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Articles

A study of the structural properties and thermal stability of human Bcl-2 by molecular dynamics simulations

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Pages 1707-1719 | Received 11 Oct 2012, Accepted 07 Aug 2013, Published online: 13 Sep 2013

References

  • Adams, J. M., & Cory, S. (1998). The Bcl-2 protein family: Arbiters of cell survival. Science (New York, NY), 281, 1322–1326.
  • Arbab, I. A., Looi, C. Y., Abdul, A. B., Cheah, F. K., Wong, W. F., Sukari, M. A., … Ibrahim Abdelwahab, S. (2012). Dentatin induces apoptosis in prostate cancer cells via Bcl-2, Bcl-xL, survivin downregulation, caspase-9, -3/7 activation, and NF-κB inhibition. Evidence-Based Complementary and Alternative Medicine, 2012, 1–15. doi:10.1155/2012/856029.
  • Azad, N., Vallyathan, V., Wang, L., Tantishaiyakul, V., Stehlik, C., Leonard, S. S., & Rojanasakul, Y. (2006). S-nitrosylation of Bcl-2 inhibits its ubiquitin-proteasomal degradation. A novel antiapoptotic mechanism that suppresses apoptosis. The Journal of Biological Chemistry, 281, 34124–34134. doi:10.1074/jbc.M602551200.
  • Baldwin, R. L. (1975). Intermediates in protein folding reactions and the mechanism of protein folding. Annual Review of Biochemistry, 44, 453–475. doi:10.1146/annurev.bi.44.070175.002321.
  • Batcho, P. F., Case, D. A., & Schlick, T. (2001). Optimized particle-mesh Ewald/multiple-time step integration for molecular dynamics simulations. The Journal of Chemical Physics, 115, 4003–4018. doi:10.1063/1.1389854.
  • Bennion, B. J., & Daggett, V. (2004). Counteraction of urea-induced protein denaturation by trimethylamine N-oxide: A chemical chaperone at atomic resolution. Proceedings of the National Academy of Sciences of the United States of America, 101, 6433–6438. doi:10.1073/pnas.0308633101.
  • Bharatham, N., Chi, S. W., & Yoon, H. S. (2011). Molecular basis of Bcl-X(L)-p53 interaction: Insights from molecular dynamics simulations. PLoS ONE, 6, e26014. doi:10.1371/journal.pone.0026014.
  • Blagosklonny, M. V. (2001). Unwinding the loop of Bcl-2 phosphorylation. Leukemia, 15, 869–874.
  • Borner, C., Martinou, I., Mattmann, C., Irmler, M., Schaerer, E., Martinou, J. C., & Tschopp, J. (1994). The protein Bcl-2 alpha does not require membrane attachment, but two conserved domains to suppress apoptosis. The Journal of Cell Biology, 126, 1059–1068.
  • Boukharta, L., Keränen, H., Stary-Weinzinger, A., Wallin, G., de Groot, B. L., & Aqvist, J. (2011). Computer simulations of structure-activity relationships for HERG channel blockers. Biochemistry, 50, 6146–6156. doi:10.1021/bi200173n.
  • Budi, A., Legge, S., Treutlein, H., & Yarovsky, I. (2004). Effect of external stresses on protein conformation: A computer modelling study. European Biophysics Journal: EBJ, 33, 121–129. doi:10.1007/s00249-003-0359-y.
  • Camperchioli, A., Mariani, M., Bartollino, S., Petrella, L., Persico, M., Orteca, N., … Fattorusso, C. (2011). Investigation of the Bcl-2 multimerisation process: Structural and functional implications. Biochimica et biophysica acta, 1813, 850–857. doi:10.1016/j.bbamcr.2011.02.006.
  • Carra, J. H., & Privalov, P. L. (1996). Thermodynamics of denaturation of staphylococcal nuclease mutants: An intermediate state in protein folding. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 10, 67–74.
  • Chan, H. S., Bromberg, S., & Dill, K. A. (1995). Models of cooperativity in protein folding. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 348, 61–70. doi:10.1098/rstb.1995.0046.
