310
Views
2
CrossRef citations to date
0
Altmetric
Research Article

Structural insights into the mechanism of resistance to bicalutamide by the clinical mutations in androgen receptor in chemo-treatment resistant prostate cancer

, , , , , , , , , & show all
Pages 1181-1190 | Received 17 Oct 2022, Accepted 28 Mar 2023, Published online: 05 May 2023

References

  • Balbas, M. D., Evans, M. J., Hosfield, D. J., Wongvipat, J., Arora, V. K., Watson, P. A., Chen, Y., Greene, G. L., Shen, Y., & Sawyers, C. L. (2013). Overcoming mutation-based resistance to antiandrogens with rational drug design. elife, 2, e00499. https://doi.org/10.7554/eLife.00499
  • Best, R. B. (2022). Analysis of molecular dynamics simulations of protein folding. In Victor Muñoz (Ed.), Protein folding (pp. 317–329). Springer.
  • Brzozowski, A. M., Pike, A. C., Dauter, Z., Hubbard, R. E., Bonn, T., Engström, O., Öhman, L., Greene, G. L., Gustafsson, J.-Å., & Carlquist, M. (1997). Molecular basis of agonism and antagonism in the oestrogen receptor. Nature, 389(6652), 753–758. https://doi.org/10.1038/39645
  • Burks, D. A., & Littleton, R. H. (1992). The epidemiology of prostate cancer in black men. Henry Ford Hospital Medical Journal, 40(1-2), 89–92.
  • Crawford, E., & DeAntoni, E. (1995). Current status of combined androgen blockade: Optimal therapy for advanced prostate cancer. The Journal of Clinical Endocrinology and Metabolism, 80(4), 1062–1066. https://doi.org/10.1210/jcem.80.4.7714067
  • Cuccurullo, V., Di Stasio, G. D., Evangelista, L., Castoria, G., & Mansi, L. (2017). Biochemical and pathophysiological premises to positron emission tomography with choline radiotracers. Journal of Cellular Physiology, 232(2), 270–275. https://doi.org/10.1002/jcp.25478
  • Culig, Z. (2014). Targeting the androgen receptor in prostate cancer. Expert Opinion on Pharmacotherapy, 15(10), 1427–1437. https://doi.org/10.1517/14656566.2014.915313
  • Daggett, V., & Levitt, M. (1993). Realistic simulations of native-protein dynamics in solution and beyond. Annual Review of Biophysics and Biomolecular Structure, 22, 353–380. https://doi.org/10.1146/annurev.bb.22.060193.002033
  • Davey, R. A., & Grossmann, M. (2016). Androgen receptor structure, function and biology: from bench to bedside. The clinical biochemist reviews, 37(1), 3.
  • Darden, T., York, D., & Pedersen, L. (1993). 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
  • Dehm, S. M., & Tindall, D. J. (2005). Regulation of androgen receptor signaling in prostate cancer. Expert Review of Anticancer Therapy, 5(1), 63–74. https://doi.org/10.1586/14737140.5.1.63
  • Durrani, F. G., Gul, R., Mirza, M. U., Kaderbhai, N. N., Froeyen, M., & Saleem, M. (2019). Mutagenesis of DsbAss is crucial for the signal recognition particle mechanism in Escherichia coli: Insights from molecular dynamics simulations. Biomolecules, 9(4), 133. https://doi.org/10.3390/biom9040133
  • 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
  • Fujita, K., & Nonomura, N. (2019). Role of androgen receptor in prostate cancer: A review. The World Journal of Men’s Health, 37(3), 288–295. https://doi.org/10.5534/wjmh.180040
  • 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
  • Gotz, A. W., Williamson, M. J., Xu, D., Poole, D., Le Grand, S., & Walker, R. C. (2012). Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born. Journal of Chemical Theory and Computation, 8(5), 1542–1555. https://doi.org/10.1021/ct200909j
  • Guterres, H., & Im, W. (2020). Improving protein–ligand docking results with high-throughput molecular dynamics simulations. Journal of Chemical Information and Modeling, 60(4), 2189–2198. https://doi.org/10.1021/acs.jcim.0c00057
  • Hara, T., Miyazaki, J-i., Araki, H., Yamaoka, M., Kanzaki, N., Kusaka, M., & Miyamoto, M. (2003). Novel mutations of androgen receptor: A possible mechanism of bicalutamide withdrawal syndrome. Cancer Research, 63(1), 149–153.
