Home Life Sciences In vitro acetylcholinesterase, tyrosinase inhibitory potentials of secondary metabolites from Euphorbia schimperiana and Euphorbia balsamifera
Article
Licensed
Unlicensed Requires Authentication

In vitro acetylcholinesterase, tyrosinase inhibitory potentials of secondary metabolites from Euphorbia schimperiana and Euphorbia balsamifera

  • Salha M. Aljubiri ORCID logo EMAIL logo , Eman Abd Elsalam , Faten K. Abd El Hady , Mohamed O. Radwan ORCID logo , Abdulrahman I. Almansour and Kamel H. Shaker
Published/Copyright: November 3, 2022

Abstract

Acetylcholinesterase, tyrosinase, and α-glucosidase inhibition activities of Euphorbia schimperiana and Euphorbia balsamifera extracts, fractions, and available pure compounds were evaluated for the first time. Acetylcholinesterase assay revealed a significant inhibitory activity of E. balsamifera total extract and n-hexane fraction with 47.7% and 43.3%, respectively, compared to the reference drug, which was 75%. The n-butanol fraction demonstrated tyrosinase inhibitory activity for E. balsamifera and E. schimperiana with 36.7% and 29.7%, respectively, compared to 60% for the reference drug. Quercetin-3-O-α-glucuronide, quercetin-3-O-β-D-glucuronide-methyl ester, quercetin-3-O-α-L-rhamnoside, 3,3′-di-O-methyl ellagic acid, 3,3′-di-O-methyl-ellagic acid-4-β-D-xylopyranoside, and 4-O-ethyl gallic acid were identified from E. schimperiana while quercetin-3-O-glucopyranoside and isoorientin were determined from E. balsamifera. The AChE inhibitory effect of pure compounds exhibited promising activity, where 4-O-ethylgallic acid demonstrated 51.1%, while the highest tyrosinase inhibition was demonstrated by isoorientin with 50.6% compared to the reference drug (60%). Finally, a molecular docking study was performed for the most promising AChE and tyrosinase inhibitors. The extracts, fractions, and isolated compounds showed no α-glucosidase inhibitory activity.


Corresponding author: Salha M. Aljubiri, Department of Chemistry, College of Science, University of Bisha, Bisha 61922, P.O. Box 551, Saudi Arabia; and Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia, E-mail:

Award Identifier / Grant number: The initiative of DSR Graduate Students Research Support (GSR)

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work was funded by Deanship of scientific research in King Saud University and supporting this research through the initiative of DSR Graduate Students Research Support (GSR).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

1. Almasieh, M, MacIntyre, JN, Pouliot, M, Casanova, C, Vaucher, E, Kelly, MEM, et al.. Acetylcholinesterase inhibition promotes retinal vasoprotection and increases ocular blood flow in experimental glaucoma. Investig Ophthalmol Vis Sci 2013;54:3171–83. https://doi.org/10.1167/iovs.12-11481.Search in Google Scholar PubMed

2. Murray, A, Faraoni, M, Castro, M, Alza, N, Cavallaro, V. Natural AChE inhibitors from plants and their contribution to Alzheimer’s disease therapy. Curr Neuropharmacol 2013;11:388–413. https://doi.org/10.2174/1570159x11311040004.Search in Google Scholar

3. Patel, SS, Attard, A, Jacobsen, P, Shergill, S. Acetylcholinesterase Inhibitors (AChEI’s) for the treatment of visual hallucinations in schizophrenia: a review of the literature. BMC Psychiatr 2010;10:69. https://doi.org/10.1186/1471-244x-10-69.Search in Google Scholar PubMed PubMed Central

4. Mohammad, D, Chan, P, Bradley, J, Lanctôt, K, Herrmann, N. Acetylcholinesterase inhibitors for treating dementia symptoms – a safety evaluation. Expert Opin Drug Saf 2017;16:1009–19. https://doi.org/10.1080/14740338.2017.1351540.Search in Google Scholar PubMed

5. Mimica, N, Presečki, P. Side effects of approved antidementives. Psychiatr Danub 2009;21:108–13.Search in Google Scholar

6. Körner, A, Pawelek, J. Mammalian tyrosinase catalyzes three reactions in the biosynthesis of melanin. Science 1982;217:1163–5.10.1126/science.6810464Search in Google Scholar PubMed

7. Brenner, M, Hearing, VJ. The protective role of melanin against UV damage in human skin. Photochem Photobiol 2008;84:539–49. https://doi.org/10.1111/j.1751-1097.2007.00226.x.Search in Google Scholar PubMed PubMed Central

