2,182
Views
11
CrossRef citations to date
0
Altmetric
Brief Report

The three-tails approach as a new strategy to improve selectivity of action of sulphonamide inhibitors against tumour-associated carbonic anhydrase IX and XII

, , , , , , ORCID Icon, ORCID Icon, , , , ORCID Icon & ORCID Icon show all
Pages 930-939 | Received 12 Feb 2022, Accepted 10 Mar 2022, Published online: 21 Mar 2022

References

  • Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77.
  • Thiry A, Dogné JM, Masereel B, et al. Targeting tumor-associated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 2006;27:566–73.
  • Semenza GL. Hypoxia and cancer. Cancer Metastasis Rev 2007;26:223–4.
  • Brahimi-Horn MC, Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett 2007;581:3582–91.
  • Hon WC, Wilson MI, Harlos K, et al. Structural basis for the recognition of hydroxyproline in HIF-1 alpha by pVHL. Nature 2002;417:975–8.
  • Vaupel P, Multhoff G. Revisiting the Warburg effect: historical dogma versus current understanding. J Physiol 2021;599:1745–57.
  • Vaupel P, Schmidberger H, Mayer A. The Warburg effect: essential part of metabolic reprogramming and central contributor to cancer progression. Int J Radiat Biol 2019;95:912–9.
  • Riemann A, Schneider B, Gündel D, et al. Acidosis promotes metastasis formation by enhancing tumor cell motility. Adv Exp Med Biol 2016;876:215–20.
  • Supuran CT. Carbonic anhydrase inhibitors: an update on experimental agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2021;30:1197–208.
  • Alterio V, Hilvo M, Di Fiore A, et al. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc Natl Acad Sci USA 2009;106:16233–8.
  • Whittington DA, Waheed A, Ulmasov B, et al. Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Proc Natl Acad Sci USA 2001;98:9545–50.
  • Chafe SC, Vizeacoumar FS, Venkateswaran G, et al. Genome-wide synthetic lethal screen unveils novel CAIX-NFS1/xCT axis as a targetable vulnerability in hypoxic solid tumors. Sci Adv 2021;7:eabj0364.
  • Koukourakis MI, Giatromanolaki A, Sivridis E, et al. Hypoxia-activated tumor pathways of angiogenesis and pH regulation independent of anemia in head-and-neck cancer. Int J Radiat Oncol Biol Phys 2004;59:67–71.
  • Angeli A, Carta F, Nocentini A, et al. Carbonic anhydrase inhibitors targeting metabolism and tumor microenvironment. Metabolites 2020;10:412.
  • Potter CP, Harris AL. Diagnostic, prognostic and therapeutic implications of carbonic anhydrases in cancer. Br J Cancer 2003;89:2–7.
  • McDonald PC, Chafe SC, Brown WS, et al. Regulation of pH by carbonic anhydrase 9 mediates survival of pancreatic cancer cells with activated KRAS in response to hypoxia. Gastroenterology 2019;157:823–37.
  • Swinson DE, Jones JL, Richardson D, et al. Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer. J Clin Oncol 2003;21:473–82.
  • Swayampakula M, McDonald PC, Vallejo M, et al. The interactome of metabolic enzyme carbonic anhydrase IX reveals novel roles in tumor cell migration and invadopodia/MMP14-mediated invasion. Oncogene 2017;36:6244–61.
  • Supuran CT. Experimental carbonic anhydrase inhibitors for the treatment of hypoxic tumors. J Exp Pharmacol 2020;12:603–17.
  • Hutchison GJ, Valentine HR, Loncaster JA, et al. West hypoxia-inducible factor 1alpha expression as an intrinsic marker of hypoxia: correlation with tumor oxygen, pimonidazole measurements, and outcome in locally advanced carcinoma of the cervix. Clin Cancer Res 2004;10:8405–12.
  • Dorai T, Sawczuk I, Pastorek J, et al. Role of carbonic anhydrases in the progression of renal cell carcinoma subtypes: proposal of a unified hypothesis. Cancer Invest 2006;24:754–79.
  • Cazzamalli S, Ziffels B, Widmayer F, et alD. Enhanced therapeutic activity of non-internalizing small-molecule-drug conjugates targeting carbonic anhydrase IX in combination with targeted interleukin-2. Clin Cancer Res 2018;24:3656–67.
  • Testa C, Papini AM, Zeidler R, et al. First studies on tumor associated carbonic anhydrases IX and XII monoclonal antibodies conjugated to small molecule inhibitors. J Enzyme Inhib Med Chem 2022;37:592–6.
  • Maxwell PH, Wiesener MS, Chang CW, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271–5.
  • Jaakkola P, Mole DR, Tian YM, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001; 292:468–72.
  • Tong CK, Brion LP, Suarez C, et al. Interstitial carbonic anhydrase (CA) activity in brain is attributable to membrane-bound CA type IV. J Neurosci 2000;20:8247–53.
  • Svichar N, Chesler M. Surface carbonic anhydrase activity on astrocytes and neurons facilitates lactate transport. Glia 2003;41:415–9.
  • Svichar N, Esquenazi S, Waheed A, et al. Functional demonstration of surface carbonic anhydrase IV activity on rat astrocytes. Glia 2006;53:241–7.
  • Stridh MH, Alt MD, Wittmann S, et al. Lactate flux in astrocytes is enhanced by a non-catalytic action of carbonic anhydrase II. J Physiol 2012;590:2333–51.
