Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter November 10, 2021

Essential oils of Uvaria boniana – chemical composition, in vitro bioactivity, docking, and in silico ADMET profiling of selective major compounds

  • Son Ninh The EMAIL logo , Anh Le Tuan , Thuy Dinh Thi Thu , Luyen Nguyen Dinh , Tuyen Tran Thi and Hai Pham-The ORCID logo EMAIL logo

Abstract

Phytochemical investigation applying GC (gas chromatography)-MS (mass spectrometry)/GC-FID (flame ionization detection) on the hydro-distilled essential oils of the Vietnamese medicinal plant Uvaria boniana leaf and twig lead to the detection of 35 constituents (97.36%) in the leaf oil and 52 constituents (98.75%) in the twig oil. Monoterpenes, monoterpenoids, sesquiterpenes, and sesquiterpenoids were characteristic of U. boniana essential oils. The leaf oil was represented by major components (E)-caryophyllene (16.90%), bicyclogermacrene (15.95%), α-humulene (14.96%), and linalool (12.40%), whereas four compounds α-cadinol (16.16%), epi-α-muurolol (10.19%), α-pinene (11.01%), and β-pinene (8.08%) were the main ones in the twig oil. As compared with the leaf oil, the twig oil was better in antimicrobial activity. With the same MIC value of 40 mg/mL, the twig oil successfully controlled the growth of Gram (+) bacterium Bacillus subtilis, Gram (−) bacterium Escherichia coli, fungus Aspergillus niger, and yeast Saccharomyces cerevisiae. In addition, both two oil samples have induced antiinflammatory activity with the IC50 values of 223.7–240.6 mg/mL in NO productive inhibition when BV2 cells had been stimulated by LPS. Docking simulations of four major compounds of U. boniana twig oil on eight relevant antibacterial targets revealed that epi-α-muurolol and α-cadinol are moderate inhibitors of E. coli DNA gyrase subunit B, penicillin binding protein 2X and penicillin binding protein 3 of Pseudomonas aeruginosa with similar free binding energies of −30.1, −29.3, and −29.3 kJ/mol, respectively. Furthermore, in silico ADMET studies indicated that all four docked compounds have acceptable oral absorption, low metabolism, and appropriated toxicological profile to be considered further as drug candidates.


Corresponding author: Son Ninh The, Institute of Chemistry, Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet, Caugiay, Hanoi, Vietnam, E-mail: ; and Hai Pham-The, Hanoi University of Pharmacy, 13–15 Le Thanh Tong, Hoan Kiem, Hanoi, Vietnam, E-mail:

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

  2. Research funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.

  3. Conflict of interest statement: The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

1. Ayedoun, MA, Moudachirou, M, Adeoti, BS, Menut, C, Lamaty, G, Bessiére, J-M. Aromatic plants of tropical West Africa. VII. Essential oil of leaf and root bark of Uvaria chamae P. Beauv. from Benin. J Essent Oil Res 1999;11:23–6. https://doi.org/10.1080/10412905.1999.9701060.Search in Google Scholar

2. Suthiphasilp, V, Maneerat, W, Andersen, RJ, Patrick, BO, Phukhatmuen, P, Pyne, SG, et al.. Uvarialuridols A-C, three new polyoxygenated cyclohexenes from the twig and leaf extracts of Uvaria lurida. Fitoterapia 2019;138:104340. https://doi.org/10.1016/j.fitote.2019.104340.Search in Google Scholar

3. Macabeo, APG, Rubio, PYM, Higuchi, T, Umezawa, N, Faderl, C, Budde, S, et al.. Polyoxygenated seco-cyclohexenes and other constituents from Uvaria valderramensis. Biochem Systemat Ecol 2017;71:200–4. https://doi.org/10.1016/j.bse.2017.02.013.Search in Google Scholar

