Location of the bioactive pentacyclic triterpene ursolic acid in the membrane. A molecular dynamics study

References

• Anézo, C., de Vries, A. H., Höltje, H.-D., Tieleman, D. P., & Marrink, S.-J. (2003). Methodological issues in lipid bilayers simulations. The Journal of Physical Chemistry B, 107, 9424–9433.10.1021/jp0348981
   Web of Science ®Google Scholar
• Bockmann, R. A., Hac, A., Heimburg, T., & Grubmuller, H. (2003). Effect of sodium chloride on a lipid bilayer. Biophysical Journal, 85, 1647–1655.10.1016/S0006-3495(03)74594-9
   PubMed Web of Science ®Google Scholar
• Broniatowski, M., Flasinski, M., & Hac-Wydro, K. (2015). Antagonistic effects of alpha-tocopherol and ursolic acid on model bacterial membranes. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1848, 2154–2162.10.1016/j.bbamem.2015.05.009
   PubMed Web of Science ®Google Scholar
• Broniatowski, M., Flasinski, M., Zieba, K., & Miskowiec, P. (2014). Interactions of pentacyclic triterpene acids with cardiolipins and related phosphatidylglycerols in model systems. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1838, 2530–2538.10.1016/j.bbamem.2014.05.027
   PubMed Web of Science ®Google Scholar
• Camer, D., Yu, Y., Szabo, A., & Huang, X. F. (2014). The molecular mechanisms underpinning the therapeutic properties of oleanolic acid, its isomer and derivatives for type 2 diabetes and associated complications. Molecular Nutrition & Food Research, 58, 1750–1759.10.1002/mnfr.v58.8
   PubMed Web of Science ®Google Scholar
• Fajardo, E., Galiano, V., & Villalain, J. (2016). Molecular dynamics study of the membrane interaction of a membranotropic dengue virus C protein derived peptide. Journal of Biomolecular Structure and Dynamics, 21, 1–12.
   Google Scholar
• Feller, S. E., Zhang, Y., & Pastor, R. W. J. (1995). Constant pressure molecular dynamics simulation: The Langevin piston method. The Journal of Chemical Physics, 103, 4613–4621.10.1063/1.470648
   Web of Science ®Google Scholar
• Flasinski, M., Hac-Wydro, K., & Broniatowski, M. (2014). Incorporation of pentacyclic triterpenes into mitochondrial membrane–studies on the interactions in model 2D lipid systems. The Journal of Physical Chemistry B, 118, 12927–12937.10.1021/jp508743j
   PubMed Web of Science ®Google Scholar
• Fontanay, S., Grare, M., Mayer, J., Finance, C., & Duval, R. E. (2008). Ursolic, oleanolic and betulinic acids: Antibacterial spectra and selectivity indexes. Journal of Ethnopharmacology, 120, 272–276.10.1016/j.jep.2008.09.001
   PubMed Web of Science ®Google Scholar
• Galiano, V., & Villalain, J. (2015). Oleuropein aglycone in lipid bilayer membranes. A molecular dynamics study. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1848, 2849–2858.10.1016/j.bbamem.2015.08.007
   PubMed Web of Science ®Google Scholar
• Galiano, V., & Villalain, J. (2016). The location of the protonated and unprotonated forms of arbidol in the membrane: A molecular dynamics study. Biochim Biophys Acta, 1848, 2849–2858.