  • Hollingsworth, S. A., & Dror, R. O. (2018). Molecular dynamics simulation for all. Neuron, 99(6), 1129–1143. https://doi.org/10.1016/j.neuron.2018.08.011
  • Inoue, T., Kobayashi, T., Terada, N., Shimizu, Y., Kamoto, T., Ogawa, O., & Nakamura, E. (2007). Roles of androgen-dependent and-independent activation of signal transduction pathways for cell proliferation of prostate cancer cells. Expert Review of Endocrinology & Metabolism, 2(5), 689–704. https://doi.org/10.1586/17446651.2.5.689
  • Jin, Y., Duan, M., Wang, X., Kong, X., Zhou, W., Sun, H., Liu, H., Li, D., Yu, H., Li, Y., & Hou, T. (2019). Communication between the ligand-binding pocket and the activation function-2 domain of androgen receptor revealed by molecular dynamics simulations. Journal of Chemical Information and Modeling, 59(2), 842–857. https://doi.org/10.1021/acs.jcim.8b00796
  • Jordan, V. C., Curpan, R., & Maximov, P. Y. (2015). Estrogen receptor mutations found in breast cancer metastases integrated with the molecular pharmacology of selective ER modulators. Journal of the National Cancer Institute, 107(6), djv075. https://doi.org/10.1093/jnci/djv075
  • Joseph, J. D., Darimont, B., Zhou, W., Arrazate, A., Young, A., Ingalla, E., Walter, K., Blake, R. A., Nonomiya, J., Guan, Z., Kategaya, L., Govek, S. P., Lai, A. G., Kahraman, M., Brigham, D., Sensintaffar, J., Lu, N., Shao, G., Qian, J., … Hager, J. H. (2016). The selective estrogen receptor downregulator GDC-0810 is efficacious in diverse models of ER + breast cancer. eLife, 5, e15828. https://doi.org/10.7554/eLife.15828
  • Junaid, M., Khan, M. T., Malik, S. I., & Wei, D.-Q. (2019). Insights into the mechanisms of the pyrazinamide resistance of three pyrazinamidase mutants N11K, P69T, and D126N. Journal of Chemical Information and Modeling, 59(1), 498–508. https://doi.org/10.1021/acs.jcim.8b00525
  • Khan, A., Gui, J., Ahmad, W., Haq, I., Shahid, M., Khan, A. A., Shah, A., Khan, A., Ali, L., Anwar, Z., Safdar, M., Abubaker, J., Uddin, N. N., Cao, L., Wei, D.-Q., & Mohammad, A. (2021). The SARS-CoV-2 B. 1.618 variant slightly alters the spike RBD–ACE2 binding affinity and is an antibody escaping variant: A computational structural perspective. RSC Advances, 11(48), 30132–30147. https://doi.org/10.1039/d1ra04694b
  • Khan, A., Junaid, M., Li, C.-D., Saleem, S., Humayun, F., Shamas, S., Ali, S. S., Babar, Z., Wei., & D.-Q., Ashfaq-Ur-Rehman. (2020). Dynamics insights into the gain of flexibility by Helix-12 in ESR1 as a mechanism of resistance to drugs in breast cancer cell lines. Frontiers in Molecular Biosciences, 6, 159. https://doi.org/10.3389/fmolb.2019.00159
  • Khan, A., Waris, H., Rafique, M., Suleman, M., Mohammad, A., Ali, S. S., Khan, T., Waheed, Y., Liao, C., & Wei, D.-Q. (2022). The Omicron (B. 1.1. 529) variant of SARS-CoV-2 binds to the hACE2 receptor more strongly and escapes the antibody response: Insights from structural and simulation data. International Journal of Biological Macromolecules, 200, 438–448. https://doi.org/10.1016/j.ijbiomac.2022.01.059
  • Khan, A., Zia, T., Suleman, M., Khan, T., Ali, S. S., Abbasi, A. A., Mohammad, A., & Wei, D. Q. (2021). Higher infectivity of the SARS-CoV-2 new variants is associated with K417N/T, E484K, and N501Y mutants: An insight from structural data. Journal of Cellular Physiology, 236(10), 7045–7057. https://doi.org/10.1002/jcp.30367
  • Koes, D. R., Baumgartner, M. P., & Camacho, C. J. (2013). Lessons learned in empirical scoring with smina from the CSAR 2011 benchmarking exercise. Journal of Chemical Information and Modeling, 53(8), 1893–1904. https://doi.org/10.1021/ci300604z
  • Liao, R. S., Ma, S., Miao, L., Li, R., Yin, Y., & Raj, G. V. (2013). Androgen receptor-mediated non-genomic regulation of prostate cancer cell proliferation. Translational Andrology and Urology, 2, 187.
