Delineating the interaction of combretastatin A-4 with αβ tubulin isotypes present in drug resistant human lung carcinoma using a molecular modeling approach

References

• Allnér, O., Nilsson, L., & Villa, A. (2012). Magnesium ion-water coordination and exchange in biomolecular simulations. Journal of Chemical Theory and Computation, 8(4), 1493–1502. doi:10.1021/ct3000734
   PubMed Web of Science ®Google Scholar
• Banerjee, A., & Luduena, R. F. (1992). Kinetics of colchicine binding to purified beta-tubulin isotypes from bovine brain. The Journal of Biological Chemistry, 267(19), 13335–13339. Retrieved from http://www.jbc.org/content/267/19/13335.short
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. Journal of Chemical Physics, 126(1), 014101. doi:10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Chakraborti, S., Chakravarty, D., Gupta, S., Chatterji, B. P., Dhar, G., Poddar, A., … Bhattacharyya, B. (2012). Discrimination of ligands with different flexibilities resulting from the plasticity of the binding site in tubulin. Biochemistry, 51(36), 7138–7148. doi:10.1021/bi300474q
   PubMed Web of Science ®Google Scholar
• Christoph, D. C., Kasper, S., Gauler, T. C., Loesch, C., Engelhard, M., Theegarten, D., … Wohlschlaeger, J. (2012). βV-tubulin expression is associated with outcome following taxane-based chemotherapy in non-small cell lung cancer. British Journal of Cancer, 107(5), 823–830. doi:10.1038/bjc.2012.324
   PubMed Web of Science ®Google Scholar
• Cowan, N. J., Lewis, S. A., Gu, W., & Burgoyne, R. D. (1988). Tubulin isotypes and their interaction with microtubule associated proteins. Protoplasma, 145(2–3), 106–111. doi:10.1007/BF01349346
   Web of Science ®Google Scholar
• Case, D. A., Darden, T. A., Cheatham, T. E. III, Simmerling, C. L., Wang, J., Duke, R. E. … Kovalenko, (2012). AmberTools12 reference manual. AMBER 12, San Francisco: University of California.
   Google Scholar
• DeLano, W. L. (2002). The PyMOL molecular graphics system, Version 1.1. Schrödinger LLC, Retrieved from http://www.pymol.org. doi:10.1038/hr.2014.17
   Google Scholar
• Derry, W. B., Wilson, L., Khan, I. A., Ludueña, R. F., & Jordan, M. A. (1997). Taxol differentially modulates the dynamics of microtubules assembled from unfractionated and purified β-tubulin isotypes. Biochemistry, 36(12), 3554–3562. doi:10.1021/bi962724m
   PubMed Web of Science ®Google Scholar
• Dumontet, C., & Sikic, B. I. (1999). Mechanisms of action of and resistance to antitubulin agents: Microtubule dynamics, drug transport, and cell death. Journal of Clinical Oncology, 17(3), 1061–1061. doi:10.1200/JCO.1999.17.3.1061 doi:10.1200/JCO.1999.17.3.1061
   PubMed Web of Science ®Google Scholar
• Gaspari, R., Prota, A. E., Bargsten, K., Cavalli, A., & Steinmetz, M. O. (2017). Structural basis of cis- and trans-combretastatin binding to tubulin. Chem, 2(1), 102–113. doi:10.1016/j.chempr.2016.12.005
   Web of Science ®Google Scholar
• Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J., & Lopez, R. (2010). A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Research, 38(Suppl. 2), W695–W659. doi:10.1093/nar/gkq313
   PubMedGoogle Scholar
• Hakeem, S., Singh, I., Sharma, P., Uppal, A., Khajuria, Y., Verma, V., … Chandra, R. (2018). Molecular dynamics analysis of the effects of GTP, GDP and benzimidazole derivative on structural dynamics of a cell division protein FtsZ from Mycobacterium tuberculosis. Journal of Biomolecular Structure and Dynamics, 22, 1–25. doi:10.1080/07391102.2018.1548979
   PubMedGoogle 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. doi:10.1002/(SICI)1096-987X(199709)18:12 < 1463::AID-JCC4 > 3.0.CO;2-H
   Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. doi:10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Hura, N., Naaz, A., Prassanawar, S. S., Guchhait, S. K., & Panda, D. (2018). Drug-clinical agent molecular hybrid: Synthesis of diaryl(trifluoromethyl)pyrazoles as tubulin targeting anticancer agents. ACS Omega, 3(2), 1955–1969. doi:10.1021/acsomega.7b01784
   PubMed Web of Science ®Google Scholar
• Jordan, M. A., & Wilson, L. (2004). Microtubules as a target for anticancer drugs. Nature Reviews. Cancer, 4(4), 253–265. doi:10.1038/nr1317
   PubMed Web of Science ®Google Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen‐bonded and geometrical features. Biopolymers, 22, 2577–2637. doi:10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Kavallaris, M. (2010). Microtubules and resistance to tubulin-binding agents. Nature Reviews Cancer, 10(3), 194–204. doi:10.1038/nrc2803
