Methoxy and bromo scans on N-(5-methoxyphenyl) methoxybenzenesulphonamides reveal potent cytotoxic compounds, especially against the human breast adenocarcinoma MCF7 cell line

References

• Dumontet C, Jordan MA. Microtubule-binding agents: a dynamic field of cancer therapeutics. Nat Rev Drug Discov 2010;9:790–803.
   PubMed Web of Science ®Google Scholar
• Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat Rev Cancer 2004;4:253–63.
   PubMed Web of Science ®Google Scholar
• Vicente‐Blázquez A, González M, Álvarez R, et al. Antitubulin sulphonamides: the successful combination of an established drug class and a multifaceted target. Med Res Rev 2019;39:775–830.
   PubMed Web of Science ®Google Scholar
• Alvarez R, Medarde M, Pelaez R. New Ligands of the tubulin colchicine site based on x-ray structures. Curr Top Med Chem 2014;14:2231–52.
   PubMed Web of Science ®Google Scholar
• Ravelli RBG, Gigant B, Curmi PA, et al. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 2004;428:198–202.
   PubMed Web of Science ®Google Scholar
• Torres F, Garcia-Rubino M, Lozano-Lopez C, et al. Imidazoles and benzimidazoles as tubulin-modulators for anti-cancer therapy. Curr Med Chem 2015;22:1312–23.
   PubMed Web of Science ®Google Scholar
• Tron GC, Pirali T, Sorba G, et al. Medicinal chemistry of combretastatin A4: present and future directions. J Med Chem 2006;49:3033–44.
   PubMed Web of Science ®Google Scholar
• Kavallaris M. Microtubules and resistance to tubulin-binding agents. Nat Rev Cancer 2010;10:194–204
   PubMed Web of Science ®Google Scholar
• Li L, Jiang S, Li X, et al. Recent advances in trimethoxyphenyl (TMP) based tubulin inhibitors targeting the colchicine binding site. Eur J Med Chem 2018;151:482–94.
   PubMed Web of Science ®Google Scholar
• Negi AS, Gautam Y, Alam S, et al. Natural antitubulin agents: importance of 3,4,5-trimethoxyphenyl fragment. Bioorg Med Chem 2015;23:373–89.
   PubMed Web of Science ®Google Scholar
• Aprile S, Del Grosso E, Tron GC, Grosa G. In vitro metabolism study of combretastatin A-4 in rat and human liver microsomes. Drug Metab Dispos 2007;35:2252–61.
   PubMed Web of Science ®Google Scholar
• Ghinet A, Rigo B, Hénichart JP, et al. Synthesis and biological evaluation of phenstatin metabolites. Bioorg Med Chem 2011;19:6042–54.
   PubMedGoogle Scholar
• Le Broc-Ryckewaert D, Pommery N, Pommery J, et al. In vitro metabolism of phenstatin: potential pharmacological consequences. Drug Metab Lett 2011;5:209–15.
   PubMedGoogle Scholar
• Hamze A, Alami M, Provot O. Developments of isoCombretastatin A-4 derivatives as highly cytotoxic agents. Eur J Med Chem 2020;190:112110.
   PubMed Web of Science ®Google Scholar
• González M, Ellahioui Y, Álvarez R, et al. The Masked Polar Group Incorporation (MPGI) strategy in drug design: effects of nitrogen substitutions on combretastatin and isocombretastatin tubulin inhibitors. Molecules 2019;24:4319.
   PubMed Web of Science ®Google Scholar
• Álvarez R, Aramburu L, Puebla P, et al. Pyridine based antitumour compounds acting at the colchicine site. Curr Med Chem 2016;23:1100–30.
   PubMed Web of Science ®Google Scholar
• Álvarez R, Aramburu L, Gajate C, et al. Methylsulfanylpyridine based diheteroaryl isocombretastatin analogs as potent anti-proliferative agents. Eur J Med Chem 2021;209:112933.
   PubMed Web of Science ®Google Scholar
• Lu Y, Shi T, Wang Y, et al. Halogen bonding-a novel interaction for rational drug design? J Med Chem 2009;52:2854–62.
   PubMed Web of Science ®Google Scholar
• Beale TM, Myers RM, Shearman JW, et al. Antivascular and anticancer activity of dihalogenated A-ring analogues of combretastatin A-4. Med Chem Comm 2010;1:202–8.
