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Research Paper

Assessment of the antiproliferative and apoptotic roles of sulfonamide carbonic anhydrase IX inhibitors in HeLa cancer cell line

ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 75-86 | Received 23 Aug 2018, Accepted 12 Sep 2018, Published online: 26 Oct 2018

References

  • (a) Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77. (b) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32. (c) Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88. (d) Supuran CT, Vullo D, Manole G, et al. Designing of novel carbonic anhydrase inhibitors and activators. Curr Med Chem Cardiovasc Hematol Agents 2004;2:49–68.
  • (a) 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 [In press]. doi: 10.1002/med.21497. (b) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem. 2016;31:345–60. (c) Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:48. (d) Ward C, Langdon SP, Mullen P, et al. New strategies for targeting the hypoxic tumour microenvironment in breast cancer. Cancer Treat Rev 2013;39:171–9. (e) Garaj V, Puccetti L, Fasolis G, et al. Carbonic anhydrase inhibitors: novel sulfonamides incorporating 1,3,5-triazine moieties as inhibitors of the cytosolic and tumour-associated carbonic anhydrase isozymes I, II and IX. Bioorg Med Chem Lett 2005;15:3102–8. (f) Casey JR, Morgan PE, Vullo D, et al. Carbonic anhydrase inhibitors. Design of selective, membrane-impermeant inhibitors targeting the human tumor-associated isozyme IX. J Med Chem 2004;47:2337–47.
  • McDonald PC, Winum JY, Supuran CT, et al. Recent developments in targeting carbonic anhydrase ix for cancer therapeutics. Oncotarget 2012;3:84.
  • Supuran CT. Carbonic anhydrases: Novel therapeutic applications for inhibitors and activators. Nature Rev Drug Discov 2008;7:168.
  • (a) Ward C, Meehan J, Gray M, et al. Carbonic anhydrase IX (CAIX), cancer, and radiation responsiveness. Metabolites 2018;8:13. (b) Krall N, Pretto F, Decurtins W, et al. A small‐molecule drug conjugate for the treatment of carbonic anhydrase IX expressing tumors. Angew Chem Int Ed Engl 2014;53:4231–5.
  • 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.
  • Faes S, Planche A, Uldry E, et al. Targeting carbonic anhydrase IX improves the anti-cancer efficacy of mTOR inhibitors. Oncotarget 2016;7:36666.
  • Swietach P, Patiar S, Supuran CT, et al. The role of carbonic anhydrase 9 in regulating extracellular and intracellular pH in three-dimensional tumor cell growths. J Biol Chem 2009;284:20299–310.
  • Maresca A, Scozzafava A, Supuran CT7. 8-disubstituted-but not 6, 7-disubstituted coumarins selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms ix and xii over the cytosolic ones i and ii in the low nanomolar/subnanomolar range. Bioorg Med Chem Lett 2010;20:7255–8.
  • Maresca A, Supuran CT. Coumarins incorporating hydroxy-and chloro-moieties selectively inhibit the transmembrane, tumor-associated carbonic anhydrase isoforms IX and XII over the cytosolic ones i and ii. Bioorg Med Chem Lett 2010;20:4511–4.
  • Supuran CT. Inhibition of carbonic anhydrase IX as a novel anticancer mechanism. W J Clin Oncol 2012;3:98.
  • Swietach P, Hulikova A, Vaughan-Jones R, et al. New insights into the physiological role of carbonic anhydrase ix in tumour ph regulation. Oncogene 2010;29:6509.
  • Durgun M, Turkmen H, Ceruso M, et al. Synthesis of schiff base derivatives of 4-(2-aminoethyl)-benzenesulfonamide with inhibitory activity against carbonic anhydrase isoforms I, II, IX and XII. Bioorg Med Chem Lett 2015;25:2377–81.
  • Koyuncu I, Gonel A, Kocyigit A, et al. Selective inhibition of carbonic anhydrase-IX by sulphonamide derivatives induces pH and reactive oxygen species-mediated apoptosis in cervical cancer HeLa cells. J Enzyme Inhib Med Chem 2018;33:1137–49.
  • Tülüce Y, Ahmed BA, Koyuncu İ, et al. The cytotoxic, apoptotic and oxidative effects of carbonic anhydrase IX inhibitor on colorectal cancer cells. J Bioenerg Biomembr 2018;50:107–16.
  • Chen R, Zou Y, Mao D, et al. The general amino acid control pathway regulates mtor and autophagy during serum/glutamine starvation. J Cell Biol 2014;206:173–82.