  • Chang, B. S., Minn, A. J., Muchmore, S. W., Fesik, S. W., & Thompson, C. B. (1997). Identification of a novel regulatory domain in Bcl-X(L) and Bcl-2. The EMBO Journal, 16, 968–977. doi:10.1093/emboj/16.5.968.
  • Chen, S., Li, X., & Ma, H. (2009). New approach for local structure analysis of the tyrosine domain in proteins by using a site-specific and polarity-sensitive fluorescent probe. Chembiochem: A European Journal of Chemical Biology, 10, 1200–1207. doi:10.1002/cbic.200900003.
  • Cheng, E. H., Kirsch, D. G., Clem, R. J., Ravi, R., Kastan, M. B., Bedi, A., … Hardwick, J. M. (1997). Conversion of Bcl-2 to a Bax-like death effector by caspases. Science (New York, NY), 278, 1966–1968.
  • Chipuk, J. E., & Green, D. R. (2008). How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends in Cell Biology, 18, 157–164. doi:10.1016/j.tcb.2008.01.007.
  • Clem, R. J., Cheng, E. H., Karp, C. L., Kirsch, D. G., Ueno, K., Takahashi, A., … Hardwick, J. M. (1998). Modulation of cell death by Bcl-xL through caspase interaction. Proceedings of the National Academy of Sciences of the United States of America, 95, 554–559.
  • Daggett, V., & Levitt, M. (1994). Protein folding↔unfolding dynamics. Current Opinion in Structural Biology, 4, 291–295. doi:10.1016/S0959-440X(94)90322-0.
  • Deng, X., Gao, F., Flagg, T., Anderson, J., & May, W. S. (2006). Bcl2’s flexible loop domain regulates p53 binding and survival. Molecular and Cellular Biology, 26, 4421–4434. doi:10.1128/MCB.01647-05.
  • Deng, X., Kornblau, S. M., Ruvolo, P. P., & May, W. S., Jr (2001). Regulation of Bcl2 phosphorylation and potential significance for leukemic cell chemoresistance. Journal of the National Cancer Institute Monographs, 28, 30–37.
  • Dlugosz, P. J., Billen, L. P., Annis, M. G., Zhu, W., Zhang, Z., Lin, J., … Andrews, D. W. (2006). Bcl-2 changes conformation to inhibit Bax oligomerization. The EMBO Journal, 25, 2287–2296. doi:10.1038/sj.emboj.7601126.
  • Fang, G., Chang, B. S., Kim, C. N., Perkins, C., Thompson, C. B., & Bhalla, K. N. (1998). “Loop” domain is necessary for taxol-induced mobility shift and phosphorylation of Bcl-2 as well as for inhibiting taxol-induced cytosolic accumulation of cytochrome c and apoptosis. Cancer Research, 58, 3202–3208.
  • Filhol, O., & Cochet, C. (2011). Protein kinases curb cell death. Science Signaling, 4, pe26. doi:10.1126/scisignal.2001921.
  • Glykos, N. M. (2006). Software news and updates. Carma: A molecular dynamics analysis program. Journal of Computational Chemistry, 27, 1765–1768. doi:10.1002/jcc.20482.
  • Gu, W., Wang, T., Zhu, J., Shi, Y., & Liu, H. (2003). Molecular dynamics simulation of the unfolding of the human prion protein domain under low pH and high temperature conditions. Biophysical Chemistry, 104, 79–94.
  • Haldar, S., Basu, A., & Croce, C. M. (1998). Serine-70 is one of the critical sites for drug-induced Bcl2 phosphorylation in cancer cells. Cancer Research, 58, 1609–1615.
  • Hinds, M. G., Smits, C., Fredericks-Short, R., Risk, J. M., Bailey, M., Huang, D. C., & Day, C. L. (2007). Bim, Bad and Bmf: Intrinsically unstructured BH3-only proteins that undergo alocalized conformational change upon binding to prosurvival Bcl-2 targets. Cell Death and Differentiation, 14, 128–136.