   Web of Science ®Google Scholar
• Giorgino, T. (2014). Computing 1-D atomic densities in macromolecular simulations: The density profile tool for VMD. Computer Physics Communications, 185, 317–322.10.1016/j.cpc.2013.08.022
   Web of Science ®Google Scholar
• Guixa-Gonzalez, R., Rodriguez-Espigares, I., Ramirez-Anguita, J. M., Carrio-Gaspar, P., Martinez-Seara, H., Giorgino, T., & Selent, J. (2014). MEMBPLUGIN: Studying membrane complexity in VMD. Bioinformatics, 30, 1478–1480.10.1093/bioinformatics/btu037
   PubMed Web of Science ®Google Scholar
• Han, S. K., Ko, Y. I., Park, S. J., Jin, I. J., & Kim, Y. M. (1997). Oleanolic acid and ursolic acid stabilize liposomal membranes. Lipids, 32, 769–773.10.1007/s11745-997-0098-9
   PubMed Web of Science ®Google Scholar
• Han, Y. Y., Xue, X. W., Shi, Z. M., Wang, P. Y., Wu, X. R., & Wang, X. J. (2014). Oleanolic acid and ursolic acid inhibit proliferation in transformed rat hepatic oval cells. World Journal of Gastroenterology, 20, 1348–1356.10.3748/wjg.v20.i5.1348
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 27–38.
   Google Scholar
• Ingolfsson, H. I., Melo, M. N., van Eerden, F. J., Arnarez, C., Lopez, C. A., Wassenaar, T. A., … Marrink, S. J. (2014). Lipid organization of the plasma membrane. Journal of the American Chemical Society, 136, 14554–14559.10.1021/ja507832e
   PubMed Web of Science ®Google Scholar
• Jager, S., Trojan, H., Kopp, T., Laszczyk, M. N., & Scheffler, A. (2009). Pentacyclic triterpene distribution in various plants – Rich sources for a new group of multi-potent plant extracts. Molecules, 14, 2016–2031.10.3390/molecules14062016
   PubMed Web of Science ®Google Scholar
• Jimenez-Arellanes, A., Luna-Herrera, J., Cornejo-Garrido, J., Lopez-Garcia, S., Castro-Mussot, M. E., Meckes-Fischer, M., … Hernandez-Pando, R. (2013). Ursolic and oleanolic acids as antimicrobial and immunomodulatory compounds for tuberculosis treatment. BMC Complementary and Alternative Medicine, 13, 258.10.1186/1472-6882-13-258
   PubMed Web of Science ®Google Scholar
• Kandt, C., Ash, W. L., & Tieleman, D. P. (2007). Setting up and running molecular dynamics simulations of membrane proteins. Methods, 41, 475–488.10.1016/j.ymeth.2006.08.006
   PubMed Web of Science ®Google Scholar
• Kashyap, D., Tuli, H. S., & Sharma, A. K. (2016). Ursolic acid (UA): A metabolite with promising therapeutic potential. Life Sciences, 146, 201–213.10.1016/j.lfs.2016.01.017
   PubMed Web of Science ®Google Scholar
• Kim, S. H., Ryu, H. G., Lee, J., Shin, J., Harikishore, A., Jung, H. Y., … Kim, K. T. (2015). Ursolic acid exerts anti-cancer activity by suppressing vaccinia-related kinase 1-mediated damage repair in lung cancer cells. Scientific Reports, 5, 14570.10.1038/srep14570
   PubMed Web of Science ®Google Scholar
• Kim, K. H., Seo, H. S., Choi, H. S., Choi, I., Shin, Y. C., & Ko, S. G. (2011). Induction of apoptotic cell death by ursolic acid through mitochondrial death pathway and extrinsic death receptor pathway in MDA-MB-231 cells. Archives of Pharmacal Research, 34, 1363–1372.10.1007/s12272-011-0817-5
   PubMed Web of Science ®Google Scholar
• Klauda, J. B., Venable, R. M., Freites, J. A., O’Connor, J. W., Tobias, D. J., Mondragon-Ramirez, C., … Pastor, R. W. (2010). Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types. The Journal of Physical Chemistry B, 114, 7830–7843.10.1021/jp101759q
   PubMed Web of Science ®Google Scholar
• Kong, L., Li, S., Liao, Q., Zhang, Y., Sun, R., Zhu, X., … Zhu, Y. (2013). Oleanolic acid and ursolic acid: Novel hepatitis C virus antivirals that inhibit NS5B activity. Antiviral Research, 98, 44–53.10.1016/j.antiviral.2013.02.003
   PubMed Web of Science ®Google Scholar
