Insights into the role of reactive sulfhydryl groups of Carbonic Anhydrase III and VII during oxidative damage

References

• Alterio V, Di Fiore A, D’Ambrosio K, et al. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
   PubMed Web of Science ®Google Scholar
• Dathan NA, Alterio V, Troiano E, et al. Biochemical characterization of the chloroplastic beta-carbonic anhydrase from Flaveria bidentis (L.) “Kuntze”. J Enz Inhib Med Chem 2014;29:500–4.
   PubMed Web of Science ®Google Scholar
• Ferry JG. The gamma class of carbonic anhydrases. Biochim Biophys Acta 2010;1804:374–81.
   PubMed Web of Science ®Google Scholar
• Alterio V, Langella E, De Simone G, Monti SM. Cadmium-containing carbonic anhydrase CDCA1 in marine diatom Thalassiosira weissflogii. Marine Drugs 2015;13:1688–97.
   PubMed Web of Science ®Google Scholar
• De Simone G, Di Fiore A, Capasso C, Supuran CT. The zinc coordination pattern in the eta-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. Bioorg Med Chem Lett 2015;25:1385–9.
   PubMed Web of Science ®Google Scholar
• Supran CT, De Simone G, eds. Carbonic anhydrases as biocatalysts: from theory to medical and industrial applications. Amsterdam: Elsevier; 2015.
   Google Scholar
• Scozzafava A, Supuran CT. Glaucoma and the applications of carbonic anhydrase inhibitors. Sub-Cell Biochem 2014;75:349–59.
   PubMedGoogle Scholar
• Thiry A, Dogne JM, Supuran CT, Masereel B. Carbonic anhydrase inhibitors as anticonvulsant agents. Curr Top Med Chem 2007;7:855–64.
   PubMed Web of Science ®Google Scholar
• Pastorek J, Pastorekova S. Hypoxia-induced carbonic anhydrase IX as a target for cancer therapy: from biology to clinical use. Semin Cancer Biol 2015;31:52–64.
   PubMed Web of Science ®Google Scholar
• Guler OO, De Simone G, Supuran CT. Drug design studies of the novel antitumor targets carbonic anhydrase IX and XII. Curr Med Chem 2010;17:1516–26.
   PubMed Web of Science ®Google Scholar
• Eriksson AE, Liljas A. Refined structure of bovine carbonic anhydrase III at 2.0 A resolution. Proteins 1993;16:29–42.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Truppo E, Supuran CT, et al. Crystal structure of the C183S/C217S mutant of human CA VII in complex with acetazolamide. Bioorg Med Chem Lett 2010;20:5023–6.
   PubMed Web of Science ®Google Scholar
• Truppo E, Supuran CT, Sandomenico A, et al. Carbonic anhydrase VII is S-glutathionylated without loss of catalytic activity and affinity for sulfonamide inhibitors. Bioorg Med Chem Lett 2012;22:1560–4.
   PubMed Web of Science ®Google Scholar
• Cabiscol E, Levine RL. Carbonic anhydrase III. Oxidative modification in vivo and loss of phosphatase activity during aging. J Biol Chem 1995;270:14742–7.
   PubMed Web of Science ®Google Scholar
• Monti SM, Supuran CT, De Simone G, Di Fiore A. Carbonic anhydrase VII. In: Supran CT, De Simone G, eds. Carbonic anhydrases as biocatalysts: from theory to medical and industrial applications. Amsterdam: Elsevier; 2015:151–68.
   Google Scholar
• Del Giudice R, Monti DM, Truppo E, et al. Human carbonic anhydrase VII protects cells from oxidative damage. Biol Chem 2013;394:1343–8.
   PubMed Web of Science ®Google Scholar
• Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000;408:239–47.
   PubMed Web of Science ®Google Scholar
• Yoshikawa T, Naito Y. What is oxidative stress? Jpn Med Assoc J 2002;45:271–6.
   Google Scholar
• Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009;7:65–74.
   PubMed Web of Science ®Google Scholar
• Machlin LJ, Bendich A. Free radical tissue damage: protective role of antioxidant nutrients. FASEB J 1987;1:441–5.
   PubMed Web of Science ®Google Scholar
• Zimmerman UJ, Wang P, Zhang X, et al. Anti-oxidative response of carbonic anhydrase III in skeletal muscle. IUBMB Life 2004;56:343–7.
   PubMed Web of Science ®Google Scholar
• Roy P, Reavey E, Rayne M, et al. Enhanced sensitivity to hydrogen peroxide-induced apoptosis in Evi1 transformed Rat1 fibroblasts due to repression of carbonic anhydrase III. FEBS J 2010;277:441–52.