  • (a) McDonald PC, Swayampakula M, Dedhar S. Coordinated regulation of metabolic transporters and migration/invasion by carbonic anhydrase IX. Metabolites 2018;8:20. (b) McDonald PC, Chafe SC, Dedhar S. Overcoming hypoxia-mediated tumor progression: combinatorial approaches targeting ph regulation, angiogenesis and immune dysfunction. Front Cell Dev Biol 2016;4:27.
  • Chiche J, Ilc K, Laferrière J, et al. Hypoxia-inducible carbonic anhydrase ix and xii promote tumor cell growth by counteracting acidosis through the regulation of the intracellular ph. Cancer Res 2009;69:358–68.
  • (a) Margheri F, Ceruso M, Carta F, et al. Overexpression of the transmembrane carbonic anhydrase isoforms IX and XII in the inflamed synovium. J Enzyme Inhib Med Chem 2016;31:60–3. (b) Ahlskog JK, Dumelin CE, Trüssel S, et al. In vivo targeting of tumor-associated carbonic anhydrases using acetazolamide derivatives. Bioorg Med Chem Lett 2009;19:4851–6.
  • (a) Bozdag M, Carta F, Ceruso M, et al. Discovery of 4-Hydroxy-3-(3-(phenylureido)benzenesulfonamides as SLC-0111 analogues for the treatment of hypoxic tumors overexpressing carbonic anhydrase IX. J Med Chem 2018;61:6328–38. (b) Boyd NH, Walker K, Fried J, et al. Addition of carbonic anhydrase 9 inhibitor SLC-0111 to temozolomide treatment delays glioblastoma growth in vivo. JCI Insight 2017;2:92928.
  • Dubois L, Douma K, Supuran CT, et al. Imaging the hypoxia surrogate marker ca ix requires expression and catalytic activity for binding fluorescent sulfonamide inhibitors. Radiother Oncol 2007;83:367–73.
  • 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.
  • 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.
  • Pacchiano F, Carta F, McDonald PC, et al. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase ix and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem 2011;54:1896–902.
  • Cianchi F, Vinci MC, Supuran CT, et al. Selective inhibition of carbonic anhydrase ix decreases cell proliferation and induces ceramide-mediated apoptosis in human cancer cells. J Pharmacol Exp Ther 2010;334:710–9.
  • Parkkila S, Rajaniemi H, Parkkila AK, et al. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Nat Acad Sci. 2000;97:2220–4.
  • Giatromanolaki A, Koukourakis M, Sivridis E, et al. Relation of hypoxia inducible factor 1α and 2α in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. Br J Cancer 2001;85:881.
  • Thiry A, Dogne JM, Masereel B, et al. Targeting tumor-associated carbonic anhydrase ix in cancer therapy. Trends Pharmacol Sci 2006;27:566–73.
  • Drenckhan A, Freytag M, Supuran CT, et al. CAIX furthers tumour progression in the hypoxic tumour microenvironment of esophageal carcinoma and is a possible therapeutic target. J Enzyme Inhib Med Chem 2018;33:1024–33.
  • Pfeffer CM, Singh AT. Apoptosis: a target for anticancer therapy. Int J Mol Sci 2018;19:448.
  • Matsuyama S, Llopis J, Deveraux QL, et al. Changes in intramitochondrial and cytosolic ph: Early events that modulate caspase activation during apoptosis. Nat Cell Biol 2000;2:318.
  • Hu X, Chao M, Wu H. Central role of lactate and proton in cancer cell resistance to glucose deprivation and its clinical translation. Signal Transduct Target Ther 2017;2:16047.
  • Nobukuni T, Joaquin M, Roccio M, et al. Amino acids mediate mtor/raptor signaling through activation of class 3 phosphatidylinositol 3oh-kinase. Proc Nat Acad Scie USA 2005;102:14238–43.
  • Polak P, Hall MN. mTOR and the control of whole body metabolism. Curr Opin Cell Biol 2009;21:209–18.
  • Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495–516.
  • Marchetti P, Castedo M, Susin SA, et al. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med 1996;184:1155–60.
  • Riemann A, Ihling A, Schneider B, et al. Impact of extracellular acidosis on intracellular pH control and cell signaling in tumor cells. In: Van Huffel S, Naulaers G, Caicedo A, Bruley DF, Harrison DK, eds. Oxygen transport to tissue XXXV. New York, NY: Springer;2013:221–28.
  • Sauvant C, Nowak M, Wirth C, et al. Acidosis induces multi-drug resistance in rat prostate cancer cells (AT1) in vitro and in vivo by increasing the activity of the p-glycoprotein via activation of p38. Int J Cancer 2008;123:2532–42.
  • Lagadic-Gossmann D, Huc L, Lecureur V. Alterations of intracellular pH homeostasis in apoptosis: origins and roles. Cell Death Differ 2004;11:953
  • Tomoda A, Tsuda-Hirota S, Minakami S. Glycolysis of red cells suspended in solutions of impermeable solutes: intracellular ph and glycolysis. J Biochem 1977;81:697–701.