   PubMed Web of Science ®Google Scholar
• Kavallaris, M., Kuo, D. Y., Burkhart, C. A., Regl, D. L., Norris, M. D., Haber, M., & Horwitz, S. B. (1997). Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. Journal of Clinical Investigation, 100(5), 1282–1293. doi:10.1172/JCI119642
   PubMed Web of Science ®Google Scholar
• Keskin, O., Durell, S. R., Bahar, I., Jernigan, R. L., & Covell, D. G. (2002). Relating molecular flexibility to function: A case study of tubulin. Biophysical Journal, 83(2), 663–680. doi:10.1016/S0006-3495(02)75199-0
   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. doi:10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Kumbhar, B. V., Borogaon, A., Panda, D., & Kunwar, A. (2016). Exploring the origin of differential binding affinities of human tubulin isotypes αβII, αβIII and αβIV for DAMA-colchicine using homology modelling, molecular docking and molecular dynamics simulations. PLoS ONE, 11(5), e0156048. doi:10.1371/journal.pone.0156048
   PubMed Web of Science ®Google Scholar
• Kumbhar, B. V., Panda, D., & Kunwar, A. (2018). Interaction of microtubule depolymerizing agent indanocine with different human αβ tubulin isotypes. PLoS ONE, 13(3), e0194934. doi:10.1371/journal.pone.0194934
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. doi:10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Ludueña, R. F. (1998). Multiple forms of tubulin: Different gene products and covalent modifications. International Review of Cytology, 178, 207–275. doi:10.1016/S0074-7696(08)62138-5
   PubMed Web of Science ®Google Scholar
• Ludueña, R. F. (2013). A hypothesis on the origin and evolution of tubulin. International Review of Cell and Molecular Biology, 302, 41–185. doi:10.1016/B978-0-12-407699-0.00002-9
   PubMed Web of Science ®Google Scholar
• Ludueña, R. F., & Banerjee, A. (2008). The isotypes of tubulin. In The role of microtubules in cell biology, neurobiology, and oncology (pp. 123–175). Berlin: Springer. doi:10.1007/978-1-59745-336-3_6
   Google Scholar
• Meagher, K. L., Redman, L. T., & Carlson, H. A. (2003). Development of polyphosphate parameters for use with the AMBER force field. Journal of Computational Chemistry, 24(9), 1016–1025. doi:10.1002/jcc.10262
   PubMed Web of Science ®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. doi:10.1021/ct300418h
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Ruth, H., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). Software news and updates AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. doi:10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Nagarajan, S., & Sakkiah, S. (2018). Exploring a potential allosteric inhibition mechanism in the motor domain of human Eg-5. Journal of Biomolecular Structure and Dynamics, 13, 1–10. doi:10.1080/07391102.2018.1486229
   Google Scholar
• Ohishi, Y., Oda, Y., Basaki, Y., Kobayashi, H., Wake, N., Kuwano, M., & Tsuneyoshi, M. (2007). Expression of beta-tubulin isotypes in human primary ovarian carcinoma. Gynecologic Oncology, 105(3), 586–592. doi:10.1016/j.ygyno.2007.01.044
   PubMed Web of Science ®Google Scholar
• Pamula, M. C., Ti, S. C., & Kapoor, T. M. (2016). The structured core of human β tubulin confers isotype-specific polymerization properties. The Journal of Cell Biology, 213(4), 425–433. doi:10.1083/jcb.201603050
   PubMed Web of Science ®Google Scholar
• Panda, D., Miller, H. P., Banerjee, A., Ludueña, R. F., & Wilson, L. (1994). Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proceedings of the National Academy of Sciences of the United States of America, 91(24), 11358–11362. doi:10.1073/pnas.91.24.11358
   PubMed Web of Science ®Google Scholar
• Pandey, R. K., Kumbhar, B. V., Srivastava, S., Malik, R., Sundar, S., Kunwar, A., & Prajapati, V. K. (2016). Febrifugine analogues as Leishmania donovani trypanothione reductase inhibitors: binding energy analysis assisted by molecular docking, ADMET and molecular dynamics simulation. Journal of Biomolecular Structure and Dynamics, 1102, 1–49. doi:10.1080/07391102.2015.1135298
   Google Scholar
• Parker, A. L., Teo, W. S., Pandzic, E., Vicente, J. J., McCarroll, J. A., Wordeman, L., & Kavallaris, M. (2018). β-Tubulin carboxy-terminal tails exhibit isotype-specific effects on microtubule dynamics in human gene-edited cells. Life Science Alliance, 1(2), e201800059. doi:10.26508/lsa.201800059
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. doi:10.1063/1.328693
   Web of Science ®Google Scholar
