Structure-based virtual screening and biological evaluation of novel small-molecule BTK inhibitors

References

• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646–74.
   PubMed Web of Science ®Google Scholar
• Singh SP, Dammeijer F, Hendriks RW. Role of Bruton’s tyrosine kinase in B cells and malignancies. Mol Cancer 2018;17:57.
   PubMed Web of Science ®Google Scholar
• Paydas S. Management of adverse effects/toxicity of ibrutinib. Crit Rev Oncol Hematol 2019;136:56–63.
   PubMed Web of Science ®Google Scholar
• Liu J, Guiadeen D, Krikorian A, et al. Discovery of 8-Amino-imidazo[1,5-a]pyrazines as reversible BTK inhibitors for the treatment of rheumatoid arthritis. ACS Med Chem Lett 2016;7:198–203.
   PubMed Web of Science ®Google Scholar
• Wang X, Barbosa J, Blomgren P, et al. Discovery of potent and selective tricyclic inhibitors of Bruton’s tyrosine kinase with improved drug like properties. ACS Med Chem Lett 2017;8:608–13.
   PubMed Web of Science ®Google Scholar
• Yue C, Niu M, Shan QQ, et al. High expression of Bruton’s tyrosine kinase (BTK) is required for EGFR-induced NF-κB activation and predicts poor prognosis in human glioma. J Exp Clin Cancer Res 2017;36:132.
   PubMed Web of Science ®Google Scholar
• Molina-Cerrillo J, Alonso-Gordoa T, Gajate P, Grande E. Bruton’s tyrosine kinase (BTK) as a promising target in solid tumors. Cancer Treat Rev 2017;58:41–50.
   PubMed Web of Science ®Google Scholar
• Lavitrano M, Ianzano L, Bonomo S, et al. BTK inhibitors synergise with 5-FU to treat drug-resistant TP53-null colon cancers. J Pathol 2020;250:134–47.
   PubMed Web of Science ®Google Scholar
• Basile D, Gerratana L, Buonadonna A, et al. Role of Bruton’s tyrosine kinase in stage III colorectal cancer. Cancers (Basel) 2019;11:880.
   PubMed Web of Science ®Google Scholar
• Wang JD, Chen XY, Ji KW, Tao F. Targeting Btk with ibrutinib inhibit gastric carcinoma cells growth. Am J Transl Res 2016;8:3003–12.
   PubMed Web of Science ®Google Scholar
• Bond DA, Woyach JA. Targeting BTK in CLL: beyond ibrutinib. Curr Hematol Malig Rep 2019;14:197–205.
   PubMed Web of Science ®Google Scholar
• Feng YF, Duan WM, Cu XC, et al. Bruton’s tyrosine kinase (BTK) inhibitors in treating cancer: a patent review (2010-2018). Expert Opin Ther Pat 2019;29:217–41.
   PubMed Web of Science ®Google Scholar
• Angst D, Gessier F, Janser P, et al. Discovery of LOU064 (Remibrutinib), a potent and highly selective covalent inhibitor of Bruton’s tyrosine kinase. J Med Chem 2020;63:5102–18.
   PubMedGoogle Scholar
• Chen J, Kinoshita T, Gururaja T, et al. The effect of Bruton’s tyrosine kinase (BTK) inhibitors on collagen-induced platelet aggregation, BTK, and tyrosine kinase expressed in hepatocellular carcinoma (TEC). Eur J Haematol 2018;101:604–12.
   Web of Science ®Google Scholar
• Lionta E, Spyrou G, Vassilatis DK, Cournia Z. Structure-based virtual screening for drug discovery: principles, applications and recent advances. Curr Top Med Chem 2014;14:1923–38.
   PubMed Web of Science ®Google Scholar
• Wang Y, Sun Y, Cao R, et al. In silico identification of a novel hinge-binding scaffold for kinase inhibitor discovery. J Med Chem 2017;60:8552–64.
   PubMed Web of Science ®Google Scholar
• Lin TE, HuangFu WC, Chao MW, et al. A novel selective JAK2 inhibitor identified using pharmacological interactions. Front Pharmacol 2018;9:1379.
   PubMed Web of Science ®Google Scholar
• LeadIT v2.3.2, 2019. Sankt Augustin, Germany: BiosolveIT GmBH. Available from: http://www.biosolveit.de/LeadIT BIOVIA,
   Google Scholar
• Berman HM, Westbrook J, Feng Z, et al. The protein data bank. Nucleic Acids Res 2000;28:235–42.
   PubMed Web of Science ®Google Scholar
• Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 2001;46:3–26.
   PubMed Web of Science ®Google Scholar
• Baell JB, Nissink JWM. Seven year itch: pan-assay interference compounds (PAINS) in 2017-utility and limitations. ACS Chem Biol 2018;13:36–44.
   PubMed Web of Science ®Google Scholar
• Gilson MK, Liu T, Baitaluk M, et al. BindingDB in 2015: a public database for medicinal chemistry, computational chemistry and systems pharmacology. Nucleic Acids Res 2016;44:D1045–53.
   PubMed Web of Science ®Google Scholar
• Warr WA. Scientific workflow systems: pipeline pilot and KNIME. J Comput Aided Mol Des 2012;26:801–4.
