 1804 326-331 (2010)
  4. The Effects of Ionising and Non-Ionising Electromagnetic Radiation on Extracellular Matrix Proteins. Tuieng RJ, Cartmell SH, Kirwan CC, Sherratt MJ. Cells 10 3041 (2021)

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  2. X-ray structure of the first `extremo-α-carbonic anhydrase', a dimeric enzyme from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1. Di Fiore A, Capasso C, De Luca V, Monti SM, Carginale V, Supuran CT, Scozzafava A, Pedone C, Rossi M, De Simone G. Acta Crystallogr D Biol Crystallogr 69 1150-1159 (2013)
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  5. Interactions between Hofmeister anions and the binding pocket of a protein. Fox JM, Kang K, Sherman W, Héroux A, Sastry GM, Baghbanzadeh M, Lockett MR, Whitesides GM. J Am Chem Soc 137 3859-3866 (2015)
  6. Neutron structure of human carbonic anhydrase II: implications for proton transfer. Fisher SZ, Kovalevsky AY, Domsic JF, Mustyakimov M, McKenna R, Silverman DN, Langan PA. Biochemistry 49 415-421 (2010)
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  14. Comparison of helical scan and standard rotation methods in single-crystal X-ray data collection strategies. Polsinelli I, Savko M, Rouanet-Mehouas C, Ciccone L, Nencetti S, Orlandini E, Stura EA, Shepard W. J Synchrotron Radiat 24 42-52 (2017)
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  17. Structural and kinetic effects on changes in the CO(2) binding pocket of human carbonic anhydrase II. West D, Kim CU, Tu C, Robbins AH, Gruner SM, Silverman DN, McKenna R. Biochemistry 51 9156-9163 (2012)
  18. Experimental determination of the bioluminescence resonance energy transfer (BRET) Förster distances of NanoBRET and red-shifted BRET pairs. Weihs F, Wang J, Pfleger KDG, Dacres H. Anal Chim Acta X 6 100059 (2020)
  19. Evaluating the impact of X-ray damage on conformational heterogeneity in room-temperature (277 K) and cryo-cooled protein crystals. Yabukarski F, Doukov T, Mokhtari DA, Du S, Herschlag D. Acta Crystallogr D Struct Biol 78 945-963 (2022)
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  21. Inhibitory effects of nitrite on the reactions of bovine carbonic anhydrase II with CO2 and bicarbonate consistent with zinc-bound nitrite. Nielsen PM, Fago A. J Inorg Biochem 149 6-11 (2015)
  22. 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)
  23. Enhanced enzymatic activity exerted by a packed assembly of a single type of enzyme. Dinh H, Nakata E, Mutsuda-Zapater K, Saimura M, Kinoshita M, Morii T. Chem Sci 11 9088-9100 (2020)
  24. Biochemical, structural, and computational studies of a γ-carbonic anhydrase from the pathogenic bacterium Burkholderia pseudomallei. Di Fiore A, De Luca V, Langella E, Nocentini A, Buonanno M, Monti SM, Supuran CT, Capasso C, De Simone G. Comput Struct Biotechnol J 20 4185-4194 (2022)
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  29. Synthesis, Biological Evaluation, and In Silico Studies of Novel Coumarin-Based 4H,5H-pyrano[3,2-c]chromenes as Potent β-Glucuronidase and Carbonic Anhydrase Inhibitors. Arif N, Shafiq Z, Mahmood K, Rafiq M, Naz S, Shahzad SA, Farooq U, Bahkali AH, Elgorban AM, Yaqub M, El-Gokha A. ACS Omega 7 28605-28617 (2022)


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