The carbonic anhydrase IX inhibitor SLC-0111 sensitises cancer cells to conventional chemotherapy

References

• Pan ST, Li ZL, He ZX, et al. Molecular mechanisms for tumour resistance to chemotherapy. Clin Exp Pharmacol Physiol 2016;3:723–37.
   Web of Science ®Google Scholar
• Nikolaou M, Pavlopoulou A, Georgakilas AG, Kyrodimos E. The challenge of drug resistance in cancer treatment: a current overview. Clin Exp Metastasis 2018;35:309–18.
   PubMed Web of Science ®Google Scholar
• Senthebane DA, Rowe A, Thomford NE, et al. The role of tumor microenvironment in chemoresistance: to survive, keep your enemies closer. Int J Mol Sci 2017;18:E7.
   Web of Science ®Google Scholar
• Son B, Lee S, Youn H, et al. The role of tumor microenvironment in therapeutic resistance. Oncotarget 2017;8:3933–45.
   PubMedGoogle Scholar
• Sowa T, Menju T, Chen-Yoshikawa TF, et al. Hypoxia-inducible factor 1 promotes chemoresistance of lung cancer by inducing carbonic anhydrase IX expression. Cancer Med 2017;6:288–97.
   PubMed Web of Science ®Google Scholar
• Mahoney BP, Raghunand N, Baggett B, Gillies RJ. Tumor acidity, ion trapping and chemotherapeutics. I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol 2003;66:1207–18.
   PubMed Web of Science ®Google Scholar
• Raghunand N, Mahoney BP, Gillies RJ. Tumor acidity, ion trapping and chemotherapeutics. II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. Biochem Pharmacol 2003; 66:1219–29.
   PubMed Web of Science ®Google Scholar
• (a) Supuran CT. Carbonic anhydrase inhibitors. Bioorg Med Chem Lett 2010;20:3467–74; (b) Supuran CT. Carbon- versus sulphur-based zinc binding groups for carbonic anhydrase inhibitors? J Enzyme Inhib Med Chem 2018;33: 485–95; (c) Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81; (d) Supuran CT. Structure-based drug discovery of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem 2012;27:759–72.
   PubMed Web of Science ®Google Scholar
• (a) McDonald PC, Winum JY, Supuran CT, Dedhar S. Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 2012;3:84–97; (b) Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88; (c) Supuran CT. Structure and function of carbonic anhydrases. Biochem J 2016;473:2023–32; (d) Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:E48.
   PubMed Web of Science ®Google Scholar
• Andreucci E, Peppicelli S, Carta F, et al. Carbonic anhydrase IX inhibition affects viability of cancer cells adapted to extracellular acidosis. J Mol Med (Berl) 2017;95:1341–53.
   PubMed Web of Science ®Google Scholar
• Ihnatko R, Kubes M, Takacova M, et al. Extracellular acidosis elevates carbonic anhydrase IX in human glioblastoma cells via transcriptional modulation that does not depend on hypoxia. Int J Oncol 2006;29:1025–33.
   PubMed Web of Science ®Google Scholar
• (a) Ameis HM, Drenckhan A, Freytag M, et al. Carbonic anhydrase IX correlates with survival and is a potential therapeutic target for neuroblastoma. J Enzyme Inhib Med Chem 2016;31:404–9; (b) 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
   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
• (a) 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(9):3364–76; (b) Pacchiano F, Aggarwal M, Avvaru BS, et al. Selective hydrophobic pocket binding observed within the carbonic anhydrase II active site accommodate different 4-substituted-ureido-benzenesulfonamides and correlate to inhibitor potency. Chem Commun (Camb). 2010;46:8371–73.
   PubMed Web of Science ®Google Scholar
• Ilie M, Mazure NM, Hofman V, et al. High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer. Br J Cancer 2010;102:1627–35.
   PubMed Web of Science ®Google Scholar
• Hussain SA, Ganesan R, Reynolds G, et al. Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer 2007;96:104–9.
   PubMed Web of Science ®Google Scholar
• (a) 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; (b) 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;38:1799–1836; doi:10.1002/med.21497; (c) Borras J, Scozzafava A, Menabuoni L, et al. Carbonic anhydrase inhibitors: synthesis of water-soluble, topically effective intraocular pressure lowering aromatic/heterocyclic sulfonamides containing 8-quinoline-sulfonyl moieties: is the tail more important than the ring? Bioorg Med Chem. 1999;7:2397–406.
