Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Experimental Approaches to Identify Selective Picomolar Inhibitors for Carbonic Anhydrase IX

Author(s): Justina Kazokaitė-Adomaitienė*, Holger M. Becker, Joana Smirnovienė, Ludwig J. Dubois and Daumantas Matulis

Volume 28, Issue 17, 2021

Published on: 02 November, 2020

Page: [3361 - 3384] Pages: 24

DOI: 10.2174/0929867327666201102112841

Price: $65

Abstract

Background: Carbonic anhydrases (CAs) regulate pH homeostasis via the reversible hydration of CO2, thereby emerging as essential enzymes for many vital functions. Among 12 catalytically active CA isoforms in humans, CA IX has become a relevant therapeutic target because of its role in cancer progression. Only two CA IX inhibitors have entered clinical trials, mostly due to low affinity and selectivity properties.

Objective: The current review presents the design, development, and identification of the selective nano- to picomolar CA IX inhibitors VD11-4-2, VR16-09, and VD12-09.

Methods and Results: Compounds were selected from our database, composed of over 400 benzensulfonamides, synthesized at our laboratory, and tested for their binding to 12 human CAs. Here we discuss the CA CO2 hydratase activity/inhibition assay and several biophysical techniques, such as fluorescent thermal shift assay and isothermal titration calorimetry, highlighting their contribution to the analysis of compound affinity and structure- activity relationships. To obtain sufficient amounts of recombinant CAs for inhibitor screening, several gene cloning and protein purification strategies are presented, including site-directed CA mutants, heterologous CAs from Xenopus oocytes, and native endogenous CAs. The cancer cell-based methods, such as clonogenicity, extracellular acidification, and mass spectrometric gas-analysis are reviewed, confirming nanomolar activities of lead inhibitors in intact cancer cells.

Conclusions: Novel CA IX inhibitors are promising derivatives for in vivo explorations. Furthermore, the simultaneous targeting of several proteins involved in proton flux upon tumor acidosis and the disruption of transport metabolons might improve cancer management.

Keywords: Drug development, organic chemistry, cancer, sulfonamide, thermal shift assay, isothermal titration calorimetry, CA IX.

« Previous Next »
[1]
Verma, S.; Prabhakar, Y.S. Target based drug design - a reality in virtual sphere. Curr. Med. Chem., 2015, 22(13), 1603-1630.
[http://dx.doi.org/10.2174/0929867322666150209151209] [PMID: 25666805]
[2]
Viayna, E.; Sola, I.; Di Pietro, O.; Muñoz-Torrero, D. Human disease and drug pharmacology, complex as real life. Curr. Med. Chem., 2013, 20(13), 1623-1634.
[http://dx.doi.org/10.2174/0929867311320130002] [PMID: 23410162]
[3]
Meldrum, N.U.; Roughton, F.J.W. Carbonic anhydrase. Its preparation and properties. J. Physiol., 1933, 80(2), 113-142.
[http://dx.doi.org/10.1113/jphysiol.1933.sp003077] [PMID: 16994489]
[4]
Del Prete, S.; Vullo, D.; De Luca, V.; Supuran, C.T.; Capasso, C. Biochemical characterization of the δ-carbonic anhydrase from the marine diatom Thalassiosira weissflogii , TweCA. J. Enzyme Inhib. Med. Chem., 2014, 29(6), 906-911.
[http://dx.doi.org/10.3109/14756366.2013.868599] [PMID: 24456295]
[5]
Samukawa, M.; Shen, C.; Hopkinson, B.M.; Matsuda, Y. Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana . Photosynth. Res., 2014, 121(2-3), 235-249.
[http://dx.doi.org/10.1007/s11120-014-9967-x] [PMID: 24414291]
[6]
Kikutani, S.; Nakajima, K.; Nagasato, C.; Tsuji, Y.; Miyatake, A.; Matsuda, Y. Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum . Proc. Natl. Acad. Sci. USA, 2016, 113(35), 9828-9833.
[http://dx.doi.org/10.1073/pnas.1603112113] [PMID: 27531955]
[7]
Zolfaghari Emameh, R.; Barker, H.R.; Syrjänen, L.; Urbański, L.; Supuran, C.T.; Parkkila, S. Identification and inhibition of carbonic anhydrases from nematodes. J. Enzyme Inhib. Med. Chem., 2016, 31(sup4), 176-184.
[http://dx.doi.org/10.1080/14756366.2016.1221826] [PMID: 27557594]
[8]
Zolfaghari Emameh, R.; Barker, H.R.; Tolvanen, M.E.E.; Parkkila, S.; Hytönen, V.P. Horizontal transfer of β-carbonic anhydrase genes from prokaryotes to protozoans, insects, and nematodes. Parasit. Vectors, 2016, 9, 152.
[http://dx.doi.org/10.1186/s13071-016-1415-7] [PMID: 26983858]
[9]
Frost, S.C. Physiological functions of the alpha class of carbonic anhydrases. Subcell. Biochem., 2014, 75, 9-30.
[http://dx.doi.org/10.1007/978-94-007-7359-2_2] [PMID: 24146372]
[10]
Kuo, W-H.; Yang, S-F.; Hsieh, Y-S.; Tsai, C-S.; Hwang, W-L.; Chu, S-C. Differential expression of carbonic anhydrase isoenzymes in various types of anemia. Clin. Chim. Acta, 2005, 351(1-2), 79-86.
[http://dx.doi.org/10.1016/j.cccn.2004.07.009] [PMID: 15563874]
[11]
Gao, B-B.; Clermont, A.; Rook, S.; Fonda, S.J.; Srinivasan, V.J.; Wojtkowski, M.; Fujimoto, J.G.; Avery, R.L.; Arrigg, P.G.; Bursell, S-E.; Aiello, L.P.; Feener, E.P. Extracellular carbonic anhydrase mediates hemorrhagic retinal and cerebral vascular permeability through prekallikrein activation. Nat. Med., 2007, 13(2), 181-188.
[http://dx.doi.org/10.1038/nm1534] [PMID: 17259996]
[12]
Chang, X.; Zheng, Y.; Yang, Q.; Wang, L.; Pan, J.; Xia, Y.; Yan, X.; Han, J. Carbonic anhydrase I (CA1) is involved in the process of bone formation and is susceptible to ankylosing spondylitis. Arthritis Res. Ther., 2012, 14(4), R176.
[http://dx.doi.org/10.1186/ar3929] [PMID: 22838845]
[13]
Takakura, M.; Yokomizo, A.; Tanaka, Y.; Kobayashi, M.; Jung, G.; Banno, M.; Sakuma, T.; Imada, K.; Oda, Y.; Kamita, M.; Honda, K.; Yamada, T.; Naito, S.; Ono, M. Carbonic anhydrase I as a new plasma biomarker for prostate cancer. ISRN Oncol., 2012, 2012, 768190.
[http://dx.doi.org/10.5402/2012/768190] [PMID: 23213568]
[14]
Mincione, F.; Starnotti, M.; Masini, E.; Bacciottini, L.; Scrivanti, C.; Casini, A.; Vullo, D.; Scozzafava, A.; Supuran, C.T. Carbonic anhydrase inhibitors: design of thioureido sulfonamides with potent isozyme II and XII inhibitory properties and intraocular pressure lowering activity in a rabbit model of glaucoma. Bioorg. Med. Chem. Lett., 2005, 15(17), 3821-3827.
[http://dx.doi.org/10.1016/j.bmcl.2005.06.054] [PMID: 16039853]
[15]
Lönnerholm, G.; Wistrand, P.J.; Bárány, E. Carbonic anhydrase isoenzymes in the rat kidney. Effects of chronic acetazolamide treatment. Acta Physiol. Scand., 1986, 126(1), 51-60.
[http://dx.doi.org/10.1111/j.1748-1716.1986.tb07788.x] [PMID: 3082105]
[16]
Thiry, A.; Dogné, J-M.; Supuran, C.T.; Masereel, B. Anticonvulsant sulfonamides/sulfamates/sulfamides with carbonic anhydrase inhibitory activity: drug design and mechanism of action. Curr. Pharm. Des., 2008, 14(7), 661-671.
[http://dx.doi.org/10.2174/138161208783877956] [PMID: 18336312]
[17]
Oksala, N.; Levula, M.; Pelto-Huikko, M.; Kytömäki, L.; Soini, J.T.; Salenius, J.; Kähönen, M.; Karhunen, P.J.; Laaksonen, R.; Parkkila, S.; Lehtimäki, T. Carbonic anhydrases II and XII are up-regulated in osteoclast-like cells in advanced human atherosclerotic plaques-Tampere Vascular Study. Ann. Med., 2010, 42(5), 360-370.
[http://dx.doi.org/10.3109/07853890.2010.486408] [PMID: 20509747]
[18]
Kenny, A.D. Role of carbonic anhydrase in bone: plasma acetazolamide concentrations associated with inhibition of bone loss. Pharmacology, 1985, 31(2), 97-107.
[http://dx.doi.org/10.1159/000138104] [PMID: 3927329]
[19]
Parkkila, S.; Lasota, J.; Fletcher, J.A.; Ou, W.B.; Kivelä, A.J.; Nuorva, K.; Parkkila, A-K.; Ollikainen, J.; Sly, W.S.; Waheed, A.; Pastorekova, S.; Pastorek, J.; Isola, J.; Miettinen, M. Carbonic anhydrase II. A novel biomarker for gastrointestinal stromal tumors. Mod. Pathol., 2010, 23(5), 743-750.
[http://dx.doi.org/10.1038/modpathol.2009.189] [PMID: 20081808]
[20]
Hynninen, P.; Parkkila, S.; Huhtala, H.; Pastorekova, S.; Pastorek, J.; Waheed, A.; Sly, W.S.; Tomas, E. Carbonic anhydrase isozymes II, IX, and XII in uterine tumors. APMIS, 2012, 120(2), 117-129.
