2H-chromene and 7H-furo-chromene derivatives selectively inhibit tumour associated human carbonic anhydrase IX and XII isoforms

References

• Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2020. CA Cancer J Clin. 2020;70(1):7–30.
   PubMed Web of Science ®Google Scholar
• Whiteman DC, Wilson LF. The fractions of cancer attributable to modifiable factors: a global review. Cancer Epidemiol. 2016;44:203–221.
   PubMed Web of Science ®Google Scholar
• Mihor A, Tomsic S, Zagar T, Lokar K, Zadnik V. Socioeconomic inequalities in cancer incidence in Europe: a comprehensive review of population-based epidemiological studies. Radiol Oncol. 2020;54(1):1–13.
   PubMed Web of Science ®Google Scholar
• Wu HX, Zhuo KQ, Wang K. Efficacy of targeted therapy in patients with HER2-positive non-small cell lung cancer: a systematic review and meta-analysis. Br J Clin Pharmacol. 2022;88(5):2019–2034.
   PubMed Web of Science ®Google Scholar
• Modi S, Jacot W, Yamashita T, Sohn J, Vidal M, Tokunaga E, Tsurutani J, Ueno NT, Prat A, Chae YS, et al. Trastuzumab deruxtecan in previously treated HER2-low advanced breast cancer. N Engl J Med. 2022;387(1):9–20.
   PubMed Web of Science ®Google Scholar
• Zhang M, Fan Y, Nie L, Wang G, Sun K, Cheng Y. Clinical outcomes of immune checkpoint inhibitor therapy in patients with advanced non-small cell lung cancer and preexisting interstitial lung diseases: a systematic review and meta-analysis. Chest. 2022;161(6):1675–1686.
   PubMed Web of Science ®Google Scholar
• Jaaks P, Coker EA, Vis DJ, Edwards O, Carpenter EF, Leto SM, Dwane L, Sassi F, Lightfoot H, Barthorpe S, et al. Effective drug combinations in breast, colon and pancreatic cancer cells. Nature. 2022;603(7899):166–173.
   PubMed Web of Science ®Google Scholar
• Global Burden of Disease Cancer Collaboration. The global burden of cancer 2013. JAMA Oncol. 2015;1(4):505–527.
   PubMed Web of Science ®Google Scholar
• de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis. Lancet Glob Health. 2020;8(2):e180–e190.
   PubMed Web of Science ®Google Scholar
• Supuran C. Carbonic anhydrases: an overview. Curr Pharm Des. 2008;14(7):603–614.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases. Bioorg Med Chem. 2013;21(6):1377–1378.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Supuran CT, Capasso C. An overview on the recently discovered iota-carbonic anhydrases. J Enzyme Inhib Med Chem. 2021;36(1):1988–1995.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites. 2017;7(4):56–74.
   PubMed Web of Science ®Google Scholar
• Angeli A, Pinteala M, Maier SS, Del Prete S, Capasso C, Simionescu BC, Supuran CT. Inhibition of α-, β-, γ-, δ-, ζ- and η-class carbonic anhydrases from bacteria, fungi, algae, diatoms and protozoans with famotidine. J Enzyme Inhib Med Chem. 2019;34(1):644–650.
   PubMed Web of Science ®Google Scholar
• Angeli A, Del Prete S, Alasmary FAS, Alqahtani LS, AlOthman Z, Donald WA, Capasso C, Supuran CT. The first activation studies of the η-carbonic anhydrase from the malaria parasite Plasmodium falciparum with amines and amino acids. Bioorg Chem. 2018;80:94–98.
   PubMed Web of Science ®Google Scholar
• Schlicker C, Hall RA, Vullo D, Middelhaufe S, Gertz M, Supuran CT, Mühlschlegel FA, Steegborn C. Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. J Mol Biol. 2009;385(4):1207–1220.
   PubMed Web of Science ®Google Scholar
• Maren TH. Carbonic anhydrase: chemistry, physiology, and inhibition. Physiol Rev. 1967;47(4):595–781.
