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Research Article

A combined ligand-based and structure-based in silico molecular modeling approach to pinpoint the key structural attributes of hydroxamate derivatives as promising meprin β inhibitors

, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Received 15 Jul 2023, Accepted 16 Oct 2023, Published online: 02 Jan 2024

References

  • Adhikari, N., Amin, S. A., Ghosh, B., & Jha, T. (2018). Shedding light on designing potential meprin β inhibitors through ligand-based robust validated computational approaches: A proposal to chemists! Journal of Biomolecular Structure & Dynamics, 36(11), 3003–3022. https://doi.org/10.1080/07391102.2017.1374210
  • Adhikari, N., Banerjee, S., Baidya, S. K., Ghosh, B., & Jha, T. (2021). Robust classification-based molecular modelling of diverse chemical entities as potential SARS-CoV-2 3CLpro inhibitors: Theoretical justification in light of experimental evidences. SAR and QSAR in Environmental Research, 32(6), 473–493. https://doi.org/10.1080/1062936X.2021.1914721
  • Aier, I., Varadwaj, P. K., & Raj, U. (2016). Structural insights into conformational stability of both wild-type and mutant EZH2 receptor. Scientific Reports, 6(1), 34984. https://doi.org/10.1038/srep34984
  • Amin, S. A., Adhikari, N., & Jha, T. (2018). Diverse classes of HDAC8 inhibitors: In search of molecular fingerprints that regulate activity. Future Medicinal Chemistry, 10(13), 1589–1602. https://doi.org/10.4155/fmc-2018-0005
  • Amin, S. A., Adhikari, N., Gayen, S., & Jha, T. (2017). First report on the structural exploration and prediction of new BPTES analogs as glutaminase inhibitors. Journal of Molecular Structure, 1143, 49–64. https://doi.org/10.1016/j.molstruc.2017.04.020
  • Arnold, P., Boll, I., Rothaug, M., Schumacher, N., Schmidt, F., Wichert, R., Schneppenheim, J., Lokau, J., Pickhinke, U., Koudelka, T., Tholey, A., Rabe, B., Scheller, J., Lucius, R., Garbers, C., Rose-John, S., & Becker-Pauly, C. (2017). Meprin metalloproteases generate biologically active soluble interleukin-6 receptor to induce trans-signaling. Scientific Reports, 7(1), 44053. https://doi.org/10.1038/srep44053
  • Banerjee, S., & Bond, J. S. (2008). Prointerleukin-18 is activated by meprin beta in vitro and in vivo in intestinal inflammation. The Journal of Biological Chemistry, 283(46), 31371–31377. https://doi.org/10.1074/jbc.M802814200
  • Banerjee, S., Amin, S. A., Adhikari, N., & Jha, T. (2020). Essential elements regulating HDAC8 inhibition: A classification based structural analysis and enzyme-inhibitor interaction study of hydroxamate based HDAC8 inhibitors. Journal of Biomolecular Structure & Dynamics, 38(18), 5513–5525. https://doi.org/10.1080/07391102.2019.1704881
  • Banerjee, S., Baidya, S. K., Ghosh, B., Adhikari, N., & Jha, T. (2022). The first report on predictive comparative ligand-based multi-QSAR modeling analysis of 4-pyrimidinone and 2-pyridinone based APJ inhibitors. New Journal of Chemistry, 46(24), 11591–11607. https://doi.org/10.1039/D2NJ01923J
  • Banerjee, S., Baidya, S. K., Ghosh, B., Nandi, S., Mandal, M., Jha, T., & Adhikari, N. (2023). Quantitative structural assessments of potential meprin β inhibitors by non-linear QSAR approaches and validation by binding mode of interaction analysis. New Journal of Chemistry, 47(15), 7051–7069. https://doi.org/10.1039/D2NJ04753E
  • Banks, J. L., Beard, H. S., Cao, Y., Cho, A. E., Damm, W., Farid, R., Felts, A. K., Halgren, T. A., Mainz, D. T., Maple, J. R., Murphy, R., Philipp, D. M., Repasky, M. P., Zhang, L. Y., Berne, B. J., Friesner, R. A., Gallicchio, E., & Levy, R. M. (2005). Integrated modeling program, applied chemical theory (IMPACT). Journal of Computational Chemistry, 26(16), 1752–1780. https://doi.org/10.1002/jcc.20292
