Selenium-analogs based on natural sources as cancer-associated carbonic anhydrase isoforms IX and XII inhibitors

References

• Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016;473(14):2023–2032.
   PubMedGoogle Scholar
• Supuran CT. Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs. 2018;27(12):963–970.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Supuran CT. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: a patent review. Expert Opin Ther Pat. 2018;28(10):729–740.
   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
• Chiche J, Ilc K, Laferrière J, Trottier E, Dayan F, Mazure NM, Brahimi-Horn MC, Pouysségur J, 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(1):358–368.
   PubMed Web of Science ®Google Scholar
• Kciuk M, Gielecińska A, Mujwar S, Mojzych M, Marciniak B, Drozda R, Kontek R. Targeting carbonic anhydrase IX and XII isoforms with small molecule inhibitors and monoclonal antibodies. J Enzyme Inhib Med Chem. 2022;37(1):1278–1298.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Experimental carbonic anhydrase inhibitors for the treatment of hypoxic tumors. J Exp Pharmacol. 2020;12:603–617.
   PubMedGoogle Scholar
• Courcier J, de la Taille A, Nourieh M, et al. Carbonic anhydrase IX in renal cell carcinoma, implications for disease management. Int J Mol Sci. 2020;21(19):7146.
   PubMed Web of Science ®Google Scholar
• Daunys S, Petrikaitė V. The roles of carbonic anhydrases IX and XII in cancer cell adhesion, migration, invasion and metastasis. Biol Cell. 2020;112(12):383–397.
   PubMed Web of Science ®Google Scholar
• Queen A, Bhutto HN, Yousuf M, et al. Carbonic anhydrase IX: a tumor acidification switch in heterogeneity and chemokine regulation. Semin Cancer Biol. 2022;86:899–913.
   PubMed Web of Science ®Google Scholar
• Lee SH, Griffiths JR. How and why are cancers acidic? carbonic anhydrase IX and the homeostatic control of tumour extracellular pH. Cancers. 2020;12(6):1616.
   PubMed Web of Science ®Google Scholar
• Tonissen KF, Poulsen SA. Carbonic anhydrase XII inhibition overcomes P-glycoprotein-mediated drug resistance: a potential new combination therapy in cancer. Cancer Drug Resist. 2021;4(2):343–355.
   PubMedGoogle Scholar
• Waheed A, Sly WS. Carbonic anhydrase XII functions in health and disease. Gene. 2017;623:33–40.
   PubMed Web of Science ®Google Scholar
• Haapasalo J, Nordfors K, Haapasalo H, Parkkila S. The expression of carbonic anhydrases II, IX and XII in brain tumors. Cancers. 2020;12(7):1723.
   PubMed Web of Science ®Google Scholar
• Barnett DH, Sheng S, Charn TH, Waheed A, Sly WS, Lin C-Y, Liu ET, Katzenellenbogen BS. Estrogen receptor regulation of carbonic anhydrase XII through a distal enhancer in breast cancer. Cancer Res. 2008;68(9):3505–3515.
   PubMed Web of Science ®Google Scholar
• McDonald PC, Chafe SC, Supuran CT, Dedhar S. Cancer therapeutic targeting of hypoxia induced carbonic anhydrase IX: from bench to bedside. Cancers. 2022;14(14):3297.
   PubMed Web of Science ®Google Scholar
• Calvo-Martín G, Plano D, Encío I, et al. Novel N,N'-disubstituted selenoureas as potential antioxidant and cytotoxic agents. Antioxidants. 2021;10(5):777.
   Web of Science ®Google Scholar
• Ruberte AC, Ramos-Inza S, Aydillo C, et al. Novel N,N'-disubstituted acylselenoureas as potential antioxidant and cytotoxic agents. Antioxidants. 2020;9(1):55.
   Web of Science ®Google Scholar
• Bartolini D, Sancineto L, Fabro de Bem A, Tew KD, Santi C, Radi R, Toquato P, Galli F. Selenocompounds in cancer therapy: an overview. Adv Cancer Res. 2017;136:259–302.
   PubMed Web of Science ®Google Scholar
• Chu CK, Ma L, Olgen S, Pierra C, Du J, Gumina G, Gullen E, Cheng YC, Schinazi RF. Synthesis and antiviral activity of oxaselenolane nucleosides. J Med Chem. 2000;43(21):3906–3912.
   PubMed Web of Science ®Google Scholar
• Mangiavacchi F, Botwina P, Menichetti E, et al. Seleno-functionalization of quercetin improves the non-covalent inhibition of M(pro) and its antiviral activity in cells against SARS-CoV-2. Int J Mol Sci. 2021;22(13):7048.
