174
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Citrus nutraceutical eriocitrin and its metabolites are partial agonists of peroxisome proliferator-activated receptor gamma (PPARγ): a molecular docking and molecular dynamics study

, , , ORCID Icon & ORCID Icon
Pages 11373-11393 | Received 01 Sep 2022, Accepted 18 Dec 2022, Published online: 28 Dec 2022

References

  • Alam, F., Islam, M. A., Mohamed, M., Ahmad, I., Kamal, M. A., Donnelly, R., Idris, I., & Gan, S. H. (2019). Efficacy and safety of pioglitazone monotherapy in type 2 diabetes mellitus: A systematic review and meta-analysis of randomised controlled. Scientific Reports, 9(1), 5389. https://doi.org/10.1038/s41598-019-41854-2
  • Amato, A. A., Rajagopalan, S., Lin, J. Z., Carvalho, B. M., Figueira, A. C., Lu, J., Ayers, S. D., Mottin, M., Silveira, R. L., Souza, P. C., Mourão, R. H., Saad, M. J., Togashi, M., Simeoni, L. A., Abdalla, D. S., Skaf, M. S., Polikparpov, I., Lima, M. C., Galdino, S. L., … Neves, F. A. (2012). GQ-16, a novel peroxisome proliferator-activated receptor γ (PPARγ) ligand, promotes insulin sensitization without weight gain. The Journal of Biological Chemistry, 287(33), 28169–28179. https://doi.org/10.1074/jbc.M111.332106
  • Ávila-Gálvez, M., Giménez-Bastida, J. A., González-Sarrías, A., & Espín, J. C. (2021). New insights into the metabolism of the flavanones eriocitrin and hesperidin: A comparative human pharmacokinetic study. Antioxidants (Basel), 10(3), 435. https://doi.org/10.10.3390/antiox10030435
  • Bahar, I., Lezon, T. R., Yang, L. W., & Eyal, E. (2010). Global dynamics of proteins: Bridging between structure and function. Annual Review of Biophysics, 39, 23–42. https://doi.org/10.1146/annurev.biophys.093008.131258
  • Bai, J., Wang, Y., Zhu, X., & Shi, J. (2019). Eriodictyol inhibits high glucose-induced extracellular matrix accumulation, oxidative stress, and inflammation in human glomerular mesangial cells. Phytotherapy Research : PTR, 33(10), 2775–2782. https://doi.org/10.1002/ptr.6463
  • Banks, A. S., McAllister, F. E., Camporez, J. P., Zushin, P. J., Jurczak, M. J., Laznik-Bogoslavski, D., Shulman, G. I., Gygi, S. P., & Spiegelman, B. M. (2015). An ERK/Cdk5 axis controls the diabetogenic actions of PPARγ. Nature, 517(7534), 391–395. https://doi.org/10.1038/nature13887
  • Bruning, J. B., Chalmers, M. J., Prasad, S., Busby, S. A., Kamenecka, T. M., He, Y., Nettles, K. W., & Griffin, P. R. (2007). Partial agonists activate PPARgamma using a helix 12 independent mechanism. Structure (London, England : 1993), 15(10), 1258–1271. https://doi.org/10.1016/j.str.2007.07.014
  • Cariou, B., Charbonnel, B., & Staels, B. (2012). Thiazolidinediones and PPARγ agonists: Time for a reassessment. Trends in Endocrinology and Metabolism: TEM, 23(5), 205–215. https://doi.org/10.1016/j.tem.2012.03.001
  • Cesar, T. B., Ramos, F. M. M., & Ribeiro, C. B. (2022). Nutraceutical Eriocitrin (Eriomin) reduces hyperglycemia by increasing glucagon-like peptide 1 and downregulates systemic inflammation: A crossover-randomized clinical trial. Journal of Medicinal Food, 25(11), 1050–1058. https://doi.org/10.1089/jmf.2021.0181
  • Chang, M. R., Ciesla, A., Strutzenberg, T. S., Novick, S. J., He, Y., Garcia-Ordonez, R. D., Frkic, R. L., Bruning, J. B., Kamenecka, T. M., & Griffin, P. R. (2019). Unique polypharmacology nuclear receptor modulator blocks inflammatory signaling pathways. ACS Chemical Biology, 14(5), 1051–1062. https://doi.org/10.1021/acschembio.9b00236
  • Choi, J. H., Banks, A. S., Kamenecka, T. M., Busby, S. A., Chalmers, M. J., Kumar, N., Kuruvilla, D. S., Shin, Y., He, Y., Bruning, J. B., Marciano, D. P., Cameron, M. D., Laznik, D., Jurczak, M. J., Schürer, S. C., Vidović, D., Shulman, G. I., Spiegelman, B. M., & Griffin, P. R. (2011). Antidiabetic actions of a non-agonist PPARγ ligand blocking Cdk5-mediated phosphorylation. Nature, 477(7365), 477–481. https://doi.org/10.1038/nature10383
