Identification of selective cyclin-dependent kinase 2 inhibitor from the library of pyrrolone-fused benzosuberene compounds: an in silico exploration

References

• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindah, E. (2015). Gromacs: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
   Google Scholar
• Ali, S. K., Sneha, P., Priyadharshini Christy, J., Zayed, H., & George Priya Doss, C. (2017). Molecular dynamics-based analyses of the structural instability and secondary structure of the fibrinogen gamma chain protein with the D356V mutation. Journal of Biomolecular Structure & Dynamics, 35(12), 2714–2724. https://doi.org/10.1080/07391102.2016.1229634
   PubMed Web of Science ®Google Scholar
• Baumli, S., Lolli, G., Lowe, E. D., Troiani, S., Rusconi, L., Bullock, A. N., Debreczeni, J. É., Knapp, S., & Johnson, L. N. (2008). The structure of P-TEFb (CDK9/cyclin T1), its complex with flavopiridol and regulation by phosphorylation. The EMBO Journal, 27(13), 1907–1918. https://doi.org/10.1038/emboj.2008.121
   PubMed Web of Science ®Google Scholar
• Betzi, S., Alam, R., Martin, M., Lubbers, D. J., Han, H., Jakkaraj, S. R., Georg, G. I., & Schönbrunn, E. (2011). Discovery of a potential allosteric ligand binding site in CDK2. ACS Chemical Biology, 6(5), 492–501. https://doi.org/10.1021/cb100410m
   PubMed Web of Science ®Google Scholar
• Bhardwaj, V. K., Singh, R., Sharma, J., Das, P., & Purohit, R. (2020). Structural based study to identify new potential inhibitors for dual specificity tyrosine-phosphorylation- regulated kinase. Computer Methods and Programs in Biomedicine, 194, 105494. https://doi.org/10.1016/j.cmpb.2020.105494
   PubMed Web of Science ®Google Scholar
• Bharti, R., Reddy, C. B., & Das, P. (2017). Oxalic acid as sustainable CO source for pyrrolone-fused benzosuberenes synthesis through palladium catalyzed carbonylative cyclization. ChemistrySelect, 2(17), 4626–4629. https://doi.org/10.1002/slct.201700592
   Web of Science ®Google Scholar
• Bohgaki, T., Bohgaki, M., & Hakem, R. (2010). DNA double-strand break signaling and human disorders. Genome Integrity, 1(1), 15. https://doi.org/10.1186/2041-9414-1-15
   PubMedGoogle Scholar
• Brooks, E. E., Gray, N. S., Joly, A., Kerwar, S. S., Lum, R., Mackman, R. L., Norman, T. C., Rosete, J., Rowe, M., Schow, S. R., Schultz, P. G., Wang, X., Wick, M. M., & Shiffman, D. (1997). CVT-313, a specific and potent inhibitor of CDK2 that prevents neointimal proliferation. J Biol Chem, 272(46), 29207–29211. https://doi.org/10.1074/jbc.272.46.29207
   PubMed Web of Science ®Google Scholar
• Calbó, J., Serna, C., Garriga, J., Graña, X., & Mazo, A. (2004). The fate of pancreatic tumor cell lines following p16 overexpression depends on the modulation of CDK2 activity. Cell Death and Differentiation, 11(10), 1055–1065. https://doi.org/10.1038/sj.cdd.4401481
   PubMed Web of Science ®Google Scholar
• Cortez, D. (2015). Preventing replication fork collapse to maintain genome integrity. DNA Repair, 32, 149–157. https://doi.org/10.1016/j.dnarep.2015.04.026
   PubMed Web of Science ®Google Scholar
• De Vivo, M., Bottegoni, G., Berteotti, A., Recanatini, M., Gervasio, F. L., & Cavalli, A. (2011). Cyclin-dependent kinases: Bridging their structure and function through computations. Future Medicinal Chemistry, 3(12), 1551–1559. https://doi.org/10.4155/fmc.11.113
   PubMed Web of Science ®Google Scholar
• Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. The Journal of Chemical Physics, 103(19), 8577–8593. https://doi.org/10.1063/1.470117
   Web of Science ®Google Scholar
• Faber, A. C., & Chiles, T. C. (2007). Inhibition of cyclin-dependent kinase-2 induces apoptosis in human diffuse large b-cell lymphomas. Cell Cycle (Georgetown, Tex.), 6(23), 2982–2989. https://doi.org/10.4161/cc.6.23.4994
   PubMed Web of Science ®Google Scholar
• Franco, L. C., Morales, F., Boffo, S., & Giordano, A. (2018). CDK9: A key player in cancer and other diseases. Journal of Cellular Biochemistry, 119(2), 1273–1284. https://doi.org/10.1002/jcb.26293
   PubMed Web of Science ®Google Scholar
