Identification of approved drugs with ALDH1A1 inhibitory potential aimed at enhancing chemotherapy sensitivity in cancer cells: an in-silico drug repurposing approach

References

• Abraham, H. M. A., White, C. M., & White, W. B. (2015). The Comparative Efficacy and Safety of the Angiotensin Receptor Blockers in the Management of Hypertension and Other Cardiovascular Diseases. Drug Safety, 38(1), 33–54. https://doi.org/10.1007/s40264-014-0239-7
   PubMed Web of Science ®Google Scholar
• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, 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
• Altis, A., Otten, M., Nguyen, P. H., Hegger, R., & Stock, G. (2008). Construction of the free energy landscape of biomolecules via dihedral angle principal component analysis. The Journal of Chemical Physics, 128(24), 245102. https://doi.org/10.1063/1.2945165
   PubMed Web of Science ®Google Scholar
• Arai, M. (2018). Unified understanding of folding and binding mechanisms of globular and intrinsically disordered proteins. Biophysical Reviews, 10(2), 163–181. https://doi.org/10.1007/s12551-017-0346-7
   Google Scholar
• Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., & Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28(1), 235–242. https://doi.org/10.1093/nar/28.1.235
   PubMed Web of Science ®Google Scholar
• Buchman, C. D., & Hurley, T. D. (2017). Inhibition of the aldehyde dehydrogenase 1/2 family by psoralen and coumarin derivatives. Journal of Medicinal Chemistry, 60(6), 2439–2455. https://doi.org/10.1021/acs.jmedchem.6b01825
   Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126(1), 014101. https://doi.org/10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Dallakyan, S., & Olson, A. J. (2015). Small-molecule library screening by docking with PyRx. Methods in Molecular Biology, 1263, 243–250. https://doi.org/10.1007/978-1-4939-2269-7_19
   PubMedGoogle Scholar
• Darden, T., York, D., & Pedersen, L. (1998). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Google Scholar
• Das, B. C., Thapa, P., Karki, R., Das, S., Mahapatra, S., Liu, T. C., Torregroza, I., Wallace, D. P., Kambhampati, S., Van Veldhuizen, P., Verma, A., Ray, S. K., & Evans, T. (2014). Retinoic acid signaling pathways in development and diseases. Bioorganic & Medicinal Chemistry, 22(2), 673–683. https://doi.org/10.1016/j.bmc.2013.11.025
   Web of Science ®Google Scholar
• Farmer, R., Thomas, C. M., & Winn, P. J. (2019). Structure, function and dynamics in acyl carrier proteins. PLOS One, 14(7), e0219435. https://doi.org/10.1371/journal.pone.0219435
   Web of Science ®Google Scholar
• Farrés, J., Wang, X., Takahashi, K., Cunningham, S. J., Wang, T. T., & Weiner, H. (1994). Effects of changing glutamate 487 to lysine in rat and human liver mitochondrial aldehyde dehydrogenase. A model to study human (Oriental type) class 2 aldehyde dehydrogenase. Journal of Biological Chemistry, 269(19), 13854–13860. https://doi.org/10.1016/S0021-9258(17)36725-x
   Web of Science ®Google Scholar
• Gelardi, E. L. M., Colombo, G., Picarazzi, F., Ferraris, D. M., Mangione, A., Petrarolo, G., Aronica, E., Rizzi, M., Mori, M., La Motta, C., & Garavaglia, S. (2021). A selective competitive inhibitor of aldehyde dehydrogenase 1A3 hinders cancer cell growth, invasiveness and stemness in vitro. Cancers, 13(2), 356. https://doi.org/10.3390/cancers13020356
   Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Gudas, L. J. (2022). Retinoid metabolism: New insights. Journal of Molecular Endocrinology, 69(4), T37–T49. https://doi.org/10.1530/JME-22-0082
   Web of Science ®Google Scholar
• Huang, J., & Mackerell, A. D. (2013). CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data. Journal of Computational Chemistry, 34(25), 2135–2145. https://doi.org/10.1002/jcc.23354