   PubMed Web of Science ®Google Scholar
• Singh S, Lomelino CL, Mboge MY, Frost SC, McKenna R. Cancer drug development of carbonic anhydrase inhibitors beyond the active site. Molecules. 2018;23(5):1045–1066.
   PubMed Web of Science ®Google Scholar
• Hilvo M, Tolvanen M, Clark A, Shen B, Shah GN, Waheed A, Halmi P, Hänninen M, Hämäläinen JM, Vihinen M, et al. Characterization of CA XV, a new GPI-anchored form of carbonic anhydrase. Biochem J. 2005;392(Pt 1):83–92.
   PubMedGoogle Scholar
• Ozensoy Guler O, Capasso C, Supuran CT. A magnificent enzyme superfamily: carbonic anhydrases, their purification and characterization. J Enzyme Inhib Med Chem. 2016;31(5):689–694.
   PubMed Web of Science ®Google Scholar
• Frost SC. Physiological functions of the alpha class of carbonic anhydrases. In: Frost SC, McKenna R, editors. Carbonic anhydrase: mechanism, regulation, links to disease, and industrial applications. Dordrecht: Springer Netherlands; 2014. p. 9–30.
   Google Scholar
• Mboge MY, Mahon BP, McKenna R, Frost SC. Carbonic anhydrases: role in pH control and cancer. Metabolites. 2018;8(1):19–50.
   PubMed Web of Science ®Google Scholar
• Pastorekova S, Parkkila S, Závada J. Tumor‐associated carbonic anhydrases and their clinical significance. Adv Clin Chem. 2006;42:167–216.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Alterio V, Di Fiore A, D' Ambrosio K, Carta F, Monti SM, De Simone G. Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: three for the price of one. Med Res Rev. 2018;38(6):1799–1836.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Donald WA, Supuran CT. Chapter 8 – human carbonic anhydrases: tissue distribution, physiological role, and druggability. In: Supuran CT, Nocentini A, editors. Carbonic anhydrases. Cham, Switzerland: Academic Press; 2019. p. 151–185.
   Google Scholar
• Becker HM. Carbonic anhydrase IX and acid transport in cancer. Br J Cancer. 2020;122(2):157–167.
   PubMed Web of Science ®Google Scholar
• Ondriskova E, Debreova M, Pastorekova S. Chapter 10 – tumor-associated carbonic anhydrases IX and XII. In: Supuran CT, De Simone G, editors. Carbonic anhydrases as biocatalysts. Amsterdam: Elsevier; 2015. p. 169–205.
   Google Scholar
• Pastorekova S, Gillies RJ. The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond. Cancer Metastasis Rev. 2019;38(1–2):65–77.
   PubMed Web of Science ®Google Scholar
• Aldera AP, Govender D. Carbonic anhydrase IX: a regulator of pH and participant in carcinogenesis. J Clin Pathol. 2021;74(6):350–354.
   Web of Science ®Google Scholar
• Wingo T, Tu C, Laipis PJ, Silverman DN. The catalytic properties of human carbonic anhydrase IX. Biochem Biophys Res Commun. 2001;288(3):666–669.
   PubMed Web of Science ®Google Scholar
• Türeci Ö, Sahin U, Vollmar E, Siemer S, Göttert E, Seitz G, Parkkila A-K, Shah GN, Grubb JH, Pfreundschuh M, et al. Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is overexpressed in some renal cell cancers. Proc Natl Acad Sci U S A. 1998;95(13):7608–7613.
   PubMed Web of Science ®Google Scholar
• Parkkila S, Parkkila A-K, Saarnio J, Kivelä J, Karttunen TJ, Kaunisto K, Waheed A, Sly WS, Türeci Ö, Virtanen I, et al. Expression of the membrane-associated carbonic anhydrase isozyme XII in the human kidney and renal tumors. J Histochem Cytochem. 2000;48(12):1601–1608.