• George Priya Doss, C., Nagasundaram, N., Chakraborty, C., Chen, L., & Zhu, H. (2013). Extrapolating the effect of deleterious nsSNPs in the binding adaptability of flavopiridol with CDK7 protein: A molecular dynamics approach. Human Genomics, 7(1). https://doi.org/10.1186/1479-7364-7-10
   Google Scholar
• Harper, J. W., & Adams, P. D. (2001). Cyclin-dependent kinases. Chemical Reviews, 101(8), 2511–2526. https://doi.org/10.1021/cr0001030
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A Linear Constraint Solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12 < 1463::AID-JCC4 > 3.0.CO;2-H
   Web of Science ®Google Scholar
• Horiuchi, D., Huskey, N. E., Kusdra, L., Wohlbold, L., Merrick, K. A., Zhang, C., Creasman, K. J., Shokat, K. M., Fisher, R. P., & Goga, A. (2012). Chemical-genetic analysis of cyclin dependent kinase 2 function reveals an important role in cellular transformation by multiple oncogenic pathways. Proceedings of the National Academy of Sciences of the United States of America, 109(17), E1019–E1027. https://doi.org/10.1073/pnas.1111317109
   PubMed Web of Science ®Google Scholar
• Hu, S., Lu, Y., Orr, B., Godek, K., Mustachio, L. M., Kawakami, M., Sekula, D., Compton, D. A., Freemantle, S., & Dmitrovsky, E. (2015). Specific CP110 phosphorylation sites mediate anaphase catastrophe after CDK2 inhibition: Evidence for cooperation with USP33 knockdown. Molecular Cancer Therapeutics, 14(11), 2576–2585. https://doi.org/10.1158/1535-7163.MCT-15-0443
   PubMed Web of Science ®Google Scholar
• Huang, H., Regan, K. M., Lou, Z., Chen, J., & Tindall, D. J. (2006). CDK2-dependent phosphorylation of FOXO1 as an apoptotic response to DNA damage. Science (New York, N.Y.), 314(5797), 294–297. https://doi.org/10.1126/science.1130512
   PubMed Web of Science ®Google Scholar
• Karagiannis, J., & Balasubramanian, M. K. (2007). A cyclin-dependent kinase that promotes cytokinesis through modulating phosphorylation of the carboxy terminal domain of the RNA pol II Rpb1p sub-unit. PLoS One, 2(5), e433. https://doi.org/10.1371/journal.pone.0000433
   PubMed Web of Science ®Google Scholar
• Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., Lee, M., Lee, T., Duan, Y., Wang, W., Donini, O., Cieplak, P., Srinivasan, J., Case, D. A., & Cheatham, T. E. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33(12), 889–897. https://doi.org/10.1021/ar000033j
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A. (2014). g_mmpbsa-a GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Lane, M. E., Yu, B., Pestell, R. G., Wadler, S., Rice, A., Lipson, K. E., Liang, C., Sun, L., Tang, C., & McMahon, G. (2001). A novel cdk2-selective inhibitor, SU9516, induces apoptosis in colon carcinoma cells. Cancer Research, 61(16), 6170–6177.
   PubMed Web of Science ®Google Scholar
• Liao, H., Ji, F., Geng, X., Xing, M., Li, W., Chen, Z., Shen, H., & Ying, S. (2017). CDK1 promotes nascent DNA synthesis and induces resistance of cancer cells to DNA-damaging therapeutic agents. Oncotarget, 8(53), 90662–90673. https://doi.org/10.18632/oncotarget.21730
   PubMedGoogle Scholar
• Li, L., Wang, L., & Alexov, E. (2015). On the energy components governing molecular recognition in the framework of continuum approaches. Frontiers in Molecular Biosciences, 2, 5. https://doi.org/10.3389/fmolb.2015.00005
   PubMed Web of Science ®Google Scholar
• Li, Y., Yang, X. H., Fang, S. J., Qin, C. F., Sun, R. L., Liu, Z. Y., Jiang, B. Y., Wu, X., & Li, G. (2015). HOXA7 stimulates human hepatocellular carcinoma proliferation through cyclin E1/CDK2. Oncology Reports, 33(2), 990–996. https://doi.org/10.3892/or.2014.3668
   PubMed Web of Science ®Google Scholar
• Malumbres, M., Harlow, E., Hunt, T., Hunter, T., Lahti, J. M., Manning, G., Morgan, D. O., Tsai, L. H., & Wolgemuth, D. J. (2009). Cyclin-dependent kinases: A family portrait. Nature Cell Biology, 11(11), 1275–1276. https://doi.org/10.1038/ncb1109-1275
   PubMed Web of Science ®Google Scholar
• Molenaar, J. J., Ebus, M. E., Geerts, D., Koster, J., Lamers, F., Valentijn, L. J., Westerhout, E. M., Versteeg, R., & Caron, H. N. (2009). Inactivation of CDK2 is synthetically lethal to MYCN over-expressing cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 106(31), 12968–12973. https://doi.org/10.1073/pnas.0901418106