4. Pham, HH. Flora of Vietnam. Hanoi, Vietnam: Youth Publisher; 1999.Search in Google Scholar

5. Thang, T, Hoang, L, Tuan, N, Dai, D, Ogunwande, I, Hung, N. Analysis of the leaf essential oils of Uvaria grandiflora Roxb. ex Hornem. and Uvaria microcarpa Champ. ex Benth. (Annonaceae) from Vietnam. J Essent Oil Bear Plants 2017;20:496–501. https://doi.org/10.1080/0972060x.2017.1321503.Search in Google Scholar

6. Thomas, PS, Essien, EE. Antiglycation, antioxidant, and cytotoxic activities of Uvaria chamae root and essential oil composition. Nat Prod Res 2020;34:880–3. https://doi.org/10.1080/14786419.2018.1504048.Search in Google Scholar

7. Hisham, AK, Pieters, L, Schepens, P, Vlietinck, AJ. The root bark essential oil of Uvaria narum wall. J Essent Oil Res 1992;4:475–7. https://doi.org/10.1080/10412905.1992.9698112.Search in Google Scholar

8. Tam, NT, Tuan, NN, Trung, HV, My Chau, LT, Anh, DTT, Luu, HV. Chemical constituents from the leaves of Uvaria boniana in Viet Nam. Vietnam J Sci Technol 2019;57:538–43. https://doi.org/10.15625/2525-2518/57/5/13024.Search in Google Scholar

9. Chen, Z, Liu, Y-L, Xu, Q-M, Liu, J-Y, Duan, H-Q, Yang, S-L. New polyoxygenated cyclohexene and polyoxygenated seco-cyclohexene from Uvaria boniana. J Asian Nat Prod Res 2013;15:53–8. https://doi.org/10.1080/10286020.2012.743529.Search in Google Scholar

10. Khan, M, Khan, M, Abdullah, MMS, Al-Wahaibi, LH, Alkhathlan, HZ. Characterization of secondary metabolites of leaf and stem essential oils of Achillea fragrantissima from central region of Saudi Arabia. Arabian J Chem 2020;13:5254–61. https://doi.org/10.1016/j.arabjc.2020.03.004.Search in Google Scholar

11. Khan, M, Khan, ST, Khan, M, Mousa, AA, Mahmood, A, Alkhathlan, HZ. Chemical diversity in leaf and stem essential oils of Origanum vulgare L. and their effects on microbicidal activities. AMB Express 2019;9:176. https://doi.org/10.1186/s13568-019-0893-3.Search in Google Scholar

12. Khan, M, Khan, ST, Khan, NA, Mahmood, A, Al-Kedhairy, AA, Alkhathlan, HZ. The composition of the essential oil and aqueous distillate of Origanum vulgare L. growing in Saudi Arabia and evaluation of their antibacterial activity. Arabian J Chem 2018;11:1189–200. https://doi.org/10.1016/j.arabjc.2018.02.008.Search in Google Scholar

13. Adams, R. Identification of essential oil components by gas chromatography/mass spectrometry, 4th ed. IL, USA: Springer Nature; 2007.Search in Google Scholar

14. Siani, AC, Ramos, MFS, Menezes-de-Lima, O, Ribeiro-dos-Santos, R, Fernadez-Ferreira, E, Soares, ROA, et al.. Evaluation of anti-inflammatory-related activity of essential oils from the leaves and resin of species of Protium. J Ethnopharmacol 1999;66:57–69. https://doi.org/10.1016/s0378-8741(98)00148-2.Search in Google Scholar

15. Paolini, J, Muselli, A, Bernardini, A-F, Bighelli, A, Casanova, J, Costa, J. Thymol derivatives from essential oil of Doronicum corsicum L. Flavour Fragrance J 2007;22:479–87. https://doi.org/10.1002/ffj.1824.Search in Google Scholar

16. Mevy, J-P, Bessiere, J-M, Greff, S, Zombre, G, Viano, J. Composition of the volatile oil from the leaves of Ximenia americana L. Biochem Systemat Ecol 2006;34:549–53. https://doi.org/10.1016/j.bse.2006.01.007.Search in Google Scholar

