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Journal of Enzyme Inhibition and Medicinal Chemistry Volume 37, 2022 - Issue 1
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Research Papers

Dependence on linkers’ flexibility designed for benzenesulfonamides targeting discovery of novel hCA IX inhibitors as potent anticancer agents

Haytham O. Tawfika Department of Pharmaceutical Chemistry, Faculty of Pharmacy, Tanta University, Tanta, EgyptCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0001-6455-5716View further author information
ORCID Icon,
Amany Belalb Medicinal Chemistry Department, Faculty of Pharmacy, Beni-Suef University, Beni-Suef, Egypt;c Department of Pharmaceutical Chemistry, College of Pharmacy, Taif University, Taif, Saudi ArabiaORCID Iconhttps://orcid.org/0000-0003-1045-0163View further author information
ORCID Icon,
Mohammed A. S. Abourehabd Department of Pharmaceutics, Faculty of Pharmacy, Umm Al-Qura University, Makkah, Saudi Arabia;e Department of Pharmaceutics and Industrial Pharmacy, College of Pharmacy, Minia University, Minia, EgyptORCID Iconhttps://orcid.org/0000-0003-1348-6567View further author information
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Andrea Angelif Department of NEUROFARBA, Section of Pharmaceutical and Nutraceutical Sciences, University of Florence, Sesto Fiorentino, ItalyORCID Iconhttps://orcid.org/0000-0002-1470-7192View further author information
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Alessandro Bonardif Department of NEUROFARBA, Section of Pharmaceutical and Nutraceutical Sciences, University of Florence, Sesto Fiorentino, ItalyView further author information
,
Claudiu T. Supuranf Department of NEUROFARBA, Section of Pharmaceutical and Nutraceutical Sciences, University of Florence, Sesto Fiorentino, ItalyCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0003-4262-0323View further author information
ORCID Icon &
Mervat H. El-Hamamsya Department of Pharmaceutical Chemistry, Faculty of Pharmacy, Tanta University, Tanta, EgyptView further author information
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Pages 2765-2785 | Received 04 Sep 2022, Accepted 22 Sep 2022, Published online: 09 Oct 2022

References

  • Feng CY, Chen ZF, Pei LL, et al. Genome-wide identification, phylogeny, and expression analysis of the CA gene family in tomato. Biotechnol Biotechnol Equip. 2020;34(1):70–83.
  • Momayyezi M, McKown AD, Bell SC, Guy RD. Emerging roles for carbonic anhydrase in mesophyll conductance and photosynthesis. Plant J. 2020;101(4):831–844.
  • Güttler A, Eiselt Y, Funtan A, et al. Betulin sulfonamides as carbonic anhydrase inhibitors and anticancer agents in breast cancer cells. Int J Mol Sci. 2021;22(16):8808–8821.
  • Becker HM, Deitmer JW. Proton transport in cancer cells: the role of carbonic anhydrases. IJMS. 2021;22(6):3171.
  • Supuran CT, Scozzafava A. Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem. 2007;15(13):4336–4350.
  • Osmaniye D, Türkeş C, Demir Y, et al. Design, synthesis, and biological activity of novel dithiocarbamate-methylsulfonyl hybrids as carbonic anhydrase inhibitors. Arch Pharm . 2022;355(8):2200132–15.
  • Zhang C, Fang L, Wang X, et al. Oncolytic adenovirus-mediated expression of decorin facilitates CAIX-targeting CAR-T therapy against renal cell carcinoma. Mol Ther Oncolytics. 2022;24:14–25.,
  • Mahon BP, Pinard MA, McKenna R. Targeting carbonic anhydrase IX activity and expression. Molecules. 2015;20(2):2323–2348.
  • Pettersen EO, Ebbesen P, Gieling RG, et al. Targeting tumour hypoxia to prevent cancer metastasis. From biology, biosensing and technology to drug development: the METOXIA consortium. J Enzyme Inhib Med Chem. 2015;30(5):689–721.
  • 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):1616–1625.
  • Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem. 2016;31(3):345–360.
  • Carta F, Vullo D, Osman SM, et al. Synthesis and carbonic anhydrase inhibition of a series of SLC-0111 analogs. Bioorg Med Chem. 2017;25(9):2569–2576.