  • Huang, D. C., Adams, J. M., & Cory, S. (1998). The conserved N-terminal BH4 domain of Bcl-2 homologues is essential for inhibition of apoptosis and interaction with CED-4. The EMBO Journal, 17, 1029–1039. doi:10.1093/emboj/17.4.1029.
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of molecular graphics, 14, 33–38, 27–28.
  • Kazi, A., Sun, J., Doi, K., Sung, S.-S., Takahashi, Y., Yin, H., … Sebti, S. M. (2011). The BH3 alpha-helical mimic BH3-M6 disrupts Bcl-X(L), Bcl-2, and MCL-1 protein-protein interactions with Bax, Bak, Bad, or Bim and induces apoptosis in a Bax- and Bim-dependent manner. The Journal of Biological Chemistry, 286, 9382–9392. doi:10.1074/jbc.M110.203638.
  • Kerr, J. F., Wyllie, A. H., & Currie, A. R. (1972). Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer, 26, 239–257.
  • Kim, K. M., Giedt, C. D., Basañez, G., O’Neill, J. W., Hill, J. J., Han, Y. H., … Zhang, K. Y. (2001). Biophysical characterization of recombinant human Bcl-2 and its interactions with an inhibitory ligand, antimycin A. Biochemistry, 40, 4911–4922.
  • Kirsch, D. G., Doseff, A., Chau, B. N., Lim, D. S., de Souza-Pinto, N. C., Hansford, R., … Hardwick, J. M. (1999). Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome c. The Journal of Biological Chemistry, 274, 21155–21161.
  • Ko, J.-K., Choi, K.-H., Peng, J., He, F., Zhang, Z., Weisleder, N., … Ma, J. (2011). Amphipathic tail-anchoring peptide and Bcl-2 homology domain-3 (BH3) peptides from Bcl-2 family proteins induce apoptosis through different mechanisms. The Journal of Biological Chemistry, 286, 9038–9048. doi:10.1074/jbc.M110.198457.
  • Kolmar, H. (2011). Natural and engineered cystine knot miniproteins for diagnostic and therapeutic applications. Current Pharmaceutical Design, 17, 4329–4336.
  • Koonin, E. V., & Aravind, L. (2002). Origin and evolution of eukaryotic apoptosis: The bacterial connection. Cell Death and Differentiation, 9, 394–404.
  • Ku, B., Liang, C., Jung, J. U., & Oh, B.-H. (2011). Evidence that inhibition of BAX activation by BCL-2 involves its tight and preferential interaction with the BH3 domain of BAX. Cell Research, 21, 627–641. doi:10.1038/cr.2010.149.
  • Lama, D., & Sankararamakrishnan, R. (2011). Molecular dynamics simulations of pro-apoptoticBH3 peptide helices in aqueous medium: Relationship between helix stability andtheir binding affinities to the anti-apoptotic protein Bcl-X(L). Journal of Computer-aided Molecular Design, 25, 413–426. doi:10.1007/s10822-011-9428-y.
  • Lewis, C. J., Thrumurthy, S. G., Pritchard, S., Armstrong, G., & Attwood, S. E. A. (2011). Comparison of COX-2, Ki-67, and BCL-2 expression in normal esophageal mucosa, Barrett’s esophagus, dysplasia, and adenocarcinoma with postablation mucosa and implications for ablative therapies. Surgical Endoscopy, 25, 2564–2569. doi:10.1007/s00464-011-1587-3.
  • Lin, B., Kolluri, S. K., Lin, F., Liu, W., Han, Y.-H., Cao, X., … Zhang, X. K. (2004). Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell, 116, 527–540.
  • MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., … Karplus, M. (1998). All-atom empirical potential for molecular modeling and dynamics studies of proteins. The Journal of Physical Chemistry B, 102, 3586–3616. doi:10.1021/jp973084f.
  • Mancinelli, F., Caraglia, M., Budillon, A., Abbruzzese, A., & Bismuto, E. (2006). Molecular dynamics simulation and automated docking of the pro-apoptotic Bax protein and its complex with a peptide designed from the Bax-binding domain of anti-apoptotic Ku70. Journal of Cellular Biochemistry, 99, 305–318. doi:10.1002/jcb.20893.