[http://dx.doi.org/10.1111/j.1600-0463.2011.02820.x] [PMID: 22229267]
[21]
Heath, R.; Schwartz, M.S.; Brown, I.R.; Carter, N.D. Carbonic anhydrase III in neuromuscular disorders. J. Neurol. Sci., 1983, 59(3), 383-388.
[http://dx.doi.org/10.1016/0022-510X(83)90023-0] [PMID: 6410007]
[22]
Mitterberger, M.C.; Kim, G.; Rostek, U.; Levine, R.L.; Zwerschke, W. Carbonic anhydrase III regulates peroxisome proliferator-activated receptor-γ2. Exp. Cell Res., 2012, 318(8), 877-886.
[http://dx.doi.org/10.1016/j.yexcr.2012.02.011] [PMID: 22507175]
[23]
Rebello, G.; Ramesar, R.; Vorster, A.; Roberts, L.; Ehrenreich, L.; Oppon, E.; Gama, D.; Bardien, S.; Greenberg, J.; Bonapace, G.; Waheed, A.; Shah, G.N.; Sly, W.S. Apoptosis-inducing signal sequence mutation in carbonic anhydrase IV identified in patients with the RP17 form of retinitis pigmentosa. Proc. Natl. Acad. Sci. USA, 2004, 101(17), 6617-6622.
[http://dx.doi.org/10.1073/pnas.0401529101] [PMID: 15090652]
[24]
Datta, R.; Shah, G.N.; Rubbelke, T.S.; Waheed, A.; Rauchman, M.; Goodman, A.G.; Katze, M.G.; Sly, W.S. Progressive renal injury from transgenic expression of human carbonic anhydrase IV folding mutants is enhanced by deficiency of p58IPK. Proc. Natl. Acad. Sci. USA, 2010, 107(14), 6448-6452.
[http://dx.doi.org/10.1073/pnas.1001905107] [PMID: 20308551]
[25]
Scozzafava, A.; Supuran, C.T.; Carta, F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin. Ther. Pat., 2013, 23(6), 725-735.
[http://dx.doi.org/10.1517/13543776.2013.790957] [PMID: 23607332]
[26]
Parkkila, A-K.; Scarim, A.L.; Parkkila, S.; Waheed, A.; Corbett, J.A.; Sly, W.S. Expression of carbonic anhydrase V in pancreatic beta cells suggests role for mitochondrial carbonic anhydrase in insulin secretion. J. Biol. Chem., 1998, 273(38), 24620-24623.
[http://dx.doi.org/10.1074/jbc.273.38.24620] [PMID: 9733757]
[27]
Price, T.O.; Eranki, V.; Banks, W.A.; Ercal, N.; Shah, G.N. Topiramate treatment protects blood-brain barrier pericytes from hyperglycemia-induced oxidative damage in diabetic mice. Endocrinology, 2012, 153(1), 362-372.
[http://dx.doi.org/10.1210/en.2011-1638] [PMID: 22109883]
[28]
Imtaiyaz Hassan, M.; Shajee, B.; Waheed, A.; Ahmad, F.; Sly, W.S. Structure, function and applications of carbonic anhydrase isozymes. Bioorg. Med. Chem., 2013, 21(6), 1570-1582.
[http://dx.doi.org/10.1016/j.bmc.2012.04.044] [PMID: 22607884]
[29]
Thiry, A.; Dogné, J-M.; Supuran, C.T.; Masereel, B. Carbonic anhydrase inhibitors as anticonvulsant agents. Curr. Top. Med. Chem., 2007, 7(9), 855-864.
[http://dx.doi.org/10.2174/156802607780636726] [PMID: 17504130]
[30]
Asiedu, M.; Ossipov, M.H.; Kaila, K.; Price, T.J. Acetazolamide and midazolam act synergistically to inhibit neuropathic pain. Pain, 2010, 148(2), 302-308.
[http://dx.doi.org/10.1016/j.pain.2009.11.015] [PMID: 20007010]
[31]
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.
[http://dx.doi.org/10.1016/j.semcancer.2014.08.002] [PMID: 25117006]
[32]
Mboge, M.Y.; Mahon, B.P.; McKenna, R.; Frost, S.C. Carbonic anhydrases: role in pH control and cancer. Metabolites, 2018, 8(1), 19.
[http://dx.doi.org/10.3390/metabo8010019] [PMID: 29495652]
[33]
Kummola, L.; Hämäläinen, J.M.; Kivelä, J.; Kivelä, A.J.; Saarnio, J.; Karttunen, T.; Parkkila, S. Expression of a novel carbonic anhydrase, CA XIII, in normal and neoplastic colorectal mucosa. BMC Cancer, 2005, 5, 41.
[http://dx.doi.org/10.1186/1471-2407-5-41] [PMID: 15836783]
[34]
Vargas, L.A.; Alvarez, B.V. Carbonic anhydrase XIV in the normal and hypertrophic myocardium. J. Mol. Cell. Cardiol., 2012, 52(3), 741-752.
[http://dx.doi.org/10.1016/j.yjmcc.2011.12.008] [PMID: 22227327]
[35]
Aggarwal, M.; Boone, C.D.; Kondeti, B.; McKenna, R. Structural annotation of human carbonic anhydrases. J. Enzyme Inhib. Med. Chem., 2013, 28(2), 267-277.
[http://dx.doi.org/10.3109/14756366.2012.737323] [PMID: 23137351]
[36]
Kazokaitė, J.; Niemans, R.; Dudutienė, V.; Becker, H.M.; Leitāns, J.; Zubrienė, A.; Baranauskienė, L.; Gondi, G.; Zeidler, R.; Matulienė, J.; Tārs, K.; Yaromina, A.; Lambin, P.; Dubois, L.J.; Matulis, D. Novel fluorinated carbonic anhydrase IX inhibitors reduce hypoxia-induced acidification and clonogenic survival of cancer cells. Oncotarget, 2018, 9(42), 26800-26816.
[http://dx.doi.org/10.18632/oncotarget.25508] [PMID: 29928486]
[37]
Dudutienė, V.; Matulienė, J.; Smirnov, A.; Timm, D.D.; Zubrienė, A.; Baranauskienė, L.; Morkūnaite, V.; Smirnovienė, J.; Michailovienė, V.; Juozapaitienė, V.; Mickevičiūtė, A.; Kazokaitė, J.; Bakšytė, S.; Kasiliauskaitė, A.; Jachno, J.; Revuckienė, J.; Kišonaitė, M.; Pilipuitytė, V.; Ivanauskaitė, E.; Milinavičiūtė, G.; Smirnovas, V.; Petrikaitė, V.; Kairys, V.; Petrauskas, V.; Norvaišas, P.; Lingė, D.; Gibieža, P.; Capkauskaitė, E.; Zakšauskas, A.; Kazlauskas, E.; Manakova, E.; Gražulis, S.; Ladbury, J.E.; Matulis, D. Discovery and characterization of novel selective inhibitors of carbonic anhydrase IX. J. Med. Chem., 2014, 57(22), 9435-9446.
[http://dx.doi.org/10.1021/jm501003k] [PMID: 25358084]
[38]
Linkuvienė, V.; Zubrienė, A.; Manakova, E.; Petrauskas, V.; Baranauskienė, L.; Zakšauskas, A.; Smirnov, A.; Gražulis, S.; Ladbury, J.E.; Matulis, D. Thermodynamic, kinetic, and structural parameterization of human carbonic anhydrase interactions toward enhanced inhibitor design. Q. Rev. Biophys., 2018, 51, e10.
[http://dx.doi.org/10.1017/S0033583518000082] [PMID: 30912486]
[39]
Dudutienė, V.; Zubrienė, A.; Smirnov, A.; Gylytė, J.; Timm, D.; Manakova, E.; Gražulis, S.; Matulis, D. 4-Substituted-2,3,5,6-tetrafluorobenzenesulfonamides as inhibitors of carbonic anhydrases I, II, VII, XII, and XIII. Bioorg. Med. Chem., 2013, 21(7), 2093-2106.
[http://dx.doi.org/10.1016/j.bmc.2013.01.008] [PMID: 23394791]
[40]
Cimmperman, P.; Baranauskienė, L.; Jachimoviciūte, S.; Jachno, J.; Torresan, J.; Michailovienė, V.; Matulienė, J.; Sereikaitė, J.; Bumelis, V.; Matulis, D. A quantitative model of thermal stabilization and destabilization of proteins by ligands. Biophys. J., 2008, 95(7), 3222-3231.
[http://dx.doi.org/10.1529/biophysj.108.134973] [PMID: 18599640]
[41]
Morrison, J.F. Kinetics of the reversible inhibition of enzyme-catalysed reactions by tight-binding inhibitors. Biochim. Biophys. Acta, 1969, 185(2), 269-286.
[http://dx.doi.org/10.1016/0005-2744(69)90420-3] [PMID: 4980133]
[42]
Williams, J.W.; Morrison, J.F. The kinetics of reversible tight-binding inhibition. Meth. Enzymol., 1979, 63, 437-467.
[http://dx.doi.org/10.1016/0076-6879(79)63019-7] [PMID: 502865]
[43]
Pantoliano, M.W.; Petrella, E.C.; Kwasnoski, J.D.; Lobanov, V.S.; Myslik, J.; Graf, E.; Carver, T.; Asel, E.; Springer, B.A.; Lane, P.; Salemme, F.R. High-density miniaturized thermal shift assays as a general strategy for drug discovery. J. Biomol. Screen., 2001, 6(6), 429-440.
[http://dx.doi.org/10.1177/108705710100600609] [PMID: 11788061]
[44]
Abbott, J.A.; Livingston, N.M.; Egri, S.B.; Guth, E.; Francklyn, C.S. Characterization of aminoacyl-tRNA synthetase stability and substrate interaction by differential scanning fluorimetry. Methods, 2017, 113, 64-71.
[http://dx.doi.org/10.1016/j.ymeth.2016.10.013] [PMID: 27794454]
[45]
Lo, M-C.; Aulabaugh, A.; Jin, G.; Cowling, R.; Bard, J.; Malamas, M.; Ellestad, G. Evaluation of fluorescence-based thermal shift assays for hit identification in drug discovery. Anal. Biochem., 2004, 332(1), 153-159.