  • Said MA, Eldehna WM, Nocentini A, et al. Sulfonamide-based ring-fused analogues for CAN508 as novel carbonic anhydrase inhibitors endowed with antitumor activity: design, synthesis, and in vitro biological evaluation. Eur J Med Chem. 2020;189:112019.,
  • Katariya KD, Shah SR, Reddy D. Anticancer, antimicrobial activities of quinoline based hydrazone analogues: synthesis, characterization and molecular docking. Bioorg Chem. 2020;94:1–14.
  • Goff GL, Ouazzani J. Natural hydrazine-containing compounds: biosynthesis, isolation, biological activities and synthesis. Bioorg Med Chem. 2014;22(23):6529–6544.
  • Alaa A-M, El-Azab AS, El-Enin MAA, et al. Synthesis of novel isoindoline-1, 3-dione-based oximes and benzenesulfonamide hydrazones as selective inhibitors of the tumor-associated carbonic anhydrase IX. Bioorg Chem. 2018;80:706–713.
  • Queen A, Khan P, Idrees D, et al. Biological evaluation of p-toluene sulphonylhydrazone as carbonic anhydrase IX inhibitors: an approach to fight hypoxia-induced tumors. Int J Biol Macromol. 2018;106:840–850.
  • Rodrigues T, da Cruz FP, Lafuente-Monasterio MJ, et al. Quinolin-4 (1 H)-imines are potent antiplasmodial drugs targeting the liver stage of malaria. J Med Chem. 2013;56(11):4811–4815.
  • Ressurreição AS, Gonçalves D, Sitoe AR, et al. Structural optimization of quinolon-4 (1 H)-imines as dual-stage antimalarials: toward increased potency and metabolic stability. J Med Chem. 2013;56(19):7679–7690.
  • Abo-Ashour MF, Eldehna WM, Nocentini A, et al. 3-Hydrazinoisatin-based benzenesulfonamides as novel carbonic anhydrase inhibitors endowed with anticancer activity: synthesis, in vitro biological evaluation and in silico insights. Eur J Med Chem. 2019;184:111768.
  • Eldeeb AH, Abo-Ashour MF, Angeli A, et al. Novel benzenesulfonamides aryl and arylsulfone conjugates adopting tail/dual tail approaches: synthesis, carbonic anhydrase inhibitory activity and molecular modeling studies. Eur J Med Chem. 2021;221:113486–12.
  • Chandak N, Ceruso M, Supuran CT, Sharma PK. Novel sulfonamide bearing coumarin scaffolds as selective inhibitors of tumor associated carbonic anhydrase isoforms IX and XII. Bioorg Med Chem. 2016;24(13):2882–2886.
  • Alaa A-M, El-Azab AS, Bua S, et al. Design, synthesis, and carbonic anhydrase inhibition activity of benzenesulfonamide-linked novel pyrazoline derivatives. Bioorg Chem. 2019;87:425–431.
  • Yamali C, Gul HI, Ozli G, et al. Exploring of tumor-associated carbonic anhydrase isoenzyme IX and XII inhibitory effects and cytotoxicities of the novel N-aryl-1-(4-sulfamoylphenyl)-5-(thiophen-2-yl)-1H-pyrazole-3-carboxamides. Bioorg Chem. 2021;115:105194–11.
  • Said MA, Eldehna WM, Nocentini A, et al. Synthesis, biological and molecular dynamics investigations with a series of triazolopyrimidine/triazole-based benzenesulfonamides as novel carbonic anhydrase inhibitors. Eur J Med Chem. 2020;185:111843–13.
  • Tawfik HO, Petreni A, Supuran CT, El-Hamamsy MH. Discovery of new carbonic anhydrase IX inhibitors as anticancer agents by toning the hydrophobic and hydrophilic rims of the active site to encounter the dual-tail approach. Eur J Med Chem. 2022;232:114190–21.
  • Jakusová K, Gáplovský M, Donovalová J, et al. Effect of reactants’ concentration on the ratio and yield of E, Z isomers of isatin-3-(4-phenyl) semicarbazone and N-methylisatin-3-(4-phenyl) semicarbazone. Chem Paper. 2013;67(1):117–126.
  • Ghorab MM, Alsaid MS, Soliman AM, Ragab FA. VEGFR-2 inhibitors and apoptosis inducers: synthesis and molecular design of new benzo [g] quinazolin bearing benzenesulfonamide moiety. J Enzyme Inhib Med Chem. 2017;32(1):893–907.