   PubMed Web of Science ®Google Scholar
• Witek K, Nasim M, Bischoff M, Gaupp R, Arsenyan P, Vasiljeva J, Marć M, Olejarz A, Latacz G, Kieć-Kononowicz K, et al. Selenazolinium salts as “small molecule catalysts” with high potency against ESKAPE bacterial pathogens. Molecules. 2017;22(12):2174.
   PubMed Web of Science ®Google Scholar
• Blessing H, Kraus S, Heindl P, Bal W, Hartwig A. Interaction of selenium compounds with zinc finger proteins involved in DNA repair. Eur J Biochem. 2004;271(15):3190–3199.
   PubMedGoogle Scholar
• Angeli A, Tanini D, Nocentini A, Capperucci A, Ferraroni M, Gratteri P, Supuran CT. Selenols: a new class of carbonic anhydrase inhibitors. Chem Commun. 2019;55(5):648–651.
   PubMed Web of Science ®Google Scholar
• Tanini D, Capperucci A, Ferraroni M, Carta F, Angeli A, Supuran CT. Direct and straightforward access to substituted alkyl selenols as novel carbonic anhydrase inhibitors. Eur J Med Chem. 2020;185:111811.
   PubMed Web of Science ®Google Scholar
• Tanc M, Carta F, Scozzafava A, Supuran CT. α-Carbonic anhydrases possess thioesterase activity. ACS Med Chem Lett. 2015;6(3):292–295.
   PubMed Web of Science ®Google Scholar
• Lopez M, Vu H, Wang CK, Wolf MG, Groenhof G, Innocenti A, Supuran CT, Poulsen S-A. Promiscuity of carbonic anhydrase II. Unexpected ester hydrolysis of carbohydrate-based sulfamate inhibitors. J Am Chem Soc. 2011;133(45):18452–18462.
   PubMed Web of Science ®Google Scholar
• Angeli A, Carta F, Donnini S, Capperucci A, Ferraroni M, Tanini D, Supuran CT. Selenolesterase enzyme activity of carbonic anhydrases. Chem Commun. 2020;56(32):4444–4447.
   PubMed Web of Science ®Google Scholar
• Astrain-Redin N, Talavera I, Moreno E, Ramírez MJ, Martínez-Sáez N, Encío I, Sharma AK, Sanmartín C, Plano D. Seleno-analogs of scaffolds resembling natural products a novel warhead toward dual compounds. Antioxidants. 2023;12(1):139.
   Web of Science ®Google Scholar
• Astrain-Redin N, Sanmartin C, Sharma A, et al. From natural sources to synthetic derivatives: allyl motif as a powerful tool for fragment-based design in cancer. J Med Chem. 2023;Submitted for publication.
   PubMed Web of Science ®Google Scholar
• Diakos CI, Charles KA, McMillan DC, Clarke SJ. Cancer-related inflammation and treatment effectiveness. Lancet Oncol. 2014; Oct15(11):e493-503–e503.
   PubMed Web of Science ®Google Scholar
• Innocenti A, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors: inhibition of mammalian isoforms I-XIV with a series of substituted phenols including paracetamol and salicylic acid. Bioorg Med Chem. 2008;16(15):7424–7428.
   PubMed Web of Science ®Google Scholar
• Cau Y, Vullo D, Mori M, Dreassi E, Supuran C, Botta M. Potent and selective carboxylic acid inhibitors of tumor-associated carbonic anhydrases IX and XII. Molecules. 2017;23(1):17.
   PubMed Web of Science ®Google Scholar
• Lomelino CL, McKenna R. Carbonic anhydrase II in complex with carboxylic acid-based inhibitors. Acta Crystallogr F Struct Biol Commun. 2019;75(Pt 3):166–170.
   PubMedGoogle Scholar
• Falsini M, Squarcialupi L, Catarzi D, Varano F, Betti M, Di Cesare Mannelli L, Tenci B, Ghelardini C, Tanc M, Angeli A, et al. 3-Hydroxy-1H-quinazoline-2,4-dione as a new scaffold to develop potent and selective inhibitors of the tumor-associated carbonic anhydrases IX and XII. J Med Chem. 2017;60(14):6428–6439.
   PubMed Web of Science ®Google Scholar
• Altıntop MD, Sever B, Akalın Çiftçi G, Kucukoglu K, Özdemir A, Soleimani SS, Nadaroglu H, Kaplancıklı ZA. Synthesis and evaluation of new benzodioxole-based dithiocarbamate derivatives as potential anticancer agents and hCA-I and hCA-II inhibitors. Eur J Med Chem. 2017;125:190–196.
   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
• Del Prete S, Angeli A, Ghobril C, Hitce J, Clavaud C, Marat X, Supuran CT, Capasso C. Sulfonamide inhibition profile of the β-carbonic anhydrase from Malassezia restricta, an opportunistic pathogen triggering scalp conditions. Metabolites. 2020;10(1):39.
