Metabolite Profiling of the Environmental-Controlled Growth of Marsilea crenata Presl. and Its In Vitro and In Silico Antineuroinflammatory Properties
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Submitted
8 February 2022
8 February 2022
Published
31 August 2022
31 August 2022
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Abstract
This study was aimed to evaluate the metabolite contents and antineuroinflammatory potential of Marsilea crenata Presl. grown under a controlled environmental condition. The antineuroinflammatory test has been carried out in vitro using ethanolic extract of M. crenata leaves on HMC3 microglia cells. An in silico approach was applied to predict the active compounds of the extract. The HMC3 microglia cells were induced with IFNγ to create prolonged inflammatory conditions and then treated with 96% ethanolic extract of the M. crenata leaves of 62.5, 125, and 250 μg/mL. The expression of MHC II was analyzed using the ICC method with the CLSM instrument. Metabolites of the extract were profiled using UPLC-QToF-MS/MS instrument and MassLynx 4.1 software. In silico evaluation was conducted with molecular docking on 3OLS protein using PyRx 0.8 software, and physicochemical properties of the compounds were analyzed using SwissADME webtool. The ethanolic extract of M. crenata leaves could reduce the MHC II expression in HMC3 microglia cells in all concentrations with the values 97.458, 139.574, and 82.128 AU. The result of metabolite profiling found 79 compounds in the extract. In silico evaluation showed that 19 compounds gave agonist interaction toward 3OLS, and three met all parameters of physicochemical analysis. The ethanolic extract of the environmental-controlled growth of M. crenata leaves antineuroinflammatory activity on HMC3 microglia cells. The extract was predicted to contain some phytoestrogen compounds which act as 3OLS agonists.
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29. Agil M, Kusumawati I, Purwitasari N. Phenotypic Variation Profile of Marsilea crenata Presl. Cultivated in Water and in the Soil. J Botany. 2017;2017:7232171. doi:10.1155/2017/7232171
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2. Webster AD, Finstad DA, Kurzer MS, Torkelson CJ. Quality of life among postmenopausal women enrolled in the Minnesota Green Tea Trial. Maturitas. 2018;108:1-6. doi:10.1016/j.maturitas.2017.10.013
3. Silva TR, Oppermann K, Reis FM, Spritzer PM. Nutrition in Menopausal Women: A Narrative Review. Nutrients. 2021;13(7):2149. doi:10.3390/nu13072149
4. Dalal PK, Agarwal M. Postmenopausal syndrome. Indian J Psychiatry. 2015;57(Suppl 2):S222-32. doi:10.4103/0019-5545.161483
5. Kwon HS, Koh SH. Neuroinflammation in neurodegenerative disorders: the roles of microglia and astrocytes. Transl Neurodegener. 2020;9(1):42. doi:10.1186/s40035-020-00221-2
6. Au A, Feher A, McPhee L, Jessa A, Oh S, Einstein G. Estrogens, inflammation and cognition. Front Neuroendocrinol. 2016;40:87–100. doi:10.1016/j.yfrne.2016.01.002
7. Matt SM, Johnson RW. Neuro-immune dysfunction during brain aging: new insights in microglial cell regulation. Curr Opin Pharmacol. 2016;26:96–101. doi:10.1016/j.coph.2015.10.009
8. Arcuri C, Mecca C, Bianchi R, Giambanco I, Donato R. The pathophysiological role of microglia in dynamic surveillance, phagocytosis and structural remodeling of the developing CNS. Front Mol Neurosci. 2017;10:191. doi:10.3389/fnmol.2017.00191
9. Prieto GA, Cotman CW. Cytokines and cytokine networks target neurons to modulate long-term potentiation. Cytokine Growth Factor Rev. 2017;34:27-33. doi:10.1016/j.cytogfr.2017.03.005
10. Radtke FA, Chapman G, Hall J, Syed YA. Modulating neuroinflammation to treat neuropsychiatric disorders. Biomed Res Int. 2017;2017:5071786. doi:10.1155/2017/5071786
11. Dong Y, Li X, Cheng J, Hou L. Drug development for alzheimer’s disease: Microglia induced neuroinflammation as a target? Int J Mol Sci. 2019;20(3):558. doi:10.3390/ijms20030558
12. Wixey JA, Reinebrant HE, Buller KM. Post-insult ibuprofen treatment attenuates damage to the serotonergic system after hypoxia-ischemia in the immature rat brain. J Neuropathol Exp Neurol. 2012;71(12):1137–48. doi:10.1097/nen.0b013e318277d4c7
13. Garrido-Mesa N, Zarzuelo A, Gálvez J. Minocycline: Far beyond an antibiotic. Br J Pharmacol. 2013;169(2):337–52. doi:10.1111/bph.12139