• Peng, L. X., Hsu, M. T., Bonomi, M., Agard, D. A., & Jacobson, M. P. (2014). The free energy profile of tubulin straight-bent conformational changes, with Implications for microtubule assembly and drug discovery. PLoS Computational Biology, 10(2), e1003464. doi:10.1371/journal.pcbi.1003464
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Pettit, G. R., Singh, S. B., Hamel, E., Lin, C. M., Alberts, D. S., & Garcia-Kendal, D. (1989). Isolation and structure of the strong cell growth and tubulin inhibitor combretastatin A-4. Experientia, 45(2), 209–211. doi:10.1007/BF01954881
   PubMedGoogle Scholar
• Pettit, G. R., Singh, S. B., Niven, M. L., Hamel, E., & Schmidt, J. M. (1987). Isolation, structure, and synthesis of combretastatins A-l and B-l, potent new inhibitors of microtubule assembly, derived from combretum caffrum. Journal of Natural Products, 50(1), 119–131. doi:10.1021/np50049a016
   PubMed Web of Science ®Google Scholar
• Ranganathan, S., Benetatos, C. A., Colarusso, P. J., Dexter, D. W., & Hudes, G. R. (1998). Altered beta-tubulin isotype expression in paclitaxel-resistant human prostate carcinoma cells. British Journal of Cancer, 77(4), 562–566. doi:10.1038/bjc.1998.91
   PubMed Web of Science ®Google Scholar
• Sali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234(3), 779–815. doi:10.1006/jmbi.1993.1626
   PubMed Web of Science ®Google Scholar
• Singh, P., Rathinasamy, K., Mohan, R., & Panda, D. (2008). Microtubule assembly dynamics: An attractive target for anticancer drugs. IUBMB Life, 60, 368–375. doi:10.1002/iub.42
   PubMed Web of Science ®Google Scholar
• Stanton, R. A., Gernert, K. M., Nettles, J. H., & Aneja, R. (2011). Drugs that target dynamic microtubules: A new molecular perspective. Medicinal Research Reviews, 31(3), 443–481. doi:10.1002/med.20242
   PubMed Web of Science ®Google Scholar
• Swails, J., Hernandez, C., Mobley, D. L., Nguyen, H., Wang, L. P., & Janowski, P. (n.d.). ParmEd. Retrieved from https://github.com/ParmEd/ParmEd
   Google Scholar
• Torin Huzil, J., Ludueña, R. F., & Tuszynski, J. (2006). Comparative modelling of human β tubulin isotypes and implications for drug binding. Nanotechnology, 17(4), S90–S100. doi:10.1088/0957-4484/17/4/014
   PubMed Web of Science ®Google Scholar
• Tozer, G. M., Kanthou, C., Parkins, C. S., & Hill, S. A. (2002). The biology of the combretastatins as tumour vascular targeting agents. International Journal of Experimental Pathology, 83, 21–38. doi:10.1046/j.1365-2613.2002.00211.x
   PubMed Web of Science ®Google Scholar
• Tripathi, S., Srivastava, G., Singh, A., Prakasham, A. P., Negi, A. S., & Sharma, A. (2018). Insight into microtubule destabilization mechanism of 3,4,5-trimethoxyphenyl indanone derivatives using molecular dynamics simulation and conformational modes analysis. Journal of Computer-Aided Molecular Design, 32(4), 559–572. doi:10.1007/s10822-018-0109-y
   PubMed Web of Science ®Google Scholar
• Tron, G. C., Pirali, T., Sorba, G., Pagliai, F., Busacca, S., & Genazzani, A. A. (2006). Medicinal chemistry of combretastatin A4: Present and future directions. Journal of Medicinal Chemistry, 49, 3033–3044. doi:10.1021/jm0512903
   PubMed Web of Science ®Google Scholar
• Valiron, O., Caudron, N., & Job, D. (2001). Microtubule dynamics. Cellular and Molecular Life Sciences, 58(14), 2069–2084. doi:10.1007/PL00000837
   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, 1701–1718. doi:10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Vemu, A., Atherton, J., Spector, J. O., Moores, C. A., & Roll-Mecak, A. (2017). Tubulin isoform composition tunes microtubule dynamics. Molecular Biology of the Cell, 28, 3563–3725. doi:10.1091/mbc.E17-02-0124
   PubMed Web of Science ®Google Scholar
• Wade, R. H., & Hyman, A. A. (1997). Microtubule structure and dynamics. Current Opinion in Cell Biology, 9, 12–17. doi:10.1016/S0955-0674(97)80146-9
   PubMed Web of Science ®Google Scholar
• Wehbe, H., Kearney, C. M., & Pinney, K. G. (2005). Combretastatin A-4 resistance in H460 human lung carcinoma demonstrates distinctive alterations in β-tubulin isotype expression. Anticancer Research, 25(6B), 3865–3870.
   PubMed Web of Science ®Google Scholar
• Xu, K., Schwarz, P. M., & Ludueña, R. F. (2002). Interaction of nocodazole with tubulin isotypes. Drug Development Research, 55(2), 91–96. doi:10.1002/ddr.10023
   Web of Science ®Google Scholar
• Zhou, X., Xu, Z., Li, A., Zhang, Z., & Xu, S. (2018). Double-sides sticking mechanism of vinblastine interacting with α,β-tubulin to get activity against cancer cells. Journal of Biomolecular Structure and Dynamics, 18, 1–12. doi:10.1080/07391102.2018.1539412
   Google Scholar