   PubMed Web of Science ®Google Scholar
• (a) 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; (b) Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60; (c) Alterio V, Di Fiore A, D'Ambrosio K, Supuran CT, De Simone, G. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 2012;112:4421–68.
   PubMed Web of Science ®Google Scholar
• Vaeteewoottacharn K, Kariya R, Dana P, et al. Inhibition of carbonic anhydrase potentiates bevacizumab treatment in cholangiocarcinoma. Tumour Biol 2016; 37:9023–35.
   PubMedGoogle Scholar
• Webb BA, Chimenti M, Jacobson MP, Barber DL. Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer 2011; 11:671–7.
   PubMed Web of Science ®Google Scholar
• Peppicelli S, Bianchini F, Calorini L. Extracellular acidity, a "reappreciated" trait of tumor environment driving malignancy: perspectives in diagnosis and therapy. Cancer Metastasis Rev 2014; 33:823–32.
   PubMed Web of Science ®Google Scholar
• Ruzzolini J, Peppicelli S, Andreucci E, et al. Everolimus selectively targets vemurafenib resistant BRAF(V600E) melanoma cells adapted to low pH. Cancer Lett 2017; 408:43–54.
   PubMed Web of Science ®Google Scholar
• Davey RJ, van der Westhuizen A, Bowden NA. Metastatic melanoma treatment: combining old and new therapies. Crit Rev Oncol Hematol 2016; 98:242–53.
   PubMed Web of Science ®Google Scholar
• Tentori L, Lacal PM, Graziani G. Challenging resistance mechanisms to therapies for metastatic melanoma. Trends Pharmacol Sci 2013; 34:656–66.
   PubMed Web of Science ®Google Scholar
• Gogas HJ, Kirkwood JM, Sondak VK. Chemotherapy for metastatic melanoma: time for a change? Cancer 2007; 109:455–64.
   PubMed Web of Science ®Google Scholar
• Quirt I, Verma S, Petrella T, et al. Temozolomide for the treatment of metastatic melanoma: a systematic review. Oncologist 2007;12:1114–23.
   PubMed Web of Science ®Google Scholar
• Lovitt CJ, Shelper TB, Avery VM. Doxorubicin resistance in breast cancer cells is mediated by extracellular matrix proteins. BMC Cancer 2018; 18:E41.
   PubMed Web of Science ®Google Scholar
• Davis T, van Niekerk G, Peres J, et al. Doxorubicin resistance in breast cancer: A novel role for the human protein AHNAK. Biochem Pharmacol 2018;148:174–83.
   PubMed Web of Science ®Google Scholar
• Wang X, Teng Z, Wang H, et al. Increasing the cytotoxicity of doxorubicin in breast cancer MCF-7 cells with multidrug resistance using a mesoporous silica nanoparticle drug delivery system. Int J Clin Exp Pathol 2014;7:1337–47.
   PubMed Web of Science ®Google Scholar
• Smith L, Watson MB, O'Kane SL, et al. The analysis of doxorubicin resistance in human breast cancer cells using antibody microarrays. Mol Cancer Ther 2006;5:2115–20.
   PubMed Web of Science ®Google Scholar
• He J, Pei L, Jiang H, et al. Chemoresistance of colorectal cancer to 5-fluorouracil is associated with silencing of the BNIP3 gene through aberrant methylation. J Cancer 2017;8:1187–96.
   PubMed Web of Science ®Google Scholar
• Bracht K, Nicholls AM, Liu Y, Bodmer WF. 5-Fluorouracil response in a large panel of colorectal cancer cell lines is associated with mismatch repair deficiency. Br J Cancer 2010;103:340–6.
   PubMed Web of Science ®Google Scholar
• (a) Wojtkowiak JW, Verduzco D, Schramm KJ, Gillies RJ. Drug resistance and cellular adaptation to tumor acidic pH microenvironment. Mol Pharm 2011;8:2032–8; (b) 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
• (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) McDonald PC, Swayampakula M, Dedhar S. Coordinated regulation of metabolic transporters and migration/invasion by carbonic anhydrase IX. Metabolites 2018;8:E20; (c) 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.
   PubMed Web of Science ®Google Scholar