Identification of indole-based natural compounds as inhibitors of PARP-1 against triple-negative breast cancer: a computational study

References

• Ávalos-Moreno, M., López-Tejada, A., Blaya-Cánovas, J. L., Cara-Lupiañez, F. E., González-González, A., Lorente, J. A., Sánchez-Rovira, P., & Granados-Principal, S. (2020). Drug repurposing for triple-negative breast cancer. Journal of Personalized Medicine, 10(4), 200. https://doi.org/10.3390/jpm10040200
   PubMed Web of Science ®Google Scholar
• Banerjee, P., Eckert, A. O., Schrey, A. K., & Preissner, R. (2018). ProTox-II: A webserver for the prediction of toxicity of chemicals. Nucleic Acids Research, 46(W1), W257–W263. https://doi.org/10.1093/nar/gky318
   PubMed Web of Science ®Google Scholar
• Barkauskaite, E., Jankevicius, G., & Ahel, I. (2015). Structures and mechanisms of enzymes employed in the synthesis and degradation of PARP-dependent protein ADP-ribosylation. Molecular Cell, 58(6), 935–946. https://doi.org/10.1016/j.molcel.2015.05.007
   PubMed Web of Science ®Google Scholar
• Bauer, K. R., Brown, M., Cress, R. D., Parise, C. A., & Caggiano, V. (2007). Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: A population-based study from the California Cancer Registry. Cancer, 109(9), 1721–1728. https://doi.org/10.1002/cncr.22618
   PubMed Web of Science ®Google Scholar
• Bayly, C. I., Cieplak, P., Cornell, W. D., & Kollman, P. A. (1993). A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. The Journal of Physical Chemistry, 97(40), 10269–10280. https://doi.org/10.1021/j100142a004
   Web of Science ®Google Scholar
• 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
   Web of Science ®Google Scholar
• Brown, J. S., Kaye, S. B., & Yap, T. A. (2016). PARP inhibitors: The race is on. British Journal of Cancer, 114(7), 713–715. https://doi.org/10.1038/bjc.2016.67
   PubMed Web of Science ®Google Scholar
• Bürkle, A., Brabeck, C., Diefenbach, J., & Beneke, S. (2005). The emerging role of poly(ADP-ribose) polymerase-1 in longevity. The International Journal of Biochemistry & Cell Biology, 37(5), 1043–1053. https://doi.org/10.1016/j.biocel.2004.10.006
   PubMed Web of Science ®Google Scholar
• Daina, A., Michielin, O., & Zoete, V. (2017). SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Scientific Reports, 7(1), 1–13. https://doi.org/10.1038/srep42717
   PubMed Web of Science ®Google Scholar
• Damaskos, C., Garmpis, N., Garmpi, A., Nikolettos, K., Sarantis, P., Georgakopoulou, V. E., Nonni, A., Schizas, D., Antoniou, E. A., Karamouzis, M. V., Nikolettos, N., Kontzoglou, K., Patsouras, A., Voutyritsa, E., Syllaios, A., Koustas, E., Trakas, N., & Dimitroulis, D. (2021). Investigational drug treatments for triple-negative breast cancer. Journal of Personalized Medicine, 11(7), 652. https://doi.org/10.3390/jpm11070652
   PubMed Web of Science ®Google Scholar
• DeLano, W. L. (2002). Pymol: An open-source molecular graphics tool. CCP4 Newsletter on Protein Crystallography, 40, 82–92.