  • Bedau, T., Peters, F., Prox, J., Arnold, P., Schmidt, F., Finkernagel, M., Köllmann, S., Wichert, R., Otte, A., Ohler, A., Stirnberg, M., Lucius, R., Koudelka, T., Tholey, A., Biasin, V., Pietrzik, C. U., Kwapiszewska, G., & Becker-Pauly, C. (2017). Ectodomain shedding of CD99 within highly conserved regions is mediated by the metalloprotease meprin β and promotes transendothelial cell migration. FASEB Journal, 31(3), 1226–1237. https://doi.org/10.1096/fj.201601113R
  • Bender, A., Mussa, H. Y., Glen, R. C., & Reiling, S. (2004). Molecular Similarity Searching Using Atom Environments, Information-Based Feature Selection, and a Naive Bayesian Classifier. Journal of Chemical Information and Computer Sciences, 44(1), 170–178. https://doi.org/10.1021/ci034207y
  • Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1-3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-E
  • Berner, D. K., Wessolowski, L., Armbrust, F., Schneppenheim, J., Schlepckow, K., Koudelka, T., Scharfenberg, F., Lucius, R., Tholey, A., Kleinberger, G., Haass, C., Arnold, P., & Becker-Pauly, C. (2020). Meprin β cleaves TREM2 and controls its phagocytic activity on macrophages. FASEB Journal, 34(5), 6675–6687. https://doi.org/10.1096/fj.201902183R
  • Beynon, R. J., Shannon, J. D., & Bond, J. S. (1981). Purification and characterization of a metallo-endoproteinase from mouse kidney. The Biochemical Journal, 199(3), 591–598. https://doi.org/10.1042/bj1990591
  • Biasin, V., Wygrecka, M., Marsh, L. M., Becker-Pauly, C., Brcic, L., Ghanim, B., Klepetko, W., Olschewski, A., & Kwapiszewska, G. (2017). Meprin β contributes to collagen deposition in lung fibrosis. Scientific Reports, 7(1), 39969. https://doi.org/10.1038/srep39969
  • Bien, J., Jefferson, T., Causević, M., Jumpertz, T., Munter, L., Multhaup, G., Weggen, S., Becker-Pauly, C., & Pietrzik, C. U. (2012). The metalloprotease meprin β generates amino terminal-truncated amyloid β peptide species. The Journal of Biological Chemistry, 287(40), 33304–33313. https://doi.org/10.1074/jbc.M112.395608
  • Bond, J. S., & Beynon, R. J. (1995). The astacin family of metalloendopeptidases. Protein Science: A Publication of the Protein Society, 4(7), 1247–1261. https://doi.org/10.1002/pro.5560040701
  • Broder, C., & Becker-Pauly, C. (2013). The metalloproteases meprin α and meprin β: Unique enzymes in inflammation, neurodegeneration, cancer and fibrosis. The Biochemical Journal, 450(2), 253–264. https://doi.org/10.1042/BJ20121751
  • Broder, C., Arnold, P., Vadon-Le Goff, S., Konerding, M. A., Bahr, K., Müller, S., Overall, C. M., Bond, J. S., Koudelka, T., Tholey, A., Hulmes, D. J., Moali, C., & Becker-Pauly, C. (2013). Metalloproteases meprin α and meprin β are C- and N-procollagen proteinases important for collagen assembly and tensile strength. Proceedings of the National Academy of Sciences of the United States of America, 110(35), 14219–14224. https://doi.org/10.1073/pnas.1305464110
  • ChemDraw Ultra 5.0. (2010). Software available at Cambridge Soft Corporation, USA. http://www.cambridgesoft.com
  • Chhatbar, D. M., Chaube, U. J., Vyas, V. K., & Bhatt, H. G. (2019). CoMFA, CoMSIA, topomer CoMFA, HQSAR, molecular docking and molecular dynamics simulations study of triazine morpholino derivatives as mTOR inhibitors for the treatment of breast cancer. Computational Biology and Chemistry, 80, 351–363. https://doi.org/10.1016/j.compbiolchem.2019.04.017
  • De Vivo, M., Masetti, M., Bottegoni, G., & Cavalli, A. (2016). Role of molecular dynamics and related methods in drug discovery. Journal of Medicinal Chemistry, 59(9), 4035–4061. https://doi.org/10.1021/acs.jmedchem.5b01684
  • Discovery Studio 3.0. (2011). Accelrys Inc., San Diego, USA. http://www.accelrys.com.