[http://dx.doi.org/10.1016/j.ab.2004.04.031] [PMID: 15301960]
[46]
Niesen, F.H.; Berglund, H.; Vedadi, M. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc., 2007, 2(9), 2212-2221.
[http://dx.doi.org/10.1038/nprot.2007.321] [PMID: 17853878]
[47]
Lavinder, J.J.; Hari, S.B.; Sullivan, B.J.; Magliery, T.J. High-throughput thermal scanning: a general, rapid dye-binding thermal shift screen for protein engineering. J. Am. Chem. Soc., 2009, 131(11), 3794-3795.
[http://dx.doi.org/10.1021/ja8049063] [PMID: 19292479]
[48]
Matulis, D.; Kranz, J.K.; Salemme, F.R.; Todd, M.J. Thermodynamic stability of carbonic anhydrase: measurements of binding affinity and stoichiometry using ThermoFluor. Biochemistry, 2005, 44(13), 5258-5266.
[http://dx.doi.org/10.1021/bi048135v] [PMID: 15794662]
[49]
Petrauskas, V.; Zubrienė, A.; Todd, M.J.; Matulis, D. Inhibitor binding to carbonic anhydrases by fluorescent thermal shift assay. In: Carbonic Anhydrase as Drug Target: Thermodynamics and Structure of Inhibitor Binding; Matulis, D., Ed.; Springer International Publishing: Cham, 2019; pp. 63-78.
[http://dx.doi.org/10.1007/978-3-030-12780-0_5]
[50]
Matulis, D.; Lovrien, R. 1-Anilino-8-naphthalene sulfonate anion-protein binding depends primarily on ion pair formation. Biophys. J., 1998, 74(1), 422-429.
[http://dx.doi.org/10.1016/S0006-3495(98)77799-9] [PMID: 9449342]
[51]
Matulis, D.; Baumann, C.G.; Bloomfield, V.A.; Lovrien, R.E. 1-anilino-8-naphthalene sulfonate as a protein conformational tightening agent. Biopolymers, 1999, 49(6), 451-458.
[http://dx.doi.org/10.1002/(SICI)1097-0282(199905)49:6<451::AID-BIP3>3.0.CO;2-6] [PMID: 10193192]
[52]
Jogaitė, V.; Zubrienė, A.; Michailovienė, V.; Gylytė, J.; Morkūnaitė, V.; Matulis, D. Characterization of human carbonic anhydrase XII stability and inhibitor binding. Bioorg. Med. Chem., 2013, 21(6), 1431-1436.
[http://dx.doi.org/10.1016/j.bmc.2012.10.016] [PMID: 23159038]
[53]
Kasiliauskaitė, A.; Časaitė, V.; Juozapaitienė, V.; Zubrienė, A.; Michailovienė, V.; Revuckienė, J.; Baranauskienė, L.; Meškys, R.; Matulis, D. Thermodynamic characterization of human carbonic anhydrase VB stability and intrinsic binding of compounds. J. Therm. Anal. Calorim., 2016, 123, 2191-2200.
[http://dx.doi.org/10.1007/s10973-015-5073-3]
[54]
Kazokaitė, J.; Milinavičiūtė, G.; Smirnovienė, J.; Matulienė, J.; Matulis, D. Intrinsic binding of 4-substituted-2,3,5,6-tetrafluorobenezenesulfonamides to native and recombinant human carbonic anhydrase VI. FEBS J., 2015, 282(5), 972-983.
[http://dx.doi.org/10.1111/febs.13196] [PMID: 25586768]
[55]
Linkuvienė, V.; Matulienė, J.; Juozapaitienė, V.; Michailovienė, V.; Jachno, J.; Matulis, D. Intrinsic thermodynamics of inhibitor binding to human carbonic anhydrase IX. Biochim. Biophys. Acta, 2016, 1860(4), 708-718.
[http://dx.doi.org/10.1016/j.bbagen.2016.01.007] [PMID: 26794023]
[56]
Mickevičiūtė, A.; Timm, D.D.; Gedgaudas, M.; Linkuvienė, V.; Chen, Z.; Waheed, A.; Michailovienė, V.; Zubrienė, A.; Smirnov, A.; Čapkauskaitė, E.; Baranauskienė, L.; Jachno, J.; Revuckienė, J.; Manakova, E.; Gražulis, S.; Matulienė, J.; Di Cera, E.; Sly, W.S.; Matulis, D. Intrinsic thermodynamics of high affinity inhibitor binding to recombinant human carbonic anhydrase IV. Eur. Biophys. J., 2018, 47(3), 271-290.
[http://dx.doi.org/10.1007/s00249-017-1256-0] [PMID: 28975383]
[57]
Zubrienė, A.; Matulis, D. Characterization of carbonic anhydrase thermal stability. In: Carbonic anhydrase as drug target: thermodynamics and structure of inhibitor binding; Matulis, D., Ed.; Springer International Publishing: Cham, 2019; pp. 51-59.
[http://dx.doi.org/10.1007/978-3-030-12780-0_4]
[58]
Chance, B. The reactions of catalase in the presence of the notatin system. Biochem. J., 1950, 46(4), 387-402.
[http://dx.doi.org/10.1042/bj0460387] [PMID: 15420164]
[59]
Earnhardt, J.N.; Qian, M.; Tu, C.; Lakkis, M.M.; Bergenhem, N.C.H.; Laipis, P.J.; Tashian, R.E.; Silverman, D.N. The catalytic properties of murine carbonic anhydrase VII. Biochemistry, 1998, 37(30), 10837-10845.
[http://dx.doi.org/10.1021/bi980046t] [PMID: 9692974]
[60]
Gibbons, B.H.; Edsall, J.T. Kinetic studies of human carbonic anhydrases B and C. J. Biol. Chem., 1964, 239, 2539-2544.
[http://dx.doi.org/10.1016/S0021-9258(18)93884-6] [PMID: 14235532]
[61]
Heck, R.W.; Boriack-Sjodin, P.A.; Qian, M.; Tu, C.; Christianson, D.W.; Laipis, P.J.; Silverman, D.N. Structure-based design of an intramolecular proton transfer site in murine carbonic anhydrase V. Biochemistry, 1996, 35(36), 11605-11611.
[http://dx.doi.org/10.1021/bi9608018] [PMID: 8794740]
[62]
Hurt, J.D.; Tu, C.; Laipis, P.J.; Silverman, D.N. Catalytic properties of murine carbonic anhydrase IV. J. Biol. Chem., 1997, 272(21), 13512-13518.
[http://dx.doi.org/10.1074/jbc.272.21.13512] [PMID: 9153196]
[63]
Jewell, D.A.; Tu, C.K.; Paranawithana, S.R.; Tanhauser, S.M.; LoGrasso, P.V.; Laipis, P.J.; Silverman, D.N. Enhancement of the catalytic properties of human carbonic anhydrase III by site-directed mutagenesis. Biochemistry, 1991, 30(6), 1484-1490.
[http://dx.doi.org/10.1021/bi00220a006] [PMID: 1899618]
[64]
Juozapaitienė, V.; Bartkutė, B.; Michailovienė, V.; Zakšauskas, A.; Baranauskienė, L.; Satkūnė, S.; Matulis, D. Purification, enzymatic activity and inhibitor discovery for recombinant human carbonic anhydrase XIV. J. Biotechnol., 2016, 240, 31-42.
[http://dx.doi.org/10.1016/j.jbiotec.2016.10.018] [PMID: 27773757]
[65]
Kernohan, J.C. A method for studying the kinetics of the inhibition of carbonic anhydrase by sulphonamides. Biochim. Biophys. Acta, 1966, 118(2), 405-412.
[http://dx.doi.org/10.1016/S0926-6593(66)80049-8] [PMID: 4960175]
[66]
Kernohan, J.C. The pH-activity curve of bovine carbonic anhydrase and its relationship to the inhibition of the enzyme by anions. Biochimica et Biophysica Acta (BBA)-. Biochim. Biophys. Acta, 1965, 96, 304-317.
[PMID: 14298834]
[67]
Khalifah, R.G. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J. Biol. Chem., 1971, 246(8), 2561-2573.
[http://dx.doi.org/10.1016/S0021-9258(18)62326-9] [PMID: 4994926]
[68]
Smirnovienė, J.; Smirnovas, V.; Matulis, D. Picomolar inhibitors of carbonic anhydrase: Importance of inhibition and binding assays. Anal. Biochem., 2017, 522, 61-72.
[http://dx.doi.org/10.1016/j.ab.2017.01.022] [PMID: 28153585]
[69]
Ulmasov, B.; Waheed, A.; Shah, G.N.; Grubb, J.H.; Sly, W.S.; Tu, C.; Silverman, D.N. Purification and kinetic analysis of recombinant CA XII, a membrane carbonic anhydrase overexpressed in certain cancers. Proc. Natl. Acad. Sci. USA, 2000, 97(26), 14212-14217.
[http://dx.doi.org/10.1073/pnas.97.26.14212] [PMID: 11121027]
[70]
Kazokaitė, J.; Kairys, V.; Smirnovienė, J.; Smirnov, A.; Manakova, E.; Tolvanen, M.; Parkkila, S.; Matulis, D. Engineered carbonic anhydrase VI-mimic enzyme switched the structure and affinities of inhibitors. Sci. Rep., 2019, 9(1), 12710.
[http://dx.doi.org/10.1038/s41598-019-49094-0] [PMID: 31481705]
[71]
Gibbons, B.H.; Edsall, J.T. Rate of hydration of carbon dioxide and dehydration of carbonic acid at 25 degrees. J. Biol. Chem., 1963, 238, 3502-3507.