   PubMed Web of Science ®Google Scholar
• Waheed A, Sly WS. Carbonic anhydrase XII functions in health and disease. Gene. 2017;623:33–40.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors and activators for novel therapeutic applications. Future Med Chem. 2011;3(9):1165–1180.
   PubMed Web of Science ®Google Scholar
• Mishra CB, Tiwari M, Supuran CT. Progress in the development of human carbonic anhydrase inhibitors and their pharmacological applications: where are we today? Med Res Rev. 2020;40(6):2485–2565.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov. 2008;7(2):168–181.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Supuran CT. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: a patent review (2008–2018). Expert Opin Ther Pat. 2018;28(10):729–740.
   PubMed Web of Science ®Google Scholar
• Al-Warhi T, Sabt A, Elkaeed EB, Eldehna WM. Recent advancements of coumarin-based anticancer agents: an up-to-date review. Bioorg Chem. 2020;103:104163–104178.
   PubMed Web of Science ®Google Scholar
• Annunziata F, Pinna C, Dallavalle S, Tamborini L, Pinto A. An overview of coumarin as a versatile and readily accessible scaffold with broad-ranging biological activities. Int J Mol Sci. 2020;21(13):4618–4699.
   PubMed Web of Science ®Google Scholar
• Riveiro EM, De Kimpe N, Moglioni A, Vazquez R, Monczor F, Shayo C, Davio C. Coumarins: old compounds with novel promising therapeutic perspectives. Curr Med Chem. 2010;17(13):1325–1338.
   PubMed Web of Science ®Google Scholar
• Wardrop D, Keeling D. The story of the discovery of heparin and warfarin. Br J Haematol. 2008;141(6):757–763.
   PubMed Web of Science ®Google Scholar
• Au N, Rettie AE. Pharmacogenomics of 4-hydroxycoumarin anticoagulants. Drug Metab Rev. 2008;40(2):355–375.
   PubMed Web of Science ®Google Scholar
• Dawood D, Batran R, Farghaly T, Khedr M, Abdalla M. New coumarin derivatives as potent selective COX-2 inhibitors: synthesis, anti-inflammatory, QSAR, and molecular modeling studies. Arch Pharm. 2015;348:878–888.
   Web of Science ®Google Scholar
• de Souza LG, Rennã MN, Figueroa-Villar JD. Coumarins as cholinesterase inhibitors: a review. Chem Biol Interact. 2016;254:11–23.
   PubMed Web of Science ®Google Scholar
• Salar U, Khan KM, Jabeen A, Faheem A, Naqvi F, Ahmed S, Iqbal E, Ali F, Kanwal  , Perveen S. ROS inhibitory activity and cytotoxicity evaluation of benzoyl, acetyl, alkyl ester, and sulfonate ester substituted coumarin derivatives. Med Chem. 2020;16(8):1099–1111.
   PubMed Web of Science ®Google Scholar
• Gormley NA, Orphanides G, Meyer A, Cullis PM, Maxwell A. The interaction of coumarin antibiotics with fragments of the DNA gyrase B protein. Biochemistry. 1996;35(15):5083–5092.
   PubMed Web of Science ®Google Scholar
• Shaikh M, Subhedar D, Khan F, Sangshetti J, Shingate B. 1,2,3-Triazole incorporated coumarin derivatives as potential antifungal and antioxidant agents. Chin Chem Lett. 2016;27(2):295–301.
   Web of Science ®Google Scholar
• Campagna M, Rivas C. Antiviral activity of resveratrol. Biochem Soc Trans. 2010;38(Pt 1):50–53.
   PubMedGoogle Scholar
• Goud NS, Kumar P, Bharath R. Recent developments of target based coumarin derivatives as potential anticancer agents. Mini Rev Med Chem. 2020;20(17):1754–1766.
   PubMed Web of Science ®Google Scholar
• Küpeli Akkol E, Genç Y, Karpuz B, Sobarzo-Sánchez E, Capasso R. Coumarins and coumarin-related compounds in pharmacotherapy of cancer. Cancers. 2020;12(7):1959–1984.