   PubMed Web of Science ®Google Scholar
• Rivera C, Voipio J, Kaila K. Two developmental switches in GABAergic signalling: the K+-Cl − cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol (Lond) 2005;562:27–36.
   Google Scholar
• Harju AK, Bootorabi F, Kuuslahti M, et al. Carbonic anhydrase III: a neglected isozyme is stepping into the limelight. J Enz Inhib Med Chem 2013;28:231–9.
   PubMed Web of Science ®Google Scholar
• Wade R, Gunning P, Eddy R, et al. Nucleotide sequence, tissue-specific expression, and chromosome location of human carbonic anhydrase III: the human CAIII gene is located on the same chromosome as the closely linked CAI and CAII genes. Proc Natl Acad Sci USA 1986;83:9571–5.
   PubMed Web of Science ®Google Scholar
• Spicer SS, Ge ZH, Tashian RE, et al. Comparative distribution of carbonic anhydrase isozymes III and II in rodent tissues. Am J Anat 1990;187:55–64.
   PubMedGoogle Scholar
• Kelly CD, Carter ND, de Boer P, et al. Detection of CAIII mRNA in rat skeletal muscle and liver by in situ hybridization. J Histochem Cytochem 1991;39:1243–7.
   PubMed Web of Science ®Google Scholar
• Shiels A, Jeffery S, Wilson C, Carter N. Radioimmunoassay of carbonic anhydrase III in rat tissues. Biochem J 1984;218:281–4.
   PubMed Web of Science ®Google Scholar
• Vaananen HK, Paloniemi M, Vuori J. Purification and localization of human carbonic anhydrase. III. Typing of skeletal muscle fibers in paraffin embedded sections. Histochemistry 1985;83:231–5.
   PubMedGoogle Scholar
• Zheng A, Rahkila P, Vuori J, et al. Quantification of carbonic anhydrase III and myoglobin in different fiber types of human psoas muscle. Histochemistry 1992;97:77–81.
   PubMedGoogle Scholar
• Jeffery S, Edwards Y, Carter N. Distribution of CAIII in fetal and adult human tissue. Biochem Genet 1980;18:843–9.
   PubMed Web of Science ®Google Scholar
• Kato K, Mokuno K. Distribution of immunoreactive carbonic anhydrase III in various human tissues determined by a sensitive enzyme immunoassay method. Clin Chim Acta 1984;141:169–77.
   PubMed Web of Science ®Google Scholar
• Raisanen SR, Lehenkari P, Tasanen M, et al. Carbonic anhydrase III protects cells from hydrogen peroxide-induced apoptosis. FASEB J 1999;13:513–22.
   PubMed Web of Science ®Google Scholar
• Chai YC, Jung CH, Lii CK, et al. Identification of an abundant S-thiolated rat liver protein as carbonic anhydrase III; characterization of S-thiolation and dethiolation reactions. Arch Biochem Biophys 1991;284:270–8.
   PubMed Web of Science ®Google Scholar
• Filomeni G, Rotilio G, Ciriolo MR. Disulfide relays and phosphorylative cascades: partners in redox-mediated signaling pathways. Cell Death Different 2005;12:1555–63.
   PubMed Web of Science ®Google Scholar
• Mallis RJ, Poland BW, Chatterjee TK, et al. Crystal structure of S-glutathiolated carbonic anhydrase III. FEBS Lett 2000;482:237–41.
   PubMed Web of Science ®Google Scholar
• Mari M, Morales A, Colell A, et al. Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 2009;11:2685–700.
   PubMed Web of Science ®Google Scholar
• Mari M, Colell A, Morales A, et al. Redox control of liver function in health and disease. Antioxid Redox Signal 2010;12:1295–331.
   PubMed Web of Science ®Google Scholar
• Mallis RJ, Hamann MJ, Zhao W, et al. Irreversible thiol oxidation in carbonic anhydrase III: protection by S-glutathiolation and detection in aging rats. Biol Chem 2002;383:649–62.
   PubMed Web of Science ®Google Scholar
• Thomas JA, Mallis RJ. Aging and oxidation of reactive protein sulfhydryls. Exp Gerontol 2001;36:1519–26.
   PubMed Web of Science ®Google Scholar
• Kim G, Lee TH, Wetzel P, et al. Carbonic anhydrase III is not required in the mouse for normal growth, development, and life span. Mol Cell Biol 2004;24:9942–7.
   PubMed Web of Science ®Google Scholar
• Morishita K, Parker DS, Mucenski ML, et al. Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines. Cell 1988;54:831–40.
   PubMed Web of Science ®Google Scholar
• Bartholomew C, Kilbey A, Clark AM, Walker M. The Evi-1 proto-oncogene encodes a transcriptional repressor activity associated with transformation. Oncogene 1997;14:569–77.