• Kosinova, P., Berka, K., Wykes, M., Otyepka, M., & Trouillas, P. (2012). Positioning of antioxidant quercetin and its metabolites in lipid bilayer membranes: Implication for their lipid-peroxidation inhibition. The Journal of Physical Chemistry B, 116, 1309–1318.10.1021/jp208731g
   PubMed Web of Science ®Google Scholar
• Li, Y., Lu, X., Qi, H., Li, X., Xiao, X., & Gao, J. (2014). Ursolic acid induces apoptosis through mitochondrial intrinsic pathway and suppression of ERK1/2 MAPK in HeLa cells. Journal of Pharmacological Sciences, 125, 202–210.10.1254/jphs.14017FP
   PubMed Web of Science ®Google Scholar
• Li, G., Zhang, X., You, J., Song, C., Sun, Z., Xia, L., & Suo, Y. (2011). Highly sensitive and selective pre-column derivatization high-performance liquid chromatography approach for rapid determination of triterpenes oleanolic and ursolic acids and application to Swertia species: Optimization of triterpenic acids extraction and pre-column derivatization using response surface methodology. Analytica Chimica Acta, 688, 208–218.10.1016/j.aca.2011.01.010
   PubMed Web of Science ®Google Scholar
• Liu, J. (2005). Oleanolic acid and ursolic acid: Research perspectives. Journal of Ethnopharmacology, 100, 92–94.10.1016/j.jep.2005.05.024
   PubMed Web of Science ®Google Scholar
• Lorincz, A., Mihaly, J., Nemeth, C., Wacha, A., & Bota, A. (2015). Effects of ursolic acid on the structural and morphological behaviours of dipalmitoyl lecithin vesicles. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1848, 1092–1098.10.1016/j.bbamem.2015.01.010
   PubMed Web of Science ®Google Scholar
• Ma, J. Q., Ding, J., Xiao, Z. H., & Liu, C. M. (2014). Ursolic acid ameliorates carbon tetrachloride-induced oxidative DNA damage and inflammation in mouse kidney by inhibiting the STAT3 and NF-κB activities. International Immunopharmacology, 21, 389–395.10.1016/j.intimp.2014.05.022
   PubMed Web of Science ®Google Scholar
• Martinez-Abundis, E., Mendez-del Villar, M., Perez-Rubio, K. G., Zuniga, L. Y., Cortez-Navarrete, M., Ramirez-Rodriguez, A., & Gonzalez-Ortiz, M. (2016). Novel nutraceutic therapies for the treatment of metabolic syndrome. World Journal of Diabetes, 7, 142–152.10.4239/wjd.v7.i7.142
   PubMed Web of Science ®Google Scholar
• Martyna, G. J., Tobias, D. J., & Klein, M. L. (1994). Constant pressure molecular dynamics algorithms. The Journal of Chemical Physics, 101, 4177–4189.10.1063/1.467468
   Web of Science ®Google Scholar
• Menendez, J. A., Joven, J., Aragones, G., Barrajon-Catalan, E., Beltran-Debon, R., Borras-Linares, I., … Segura-Carretero, A. (2013). Xenohormetic and anti-aging activity of secoiridoid polyphenols present in extra virgin olive oil. Cell Cycle, 12, 555–578.10.4161/cc.23756
   PubMed Web of Science ®Google Scholar
• Meng, Y., Lin, Z. M., Ge, N., Zhang, D. L., Huang, J., & Kong, F. (2015). Ursolic acid induces apoptosis of prostate cancer cells via the PI3K/Akt/mTOR pathway. The American Journal of Chinese Medicine, 43, 1471–1486.10.1142/S0192415X15500834
   PubMed Web of Science ®Google Scholar
• Murzyn, K., Rog, T., Jezierski, G., Takaoka, Y., & Pasenkiewicz-Gierula, M. (2001). Effects of phospholipid unsaturation on the membrane/water interface: A molecular simulation study. Biophysical Journal, 81, 170–183.10.1016/S0006-3495(01)75689-5
   PubMed Web of Science ®Google Scholar
• Ozu, M., Alvarez, H. A., McCarthy, A. N., Grigera, J. R., & Chara, O. (2013). Molecular dynamics of water in the neighborhood of aquaporins. European Biophysics Journal, 42, 223–239.10.1007/s00249-012-0880-y
   PubMed Web of Science ®Google Scholar