   PubMed Web of Science ®Google Scholar
• Melis C, Distinto S, Bianco G, Meleddu R, Cottiglia F, Fois B, Taverna D, Angius R, Alcaro S, Ortuso F, et al. Targeting tumor associated carbonic anhydrases IX and XII: highly isozyme selective coumarin and psoralen inhibitors. ACS Med Chem Lett. 2018;9(7):725–729.
   PubMed Web of Science ®Google Scholar
• Meleddu R, Deplano S, Maccioni E, Ortuso F, Cottiglia F, Secci D, Onali A, Sanna E, Angeli A, Angius R, et al. Selective inhibition of carbonic anhydrase IX and XII by coumarin and psoralen derivatives. J Enzyme Inhib Med Chem. 2021;36(1):685–692.
   PubMed Web of Science ®Google Scholar
• Fois B, Distinto S, Meleddu R, Deplano S, Maccioni E, Floris C, Rosa A, Nieddu M, Caboni P, Sissi C, et al. Coumarins from Magydaris pastinacea as inhibitors of the tumour-associated carbonic anhydrases IX and XII: isolation, biological studies and in silico evaluation. J Enzyme Inhib Med Chem. 2020;35(1):539–548.
   PubMed Web of Science ®Google Scholar
• Park H, Choe H, Hong S. Virtual screening and biochemical evaluation to identify new inhibitors of mammalian target of rapamycin (mTOR). Bioorg Med Chem Lett. 2014;24(3):835–838.
   PubMed Web of Science ®Google Scholar
• Mi C, Ma J, Wang KS, Zuo HX, Wang Z, Li MY, Piao LX, Xu GH, Li X, Quan ZS, et al. Imperatorin suppresses proliferation and angiogenesis of human colon cancer cell by targeting HIF-1α via the mTOR/p70S6K/4E-BP1 and MAPK pathways. J Ethnopharmacol. 2017;203:27–38.
   PubMed Web of Science ®Google Scholar
• Ma C-C, Liu Z-P. Design and synthesis of coumarin derivatives as novel PI3K inhibitors. Anticancer Agents Med Chem. 2017;17(3):395–403.
   PubMed Web of Science ®Google Scholar
• Menezes JC, Diederich M. Translational role of natural coumarins and their derivatives as anticancer agents. Future Med Chem. 2019;11(9):1057–1082.
   PubMed Web of Science ®Google Scholar
• Meleddu R, Maccioni E, Distinto S, Bianco G, Melis C, Alcaro S, Cottiglia F, Ceruso M, Supuran CT. New 4-[(3-cyclohexyl-4-aryl-2,3-dihydro-1,3-thiazol-2-ylidene)amino]benzene-1-sulfonamides, synthesis and inhibitory activity toward carbonic anhydrase I, II, IX, XII. Bioorg Med Chem Lett. 2015;25(16):3281–3284.
   PubMed Web of Science ®Google Scholar
• Melis C, Meleddu R, Angeli A, Distinto S, Bianco G, Capasso C, Cottiglia F, Angius R, Supuran CT, Maccioni E. Isatin: a privileged scaffold for the design of carbonic anhydrase inhibitors. J Enzyme Inhib Med Chem. 2017;32(1):68–73.
   PubMed Web of Science ®Google Scholar
• Distinto S, Meleddu R, Ortuso F, Cottiglia F, Deplano S, Sequeira L, Melis C, Fois B, Angeli A, Capasso C, et al. Exploring new structural features of the 4-[(3-methyl-4-aryl-2,3-dihydro-1,3-thiazol-2-ylidene)amino]benzenesulphonamide scaffold for the inhibition of human carbonic anhydrases. J Enzyme Inhib Med Chem. 2019;34(1):1526–1533.
   PubMed Web of Science ®Google Scholar
• Skaraitė I, Maccioni E, Petrikaitė V. Anticancer activity of sunitinib analogues in human pancreatic cancer cell cultures under normoxia and hypoxia. Int J Mol Sci. 2023;24(6):5422.
