Pyrrolo and pyrrolopyrimidine sulfonamides act as cytotoxic agents in hypoxia via inhibition of transmembrane carbonic anhydrases

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2/15/2020

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Article

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Elsevier Masson SAS

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European Journal of Medicinal Chemistry;Volume 188, 15 February 2020, Article number 112021

Abstract

A series of novel sulfonamide derivatives bearing pyrrole and pyrrolopyrimidine scaffolds were synthesized and screened as carbonic anhydrase inhibitors. The inhibition activity of the synthesized compounds was evaluated against the cytosolic human carbonic anhydrase isoforms I and II and the transmembranal isoforms IX and XII. Several candidates showed potent inhibitory activity against IX and XII isoforms. Furthermore, ex vivo screening of cytotoxic selectivity and activity of the most potent derivatives were carried out against normal cells (WI38) and cervical cancer cell line (HeLa) under normal and hypoxic conditions using acetazolamide as reference drug. Compound 11b potency was nearly three folds higher in hypoxic than normoxic condition whereas that of compound 11f was nearly four folds higher in hypoxic vs. normoxic HeLa cells. All the screened derivatives exhibited less potency on normal cells (WI38). Molecular docking was carried out to discover the possible binding mode of compounds within the active site of isoform CA IX. © 2019 Elsevier Masson SAS

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scopus

Keywords

Sulfonamide, Pyrrolopyrimidine, Cytotoxic, Carbonic anhydrase inhibitor

Citation

Siegel, R.L., Miller, K.D., Jemal, A. Cancer statistics, 2018 (Open Access) (2018) CA Cancer Journal for Clinicians, 68 (1), pp. 7-30. Cited 2605 times. http://onlinelibrary.wiley.com/journal/10.3322/(ISSN)1542-4863 doi: 10.3322/caac.21442 View at Publisher 2 Boyle, P., Levin, B. World Cancer Report 2008 (2008) . Cited 1503 times. IARC Press, International Agency for Research on Cancer 3 Kakde, D., Jain, D., Shrivastava, V., Kakde, R., Patil, A. T. Cancer therapeutics- opportunities, challenges and advances in drug delivery (2011) Journal of Applied Pharmaceutical Science, 1 (9), pp. 1-10. Cited 55 times. http://www.japsonline.com/admin/php/uploads/252_pdf.pdf 4 Ezabadi, I.R., Camoutsis, C., Zoumpoulakis, P., Geronikaki, A., Soković, M., Glamočilija, J., Ćirić, A. Sulfonamide-1,2,4-triazole derivatives as antifungal and antibacterial agents: Synthesis, biological evaluation, lipophilicity, and conformational studies (2008) Bioorganic and Medicinal Chemistry, 16 (3), pp. 1150-1161. Cited 170 times. doi: 10.1016/j.bmc.2007.10.082 View at Publisher 5 Scozzafava, A., Owa, T., Mastrolorenzo, A., Supuran, C.T. Anticancer and antiviral sulfonamides (2003) Current Medicinal Chemistry, 10 (11), pp. 925-953. Cited 522 times. doi: 10.2174/0929867033457647 View at Publisher 6 Chen, Z., Xu, W., Liu, K., Yang, S., Fan, H., Bhadury, P.S., Hu, D.