8. Ebanks, JP, Wickett, RR, Boissy, RE. Mechanisms regulating skin pigmentation: the rise and fall of complexion coloration. Int J Mol Sci 2009;10:4066–87. https://doi.org/10.3390/ijms10094066.Search in Google Scholar PubMed PubMed Central

9. Fahn, S, Sulzer, D. Neurodegeneration and neuroprotection in Parkinson disease. NeuroRx 2004;1:139–54. https://doi.org/10.1602/neurorx.1.1.139.Search in Google Scholar PubMed PubMed Central

10. Chen, CY, Kuo, PL, Chen, YH, Huang, JC, Ho, ML, Lin, RJ, et al.. Tyrosinase inhibition, free radical scavenging, antimicroorganism and anticancer proliferation activities of Sapindus mukorossi extracts. J Taiwan Inst Chem Eng 2010;41:129–35. https://doi.org/10.1016/j.jtice.2009.08.005.Search in Google Scholar

11. Shiino, M, Watanabe, Y, Umezawa, K. Synthesis of N-substituted N-nitrosohydroxylamines as inhibitors of mushroom tyrosinase. Bioorg Med Chem 2001;9:1233–40. https://doi.org/10.1016/s0968-0896(01)00003-7.Search in Google Scholar PubMed

12. Bolen, S, Feldman, L, Vassy, J, Wilson, L, Yeh, HC, Marinopoulos, S, et al.. Systematic review: comparative effectiveness and safety of oral medications for type 2 diabetes mellitus. Ann Intern Med 2007;147:386–99. https://doi.org/10.7326/0003-4819-147-6-200709180-00178.Search in Google Scholar PubMed

13. Fujisawa, T, Ikegami, H, Inoue, K, Kawabata, Y, Ogihara, T. Effect of two alpha-glucosidase inhibitors, voglibose and acarbose, on postprandial hyperglycemia correlates with subjective abdominal symptoms. Metabolism 2005;54:387–90. https://doi.org/10.1016/j.metabol.2004.10.004.Search in Google Scholar PubMed

14. Ajmal Shah, M, Khalil, R, Ul-Haq, Z, Panichayupakaranant, P. α-Glucosidase inhibitory effect of rhinacanthins-rich extract from Rhinacanthus nasutus leaf and synergistic effect in combination with acarbose. J Funct Foods 2017;36:325–31. https://doi.org/10.1016/j.jff.2017.07.021.Search in Google Scholar

15. Zhou, J, Zhang, L, Meng, Q, Wang, Y, Long, P, Ho, C-T, et al.. Roasting improves the hypoglycemic effects of a large-leaf yellow tea infusion by enhancing the levels of epimerized catechins that inhibit α-glucosidase. Food Funct 2018;9:5162–8. https://doi.org/10.1039/c8fo01429a.Search in Google Scholar PubMed

16. McRae, J, Yang, Q, Crawford, R, Palombo, E. Review of the methods used for isolating pharmaceutical lead compounds from traditional medicinal plants. Environmentalist 2007;27:165–74. https://doi.org/10.1007/s10669-007-9024-9.Search in Google Scholar

17. Fellows, L, Scofield, A. Chemical diversity in plants. In: Intellectual property rights and biodiversity conservation. UK: Cambridge University Press; 1995:19–44 pp.10.1017/CBO9780511623417.003Search in Google Scholar

18. Harvey, AL. Natural products in drug discovery. Drug Discov Today 2008;13:894–901. https://doi.org/10.1016/j.drudis.2008.07.004.Search in Google Scholar PubMed

19. Ahmad, S, Zeb, A, Ayaz, M, Murkovic, M. Characterization of phenolic compounds using UPLC–HRMS and HPLC–DAD and anti-cholinesterase and anti-oxidant activities of Trifolium repens L. leaves. Eur Food Res Technol 2020;246:485–96. https://doi.org/10.1007/s00217-019-03416-8.Search in Google Scholar

20. Chen, H, Liang, Q, Zhou, X, Wang, X. Preparative separation of the flavonoid fractions from Periploca forrestii Schltr. ethanol extracts using macroporous resin combined with HPLC analysis and evaluation of their biological activities. J Separ Sci 2019;42:650–61. https://doi.org/10.1002/jssc.201800422.Search in Google Scholar PubMed

21. Zhao, Y, Wang, D, Bais, S, Wang, H. Modulation of pro-inflammatory mediators by eugenol in AlCl3 induced dementia in rats. Int J Pharmacol 2019;15:457–64. https://doi.org/10.3923/ijp.2019.457.464.Search in Google Scholar

22. Wickens, GE, Burkill, HM. The useful plants of West Tropical Africa. Kew Bull 1986;41:471. https://doi.org/10.2307/4102963.Search in Google Scholar