  • Choi, S. S., Kim, E. S., Koh, M., Lee, S. J., Lim, D., Yang, Y. R., Jang, H. J., Seo, K. A., Min, S. H., Lee, I. H., Park, S. B., Suh, P. G., & Choi, J. H. (2014). A novel non-agonist peroxisome proliferator-activated receptor γ (PPARγ) ligand UHC1 blocks PPARγ phosphorylation by cyclin-dependent kinase 5 (CDK5) and improves insulin sensitivity. The Journal of Biological Chemistry, 289(38), 26618–26629. https://doi.org/10.1074/jbc.M114.566794
  • Cronet, P., Petersen, J. F., Folmer, R., Blomberg, N., Sjöblom, K., Karlsson, U., Lindstedt, E. L., & Bamberg, K. (2001). Structure of the PPARalpha and -gamma ligand binding domain in complex with AZ 242; ligand selectivity and agonist activation in the PPAR family. Structure (London, England : 1993), 9(8), 699–706. https://doi.org/10.1016/S0969-2126(01)00634-7
  • Dallakyan, S., & Olson, A. J. (2015). Small-molecule library screening by docking with PyRx. Methods in Molecular Biology (Clifton, N.J.), 1263, 243–250. https://doi.org/10.1007/978-1-4939-2269-7_19
  • Darband, S. G., Kaviani, M., Yousefi, B., Sadighparvar, S., Pakdel, F. G., Attari, J. A., Mohebbi, I., Naderi, S., & Majidinia, M. (2018). Quercetin: A functional dietary flavonoid with potential chemo-preventive properties in colorectal cancer. Journal of Cellular Physiology, 233(9), 6544–6560. https://doi.org/10.1002/jcp.26595
  • 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
  • David, C. C., &Jacobs, D. (2014). Principal component analysis: a method for determining the essential dynamics of proteins. Methods in Molecular Biology, 1084, 193–226. https://doi.org/10.1007/978-1-62703-658-0_11.
  • de Groot, J. C., Weidner, C., Krausze, J., Kawamoto, K., Schroeder, F. C., Sauer, S., & Büssow, K. (2013). Structural characterization of amorfrutins bound to the peroxisome proliferator-activated receptor γ. Journal of Medicinal Chemistry, 56(4), 1535–1543. https://doi.org/10.1021/jm3013272
  • Delfosse, V., Maire, A. L., Balaguer, P., & Bourguet, W. (2015). A structural perspective on nuclear receptors as targets of environmental compounds. Acta Pharmacologica Sinica, 36(1), 88–101. https://doi.org/10.1038/aps.2014.133
  • Desterke, C., Turhan, A. G., Bennaceur-Griscelli, A., & Griscelli, F. (2020). PPARγ cistrome repression during activation of lung monocyte-macrophages in severe COVID-19. iScience, 23(10), 101611. https://doi.org/10.1016/j.isci.2020.101611
  • Elzahhar, P. A., Alaaeddine, R., Ibrahim, T. M., Nassra, R., Ismail, A., Chua, B. S. K., Frkic, R. L., Bruning, J. B., Wallner, N., Knape, T., von Knethen, A., Labib, H., El-Yazbi, A. F., & Belal, A. S. F. (2019). Shooting three inflammatory targets with a single bullet: Novel multi-targeting anti-inflammatory glitazones. European Journal of Medicinal Chemistry, 167, 562–582. https://doi.org/10.1016/j.ejmech.2019.02.034
  • Farce, A., Renault, N., & Chavatte, P. (2009). Structural insight into PPARgamma ligands binding. Current Medicinal Chemistry, 16(14), 1768–1789. https://doi.org/10.2174/092986709788186165
  • Ferreira, P. S., Manthey, J. A., Nery, M. S., & Cesar, T. B. (2021). Pharmacokinetics and biodistribution of eriocitrin in rats. Journal of Agricultural and Food Chemistry, 69(6), 1796–1805. https://doi.org/10.1021/acs.jafc.0c04553
  • Ferreira, P. S., Manthey, J. A., Nery, M. S., Spolidorio, L. C., & Cesar, T. B. (2020). Low doses of eriocitrin attenuate metabolic impairment of glucose and lipids in ongoing obesogenic diet in mice. Journal of Nutritional Science, 9, e59. https://doi.org/10.1017/jns.2020.52
  • Ferreira, P. S., Spolidorio, L. C., Manthey, J. A., & Cesar, T. B. (2016). Citrus flavanones prevent systemic inflammation and ameliorate oxidative stress in C57BL/6J mice fed high-fat diet. Food & Function, 7(6), 2675–2681. https://doi.org/10.1039/c5fo01541c
  • Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., Repasky, M. P., Knoll, E. H., Shelley, M., Perry, J. K., Shaw, D. E., Francis, P., & Shenkin, P. S. (2004). Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. Journal of Medicinal Chemistry, 47(7), 1739–1749. https://doi.org/10.1021/jm0306430
  • Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C., & Mainz, D. T. (2006). Extra precision glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. Journal of Medicinal Chemistry, 49(21), 6177–6196. https://doi.org/10.1021/jm051256o
  • Frkic, R. L., Richter, K., & Bruning, J. B. (2021). The therapeutic potential of inhibiting PPARγ phosphorylation to treat type 2 diabetes. The Journal of Biological Chemistry, 297(3), 101030. https://doi.org/10.1016/j.jbc.2021.101030
  • Gaillard, T. (2018). Evaluation of AutoDock and AutoDock Vina on the CASF-2013 Benchmark. Journal of Chemical Information and Modeling, 58(8), 1697–1706. https://doi.org/10.1021/acs.jcim.8b00312
  • Garcia-Vallvé, S., Guasch, L., Tomas-Hernández, S., del Bas, J. M., Ollendorff, V., Arola, L., Pujadas, G., & Mulero, M. (2015). Peroxisome proliferator-activated receptor γ (PPARγ) and ligand choreography: Newcomers take the stage. Journal of Medicinal Chemistry, 58(14), 5381–5394. https://doi.org/10.1021/jm501155f
  • Gohlke, H., Kiel, C., & Case, D. A. (2003). Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes. Journal of Molecular Biology, 330(4), 891–913. https://doi.org/10.1016/S0022-2836(03)00610-7
  • Greenwood, J. R., Calkins, D., Sullivan, A. P., & Shelley, J. C. (2010). Towards the comprehensive, rapid, and accurate prediction of the favorable tautomeric states of drug-like molecules in aqueous solution. Journal of Computer-Aided Molecular Design, 24(6-7), 591–604. https://doi.org/10.1007/s10822-010-9349-1
  • Halgren, T. A., Murphy, R. B., Friesner, R. A., Beard, H. S., Frye, L. L., Pollard, W. T., & Banks, J. L. (2004). Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. Journal of Medicinal Chemistry, 47(7), 1750–1759. https://doi.org/10.1021/jm030644s
  • Hameed, A., Hafizur, R. M., Hussain, N., Raza, S. A., Rehman, M., Ashraf, S., Ul-Haq, Z., Khan, F., Abbas, G., & Choudhary, M. I. (2018). Eriodictyol stimulates insulin secretion through cAMP/PKA signaling pathway in mice islets. European Journal of Pharmacology, 820, 245–255. https://doi.org/10.1016/j.ejphar.2017.12.015
  • Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraints solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12 < 1463::AID-JCC4 > 3.0.CO;2-H
  • Hossain, M. U., Khan, M. A., Rakib-Uz-Zaman, S. M., Ali, M. T., Islam, M. S., Keya, C. A., & Salimullah, M. (2016). Treating diabetes mellitus: pharmacophore based designing of potential drugs from Gymnema sylvestre against insulin receptor protein. BioMed Research International, 2016, 3187647. https://doi.org/10.1155/2016/3187647
  • Janani, C., & Ranjitha Kumari, B. D. (2015). PPAR gamma gene–a review. Diabetes & Metabolic Syndrome, 9(1), 46–50. https://doi.org/10.1016/j.dsx.2014.09.015
  • Kroker, A. J., & Bruning, J. B. (2015). Review of the structural and dynamic mechanisms of PPARγ partial agonism. PPAR Research, 2015, 816856. https://doi.org/10.1155/2015/816856
  • 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. https://doi.org/10.1021/ci500020m
  • Kwon, E. Y., & Choi, M. S. (2020). Eriocitrin improves adiposity and related metabolic disorders in high-fat diet-induced obese mice. Journal of Medicinal Food, 23(3), 233–241. https://doi.org/10.1089/jmf.2019.4638
  • Kwon, E.-Y., & Choi, M.-S. (2019). Dietary eriodictyol alleviates adiposity, hepatic steatosis, insulin resistance, and inflammation in diet-induced obese mice. International Journal of Molecular Sciences, 20(5), 1227. https://doi.org/10.3390/ijms20051227