   PubMed Web of Science ®Google Scholar
• Vullo D, Del Prete S, Nocentini A, Osman SM, AlOthman Z, Capasso C, Bozdag M, Carta F, Gratteri P, Supuran CT, et al. Dithiocarbamates effectively inhibit the β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa. Bioorg Med Chem. 2017;25(3):1260–1265.
   PubMed Web of Science ®Google Scholar
• Akgul O, Di Cesare Mannelli L, Vullo D, Angeli A, Ghelardini C, Bartolucci G, Alfawaz Altamimi AS, Scozzafava A, Supuran CT, Carta F, et al. Discovery of novel nonsteroidal anti-inflammatory drugs and carbonic anhydrase inhibitors hybrids (NSAIDs-CAIs) for the management of rheumatoid arthritis. J Med Chem. 2018;61(11):4961–4977.
   PubMed Web of Science ®Google Scholar
• Bua S, Di Cesare Mannelli L, Vullo D, Ghelardini C, Bartolucci G, Scozzafava A, Supuran CT, Carta F. Design and synthesis of novel nonsteroidal anti-inflammatory drugs and carbonic anhydrase inhibitors hybrids (NSAIDs-CAIs) for the treatment of rheumatoid arthritis. J Med Chem. 2017;60(3):1159–1170.
   PubMed Web of Science ®Google Scholar
• Vomasta D, Innocenti A, König B, Supuran CT. Carbonic anhydrase inhibitors: two-prong versus mono-prong inhibitors of isoforms I, II, IX, and XII exemplified by photochromic cis-1,2-alpha-dithienylethene derivatives. Bioorg Med Chem Lett. 2009;19(5):1283–1286.
   PubMed Web of Science ®Google Scholar
• Behnke CA, Le Trong I, Godden JW, Merritt EA, Teller DC, Bajorath J, Stenkamp RE. Atomic resolution studies of carbonic anhydrase II. Acta Crystallogr D Biol Crystallogr. 2010 May;66(Pt 5):616–627.
   PubMedGoogle 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
• Whittington DA, Waheed A, Ulmasov B, Shah GN, Grubb JH, Sly WS, Christianson DW. 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 U S A. 2001;98(17):9545–9550.
   PubMed Web of Science ®Google Scholar
• Burley SK, Bhikadiya C, Bi C, Bittrich S, Chen L, Crichlow GV, Christie CH, Dalenberg K, Di Costanzo L, Duarte JM, et al. RCSB protein data bank: powerful new tools for exploring 3D structures of biological macromolecules for basic and applied research and education in fundamental biology, biomedicine, biotechnology, bioengineering and energy sciences. Nucleic Acids Res. 2021;49(D1):D437–D451.
   PubMed Web of Science ®Google Scholar
• Schrödinger Suite Release 2022–3. New York (NY): Schrödinger, LLC; 2022:(a) Maestro v.12.9. (b) Epik, v.5.7. (c) Impact, v.9.2. (d) Prime, v.5.5. (e) Macromodel v.13.3. (f) Glide, v.9.2. (g) Jaguar, v.11.3. (h) Desmond, v.6.7.
   Google Scholar
• Ibrahim HS, Allam HA, Mahmoud WR, Bonardi A, Nocentini A, Gratteri P, Ibrahim ES, Abdel-Aziz HA, Supuran CT. Dual-tail arylsulfone-based benzenesulfonamides differently match the hydrophobic and hydrophilic halves of human carbonic anhydrases active sites: selective inhibitors for the tumor-associated hCA IX isoform. Eur J Med Chem. 2018;152:1–9.
   PubMed Web of Science ®Google Scholar
• Lu C, Wu C, Ghoreishi D, Chen W, Wang L, Damm W, Ross GA, Dahlgren MK, Russell E, Von Bargen CD, et al. OPLS4: improving force field accuracy on challenging regimes of chemical space. J Chem Theory Comput. 2021;17(7):4291–4300.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Bonardi A, Gratteri P, Cerra B, Gioiello A, Supuran CT. Steroids interfere with human carbonic anhydrase activity by using alternative binding mechanisms. J Enzyme Inhib Med Chem. 2018;33(1):1453–1459.
   PubMed Web of Science ®Google Scholar
• Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem. 2004;25(13):1605–1612.
   PubMed Web of Science ®Google Scholar
• Angeli A, Ferraroni M, Capperucci A, Tanini D, Costantino G, Supuran CT. Selenocarbamates as a prodrug-based approach to carbonic anhydrase inhibition. ChemMedChem. 2022;17(11):e202200085.
   PubMed Web of Science ®Google Scholar