[http://dx.doi.org/10.1016/S0021-9258(18)48696-6] [PMID: 14085409]
[72]
Kuzmic, P.; Elrod, K.C.; Cregar, L.M.; Sideris, S.; Rai, R.; Janc, J.W. High-throughput screening of enzyme inhibitors: simultaneous determination of tight-binding inhibition constants and enzyme concentration. Anal. Biochem., 2000, 286(1), 45-50.
[http://dx.doi.org/10.1006/abio.2000.4685] [PMID: 11038272]
[73]
Murphy, D.J. Determination of accurate KI values for tight-binding enzyme inhibitors: an in silico study of experimental error and assay design. Anal. Biochem., 2004, 327(1), 61-67.
[http://dx.doi.org/10.1016/j.ab.2003.12.018] [PMID: 15033511]
[74]
Copeland. R.A. In: Evaluation of Enzyme Inhibitors in Drug Discovery: A Guide for Medicinal Chemists and Pharmacologists, Second Edition; John Wiley & Sons, Inc., 2013.
[http://dx.doi.org/10.1002/9781118540398]
[75]
de Azevedo, W.F., Jr; Dias, R. Experimental approaches to evaluate the thermodynamics of protein-drug interactions. Curr. Drug Targets, 2008, 9(12), 1071-1076.
[http://dx.doi.org/10.2174/138945008786949441] [PMID: 19128217]
[76]
Baker, B.M.; Murphy, K.P. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys. J., 1996, 71(4), 2049-2055.
[http://dx.doi.org/10.1016/S0006-3495(96)79403-1] [PMID: 8889179]
[77]
Leavitt, S.; Freire, E. Direct measurement of protein binding energetics by isothermal titration calorimetry. Curr. Opin. Struct. Biol., 2001, 11(5), 560-566.
[http://dx.doi.org/10.1016/S0959-440X(00)00248-7] [PMID: 11785756]
[78]
Zubrienė, A.; Smirnov, A.; Dudutienė, V.; Timm, D.D.; Matulienė, J.; Michailovienė, V.; Zakšauskas, A.; Manakova, E.; Gražulis, S.; Matulis, D. Intrinsic thermodynamics and structures of 2,4- and 3,4-substituted fluorinated benzenesulfonamides binding to carbonic anhydrases. Chem. Med. Chem., 2017, 12(2), 161-176.
[http://dx.doi.org/10.1002/cmdc.201600509] [PMID: 28001003]
[79]
Zubrienė, A.; Smirnovienė, J.; Smirnov, A.; Morkūnaitė, V.; Michailovienė, V.; Jachno, J.; Juozapaitienė, V.; Norvaišas, P.; Manakova, E.; Gražulis, S.; Matulis, D. Intrinsic thermodynamics of 4-substituted-2,3,5,6-tetrafluorobenzenesulfonamide binding to carbonic anhydrases by isothermal titration calorimetry. Biophys. Chem., 2015, 205, 51-65.
[http://dx.doi.org/10.1016/j.bpc.2015.05.009] [PMID: 26079542]
[80]
Wiseman, T.; Williston, S.; Brandts, J.F.; Lin, L.N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem., 1989, 179(1), 131-137.
[http://dx.doi.org/10.1016/0003-2697(89)90213-3] [PMID: 2757186]
[81]
Krainer, G.; Broecker, J.; Vargas, C.; Fanghänel, J.; Keller, S. Quantifying high-affinity binding of hydrophobic ligands by isothermal titration calorimetry. Anal. Chem., 2012, 84(24), 10715-10722.
[http://dx.doi.org/10.1021/ac3025575] [PMID: 23130786]
[82]
Sigurskjold, B.W. Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal. Biochem., 2000, 277(2), 260-266.
[http://dx.doi.org/10.1006/abio.1999.4402] [PMID: 10625516]
[83]
Kaczor, A.A.; Selent, J. Oligomerization of G protein-coupled receptors: biochemical and biophysical methods. Curr. Med. Chem., 2011, 18(30), 4606-4634.
[http://dx.doi.org/10.2174/092986711797379285] [PMID: 21864280]
[84]
Celie, P.H.; Parret, A.H.; Perrakis, A. Recombinant cloning strategies for protein expression. Curr. Opin. Struct. Biol., 2016, 38, 145-154.
[http://dx.doi.org/10.1016/j.sbi.2016.06.010] [PMID: 27391134]
[85]
Bachman, J. Site-directed mutagenesis. Methods Enzymol., 2013, 529, 241-248.
[http://dx.doi.org/10.1016/B978-0-12-418687-3.00019-7] [PMID: 24011050]
[86]
Behravan, G.; Jonasson, P.; Jonsson, B.H.; Lindskog, S. Structural and functional differences between carbonic anhydrase isoenzymes I and II as studied by site-directed mutagenesis. Eur. J. Biochem., 1991, 198(3), 589-592.
[http://dx.doi.org/10.1111/j.1432-1033.1991.tb16054.x] [PMID: 1904817]
[87]
De Simone, G.; Di Fiore, A.; Truppo, E.; Langella, E.; Vullo, D.; Supuran, C.T.; Monti, S.M. Exploration of the residues modulating the catalytic features of human carbonic anhydrase XIII by a site-specific mutagenesis approach. J. Enzyme Inhib. Med. Chem., 2019, 34(1), 1506-1510.
[http://dx.doi.org/10.1080/14756366.2019.1653290] [PMID: 31431090]
[88]
Mickevičiūtė, A.; Juozapaitienė, V.; Michailovienė, V.; Jachno, J.; Matulienė, J.; Matulis, D. Recombinant production of 12 catalytically active human CA isoforms. In: Carbonic Anhydrase as Drug Target: Thermodynamics and Structure of Inhibitor Binding; Matulis, D., Ed.; Springer International Publishing: Cham, 2019; pp. 15-37.
[http://dx.doi.org/10.1007/978-3-030-12780-0_2]
[89]
Tars, K.; Vullo, D.; Kazaks, A.; Leitans, J.; Lends, A.; Grandane, A.; Zalubovskis, R.; Scozzafava, A.; Supuran, C.T. Sulfocoumarins (1,2-benzoxathiine-2,2-dioxides): a class of potent and isoform-selective inhibitors of tumor-associated carbonic anhydrases. J. Med. Chem., 2013, 56(1), 293-300.
[http://dx.doi.org/10.1021/jm301625s] [PMID: 23241068]
[90]
Genis, C.; Sippel, K.H.; Case, N.; Cao, W.; Avvaru, B.S.; Tartaglia, L.J.; Govindasamy, L.; Tu, C.; Agbandje-McKenna, M.; Silverman, D.N.; Rosser, C.J.; McKenna, R. Design of a carbonic anhydrase IX active-site mimic to screen inhibitors for possible anticancer properties. Biochemistry, 2009, 48(6), 1322-1331.
[http://dx.doi.org/10.1021/bi802035f] [PMID: 19170619]
[91]
Sippel, K.H.; Stander, A.; Tu, C.; Venkatakrishnan, B.; Robbins, A.H.; Agbandje-McKenna, M.; Fourie, J.; Joubert, A.M.; McKenna, R. Characterization of carbonic anhydrase isozyme specific inhibition by sulfamated 2-ethylestra compounds. Lett. Drug Des. Discov., 2011, 8, 1-25.
[http://dx.doi.org/10.2174/157018011796576105]
[92]
Moeker, J.; Mahon, B.P.; Bornaghi, L.F.; Vullo, D.; Supuran, C.T.; McKenna, R.; Poulsen, S-A. Structural insights into carbonic anhydrase IX isoform specificity of carbohydrate-based sulfamates. J. Med. Chem., 2014, 57(20), 8635-8645.
[http://dx.doi.org/10.1021/jm5012935] [PMID: 25254302]
[93]
Mahon, B.P.; Hendon, A.M.; Driscoll, J.M.; Rankin, G.M.; Poulsen, S-A.; Supuran, C.T.; McKenna, R. Saccharin: a lead compound for structure-based drug design of carbonic anhydrase IX inhibitors. Bioorg. Med. Chem., 2015, 23(4), 849-854.
[http://dx.doi.org/10.1016/j.bmc.2014.12.030] [PMID: 25614109]
[94]
Pinard, M.A.; Aggarwal, M.; Mahon, B.P.; Tu, C.; McKenna, R. A sucrose-binding site provides a lead towards an isoform-specific inhibitor of the cancer-associated enzyme carbonic anhydrase IX. Acta Crystallogr. F Struct. Biol. Commun., 2015, 71(Pt 10), 1352-1358.
[http://dx.doi.org/10.1107/S2053230X1501239X] [PMID: 26457530]
[95]
Pinard, M.A.; Boone, C.D.; Rife, B.D.; Supuran, C.T.; McKenna, R. Structural study of interaction between brinzolamide and dorzolamide inhibition of human carbonic anhydrases. Bioorg. Med. Chem., 2013, 21(22), 7210-7215.
[http://dx.doi.org/10.1016/j.bmc.2013.08.033] [PMID: 24090602]
[96]
Shapiro, H.A.; Zwarenstein, H. A rapid test for pregnancy on Xenopus laevis. Nature, 1934, 133, 762.
[http://dx.doi.org/10.1038/133762a0]
[97]
Gurdon, J.B.; Lane, C.D.; Woodland, H.R.; Marbaix, G. Use of frog eggs and oocytes for the study of messenger RNA and its translation in living cells. Nature, 1971, 233(5316), 177-182.
[http://dx.doi.org/10.1038/233177a0] [PMID: 4939175]
[98]
Sasaki, S.; Ishibashi, K.; Nagai, T.; Marumo, F. Regulation mechanisms of intracellular pH of Xenopus laevis oocyte. Biochim. Biophys. Acta, 1992, 1137(1), 45-51.
[http://dx.doi.org/10.1016/0167-4889(92)90098-V] [PMID: 1327152]
[99]
Terhag, J.; Cavara, N.A.; Hollmann, M. Cave Canalem: how endogenous ion channels may interfere with heterologous expression in Xenopus oocytes. Methods, 2010, 51(1), 66-74.
[http://dx.doi.org/10.1016/j.ymeth.2010.01.034] [PMID: 20123125]
[100]
Dumont, J.N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morphol., 1972, 136(2), 153-179.