   PubMed Web of Science ®Google Scholar
• Wieser R. The oncogene and developmental regulator EVI1: expression, biochemical properties, and biological functions. Gene 2007;396:346–57.
   PubMed Web of Science ®Google Scholar
• Tweedie S, Morrison K, Charlton J, Edwards YH. CAIII a marker for early myogenesis: analysis of expression in cultured myogenic cells. Som Cell Mol Genet 1991;17:215–28.
   PubMedGoogle Scholar
• Nucifora G, Laricchia-Robbio L, Senyuk V. EVI1 and hematopoietic disorders: history and perspectives. Gene 2006;368:1–11.
   PubMed Web of Science ®Google Scholar
• Liu Y, Chen L, Ko TC, et al. Evi1 is a survival factor which conveys resistance to both TGFbeta- and taxol-mediated cell death via PI3K/AKT. Oncogene 2006;25:3565–75.
   PubMed Web of Science ®Google Scholar
• Kaila K, Lamsa K, Smirnov S, et al. Long-lasting GABA-mediated depolarization evoked by high-frequency stimulation in pyramidal neurons of rat hippocampal slice is attributable to a network-driven, bicarbonate-dependent K + transient. J Neurosci 1997;17:7662–72.
   PubMed Web of Science ®Google Scholar
• Ruusuvuori E, Huebner AK, Kirilkin I, et al. Neuronal carbonic anhydrase VII provides GABAergic excitatory drive to exacerbate febrile seizures. EMBO J 2013;32:2275–86.
   PubMed Web of Science ®Google Scholar
• Bootorabi F, Janis J, Smith E, et al. Analysis of a shortened form of human carbonic anhydrase VII expressed in vitro compared to the full-length enzyme. Biochimie 2010;92:1072–80.
   PubMed Web of Science ®Google Scholar
• Shah GN, Hewett-Emmett D, Grubb JH, et al. Mitochondrial carbonic anhydrase CA VB: differences in tissue distribution and pattern of evolution from those of CA VA suggest distinct physiological roles. Proc Natl Acad Sci USA 2000;97:1677–82.
   PubMed Web of Science ®Google Scholar
• Parkkila S, Kivela AJ, Kaunisto K, et al. The plasma membrane carbonic anhydrase in murine hepatocytes identified as isozyme XIV. BMC Gastroenterol 2002;2:13.
   PubMedGoogle Scholar
• Bootorabi F, Haapasalo J, Smith E, et al. Carbonic anhydrase VII – a potential prognostic marker in gliomas. Health 2011;3:6–12.
   Google Scholar
• Yang GZ, Hu L, Cai J, et al. Prognostic value of carbonic anhydrase VII expression in colorectal carcinoma. BMC Cancer 2015;15:209.
   PubMed Web of Science ®Google Scholar
• Birkenkamp-Demtroder K, Olesen SH, Sorensen FB, et al. Differential gene expression in colon cancer of the caecum versus the sigmoid and rectosigmoid. Gut 2005;54:374–84.
   PubMed Web of Science ®Google Scholar
• Chu CM, Yao CT, Chang YT, et al. Gene expression profiling of colorectal tumors and normal mucosa by microarrays meta-analysis using prediction analysis of microarray, artificial neural network, classification, and regression trees. Dis Mark 2014;2014:634123.
   PubMed Web of Science ®Google Scholar
• Sosa V, Moline T, Somoza R, et al. Oxidative stress and cancer: an overview. Ageing Res Rev 2013;12:376–90.
   PubMed Web of Science ®Google Scholar
• Fang J, Seki T, Maeda H. Therapeutic strategies by modulating oxygen stress in cancer and inflammation. Adv Drug Deliv Rev 2009;61:290–302.
   PubMed Web of Science ®Google Scholar
• Perse M. Oxidative stress in the pathogenesis of colorectal cancer: cause or consequence? Biomed Res Int 2013;2013:725710.
   PubMed Web of Science ®Google Scholar
• Stone WL, Krishnan K, Campbell SE, Palau VE. The role of antioxidants and pro-oxidants in colon cancer. World J Gastrointest Oncol 2014;6:55–66.
   PubMed Web of Science ®Google Scholar
• Duda DM, Tu C, Fisher SZ, et al. Human carbonic anhydrase III: structural and kinetic study of catalysis and proton transfer. Biochemistry 2005;44:10046–53.
   PubMed Web of Science ®Google Scholar
• Elder I, Fisher Z, Laipis PJ, et al. Structural and kinetic analysis of proton shuttle residues in the active site of human carbonic anhydrase III. Proteins 2007;68:337–43.
   PubMed Web of Science ®Google Scholar
• Kannan KK, Ramanadham M, Jones TA. Structure, refinement, and function of carbonic anhydrase isozymes: refinement of human carbonic anhydrase I. Ann N Y Acad Sci 1984;429:49–60.