  • Liu, H., An, X., Li, S., Wang, Y., Li, J., & Liu, H. (2015). Interaction mechanism exploration of R-bicalutamide/S-1 with WT/W741L AR using molecular dynamics simulations. Molecular bioSystems, 11(12), 3347–3354. https://doi.org/10.1039/c5mb00499c
  • Liu, H., Han, R., Li, J., Liu, H., & Zheng, L. (2016). Molecular mechanism of R-bicalutamide switching from androgen receptor antagonist to agonist induced by amino acid mutations using molecular dynamics simulations and free energy calculation. Journal of Computer-Aided Molecular Design, 30(12), 1189–1200. https://doi.org/10.1007/s10822-016-9992-2
  • Marcelli, M., Ittmann, M., Mariani, S., Sutherland, R., Nigam, R., Murthy, L., Zhao, Y., DiConcini, D., Puxeddu, E., Esen, A., Eastham, J., Weigel, N. L., & Lamb, D. J. (2000). Androgen receptor mutations in prostate cancer. Cancer Research, 60(4), 944–949.
  • Masters, L., Eagon, S., & Heying, M. (2020). Evaluation of consensus scoring methods for AutoDock Vina, smina and idock. Journal of Molecular Graphics & Modelling, 96, 107532. https://doi.org/10.1016/j.jmgm.2020.107532
  • Miyamoto, H., Messing, E. M., & Chang, C. (2004). Androgen deprivation therapy for prostate cancer: Current status and future prospects. The Prostate, 61(4), 332–353. https://doi.org/10.1002/pros.20115
  • Mukherjee, A., Kirkovsky, L., Yao, X., Yates, R., Miller, D., & Dalton, J. (1996). Enantioselective binding of Casodex to the androgen receptor. Xenobiotica; the Fate of Foreign Compounds in Biological Systems, 26(2), 117–122. https://doi.org/10.3109/00498259609046693
  • Nadal, M., Prekovic, S., Gallastegui, N., Helsen, C., Abella, M., Zielinska, K., Gay, M., Vilaseca, M., Taulès, M., Houtsmuller, A. B., van Royen, M. E., Claessens, F., Fuentes-Prior, P., & Estébanez-Perpiñá, E. (2017). Structure of the homodimeric androgen receptor ligand-binding domain. Nature Communications, 8, 14388. https://doi.org/10.1038/ncomms14388
  • Nisar, H., Pasha, U., Mirza, M. U., Abid, R., Hanif, K., Kadarmideen, H. N., & Sadaf, S. (2021). Impact of IL-17F 7488T/C functional polymorphism on progressive rheumatoid arthritis: Novel insight from the molecular dynamic simulations. Immunological Investigations, 50(4), 416–426. https://doi.org/10.1080/08820139.2020.1775642
  • Pal, A., Curtin, J. F., & Kinsella, G. K. (2021). In silico and in vitro screening for potential anticancer candidates targeting GPR120. Bioorganic & Medicinal Chemistry Letters, 31, 127672. https://doi.org/10.1016/j.bmcl.2020.127672
  • Papaleo, E. (2015). Integrating atomistic molecular dynamics simulations, experiments, and network analysis to study protein dynamics: Strength in unity. Frontiers in Molecular Biosciences, 2, 28. https://doi.org/10.3389/fmolb.2015.00028
  • Parveen, A., Khan, S. A., Mirza, M. U., Bashir, H., Arshad, F., Iqbal, M., Ahmad, W., Wahab, A., Fiaz, A., Naz, S., Ashraf, F., Mobeen, T., Aziz, S., Ahmed, S. S., Muhammad, N., Hassib, N. F., Mostafa, M. I., Gaboon, N. E., Gul, R., … Wasif, N. (2019). Deleterious variants in WNT10A, EDAR, and EDA causing isolated and syndromic tooth agenesis: A structural perspective from molecular dynamics simulations. International Journal of Molecular Sciences, 20(21), 5282. https://doi.org/10.3390/ijms20215282