• Patra, M., Karttunen, M., Hyvonen, M. T., Falck, E., Lindqvist, P., & Vattulainen, I. (2003). Molecular dynamics simulations of lipid bilayers: Major artifacts due to truncating electrostatic interactions. Biophysical Journal, 84, 3636–3645.10.1016/S0006-3495(03)75094-2
   PubMed Web of Science ®Google Scholar
• 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, 1781–1802.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Prades, J., Vogler, O., Alemany, R., Gomez-Florit, M., Funari, S. S., Ruiz-Gutierrez, V., & Barcelo, F. (2011). Plant pentacyclic triterpenic acids as modulators of lipid membrane physical properties. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1808, 752–760.10.1016/j.bbamem.2010.12.007
   PubMed Web of Science ®Google Scholar
• Prasad, S., Yadav, V. R., Kannappan, R., & Aggarwal, B. B. (2011). Ursolic acid, a pentacyclin triterpene, potentiates TRAIL-induced apoptosis through p53-independent up-regulation of death receptors: Evidence for the role of reactive oxygen species and JNK. Journal of Biological Chemistry, 286, 5546–5557.10.1074/jbc.M110.183699
   PubMed Web of Science ®Google Scholar
• Prasad, S., Yadav, V. R., Sung, B., Gupta, S. C., Tyagi, A. K., & Aggarwal, B. B. (2016). Ursolic acid inhibits the growth of human pancreatic cancer and enhances the antitumor potential of gemcitabine in an orthotopic mouse model through suppression of the inflammatory microenvironment. Oncotarget, 7, 13182–13196.
   PubMed Web of Science ®Google Scholar
• Prasad, S., Yadav, V. R., Sung, B., Reuter, S., Kannappan, R., Deorukhkar, A., … Aggarwal, B. B. (2012). Ursolic acid inhibits growth and metastasis of human colorectal cancer in an orthotopic nude mouse model by targeting multiple cell signaling pathways: Chemosensitization with capecitabine. Clinical Cancer Research, 18, 4942–4953.10.1158/1078-0432.CCR-11-2805
   PubMed Web of Science ®Google Scholar
• Saini, P., Gayen, P., Kumar, D., Nayak, A., Mukherjee, N., Mukherjee, S., … Babu, S. P. (2014). Antifilarial effect of ursolic acid from Nyctanthes arbortristis: Molecular and biochemical evidences. Parasitology International, 63, 717–728.10.1016/j.parint.2014.06.008
   PubMed Web of Science ®Google Scholar
• Tanachatchairatana, T., Bremner, J. B., Chokchaisiri, R., & Suksamrarn, A. (2008). Antimycobacterial activity of cinnamate-based esters of the triterpenes betulinic, oleanolic and ursolic acids. Chemical & Pharmaceutical Bulletin, 56, 194–198.10.1248/cpb.56.194
   PubMed Web of Science ®Google Scholar
• Tieleman, D. P., Marrink, S. J., & Berendsen, H. J. (1997). A computer perspective of membranes: Molecular dynamics studies of lipid bilayer systems. Biochimica et Biophysica Acta (BBA) – Reviews on Biomembranes, 1331, 235–270.10.1016/S0304-4157(97)00008-7
   PubMed Web of Science ®Google Scholar
• Tsai, H. H., Lee, J. B., Li, H. S., Hou, T. Y., Chu, W. Y., Shen, P. C., … Chiu, C. C. (2015). Geometrical effects of phospholipid olefinic bonds on the structure and dynamics of membranes: A molecular dynamics study. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1848, 1234–1247.10.1016/j.bbamem.2015.02.016
   PubMed Web of Science ®Google Scholar
• Tsuchiya, H. (2015). Membrane interactions of phytochemicals as their molecular mechanism applicable to the discovery of drug leads from plants. Molecules, 20, 18923–18966.10.3390/molecules201018923
   PubMed Web of Science ®Google Scholar
• van Meer, G., Voelker, D. R., & Feigenson, G. W. (2008). Membrane lipids: Where they are and how they behave. Nature Reviews Molecular Cell Biology, 9, 112–124.10.1038/nrm2330
   PubMed Web of Science ®Google Scholar
• Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., … Mackerell, A. D., Jr. (2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31, 671–690.