-Y., (...), Zhang, Y. Synthesis and antiviral activity of 5-(4-chlorophenyl)-1,3,4- thiadiazole sulfonamides (Open Access) (2010) Molecules, 15 (12), pp. 9046-9056. Cited 83 times. http://www.mdpi.com/1420-3049/15/12/9046/pdf doi: 10.3390/molecules15129046 View at Publisher 7 Bano, S., Javed, K., Ahmad, S., Rathish, I.G., Singh, S., Alam, M.S. Synthesis and biological evaluation of some new 2-pyrazolines bearing benzene sulfonamide moiety as potential anti-inflammatory and anti-cancer agents (2011) European Journal of Medicinal Chemistry, 46 (12), pp. 5763-5768. Cited 93 times. doi: 10.1016/j.ejmech.2011.08.015 View at Publisher 8 Shah, S.S.A., Rivera, G., Ashfaq, M. Recent advances in medicinal chemistry of sulfonamides. rational design as anti-tumoral, anti-bacterial and anti-inflammatory agents (2013) Mini-Reviews in Medicinal Chemistry, 13 (1), pp. 70-86. Cited 77 times. View at Publisher 9 Temperini, C., Cecchi, A., Scozzafava, A., Supuran, C.T. Carbonic anhydrase inhibitors. Sulfonamide diuretics revisited-old leads for new applications? (2008) Organic and Biomolecular Chemistry, 6 (14), pp. 2499-2506. Cited 70 times. doi: 10.1039/b800767e View at Publisher 10 Carta, F., Supuran, C.T. Diuretics with carbonic anhydrase inhibitory action: A patent and literature review (2005-2013) (2013) Expert Opinion on Therapeutic Patents, 23 (6), pp. 681-691. Cited 178 times. doi: 10.1517/13543776.2013.780598 View at Publisher 11 Loubatières-Mariani, M.-M. The discovery of hypoglycemic sulfonamides (2007) Journal de la Societe de Biologie, 201 (2), pp. 121-125. Cited 15 times. doi: 10.1051/jbio:2007014 View at Publisher 12 Supuran, C.T., Casini, A., Scozzafava, A. Protease inhibitors of the sulfonamide type: Anticancer, antiinflammatory, and antiviral agents (2003) Medicinal Research Reviews, 23 (5), pp. 535-558. Cited 300 times. doi: 10.1002/med.10047 View at Publisher 13 Göçer, H., Akincioǧlu, A., Öztaşkin, N., Göksu, S., Gülçin, I. Synthesis, antioxidant, and antiacetylcholinesterase activities of sulfonamide derivatives of dopamine-related compounds (2013) Archiv der Pharmazie, 346 (11), pp. 783-792. Cited 98 times. www.interscience.wiley.com doi: 10.1002/ardp.201300228 View at Publisher 14 Köksal, Z., Kalin, R., Camadan, Y., Usanmaz, H., Almaz, Z., Gülçin, I., Gokcen, T., (...), Ozdemir, H. Secondary sulfonamides as effective lactoperoxidase inhibitors (Open Access) (2017) Molecules, 22 (6), art. no. 793. Cited 17 times. http://www.mdpi.com/1420-3049/22/6/914/pdf doi: 10.3390/molecules22060793 View at Publisher 15 Biçer, A., Kaya, R., Anıl, B., Turgut Cin, G., Gülcin, İ., Gültekin, M.S. Synthesis of novel bis-sulfone derivatives and their inhibition properties on some metabolic enzymes including carbonic anhydrase, acetylcholinesterase, and butyrylcholinesterase (2019) Journal of Biochemical and Molecular Toxicology, 33 (11), art. no. e22401. http://onlinelibrary.wiley.com/journal/10.1002/(ISSN)1099-0461 doi: 10.1002/jbt.22401 View at Publisher 16 Casini, A., Scozzafava, A., Mastrolorenzo, A., Supuran, C.T. Sulfonamides and sulfonylated derivatives as anticancer agents (2002) Current Cancer Drug Targets, 2 (1), pp. 55-75. Cited 201 times. doi: 10.2174/1568009023334060 View at Publisher 17 Supuran, C.T., Casini, A., Mastrolorenzo, A., Scozzafava, A. COX-2 selective inhibitors, carbonic anhydrase inhibition and anticancer properties of sulfonamides belonging to this class of pharmacological agents (2004) Mini-Reviews in