  • Fawcett, T. (2006). An introduction to ROC analysis. Pattern Recognition Letters, 27(8), 861–874. https://doi.org/10.1016/j.patrec.2005.10.010
  • Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. https://doi.org/10.1517/17460441.2015.1032936
  • Glick, M., Jenkins, J. L., Nettles, J. H., Hitchings, H., & Davies, J. W. (2006). Enrichment of high-throughput screening data with increasing levels of noise using support vector machines, recursive partitioning, and laplacian-modified naive bayesian classifiers. Journal of Chemical Information and Modeling, 46(1), 193–200. https://doi.org/10.1021/ci050374h
  • Guttikonda, V., Raavi, D., Maadwar, S. K., & Gade, D. R. (2015). Molecular insights of benzodipyrazole as CDK2 inhibitors: Combined molecular docking, molecular dynamics, and 3D QSAR studies. Journal of Receptor and Signal Transduction Research, 35(5), 439–449. https://doi.org/10.3109/10799893.2015.1018433
  • Haider, S., Parkinson, G. N., & Neidle, S. (2008). Molecular dynamics and principal components analysis of human telomeric quadruplex multimers. Biophysical Journal, 95(1), 296–311. https://doi.org/10.1529/biophysj.107.120501
  • Heritage, T. W., & Lowis, D. R. (1999). Molecular hologram QSAR. In A. L. Parrill, & M. R. Reddy (Eds.), Rational drug design: Novel methodology and practical applications (pp. 212–225). American Chemical Society. https://www.gromacs.org/
  • Kagami, L. P., das Neves, G. M., Timmers, L. F. S. M., Caceres, R. A., & Eifler-Lima, V. L. (2020). Geo-Measures: A PyMOL plugin for protein structure ensembles analysis. Computational Biology and Chemistry, 87, 107322. https://doi.org/10.1016/j.compbiolchem.2020.107322
  • Li, H., Robertson, A. D., & Jensen, J. H. (2005). Very fast empirical prediction and interpretation of protein pKa values. Proteins, 61(4), 704–721. https://doi.org/10.1002/prot.20660
  • Mukerjee, N., Das, A., Maitra, S., Ghosh, A., Khan, P., Alexiou, A., Dey, A., Baishya, D., Ahmad, F., Sachdeva, P., & Al-Muhanna, M. K. (2022). Dynamics of natural product Lupenone as a potential fusion inhibitor against the spike complex of novel Semliki Forest Virus. PloS One, 17(2), e0263853. https://doi.org/10.1371/journal.pone.0263853
  • Oneda, B., Lods, N., Lottaz, D., Becker-Pauly, C., Stöcker, W., Pippin, J., Huguenin, M., Ambort, D., Marti, H. P., & Sterchi, E. E. (2008). Metalloprotease meprin beta in rat kidney: Glomerular localization and differential expression in glomerulonephritis. PloS One, 3(5), e2278. https://doi.org/10.1371/journal.pone.0002278
  • Papaleo, E., Mereghetti, P., Fantucci, P., Grandori, R., & De Gioia, L. (2009). Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: The myoglobin case. Journal of Molecular Graphics & Modelling, 27(8), 889–899. https://doi.org/10.1016/j.jmgm.2009.01.006
  • Peters, F., & Becker-Pauly, C. (2019). Role of meprin metalloproteases in metastasis and tumor microenvironment. Cancer Metastasis Reviews, 38(3), 347–356. https://doi.org/10.1007/s10555-019-09805-5
  • Peters, F., Rahn, S., Mengel, M., Scharfenberg, F., Otte, A., Koudelka, T., Wagner, E. F., Wunderlich, F. T., Haase, M., Naumann, R., Tholey, A., & Becker-Pauly, C. (2021). Syndecan-1 shedding by meprin β impairs keratinocyte adhesion and differentiation in hyperkeratosis. Matrix Biology: Journal of the International Society for Matrix Biology, 102, 37–69. https://doi.org/10.1016/j.matbio.2021.08.002
  • Ramsbeck, D., Hamann, A., Richter, G., Schlenzig, D., Geissler, S., Nykiel, V., Cynis, H., Schilling, S., & Buchholz, M. (2018). Structure-guided design, synthesis, and characterization of next-generation meprin β inhibitors. Journal of Medicinal Chemistry, 61(10), 4578–4592. https://doi.org/10.1021/acs.jmedchem.8b00330
  • Ramsbeck, D., Hamann, A., Schlenzig, D., Schilling, S., & Buchholz, M. (2017). First insight into structure-activity relationships of selective meprin β inhibitors. Bioorganic & Medicinal Chemistry Letters, 27(11), 2428–2431. https://doi.org/10.1016/j.bmcl.2017.04.012