   PubMed Web of Science ®Google Scholar
• Villar, V. H., Vogler, O., Barcelo, F., Martin-Broto, J., Martinez-Serra, J., Ruiz-Gutierrez, V., & Alemany, R. (2016). Down-regulation of AKT signalling by ursolic acid induces intrinsic apoptosis and sensitization to doxorubicin in soft tissue sarcoma. PLoS One, 11, e0155946.10.1371/journal.pone.0155946
   PubMed Web of Science ®Google Scholar
• Wang, Y., He, Z., & Deng, S. (2016). Ursolic acid reduces the metalloprotease/anti-metalloprotease imbalance in cerebral ischemia and reperfusion injury. Drug Design, Development and Therapy, 10, 1663–1674.10.2147/DDDT
   PubMed Web of Science ®Google Scholar
• Wang, W. J., Sui, H., Qi, C., Li, Q., Zhang, J., Wu, S. F., … Guo, P. T. (2016). Ursolic acid inhibits proliferation and reverses drug resistance of ovarian cancer stem cells by downregulating ABCG2 through suppressing the expression of hypoxia-inducible factor-1alpha in vitro. Oncol Rep, 36, 428–440.
   PubMed Web of Science ®Google Scholar
• Wozniak, L., Skapska, S., & Marszalek, K. (2015). Ursolic acid–A pentacyclic triterpenoid with a wide spectrum of pharmacological activities. Molecules, 20, 20614–20641.10.3390/molecules201119721
   PubMed Web of Science ®Google Scholar
• Wu, E. L., Cheng, X., Jo, S., Rui, H., Song, K. C., Davila-Contreras, E. M., … Im, W. (2014). CHARMM-GUI Membrane Builder toward realistic biological membrane simulations. Journal of Computational Chemistry, 35, 1997–2004.10.1002/jcc.v35.27
   PubMed Web of Science ®Google Scholar
• Wu, C. C., Cheng, C. H., Lee, Y. H., Chang, I. L., Chen, H. Y., Hsieh, C. P., & Chueh, P. J. (2016). Ursolic acid triggers apoptosis in human osteosarcoma cells via caspase activation and the ERK1/2 MAPK pathway. Journal of Agricultural and Food Chemistry, 64, 4220–4226.10.1021/acs.jafc.6b00542
   PubMed Web of Science ®Google Scholar
• Xiang, L., Chi, T., Tang, Q., Yang, X., Ou, M., Chen, X., … Jia, L. (2015). A pentacyclic triterpene natural product, ursolic acid and its prodrug US597 inhibit targets within cell adhesion pathway and prevent cancer metastasis. Oncotarget, 6, 9295–9312.10.18632/oncotarget
   PubMed Web of Science ®Google Scholar
• Xiang, F., Pan, C., Kong, Q., Wu, R., Jiang, J., Zhan, Y., … Kang, X. (2014). Ursolic acid inhibits the proliferation of gastric cancer cells by targeting miR-133a. Oncology Research, 22, 267–273.
   PubMed Web of Science ®Google Scholar
• Zhuang, X., Makover, J. R., Im, W., & Klauda, J. B. (2014). A systematic molecular dynamics simulation study of temperature dependent bilayer structural properties. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1838, 2520–2529.10.1016/j.bbamem.2014.06.010
   PubMed Web of Science ®Google Scholar