   PubMed Web of Science ®Google Scholar
• Huddle, B. C., Grimley, E., Chtcherbinine, M., Buchman, C. D., Takahashi, C., Debnath, B., McGonigal, S. C., Mao, S., Li, S., Felton, J., Pan, S., Wen, B., Sun, D., Neamati, N., Buckanovich, R. J., Hurley, T. D., & Larsen, S. D. (2021). Development of 2,5-dihydro-4H-pyrazolo[3,4-d]pyrimidin-4-one inhibitors of Aldehyde Dehydrogenase 1A (ALDH1A) as potential adjuncts to ovarian cancer chemotherapy. European Journal of Medicinal Chemistry, 211, 113060. https://doi.org/10.1016/j.ejmech.2020.113060
   Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Jakher, H., Chang, T. I., Tan, M., & Mahaffey, K. W. (2019). Canagliflozin review – safety and efficacy profile in patients with T2DM. Diabetes, Metabolic Syndrome and Obesity, 12, 209–215. https://doi.org/10.2147/dmso.s184437
   PubMed Web of Science ®Google Scholar
• Jolliffe, I. T., & Cadima, J. (2016). Principal component analysis: A review and recent developments. Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences, 374(2065), 20150202. https://doi.org/10.1098/rsta.2015.0202
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Khoury, T., Ademuyiwa, F. O., Chandrasekhar, R., Jabbour, M., Deleo, A., Ferrone, S., Wang, Y., & Wang, X. (2011). Aldehyde dehydrogenase 1A1 expression in breast cancer is associated with stage, triple negativity, and outcome to neoadjuvant chemotherapy. Modern Pathology 25(3), 388–397. https://doi.org/10.1038/modpathol.2011.172
   Web of Science ®Google Scholar
• Kim, H., Fábián, B., & Hummer, G. (2023). Neighbor list artifacts in molecular dynamics simulations. Journal of Chemical Theory and Computation 19, 23. https://doi.org/10.26434/chemrxiv-2023-zbj6j
   Web of Science ®Google Scholar
• Kim, S., Chen, J., Cheng, T., Gindulyte, A., He, J., He, S., Li, Q., Shoemaker, B. A., Thiessen, P. A., Yu, B., Zaslavsky, L., Zhang, J., & Bolton, E. E. (2021). PubChem in 2021: New data content and improved web interfaces. Nucleic Acids Research, 49(D1), D1388–D1395. https://doi.org/10.1093/nar/gkaa971
   PubMed Web of Science ®Google Scholar
• Koch, M. F., Harteis, S., Blank, I. D., Pestel, G., Tietze, L. F., Ochsenfeld, C., Schneider, S., & Sieber, S. A. (2015). Structural, Biochemical, and Computational Studies Reveal the Mechanism of Selective Aldehyde Dehydrogenase 1A1 Inhibition by Cytotoxic Duocarmycin Analogues. Angewandte Chemie, 54(46), 13550–13554. https://doi.org/10.1002/anie.201505749
   Google Scholar
• Koppaka, V., Thompson, D. C., Chen, Y., Ellermann, M., Nicolaou, K. C., Juvonen, R. O., Petersen, D., Deitrich, R. A., Hurley, T. D., & Vasiliou, V. (2012). Aldehyde dehydrogenase inhibitors: A comprehensive review of the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacological Reviews, 64(3), 520–539. https://doi.org/10.1124/pr.111.005538
   PubMed Web of Science ®Google Scholar
• Lever, J., Krzywinski, M., & Altman, N. (2017). Points of Significance: Principal component analysis. Nature Methods, 14(7), 641–642. https://doi.org/10.1038/nmeth.4346
   Web of Science ®Google Scholar
• Li, B., Yang, K., Liang, D., Jiang, C., & Ma, Z. (2021). Discovery and development of selective aldehyde dehydrogenase 1A1 (ALDH1A1) inhibitors. European Journal of Medicinal Chemistry, 209, 112940. https://doi.org/10.1016/j.ejmech.2020.112940
   Web of Science ®Google Scholar
• Li, T., Su, Y., Mei, Y., Leng, Q., Leng, B., Liu, Z., Stass, S. A., & Jiang, F. (2010). ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients’ outcome. Laboratory Investigation; a Journal of Technical Methods and Pathology, 90(2), 234–244. https://doi.org/10.1038/labinvset.2009.127
   PubMed Web of Science ®Google Scholar