   Google Scholar
• Loe DW, Deeley RG, Cole SP. Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J Pharmacol Exp Ther 2000;293:530–8.
   PubMed Web of Science ®Google Scholar
• Greene LM, O'Boyle NM, Nolan DP, et al. The vascular targeting agent Combretastatin-A4 directly induces autophagy in adenocarcinoma-derived colon cancer cells. Biochem Pharmacol 2012;84:612–24.
   PubMed Web of Science ®Google Scholar
• Wei RJ, Lin SS, Wu WR, et al. A microtubule inhibitor, ABT-751, induces autophagy and delays apoptosis in Huh-7 cells. Toxicol Appl Pharmacol 2016;311:88–98.
   PubMed Web of Science ®Google Scholar
• Dumortier C, Gorbunoff MJ, Andreu JM, Engelborghs Y. Different kinetic pathways of the binding of two biphenyl analogues of colchicine to tubulin. Biochemistry 1996;35:4387–95.
   PubMed Web of Science ®Google Scholar
• Shelanski ML, Gaskin F, Cantor CR. Microtubule assembly in the absence of added nucleotides. Proc Nat Acad Sci U.S.A. 1973;70:765–8.
   PubMed Web of Science ®Google Scholar
• Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–54.
   PubMed Web of Science ®Google Scholar
• Álvarez R, Aramburu L, Gajate C, et al. Potent colchicine-site ligands with improved intrinsic solubility by replacement of the 3,4,5-trimethoxyphenyl ring with a 2-methylsulfanyl-6-methoxypyridine ring. Bioorg Chem 2020;98:103755.
   PubMed Web of Science ®Google Scholar
• Korb O, Stützle T, Exner TE. Empirical scoring functions for advanced protein-ligand docking with plants. J Chem Inf Model 2009;49:84–96.
   PubMed Web of Science ®Google Scholar
• Forli S, Huey R, Pique ME, et al. Computational protein-ligand docking and virtual drug screening with the AutoDock suite. Nat Protoc 2016;11:905–19.
   PubMed Web of Science ®Google Scholar
• Berthold MR, Cebron N, Dill F, et al. KNIME: the Konstanz information miner. Studies in classification, data analysis, and knowledge organization. Berlin, Germany: Springer; 2007:319–326.
   Google Scholar
• Pettersen EF, Goddard TD, Huang CC, et al. UCSF Chimera-A visualization system for exploratory research and analysis. J Comput Chem 2004;25:1605–12.
   PubMed Web of Science ®Google Scholar
• Marvin 17.8 ChemAxon. 2017 [accessed 2020 May 2]. https://www.chemaxon.com
   Google Scholar
• OpenEye Scientific Software, Inc, Santa Fe. 2019 [accessed 2020 May 2]. https://www.eyesopen.com/
   Google Scholar
• Garcia-Perez C, Pelaez R, Theron R, Luis Lopez-Perez J. JADOPPT: Java based AutoDock preparing and processing tool. Bioinformatics 2017;33:583–5.
   PubMed Web of Science ®Google Scholar
• Cafici L, Pirali T, Condorelli F, et al. Solution-phase parallel synthesis and biological evaluation of combretatriazoles. J Comb Chem 2008;10:732–40.
   PubMedGoogle Scholar
• Liao SY, Qian L, Miao TF, et al. Theoretical studies on QSAR and mechanism of 2-indolinone derivatives as tubulin inhibitors. Int J Quantum Chem 2009;109:999–1008.
   Web of Science ®Google Scholar
• Mu F, Hamel E, Lee DJ, et al. Synthesis, anticancer activity, and inhibition of tubulin polymerization by conformationally restricted analogues of lavendustin A. J Med Chem 2003;46:1670–82.
   PubMed Web of Science ®Google Scholar
• Stocker V, Ghinet A, Leman M, et al. On the synthesis and biological properties of isocombretastatins: a case of ketone homologation during Wittig reaction attempts. RSC Adv 2013;3:3683–96.
   Web of Science ®Google Scholar
• Hu L, Jiang J, Dong Qu J, et al. Novel potent antimitotic heterocyclic ketones: synthesis, antiproliferative activity, and structure-activity relationships. Bioorg Med Chem Lett 2007;17:3613–7.