  • RCSB Protein Data Bank. (2023). https://www.rcsb.org/as
  • Rizzo, R. C., Toba, S., & Kuntz, I. D. (2004). A molecular basis for the selectivity of thiadiazole urea inhibitors with stromelysin-1 and gelatinase-A from generalized born molecular dynamics simulations. Journal of Medicinal Chemistry, 47(12), 3065–3074. https://doi.org/10.1021/jm030570k
  • Schrodinger Suite, Schrodinger LLC. (2019). New York, USA. https://www.schrodinger.com
  • Schütte, A., Ermund, A., Becker-Pauly, C., Johansson, M. E., Rodriguez-Pineiro, A. M., Bäckhed, F., Müller, S., Lottaz, D., Bond, J. S., & Hansson, G. C. (2014). Microbial-induced meprin β cleavage in MUC2 mucin and a functional CFTR channel are required to release anchored small intestinal mucus. Proceedings of the National Academy of Sciences of the United States of America, 111(34), 12396–12401. https://doi.org/10.1073/pnas.1407597111
  • Sterchi, E. E., Green, J. R., & Lentze, M. J. (1982). Non-pancreatic hydrolysis of N-benzoyl-l-tyrosyl-p-aminobenzoic acid (PABA-peptide) in the human small intestine. Clinical Science (London, England: 1979), 62(5), 557–560. https://doi.org/10.1042/cs0620557
  • Stockfisch, T. P. (2003). Partially unified multiple property recursive partitioning (PUMP-RP): A new method for predicting and understanding drug selectivity. Journal of Chemical Information and Computer Sciences, 43(5), 1608–1613. https://doi.org/10.1021/ci0203794
  • SYBYL-X 2.0 Software. (2012). Tripos Inc., St. Louis. MO, USA; software available at http://www.certara.com.
  • Tan, K., Jäger, C., Schlenzig, D., Schilling, S., Buchholz, M., & Ramsbeck, D. (2018). Tertiary-amine-based inhibitors of the astacin protease meprin α. ChemMedChem. 13(16), 1619–1624. https://doi.org/10.1002/cmdc.201800300
  • Tong, J. B., Bian, S., Zhang, X., & Luo, D. (2022). QSAR analysis of 3-pyrimidin-4-yl-oxazolidin-2-one derivatives isocitrate dehydrogenase inhibitors using Topomer CoMFA and HQSAR methods. Molecular Diversity, 26(2), 1017–1037. https://doi.org/10.1007/s11030-021-10222-6
  • Tong, W., Lowis, D. R., Perkins, R., Chen, Y., Welsh, W. J., Goddette, D. W., Heritage, T. W., & Sheehan, D. M. (1998). Evaluation of quantitative structure-activity relationship methods for large-scale prediction of chemicals binding to the estrogen receptor. Journal of Chemical Information and Computer Sciences, 38(4), 669–677. https://doi.org/10.1021/ci980008g
  • Wold, S., Esbensen, K., & Geladi, P. (1987). Principal component analysis. Chemometrics and Intelligent Laboratory Systems, 2(1-3), 37–52. https://doi.org/10.1016/0169-7439(87)80084-9
  • Xia, X., Maliski, E. G., Gallant, P., & Rogers, D. (2004). Classification of kinase inhibitors using a Bayesian model. Journal of Medicinal Chemistry, 47(18), 4463–4470. https://doi.org/10.1021/jm0303195
  • Yadav, V., Banerjee, S., Baidya, S. K., Adhikari, N., & Jha, T. (2022). Applying comparative molecular modelling techniques on diverse hydroxamate-based HDAC2 inhibitors: An attempt to identify promising structural features for potent HDAC2 inhibition. SAR and QSAR in Environmental Research, 33(1), 1–22. https://doi.org/10.1080/1062936X.2021.2013317
  • Yap, C. W. (2011). PaDEL-descriptor: An open source software to calculate molecular descriptors and fingerprints. Journal of Computational Chemistry, 32(7), 1466–1474. https://doi.org/10.1002/jcc.21707
  • Zhao, T., Zhao, Z., Lu, F., Chang, S., Zhang, J., Pang, J., & Tian, Y. (2020). Two- and three-dimensional QSAR studies on hURAT1 inhibitors with flexible linkers: Topomer CoMFA and HQSAR. Molecular Diversity, 24(1), 141–154. https://doi.org/10.1007/s11030-019-09936-5
  • Zweig, M. H., & Campbell, G. (1993). Receiver-operating characteristic (ROC) plots: A fundamental evaluation tool in clinical medicine. Clinical Chemistry, 39(4), 561–577. https://doi.org/10.1093/clinchem/39.4.561

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