17. Salido, S, Valenzuela, LR, Altarejos, J, Nogueras, M, Sánchez, A, Cano, E. Composition and infraspecific variability of Artemisia herba-alba from Southern Spain. Biochem Systemat Ecol 2004;32:265–77. https://doi.org/10.1016/j.bse.2003.09.002.Search in Google Scholar

18. Roslon, W, Wajs-Bonikowska, A, Geszprych, A, Osinska, E. Characteristics of essential oil from Young Shoots of Garden Angelica (Angelica archangelica L.). J Essent Oil Bear Plants 2016;19:1462–70. https://doi.org/10.1080/0972060x.2016.1238322.Search in Google Scholar

19. Son, NT, Oda, M, Hayashi, N, Yamaguchi, D, Kawagishi, Y, Takahashi, F, et al.. Antimicrobial activity of the constituents of Dalbergia tonkinensis and structural-bioactive highlights. Nat Prod Commun 2018;13:157–61. https://doi.org/10.1177/1934578x1801300212.Search in Google Scholar

20. Son, NT, Harada, K, Cuong, NM, Fukuyama, Y. Two new carboxyethylflavanones from the heartwood of Dalbergia tonkinensis and their antimicrobial activities. Nat Prod Commun 2017;12:1721–3. https://doi.org/10.1177/1934578x1701201115.Search in Google Scholar

21. Cuong, NM, Nhan, NT, Son, NT, Nghi, DH, Cuong, TD. Daltonkins A and B, two new carboxyethylflavanones from the heartwood of Dalbergia tonkinensis. Bull Kor Chem Soc 2017;38:1511–4. https://doi.org/10.1002/bkcs.11313.Search in Google Scholar

22. Dung, DT, Yen, PH, Nhiem, NX, Quang, TH, Tai, BH, Minh, CV, et al.. New acetylated terpenoids from Sponge Rhabdastrella providentiae inhibit NO production in LPS stimulated BV2 cells. Nat Prod Commun 2018;13:661–4. https://doi.org/10.1177/1934578x1801300602.Search in Google Scholar

23. Löwe, J, Amos, LA. Crystal structure of the bacterial cell-division protein FtsZ. Nature 1998;391:203–6. https://doi.org/10.1038/34472.Search in Google Scholar

24. Zhou, Y, Luo, H, Liu, Z, Yang, M, Pang, X, Sun, F, et al.. Structural Insight into the specific DNA template binding to DnaG primase in bacteria. Sci Rep 2017;7:659. https://doi.org/10.1038/s41598-017-00767-8.Search in Google Scholar

25. Heaslet, H, Harris, M, Fahnoe, K, Sarver, R, Putz, H, Chang, J, et al.. Structural comparison of chromosomal and exogenous dihydrofolate reductase from Staphylococcus aureus in complex with the potent inhibitor trimethoprim. Proteins 2009;76:706–17. https://doi.org/10.1002/prot.22383.Search in Google Scholar

26. Firczuk, M, Mucha, A, Bochtler, M. Crystal structures of active LytM. J Mol Biol 2005;354:578–90. https://doi.org/10.1016/j.jmb.2005.09.082.Search in Google Scholar

27. Surivet, J-P, Zumbrunn, C, Rueedi, G, Hubschwerlen, C, Bur, D, Bruyère, T, et al.. Design, synthesis, and characterization of novel tetrahydropyran-based bacterial topoisomerase inhibitors with potent anti-gram-positive activity. J Med Chem 2013;56:7396–415. https://doi.org/10.1021/jm400963y.Search in Google Scholar

28. Holdgate, GA, Tunnicliffe, A, Ward, WHJ, Weston, SA, Rosenbrock, G, Barth, PT, et al.. The entropic penalty of ordered water accounts for weaker binding of the antibiotic novobiocin to a resistant mutant of DNA gyrase: a thermodynamic and crystallographic study. Biochemistry 1997;36:9663–73. https://doi.org/10.1021/bi970294+.10.1021/bi970294+Search in Google Scholar PubMed

29. Gordon, E, Mouz, N, Duée, E, Dideberg, O. The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance 11 edited by R. Huber. J Mol Biol 2000;299:477–85. https://doi.org/10.1006/jmbi.2000.3740.Search in Google Scholar