  • Sharma PK, Balwani S, Mathur D, et al. Synthesis and anti-inflammatory activity evaluation of novel triazolyl-isatin hybrids. J Enzyme Inhib Med Chem. 2016;31(6):1520–1526.
  • AboulWafa OM, Daabees HM, Badawi WA. 2-Anilinopyrimidine derivatives: design, synthesis, in vitro anti-proliferative activity, EGFR and ARO inhibitory activity, cell cycle analysis and molecular docking study. Bioorg Chem. 2020;99:103798–19.
  • Salem MS, Sakr SI, El-Senousy WM, Madkour HM. Synthesis, antibacterial, and antiviral evaluation of new heterocycles containing the pyridine moiety. Arch Pharm (Weinheim)). 2013;346(10):766–773.
  • Othman IMM, Gad-Elkareem MAM, Anouar EH, et al. Novel fused pyridine derivatives containing pyrimidine moiety as prospective tyrosyl-tRNA synthetase inhibitors: design, synthesis, pharmacokinetics and molecular docking studies. J Mol Struct. 2020;1219:128651.
  • George RF, Said MF, Bua S, Supuran CT. Synthesis and selective inhibitory effects of some 2-oxindole benzenesulfonamide conjugates on human carbonic anhydrase isoforms CA I, CA II, CA IX and CAXII. Bioorg Chem. 2020;95:103514.
  • Ghorab MM, Alsaid MS, Ceruso M, et al. Carbonic anhydrase inhibitors: synthesis, molecular docking, cytotoxic and inhibition of the human carbonic anhydrase isoforms I, II, IX, XII with novel benzenesulfonamides incorporating pyrrole, pyrrolopyrimidine and fused pyrrolopyrimidine moieties. Bioorg Med Chem. 2014;22(14):3684–3695.
  • Eldehna WM, Abo-Ashour MF, Nocentini A, et al. Enhancement of the tail hydrophobic interactions within the carbonic anhydrase IX active site via structural extension: Design and synthesis of novel N-substituted isatins-SLC-0111 hybrids as carbonic anhydrase inhibitors and antitumor agents. Eur J Med Chem. 2019;162:147–160.
  • Nocentini A, Trallori E, Singh S, et al. 4-Hydroxy-3-nitro-5-ureido-benzenesulfonamides selectively target the tumor-associated carbonic anhydrase isoforms IX and XII showing hypoxia-enhanced antiproliferative profiles. J Med Chem. 2018;61(23):10860–10874.
  • Demir-Yazıcı K, Bua S, Akgüneş NM, et al. Indole-based hydrazones containing A sulfonamide moiety as selective inhibitors of tumor-associated human carbonic anhydrase isoforms IX and XII. Int J Mol Sci. 2019;20:1–14.
  • Shaldam M, Nocentini A, Elsayed ZM, et al. Development of novel quinoline-based sulfonamides as selective cancer-associated carbonic anhydrase isoform IX inhibitors. Int J Mol Sci. 2021;22(20):11119–16.
  • Aggarwal M, Kondeti B, McKenna R. Insights towards sulfonamide drug specificity in α-carbonic anhydrases. Bioorg Med Chem. 2013;21(6):1526–1533.
  • 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(22):7210–7215.
  • Boyd MR, Paull KD. Some practical considerations and applications of the National Cancer Institute in vitro anticancer drug discovery screen. Drug Dev Res. 1995;34(2):91–109.
  • Rashid M, Husain A, Mishra R, et al. Design and synthesis of benzimidazoles containing substituted oxadiazole, thiadiazole and triazolo-thiadiazines as a source of new anticancer agents. Arab J Chem. 2019;12(8):3202–3224.
  • Singla P, Luxami V, Paul K. Synthesis and in vitro evaluation of novel triazine analogues as anticancer agents and their interaction studies with bovine serum albumin. Eur J Med Chem. 2016;117:59–69.
  • Acton EM, Narayanan VL, Risbood PA, et al. Anticancer specificity of some ellipticinium salts against human brain tumors in vitro. J Med Chem. 1994;37(14):2185–2189.
