539
Views
3
CrossRef citations to date
0
Altmetric
Research Articles

Virtual screening of natural products inspired in-house library to discover potential lead molecules against the SARS-CoV-2 main protease

, , , ORCID Icon, , , , , , , & show all
Pages 2033-2045 | Received 26 May 2021, Accepted 05 Jan 2022, Published online: 19 Jan 2022

References

  • Acharya, C., Achari, A., & Jaisankar, P. J. T. L. (2018). Daucus carota root enzyme catalyzed Henry reaction: A green approach. Tetrahedron Letters, 59(7), 663–666. https://doi.org/10.1016/j.tetlet.2018.01.009
  • Anand, K., Ziebuhr, J., Wadhwani, P., Mesters, J. R., & Hilgenfeld, R. J. S. (2003). Coronavirus main proteinase (3CLpro) structure: Basis for design of anti-SARS drugs. Science (New York, N.Y.), 300(5626), 1763–1767. https://doi.org/10.1126/science.1085658
  • Basu, S., Maruthanayagam, V., Chakraborty, S., Pramanik, A., Achari, A., Jaisankar, P., Mukherjee, J., & Sciences, E. (2021). Cyanobacteria of the Indian Sundarbans: A potential source of powerful therapeutic agents. International Journal of Chemical and Environmental Sciences, 2(2), 56–61. https://doi.org/10.15864/ijcaes.2205
  • Bhardwaj, V. K., Singh, R., Das, P., & Purohit, R. (2021). Evaluation of acridinedione analogs as potential SARS-CoV-2 main protease inhibitors and their comparison with repurposed anti-viral drugs. Computers in Biology and Medicine, 128, 104117. https://doi.org/10.1016/j.compbiomed.2020.104117
  • Bhardwaj, V. K., Singh, R., Sharma, J., Rajendran, V., Purohit, R., & Kumar, S. (2021). Bioactive molecules of tea as potential inhibitors for RNA-dependent RNA polymerase of SARS-CoV-2. Frontiers in Medicine, 8, 1–11.
  • Bhardwaj, V. K., Singh, R., Sharma, J., Rajendran, V., Purohit, R., & Kumar, S. (2021). Identification of bioactive molecules from tea plant as SARS-CoV-2 main protease inhibitors. Journal of Biomolecular Structure and Dynamics, 39(10), 3449–3458. https://doi.org/10.1080/07391102.2020.1766572
  • Bhattacharjee, P., Chatterjee, S., Achari, A., Saha, A., Nandi, D., Acharya, C., Chatterjee, K., Ghosh, S., Swarnakar, S., & Jaisankar, P. J. A. (2020). A bis-indole/carbazole based C5-curcuminoid fluorescent probe with large Stokes shift for selective detection of biothiols and application to live cell imaging. The Analyst, 145(4), 1184–1189. https://doi.org/10.1039/c9an02190f
  • Cao, B., Wang, Y., Wen, D., Liu, W., Wang, J., Fan, G., Ruan, L., Song, B., Cai, Y., & Wei, M. (2020). A trial of lopinavir–ritonavir in adults hospitalized with severe Covid-19. The New England Journal of Medicine, 382(19), 1787-1799
  • Chatterjee, S., Bhattacharjee, P., Butterfoss, G. L., Achari, A., & Jaisankar, P. J. R. A. (2019). Establishment of atropisomerism in 3-indolyl furanoids: A synthetic, experimental and theoretical perspective. RSC Advances, 9(39), 22384–22388. https://doi.org/10.1039/C9RA05350F
  • Chatterjee, S., Bhattacharjee, P., Temburu, J., Nandi, D., & Jaisankar, P. J. T. L. (2014). Indium trichloride catalyzed sp3 C–H bond functionalization of 2-alkyl azaarenes under microwave irradiation. Tetrahedron Letters, 55(49), 6680–6683. https://doi.org/10.1016/j.tetlet.2014.10.058
  • Chatterjee, S., Hintermann, L., Mandal, M., Achari, A., Gupta, S., & Jaisankar, P. J. O. l. (2017). Fiaud’s acid: A Brønsted acid catalyst for enantioselective Friedel–Crafts alkylation of indoles with 2-alkene-1, 4-diones. Organic Letters, 19(13), 3426–3429.