  • Lamothe, S. M.,Guo, J.,Li, W.,Yang, T., &Zhang, S. (2016). The Human Ether-a-go-go-related Gene (hERG) Potassium Channel Represents an Unusual Target for Protease-mediated Damage. The Journal of Biological Chemistry, 291(39), 20387–20401. https://doi.org/10.1074/jbc.M116.743138
  • Lebovitz, H. E. (2019). Thiazolidinediones: The forgotten diabetes medications. Current Diabetes Reports, 19(12), 151. https://doi.org/10.1007/s11892-019-1270-y
  • Lee, M. A., Tan, L., Yang, H., Im, Y. G., & Im, Y. J. (2017). Structures of PPARγ complexed with lobeglitazone and pioglitazone reveal key determinants for the recognition of antidiabetic drugs. Scientific Reports, 7(1), 16837. https://doi.org/10.1038/s41598-017-17082-x
  • Li, L., Feng, X., Chen, Y., Li, S., Sun, Y., & Zhang, L. (2019). A comprehensive study of eriocitrin metabolism. RSC Advances, 9(43), 24963–24980. https://doi.org/10.1039/C9RA03037A
  • Ming, Y., Hu, X., Song, Y., Liu, Z., Li, J., Gao, R., Zhang, Y., Mei, H., Guo, T., Xiao, L., Wang, B., Wu, C., & Xiao, X. (2014). CMHX008, a novel peroxisome proliferator-activated receptor γ partial agonist, enhances insulin sensitivity in vitro and in vivo. PLoS One, 9(7), e102102. https://doi.org/10.1371/journal.pone.0102102
  • Miyake, Y., Sakurai, C., Usuda, M., Fukumoto, S., Hiramitsu, M., Sakaida, K., Osawa, T., & Kondo, K. (2006). Difference in plasma metabolite concentration after ingestion of lemon flavonoids and their aglycones in humans. Journal of Nutritional Science and Vitaminology, 52(1), 54–60. https://doi.org/10.3177/jnsv.52.54
  • Miyake, Y., Yamamoto, K., & Osawa, T. (1997). Metabolism of antioxidant in lemon fruit (Citrus limon BURM. f.) by human intestinal bacteria. Journal of Agricultural and Food Chemistry, 45(10), 3738–3742. https://doi.org/10.1021/jf970403r
  • Moseti, D., Regassa, A., & Kim, W. K. (2016). Molecular regulation of adipogenesis and potential anti-adipogenic bioactive molecules. International Journal of Molecular Sciences, 17(1), 124. https://doi.org/10.3390/ijms17010124
  • Németh, K., Plumb, G. W., Berrin, J. G., Juge, N., Jacob, R., Naim, H. Y., Williamson, G., Swallow, D. M., & Kroon, P. A. (2003). Deglycosylation by small intestinal epithelial cell beta-glucosidases is a critical step in the absorption and metabolism of dietary flavonoid glycosides in humans. European Journal of Nutrition, 42(1), 29–42. https://doi.org/10.1007/s00394-003-0397-3
  • Nolte, R. T., Wisely, G. B., Westin, S., Cobb, J. E., Lambert, M. H., Kurokawa, R., Rosenfeld, M. G., Willson, T. M., Glass, C. K., & Milburn, M. V. (1998). Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature, 395(6698), 137–143. https://doi.org/10.1038/25931
  • 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
  • Pathak, R. K., Gupta, A., Shukla, R., & Baunthiyal, M. (2018). Identification of new drug-like compounds from millets as Xanthine oxidoreductase inhibitors for treatment of Hyperuricemia: A molecular docking and simulation study. Computational Biology and Chemistry, 76, 32–41. https://doi.org/10.1016/j.compbiolchem.2018.05.015
  • 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
  • Pirat, C., Farce, A., Lebègue, N., Renault, N., Furman, C., Millet, R., Yous, S., Speca, S., Berthelot, P., Desreumaux, P., & Chavatte, P. (2012). Targeting peroxisome proliferator-activated receptors (PPARs): Development of modulators. Journal of Medicinal Chemistry, 55(9), 4027–4061. https://doi.org/10.1021/jm101360s
  • Pires, D. E., Blundell, T. L., & Ascher, D. B. (2015). pkCSM: Predicting small-molecule pharmacokinetic and toxicity properties using graph-based signatures. Journal of Medicinal Chemistry, 58(9), 4066–4072. https://doi.org/10.1021/acs.jmedchem.5b00104