[http://dx.doi.org/10.1002/jmor.1051360203] [PMID: 4109871]
[101]
Wagner, C.A.; Friedrich, B.; Setiawan, I.; Lang, F.; Bröer, S. The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell. Physiol. Biochem., 2000, 10(1-2), 1-12.
[http://dx.doi.org/10.1159/000016341] [PMID: 10844393]
[102]
Bröer, S. Xenopus laevis oocytes. In: Membrane transporters in drug discovery and development: methods and protocols; Yan, Q., Ed.; Methods in Molecular Biology; Humana Press: Totowa, NJ, 2010.
[103]
Nakhoul, N.L.; Davis, B.A.; Romero, M.F.; Boron, W.F. Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes. Am. J. Physiol., 1998, 274(2), C543-C548.
[http://dx.doi.org/10.1152/ajpcell.1998.274.2.C543] [PMID: 9486145]
[104]
Lu, J.; Daly, C.M.; Parker, M.D.; Gill, H.S.; Piermarini, P.M.; Pelletier, M.F.; Boron, W.F. Effect of human carbonic anhydrase II on the activity of the human electrogenic Na/HCO3 cotransporter NBCe1-A in Xenopus oocytes. J. Biol. Chem., 2006, 281(28), 19241-19250.
[http://dx.doi.org/10.1074/jbc.M602181200] [PMID: 16687407]
[105]
Schueler, C.; Becker, H.M.; McKenna, R.; Deitmer, J.W. Transport activity of the sodium bicarbonate cotransporter NBCe1 is enhanced by different isoforms of carbonic anhydrase. PLoS One, 2011, 6(11), e27167.
[http://dx.doi.org/10.1371/journal.pone.0027167] [PMID: 22076132]
[106]
Schneider, H-P.; Alt, M.D.; Klier, M.; Spiess, A.; Andes, F.T.; Waheed, A.; Sly, W.S.; Becker, H.M.; Deitmer, J.W. GPI-anchored carbonic anhydrase IV displays both intra- and extracellular activity in cRNA-injected oocytes and in mouse neurons. Proc. Natl. Acad. Sci. USA, 2013, 110(4), 1494-1499.
[http://dx.doi.org/10.1073/pnas.1221213110] [PMID: 23297198]
[107]
Musa-Aziz, R.; Occhipinti, R.; Boron, W.F. Evidence from simultaneous intracellular- and surface-pH transients that carbonic anhydrase II enhances CO2 fluxes across Xenopus oocyte plasma membranes. Am. J. Physiol. Cell Physiol., 2014, 307(9), C791-C813.
[http://dx.doi.org/10.1152/ajpcell.00051.2014] [PMID: 24965587]
[108]
Vilas, G.; Krishnan, D.; Loganathan, S.K.; Malhotra, D.; Liu, L.; Beggs, M.R.; Gena, P.; Calamita, G.; Jung, M.; Zimmermann, R.; Tamma, G.; Casey, J.R.; Alexander, R.T. Increased water flux induced by an aquaporin-1/carbonic anhydrase II interaction. Mol. Biol. Cell, 2015, 26(6), 1106-1118.
[http://dx.doi.org/10.1091/mbc.E14-03-0812] [PMID: 25609088]
[109]
Klier, M.; Jamali, S.; Ames, S.; Schneider, H-P.; Becker, H.M.; Deitmer, J.W. Catalytic activity of human carbonic anhydrase isoform IX is displayed both extra- and intracellularly. FEBS J., 2016, 283(1), 191-200.
[http://dx.doi.org/10.1111/febs.13562] [PMID: 26470855]
[110]
Kazokaitė, J.; Ames, S.; Becker, H.M.; Deitmer, J.W.; Matulis, D. Selective inhibition of human carbonic anhydrase IX in Xenopus oocytes and MDA-MB-231 breast cancer cells. J. Enzyme Inhib. Med. Chem., 2016, 31(sup4), 38-44.
[http://dx.doi.org/10.1080/14756366.2016.1217854] [PMID: 27557419]
[111]
Aspatwar, A.; Tolvanen, M.E.E.; Schneider, H-P.; Becker, H.M.; Narkilahti, S.; Parkkila, S.; Deitmer, J.W. Catalytically inactive carbonic anhydrase-related proteins enhance transport of lactate by MCT1. FEBS Open Bio, 2019, 9(7), 1204-1211.
[http://dx.doi.org/10.1002/2211-5463.12647] [PMID: 31033227]
[112]
Becker, H.M.; Hirnet, D.; Fecher-Trost, C.; Sültemeyer, D.; Deitmer, J.W. Transport activity of MCT1 expressed in Xenopus oocytes is increased by interaction with carbonic anhydrase. J. Biol. Chem., 2005, 280(48), 39882-39889.
[http://dx.doi.org/10.1074/jbc.M503081200] [PMID: 16174776]
[113]
Becker, H.M.; Klier, M.; Schüler, C.; McKenna, R.; Deitmer, J.W. Intramolecular proton shuttle supports not only catalytic but also noncatalytic function of carbonic anhydrase II. Proc. Natl. Acad. Sci. USA, 2011, 108(7), 3071-3076.
[http://dx.doi.org/10.1073/pnas.1014293108] [PMID: 21282642]
[114]
Klier, M.; Schüler, C.; Halestrap, A.P.; Sly, W.S.; Deitmer, J.W.; Becker, H.M. Transport activity of the high-affinity monocarboxylate transporter MCT2 is enhanced by extracellular carbonic anhydrase IV but not by intracellular carbonic anhydrase II. J. Biol. Chem., 2011, 286(31), 27781-27791.
[http://dx.doi.org/10.1074/jbc.M111.255331] [PMID: 21680735]
[115]
Jamali, S.; Klier, M.; Ames, S.; Barros, L.F.; McKenna, R.; Deitmer, J.W.; Becker, H.M. Hypoxia-induced carbonic anhydrase IX facilitates lactate flux in human breast cancer cells by non-catalytic function. Sci. Rep., 2015, 5, 13605.
[http://dx.doi.org/10.1038/srep13605] [PMID: 26337752]
[116]
Ames, S.; Andring, J.T.; McKenna, R.; Becker, H.M. CAIX forms a transport metabolon with monocarboxylate transporters in human breast cancer cells. Oncogene, 2019, 39(8), 1710-1723.
[http://dx.doi.org/10.1038/s41388-019-1098-6] [PMID: 31723238]
[117]
Becker, H.M.; Deitmer, J.W. Carbonic anhydrase II increases the activity of the human electrogenic Na+/HCO3- cotransporter. J. Biol. Chem., 2007, 282(18), 13508-13521.
[http://dx.doi.org/10.1074/jbc.M700066200] [PMID: 17353189]
[118]
Dahl, N.K.; Jiang, L.; Chernova, M.N.; Stuart-Tilley, A.K.; Shmukler, B.E.; Alper, S.L. Deficient HCO3- transport in an AE1 mutant with normal Cl- transport can be rescued by carbonic anhydrase II presented on an adjacent AE1 protomer. J. Biol. Chem., 2003, 278(45), 44949-44958.
[http://dx.doi.org/10.1074/jbc.M308660200] [PMID: 12933803]
[119]
Becker, H. Transport of lactate: characterization of the transporters involved in transport at the plasma membrane by heterologous protein expression in Xenopus Oocytes. In: Brain energy Metabolism; Hirrlinger, J.; Waagepetersen, H.S, Eds.; Springer: Neuromethods; New York, 2014; pp. 25-43.
[120]
Aspatwar, A.; Becker, H.M.; Parvathaneni, N.K.; Hammaren, M.; Svorjova, A.; Barker, H.; Supuran, C.T.; Dubois, L.; Lambin, P.; Parikka, M.; Parkkila, S.; Winum, J-Y. Nitroimidazole-based inhibitors DTP338 and DTP348 are safe for zebrafish embryos and efficiently inhibit the activity of human CA IX in Xenopus oocytes. J. Enzyme Inhib. Med. Chem., 2018, 33(1), 1064-1073.
[http://dx.doi.org/10.1080/14756366.2018.1482285] [PMID: 29909747]
[121]
Lindskog, S. Purification and properties of bovine erythrocyte carbonic anhydrase. Biochim. Biophys. Acta, 1960, 39, 218-226.
[http://dx.doi.org/10.1016/0006-3002(60)90156-6] [PMID: 14417215]
[122]
Nyman, P.O. Purification and properties of carbonic anhydrase from human erythrocytes. Biochim. Biophys. Acta, 1961, 52, 1-12.
[http://dx.doi.org/10.1016/0006-3002(61)90898-8] [PMID: 14480808]
[123]
Blackburn, M.N.; Chirgwin, J.M.; James, G.T.; Kempe, T.D.; Parsons, T.; Register, A.M.; Schnackerz, K.D.; Noltmann, E.A. Pseudoisoenzymes of rabbit muscle phosphoglucose isomerase. J. Biol. Chem., 1972, 247(4), 1170-1179.
[http://dx.doi.org/10.1016/S0021-9258(19)45630-5] [PMID: 5010064]
[124]
Whitney, P.L.; Briggle, T.V. Membrane-associated carbonic anhydrase purified from bovine lung. J. Biol. Chem., 1982, 257(20), 12056-12059.
[http://dx.doi.org/10.1016/S0021-9258(18)33676-7] [PMID: 6811592]
[125]
Wistrand, P.J. Properties of membrane-bound carbonic anhydrase. Ann. N. Y. Acad. Sci., 1984, 429, 195-206.
[http://dx.doi.org/10.1111/j.1749-6632.1984.tb12333.x] [PMID: 6430159]
[126]
Dodgson, S.J. Inhibition of mitochondrial carbonic anhydrase and ureagenesis: a discrepancy examined. J. Appl. Physiol., 1987, 63(5), 2134-2141.