• Maisuradze, G. G., Liwo, A., & Scheraga, H. A. (2009). Principal component analysis for protein folding dynamics. Journal of Molecular Biology, 385(1), 312–329. https://doi.org/10.1016/j.jmb.2008.10.018
   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
• Massova, I., & Kollman, P. A. (2000). Combined molecular mechanical and continuum solvent approach (MM- PBSA/GBSA) to predict ligand binding. Perspectives in Drug Discovery and Design, 18(1), 113–135. https://doi.org/10.1023/a:1008763014207/metrics
   Google Scholar
• Miller, B. R., McGee, T. D., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA.py: An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8(9), 3314–3321. https://doi.org/10.1021/ct300418h
   PubMed Web of Science ®Google Scholar
• Morgan, C. A., & Hurley, T. D. (2015). Characterization of two distinct structural classes of selective aldehyde dehydrogenase 1A1 inhibitors. Journal of Medicinal Chemistry, 58(4), 1964–1975. https://doi.org/10.1021/jm501900s
   PubMed Web of Science ®Google Scholar
• Morgan, C. A., & Hurley, T. D. (2015). Development of a high-throughput in vitro assay to identify selective inhibitors for human ALDH1A1. Chemico-Biological Interactions, 234, 29–37. https://doi.org/10.1016/j.cbi.2014.10.028
   PubMed Web of Science ®Google Scholar
• Niederreither, K., Fraulob, V., Garnier, J. M., Chambon, P., & Dollé, P. (2002). Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mechanisms of Development, 110(1–2), 165–171. https://doi.org/10.1016/s0925-4773(01)00561-5
   Web of Science ®Google Scholar
• O’Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open Babel: An open chemical toolbox. Journal of Cheminformatics, 3(10), 33. https://doi.org/10.1186/1758-2946-3-33
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
   Web of Science ®Google Scholar
• Paul, S. K., Dutta Chowdhury, K., Dey, S. R., Paul, A., & Haldar, R. (2022). Exploring the possibility of drug repurposing for cancer therapy targeting human lactate dehydrogenase A: A computational approach. Journal of Biomolecular Structure & Dynamics, 41(19), 9967–9976. https://doi.org/10.1080/07391102.2022.2158134
   Web of Science ®Google Scholar
• Pequerul, R., Vera, J., Giménez-Dejoz, J., Crespo, I., Coines, J., Porté, S., Rovira, C., Parés, X., & Farrés, J. (2020). Structural and kinetic features of aldehyde dehydrogenase 1A (ALDH1A) subfamily members, cancer stem cell markers active in retinoic acid biosynthesis. Archives of Biochemistry and Biophysics, 681, 108256. https://doi.org/10.1016/j.abb.2020.108256
   PubMed Web of Science ®Google Scholar
• Plattner, N., & Noé, F. (2015). Protein conformational plasticity and complex ligand-binding kinetics explored by atomistic simulations and Markov models. Nature Communications, 2015 6:16(1), 7653. https://doi.org/10.1038/ncomms8653
   PubMedGoogle Scholar
• Poturnajova, M., Kozovska, Z., & Matuskova, M. (2021). Aldehyde dehydrogenase 1A1 and 1A3 isoforms – mechanism of activation and regulation in cancer. Cellular Signalling, 87, 110120. https://doi.org/10.1016/j.cellsig.2021.110120
   PubMed Web of Science ®Google Scholar
• Ray, N. (2008). Maraviroc in the treatment of HIV infection. Drug Design, Development and Therapy, 2(2), 151–161. https://doi.org/10.2147/dddt.s3474
   Google Scholar
• Rodriguez-Torres, M., & Allan, A. L. (2015). Aldehyde dehydrogenase as a marker and functional mediator of metastasis in solid tumors. Clinical & Experimental Metastasis, 33(1), 97–113. https://doi.org/10.1007/s10585-015-9755-9
   Web of Science ®Google Scholar
• Sanner, M. (1999). Python: A programming language for software integration and development. Journal of Molecular Graphics & Modelling, 17(1):57–61.