  • Forero-Quintero LS, Ames S, Schneider H-P, et al. Membrane-anchored carbonic anhydrase IV interacts with monocarboxylate transporters via their chaperones CD147 and GP70. J Biol Chem 2019;294:593–607.
  • Ferrari S, Di Iorio E, Barbaro V, et al. Retinitis pigmentosa: genes and disease mechanisms. Curr Genomics 2011;12:238–49.
  • Pacchiano F, Carta F, McDonald PC, et al. Supuran. 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.
  • 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;46:8371–3.
  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
  • Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
  • Bonardi A, Nocentini A, Bua S, et al. Sulfonamide inhibitors of human carbonic anhydrases designed through a three-tails approach: improving ligand/isoform matching and selectivity of action. J Med Chem 2020;63:7422–44.
  • Scozzafava A, Menabuoni L, Mincione F, et al. Carbonic anhydrase inhibitors. Synthesis of water-soluble, topically effective, intraocular pressure-lowering aromatic/heterocyclic sulfonamides containing cationic or anionic moieties: is the tail more important than the ring. J Med Chem 1999;42:2641–50.
  • Tanpure RP, Ren B, Peat TS, et al. Carbonic anhydrase inhibitors with dual-tail moieties to match the hydrophobic and hydrophilic halves of the carbonic anhydrase active site. J Med Chem 2015;58:1494–501.
  • Fares M, Eldehna WM, Bua S, et al. Discovery of potent dual-tailed benzenesulfonamide inhibitors of human carbonic anhydrases implicated in glaucoma and in vivo profiling of their intraocular pressure-lowering action. J Med Chem 2020;63:3317–26.
  • Wilkinson BL, Bornaghi LF, Houston TA, et al. A novel class of carbonic anhydrase inhibitors: glycoconjugate benzene sulfonamides prepared by “click-tailing”. J Med Chem 2006;49:6539–48.
  • Khalifah RG. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 1971;246:2561–73.
  • Petreni A, Bonardi A, Lomelino C, et al. Inclusion of a 5-fluorouracil moiety in nitrogenous bases derivatives as human carbonic anhydrase IX and XII inhibitors produced a targeted action against MDA-MB-231 and T47D breast cancer cells. Eur J Med Chem 2020;190:112112.
  • a) Scozzafava A, Briganti F, Mincione G, et al. Carbonic anhydrase inhibitors: synthesis of water-soluble, aminoacyl/dipeptidyl sulfonamides possessing long-lasting intraocular pressure-lowering properties via the topical route. J Med Chem 2021;42:3669–700; b) Berrino E, Michelet B, Martin-Mingot A, et al. Modulating the efficacy of carbonic anhydrase inhibitors through fluorine substitution. Angew Chem Int Ed Engl 60: 23068–82.
  • Pinard MA, Boone CD, Rife BD, et al. Structural study of interaction between brinzolamide and dorzolamide inhibition of human carbonic anhydrases. Bioorg Med Chem 2013;21:7210–5.
  • Tanhauser SM, Jewell DA, Tu CK, et al. A T7 expression vector optimized for site-directed mutagenesis using oligodeoxyribonucleotide cassettes. Gene 1992;117:113–7.
  • Kabsch W. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 2010;66:133–44.
  • Evans PR, Murshudov GN. How good are my data and what is the resolution? Acta Crystallogr D Biol Crystallogr 2013;69:1204–14.
  • Winn MD, Ballard CC, Cowtan KD, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 2011;67:235–42.
  • Avvaru BS, Kim CU, Sippel KH, et al. A short, strong hydrogen bond in the active site of human carbonic anhydrase II. Biochemistry 2010;49:249–51.
  • Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004;D60:2126–32.
  • Adams PD, Afonine PV, Bunkoczi G, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 2010;66:213–21.
  • Laskowski RA, Swindells MB. LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model 2011;51:2778–86.
  • a) Nocentini A, Supuran CT. Advances in the structural annotation of human carbonic anhydrases and impact on future drug discovery. Expert Opin Drug Discovery 14:1175–97; b) Supuran CT. Emerging role of carbonic anhydrase inhibitors. Clin Sci (Lond) 2021;135:1233–49.
  • Terry S, Buart S, Chouaib S. Hypoxic stress-induced tumor and immune plasticity, suppression, and impact on tumor heterogeneity. Front Immunol 2017;8:1625.
  • 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;38:1799–836.
  • Bua S, Lucarini L, Micheli L, et al. Bioisosteric development of multitarget nonsteroidal anti-inflammatory drug-carbonic anhydrases inhibitor hybrids for the management of rheumatoid arthritis. J Med Chem 2020;63:2325–42.
  • a) 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. b) Nocentini A, Angeli A, Carta F, et al. Reconsidering anion inhibitors in the general context of drug design studies of modulators of activity of the classical enzyme carbonic anhydrase. J Enzyme Inhib Med Chem 2021;36:561–80.
  • Bua S, Supuran CT. Diagnostic markers for glaucoma: a patent and literature review (2013-2019). Expert Opin Ther Pat 2019;29:829–39.