Medicinal Chemistry, 4 (6), pp. 625-632. Cited 151 times. http://www.benthamdirect.org/pages/all_b_bypublication.php doi: 10.2174/1389557043403792 View at Publisher 18 Owa, T., Ozawa, Y., Semba, T., Hata, N. Novel Concomitant Use of Sulfonamide Compound with Anti-cancer Agent (2009) 19 Supuran, C.T. Carbonic anhydrase inhibitors and activators for novel therapeutic applications (2011) Future Medicinal Chemistry, 3 (9), pp. 1165-1180. Cited 212 times. doi: 10.4155/fmc.11.69 View at Publisher 20 Abbate, F., Casini, A., Owa, T., Scozzafava, A., Supuran, C.T. Carbonic anhydrase inhibitors: E7070, a sulfonamide anticancer agent, potently inhibits cytosolic isozymes I and II, and transmembrane, tumor-associated isozyme IX (2004) Bioorganic and Medicinal Chemistry Letters, 14 (1), pp. 217-223. Cited 233 times. http://www.journals.elsevier.com/bioorganic-and-medicinal-chemistry-letters/ doi: 10.1016/j.bmcl.2003.09.062 View at Publisher 21 Supuran, C.T. Structure-based drug discovery of carbonic anhydrase inhibitors (2012) Journal of Enzyme Inhibition and Medicinal Chemistry, 27 (6), pp. 759-772. Cited 406 times. doi: 10.3109/14756366.2012.672983 View at Publisher 22 Petrou, A., Geronikaki, A., Terzi, E., Guler, O.O., Tuccinardi, T., Supuran, C.T. Inhibition of carbonic anhydrase isoforms I, II, IX and XII with secondary sulfonamides incorporating benzothiazole scaffolds (Open Access) (2016) Journal of Enzyme Inhibition and Medicinal Chemistry, 31 (6), pp. 1306-1311. Cited 13 times. doi: 10.3109/14756366.2015.1128427 View at Publisher 23 Krawczyk, S.H., Nassiri, M.R., Kucera, L.S., Kern, E.R., Ptak, R.G., Wotring, L.L., Drach, J.C., (...), Townsend, L.B. Synthesis and Antiproliferative and Antiviral Activity of 2′-Deoxy-2′-fluoroarabinofuranosyl Analogs of the Nucleoside Antibiotics Toyocamycin and Sangivamycin (1995) Journal of Medicinal Chemistry, 38 (20), pp. 4106-4114. Cited 55 times. doi: 10.1021/jm00020a026 View at Publisher 24 Ghorab, M.M., Heiba, H.I., Khalil, A.I., El Ella, D.A.A., Noaman, E. Computer-based ligand design and synthesis of some new sulfonamides bearing Pyrrole or pyrrolopyrimidine moieties having potential antitumor and radioprotective activities (2008) Phosphorus, Sulfur and Silicon and the Related Elements, 183 (1), pp. 90-104. Cited 13 times. doi: 10.1080/10426500701557104 View at Publisher 25 Ghorab, M.M., Alsaid, M.S., Nissan, Y.M. Anti-breast cancer of some novel pyrrole and pyrrolopyrimidine derivatives bearing a biologically active sulfonamide moiety (2013) Life Science Journal, 10 (4), art. no. 290, pp. 2170-2183. Cited 7 times. http://www.lifesciencesite.com/lsj/life1004/290_18834life1004_2170_2183.pdf 26 Ghorab, M.M., Alsaid, M.S., Nissan, Y.M. Synthesis and molecular docking of some novel anticancer sulfonamides carrying a biologically active pyrrole and pyrrolopyrimidine moieties (2014) Acta Poloniae Pharmaceutica - Drug Research, 71 (4), pp. 603-614. Cited 8 times. http://www.ptfarm.pl/pub/File/Acta_Poloniae/1998/acta4-2014.pdf 27 Ghorab, M.M., Alsaid, M.S., Ceruso, M., Nissan, Y.M., Supuran, C.T. Carbonic anhydrase inhibitors: Synthesis, molecular docking, cytotoxic and inhibition of the human carbonic anhydrase isoforms I, II, IX, XII with novel benzenesulfonamides incorporating