   PubMed Web of Science ®Google Scholar
• Shimizu, R., Sonoyama, T., Fukuhara, T., Kuwata, A., Matsuo, Y., & Kubota, R. (2022). Safety, tolerability, and pharmacokinetics of the novel antiviral agent ensitrelvir fumaric acid, a SARS-CoV-2 3CL protease inhibitor, in healthy adults. Antimicrobial Agents and Chemotherapy, 66(10) https://doi.org/10.1128/aac.00632-22
   Web of Science ®Google Scholar
• Shortall, K., Djeghader, A., Magner, E., & Soulimane, T. (2021). Insights into aldehyde dehydrogenase enzymes: A structural perspective. Frontiers in Molecular Biosciences, 8, 659550. https://doi.org/10.3389/fmolb.2021.659550
   PubMed Web of Science ®Google Scholar
• Tavernelli, I., Cotesta, S., & Di Iorio, E. E. (2003). Protein dynamics, thermal stability, and free-energy landscapes: A molecular dynamics investigation. Biophysical Journal, 85(4), 2641–2649. https://doi.org/10.1016/s0006-3495(03)74687-6
   Web of Science ®Google Scholar
• Thomsen, R., & Christensen, M. H. (2006). MolDock: A new technique for high-accuracy molecular docking. Journal of Medicinal Chemistry, 49(11), 3315–3321. https://doi.org/10.1021/jm051197E/suppl_file/jm051197esi20060314_081922.PDF
   PubMed Web of Science ®Google Scholar
• Tomita, H., Tanaka, K., Tanaka, T., Hara, A., Tomita, H., Tanaka, K., Tanaka, T., & Hara, A. (2016). Aldehyde dehydrogenase 1A1 in stem cells and cancer. Oncotarget, 7(10), 11018–11032. https://doi.org/10.18632/oncotarget.6920
   PubMedGoogle Scholar
• Trott, O., & Olson, A. J. (2009). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
   Web of Science ®Google Scholar
• Valdés-Tresanco, M. S., Valdés-Tresanco, M. E., Valiente, P. A., & Moreno, E. (2021). Gmx_MMPBSA: A new tool to perform end-state free energy calculations with GROMACS. Journal of Chemical Theory and Computation, 17(10), 6281–6291. https://doi.org/10.1021/acs.jctc.1c00645
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Vanommeslaeghe, K., & MacKerell, A. D. (2012). Automation of the CHARMM general force field (CGenFF) I: Bond perception and atom typing. Journal of Chemical Information and Modeling, 52(12), 3144–3154. https://doi.org/10.1021/ci300363c
   PubMed Web of Science ®Google Scholar
• Verma, H., Singh Bahia, M., Choudhary, S., Kumar Singh, P., & Silakari, O. (2019). Drug metabolizing enzymes-associated chemo resistance and strategies to overcome it. Drug Metabolism Reviews, 51(2), 196–223. https://doi.org/10.1080/03602532.2019.1632886
   PubMed Web of Science ®Google Scholar
• Wang, C., Greene, D., Xiao, L., Qi, R., & Luo, R. (2017). Recent developments and applications of the MMPBSA method. Frontiers in Molecular Biosciences, 4, 87. https://doi.org/10.3389/fmolb.2017.00087
   PubMed Web of Science ®Google Scholar
• Wankowicz, S. A., de Oliveira, S. H. P., Hogan, D. W., van den Bedem, H., & Fraser, J. S. (2022). Ligand binding remodels protein side chain conformational heterogeneity. eLife, 11, e74114. https://doi.org/10.7554/elife.74114