  • Masood, A., Azmi, A. S., & Mohammad, R. M. (2011). Small molecule inhibitors of Bcl-2 family proteins for pancreatic cancer therapy. Cancers, 3, 1527–1549. doi:10.3390/cancers3021527.
  • Moroy, G., Martin, E., Dejaegere, A., & Stote, R. H. (2009). Molecular basis for Bcl-2 homology 3 domain recognition in the Bcl-2 protein family: Identification of conserved hot spot interactions. The Journal of Biological Chemistry, 284, 17499–17511. doi:10.1074/jbc.M805542200.
  • Oakes, S. R., Vaillant, F., Lim, E., Lee, L., Breslin, K., Feleppa, F., … Lindeman, G. J. (2012). Sensitization of BCL-2-expressing breast tumors to chemotherapy by the BH3 mimetic ABT-737. Proceedings of the National Academy of Sciences of the United States of America, 109, 2766–2771. doi:10.1073/pnas.1104778108.
  • Ola, M. S., Nawaz, M., & Ahsan, H. (2011). Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Molecular and Cellular Biochemistry, 351, 41–58. doi:10.1007/s11010-010-0709-x.
  • Oltvai, Z. N., Milliman, C. L., & Korsmeyer, S. J. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 74, 609–619.
  • Onuchic, J. N., & Wolynes, P. G. (2004). Theory of protein folding. Current Opinion in Structural Biology, 14, 70–75. doi:10.1016/j.sbi.2004.01.009.
  • Otsuki, T., Hayashi, H., Nishimura, Y., Hyodo, F., Maeda, M., Kumagai, N., … Uragami, K. (2011). Dysregulation of autoimmunity caused by silica exposure and alteration of Fas-mediated apoptosis in T lymphocytes derived from silicosis patients. International Journal of Immunopathology and Pharmacology, 24, 11S–16S.
  • Petros, A. M., Medek, A., Nettesheim, D. G., Kim, D. H., Yoon, H. S., Swift, K., … Fesik, S. W. (2001). Solution structure of the antiapoptotic protein Bcl-2. Proceedings of the National Academy of Sciences of the United States of America, 98, 3012–3017. doi:10.1073/pnas.041619798.
  • Petros, A. M., Olejniczak, E. T., & Fesik, S. W. (2004). Structural biology of the Bcl-2 family of proteins. Biochimica et biophysica acta, 1644, 83–94. doi:10.1016/j.bbamcr.2003.08.012.
  • Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., … Schulten, K. (2005). Scalable molecular dynamics with NAMD. Journal of Computational Chemistry, 26, 1781–1802. doi:10.1002/jcc.20289.
  • Pinto, M., Orzaez, M. M., Delgado-Soler, L., Perez, J. J., & Rubio-Martinez, J. (2011). Rational design of new class of BH3-mimetics as inhibitors of the Bcl-xL protein. Journal of Chemical Information and Computer Sciences, 51, 1249–1258. doi:10.1021/ci100501d.
  • Raghav, P. K., Verma, Y. K., & Gangenahalli, G. U. (2012). Molecular dynamics simulations of the Bcl-2 protein to predict the structure of its unordered flexible loop domain. Journal of Molecular Modeling, 18, 1885–1906. doi:10.1007/s00894-011-1201-6.
  • Reed, J. C., Zha, H., Aime-Sempe, C., Takayama, S., & Wang, H. G. (1996). Structure-function analysis of Bcl-2 family proteins. Regulators of programmed cell death. Advances in Experimental Medicine and Biology, 406, 99–112.
  • Romero, P. R., Zaidi, S., Fang, Y. Y., Uversky, V. N., Radivojac, P., Oldfield, C. J., … Dunker, A. K. (2006). Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proceeding of the National Academy of Science of the United States of America, 103, 8390–8395.
  • Rosales-Hernández, M. C., Mendieta-Wejebe, J. E., Trujillo-Ferrara, J. G., & Correa-Basurto, J. (2010). Homology modeling and molecular dynamics of CYP1A1 and CYP2B1 to explore the metabolism of aryl derivatives by docking and experimental assays. European Journal of Medicinal Chemistry, 45, 4845–4855. doi:10.1016/j.ejmech.2010.07.055.