  • Parveen, A., Mirza, M. U., Vanmeert, M., Akhtar, J., Bashir, H., Khan, S., Shehzad, S., Froeyen, M., Ahmed, W., Ansar, M., & Wasif, N. (2019). A novel pathogenic missense variant in CNNM4 underlying Jalili syndrome: Insights from molecular dynamics simulations. Molecular Genetics & Genomic Medicine, 7(9), e902. https://doi.org/10.1002/mgg3.902
  • Petrylak, D. P. (1999). Chemotherapy for advanced hormone refractory prostate cancer. Urology, 54(6A Suppl), 30–35. https://doi.org/10.1016/s0090-4295(99)00452-5
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera—a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
  • Pires, D. E., Ascher, D. B., & Blundell, T. L. (2014). mCSM: Predicting the effects of mutations in proteins using graph-based signatures. Bioinformatics (Oxford, England), 30(3), 335–342. https://doi.org/10.1093/bioinformatics/btt691
  • Prostate Cancer Trialists Collaborative Group. (2000). Maximum androgen blockade in advanced prostate cancer: An overview of the randomised trials. The Lancet, 355, 1491–1498.
  • Rodrigues, C. H., Pires, D. E., & Ascher, D. B. (2018). DynaMut: Predicting the impact of mutations on protein conformation, flexibility and stability. Nucleic Acids Research, 46(W1), W350–W355. https://doi.org/10.1093/nar/gky300
  • Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. https://doi.org/10.1016/0021-9991(77)90098-5
  • Saad, F., & Hotte, S. J. (2010). Guidelines for the management of castrate-resistant prostate cancer. Canadian Urological Association Journal Journal de L'Association Des Urologues du Canada, 4(6), 380–384. https://doi.org/10.5489/cuaj.10167
  • Sakkiah, S., Kusko, R., Pan, B., Guo, W., Ge, W., Tong, W., & Hong, H. (2018). Structural changes due to antagonist binding in ligand binding pocket of androgen receptor elucidated through molecular dynamics simulations. Frontiers in Pharmacology, 9. https://doi.org/10.3389/fphar.2018.00492
  • Salo-Ahen, O. M. H., Alanko, I., Bhadane, R., Bonvin, A. M. J. J., Honorato, R. V., Hossain, S., Juffer, A. H., Kabedev, A., Lahtela-Kakkonen, M., Larsen, A. S., Lescrinier, E., Marimuthu, P., Mirza, M. U., Mustafa, G., Nunes-Alves, A., Pantsar, T., Saadabadi, A., Singaravelu, K., & Vanmeert, M. (2020). Molecular dynamics simulations in drug discovery and pharmaceutical development. Processes, 9(1), 71. https://doi.org/10.3390/pr9010071
  • Salomon‐Ferrer, R., Case, D. A., & Walker, R. C. (2013). An overview of the Amber biomolecular simulation package. Wiley Interdisciplinary Reviews: Computational Molecular Science, 3(2), 198–210. https://doi.org/10.1002/wcms.1121
  • Saraon, P., Drabovich, A. P., Jarvi, K. A., & Diamandis, E. P. (2014). Mechanisms of androgen-independent prostate cancer. Ejifcc, 25(1), 42–54.