  • Chen, Y., Zheng, Y., Fong, P., Mao, S., & Wang, Q. (2020). The application of the MM/GBSA method in the binding pose prediction of FGFR inhibitors. Physical Chemistry Chemical Physics: PCCP, 22(17), 9656–9663. https://doi.org/10.1039/d0cp00831a
  • Cherrak, S. A., Merzouk, H., & Mokhtari-Soulimane, N. J. P. O. (2020). Potential bioactive glycosylated flavonoids as SARS-CoV-2 main protease inhibitors: A molecular docking and simulation studies. PloS One, 15(10), e0240653. https://doi.org/10.1371/journal.pone.0240653
  • Choudhary, M. I., Shaikh, M., Tul-Wahab, A., & Ur-Rahman, A.-J. P. O. (2020). In silico identification of potential inhibitors of key SARS-CoV-2 3CL hydrolase (Mpro) via molecular docking, MMGBSA predictive binding energy calculations, and molecular dynamics simulation. PloS One, 15(7), e0235030. https://doi.org/10.1371/journal.pone.0235030
  • Dey, S., Nandi, D., Pradhan, P. K., Giri, V. S., & Jaisankar, P. J. T. l. (2007). Indium trichloride catalyzed efficient one-pot synthesis of highly substituted furans. Tetrahedron Letters, 48(14), 2573–2575. https://doi.org/10.1016/j.tetlet.2007.02.019
  • Fu, L., Ye, F., Feng, Y., Yu, F., Wang, Q., Wu, Y., Zhao, C., Sun, H., Huang, B., & Niu, P. J. N. C. (2020). Both Boceprevir and GC376 efficaciously inhibit SARS-CoV-2 by targeting its main protease. Nature Communications, 11(1), 1–8.
  • 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
  • Goel, N., Gajbhiye, R. L., Saha, M., Nagendra, C., Reddy, A. M., Ravichandiran, V., Saha, K. D., & Jaisankar, P. J. R. A. (2021). A comparative assessment of in vitro cytotoxic activity and phytochemical profiling of Andrographis nallamalayana JL Ellis and Andrographis paniculata (Burm. f.) Nees using UPLC-QTOF-MS/MS approach. RSC Advances, 11(57), 35918–35936.
  • Gogoi, N., Chowdhury, P., Goswami, A. K., Das, A., Chetia, D., & J. M. D. Gogoi, B. (2020). Computational guided identification of a citrus flavonoid as potential inhibitor of SARS-CoV-2 main protease. Molecular Diversity, 25, 1–15.
  • Goyal, B., & Goyal, D. (2020). Targeting the dimerization of the main protease of coronaviruses: A potential broad-spectrum therapeutic strategy. ACS Combinatorial Science, 22(6), 297–305. https://doi.org/10.1021/acscombsci.0c00058
  • Grottesi, A., Bešker, N., Emerson, A., Manelfi, C., Beccari, A. R., Frigerio, F., Lindahl, E., Cerchia, C., & Talarico, C. (2020). Computational studies of SARS-CoV-2 3CLpro: Insights from MD simulations. International Journal of Molecular Sciences, 21(15), 5346. https://doi.org/10.3390/ijms21155346
  • Gupta, S., Do, Y., Lee, J. H., Lee, M., Han, J., Rhee, Y. H., & Park, J. J. C. A. E. J. (2014). Novel catalyst system for hydrostannation of alkynes. Chemistry (Weinheim an Der Bergstrasse, Germany), 20(5), 1267–1271. https://doi.org/10.1002/chem.201303057
  • Harvey, M. J., & De Fabritiis, G. (2009). An implementation of the smooth particle mesh Ewald method on GPU hardware. Journal of Chemical Theory and Computation, 5(9), 2371–2377. https://doi.org/10.1021/ct900275y
  • Hilgenfeld, R. (2014). From SARS to MERS: Crystallographic studies on coronaviral proteases enable antiviral drug design. The FEBS Journal, 281(18), 4085–4096. https://doi.org/10.1111/febs.12936
  • Hoffmann, M., Kleine-Weber, H., Schroeder, S., Krüger, N., Herrler, T., Erichsen, S., Schiergens, T. S., Herrler, G., Wu, N.-H., Nitsche, A., Müller, M. A., Drosten, C., & Pöhlmann, S. (2020). SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell, 181(2), 271–280.e278. https://doi.org/10.1016/j.cell.2020.02.052