   Google Scholar
• Elmeliegy, M., Yu, Y., Litton, J. K., Czibere, A., Wilson, G. G., Tudor, I. C., Zheng, J., & Wang, D. D. (2020). Exposure-safety analyses of talazoparib in patients with advanced breast cancer and germline BRCA1/2 mutations in the EMBRACA and ABRAZO trials. Journal of Clinical Pharmacology, 60(10), 1334–1343. https://doi.org/10.1002/jcph.1626
   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
• Esther Rubavathy, S. M., Palanisamy, K., Priyankha, S., Thilagavathi, R., Prakash, M., & Selvam, C. (2022). Discovery of novel HDAC8 inhibitors from natural compounds by in silico high throughput screening. Journal of Biomolecular Structure and Dynamics, 0(0), 1–11. https://doi.org/10.1080/07391102.2022.2142668
   Google Scholar
• Eustermann, S., Wu, W. F., Langelier, M. F., Yang, J. C., Easton, L. E., Riccio, A. A., Pascal, J. M., & Neuhaus, D. (2015). Structural basis of detection and signaling of DNA single-strand breaks by human PARP-1. Molecular Cell, 60(5), 742–754. https://doi.org/10.1016/j.molcel.2015.10.032
   PubMed Web of Science ®Google Scholar
• Ferreira, L. L. G., & Andricopulo, A. D. (2019). ADMET modeling approaches in drug discovery. Drug Discovery Today, 24(5), 1157–1165. https://doi.org/10.1016/j.drudis.2019.03.015
   PubMed Web of Science ®Google Scholar
• Gao, Y., Li, C., Wei, L., Teng, Y., Nakajima, S., Chen, X., Xu, J., Leger, B., Ma, H., Spagnol, S. T., Wan, Y., Dahl, K. N., Liu, Y., Levine, A. S., & Lan, L. (2017). SSRP1 cooperates with PARP and XRCC1 to facilitate single-strand DNA break repair by chromatin priming. Cancer Research, 77(10), 2674–2685. https://doi.org/10.1158/0008-5472.CAN-16-3128
   PubMed Web of Science ®Google Scholar
• Gudd, C. L. C., & Possamai, L. A. (2022). The role of myeloid cells in hepatotoxicity related to cancer immunotherapy. Cancers, 14(8), 1913. https://doi.org/10.3390/cancers14081913
   PubMed Web of Science ®Google Scholar
• Guney Eskiler, G., Cecener, G., Egeli, U., & Tunca, B. (2020). Talazoparib nanoparticles for overcoming multidrug resistance in triple-negative breast cancer. Journal of Cellular Physiology, 235(9), 6230–6245. https://doi.org/10.1002/jcp.29552
   PubMed Web of Science ®Google Scholar
• Herceg, Z., & Wang, Z. Q. (2001). Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutation Research, 477(1-2), 97–110. https://doi.org/10.1016/s0027-5107(01)00111-7
   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
• Hoy, S. M. (2018). Talazoparib: First global approval. Drugs, 78(18), 1939–1946. https://doi.org/10.1007/s40265-018-1026-z
   PubMed Web of Science ®Google Scholar
• Jamdade, V. S., Sethi, N., Mundhe, N. A., Kumar, P., Lahkar, M., & Sinha, N. (2015). Therapeutic targets of triple-negative breast cancer: A review. British Journal of Pharmacology, 172(17), 4228–4237. https://doi.org/10.1111/bph.13211
   PubMed Web of Science ®Google Scholar
• Ji, H. F., Li, X. J., & Zhang, H. Y. (2009). Natural products and drug discovery: Can thousands of years of ancient medical knowledge lead us to new and powerful drug combinations in the fight against cancer and dementia? EMBO Reports, 10(3), 194–200. https://doi.org/10.1038/embor.2009.12
   PubMed Web of Science ®Google Scholar
• Kim, M. Y., Zhang, T., & Kraus, W. L. (2005). Poly (ADP-ribosyl) ation by PARP-1: ‘PAR-laying ’ NAD + into a nuclear signal. 1963, 1951–1967. https://doi.org/10.1101/gad.1331805
   Google Scholar
• Knickle, A., Fernando, W., Greenshields, A. L., Rupasinghe, H. P. V., & Hoskin, D. W. (2018). Myricetin-induced apoptosis of triple-negative breast cancer cells is mediated by the iron-dependent generation of reactive oxygen species from hydrogen peroxide. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 118, 154–167. https://doi.org/10.1016/j.fct.2018.05.005
   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