   PubMed Web of Science ®Google Scholar
• Neganova, I., Vilella, F., Atkinson, S. P., Lloret, M., Passos, J. F., von Zglinicki, T., O'Connor, J.-E., Burks, D., Jones, R., Armstrong, L., & Lako, M. (2011). An important role for CDK2 in G1 to S checkpoint activation and DNA damage response in human embryonic stem cells. Stem Cells (Dayton, Ohio), 29(4), 651–659. https://doi.org/10.1002/stem.620
   PubMed Web of Science ®Google Scholar
• Peng, C., Zeng, W., Su, J., Kuang, Y., He, Y., Zhao, S., Zhang, J., Ma, W., Bode, A. M., Dong, Z., & Chen, X. (2016). Cyclin-dependent kinase 2 (CDK2) is a key mediator for EGF-induced cell transformation mediated through the ELK4/c-Fos signaling pathway. Oncogene, 35(9), 1170–1179. https://doi.org/10.1038/onc.2015.175
   PubMed Web of Science ®Google Scholar
• Pierson-Mullany, L. K., & Lange, C. A. (2004). Phosphorylation of progesterone receptor serine 400 mediates ligand-independent transcriptional activity in response to activation of cyclin-dependent protein kinase 2. Molecular and Cellular Biology, 24(24), 10542–10557.https://doi.org/10.1128/mcb.24.24.10542-10557.2004
   PubMed Web of Science ®Google Scholar
• Reulecke, I., Lange, G., Albrecht, J., Klein, R., & Rarey, M. (2008). Towards an integrated description of hydrogen bonding and dehydration: Decreasing false positives in virtual screening with the HYDE scoring function. ChemMedChem., 3(6), 885–897. https://doi.org/10.1002/cmdc.200700319
   PubMed Web of Science ®Google Scholar
• Rogatsky, I., Trowbridge, J. M., & Garabedian, M. J. (1999). Potentiation of human estrogen receptor alpha transcriptional activation through phosphorylation of serines 104 and 106 by the cyclin A-CDK2 complex. The Journal of Biological Chemistry, 274(32), 22296–22302. https://doi.org/10.1074/jbc.274.32.22296
   PubMed Web of Science ®Google Scholar
• Satyanarayana, A., & Kaldis, P. (2009). A dual role of Cdk2 in DNA damage response. Cell Division, 4, 9. https://doi.org/10.1186/1747-1028-4-9
   PubMed Web of Science ®Google Scholar
• Schneider, N., Lange, G., Hindle, S., Klein, R., & Rarey, M. (2013). A consistent description of HYdrogen bond and DEhydration energies in protein-ligand complexes: Methods behind the HYDE scoring function. Journal of Computer-Aided Molecular Design, 27(1), 15–29. https://doi.org/10.1007/s10822-012-9626-2
   PubMed Web of Science ®Google Scholar
• Schüttelkopf, A. W., & Van Aalten, D. M. F. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica. Section D, Biological Crystallography, 60(Pt 8), 1355–1363. https://doi.org/10.1107/S0907444904011679
   PubMedGoogle Scholar
• Sharma, J., Bhardwaj, V., & Purohit, R. (2019). Structural perturbations due to mutation (H1047R) in phosphoinositide-3-kinase (PI3Kα) and its involvement in oncogenesis: An in silico insight. ACS Omega, 4(14), 15815–15823. https://doi.org/10.1021/acsomega.9b01439
   PubMed Web of Science ®Google Scholar
• Singh, R., Bhardwaj, V., Das, P., & Purohit, R. (2020). Natural analogues inhibiting selective cyclin-dependent kinase protein isoforms: A computational perspective. Journal of Biomolecular Structure & Dynamics, 38(17), 5126–5135. https://doi.org/10.1080/07391102.2019.1696709
   PubMed Web of Science ®Google Scholar
• Singh, R., Bhardwaj, V., & Purohit, R. (2021a). Identification of a novel binding mechanism of Quinoline based molecules with lactate dehydrogenase of Plasmodium falciparum. Journal of Biomolecular Structure & Dynamics, 39(1), 348–315. https://doi.org/10.1080/07391102.2020.1711809
   PubMed Web of Science ®Google Scholar
• Singh, R., Bhardwaj, V. K., Sharma, J., Das, P., & Purohit, R. (2021b). Discovery and in silico evaluation of aminoarylbenzosuberene molecules as novel checkpoint kinase 1 inhibitor determinants. Genomics, 113(1), 707–715. https://doi.org/10.1016/j.ygeno.2020.10.001
   PubMed Web of Science ®Google Scholar
• Studio, D. (2015). Dassault systemes BIOVIA, discovery studio modelling environment, release 4.5. Accelrys Software Inc, 98–104.