pyrrole, pyrrolopyrimidine and fused pyrrolopyrimidine moieties (2014) Bioorganic and Medicinal Chemistry, 22 (14), pp. 3684-3695. Cited 43 times. http://www.journals.elsevier.com/bioorganic-and-medicinal-chemistry/ doi: 10.1016/j.bmc.2014.05.009 View at Publisher 28 Ghorab, M.M., Ceruso, M., Alsaid, M.S., Nissan, Y.M., Arafa, R.K., Supuran, C.T. Novel sulfonamides bearing pyrrole and pyrrolopyrimidine moieties as carbonic anhydrase inhibitors: Synthesis, cytotoxic activity and molecular modeling (2014) European Journal of Medicinal Chemistry, 87, pp. 186-196. Cited 34 times. http://www.journals.elsevier.com/european-journal-of-medicinal-chemistry/ doi: 10.1016/j.ejmech.2014.09.059 View at Publisher 29 Ghorab, M.M., Alsaisd, M.S., Nissan, Y.M. Novel pyrrolopyrimidines and triazolopyrrolopyrimidines carrying a biologically active sulfonamide moieties as anticancer agents (2015) Acta Poloniae Pharmaceutica - Drug Research, 72 (1), pp. 65-78. Cited 3 times. http://www.ptfarm.pl/pub/File/Acta_Poloniae/2015/1/065.pdf 30 Şentürk, M., Gülçin, I., Daştan, A., Irfan Küfrevioǧlu, O., Supuran, C.T. Carbonic anhydrase inhibitors. Inhibition of human erythrocyte isozymes I and II with a series of antioxidant phenols (2009) Bioorganic and Medicinal Chemistry, 17 (8), pp. 3207-3211. Cited 179 times. doi: 10.1016/j.bmc.2009.01.067 View at Publisher 31 Abdülkadir Coban, T., Beydemir, S., Gücin, I., Ekinci, D., Innocenti, A., Vullo, D., Supuran, C.T. Sildenafil is a strong activator of mammalian carbonic anhydrase isoforms I-XIV (2009) Bioorganic and Medicinal Chemistry, 17 (16), pp. 5791-5795. Cited 87 times. http://www.journals.elsevier.com/bioorganic-and-medicinal-chemistry/ doi: 10.1016/j.bmc.2009.07.019 View at Publisher 32 Innocenti, A., Beyza Öztürk Sarikaya, S., Gülçin, I., Supuran, C.T. Carbonic anhydrase inhibitors. Inhibition of mammalian isoforms I-XIV with a series of natural product polyphenols and phenolic acids (2010) Bioorganic and Medicinal Chemistry, 18 (6), pp. 2159-2164. Cited 165 times. doi: 10.1016/j.bmc.2010.01.076 View at Publisher 33 Innocenti, A., Gülçin, I., Scozzafava, A., Supuran, C.T. Carbonic anhydrase inhibitors. Antioxidant polyphenols effectively inhibit mammalian isoforms I-XV (2010) Bioorganic and Medicinal Chemistry Letters, 20 (17), pp. 5050-5053. Cited 110 times. doi: 10.1016/j.bmcl.2010.07.038 View at Publisher 34 Öztürk Sarikaya, S.B., Topal, F., Şentürk, M., Gülin, I., Supuran, C.T. In vitro inhibition of α-carbonic anhydrase isozymes by some phenolic compounds (2011) Bioorganic and Medicinal Chemistry Letters, 21 (14), pp. 4259-4262. Cited 135 times. doi: 10.1016/j.bmcl.2011.05.071 View at Publisher 35 Akincioǧlu, A., Akbaba, Y., Göçer, H., Göksu, S., Gülçin, I., Supuran, C.T. Novel sulfamides as potential carbonic anhydrase isoenzymes inhibitors (2013) Bioorganic and Medicinal Chemistry, 21 (6), pp. 1379-1385. Cited 90 times. doi: 10.1016/j.bmc.2013.01.019 View at Publisher 36 Chegwidden, W.R., Carter, N.D., Edwards, Y.H. The Carbonic Anhydrases: New Horizons (2013) . Cited 126 times. Birkhäuser 37 Aksu, K., Nar, M., Tanc, M., Vullo, D., Gülçin, I., Göksu, S., Tümer, F., (...), Supuran, C.T. Synthesis and carbonic anhydrase inhibitory properties of sulfamides structurally related to dopamine (2013) Bioorganic and Medicinal Chemistry, 21 (11), pp. 2925-2931. Cited 96 times. doi: 10.1016/j.bmc.2013.03.077 View at Publisher 38 Güney, M., Coşkun, A., Topal, F., Daştan, A., Gülçin, I., Supuran, C.T. Oxidation of cyanobenzocycloheptatrienes: Synthesis, photooxygenation reaction and carbonic anhydrase isoenzymes inhibition properties of some new benzotropone derivatives (2014) Bioorganic and Medicinal Chemistry, 22 (13), pp. 3537-3543. Cited 84 times. http://www.journals.elsevier.com/bioorganic-and-medicinal-chemistry/ doi: 10.1016/j.bmc.2014.04.007 View at Publisher 39 Smith, K.S., Jakubzick, C., Whittam, T.S., Ferry, J.G. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes (Open Access) (1999) Proceedings of the National Academy of Sciences of the United States of America, 96 (26), pp. 15184-15189. Cited 270 times. doi: 10.1073/pnas.96.26.15184 View at Publisher 40 Tripp, B.C., Smith, K., Ferry, J.G. Carbonic Anhydrase: New Insights for an Ancient Enzyme (Open Access) (2001) Journal of Biological Chemistry, 276 (52), pp. 48615-48618. Cited 383 times. doi: 10.1074/jbc.R100045200 View at Publisher 41 Bong, G.-M., Stringer, J., Brandvold, D.K., Simsek, F.A., Medina, M.-G., Egeland, G. Development of integrated system for biomimetic CO2 sequestration using the enzyme carbonic anhydrase (2001) Energy and Fuels, 15 (2), pp. 309-316. Cited 198 times. doi: 10.1021/ef000246p View at Publisher 42 Del Prete, S., Bua, S., Alasmary, F.A.S., AlOthman, Z., Tambutté, S., Zoccola, D., Supuran, C.T., (...), Capasso, C. Comparison of the sulfonamide inhibition profiles of the α-carbonic anhydrase isoforms (SpiCA1, SpiCA2 and SpiCA3) encoded by the genome of the scleractinian coral stylophora pistillata (Open Access) (2019) Marine Drugs, 17 (3), art. no. 146. https://www.mdpi.com/1660-3397/17/3/146/pdf doi: 10.3390/md17030146 View at Publisher 43 Alterio, V., Hilvo, M., Di Fiore, A., Supuran, C.T., Pan, P., Parkkila, S., Scaloni, A., (...), De Simone, G. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX (Open Access) (2009) Proceedings of the National Academy of Sciences of the United States of America, 106 (38), pp. 16233-16238. Cited 313 times. http://www.pnas.org/content/106/38/16233.full.pdf doi: 10.1073/pnas.0908301106 View at Publisher 44 Ghorab, M.M., Alsaid, M.S., Al-Dosari, M.S., El-Gazzar, M.G., Arbab, A.H. In-vitro anticancer evaluation of some novel thioureido-benzensulfonamide derivatives (Open Access) (2016) Molecules, 21 (4), art. no. 409. Cited 5 times. http://www.mdpi.com/1420-3049/21/4/409/pdf doi: 10.3390/molecules21040409 View at Publisher 45 Závada, J., Závadová, Z., Pastoreková, S., Čiampor, F., Pastorek, J., Zelník, V. Expression of MaTu‐MN protein in human tumor cultures and in clinical specimens (1993) International Journal of Cancer, 54 (2), pp. 268-274. Cited 168 times. doi: 10.1002/ijc.2910540218 View at Publisher 46 Swinson, D.E.B., Jones, J.L., Richardson, D., Wykoff, C., Turley, H., Pastorek, J., Taub, N., (...), O'Byrne, K.J. Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer (2003) Journal of Clinical Oncology, 21 (3), pp. 473-482. Cited 215 times. doi: 10.1200/JCO.2003.11.132 View at Publisher 47 Korkeila, E., Talvinen, K., Jaakkola, P.M., Minn, H., Syrjänen, K., Sundström, J., Pyrhönen, S. Expression of carbonic anhydrase IX suggests poor outcome in rectal cancer (Open Access) (2009) British Journal of Cancer, 100 (6), pp. 874-880. Cited 76 times. doi: 10.1038/sj.bjc.6604949 View at Publisher 48 Tan, E.Y., Yan, M., Campo, L., Han, C., Takano, E., Turley, H., Candiloro, I., (...), Fox, S.B. The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy (Open Access) (2009) British Journal of Cancer, 100 (2), pp. 405-411. Cited 126 times. doi: 10.1038/sj.bjc.6604844 View at Publisher 49 Nordfors, K., Haapasalo, J., Korja, M., Niemelä, A., Laine, J., Parkkila, A., Pastorekova, S., (...), Haapasalo, H. The tumour-associated carbonic anhydrases CA II, CA IX and CA XII in a group of medulloblastomas and supratentorial primitive neuroectodermal tumours: An association of CA IX with poor prognosis (Open Access) (2010) BMC Cancer, 10, art. no. 148. Cited 38 times. http://www.biomedcentral.com/1471-2407/10/148 doi: 10.1186/1471-2407-10-148 View at Publisher 50 Lee, S., Shin, H.-J., Han, I.-O., Hong, E.-K., Park, S.-Y., Roh, J.-W., Shin, K.H., (...), Kim, J.-Y. Tumor carbonic anhydrase 9 expression is associated with the presence of lymph node metastases in uterine cervical cancer (2007) Cancer Science, 98 (3), pp. 329-333. Cited 41 times. doi: 10.1111/j.1349-7006.2007.00396.x View at Publisher 51 Zatovicova, M., Jelenska, L., Hulikova, A., Csaderova, L., Ditte, Z., Ditte, P., Goliasova, T., (...), Pastorekova, S. Carbonic anhydrase IX as an anticancer therapy target: Preclinical evaluation of internalizing monoclonal antibody directed to catalytic domain (2010) Current Pharmaceutical Design, 16 (29), pp. 3255-3263. Cited 78 times. doi: 10.2174/138161210793429832 View at Publisher 52 McDonald, P.C., Winum, J.-Y., Supuran, C.T., Dedhar, S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics (Open Access) (2012) Oncotarget, 3 (1), pp. 84-97. Cited 251 times. http://www.impactjournals.com/oncotarget/index.php?journal=oncotarget&page=article&op=download&path%5B%5D=422&path%5B%5D=718 doi: 10.18632/oncotarget.422 View at Publisher 53 Rami, M., Dubois, L., Parvathaneni, N.-K., Alterio, V., Van Kuijk, S.J.A., Monti, S.M., Lambin, P., (...), Winum, J.-Y. Hypoxia-targeting carbonic anhydrase IX inhibitors by a new series of nitroimidazole-sulfonamides/sulfamides/sulfamates (2013) Journal of Medicinal Chemistry, 56 (21), pp. 8512-8520. Cited 50 times. doi: 10.1021/jm4009532 View at Publisher 54 Yogeeswari, D.S.P. Medicinal Chemistry. 2 edIndia (2010) Pearson India 55 Maresca, A., Temperini, C., Pochet, L., Masereel, B., Scozzafava, A., Supuran, C.T. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins (2010) Journal of Medicinal Chemistry, 53 (1), pp. 335-344. Cited 254 times. http://pubs.acs.org/doi/pdfplus/10.1021/jm901287j doi: 10.1021/jm901287j View at Publisher 56 Maresca, A., Temperini, C., Vu, H., Pham, N.B., Poulsen, S.