23. Bramwell, D, Bramwell, ZI. Wild flowers of the Canary Islands, 2nd ed. Madrid: Editorial Rueda S.L.; 2001.Search in Google Scholar

24. Salehi, B, Iriti, M, Vitalini, S, Antolak, H, Pawlikowska, E, Kręgiel, D, et al.. Euphorbia-derived natural products with potential for use in health maintenance. Biomolecules 2019;9:337. https://doi.org/10.3390/biom9080337.Search in Google Scholar PubMed PubMed Central

25. Shi, QW, Su, XH, Kiyota, H. Chemical and pharmacological research of the plants in genus Euphorbia. Chem Rev 2008;108:4295–327. https://doi.org/10.1021/cr078350s.Search in Google Scholar PubMed

26. Hohmann, J, Rédei, D, Forgo, P, Molnár, J, Dombi, G, Zorig, T. Jatrophane diterpenoids from Euphorbia mongolica as modulators of the multidrug resistance of L5128 mouse lymphoma cells. J Nat Prod 2003;66:976–9. https://doi.org/10.1021/np030036f.Search in Google Scholar PubMed

27. Pisano, MB, Cosentino, S, Viale, S, Spanò, D, Corona, A, Esposito, F, et al.. Biological activities of aerial parts extracts of Euphorbia characias. Biomed Res Int 2016;2016:1–11. https://doi.org/10.1155/2016/1538703.Search in Google Scholar PubMed PubMed Central

28. Pintus, F, Spanò, D, Mascia, C, Macone, A, Floris, G, Medda, R. Acetylcholinesterase inhibitory and antioxidant properties of Euphorbia characias latex. Nat Prod 2013;7:147–51.Search in Google Scholar

29. Pintus, F, Spanò, D, Corona, A, Medda, R. Antityrosinase activity of Euphorbia characias extracts. PeerJ 2015;2015:e1305. https://doi.org/10.7717/peerj.1305.Search in Google Scholar PubMed PubMed Central

30. Sheliya, MA, Rayhana, B, Ali, A, Pillai, KK, Aeri, V, Sharma, M, et al.. Inhibition of α-glucosidase by new prenylated flavonoids from Euphorbia hirta L. herb. J Ethnopharmacol 2015;176:1–8. https://doi.org/10.1016/j.jep.2015.10.018.Search in Google Scholar PubMed

31. Aljubiri, SM, Mahgoub, SA, Almansour, AI, Shaaban, M, Shaker, KH. Isolation of diverse bioactive compounds from Euphorbia balsamifera: cytotoxicity and antibacterial activity studies. Saudi J Biol Sci 2021;28:417–26. https://doi.org/10.1016/j.sjbs.2020.10.025.Search in Google Scholar PubMed PubMed Central

32. Aljubiri, SM, Mahmoud, K, Mahgoub, SA, Almansour, AI, Shaker, KH. Bioactive compounds from Euphorbia schimperiana with cytotoxic and antibacterial activities. South Afr J Bot 2021;141:357–66. https://doi.org/10.1016/j.sajb.2021.05.021.Search in Google Scholar

33. Khan, I, Nisar, M, Khan, N, Saeed, M, Nadeem, S, Fazal-Ur-Rehman, et al.. Structural insights to investigate conypododiol as a dual cholinesterase inhibitor from Asparagus adscendens. Fitoterapia 2010;81:1020–5. https://doi.org/10.1016/j.fitote.2010.06.022.Search in Google Scholar PubMed

34. Kim, YJ. Antimelanogenic and antioxidant properties of gallic acid. Biol Pharm Bull 2007;30:1052–5. https://doi.org/10.1248/bpb.30.1052.Search in Google Scholar PubMed

35. Dong, HQ, Li, M, Zhu, F, Liu, FL, Huang, JB. Inhibitory potential of trilobatin from Lithocarpus polystachyus Rehd against α-glucosidase and α-amylase linked to type 2 diabetes. Food Chem 2012;130:261–6. https://doi.org/10.1016/j.foodchem.2011.07.030.Search in Google Scholar

36. Cheung, J, Rudolph, MJ, Burshteyn, F, Cassidy, MS, Gary, EN, Love, J, et al.. Structures of human acetylcholinesterase in complex with pharmacologically important ligands. J Med Chem 2012;55:10282–6. https://doi.org/10.1021/jm300871x.Search in Google Scholar PubMed

37. Ismaya, WT, Rozeboom, HJ, Weijn, A, Mes, JJ, Fusetti, F, Wichers, HJ, et al.. Crystal structure of Agaricus bisporus mushroom tyrosinase: identity of the tetramer subunits and interaction with tropolone. Biochemistry 2011;50:5477–86. https://doi.org/10.1021/bi200395t.Search in Google Scholar PubMed