   PubMed Web of Science ®Google Scholar
• Hu L, Li ZR, Li Y, et al. Synthesis and structure-activity relationships of carbazole sulphonamides as a novel class of antimitotic agents against solid tumors. J Med Chem 2006;49:6273–82.
   PubMed Web of Science ®Google Scholar
• Dohle W, Jourdan FL, Menchon G, et al. Quinazolinone-based anticancer agents: synthesis, antiproliferative SAR, antitubulin activity, and tubulin co-crystal structure. J Med Chem 2018;61:1031–44.
   PubMed Web of Science ®Google Scholar
• González M, Ovejero-Sánchez M, Vicente-Blázquez A, et al. Microtubule destabilizing sulphonamides as an alternative to taxane-based chemotherapy. Int J Mol Sci 2021;22:1907.
   PubMed Web of Science ®Google Scholar
• Schobert R, Effenberger-Neidnicht K, Biersack B. Stable combretastatin A-4 analogues with sub-nanomolar efficacy against chemoresistant HT-29 cells. Int J Clin Pharmacol Ther 2011;49:71–2.
   PubMed Web of Science ®Google Scholar
• Cummings J, Zelcer N, Allen JD, et al. Glucuronidation as a mechanism of intrinsic drug resistance in colon cancer cells: contribution of drug transport proteins. Biochem Pharmacol 2004;67:31–9.
   PubMed Web of Science ®Google Scholar
• Nam N-H. Combretastatin A-4 analogues as antimitotic antitumor agents. Curr Med Chem 2003;10:1697–722.
   PubMed Web of Science ®Google Scholar
• Andreu JM, Perez-Ramirez B, Gorbunoff MJ, et al. Role of the colchicine ring A and its methoxy groups in the binding to tubulin and microtubule inhibition. Biochemistry 1998;37:8356–68.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wu Y, Sun L, et al. Synthesis and structure-activity relationship study of water-soluble carbazole sulphonamide derivatives as new anticancer agents. Eur J Med Chem 2020;191:112181.
   Web of Science ®Google Scholar
• Liu J, Liu C, Zhang X, et al. Anticancer sulphonamide hybrids that inhibit bladder cancer cells growth and migration as tubulin polymerisation inhibitors. J Enzyme Inhib Med Chem 2019;34:1380–1387.
   PubMed Web of Science ®Google Scholar
• Sharom FJ. The P-glycoprotein multidrug transporter. Essays in Biochem 2011;50:161–178.
   PubMed Web of Science ®Google Scholar
• Álvarez R, Gajate C, Puebla P, et al. Substitution at the indole 3 position yields highly potent indolecombretastatins against human tumor cells. Eur J Med Chem 2018;158:167–183.
   Web of Science ®Google Scholar
• Lee MM, Gao Z, Peterson BR. Synthesis of a fluorescent analogue of paclitaxel that selectively binds microtubules and sensitively detects efflux by P-glycoprotein. Angew Chem Int Ed Engl 2017;56:6927–31
   PubMed Web of Science ®Google Scholar
• Jänicke RU, Sprengart ML, Wati MR, Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 1998;273:9357–9360.
   PubMed Web of Science ®Google Scholar
• Yang XH, Sladek TL, Liu X, et al. Reconstitution of caspase 3 sensitizes MCF-7 breast cancer cells to doxorubicin- and etoposide-induced apoptosis. Cancer Res 2001;61:348–354.
   PubMed Web of Science ®Google Scholar
• Mollinedo F, Gajate C. Microtubules, microtubule-interfering agents and apoptosis. Apoptosis 2003;8:413–50.
   PubMed Web of Science ®Google Scholar
• Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008;15:1153–62.
   PubMed Web of Science ®Google Scholar
• Castedo M, Perfettini JL, Roumier T, et al. Cell death by mitotic catastrophe: a molecular definition. Oncogene 2004;23:2825–2837.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 2016;12:1–222.
   PubMed Web of Science ®Google Scholar
• Bitto A, Lerner CA, Nacarelli T, et al. p62/SQSTM1 at the interface of aging, autophagy, and disease. Age 2014;36:1137–9626.
   Google Scholar
• Amaro RE, Baudry J, Chodera J, et al. Ensemble docking in drug discovery. Biophys J 2018;114:2271–78.
   PubMed Web of Science ®Google Scholar