  • Hu, Y., Ma, C., Szeto, T., Hurst, B., Tarbet, B., & Wang, J. J. (2021). Boceprevir, calpain inhibitors II and XII, and GC-376 have broad-spectrum antiviral activity against coronaviruses. ACS Infectious Diseases, 7(3), 586–597. https://doi.org/10.1021/acsinfecdis.0c00761
  • Jain, A. N. (2008). Bias, reporting, and sharing: computational evaluations of docking methods. Journal of Computer-Aided Molecular Design, 22(3–4), 201–212. https://doi.org/10.1007/s10822-007-9151-x
  • Jena, N. R., Pant, S., & Srivastava, H. K. (2021). Artificially expanded genetic information systems (AEGISs) as potent inhibitors of the RNA-dependent RNA polymerase of the SARS-CoV-2. Journal of Biomolecular Structure and Dynamics, 1–17. https://doi.org/10.1080/07391102.2021.1883112
  • Jorgensen, W. L., Maxwell, D. S., & Tirado-Rives, J. J. (1996). Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. Journal of the American Chemical Society, 118(45), 11225–11236. https://doi.org/10.1021/ja9621760
  • Kaldhi, D., Vodnala, N., Gujjarappa, R., Malakar, C., Nayak, S., Ravichandiran, V., Gupta, S., & Hazra, C. J. T. L. (2019). Organocatalytic oxidative synthesis of C2-functionalized benzoxazoles, naphthoxazoles, benzothiazoles and benzimidazoles. Tetrahedron Letters, 60(3), 223–229. https://doi.org/10.1016/j.tetlet.2018.12.017
  • Khan, M. I., Khan, Z. A., Baig, M. H., Ahmad, I., Farouk, A.-E., Song, Y. G., & Dong, J.-J J. P. O. (2020). Comparative genome analysis of novel coronavirus (SARS-CoV-2) from different geographical locations and the effect of mutations on major target proteins: An in silico insight. PLoS One, 15(9), e0238344. https://doi.org/10.1371/journal.pone.0238344
  • Kräutler, V., van Gunsteren, W. F., & Hünenberger, P. H. (2001). A fast SHAKE algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. Journal of Computational Chemistry, 22(5), 501–508. https://doi.org/10.1002/1096-987X(20010415)22:5<501::AID-JCC1021>3.0.CO;2-V
  • Kuba, K., Imai, Y., Rao, S., Gao, H., Guo, F., Guan, B., Huan, Y., Yang, P., Zhang, Y., Deng, W., Bao, L., Zhang, B., Liu, G., Wang, Z., Chappell, M., Liu, Y., Zheng, D., Leibbrandt, A., … Wada, T. (2005). A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nature Medicine, 11(8), 875–879. https://doi.org/10.1038/nm1267
  • Kumar, L., & Verma, R. J. L. (2018). Design, drug likeness and molecular docking of novel molecules for anti-tubercular activity, Latin American Journal of Pharmacy, 37(4), 759–767.
  • Lahlou, M. (2013). The success of natural products in drug discovery. Pharmacology & Pharmacy, 4, 17-31.
  • Lahlou, M. J. E. (2007). Screening of natural products for drug discovery. Expert Opinion on Drug Discovery, 2(5), 697–705. https://doi.org/10.1517/17460441.2.5.697
  • Lan, J., Ge, J., Yu, J., Shan, S., Zhou, H., Fan, S., Zhang, Q., Shi, X., Wang, Q., Zhang, L., & Wang, X. (2020). Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature, 581(7807), 215–220. https://doi.org/10.1038/s41586-020-2180-5
  • Lee, J., Worrall, L. J., Vuckovic, M., Rosell, F. I., Gentile, F., Ton, A.-T., Caveney, N. A., Ban, F., Cherkasov, A., & Paetzel, M. J. N. c. (2020). Crystallographic structure of wild-type SARS-CoV-2 main protease acyl-enzyme intermediate with physiological C-terminal autoprocessing site. Nature Communications, 11(1), 1–9.
