1,448
Views
11
CrossRef citations to date
0
Altmetric
Research Article

Quantitative assessment of specific carbonic anhydrase inhibitors effect on hypoxic cells using electrical impedance assays

, , , , , , , & show all
Pages 1079-1090 | Received 20 Jun 2017, Accepted 11 Jul 2017, Published online: 07 Aug 2017

References

  • McDonald PC, Winum JY, Supuran CT, Dedhar S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 2012;3:84–97.
  • Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77.
  • Lou Y, McDonald PC, Oloumi A, et al. Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res 2011;71:3364–76.
  • Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88.
  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32.
  • 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.
  • Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
  • Tars K, Vullo D, Kazaks A, et al. Sulfocoumarins (1,2-benzoxathiine-2,2-dioxides): a class of potent and isoform-selective inhibitors of tumor-associated carbonic anhydrases. J Med Chem 2013;56:293–300.
  • Gheorghiu M, Enciu AM, Popescu BO, Gheorghiu E. Functional and molecular characterization of the effect of amyloid-beta42 on an in vitro epithelial barrier model. J Alzheimers Dis 2014;38:787–98.
  • Gheorghiu M, David S, Polonschii C, et al. Label free sensing platform for amyloid fibrils effect on living cells. Biosens Bioelectron 2014;52:89–97.
  • Gheorghiu E. Characterizing cellular systems by means of dielectric spectroscopy. Bioelectromagnetics 1996;17:475–82.
  • Wang J, Wu C, Hu N, et al. Microfabricated electrochemical cell-based biosensors for analysis of living cells in vitro. Biosensors 2012;2:127–70.
  • Eales KL, Hollinshead KER, Tennant DA. Hypoxia and metabolic adaptation of cancer cells. Oncogenesis 2016;5:e190.
  • Chanakira A, Kir D, Barke RA, et al. Hypoxia differentially regulates arterial and venous smooth muscle cell migration. PLoS One 2015;10:e0138587.
  • Kangwantas K, Pinteaux E, Penny J. The extracellular matrix protein laminin-10 promotes blood-brain barrier repair after hypoxia and inflammation in vitro. J Neuroinflammation 2016;13:25.
  • Dubois L, Peeters S, Lieuwes NG, et al. Specific inhibition of carbonic anhydrase IX activity enhances the in vivo therapeutic effect of tumor irradiation. Radiother Oncol 2011;99:424–31.
  • 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.
  • Svastová E, Huliková A, Rafajová M, et al. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett 2004;577:439–45.
  • Supuran CT, Scozzafava A, Ilies MA, et al. Carbonic anhydrase inhibitors – Part 53. Synthesis of substituted-pyridinium derivatives of aromatic sulfonamides: the first non-polymeric membrane-impermeable inhibitors with selectivity for isozyme IV. Eur J Med Chem 1998;33:577–94.
  • Grandane A, Belyakov S, Trapencieris P, Zalubovskis R. Facile synthesis of coumarin bioisosteres – 1,2-benzoxathiine 2,2-dioxides. Tetrahedron 2012;68:5541–6.
  • Žalubovskis R. In a search for selective inhibitors of carbonic anhydrases: coumarin and its bioisosteres – synthesis and derivatization. Chem Heterocycl Compd 2015;51:607–12.
  • Krinke D, Jahnke H-G, Pänke O, Robitzki AA. A microelectrode-based sensor for label-free in vitro detection of ischemic effects on cardiomyocytes. Biosens Bioelectron 2009;24:2798–803.
  • Dinischiotu A, Stanca L, Gradinaru D, et al. Lipid peroxidation due to in vitro and in vivo exposure of biological samples to nanoparticles. In: Armstrong D, Bharali DJ, eds. Oxidative stress and nanotechnology: methods and protocols. Totowa (NJ): Humana Press; 2013:155–64.
