Nitroimidazole-based inhibitors DTP338 and DTP348 are safe for zebrafish embryos and efficiently inhibit the activity of human CA IX in Xenopus oocytes

References

• Pastorekova S, Parkkila S, Zavada J. Tumor-associated carbonic anhydrases and their clinical significance. Adv Clin Chem 2006;42:167–216.
   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
• Opavsky R, Pastorekova S, Zelnik V, et al. Human MN/CA9 gene, a novel member of the carbonic anhydrase family: structure and exon to protein domain relationships. Genomics 1996;33:480–7.
   PubMed Web of Science ®Google Scholar
• Gatenby RA, Gawlinski ET. A reaction-diffusion model of cancer invasion. Cancer Res 1996;56:5745–53.
   PubMed Web of Science ®Google Scholar
• Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Winum JY. Carbonic anhydrase IX inhibitors in cancer therapy: an update. Future Med Chem 2015;7:1407–14.
   PubMed Web of Science ®Google Scholar
• Pastorekova S, Ratcliffe PJ, Pastorek J. Molecular mechanisms of carbonic anhydrase IX-mediated pH regulation under hypoxia. BJU Int 2008;101:8–15.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Alterio V, Di Fiore A, et al. Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: three for the price of one. Med Res Rev 2018. [Epub ahead of print]. doi:10.1002/med.21497
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:48.
   PubMed Web of Science ®Google Scholar
• Pastorekova S, Parkkila S, Parkkila AK, et al. Carbonic anhydrase IX, MN/CA IX: analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts. Gastroenterology 1997;112:398–408.
   PubMed Web of Science ®Google Scholar
• van Kuijk SJ, Yaromina A, Houben R, et al. Prognostic significance of carbonic anhydrase IX expression in cancer patients: a meta-analysis. Front Oncol 2016;6:69.
   PubMed Web of Science ®Google Scholar
• Pettersen EO, Ebbesen P, Gieling RG, et al. Targeting tumour hypoxia to prevent cancer metastasis. From biology, biosensing and technology to drug development: the METOXIA consortium. J Enzyme Inhib Med Chem 2015;30:689–721.
   PubMed Web of Science ®Google Scholar
• McDonald PC, Winum JY, Supuran CT, et al. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 2012;3:84–97.
   PubMed Web of Science ®Google Scholar
• Winum JY, Scozzafava A, Montero JL, et al. Inhibition of carbonic anhydrase IX: a new strategy against cancer. Anticancer Agents Med Chem 2009;9:693–702.
   PubMed Web of Science ®Google Scholar
• Thiry A, Dogne JM, Masereel B, et al. Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 2006;27:566–73.
   PubMed Web of Science ®Google Scholar
• Cecchi A, Hulikova A, Pastorek J, et al. 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;48:4834–41.
   PubMed Web of Science ®Google Scholar
• Alterio V, Vitale RM, Monti SM, et al. Carbonic anhydrase inhibitors: X-ray and molecular modeling study for the interaction of a fluorescent antitumor sulfonamide with isozyme II and IX. J Am Chem Soc 2006;128:8329–35.
   PubMed Web of Science ®Google Scholar
• Rami M, Dubois L, Parvathaneni NK, et al. Hypoxia-targeting carbonic anhydrase IX inhibitors by a new series of nitroimidazole-sulfonamides/sulfamides/sulfamates. J Med Chem 2013;56:8512–20.
   PubMed Web of Science ®Google Scholar
• D'Ambrosio K, Smaine FZ, Carta F, et al. Development of potent carbonic anhydrase inhibitors incorporating both sulfonamide and sulfamide groups. J Med Chem 2012;55:6776–83.
   PubMed Web of Science ®Google Scholar
• Winum JY, Carta F, Ward C, et al. Ureido-substituted sulfamates show potent carbonic anhydrase IX inhibitory and antiproliferative activities against breast cancer cell lines. Bioorg Med Chem Lett 2012;22:4681–5.
   PubMed Web of Science ®Google Scholar
• Liu K, Zhu HL. Nitroimidazoles as anti-tumor agents. Anticancer Agents Med Chem 2011;11:687–91.
   PubMed Web of Science ®Google Scholar
• Overgaard J, Overgaard M, Nielsen OS, et al. A comparative investigation of nimorazole and misonidazole as hypoxic radiosensitizers in a C3H mammary carcinoma in vivo. Br J Cancer 1982;46:904–11.
   PubMed Web of Science ®Google Scholar
• MacRae CA, Peterson RT. Zebrafish as tools for drug discovery. Nat Rev Drug Discov 2015;14:721–31.