  • Li, R., Narita, R., Ouda, R., Kimura, C., Nishimura, H., Yatagai, M., Fujita, T., & Watanabe, T. J. R. A. (2018). Structure-dependent antiviral activity of catechol derivatives in pyroligneous acid against the encephalomycarditis virus. RSC Advances, 8(63), 35888–35896. https://doi.org/10.1039/C8RA07096B
  • Ma, C., Sacco, M. D., Hurst, B., Townsend, J. A., Hu, Y., Szeto, T., Zhang, X., Tarbet, B., Marty, M. T., Chen, Y., & Wang, J. (2020). Boceprevir, GC-376, and calpain inhibitors II, XII inhibit SARS-CoV-2 viral replication by targeting the viral main protease. Cell Research, 30(8), 678–692. https://doi.org/10.1038/s41422-020-0356-z
  • Majumder, M., Debnath, S., Gajbhiye, R. L., Saikia, R., Gogoi, B., Samanta, S. K., Das, D. K., Biswas, K., Jaisankar, P., & Mukhopadhyay, R. J. S. r. (2019). Ricinus communis L. fruit extract inhibits migration/invasion, induces apoptosis in breast cancer cells and arrests tumor progression in vivo. Scientific Reports,9(1), 1–14.
  • Mandal, S. P., Mithuna, M., Garg, A., Sahetya, S. S., Nagendra, S. R., Sripad, H. S., Manjunath, M. M., Sitaram, S., Soni, M., Baig, R. N., Kumar, S. V., & Kumar, B. R. P. (2016). Novel rhodanines with anticancer activity: Design, synthesis and CoMSIA study. RSC Advances, 6(63), 58641–58653. https://doi.org/10.1039/C6RA08785J
  • Mark, P., & Nilsson, L. J. (2001). Structure and dynamics of the TIP3P, SPC, and SPC/E water models at 298 K. The Journal of Physical Chemistry A, 105(43), 9954–9960. https://doi.org/10.1021/jp003020w
  • Markowitz, M., Saag, M., Powderly, W. G., Hurley, A. M., Hsu, A., Valdes, J. M., Henry, D., Sattler, F., Marca, A. L., & Leonard, J. M. (1995). A preliminary study of ritonavir, an inhibitor of HIV-1 protease, to treat HIV-1 infection. The New England Journal of Medicine, 333(23), 1534–1540. https://doi.org/10.1056/NEJM199512073332204
  • Nandi, D., Besra, S. E., Vedasiromoni, J. R., Giri, V. S., Rana, P., & Jaisankar, P. J. (2012). Anti-leukemic activity of Wattakaka volubilis leaf extract against human myeloid leukemia cell lines. Journal of Ethnopharmacology, 144(3), 466–473. https://doi.org/10.1016/j.jep.2012.08.021
  • Pachetti, M., Marini, B., Benedetti, F., Giudici, F., Mauro, E., Storici, P., Masciovecchio, C., Angeletti, S., Ciccozzi, M., & Gallo, R. C. J. (2020). Emerging SARS-CoV-2 mutation hot spots include a novel RNA-dependent-RNA polymerase variant. Journal of Translational Medicine, 18(1), 1–9.