  • Al-Saadi MS, Rostom SA, HM. Faidallah 3-Methyl-2-(4-substituted phenyl)-4, 5-dihydronaphtho [1, 2-c]-pyrazoles: synthesis and inivitro biological evaluation as antitumour agents. Arch Pharm (Weinheim). 2008;341(3):181–190.
  • Krymov SK, Scherbakov AM, Salnikova DI, et al. Synthesis, biological evaluation, and in silico studies of potential activators of apoptosis and carbonic anhydrase inhibitors on isatin-5-sulfonamide scaffold. Eur J Med Chem. 2022;228:113997.
  • An B, Liu J, Fan Y, et al. Novel third-generation pyrimidines-based EGFR tyrosine kinase inhibitors targeting EGFR T790M mutation in advanced non-small cell lung cancer. Bioorg Chem. 2022;122:105743–14.
  • Hassan RA, Hamed MI, Abdou AM, El-Dash Y. Novel antiproliferative agents bearing substituted thieno [2, 3-d] pyrimidine scaffold as dual VEGFR-2 and BRAF kinases inhibitors and apoptosis inducers; design, synthesis and molecular docking. Bioorg Chem. 2022;125:105861–19.
  • Kadagathur M, Sujat Shaikh A, Panda B, et al. Synthesis of indolo/pyrroloazepinone-oxindoles as potential cytotoxic, DNA-intercalating and topo I inhibitors. Bioorg Chem. 2022;122:105706–105716.
  • Abdel-Aziz AA-M, El-Azab AS, AlSaif NA, et al. Synthesis, potential antitumor activity, cell cycle analysis, and multitarget mechanisms of novel hydrazones incorporating a 4-methylsulfonylbenzene scaffold: a molecular docking study. J Enzyme Inhib Med Chem. 2021;36(1):1521–1539.
  • Pfeffer CM, Singh AT. Apoptosis: a target for anticancer therapy. Int J Mol Sci. 2018;19:1–10.
  • Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J Immunol Methods. 1995;184(1):39–51.
  • Abdelrahman MA, Eldehna WM, Nocentini A, et al. Novel diamide-based benzenesulfonamides as selective carbonic anhydrase IX inhibitors endowed with antitumor activity: synthesis, biological evaluation and in silico insights. Int J Mol Sci. 2019;20:1–16.
  • Qin JL, Shen WY, Chen ZF, et al. Oxoaporphine metal complexes (Co II, Ni II, Zn II) with high antitumor activity by inducing mitochondria-mediated apoptosis and S-phase arrest in HepG2. Sci. Rep. 2017;7:1–18.
  • Zhong S, Li YG, Ji DF, et al. Protocatechualdehyde induces S-phase arrest and apoptosis by stimulating the p27KIP1-cyclin A/D1-CDK2 and mitochondrial apoptotic pathways in HT-29 Cells. Molecules. 2016;21(7):934–1 21.
  • Musa MA, Gbadebo AJ, Latinwo LM, Badisa VL. 7, 8-Dihydroxy-3-(4-nitrophenyl) coumarin induces cell death via reactive oxygen species–independent S-phase cell arrest. J. Biochem. Mol. Toxicol. 2018;32:794–801.
  • Nemr MT, AboulMagd AM, Hassan HM, et al. Design, synthesis and mechanistic study of new benzenesulfonamide derivatives as anticancer and antimicrobial agents via carbonic anhydrase IX inhibition. RSC Adv. 2021;11(42):26241–26257.
  • Dawood DH, Srour AM, Saleh DO, et al. New pyridine and chromene scaffolds as potent vasorelaxant and anticancer agents. RSC Adv. 2021;11(47):29441–29452.
  • Kim KH, Sederstrom JM. Assaying cell cycle status using flow cytometry. Curr Protoc Mol Biol. 2015;111:1–11.
  • Cvijetić IN, Tanç M, Juranić IO, et al. 5-Aryl-1H-pyrazole-3-carboxylic acids as selective inhibitors of human carbonic anhydrases IX and XII. Bioorg Med Chem. 2015;23(15):4649–4659.
  • Supuran CT. Multitargeting approaches involving carbonic anhydrase inhibitors: hybrid drugs against a variety of disorders. J Enzyme Inhib Med Chem. 2021;36(1):1702–1714.