[http://dx.doi.org/10.1152/jappl.1987.63.5.2134] [PMID: 3121580]
[127]
Fernley, R.T.; Wright, R.D.; Coghlan, J.P. A novel carbonic anhydrase from the ovine parotid gland. FEBS Lett., 1979, 105(2), 299-302.
[http://dx.doi.org/10.1016/0014-5793(79)80634-1] [PMID: 114424]
[128]
Murakami, H.; Sly, W.S. Purification and characterization of human salivary carbonic anhydrase. J. Biol. Chem., 1987, 262(3), 1382-1388.
[http://dx.doi.org/10.1016/S0021-9258(19)75797-4] [PMID: 2433278]
[129]
Lehtonen, J.; Shen, B.; Vihinen, M.; Casini, A.; Scozzafava, A.; Supuran, C.T.; Parkkila, A-K.; Saarnio, J.; Kivelä, A.J.; Waheed, A.; Sly, W.S.; Parkkila, S. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J. Biol. Chem., 2004, 279(4), 2719-2727.
[http://dx.doi.org/10.1074/jbc.M308984200] [PMID: 14600151]
[130]
Hilvo, M.; Baranauskiene, L.; Salzano, A.M.; Scaloni, A.; Matulis, D.; Innocenti, A.; Scozzafava, A.; Monti, S.M.; Di Fiore, A.; De Simone, G.; Lindfors, M.; Jänis, J.; Valjakka, J.; Pastoreková, S.; Pastorek, J.; Kulomaa, M.S.; Nordlund, H.R.; Supuran, C.T.; Parkkila, S. Biochemical characterization of CA IX, one of the most active carbonic anhydrase isozymes. J. Biol. Chem., 2008, 283(41), 27799-27809.
[http://dx.doi.org/10.1074/jbc.M800938200] [PMID: 18703501]
[131]
Ferrer-Miralles, N.; Domingo-Espín, J.; Corchero, J.L.; Vázquez, E.; Villaverde, A. Microbial factories for recombinant pharmaceuticals. Microb. Cell Fact., 2009, 8, 17.
[http://dx.doi.org/10.1186/1475-2859-8-17] [PMID: 19317892]
[132]
Narang, A.S.; Desai, D.S. Anticancer drug development. In: Pharmaceutical Perspectives of Cancer Therapeutics; Springer: New York, NY, USA, 2009; pp. 49-92.
[http://dx.doi.org/10.1007/978-1-4419-0131-6_2]
[133]
Pital, A.; Cooper, R.E.; Leise, J.M. Rapid method for determining carbohydrate utilization by Brucellae. J. Bacteriol., 1958, 75(4), 422-425.
[http://dx.doi.org/10.1128/JB.75.4.422-425.1958] [PMID: 13525347]
[134]
Twigg, R.S. Oxidation-reduction aspects of resazurin. Nature, 1945, 155, 401-402.
[http://dx.doi.org/10.1038/155401a0]
[135]
Yajko, D.M.; Madej, J.J.; Lancaster, M.V.; Sanders, C.A.; Cawthon, V.L.; Gee, B.; Babst, A.; Hadley, W.K. Colorimetric method for determining MICs of antimicrobial agents for Mycobacterium tuberculosis . J. Clin. Microbiol., 1995, 33(9), 2324-2327.
[http://dx.doi.org/10.1128/JCM.33.9.2324-2327.1995] [PMID: 7494021]
[136]
Tiballi, R.N.; He, X.; Zarins, L.T.; Revankar, S.G.; Kauffman, C.A. Use of a colorimetric system for yeast susceptibility testing. J. Clin. Microbiol., 1995, 33(4), 915-917.
[http://dx.doi.org/10.1128/JCM.33.4.915-917.1995] [PMID: 7790460]
[137]
Yamaguchi, H.; Uchida, K.; Nagino, K.; Matsunaga, T. Usefulness of a colorimetric method for testing antifungal drug susceptibilities of Aspergillus species to voriconazole. J. Infect. Chemother., 2002, 8(4), 374-377.
[http://dx.doi.org/10.1007/s10156-002-0201-Y] [PMID: 12525904]
[138]
Mikus, J.; Steverding, D. A simple colorimetric method to screen drug cytotoxicity against Leishmania using the dye Alamar Blue. Parasitol. Int., 2000, 48(3), 265-269.
[http://dx.doi.org/10.1016/S1383-5769(99)00020-3] [PMID: 11227767]
[139]
Byth, H.A.; Mchunu, B.I.; Dubery, I.A.; Bornman, L. Assessment of a simple, non-toxic Alamar blue cell survival assay to monitor tomato cell viability. Phytochem. Anal., 2001, 12(5), 340-346.
[http://dx.doi.org/10.1002/pca.595] [PMID: 11705263]
[140]
O’Brien, J.; Wilson, I.; Orton, T.; Pognan, F. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem., 2000, 267(17), 5421-5426.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01606.x] [PMID: 10951200]
[141]
de Fries, R.; Mitsuhashi, M. Quantification of mitogen induced human lymphocyte proliferation: comparison of alamarBlue assay to 3H-thymidine incorporation assay. J. Clin. Lab. Anal., 1995, 9(2), 89-95.
[http://dx.doi.org/10.1002/jcla.1860090203] [PMID: 7714668]
[142]
Mboge, M.Y.; Chen, Z.; Wolff, A.; Mathias, J.V.; Tu, C.; Brown, K.D.; Bozdag, M.; Carta, F.; Supuran, C.T.; McKenna, R.; Frost, S.C. Selective inhibition of carbonic anhydrase IX over carbonic anhydrase XII in breast cancer cells using benzene sulfonamides: disconnect between activity and growth inhibition. PLoS One, 2018, 13(11), e0207417.
[http://dx.doi.org/10.1371/journal.pone.0207417] [PMID: 30452451]
[143]
Marks, I.S.; Gardeen, S.S.; Kurdziel, S.J.; Nicolaou, S.T.; Woods, J.E.; Kularatne, S.A.; Low, P.S. Development of a small molecule tubulysin B conjugate for treatment of carbonic anhydrase IX receptor expressing cancers. Mol. Pharm., 2018, 15(6), 2289-2296.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00139] [PMID: 29715036]
[144]
van Kuijk, S.J.A.; Gieling, R.G.; Niemans, R.; Lieuwes, N.G.; Biemans, R.; Telfer, B.A.; Haenen, G.R.M.M.; Yaromina, A.; Lambin, P.; Dubois, L.J.; Williams, K.J. The sulfamate small molecule CAIX inhibitor S4 modulates doxorubicin efficacy. PLoS One, 2016, 11(8), e0161040.
[http://dx.doi.org/10.1371/journal.pone.0161040] [PMID: 27513947]
[145]
Angeli, A.; Tanini, D.; Peat, T.S.; Di Cesare Mannelli, L.; Bartolucci, G.; Capperucci, A.; Ghelardini, C.; Supuran, C.T.; Carta, F. Discovery of new selenoureido analogues of 4-(4-fluorophenylureido)benzenesulfonamide as carbonic anhydrase inhibitors. ACS Med. Chem. Lett., 2017, 8(9), 963-968.
[http://dx.doi.org/10.1021/acsmedchemlett.7b00280] [PMID: 28947945]
[146]
Meehan, J.; Ward, C.; Turnbull, A.; Bukowski-Wills, J.; Finch, A.J.; Jarman, E.J.; Xintaropoulou, C.; Martinez-Perez, C.; Gray, M.; Pearson, M.; Mullen, P.; Supuran, C.T.; Carta, F.; Harrison, D.J.; Kunkler, I.H.; Langdon, S.P. Inhibition of pH regulation as a therapeutic strategy in hypoxic human breast cancer cells. Oncotarget, 2017, 8(26), 42857-42875.
[http://dx.doi.org/10.18632/oncotarget.17143] [PMID: 28476026]
[147]
van Kuijk, S.J.A.; Parvathaneni, N.K.; Niemans, R.; van Gisbergen, M.W.; Carta, F.; Vullo, D.; Pastorekova, S.; Yaromina, A.; Supuran, C.T.; Dubois, L.J.; Winum, J-Y.; Lambin, P. New approach of delivering cytotoxic drugs towards CAIX expressing cells: a concept of dual-target drugs. Eur. J. Med. Chem., 2017, 127, 691-702.
[http://dx.doi.org/10.1016/j.ejmech.2016.10.037] [PMID: 27823879]
[148]
McIntyre, A.; Patiar, S.; Wigfield, S.; Li, J.L.; Ledaki, I.; Turley, H.; Leek, R.; Snell, C.; Gatter, K.; Sly, W.S.; Vaughan-Jones, R.D.; Swietach, P.; Harris, A.L. Carbonic anhydrase IX promotes tumor growth and necrosis in vivo and inhibition enhances anti-VEGF therapy. Clin. Cancer Res., 2012, 18(11), 3100-3111.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-1877] [PMID: 22498007]
[149]
Chiche, J.; Ilc, K.; Laferrière, J.; Trottier, E.; Dayan, F.; Mazure, N.M.; Brahimi-Horn, M.C.; Pouysségur, J. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res., 2009, 69(1), 358-368.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-2470] [PMID: 19118021]
[150]
Parks, S.K.; Cormerais, Y.; Durivault, J.; Pouyssegur, J. Genetic disruption of the pHi-regulating proteins Na+/H+ exchanger 1 (SLC9A1) and carbonic anhydrase 9 severely reduces growth of colon cancer cells. Oncotarget, 2017, 8(6), 10225-10237.
[http://dx.doi.org/10.18632/oncotarget.14379] [PMID: 28055960]
[151]
Puck, T.T.; Marcus, P.I. A Rapid method for viable cell titration and clone production with hela cells in tissue culture: the use of X-irradiated cells to supply conditioning factors. Proc. Natl. Acad. Sci. USA, 1955, 41(7), 432-437.
[http://dx.doi.org/10.1073/pnas.41.7.432] [PMID: 16589695]
[152]
Puck, T.T.; Marcus, P.I.; Cieciura, S.J. Clonal growth of mammalian cells in vitro; growth characteristics of colonies from single HeLa cells with and without a feeder layer. J. Exp. Med., 1956, 103(2), 273-283.