   PubMed Web of Science ®Google Scholar
• McGrath P, Li CQ. Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov Today 2008;13:394–401.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Hammaren M, Koskinen S, et al. Beta-CA-specific inhibitor dithiocarbamate Fc14-584B: a novel antimycobacterial agent with potential to treat drug-resistant tuberculosis. J Enzyme Inhib Med Chem 2017;32:832–40.
   PubMed Web of Science ®Google Scholar
• Kazokaitė J, Aspatwar A, Kairys V, et al. Fluorinated benzenesulfonamide anticancer inhibitors of carbonic anhydrase IX exhibit lower toxic effects on zebrafish embryonic development than ethoxzolamide. Drug Chem Toxicol 2017;40:309–19.
   PubMed Web of Science ®Google Scholar
• Becker HM. Transport of Lactate: Characterization of the transporters involved in transport at the plasma membrane by heterologous protein expression in Xenopus oocytes. Ney York (NY): Springer; 2014.
   Google Scholar
• Nakhoul NL, Davis BA, Romero MF, et al. Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes. Am J Physiol 1998;274:C543–8.
   PubMed Web of Science ®Google Scholar
• Becker HM, Hirnet D, Fecher-Trost C, et al. Transport activity of MCT1 expressed in Xenopus oocytes is increased by interaction with carbonic anhydrase. J Biol Chem 2005;280:39882–9.
   PubMed Web of Science ®Google Scholar
• Schneider HP, Alt MD, Klier M, et al. 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;110:1494–9.
   PubMed Web of Science ®Google Scholar
• Klier M, Jamali S, Ames S, et al. Catalytic activity of human carbonic anhydrase isoform IX is displayed both extra- and intracellularly. Febs j 2016;283:191–200.
   PubMed Web of Science ®Google Scholar
• Ritz C, Baty F, Streibig JC, et al. Dose-response analysis using R. PLoS One 2015;10:e0146021.
   PubMed Web of Science ®Google Scholar
• Hall L, Jude KP, Clark SL, et al. Antimicrobial susceptibility testing of Mycobacterium tuberculosis complex for first and second line drugs by broth dilution in a microtiter plate format. J Visualized Exp 2011;52:e3094.
   Google Scholar
• Becker HM, Broer S, Deitmer JW. Facilitated lactate transport by MCT1 when coexpressed with the sodium bicarbonate cotransporter (NBC) in Xenopus oocytes. Biophys J 2004;86:235–47.
   PubMed Web of Science ®Google Scholar
• Vincent SH, Silverman DN. Carbonic anhydrase activity in mitochondria from rat liver. J Biol Chem 1982;257:6850–5.
   PubMed Web of Science ®Google Scholar
• Sultemeyer DF, Fock HP, Canvin DT. Mass spectrometric measurement of intracellular carbonic anhydrase activity in high and low C(i) cells of Chlamydomonas: studies using O exchange with C/O labeled bicarbonate. Plant Physiol 1990;94:1250–7.
   PubMed Web of Science ®Google Scholar
• Badger MR, Price GD. Carbonic anhydrase activity associated with the cyanobacterium synechococcus PCC7942. Plant Physiol 1989;89:51–60.
   PubMed Web of Science ®Google Scholar
• Johnson BK, Colvin CJ, Needle DB, et al. The carbonic anhydrase inhibitor ethoxzolamide inhibits the Mycobacterium tuberculosis PhoPR regulon and Esx-1 secretion and attenuates virulence. Antimicrob Agents Chemother 2015;59:4436–45.
   PubMed Web of Science ®Google Scholar
• Dubois L, Peeters SG, van Kuijk SJ, et al. 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;108:523–8.
   PubMed Web of Science ®Google Scholar
• Hill AJ, Teraoka H, Heideman W, et al. Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 2005;86:6–19.
   PubMed Web of Science ®Google Scholar
• Peterson RE, Theobald HM, Kimmel GL. Developmental and reproductive toxicity of dioxins and related compounds: cross-species comparisons. Crit Rev Toxicol 1993;23:283–335.
   PubMed Web of Science ®Google Scholar
• Kazokaitė J, Ames S, Becker HM, et al. Selective inhibition of human carbonic anhydrase IX in Xenopus oocytes and MDA-MB-231 breast cancer cells. J Enzyme Inhib Med Chem 2016;31:38–44.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Tolvanen ME, Jokitalo E, et al. Abnormal cerebellar development and ataxia in CARP VIII morphant zebrafish. Hum Mol Genet 2013;22:417–32.
   PubMed Web of Science ®Google Scholar