   PubMed Web of Science ®Google Scholar
• Bissantz C, Folkers G, Rognan D. Protein-based virtual screening of chemical databases. 1. Evaluation of different docking/scoring combinations. J Med Chem 2000;43:4759–67.
   PubMed Web of Science ®Google Scholar
• Lee KC, Chen YL, Wang CC, et al. Refluxed esterification of fullerene-conjugated P25 TiO2 promotes free radical scavenging capacity and facilitates anti-aging potentials in human cells. ACS Appl Mater Interfaces 2019;11:311–9.
   PubMed Web of Science ®Google Scholar
• Lin MH, Wang JS, Hsieh YC, et al. NO2 functionalized coumarin derivatives suppress cancer progression and facilitate apoptotic cell death in KRAS mutant colon cancer. Chem-Biol Interact 2019;309:108708.
   PubMed Web of Science ®Google Scholar
• Lo PY, Lee GY, Zheng JH, et al. Intercalating pyrene with polypeptide as a novel self-assembly nano-carrier for colon cancer suppression in vitro and in vivo. Mat Sci Eng C-Mater 2020;109:110593.
   Google Scholar
• Hung WH, Zheng JH, Lee KC, Cho EC. Doxorubicin conjugated AuNP/biopolymer composites facilitate cell cycle regulation and exhibit superior tumor suppression potential in KRAS mutant colorectal cancer. J Biotechnol 2019;306:149–58.
   PubMed Web of Science ®Google Scholar
• Chen CH, Hsieh YC, Yang PM, et al. Dicoumarol suppresses HMGA2-mediated oncogenic capacities and inhibits cell proliferation by inducing apoptosis in colon cancer. Biochem Biophys Res Commun 2020;524:1003–9.
   PubMed Web of Science ®Google Scholar
• Dassault Systèmes BIOVIA Pipeline Pilot, Release 2017. San Diego: Dassault Systemes.
   Google Scholar
• Cho EC, Kuo ML, Cheng JH, et al. RRM2B-mediated regulation of mitochondrial activity and inflammation under oxidative stress. Mediat Inflamm 2015;2015:1–8.
   Web of Science ®Google Scholar
• Lee KC, Lo PY, Lee GY, et al. Carboxylated carbon nanomaterials in cell cycle and apoptotic cell death regulation. J Biotechnol 2019;296:14–21.
   PubMed Web of Science ®Google Scholar
• Brylinski M, Skolnick J. Comprehensive structural and functional characterization of the human kinome by protein structure modeling and ligand virtual screening. J Chem Inf Model 2010;50:1839–54.
   PubMed Web of Science ®Google Scholar
• BIOVIA, Dassault Systèmes BIOVIA Discovery Studio, Release 2017, San Diego: Dassault Systemes.
   Google Scholar
• Kirchmair J, Markt P, Distinto S, et al. Evaluation of the performance of 3D virtual screening protocols: RMSD comparisons, enrichment assessments, and decoy selection-what can we learn from earlier mistakes? J Comput Aided Mol Des 2008;22:213–28.
   PubMed Web of Science ®Google Scholar
• Johnson AR, Kohli PB, Katewa A, et al. Battling Btk mutants with noncovalent inhibitors that overcome Cys481 and Thr474 mutations. ACS Chem Biol 2016;11:2897–907.
   PubMed Web of Science ®Google Scholar
• Bukhtiyarova M, Northrop K, Chai X, et al. Improved expression, purification, and crystallization of p38alpha MAP kinase. Protein Expr Purif 2004;37:154–61.
   PubMed Web of Science ®Google Scholar
• Giordano F, Vaira V, Cortinovis D, et al. Grassilli, E. p65BTK is a novel potential actionable target in KRAS-mutated/EGFR-wild type lung adenocarcinoma. J Exp Clin Cancer Res 2019;38:260.
   PubMed Web of Science ®Google Scholar
• Rushworth SA, Murray MY, Zaitseva L, et al. Identification of Bruton's tyrosine kinase as a therapeutic target in acute myeloid leukemia. Blood 2014;123:1229–38.
   PubMed Web of Science ®Google Scholar
• Wessel MD, Jurs PC, Tolan JW, Muskal SM. Prediction of human intestinal absorption of drug compounds from molecular structure. J Chem Inf Comput Sci 1998;38:726–35.
   PubMedGoogle Scholar
• Wang J, Liu XY, Hong YZ, et al. Ibrutinib, a Bruton’s tyrosine kinase inhibitor, exhibits antitumoral activity and induces autophagy in glioblastoma. J Exp Clin Canc Res 2017;36:96.
   PubMed Web of Science ®Google Scholar
• Sun FD, Wang PC, Shang J, et al. Ibrutinib presents antitumor activity in skin cancer and induces autophagy. Eur Rev Med Pharmacol 2018;22:561–6.
   PubMed Web of Science ®Google Scholar
• Rossin A, Lounnas N, Durivault J, et al. The Btk-dependent PIP5K1γ lipid kinase activation by Fas counteracts FasL-induced cell death. Apoptosis 2017;22:1344–52.
   PubMed Web of Science ®Google Scholar