  • Malebari AM, Ibrahim TS, Salem IM, et al. The anticancer activity for the bumetanide-based analogs via targeting the tumor-associated membrane-bound human carbonic anhydrase-IX enzyme. Pharmaceuticals. 2020;13(9):252–220.
  • Supuran CT, Scozzafava A. Carbonic anhydrase inhibitors: aromatic sulfonamides and disulfonamides act as efficient tumor growth inhibitors. J Enzyme Inhib. 2000;15(6):597–610.
  • Yousef RG, Ibrahim A, Khalifa MM, et al. Discovery of new nicotinamides as apoptotic VEGFR-2 inhibitors: virtual screening, synthesis, anti-proliferative, immunomodulatory, ADMET, toxicity, and molecular dynamic simulation studies. J Enzyme Inhib Med Chem. 2022;37(1):1389–1403.
  • Elrazaz EZ, Serya RA, Ismail NS, et al. Discovery of potent thieno [2, 3-d] pyrimidine VEGFR-2 inhibitors: design, synthesis and enzyme inhibitory evaluation supported by molecular dynamics simulations. Bioorg Chem. 2021;113:105019–16.
  • Belhassan A, Zaki H, Chtita S, et al. Camphor, artemisinin and sumac phytochemicals as inhibitors against COVID-19: computational approach. Comput Biol Med. 2021;136:104758–17.
  • Guterres H, Im W. Improving protein-ligand docking results with high-throughput molecular dynamics simulations. J Chem Inf Model. 2020;60(4):2189–2198.
  • Jena AB, Kanungo N, Nayak V, et al. Catechin and curcumin interact with S protein of SARS-CoV2 and ACE2 of human cell membrane: insights from computational studies. Sci Rep. 2021;11(1):14.
  • Ali A, Ali A, Warsi MH, et al. Toward the discovery of a novel class of leads for high altitude disorders by virtual screening and molecular dynamics approaches targeting carbonic anhydrase. Int J Mol Sci. 2022;23(9):5054.
  • Costa RA, Rocha JA, Pinheiro AS, et al. A computational approach applied to the study of potential allosteric inhibitors protease NS2B/NS3 from dengue virus. Molecules. 2022;27(13):4118–4120.
  • Lee S, Wong AR, Yang AWH, Hung A. Interaction of compounds derived from the Chinese medicinal formula Huangqi Guizhi Wuwu Tang with stroke-related numbness and weakness targets: an in-silico docking and molecular dynamics study. Comput Biol Med. 2022;146:105568–105569.
  • Abdel-Aziz AAM, El-Azab AS, Alanazi AM, et al. Synthesis and potential antitumor activity of 7-(4-substituted piperazin-1-yl)-4-oxoquinolines based on ciprofloxacin and norfloxacin scaffolds: in silico studies. J Enzyme Inhib Med Chem. 2016;31(5):796–809.
  • Mussi S, Rezzola S, Chiodelli P, et al. Antiproliferative effects of sulphonamide carbonic anhydrase inhibitors C18, SLC-0111 and acetazolamide on bladder, glioblastoma and pancreatic cancer cell lines. J Enzyme Inhib Med Chem. 2022;37(1):280–286.
  • Eldehna WM, Abo-Ashour MF, Ibrahim HS, et al. Novel [(3-indolylmethylene) hydrazono] indolin-2-ones as apoptotic anti-proliferative agents: design, synthesis and in vitro biological evaluation. J Enzyme Inhib Med Chem. 2018;33(1):686–700.
  • Said MA, Eldehna WM, Nocentini A, et al. Sulfonamide-based ring-fused analogues for CAN508 as novel carbonic anhydrase inhibitors endowed with antitumor activity: design, synthesis, and in vitro biological evaluation. Eur. J. Med. Chem. 2020;189:1–14.
  • Eldehna WM, El-Naggar DH, Hamed AR, et al. One-pot three-component synthesis of novel spirooxindoles with potential cytotoxic activity against triple-negative breast cancer MDA-MB-231 cells. J Enzyme Inhib Med Chem. 2018;33(1):309–318.
  • Ewies EF, Sabry E, Bekheit MS, et al. Click chemistry-based synthesis of new benzenesulfonamide derivatives bearing triazole ring as selective carbonic anhydrase II inhibitors. Drug Dev Res . 2022;83(6):1281–1291.

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