30. Sainsbury, S, Bird, L, Rao, V, Shepherd, SM, Stuart, DI, Hunter, WN, et al.. Crystal structures of penicillin-binding protein 3 from Pseudomonas aeruginosa: comparison of native and antibiotic-bound forms. J Mol Biol 2011;405:173–84. https://doi.org/10.1016/j.jmb.2010.10.024.Search in Google Scholar

31. Dallakyan, S, Olson, AJ. Small-molecule library screening by docking with PyRx. Methods Mol Biol 2015;1263:243–50. https://doi.org/10.1007/978-1-4939-2269-7_19.Search in Google Scholar

32. Chemical Computing Group (CCG). Molecular operating environment (MOE). version 2015.10. Canada: Discovery Platform; 2015.Search in Google Scholar

33. Trott, O, Olson, AJ. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 2010;31:455–61. https://doi.org/10.1002/jcc.21334.Search in Google Scholar

34. Daina, A, Michielin, O, Zoete, V. SwissADME: a free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci Rep 2017;7:42717. https://doi.org/10.1038/srep42717.Search in Google Scholar

35. Yang, H, Lou, C, Sun, L, Li, J, Cai, Y, Wang, Z, et al.. AdmetSAR 2.0: web-service for prediction and optimization of chemical ADMET properties. Bioinformatics 2019;35:1067–9. https://doi.org/10.1093/bioinformatics/bty707.Search in Google Scholar

36. Silva, MH. Use of computational toxicology (CompTox) tools to predict in vivo toxicity for risk assessment. Regul Toxicol Pharmacol 2020;116:104724. https://doi.org/10.1016/j.yrtph.2020.104724.Search in Google Scholar

37. Cruciani, G, Pastor, M, Guba, W. VolSurf: a new tool for the pharmacokinetic optimization of lead compounds. Eur J Pharmaceut Sci 2000;11(2 Suppl):S29–39. https://doi.org/10.1016/s0928-0987(00)00162-7.Search in Google Scholar

38. Kim, S, Thiessen, PA, Bolton, EE, Chen, J, Fu, G, Gindulyte, A, et al.. PubChem substance and compound databases. Nucleic Acids Res 2016;44:D1202–13. https://doi.org/10.1093/nar/gkv951.Search in Google Scholar

39. Cabrera-Pérez, MÁ, Pham-The, H, Cervera, MF, Hernández-Armengol, R, Miranda-Pérez de Alejo, C, Brito-Ferrer, Y. Integrating theoretical and experimental permeability estimations for provisional biopharmaceutical classification: application to the WHO essential medicines. Biopharm Drug Dispos 2018;39:354–68. https://doi.org/10.1002/bdd.2152.Search in Google Scholar

40. Teague, SJ, Davis, AM, Leeson, PD, Oprea, T. The design of leadlike combinatorial libraries. Angew Chem Int Ed 1999;38:3743–8. https://doi.org/10.1002/(sici)1521-3773(19991216)38:24<3743::aid-anie3743>3.0.co;2-u.10.1002/(SICI)1521-3773(19991216)38:24<3743::AID-ANIE3743>3.0.CO;2-USearch in Google Scholar

41. Lipinski, CA, Lombardo, F, Dominy, BW, Feeney, PJ. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 1997;23:3–25. https://doi.org/10.1016/s0169-409x(96)00423-1.Search in Google Scholar

42. Martin, YC. A bioavailability score. J Med Chem 2005;48:3164–70. https://doi.org/10.1021/jm0492002.Search in Google Scholar

43. Thang, TD, Dai, DN, Hoi, TM, Ogunwande, IA. Chemical compositions of the leaf essential oils of some Annonaceae from Vietnam. J Essent Oil Res 2013;25:85–91. https://doi.org/10.1080/10412905.2012.755475.Search in Google Scholar

44. Singh, D, Bhardwaj, SV, Kumar, A, Kaushik, V, Mahajan, S, Satija, S. Antimicrobial activity and molecular docking studies of a sesquiterpenoid alcohol from leaf solvent extracts of Juniperus Communis L. Int J Green Pharm 2018;12:22–8.Search in Google Scholar