[http://dx.doi.org/10.1084/jem.103.2.273] [PMID: 13286432]
[153]
Liu, Q.; Wang, M.; Kern, A.M.; Khaled, S.; Han, J.; Yeap, B.Y.; Hong, T.S.; Settleman, J.; Benes, C.H.; Held, K.D.; Efstathiou, J.A.; Willers, H. Adapting a drug screening platform to discover associations of molecular targeted radiosensitizers with genomic biomarkers. Mol. Cancer Res., 2015, 13(4), 713-720.
[http://dx.doi.org/10.1158/1541-7786.MCR-14-0570] [PMID: 25667133]
[154]
Zanoni, M.; Piccinini, F.; Arienti, C.; Zamagni, A.; Santi, S.; Polico, R.; Bevilacqua, A.; Tesei, A. 3D tumor spheroid models for in vitro therapeutic screening: a systematic approach to enhance the biological relevance of data obtained. Sci. Rep., 2016, 6, 19103.
[http://dx.doi.org/10.1038/srep19103] [PMID: 26752500]
[155]
Baker, B.M.; Chen, C.S. Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues. J. Cell Sci., 2012, 125(Pt 13), 3015-3024.
[http://dx.doi.org/10.1242/jcs.079509] [PMID: 22797912]
[156]
Kimlin, L.C.; Casagrande, G.; Virador, V.M. In vitro three-dimensional (3D) models in cancer research: an update. Mol. Carcinog., 2013, 52(3), 167-182.
[http://dx.doi.org/10.1002/mc.21844] [PMID: 22162252]
[157]
Abo-Ashour, M.F.; Eldehna, W.M.; Nocentini, A.; Bonardi, A.; Bua, S.; Ibrahim, H.S.; Elaasser, M.M.; Kryštof, V.; Jorda, R.; Gratteri, P.; Abou-Seri, S.M.; Supuran, C.T. 3-Hydrazinoisatin-based benzenesulfonamides as novel carbonic anhydrase inhibitors endowed with anticancer activity: Synthesis, in vitro biological evaluation and in silico insights. Eur. J. Med. Chem., 2019, 184, 111768.
[http://dx.doi.org/10.1016/j.ejmech.2019.111768] [PMID: 31629164]
[158]
Dubois, L.; Peeters, S.; Lieuwes, N.G.; Geusens, N.; Thiry, A.; Wigfield, S.; Carta, F.; McIntyre, A.; Scozzafava, A.; Dogné, J-M.; Supuran, C.T.; Harris, A.L.; Masereel, B.; Lambin, P. Specific inhibition of carbonic anhydrase IX activity enhances the in vivo therapeutic effect of tumor irradiation. Radiother. Oncol., 2011, 99(3), 424-431.
[http://dx.doi.org/10.1016/j.radonc.2011.05.045] [PMID: 21676479]
[159]
Dubois, L.; Peeters, S.G.J.A.; van Kuijk, S.J.A.; Yaromina, A.; Lieuwes, N.G.; Saraya, R.; Biemans, R.; Rami, M.; Parvathaneni, N.K.; Vullo, D.; Vooijs, M.; Supuran, C.T.; Winum, J-Y.; Lambin, P. Targeting carbonic anhydrase IX by nitroimidazole based sulfamides enhances the therapeutic effect of tumor irradiation: a new concept of dual targeting drugs. Radiother. Oncol., 2013, 108(3), 523-528.
[http://dx.doi.org/10.1016/j.radonc.2013.06.018] [PMID: 23849171]
[160]
Lee, S-H.; McIntyre, D.; Honess, D.; Hulikova, A.; Pacheco-Torres, J.; Cerdán, S.; Swietach, P.; Harris, A.L.; Griffiths, J.R. Carbonic anhydrase IX is a pH-stat that sets an acidic tumour extracellular pH in vivo. Br. J. Cancer, 2018, 119(5), 622-630.
[http://dx.doi.org/10.1038/s41416-018-0216-5] [PMID: 30206370]
[161]
Svastová, E.; Hulíková, A.; Rafajová, M.; Zat’ovicová, M.; Gibadulinová, A.; Casini, A.; Cecchi, A.; Scozzafava, A.; Supuran, C.T.; Pastorek, J.; Pastoreková, S. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett., 2004, 577(3), 439-445.
[http://dx.doi.org/10.1016/j.febslet.2004.10.043] [PMID: 15556624]
[162]
Dubois, L.; Douma, K.; Supuran, C.T.; Chiu, R.K.; van Zandvoort, M.A.M.J.; Pastoreková, S.; Scozzafava, A.; Wouters, B.G.; Lambin, P. Imaging the hypoxia surrogate marker CA IX requires expression and catalytic activity for binding fluorescent sulfonamide inhibitors. Radiother. Oncol., 2007, 83(3), 367-373.
[http://dx.doi.org/10.1016/j.radonc.2007.04.018] [PMID: 17502120]
[163]
Rami, M.; Dubois, L.; Parvathaneni, N-K.; Alterio, V.; van Kuijk, S.J.A.; Monti, S.M.; Lambin, P.; De Simone, G.; Supuran, C.T.; Winum, J-Y. Hypoxia-targeting carbonic anhydrase IX inhibitors by a new series of nitroimidazole-sulfonamides/sulfamides/sulfamates. J. Med. Chem., 2013, 56(21), 8512-8520.
[http://dx.doi.org/10.1021/jm4009532] [PMID: 24128000]
[164]
Silverman, D.N. Carbonic anhydrase catalyzed oxygen-18 exchange between bicarbonate and water. Arch. Biochem. Biophys., 1973, 155(2), 452-457.
[http://dx.doi.org/10.1016/0003-9861(73)90136-7] [PMID: 4196184]
[165]
Itada, N.; Forster, R.E. Carbonic anhydrase activity in intact red blood cells measured with 18O exchange. J. Biol. Chem., 1977, 252(11), 3881-3890.
[http://dx.doi.org/10.1016/S0021-9258(17)40334-6] [PMID: 405387]
[166]
Silverman, D.N.; Backman, L.; Tu, C. Role of hemoglobin in proton transfer to the active site of carbonic anhydrase. J. Biol. Chem., 1979, 254(8), 2588-2591.
[http://dx.doi.org/10.1016/S0021-9258(17)30111-4] [PMID: 107161]
[167]
Endeward, V.; Gros, G. Low carbon dioxide permeability of the apical epithelial membrane of guinea-pig colon. J. Physiol., 2005, 567(Pt 1), 253-265.
[http://dx.doi.org/10.1113/jphysiol.2005.085761] [PMID: 15932894]
[168]
Sültemeyer, D.F.; Fock, H.P.; Canvin, D.T. Mass spectrometric measurement of intracellular carbonic anhydrase activity in high and low Ci cells of Chlamydomonas. Studies using 18O exchange with 13C/18O labeled bicarbonate. Plant Physiol., 1990, 94(3), 1250-1257.
[http://dx.doi.org/10.1104/pp.94.3.1250] [PMID: 16667825]
[169]
Badger, M.R.; Price, G.D. Carbonic anhydrase activity associated with the Cyanobacterium synechococcus PCC7942 . Plant Physiol., 1989, 89(1), 51-60.
[http://dx.doi.org/10.1104/pp.89.1.51] [PMID: 16666546]
[170]
Fisher, Z.; Hernandez Prada, J.A.; Tu, C.; Duda, D.; Yoshioka, C.; An, H.; Govindasamy, L.; Silverman, D.N.; McKenna, R. Structural and kinetic characterization of active-site histidine as a proton shuttle in catalysis by human carbonic anhydrase II. Biochemistry, 2005, 44(4), 1097-1105.
[http://dx.doi.org/10.1021/bi0480279] [PMID: 15667203]
[171]
Ames, S.; Pastorekova, S.; Becker, H.M. The proteoglycan-like domain of carbonic anhydrase IX mediates non-catalytic facilitation of lactate transport in cancer cells. Oncotarget, 2018, 9(46), 27940-27957.
[http://dx.doi.org/10.18632/oncotarget.25371] [PMID: 29963253]
[172]
Endeward, V.; Musa-Aziz, R.; Cooper, G.J.; Chen, L-M.; Pelletier, M.F.; Virkki, L.V.; Supuran, C.T.; King, L.S.; Boron, W.F.; Gros, G. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB J., 2006, 20(12), 1974-1981.
[http://dx.doi.org/10.1096/fj.04-3300com] [PMID: 17012249]
[173]
Arias-Hidalgo, M.; Al-Samir, S.; Weber, N.; Geers-Knörr, C.; Gros, G.; Endeward, V. CO2 permeability and carbonic anhydrase activity of rat cardiomyocytes. Acta Physiol. (Oxf.), 2017, 221(2), 115-128.
[http://dx.doi.org/10.1111/apha.12887] [PMID: 28429509]
[174]
Arias-Hidalgo, M.; Yuan, Q.; Carta, F.; Supuran, C.T.; Gros, G.; Endeward, V. CO2 Permeability of Rat Hepatocytes and Relation of CO2 Permeability to CO2 Production. Cell. Physiol. Biochem., 2018, 46(3), 1198-1208.
[http://dx.doi.org/10.1159/000489070] [PMID: 29684917]
[175]
Arias-Hidalgo, M.; Hegermann, J.; Tsiavaliaris, G.; Carta, F.; Supuran, C.T.; Gros, G.; Endeward, V. CO2 and HCO3- permeability of the rat liver mitochondrial membrane. Cell. Physiol. Biochem., 2016, 39(5), 2014-2024.
[http://dx.doi.org/10.1159/000447897] [PMID: 27771717]
[176]
Itel, F.; Al-Samir, S.; Öberg, F.; Chami, M.; Kumar, M.; Supuran, C.T.; Deen, P.M.T.; Meier, W.; Hedfalk, K.; Gros, G.; Endeward, V. CO2 permeability of cell membranes is regulated by membrane cholesterol and protein gas channels. FASEB J., 2012, 26(12), 5182-5191.