  • Paul, K., Chakraborty, S., Mallick, P., Bhattacharjee, P., Pal, T. K., Chatterjee, N., & Chakrabarti, S. J. (2021). Supercritical carbon dioxide extracts of small cardamom and yellow mustard seeds have fasting hypoglycaemic effects: Diabetic rat, predictive iHOMA2 models and molecular docking study. The British Journal of Nutrition, 125(4), 377–388. https://doi.org/10.1017/S000711452000286X
  • Pavan, M., Bolcato, G., Bassani, D., Sturlese, M., Moro, S. J., & Chemistry, M. (2021). Supervised molecular dynamics (SuMD) Insights into the mechanism of action of SARS-CoV-2 main protease inhibitor PF-07321332. Journal of Enzyme Inhibition and Medicinal Chemistry, 36(1), 1646–1650. https://doi.org/10.1080/14756366.2021.1954919
  • Putta, V. R. K., Vodnala, N., Gujjarappa, R., Tyagi, U., Garg, A., Gupta, S., Pujar, P. P., & Malakar, C. C. (2020). Reagent-controlled divergent synthesis of 2-amino-1,3-benzoxazines and 2-amino-1,3-benzothiazines. The Journal of Organic Chemistry, 85(2), 380–396. https://doi.org/10.1021/acs.joc.9b02384
  • Rizvi, S. M. D., Hussain, T., Moin, A., Dixit, S. R., Mandal, S. P., Adnan, M., Jamal, Q. M. S., Sharma, D. C., Alanazi, A. S., & Unissa, R. J. P. (2021). Identifying the most potent dual-targeting compound (s) against 3CL protease and NSP15 exonuclease of SARS-CoV-2 from Nigella sativa: Virtual screening via physicochemical properties. Docking and Dynamic Simulation Analysis, 9(10), 1814.
  • Romano, J. D., & Tatonetti, N. P. J. (2019). Informatics and computational methods in natural product drug discovery: A review and perspectives. Frontiers in Genetics, 10(368), 1–16.
  • Sacco, M. D., Ma, C., Lagarias, P., Gao, A., Townsend, J. A., Meng, X., Dube, P., Zhang, X., Hu, Y., & Kitamura, N. J. S. A. (2020). Structure and inhibition of the SARS-CoV-2 main protease reveal strategy for developing dual inhibitors against Mpro and cathepsin L. Science Advances, 6(50), eabe0751.
  • Sahlgren, C., Meinander, A., Zhang, H., Cheng, F., Preis, M., Xu, C., Salminen, T. A., Toivola, D., Abankwa, D., Rosling, A., Karaman, D. Ş., Salo-Ahen, O. M. H., Österbacka, R., Eriksson, J. E., Willför, S., Petre, I., Peltonen, J., Leino, R., … Johnson, M. (2017). Tailored approaches in drug development and diagnostics: From molecular design to biological model systems. Advanced Healthcare Materials, 6(21), 1700258. https://doi.org/10.1002/adhm.201700258
  • Shin, D., Mukherjee, R., Grewe, D., Bojkova, D., Baek, K., Bhattacharya, A., Schulz, L., Widera, M., Mehdipour, A. R., Tascher, G., Geurink, P. P., Wilhelm, A., van der Heden van Noort, G. J., Ovaa, H., Müller, S., Knobeloch, K.-P., Rajalingam, K., Schulman, B. A., … Cinatl, J. (2020). Papain-like protease regulates SARS-CoV-2 viral spread and innate immunity. Nature, 587(7835), 657–662. https://doi.org/10.1038/s41586-020-2601-5
  • Singh, R., Bhardwaj, V. K., Das, P., & Purohit, R. (2021). A computational approach for rational discovery of inhibitors for non-structural protein 1 of SARS-CoV-2. Computers in Biology and Medicine, 135, 104555. https://doi.org/10.1016/j.compbiomed.2021.104555
  • Singh, R., Bhardwaj, V. K., Sharma, J., Kumar, D., & Purohit, R. (2021). Identification of potential plant bioactive as SARS-CoV-2 spike protein and human ACE2 fusion inhibitors. Computers in Biology and Medicine, 136, 104631. https://doi.org/10.1016/j.compbiomed.2021.104631
  • Singh, R., Bhardwaj, V. K., Sharma, J., Purohit, R., & Kumar, S. J. (2021). In-silico evaluation of bioactive compounds from tea as potential SARS-CoV-2 nonstructural protein 16 inhibitors. Journal of Traditional and Complementary Medicine. in press. https://doi.org/10.1016/j.jtcme.2021.05.005
  • Thakur, A., Patwa, J., Pant, S., Sharma, A., & Flora, S. J. S. r. (2021). Interaction study of monoisoamyl dimercaptosuccinic acid with bovine serum albumin using biophysical and molecular docking approaches. Scientific Reports, 11(1), 1–14.