  • Selvaraj, D., Hariharan, S., & Muthiah, R. (2017). Identification of pharmacophore for wild and T877A mutant androgen receptor antagonist: Challenges in designing 3D-QSAR for mutant protein. International Journal of Quantitative Structure-Property Relationships, 2(2), 47–61. https://doi.org/10.4018/IJQSPR.2017070105
  • Selvaraj, D., Muthu, S., Kotha, S., Siddamsetty, R. S., Andavar, S., & Jayaraman, S. (2021). Syringaresinol as a novel androgen receptor antagonist against wild and mutant androgen receptors for the treatment of castration-resistant prostate cancer: Molecular docking, in-vitro and molecular dynamics study. Journal of Biomolecular Structure & Dynamics, 39(2), 621–634. https://doi.org/10.1080/07391102.2020.1715261
  • Shaw, D. E., Maragakis, P., Lindorff-Larsen, K., Piana, S., Dror, R. O., Eastwood, M. P., Bank, J. A., Jumper, J. M., Salmon, J. K., Shan, Y., & Wriggers, W. (2010). Atomic-level characterization of the structural dynamics of proteins. Science (New York, N.Y.), 330(6002), 341–346. https://doi.org/10.1126/science.1187409
  • Sun, H., Duan, L., Chen, F., Liu, H., Wang, Z., Pan, P., Zhu, F., Zhang, J. Z. H., & Hou, T. (2018). Assessing the performance of MM/PBSA and MM/GBSA methods. 7. Entropy effects on the performance of end-point binding free energy calculation approaches. Physical Chemistry Chemical Physics: PCCP, 20(21), 14450–14460. https://doi.org/10.1039/c7cp07623a
  • Sung, H., Ferlay, J., Siegel, R. L., Laversanne, M., Soerjomataram, I., Jemal, A., & Bray, F. (2021). Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians, 71(3), 209–249. https://doi.org/10.3322/caac.21660
  • Talluri, S. (2021). Molecular docking and virtual screening based prediction of drugs for COVID-19. Combinatorial Chemistry & High Throughput Screening, 24(5), 716–728. https://doi.org/10.2174/1386207323666200814132149
  • Tan, M., Li, J., Xu, H. E., Melcher, K., & Yong, E-l (2015). Androgen receptor: Structure, role in prostate cancer and drug discovery. Acta Pharmacologica Sinica, 36(1), 3–23. https://doi.org/10.1038/aps.2014.18
  • Taplin, M.-E., Bubley, G. J., Ko, Y.-J., Small, E. J., Upton, M., Rajeshkumar, B., & Balk, S. P. (1999). Selection for androgen receptor mutations in prostate cancers treated with androgen antagonist. Cancer Research, 59(11), 2511–2515.
  • Taplin, M.-E., Bubley, G. J., Shuster, T. D., Frantz, M. E., Spooner, A. E., Ogata, G. K., Keer, H. N., & Balk, S. P. (1995). Mutation of the androgen-receptor gene in metastatic androgen-independent prostate cancer. The New England Journal of Medicine, 332(21), 1393–1398. https://doi.org/10.1056/NEJM199505253322101
  • Wang, E., Sun, H., Wang, J., Wang, Z., Liu, H., Zhang, J. Z. H., & Hou, T. (2019). End-point binding free energy calculation with MM/PBSA and MM/GBSA: Strategies and applications in drug design. Chemical Reviews, 119(16), 9478–9508. https://doi.org/10.1021/acs.chemrev.9b00055
  • Weikum, E. R., Liu, X., & Ortlund, E. A. (2018). The nuclear receptor superfamily: A structural perspective. Protein Science : A Publication of the Protein Society, 27(11), 1876–1892. https://doi.org/10.1002/pro.3496
  • Zwanzig, R. (1973). Nonlinear generalized Langevin equations. Journal of Statistical Physics, 9(3), 215–220. https://doi.org/10.1007/BF01008729

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.