   Web of Science ®Google Scholar
• Wei, Y., Li, Y., Chen, Y., Liu, P., Huang, S., Zhang, Y., Sun, Y., Wu, Z., Hu, M., Wu, Q., Wu, H., Liu, F., She, T., & Ning, Z. (2022). ALDH1: A potential therapeutic target for cancer stem cells in solid tumors. Frontiers in Oncology, 12, 1026278. https://doi.org/10.3389/fonc.2022.1026278
   Google Scholar
• Weikl, T. R., & Paul, F. (2014). Conformational selection in protein binding and function. Protein Science, 23(11), 1508–1518. https://doi.org/10.1002/pro.2539
   PubMed Web of Science ®Google Scholar
• Wishart, D. S., Feunang, Y. D., Guo, A. C., Lo, E. J., Marcu, A., Grant, J. R., Sajed, T., Johnson, D., Li, C., Sayeeda, Z., Assempour, N., Iynkkaran, I., Liu, Y., Maciejewski, A., Gale, N., Wilson, A., Chin, L., Cummings, R., Le, D., … Wilson, M. (2018). DrugBank 5.0: A major update to the DrugBank database for 2018. Nucleic Acids Research, 46(D1), D1074–D1082. https://doi.org/10.1093/nar/gkx1037
   PubMed Web of Science ®Google Scholar
• Xia, J., Li, S., Liu, S., & Zhang, L. (2023). Aldehyde dehydrogenase in solid tumors and other diseases: Potential biomarkers and therapeutic targets. MedComm, 4(1), e195. https://doi.org/10.1002/mco2.195
   Google Scholar
• Yang, L. Q., Ji, X. L., & Liu, S. Q. (2013). The free energy landscape of protein folding and dynamics: A global view. Journal of Biomolecular Structure & Dynamics, 31(9), 982–992. https://doi.org/10.1080/07391102.2012.748536
   PubMed Web of Science ®Google Scholar
• Yang, W., Wang, Y., Wang, W., Chen, Z., & Bai, G. (2018). Expression of aldehyde dehydrogenase 1A1 (ALDH1A1) as a prognostic biomarker in colorectal cancer using immunohistochemistry. Medical Science Monitor, 24, 2864–2872. https://doi.org/10.12659/msm.910109
   Web of Science ®Google Scholar
• Yue, H., Hu, Z., Hu, R., Guo, Z., Zheng, Y., Wang, Y., & Zhou, Y. (2022). ALDH1A1 in cancers: Bidirectional function, drug resistance, and regulatory mechanism. Frontiers in Oncology, 12, 918778. https://doi.org/10.3389/fonc.2022.918778
   Web of Science ®Google Scholar
• Zhang, Z., Zhou, L., Xie, N., Nice, E. C., Zhang, T., Cui, Y., & Huang, C. (2020). Overcoming cancer therapeutic bottleneck by drug repurposing. Signal Transduction and Targeted Therapy 5(1), 113. https://doi.org/10.1038/s41392-020-00213-8
   PubMed Web of Science ®Google Scholar
• Zhao, H., & Caflisch, A. (2013). Discovery of ZAP70 inhibitors by high-throughput docking into a conformation of its kinase domain generated by molecular dynamics. Bioorganic & Medicinal Chemistry Letters, 23(20), 5721–5726. https://doi.org/10.1016/j.bmcl.2013.08.009
   PubMed Web of Science ®Google Scholar
• Zoete, V., Cuendet, M. A., Grosdidier, A., & Michielin, O. (2011). SwissParam: A fast force field generation tool for small organic molecules. Journal of Computational Chemistry, 32(11), 2359–2368. https://doi.org/10.1002/JCC.21816
   PubMed Web of Science ®Google Scholar