• Leung, A. K. L. (2014). Poly(ADP-ribose): An organizer of cellular architecture. The Journal of Cell Biology, 205(5), 613–619. https://doi.org/10.1083/jcb.201402114
   PubMed Web of Science ®Google Scholar
• Li, X. H., He, X. R., Zhou, Y. Y., Zhao, H. Y., Zheng, W. X., Jiang, S. T., Zhou, Q., Li, P. P., & Han, S. Y. (2017). Taraxacum mongolicum extract induced endoplasmic reticulum stress associated-apoptosis in triple-negative breast cancer cells. Journal of Ethnopharmacology, 206, 55–64. https://doi.org/10.1016/j.jep.2017.04.025
   PubMed Web of Science ®Google Scholar
• Lipinski, C. A. (2004). Lead- and drug-like compounds: The rule-of-five revolution. Drug Discovery Today. Technologies, 1(4), 337–341. https://doi.org/10.1016/j.ddtec.2004.11.007
   PubMedGoogle Scholar
• Lipinski, C. A., Lombardo, F., Dominy, B. W., & Feeney, P. J. (2012). Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advanced Drug Delivery Reviews, 64(SUPPL), 4–17. https://doi.org/10.1016/j.addr.2012.09.019
   Google Scholar
• Litton, J. K., Rugo, H. S., Ettl, J., Hurvitz, S. A., Gonçalves, A., Lee, K.-H., Fehrenbacher, L., Yerushalmi, R., Mina, L. A., Martin, M., Roché, H., Im, Y.-H., Quek, R. G. W., Markova, D., Tudor, I. C., Hannah, A. L., Eiermann, W., & Blum, J. L. (2018). Talazoparib in patients with advanced breast cancer and a germline BRCA mutation. The New England Journal of Medicine, 379(8), 753–763. https://doi.org/10.1056/NEJMoa1802905
   PubMed Web of Science ®Google Scholar
• McGann, M. (2011). Fred pose prediction and virtual screening accuracy. Journal of Chemical Information and Modeling, 51(1), 578–596.
   PubMedGoogle Scholar
• Maier, J. A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K., Simmerling, C., & Hauser, K. E. (2015). Subscriber access provided by UNIV OF MISSISSIPPI ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB ff14SB: Improving the accuracy of protein side chain and backbone parameters from ff99SB.
   Google Scholar
• Manasaryan, G., Suplatov, D., Pushkarev, S., Drobot, V., Kuimov, A., Švedas, V., & Nilov, D. (2021). Bioinformatic analysis of the nicotinamide binding site in poly(Adp‐ribose) polymerase family proteins. Cancers, 13(6), 1201. https://doi.org/10.3390/cancers13061201
   PubMed Web of Science ®Google Scholar
• Mark, P., & Nilsson, L. (2001). Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. The Journal of Physical Chemistry A, 105(43), 9954–9960. https://doi.org/10.1021/jp003020w
   Web of Science ®Google Scholar
• Mehta, A. K., Cheney, E. M., Hartl, C. A., Pantelidou, C., Oliwa, M., Castrillon, J. A., Lin, J.-R., Hurst, K. E., de Oliveira Taveira, M., Johnson, N. T., Oldham, W. M., Kalocsay, M., Berberich, M. J., Boswell, S. A., Kothari, A., Johnson, S., Dillon, D. A., Lipschitz, M., Rodig, S., … Guerriero, J. L. (2021). Targeting immunosuppressive macrophages overcomes PARP inhibitor resistance in BRCA1-associated triple-negative breast cancer. Nature Cancer, 2(1), 66–82. https://doi.org/10.1038/s43018-020-00148-7
   PubMedGoogle Scholar
• Metzger-Filho, O., Tutt, A., De Azambuja, E., Saini, K. S., Viale, G., Loi, S., Bradbury, I., Bliss, J. M., Azim, H. A., Ellis, P., Di Leo, A., Baselga, J., Sotiriou, C., & Piccart-Gebhart, M. (2012). Dissecting the heterogeneity of triple-negative breast cancer. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology, 30(15), 1879–1887. https://doi.org/10.1200/JCO.2011.38.2010
   PubMedGoogle Scholar
• Mylavarapu, S., Das, A., & Roy, M. (2018). Role of BRCA mutations in the modulation of response to platinum therapy. Frontiers in Oncology, 8(FEB), 1–11. https://doi.org/10.3389/fonc.2018.00016
   PubMedGoogle Scholar
• Pantelidou, C., Sonzogni, O., Taveira, M. D. O., Mehta, A. K., Cheney, E. M., Bouwman, P., Jonkers, J., & Rottenberg, S. (n.d.). PARP inhibitor efficacy depends on CD8+ T cell recruitment via intratumoral STING pathway activation in. 168504.