   PubMed Web of Science ®Google Scholar
• Di Maria S, Picarazzi F, Mori M, Cianciusi A, Carbone A, Crespan E, Perini C, Sabetta S, Deplano S, Poggialini F, et al. Novel pyrazolo[3,4-d]pyrimidines as dual Src/Bcr-Abl kinase inhibitors: synthesis and biological evaluation for chronic myeloid leukemia treatment. Bioorg Chem. 2022;128:106071.
   PubMed Web of Science ®Google Scholar
• Maresca A, Temperini C, Pochet L, Masereel B, Scozzafava A, Supuran CT. Deciphering the mechanism of carbonic anhydrase inhibition with coumarins and thiocoumarins. J Med Chem. 2010;53(1):335–344.
   PubMed Web of Science ®Google Scholar
• Bilginer S, Gonder B, Gul HI, Kaya R, Gulcin I, Anil B, Supuran CT. Novel sulphonamides incorporating triazene moieties show powerful carbonic anhydrase I and II inhibitory properties. J Enzyme Inhib Med Chem. 2020;35(1):325–329.
   PubMed Web of Science ®Google Scholar
• Maresca A, Temperini C, Vu H, Pham NB, Poulsen S-A, Scozzafava A, Quinn RJ, Supuran CT. Non-zinc mediated inhibition of carbonic anhydrases: coumarins are a new class of suicide inhibitors. J Am Chem Soc. 2009;131(8):3057–3062.
   PubMed Web of Science ®Google Scholar
• Mohamadi F, Richards NGJ, Guida WC, Liskamp R, Lipton M, Caufield C, Chang G, Hendrickson T, Still WC. Macromodel—an integrated software system for modeling organic and bioorganic molecules using molecular mechanics. J Comput Chem. 1990;11(4):440–467.
   Web of Science ®Google Scholar
• Halgren TA. Merck molecular force field. II. MMFF94 van der Waals and electrostatic parameters for intermolecular interactions. J Comput Chem. 1996;17(5–6):520–552.
   Web of Science ®Google Scholar
• Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, Chong L, Lee M, Lee T, Duan Y, Wang W, et al. Calculating structures and free energies of complex molecules:  combining molecular mechanics and continuum models. Acc Chem Res. 2000;33(12):889–897.
   PubMed Web of Science ®Google Scholar
• Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res. 2000;28(1):235–242.
   PubMed Web of Science ®Google Scholar
• Leitans J, Kazaks A, Balode A, Ivanova J, Zalubovskis R, Supuran CT, Tars K. Efficient expression and crystallization system of cancer-associated carbonic anhydrase isoform IX. J Med Chem. 2015;58(22):9004–9009.
   PubMed Web of Science ®Google Scholar
• Smirnov A, Zubrienė A, Manakova E, Gražulis S, Matulis D. Crystal structure correlations with the intrinsic thermodynamics of human carbonic anhydrase inhibitor binding. PeerJ. 2018;6:e4412.
   PubMed Web of Science ®Google Scholar
• Chung JY, Hah J-M, Cho AE. Correlation between performance of QM/MM docking and simple classification of binding sites. J Chem Inf Model. 2009;49(10):2382–2387.
   PubMed Web of Science ®Google Scholar
• 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(8):2561–2573.
   PubMed Web of Science ®Google Scholar
• Berrino E, Angeli A, Zhdanov DD, Kiryukhina AP, Milaneschi A, De Luca A, Bozdag M, Carradori S, Selleri S, Bartolucci G, et al. Azidothymidine “Clicked” into 1,2,3-triazoles: first report on carbonic anhydrase–telomerase dual-hybrid inhibitors. J Med Chem. 2020;63(13):7392–7409.
   PubMed Web of Science ®Google Scholar
• Pacchiano F, Carta F, McDonald PC, Lou Y, Vullo D, Scozzafava A, Dedhar S, Supuran CT. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem. 2011;54(6):1896–1902.
   PubMed Web of Science ®Google Scholar