-A., Scozzafava, A., Quinn, R.J., (...), Supuran, C.T. Non-zinc mediated inhibition of carbonic anhydrases: Coumarins are a new class of suicide inhibitors (2009) Journal of the American Chemical Society, 131 (8), pp. 3057-3062. Cited 321 times. http://pubs.acs.org/doi/pdfplus/10.1021/ja809683v doi: 10.1021/ja809683v View at Publisher 57 Lou, Y., McDonald, P.C., Oloumi, A., Chia, S., Ostlund, C., Ahmadi, A., Kyle, A., (...), Dedhar, S. Targeting tumor hypoxia: Suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors (Open Access) (2011) Cancer Research, 71 (9), pp. 3364-3376. Cited 421 times. http://cancerres.aacrjournals.org/content/71/9/3364.full.pdf+html doi: 10.1158/0008-5472.CAN-10-4261 View at Publisher 58 Tars, K., Vullo, D., Kazaks, A., Leitans, J., Lends, A., Grandane, A., Zalubovskis, R., (...), Supuran, C.T. Sulfocoumarins (1,2-benzoxathiine-2,2-dioxides): A class of potent and isoform-selective inhibitors of tumor-associated carbonic anhydrases (2013) Journal of Medicinal Chemistry, 56 (1), pp. 293-300. Cited 127 times. doi: 10.1021/jm301625s View at Publisher 59 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? (2012) Chemical Reviews, 112 (8), pp. 4421-4468. Cited 667 times. doi: 10.1021/cr200176r View at Publisher 60 Monti, S.M., Maresca, A., Viparelli, F., Carta, F., Simone, G.D., Mühlschlegel, F.A., Scozzafava, A., (...), Supuran, C.T. Dithiocarbamates are strong inhibitors of the beta-class fungal carbonic anhydrases from Cryptococcus neoformans, Candida albicans and Candida glabrata (2012) Bioorganic and Medicinal Chemistry Letters, 22 (2), pp. 859-862. Cited 83 times. doi: 10.1016/j.bmcl.2011.12.033 View at Publisher 61 Davis, R.A., Vullo, D., Maresca, A., Supuran, C.T., Poulsen, S.-A. Natural product coumarins that inhibit human carbonic anhydrases (2013) Bioorganic and Medicinal Chemistry, 21 (6), pp. 1539-1543. Cited 65 times. doi: 10.1016/j.bmc.2012.07.021 View at Publisher 62 Supuran, C.T. Carbonic Anhydrases: from Biomedical Applications of the Inhibitors and Activators to Biotechnological Use for CO2 Capture (2013) 63 DeGraff, W.G., Mitchell, J.B. Evaluation of a Tetrazolium-based Semiautomated Colorimetric Assay: Assessment of Chemosensitivity Testing (1987) Cancer Research, 47 (4), pp. 936-942. Cited 3712 times. 64 Edmondson, J.M., Armstrong, L.S., Martinez, A.O. A rapid and simple MTT-based spectrophotometric assay for determining drug sensitivity in monolayer cultures (1988) Journal of Tissue Culture Methods, 11 (1), pp. 15-17. Cited 201 times. doi: 10.1007/BF01404408 View at Publisher 65 Vistica, D.T., Monks, A., Pittman, A., Boyd, M.R. Tetrazolium-based Assays for Cellular Viability: A Critical Examination of Selected Parameters Affecting Formazan Production (1991) Cancer Research, 51 (10), pp. 2515-2520. Cited 512 times. 66 Takeuchi, H., Baba, M., Shigeta, S. An application of tetrazolium (MTT) colorimetric assay for the screening of anti-herpes simplex virus compounds (1991) Journal of Virological Methods, 33 (1-2), pp. 61-71. Cited 104 times. doi: 10.1016/0166-0934(91)90008-N View at Publisher 67 Slater, T.F., Sawyer, B., Sträuli, U. Studies on succinate-tetrazolium reductase systems. III. Points of coupling of four different tetrazolium salts III. Points of coupling of four different tetrazolium salts (1963) BBA - Biochimica et Biophysica Acta, 77 (C), pp. 383-393. Cited 583 times. doi: 10.1016/0006-3002(63)90513-4 View at Publisher 68 Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays (1983) Journal of Immunological Methods, 65 (1-2), pp. 55-63. Cited 38980 times. doi: 10.1016/0022-1759(83)90303-4

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