  • Ullrich, S., Nitsche, C. J. B., & Letters, M. C. (2020). The SARS-CoV-2 main protease as drug target. Bioorganic & Medicinal Chemistry Letters, 30(17), 127377. https://doi.org/10.1016/j.bmcl.2020.127377
  • Verma, P., Tiwari, M., & Tiwari, V. (2018). In silico high-throughput virtual screening and molecular dynamics simulation study to identify inhibitor for AdeABC efflux pump of Acinetobacter baumannii. Journal of Biomolecular Structure & Dynamics, 36(5), 1182–1194. https://doi.org/10.1080/07391102.2017.1317025
  • Wan, S., Bhati, A. P., Zasada, S. J., & Coveney, P. V. J. I. F. (2020). Rapid, accurate, precise and reproducible ligand-protein binding free energy prediction. Interface Focus, 10(6), 20200007. https://doi.org/10.1098/rsfs.2020.0007
  • White, M. A., Lin, W., & Cheng, X. J. (2020). Discovery of COVID-19 inhibitors targeting the SARS-CoV-2 Nsp13 helicase. The Journal of Physical Chemistry Letters, 11(21), 9144–9151. https://doi.org/10.1021/acs.jpclett.0c02421
  • Yadav, R., Imran, M., Dhamija, P., Chaurasia, D. K., & Handu, S. (2021). Virtual screening, ADMET prediction and dynamics simulation of potential compounds targeting the main protease of SARS-CoV-2. Journal of Biomolecular Structure & Dynamics, 39(17), 6617–6632. https://doi.org/10.1080/07391102.2020.1796812
  • Yathisha, U. G., Srinivasa, M. G., Siddappa Bc, R., Mandal, S. P., Dixit, S. R., & Pujar, G. (2021). Isolation and characterization of ACE‐I inhibitory peptides from ribbonfish for a potential inhibitor of the main protease of SARS‐CoV‐2; an in‐silico analysis. Proteins: Structure, Function, and Bioinformatics, 1-11. https://doi.org/10.1002/prot.26291
  • Yu, Y., Zheng, J., Cao, L., Li, S., Li, X., Zhou, H.-B., Liu, X., Wu, S., & Dong, C. J. R. (2017). Furan-carboxamide derivatives as novel inhibitors of lethal H5N1 influenza A viruses. RSC Advances, 7(16), 9620–9627. https://doi.org/10.1039/C7RA00305F
  • Zemtsova, M., Zimichev, A., Trakhtenberg, P., Klimochkin, Y. N., Leonova, M., Balakhnin, S., Bormotov, N., Serova, O., & Belanov, E. J. P. C. J. (2011). Synthesis and antiviral activity of several quinoline derivatives. Pharmaceutical Chemistry Journal, 45(5), 267.
  • Zhang, L., Lin, D., Sun, X., Curth, U., Drosten, C., Sauerhering, L., Becker, S., Rox, K., & Hilgenfeld, R. J. S. (2020). Crystal structure of SARS-CoV-2 main protease provides a basis for design of improved α-ketoamide inhibitors. Science (New York, N.Y.), 368(6489), 409–412. https://doi.org/10.1126/science.abb3405
  • Zhang, M.-Z., Chen, Q., & Yang, J. E. (2015). A review on recent developments of indole-containing antiviral agents. European Journal of Medicinal Chemistry, 89, 421–441. https://doi.org/10.1016/j.ejmech.2014.10.065
  • Zhang, R., Li, Y., Zhang, A. L., Wang, Y., & Molina, M. J. (2020). Identifying airborne transmission as the dominant route for the spread of COVID-19. Proceedings of the National Academy of Sciences of the United States of America, 117(26), 14857–14863. https://doi.org/10.1073/pnas.2009637117
  • Zhang, X., Perez-Sanchez, H., & Lightstone, F. J. (2017). A comprehensive docking and MM/GBSA rescoring study of ligand recognition upon binding antithrombin. Current Topics in Medicinal Chemistry, 17(14), 1631–1639. https://doi.org/10.2174/1568026616666161117112604
  • Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., & Shi, W. (2020). A novel coronavirus from patients with pneumonia in China, 2019. New England Journal of Medicine, 8, 727-733.

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.