   PubMed Web of Science ®Google Scholar
• Eriksson AE, Jones TA, Liljas A. Refined structure of human carbonic anhydrase II at 2.0 A resolution. Proteins 1988;4:274–82.
   PubMed Web of Science ®Google Scholar
• Stams T, Nair SK, Okuyama T, et al. Crystal structure of the secretory form of membrane-associated human carbonic anhydrase IV at 2.8-A resolution. Proc Natl Acad Sci USA 1996;93:13589–94.
   PubMed Web of Science ®Google Scholar
• Boriack-Sjodin PA, Heck RW, Laipis PJ, et al. Structure determination of murine mitochondrial carbonic anhydrase V at 2.45-A resolution: implications for catalytic proton transfer and inhibitor design. Proc Natl Acad Sci USA 1995;92:10949–53.
   PubMed Web of Science ®Google Scholar
• Pilka ES, Kochan G, Oppermann U, Yue WW. Crystal structure of the secretory isozyme of mammalian carbonic anhydrases CA VI: implications for biological assembly and inhibitor development. Biochem Biophys Res Commun 2012;419:485–9.
   PubMed Web of Science ®Google Scholar
• Alterio V, Hilvo M, Di Fiore A, et al. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc Natl Acad Sci USA 2009;106:16233–8.
   PubMed Web of Science ®Google Scholar
• Whittington DA, Waheed A, Ulmasov B, et al. Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Proc Natl Acad Sci USA 2001;98:9545–50.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, Monti SM, Hilvo M, et al. Crystal structure of human carbonic anhydrase XIII and its complex with the inhibitor acetazolamide. Proteins 2009;74:164–75.
   PubMed Web of Science ®Google Scholar
• Whittington DA, Grubb JH, Waheed A, et al. Expression, assay, and structure of the extracellular domain of murine carbonic anhydrase XIV: implications for selective inhibition of membrane-associated isozymes. J Biol Chem 2004;279:7223–8.
   PubMed Web of Science ®Google Scholar
• Mikulski RL, Silverman DN. Proton transfer in catalysis and the role of proton shuttles in carbonic anhydrase. Biochim Biophys Acta 2010;1804:422–6.
   PubMed Web of Science ®Google Scholar
• Silverman DN, McKenna R. Solvent-mediated proton transfer in catalysis by carbonic anhydrase. Acc Chem Res 2007;40:669–75.
   PubMed Web of Science ®Google Scholar
• LoGrasso PV, Tu C, Chen X, et al. Influence of amino acid replacement at position 198 on catalytic properties of zinc-bound water in human carbonic anhydrase III. Biochemistry 1993;32:5786–91.
   PubMed Web of Science ®Google Scholar
• Cabiscol E, Levine RL. The phosphatase activity of carbonic anhydrase III is reversibly regulated by glutathiolation. Proc Natl Acad Sci USA 1996;93:4170–4.
   PubMed Web of Science ®Google Scholar
• Ji Y, Akerboom TP, Sies H, Thomas JA. Gel electrofocusing method for studying protein S-nitrosylation. Meth Enzymol 1999;301:145–51.
   PubMed Web of Science ®Google Scholar
• Kim G, Levine RL. Molecular determinants of S-glutathionylation of carbonic anhydrase 3. Antioxid Redox Signal 2005;7:849–54.
   PubMed Web of Science ®Google Scholar
• Domsic JF, Avvaru BS, Kim CU, et al. Entrapment of carbon dioxide in the active site of carbonic anhydrase II. J Biol Chem 2008;283:30766–71.
   PubMed Web of Science ®Google Scholar
• Fisher SZ, Maupin CM, Budayova-Spano M, et al. Atomic crystal and molecular dynamics simulation structures of human carbonic anhydrase II: insights into the proton transfer mechanism. Biochemistry 2007;46:2930–7.
   PubMed Web of Science ®Google Scholar
• Roy A, Taraphder S. Identification of proton-transfer pathways in human carbonic anhydrase II. J Phys Chem B 2007;111:10563–76.
   PubMed Web of Science ®Google Scholar
• Alterio V, Di Fiore A, D’Ambrosio K, et al. X-ray crystallography of carbonic anhydrase inhibitors and its importance in drug design. In: Supuran CT, Winum J-Y, eds. Design of zinc-enzyme inhibitors: functional, structural, and disease applications. Hoboken (NJ): Wiley; 2009:73–138.
   Google Scholar
• Kadokura H, Katzen F, Beckwith J. Protein disulfide bond formation in prokaryotes. Ann Rev Biochem 2003;72:111–35.
   PubMed Web of Science ®Google Scholar
• Sievers F, Wilm A, Dineen D, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011;7:539.
   PubMed Web of Science ®Google Scholar