   Google Scholar
• Peyraud, F., & Italiano, A. (2020). Combined parp inhibition and immune checkpoint therapy in solid tumors. Cancers, 12(6), 1502. https://doi.org/10.3390/cancers12061502
   PubMed Web of Science ®Google Scholar
• Piskunova, T. S., Yurova, M. N., Ovsyannikov, A. I., Semenchenko, A. V., Zabezhinski, M. A., Popovich, I. G., Wang, Z.-Q., & Anisimov, V. N. (2008). Deficiency in Poly(ADP-ribose) polymerase-1 (PARP-1) accelerates aging and spontaneous carcinogenesis in mice. Current Gerontology and Geriatrics Research, 2008, 1–11. https://doi.org/10.1155/2008/754190
   Google Scholar
• Ramasamy, T., Priyankha, S., Kannan, M., Prakash, M., & Selvam, C. (2022). Compounds from diverse natural origin against triple‐negative breast cancer: a comprehensive review. Chemical Biology & Drug Design, 101(1), 1–26.
   Web of Science ®Google Scholar
• Shen, Y., Aoyagi-Scharber, M., & Wang, B. (2015). Minireview trapping poly (ADP-Ribose) polymerase. Journal of Pharmacology and Experimental Therapeutics, 353(3), 446–457. June, https://doi.org/10.1124/jpet.114.222448
   PubMed Web of Science ®Google Scholar
• Shirts, M. R., Klein, C., Swails, J. M., Yin, J., Gilson, M. K., Mobley, D. L., Case, D. A., & Zhong, E. D. (2017). Lessons learned from comparing molecular dynamics engines on the SAMPL5 dataset. Journal of Computer-Aided Molecular Design, 31(1), 147–161. https://doi.org/10.1007/s10822-016-9977-1
   PubMed Web of Science ®Google Scholar
• Shridhar Deshpande, N., Mahendra, G. S., Aggarwal, N. N., Gatphoh, B. F. D., & Revanasiddappa, B. C. (2021). Insilico design, ADMET screening, MM-GBSA binding free energy of novel 1,3,4 oxadiazoles linked Schiff bases as PARP-1 inhibitors targeting breast cancer. Future Journal of Pharmaceutical Sciences, 7(1), 174. https://doi.org/10.1186/s43094-021-00321-4
   Web of Science ®Google Scholar
• Siegel, R. L., Miller, K. D., & Jemal, A. (2020). Cancer statistics, 2020. CA: A Cancer Journal for Clinicians, 70(1), 7–30. https://doi.org/10.3322/caac.21590
   PubMed Web of Science ®Google Scholar
• Smith, S. (2001). The world according to PARP. Trends in Biochemical Sciences, 26(3), 174–179. https://doi.org/10.1016/s0968-0004(00)01780-1
   PubMed Web of Science ®Google Scholar
• Teles, R. H. G., Moralles, H. F., & Cominetti, M. R. (2018). Global trends in nanomedicine research on triple negative breast cancer: A bibliometric analysis. International Journal of Nanomedicine, 13, 2321–2336. https://doi.org/10.2147/IJN.S164355
   PubMed Web of Science ®Google Scholar
• Van Gunsteren, W. F., & Berendsen, H. J. C. (1988). A leap-frog algorithm for stochastic dynamics. Molecular Simulation, 1(3), 173–185. https://doi.org/10.1080/08927028808080941
   Web of Science ®Google Scholar
• Vikas, P., Borcherding, N., Chennamadhavuni, A., & Garje, R. (2020). Therapeutic potential of combining PARP inhibitor and immunotherapy in solid tumors. Frontiers in Oncology, 10(April), 1–10. https://doi.org/10.3389/fonc.2020.00570