   Google Scholar
• Takada, M., Zhang, W., Suzuki, A., Kuroda, T. S., Yu, Z., Inuzuka, H., Gao, D., Wan, L., Zhuang, M., Hu, L., Zhai, B., Fry, C. J., Bloom, K., Li, G., Karpen, G. H., Wei, W., & Zhang, Q. (2017). FBW7 loss promotes chromosomal instability and tumorigenesis via cyclin E1/CDK2-Mediated Phosphorylation of CENP-A. Cancer Research, 77(18), 4881–4893. https://doi.org/10.1158/0008-5472.CAN-17-1240
   PubMed Web of Science ®Google Scholar
• Tanwar, G., Mazumder, A. G., Bhardwaj, V., Kumari, S., Bharti, R., Yamini, Singh, D., Das, P., & Purohit, R. (2019). Target identification, screening and in vivo evaluation of pyrrolone-fused benzosuberene compounds against human epilepsy using Zebrafish model of pentylenetetrazol-induced seizures. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-44264-6
   Google Scholar
• Thirumal Kumar, D., & George Priya Doss, C. (2016). Investigating the inhibitory effect of Wortmannin in the hotspot mutation at codon 1047 of PIK3CA kinase domain: A molecular docking and molecular dynamics approach. Advances in Protein Chemistry and Structural Biology, 102, 267–297. https://doi.org/10.1016/bs.apcsb.2015.09.008
   PubMed Web of Science ®Google Scholar
• Viera, A., Rufas, J. S., Martínez, I., Barbero, J. L., Ortega, S., & Suja, J. A. (2009). CDK2 is required for proper homologous pairing, recombination and sex-body formation during male mouse meiosis. Journal of Cell Science, 122(Pt 12), 2149–2159. https://doi.org/10.1242/jcs.046706
   PubMed Web of Science ®Google Scholar
• Wang, J., Yang, T., Xu, G., Liu, H., Ren, C., Xie, W., & Wang, M. (2016). Cyclin-dependent kinase 2 promotes tumor proliferation and induces radio resistance in glioblastoma. Translational Oncology, 9(6), 548–556. https://doi.org/10.1016/j.tranon.2016.08.007
   PubMed Web of Science ®Google Scholar
• Wood, D. J., Korolchuk, S., Tatum, N. J., Wang, L. Z., Endicott, J. A., Noble, M. E. M., & Martin, M. P. (2019). Differences in the conformational energy landscape of CDK1 and CDK2 suggest a mechanism for achieving selective CDK inhibition. Cell Chemical Biology, 26(1), 121–130.e5. https://doi.org/10.1016/j.chembiol.2018.10.015
   PubMed Web of Science ®Google Scholar
• Yang, L., Fang, D., Chen, H., Lu, Y., Dong, Z., Ding, H. F., Jing, Q., Su, S. B., & Huang, S. (2015). Cyclin-dependent kinase 2 is an ideal target for ovary tumors with elevated cyclin E1 expression. Oncotarget, 6(25), 20801–20812. https://doi.org/10.18632/oncotarget.4600
   PubMedGoogle Scholar
• Yin, X., Yu, J., Zhou, Y., Wang, C., Jiao, Z., Qian, Z., Sun, H., & Chen, B. (2018). Identification of CDK2 as a novel target in treatment of prostate cancer. Future Oncology (London, England), 14(8), 709–718. https://doi.org/10.2217/fon-2017-0561
   PubMed Web of Science ®Google Scholar
• Ying, M., Shao, X., Jing, H., Liu, Y., Qi, X., Cao, J., Chen, Y., Xiang, S., Song, H., Hu, R., Wei, G., Yang, B., & He, Q. (2018). Ubiquitin-dependent degradation of CDK2 drives the therapeutic differentiation of AML by targeting PRDX2. Blood, 131(24), 2698–2711. https://doi.org/10.1182/blood-2017-10-813139
   PubMed Web of Science ®Google Scholar
• Zheng, J., & Frisch, M. J. (2017). Efficient geometry minimization and transition structure optimization using interpolated potential energy surfaces and iteratively updated hessians. Journal of Chemical Theory and Computation, 13(12), 6424–6432. https://doi.org/10.1021/acs.jctc.7b00719
   PubMed Web of Science ®Google Scholar
• Zhou, Q., Li, T., & Price, D. H. (2012). RNA polymerase II elongation control. Annual Review of Biochemistry, 81, 119–143. https://doi.org/10.1146/annurev-biochem-052610-095910
   PubMed Web of Science ®Google Scholar