  • Arndt S, Seebach J, Psathaki K, et al. Bioelectrical impedance assay to monitor changes in cell shape during apoptosis. Biosens Bioelectron 2004;19:583–94.
  • Ivanov S, Liao SY, Ivanova A, et al. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am J Pathol 2001;158:905–19.
  • Supuran CT. Carbonic anhydrase inhibitors and activators for novel therapeutic applications. Future Med Chem 2011;3:1165–80.
  • Liu T, Laurell C, Selivanova G, et al. Hypoxia induces p53-dependent transactivation and Fas/CD95-dependent apoptosis. Cell Death Differ 2006;14:411–21.
  • Behn C, Araneda OF, Llanos AJ, et al. Hypoxia-related lipid peroxidation: evidences, implications and approaches. Respir Physiol Neurobiol 2007;158:143–50.
  • Koumenis C, Alarcon R, Hammond E, et al. Regulation of p53 by hypoxia: dissociation of transcriptional repression and apoptosis from p53-dependent transactivation. Mol Cell Biol 2001;21:1297–310.
  • Supuran CT, Scozzafava A, Casini A. Carbonic anhydrase inhibitors. Med Res Rev 2003;23:146–89.
  • Winum JY, Poulsen SA, Supuran CT. Therapeutic applications of glycosidic carbonic anhydrase inhibitors. Med Res Rev 2009;29:419–35.
  • Carta F, Supuran CT, Scozzafava A. Sulfonamides and their isosters as carbonic anhydrase inhibitors. Future Med Chem 2014;6:1149–65.
  • Menchise V, De Simone G, Alterio V, et al. Carbonic anhydrase inhibitors: stacking with Phe131 determines active site binding region of inhibitors as exemplified by the X-ray crystal structure of a membrane-impermeant antitumor sulfonamide complexed with isozyme II. J Med Chem 2005;48:5721–7.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • Dubois L, Lieuwes NG, Maresca A, et al. Imaging of CA IX with fluorescent labelled sulfonamides distinguishes hypoxic and (re)-oxygenated cells in a xenograft tumour model. Radiother Oncol 2009;92:423–8.
  • Mansfield KD, Simon MC, Keith B. Hypoxic reduction in cellular glutathione levels requires mitochondrial reactive oxygen species. J Appl Physiol (1985) 2004;97:1358–66.
  • Meyer AJ, Hell R. Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth Res 2005;86:435–57.
  • Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 2008;283:10892–903.
  • Lai MC, Chang CM, Sun HS. Hypoxia induces autophagy through translational up-regulation of lysosomal proteins in human colon cancer cells. PLoS One 2016;11:e0153627.
  • Alterio V, Di Fiore A, D’Ambrosio K, et al. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68.
  • Tanc M, Carta F, Bozdag M, et al. 7-Substituted-sulfocoumarins are isoform-selective, potent carbonic anhydrase II inhibitors. Bioorg Med Chem 2013;21:4502–10.
  • Nocentini A, Ceruso M, Carta F, Supuran CT. 7-Aryl-triazolyl-substituted sulfocoumarins are potent, selective inhibitors of the tumor-associated carbonic anhydrase IX and XII. J Enzyme Inhib Med Chem 2016;31:1226–33.
  • Grandane A, Tanc M, Di Cesare Mannelli L, et al. 6-Substituted sulfocoumarins are selective carbonic anhydrase IX and XII inhibitors with significant cytotoxicity against colorectal cancer cells. J Med Chem 2015;58:3975–83.
  • Gu W, Zhao Y. Cellular electrical impedance spectroscopy: an emerging technology of microscale biosensors. Expert Rev Med Devices 2010;7:767–79.
  • Hong J, Kandasamy K, Marimuthu M, et al. Electrical cell-substrate impedance sensing as a non-invasive tool for cancer cell study. Analyst 2011;136:237–45.
  • Abassi YA, Xi B, Zhang W, et al. Kinetic cell-based morphological screening: prediction of mechanism of compound action and off-target effects. Chem Biol 2009;16:712–23.
  • Zieseniss A. Hypoxia and the modulation of the actin cytoskeleton – emerging interrelations. Hypoxia (Auckl) 2014;2:11–21.