   PubMedGoogle Scholar
• Wang, Q., He, J., Wu, D., Wang, J., Yan, J., & Li, H. (2015). Interaction of α-cyperone with human serum albumin: Determination of the binding site by using Discovery Studio and via spectroscopic methods. Journal of Luminescence, 164, 81–85. https://doi.org/10.1016/j.jlumin.2015.03.025
   Web of Science ®Google Scholar
• Wang, Y., Peng, C., Wang, G., Xu, Z., Luo, Y., Wang, J., & Zhu, W. (2019). Exploring binding mechanisms of VEGFR2 with three drugs lenvatinib, sorafenib, and sunitinib by molecular dynamics simulation and free energy calculation. Chemical Biology & Drug Design, 93(5), 934–948. https://doi.org/10.1111/cbdd.13493
   PubMed Web of Science ®Google Scholar
• Webb, M. J., & Kukard, C. (2020). A review of natural therapies potentially relevant in triple negative breast cancer aimed at targeting cancer cell vulnerabilities. Integrative Cancer Therapies, 19, 153473542097586. https://doi.org/10.1177/1534735420975861
   Web of Science ®Google Scholar
• Wu, S., Gao, F., Zheng, S., Zhang, C., Martinez-Ledesma, E., Ezhilarasan, R., Ding, J., Li, X., Feng, N., Multani, A., Sulman, E. P., Verhaak, R. G., de Groot, J. F., Heffernan, T. P., Alfred Yung, W. K., & Koul, D. (2020). EGFR amplification induces increased DNA damage response and renders selective sensitivity to talazoparib (PARP inhibitor) in glioblastoma. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 26(6), 1395–1407. https://doi.org/10.1158/1078-0432.CCR-19-2549
   PubMed Web of Science ®Google Scholar
• Xiang, K., Li, C., Li, M. X., Song, Z. R., Ma, X. X., Sun, D. J., Li, H., & Chen, L. X. (2021). Withanolides isolated from Tubocapsicum anomalum and their antiproliferative activity. Bioorganic Chemistry, 110(February), 104809. https://doi.org/10.1016/j.bioorg.2021.104809
   PubMedGoogle Scholar
• Yu, S. W., Andrabi, S. A., Wang, H., No, S. K., Poirier, G. G., Dawson, T. M., & Dawson, V. L. (2006). Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proceedings of the National Academy of Sciences of the United States of America, 103(48), 18314–18319. https://doi.org/10.1073/pnas.0606528103
   PubMed Web of Science ®Google Scholar
• Yu, Y., Durairaj, C., Shi, H., & Wang, D. D. (2020). Population pharmacokinetics of talazoparib in patients with advanced cancer. Journal of Clinical Pharmacology, 60(2), 218–228. https://doi.org/10.1002/jcph.1520
   PubMed Web of Science ®Google Scholar
• Zhang, S., Gong, C., Ruiz-Martinez, A., Wang, H., Davis-Marcisak, E., Deshpande, A., Popel, A. S., & Fertig, E. J. (2021). Integrating single cell sequencing with a spatial quantitative systems pharmacology model spQSP for personalized prediction of triple-negative breast cancer immunotherapy response. ImmunoInformatics, 1–2, 100002. https://doi.org/10.1016/j.immuno.2021.100002
   PubMedGoogle Scholar