  • Ribeiro, C. B., Ramos, F. M., Manthey, J. A., & Cesar, T. B. (2019). Effectiveness of Eriomin® in managing hyperglycemia and reversal of prediabetes condition: A double-blind, randomized, controlled study. Phytotherapy Research : PTR, 33(7), 1921–1933. https://doi.org/10.1002/ptr.6386
  • Roos, K., Wu, C., Damm, W., Reboul, M., Stevenson, J. M., Lu, C., Dahlgren, M. K., Mondal, S., Chen, W., Wang, L., Abel, R., Friesner, R. A., & Harder, E. D. (2019). OPLS3e: Extending force field coverage for drug-like small molecules. Journal of Chemical Theory and Computation, 15(3), 1863–1874. https://doi.org/10.1021/acs.jctc.8b01026
  • Rusznyak, S., & Szent-Gyorgyi, A. (1936). Vitamin P: Flavonols as vitamins. Nature, 138, 27. https://doi.org/10.1038/138027a0
  • Sastry, G. M., Adzhigirey, M., Day, T., Annabhimoju, R., & Sherman, W. (2013). Protein and ligand preparation: Parameters, protocols, and influence on virtual screening enrichments. Journal of Computer-Aided Molecular Design, 27(3), 221–234. https://doi.org/10.1007/s10822-013-9644-8
  • Strand, D. W., Jiang, M., Murphy, T. A., Yi, Y., Konvinse, K. C., Franco, O. E., Wang, Y., Young, J. D., & Hayward, S. W. (2012). PPARγ isoforms differentially regulate metabolic networks to mediate mouse prostatic epithelial differentiation. Cell Death & Disease, 3(8), e361. https://doi.org/10.1038/cddis.2012.99
  • Sugiyama, Y., Kawakishi, S., & Osawa, T. (1996). Involvement of the beta-diketone moiety in the antioxidative mechanism of tetrahydrocurcumin. Biochemical Pharmacology, 52(4), 519–525. https://doi.org/10.1016/0006-2952(96)00302-4
  • Trott, O., & Olson, A. J. (2010). 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
  • Umemoto, T., & Fujiki, Y. (2012). Ligand-dependent nucleo-cytoplasmic shuttling of peroxisome proliferator-activated receptors, PPARα and PPARγ. Genes to Cells : Devoted to Molecular & Cellular Mechanisms, 17(7), 576–596. https://doi.org/10.1111/j.1365-2443.2012.01607.x
  • Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., & Mackerell, A. D. (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. https://doi.org/10.1002/jcc.21367
  • Waku, T., Shiraki, T., Oyama, T., Maebara, K., Nakamori, R., & Morikawa, K. (2010). The nuclear receptor PPARγ individually responds to serotonin- and fatty acid-metabolites. The EMBO Journal, 29(19), 3395–3407. https://doi.org/10.1038/emboj.2010.197
  • Wan, J., Feng, Y., Du, L., Veeraraghavan, V. P., Mohan, S. K., & Guo, S. (2020). Antiatherosclerotic activity of eriocitrin in high-fat-diet-induced atherosclerosis model rats. Journal of Environmental Pathology, Toxicology and Oncology, 39(1), 61–75. https://doi.org/10.1615/JEnvironPatholToxicolOncol.2020031478
  • Wang, T. Y., Li, Q., & Bi, K. S. (2018). Bioactive flavonoids in medicinal plants: Structure, activity and biological fate. Asian Journal of Pharmaceutical Sciences, 13(1), 12–23. https://doi.org/10.1016/j.ajps.2017.08.004
  • Xie, X., Zhou, X., Chen, W., Long, L., Li, W., Yang, X., Li, S., & Wang, L. (2015). L312, a novel PPARγ ligand with potent anti-diabetic activity by selective regulation. Biochimica et Biophysica Acta, 1850(1), 62–72. https://doi.org/10.1016/j.bbagen.2014.09.027
  • Yadava, U., Gupta, H., & Roychoudhury, M. (2015). Stabilization of microtubules by taxane diterpenoids: Insight from docking and MD simulations. Journal of Biological Physics, 41(2), 117–133. https://doi.org/10.1007/s10867-014-9369-5
  • Zheng, W., Qiu, L., Wang, R., Feng, X., Han, Y., Zhu, Y., Chen, D., Liu, Y., Jin, L., & Li, Y. (2015). Selective targeting of PPARγ by the natural product chelerythrine with a unique binding mode and improved antidiabetic potency. Scientific Reports, 5, 12222. https://doi.org/10.1038/srep12222

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.