[http://dx.doi.org/10.1096/fj.12-209916] [PMID: 22964306]
[177]
Mullard, A. 2019 FDA drug approvals. Nat. Rev. Drug Discov., 2020, 19(2), 79-84.
[http://dx.doi.org/10.1038/d41573-020-00001-7] [PMID: 32020068]
[178]
Mullard, A. 2018 FDA drug approvals. Nat. Rev. Drug Discov., 2019, 18(2), 85-89.
[http://dx.doi.org/10.1038/d41573-019-00014-x] [PMID: 30710142]
[179]
Hingorani, A.D.; Kuan, V.; Finan, C.; Kruger, F.A.; Gaulton, A.; Chopade, S.; Sofat, R.; MacAllister, R.J.; Overington, J.P.; Hemingway, H.; Denaxas, S.; Prieto, D.; Casas, J.P. Improving the odds of drug development success through human genomics: modelling study. Sci. Rep., 2019, 9(1), 18911.
[http://dx.doi.org/10.1038/s41598-019-54849-w] [PMID: 31827124]
[180]
Dowden, H.; Munro, J. Trends in clinical success rates and therapeutic focus. Nat. Rev. Drug Discov., 2019, 18(7), 495-496.
[http://dx.doi.org/10.1038/d41573-019-00074-z] [PMID: 31267067]
[181]
Pastoreková, S.; Parkkila, S.; Parkkila, A.K.; Opavský, R.; Zelník, V.; Saarnio, J.; Pastorek, J. Carbonic anhydrase IX, MN/CA IX: analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts. Gastroenterology, 1997, 112(2), 398-408.
[http://dx.doi.org/10.1053/gast.1997.v112.pm9024293] [PMID: 9024293]
[182]
Pastorekova, S.; Gillies, R.J. The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond. Cancer Metastasis Rev., 2019, 38(1-2), 65-77.
[http://dx.doi.org/10.1007/s10555-019-09799-0] [PMID: 31076951]
[183]
Alterio, V.; Di Fiore, A.; D’Ambrosio, K.; Supuran, C.T.; De Simone, G. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem. Rev., 2012, 112(8), 4421-4468.
[http://dx.doi.org/10.1021/cr200176r] [PMID: 22607219]
[184]
Cecchi, A.; Hulikova, A.; Pastorek, J.; Pastoreková, S.; Scozzafava, A.; Winum, J-Y.; Montero, J-L.; Supuran, C.T. Carbonic anhydrase inhibitors. Design of fluorescent sulfonamides as probes of tumor-associated carbonic anhydrase IX that inhibit isozyme IX-mediated acidification of hypoxic tumors. J. Med. Chem., 2005, 48(15), 4834-4841.
[http://dx.doi.org/10.1021/jm0501073] [PMID: 16033263]
[185]
Lau, J.; Lin, K-S.; Bénard, F. Past, present, and future: development of theranostic agents targeting carbonic anhydrase IX. Theranostics, 2017, 7(17), 4322-4339.
[http://dx.doi.org/10.7150/thno.21848] [PMID: 29158829]
[186]
Chaturvedi, S.K.; Ma, J.; Zhao, H.; Schuck, P. Use of fluorescence-detected sedimentation velocity to study high-affinity protein interactions. Nat. Protoc., 2017, 12(9), 1777-1791.
[http://dx.doi.org/10.1038/nprot.2017.064] [PMID: 28771239]
[187]
Zhao, H.; Mayer, M.L.; Schuck, P. Analysis of protein interactions with picomolar binding affinity by fluorescence-detected sedimentation velocity. Anal. Chem., 2014, 86(6), 3181-3187.
[http://dx.doi.org/10.1021/ac500093m] [PMID: 24552356]
[188]
Jerabek-Willemsen, M.; André, T.; Wanner, R.; Roth, H.M.; Duhr, S.; Baaske, P.; Breitsprecher, D. MicroScale thermophoresis: interaction analysis and beyond. J. Mol. Struct., 2014, 1077, 101-113.
[http://dx.doi.org/10.1016/j.molstruc.2014.03.009]
[189]
Zubrienė, A.; Matulienė, J.; Baranauskienė, L.; Jachno, J.; Torresan, J.; Michailovienė, V.; Cimmperman, P.; Matulis, D. Measurement of nanomolar dissociation constants by titration calorimetry and thermal shift assay - radicicol binding to Hsp90 and ethoxzolamide binding to CAII. Int. J. Mol. Sci., 2009, 10(6), 2662-2680.
[http://dx.doi.org/10.3390/ijms10062662] [PMID: 19582223]
[190]
Talibov, V.O.; Linkuvienė, V.; Matulis, D.; Danielson, U.H. Kinetically selective inhibitors of human carbonic anhydrase isozymes I, II, VII, IX, XII, and XIII. J. Med. Chem., 2016, 59(5), 2083-2093.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01723] [PMID: 26805033]
[191]
Koyuncu, I.; Gonel, A.; Durgun, M.; Kocyigit, A.; Yuksekdag, O.; Supuran, C.T. Assessment of the antiproliferative and apoptotic roles of sulfonamide carbonic anhydrase IX inhibitors in HeLa cancer cell line. J. Enzyme Inhib. Med. Chem., 2019, 34(1), 75-86.
[http://dx.doi.org/10.1080/14756366.2018.1524380] [PMID: 30362386]
[192]
Abdelrahman, M.A.; Eldehna, W.M.; Nocentini, A.; Bua, S.; Al-Rashood, S.T.; Hassan, G.S.; Bonardi, A.; Almehizia, A.A.; Alkahtani, H.M.; Alharbi, A.; Gratteri, P.; Supuran, C.T. Novel diamide-based benzenesulfonamides as selective carbonic anhydrase IX inhibitors endowed with antitumor activity: synthesis, biological evaluation and in silico insights. Int. J. Mol. Sci., 2019, 20(10), 20.
[http://dx.doi.org/10.3390/ijms20102484] [PMID: 31137489]
[193]
Svastova, E.; Witarski, W.; Csaderova, L.; Kosik, I.; Skvarkova, L.; Hulikova, A.; Zatovicova, M.; Barathova, M.; Kopacek, J.; Pastorek, J.; Pastorekova, S. Carbonic anhydrase IX interacts with bicarbonate transporters in lamellipodia and increases cell migration via its catalytic domain. J. Biol. Chem., 2012, 287(5), 3392-3402.
[http://dx.doi.org/10.1074/jbc.M111.286062] [PMID: 22170054]
[194]
Swayampakula, M.; McDonald, P.C.; Vallejo, M.; Coyaud, E.; Chafe, S.C.; Westerback, A.; Venkateswaran, G.; Shankar, J.; Gao, G.; Laurent, E.M.N.; Lou, Y.; Bennewith, K.L.; Supuran, C.T.; Nabi, I.R.; Raught, B.; Dedhar, S. The interactome of metabolic enzyme carbonic anhydrase IX reveals novel roles in tumor cell migration and invadopodia/MMP14-mediated invasion. Oncogene, 2017, 36(45), 6244-6261.
[http://dx.doi.org/10.1038/onc.2017.219] [PMID: 28692057]
[195]
Parks, S.K.; Chiche, J.; Pouysségur, J. Disrupting proton dynamics and energy metabolism for cancer therapy. Nat. Rev. Cancer, 2013, 13(9), 611-623.
[http://dx.doi.org/10.1038/nrc3579] [PMID: 23969692]
[196]
Federici, C.; Lugini, L.; Marino, M.L.; Carta, F.; Iessi, E.; Azzarito, T.; Supuran, C.T.; Fais, S. Lansoprazole and carbonic anhydrase IX inhibitors sinergize against human melanoma cells. J. Enzyme Inhib. Med. Chem., 2016, 31(sup1), 119-125.
[http://dx.doi.org/10.1080/14756366.2016.1177525]
[197]
Liskova, V.; Hudecova, S.; Lencesova, L.; Iuliano, F.; Sirova, M.; Ondrias, K.; Pastorekova, S.; Krizanova, O. Type 1 sodium calcium exchanger forms a complex with carbonic anhydrase IX and via reverse mode activity contributes to pH control in hypoxic tumors. Cancers (Basel), 2019, 11(8), 11.
[http://dx.doi.org/10.3390/cancers11081139] [PMID: 31395807]
[198]
Becker, H.M. Carbonic anhydrase IX and acid transport in cancer. Br. J. Cancer, 2020, 122(2), 157-167.
[http://dx.doi.org/10.1038/s41416-019-0642-z] [PMID: 31819195]
[199]
McDonald, P.C.; Chafe, S.C.; Brown, W.S.; Saberi, S.; Swayampakula, M.; Venkateswaran, G.; Nemirovsky, O.; Gillespie, J.A.; Karasinska, J.M.; Kalloger, S.E.; Supuran, C.T.; Schaeffer, D.F.; Bashashati, A.; Shah, S.P.; Topham, J.T.; Yapp, D.T.; Li, J.; Renouf, D.J.; Stanger, B.Z.; Dedhar, S. Regulation of pH by carbonic anhydrase 9 mediates survival of pancreatic cancer cells with activated KRAS in response to hypoxia. Gastroenterology, 2019, 157(3), 823-837.
[http://dx.doi.org/10.1053/j.gastro.2019.05.004] [PMID: 31078621]
[200]
Hedlund, E.E.; McDonald, P.C.; Nemirovsky, O.; Awrey, S.; Jensen, L.D.E.; Dedhar, S. Harnessing induced essentiality: targeting carbonic anhydrase IX and angiogenesis reduces lung metastasis of triple negative breast cancer xenografts. Cancers (Basel), 2019, 11(7), 1002.
[http://dx.doi.org/10.3390/cancers11071002] [PMID: 31319613]

Rights & Permissions Print Cite
Article Metrics
37
1
Wayfinder Image
World Antimicrobial Awareness Week
© 2024 Bentham Science Publishers | Privacy Policy