  • Rosas-Trigueros, J. L., Correa-Basurto, J., Benítez-Cardoza, C. G., & Zamorano-Carrillo, A. (2011). Insights into the structural stability of Bax from molecular dynamics simulations at high temperatures. Protein Science: A Publication of the Protein Society, 20, 2035–2046. doi:10.1002/pro.740.
  • Rosas-Trigueros, J. L., Ilizaliturri-Flores, I., Benítez-Cardoza, C. G., Correa-Basurto, J., & Zamorano-Carrillo, A. (2012). Computational modeling and simulation of the Bcl-2 family: Paving the way for rational drug design. Current Medicinal Chemistry, 19, 6081–6094.
  • Roy, A., Kucukural, A., & Zhang, Y. (2010). I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols, 5, 725–738. doi:10.1038/nprot.2010.5.
  • Ruvolo, P. P., Deng, X., & May, W. S. (2001). Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia, 15, 515–522.
  • 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, 327–341. doi:10.1016/0021-9991(77)90098-5.
  • Smits, C., Czabotar, P. E., Hinds, M. G., & Day, C. L. (2008). Structural plasticity underpinspromiscuous binding of the prosurvival protein A1. Structure, 16, 818–829. doi:10.1016/j.str.2008.02.009.
  • Son, Y.-O., Heo, J.-S., Kim, T.-G., Jeon, Y.-M., Kim, J.-G., & Lee, J.-C. (2010). Over-expression of JunB inhibits mitochondrial stress and cytotoxicity in human lymphoma cells exposed to chronic oxidative stress. BMB Reports, 43, 57–61.
  • Srivastava, R. K., Mi, Q. S., Hardwick, J. M., & Longo, D. L. (1999). Deletion of the loop region of Bcl-2 completely blocks paclitaxel-induced apoptosis. Proceedings of the National Academy of Sciences of the United States of America, 96, 3775–3780.
  • Szilák, L., Moitra, J., Krylov, D., & Vinson, C. (1997). Phosphorylation destabilizes alpha-helices. Nature Structural Biology, 4, 112–114.
  • Tan, N., Malek, M., Zha, J., Yue, P., Kassees, R., Berry, L., … Belmont, L. D. (2011). Navitoclax enhances the efficacy of taxanes in non-small cell lung cancer models. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 17, 1394–1404. doi:10.1158/1078-0432.CCR-10-2353.
  • Tsujimoto, Y., Finger, L. R., Yunis, J., Nowell, P. C., & Croce, C. M. (1984). Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science (New York, NY), 226, 1097–1099.
  • Wang, Q., Xu, W., Wu, P., Zhang, H., Cai, C., & Zhao, B. (2010). New insights into the effects of thermal treatment on the catalytic activity and conformational structure of glucose oxidase studied by electrochemistry, IR spectroscopy, and theoretical calculation. The Journal of Physical Chemistry. B, 114, 12754–12764. doi:10.1021/jp106214v.
  • Wesarg, E., Hoffarth, S., Wiewrodt, R., Kröll, M., Biesterfeld, S., Huber, C., & Schuler, M. (2007). Targeting BCL-2 family proteins to overcome drug resistance in non-small cell lung cancer. International Journal of Cancer. Journal International du Cancer, 121, 2387–2394. doi:10.1002/ijc.22977.
  • Yamamoto, K., Ichijo, H., & Korsmeyer, S. J. (1999). BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Molecular and Cellular Biology, 19, 8469–8478.
  • Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40. doi:10.1186/1471-2105-9-40.
  • Zhang, B., Corbel, C., Guéritte, F., Couturier, C., Bach, S., & Tan, V. B. C. (2011). An in silico approach for the discovery of CDK5/p25 interaction inhibitors. Biotechnology Journal, 6, 871–881. doi:10.1002/biot.201100139.
  • Zhang, Y., Kolinski, A., & Skolnick, J. (2003). TOUCHSTONE II: A new approach to ab initioprotein structure prediction. Biophysical Journal, 85, 1145–1164.

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