45. Šarac, Z, Matejić, JS, Stojanović-Radić, ZZ, Veselinović, JB, Džamić, AM, Bojović, S, et al.. Biological activity of Pinus nigra terpenes – evaluation of FtsZ inhibition by selected compounds as contribution to their antimicrobial activity. Comput Biol Med 2014;54:72–8. https://doi.org/10.1016/j.compbiomed.2014.08.022.Search in Google Scholar

46. Daisy, P, Mathew, S, Suveena, S, Rayan, NA. A novel terpenoid from Elephantopus scaber – antibacterial activity on Staphylococcus aureus: a substantiate computational approach. Int J Biomed Sci 2008;4:196–203.Search in Google Scholar

47. Collin, F, Karkare, S, Maxwell, A. Exploiting bacterial DNA gyrase as a drug target: current state and perspectives. Appl Microbiol Biotechnol 2011;92:479–97. https://doi.org/10.1007/s00253-011-3557-z.Search in Google Scholar

48. Sauvage, E, Kerff, F, Terrak, M, Ayala, JA, Charlier, P. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 2008;32:234–58. https://doi.org/10.1111/j.1574-6976.2008.00105.x.Search in Google Scholar

49. Chen, W, Zhang, Y-M, Davies, C. Penicillin-binding protein 3 is essential for growth of Pseudomonas aeruginosa. Antimicrob Agents Chemother 2017;61:e01651–16. https://doi.org/10.1128/AAC.01651-16.Search in Google Scholar

50. Taylor, PW. Alternative natural sources for a new generation of antibacterial agents. Int J Antimicrob Agents 2013;42:195–201. https://doi.org/10.1016/j.ijantimicag.2013.05.004.Search in Google Scholar

51. Ntie-Kang, F, Nyongbela, KD, Ayimele, GA, Shekfeh, S. “Drug-likeness” properties of natural compounds. Phys Sci Rev 2019;4:1–14. https://doi.org/10.1515/psr-2018-0169.Search in Google Scholar

52. Muegge, I. Selection criteria for drug-like compounds. Med Res Rev 2003;23:302–21. https://doi.org/10.1002/med.10041.Search in Google Scholar

53. Congreve, M, Carr, R, Murray, C, Jhoti, HA. A ‘rule of three’ for fragment-based lead discovery. Drug Discov Today 2003;8:876–7. https://doi.org/10.1016/s1359-6446(03)02831-9.Search in Google Scholar

54. Hai, P-T, Miguel, ÁC-P, Nguyen-Hai, N, Juan, AC-G, Bakhtiyor, R, Huong, L-T-T, et al.. In slico assessment of ADME properties: advances in caco-2 cell monolayer permeability modeling. Curr Top Med Chem 2018;18:2209–29.Search in Google Scholar

55. Juan, AC-G, Gerardo, MC-M, Huong, L-T-T, Hai, P-T, Stephen, JB. A simple method to predict blood-brain barrier permeability of drug-like compounds using classification trees. Med Chem 2017;13:664–9.Search in Google Scholar

56. Cabrera-Perez, MA, Pham-The, H, Bermejo, M, Alvarez, IG, Alvarez, MG, Garrigues, TM. QSPR in oral bioavailability: specificity or integrality? Mini Rev Med Chem 2012;12:534–50. https://doi.org/10.2174/138955712800493753.Search in Google Scholar

57. Vandenberg, JI, Perry, MD, Perrin, MJ, Mann, SA, Ke, Y, Hill, AP. hERG K+ channels: structure, function, and clinical significance. Physiol Rev 2012;92:1393–478. https://doi.org/10.1152/physrev.00036.2011.Search in Google Scholar

Received: 2021-04-15
Accepted: 2021-10-16
Published Online: 2021-11-10
Published in Print: 2022-05-25

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 3.10.2023 from https://www.degruyter.com/document/doi/10.1515/znc-2021-0111/pdf
Scroll to top button