38. Mingle, D, Ospanov, M, Radwan, MO, Ashpole, N, Otsuka, M, Ross, SA, et al.. First in class (S,E)-11-[2-(arylmethylene)hydrazono]-PBD analogs as selective CB2 modulators targeting neurodegenerative disorders. Med Chem Res 2021;30:98–108. https://doi.org/10.1007/s00044-020-02640-2.Search in Google Scholar PubMed PubMed Central

39. El-Shaheny, R, Radwan, MO, Belal, F, Yamada, K. Pentabromobenzyl-RP versus triazole-HILIC columns for separation of the polar basic analytes famotidine and famotidone: LC method development combined with in silico tools to follow the potential consequences of famotidine gastric instability. J Pharm Biomed Anal 2020;186:113305. https://doi.org/10.1016/j.jpba.2020.113305.Search in Google Scholar PubMed

40. Jamila, N, Khairuddean, M, Yeong, KK, Osman, H, Murugaiyah, V. Cholinesterase inhibitory triterpenoids from the bark of Garcinia hombroniana. J Enzym Inhib Med Chem 2015;30:133–9. https://doi.org/10.3109/14756366.2014.895720.Search in Google Scholar PubMed

41. Ahmad, Z, Mehmood, S, Ifzal, R, Malik, A, Afza, N, Ashraf, M, et al.. A new ursane-type triterpenoid from Salvia santolinifolia. Turk J Chem 2007;31:495–501.Search in Google Scholar

42. Xiao, J. Dietary flavonoid aglycones and their glycosides: which show better biological significance? Crit Rev Food Sci Nutr 2017;57:1874–905. https://doi.org/10.1080/10408398.2015.1032400.Search in Google Scholar PubMed

43. Taslimi, P. In vitro inhibitory effects of some acetophenone derivatives on some metabolic enzymes and molecular docking. Arch Pharm (Weinheim) 2020;353:2000210. https://doi.org/10.1002/ardp.202000210.Search in Google Scholar PubMed

44. Kiasalari, Z, Heydarifard, R, Khalili, M, Afshin-Majd, S, Baluchnejadmojarad, T, Zahedi, E, et al.. Ellagic acid ameliorates learning and memory deficits in a rat model of Alzheimer’s disease: an exploration of underlying mechanisms. Psychopharmacology (Berl) 2017;234:1841–52. https://doi.org/10.1007/s00213-017-4589-6.Search in Google Scholar PubMed

45. Ding, X, Ouyang, MA, Liu, X, Wang, RZ. Acetylcholinesterase inhibitory activities of flavonoids from the leaves of Ginkgo biloba against brown planthopper. J Chem 2013;2013:1–4. https://doi.org/10.1155/2013/645086.Search in Google Scholar

46. Jung, M, Park, M. Acetylcholinesterase inhibition by flavonoids from Agrimonia pilosa. Molecules 2007;12:2130–9. https://doi.org/10.3390/12092130.Search in Google Scholar PubMed PubMed Central

47. Choi, JS, Islam, MN, Ali, MY, Kim, YM, Park, HJ, Sohn, HS, et al.. The effects of C-glycosylation of luteolin on its antioxidant, anti-Alzheimer’s disease, anti-diabetic, and anti-inflammatory activities. Arch Pharm Res 2014;37:1354–63. https://doi.org/10.1007/s12272-014-0351-3.Search in Google Scholar PubMed

48. Panzella, L, Napolitano, A. Natural and bioinspired phenolic compounds as tyrosinase inhibitors for the treatment of skin hyperpigmentation: recent Advances. Cosmetics 2019;6:57. https://doi.org/10.3390/cosmetics6040057.Search in Google Scholar

49. Nam, SH, Park, J, Jun, W, Kim, D, Ko, JA, Abd El-Aty, AM, et al.. Transglycosylation of gallic acid by using Leuconostoc glucansucrase and its characterization as a functional cosmetic agent. AMB Express 2017;7:224. https://doi.org/10.1186/s13568-017-0523-x.Search in Google Scholar PubMed PubMed Central

50. Kumar, KJS, Vani, MG, Wang, SY, Liao, JW, Hsu, LS, Yang, HL, et al.. In vitro and in vivo studies disclosed the depigmenting effects of gallic acid: a novel skin lightening agent for hyperpigmentary skin diseases. BioFactors 2013;39:259–70. https://doi.org/10.1002/biof.1064.Search in Google Scholar PubMed

Received: 2021-06-22
Accepted: 2022-10-14
Published Online: 2022-11-03
Published in Print: 2023-05-25

© 2022 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 30.12.2025 from https://www.degruyterbrill.com/document/doi/10.1515/znc-2021-0178/html
Scroll to top button