14. Zheng X, Yue P, Liu L, Tang C, Ma F, Zhang Y, et al. Efficacy between low and high dose aspirin for the initial treatment of Kawasaki disease: Current evidence based on a meta-analysis. PLoS One. 2019;14(5):e0217274. doi:10.1371/journal.pone.0217274
15. Rietjens IMCM, Louisse J, Beekmann K. The potential health effects of dietary phytoestrogens. Br J Pharmacol. 2017;174(11):1263-80. doi:10.1111/bph.13622
16. Jantaratnotai N, Utaisincharoen P, Sanvarinda P, Thampithak A, Sanvarinda Y. Phytoestrogens mediated anti-inflammatory effect through suppression of IRF-1 and pSTAT1 expressions in lipopolysaccharide-activated microglia. Int Immunopharmacol. 2013;17(2):483–8. doi:10.1016/j.intimp.2013.07.013
17. Villa A, Vegeto E, Poletti A, Maggi A. Estrogens, neuroinflammation, and neurodegeneration. Endocr Rev. 2016;37(4):372–402. doi:10.1210/er.2016-1007
18. Ma’arif B, Fitri H, Saidah NL, Najib LA, Yuwafi AH, Atmaja RRD, et al. Prediction of compounds with antiosteoporosis activity in Chrysophyllum cainito L. leaves through in silico approach. J Basic Clin Physiol Pharmacol. 2021;32(4):803–8. doi:10.1515/jbcpp-2020-0393
19. Desmawati D, Sulastri D. Phytoestrogens and Their Health Effect. Open AccessMaced J Med Sci. 2019;7(3):495-9. doi:10.3889/oamjms.2019.044
20. Liu T, Li N, Yan YQ, Liu Y, Xiong K, Liu Y, et al. Recent advances in the anti-aging effects of phytoestrogens on collagen, water content, and oxidative stress. Phytother Res. 2020;34(3):435-47. doi:10.1002/ptr.6538
21. Ma’arif B, Aditama AP. Activity of 96% Ethanol Extract of Chrysophyllum Cainito L. in Increasing Vertebrae Trabecular Osteoblast Cell Number in Male Mice. Asian J Pharm Clin Res. 2019;12(1):286-8. doi:10.22159/ajpcr.2019.v12i1.28994
22. Agil M, Laswati H, Kuncoro H, Ma’arif B. In silico Analysis of Phytochemical Compounds in Ethyl Acetate Fraction of Semanggi (Marsilea crenata Presl.) Leaves As Neuroprotective Agent. Res J Pharm Technol. 2020;13(8):3745–52. doi:10.5958/0974-360x.2020.00663.0
23. Putra HL. Green clover Potentiates Delaying the Increment of Imbalance Bone Remodeling Process in Postmenopausal Women. Folia Medica Indonesiana. 2011;47(2):112–7.
24. Nurjanah, Azka A, Abdullah A. Aktivitas Antioksidan Dan Komponen Bioaktif Semanggi Air (Marsilea Crenata). Asian J Innov Entrep. 2012;1(3):152–8. doi:10.20885/ajie.vol1.iss3.art2
25. Ma ’arif B, Agil M, Laswati H. Phytochemical Assessment on N-Hexane Extract and Fractions of Marsilea crenata Presl. Leaves through GC-MS. Trad Med J. 2016;21(2):77–85. doi:10.22146/tradmedj.12821
26. Ma’arif B, Agil M, Laswati H. Alkaline phosphatase activity of Marsilea crenata Presl. extract and fractions as marker of MC3T3-E1 osteoblast cell differentiation. J Appl Pharm Sci. 2018;8(3):55–9. doi:10.7324/JAPS.2018.8308
27. Ma’arif B, Mirza DM, Suryadinata A, Muchlisin MA, Laswati H, Agil M. Metabolite Profiling of 96% Ethanol Extract from Marsilea crenata Presl. Leaves Using UPLC-QToF-MS/MS and Anti-Neuroinflammatory Predicition Activity with Molecular Docking. J Trop Pharm Chem. 2019;4(6):261–70. doi:10.25026/jtpc.v4i6.213
28. Ma’arif B, Agil M, Laswati H. The enhancement of Arg1 and activated ERβ expression in microglia HMC3 by induction of 96% ethanol extract of Marsilea crenata Presl. leaves. J Basic Clin Physiol Pharmacol. 2019;30(6):20190284. doi:10.1515/jbcpp-2019-0284
29. Agil M, Kusumawati I, Purwitasari N. Phenotypic Variation Profile of Marsilea crenata Presl. Cultivated in Water and in the Soil. J Botany. 2017;2017:7232171. doi:10.1155/2017/7232171
30. Opačić N, Radman S, Uher SF, Benko B, Voća S, Žlabur JŠ. Nettle Cultivation Practices-From Open Field to Modern Hydroponics: A Case Study of Specialized Metabolites. Plants. 2022;11(4):483. doi:10.3390/plants11040483
31. Fussy A, Papenbrock J. An Overview of Soil and Soilless Cultivation Techniques-Chances, Challenges and the Neglected Question of Sustainability. Plants. 2022;11(9):1153. doi:10.3390/plants11091153
32. Chen SL, Yu H, Luo HM, Wu Q, Li CF, Steinmetz A. Conservation and sustainable use of medicinal plants: Problems, progress, and prospects. Chin Med. 2016;11:37. doi:10.1186/s13020-016-0108-7
33. Ma’arif B, Suleman HF, Annisa R, Dianti MR, Laswati H, Agil M. Efek Antineuroinflamasi Ekstrak Etanol 96% Daun Marsilea crenata Presl. Budidaya Papda Sel Mikroglia HMC3. J Farmasi Udayana. 2020;9(2):91-9. doi:10.24843/JFU.2020.v09.i02.p04
34. Engler-Chiurazzi EB, Brown CM, Povroznik JM, Simpkins JW. Estrogens as neuroprotectants: Estrogenic actions in the context of cognitive aging and brain injury. Prog Neurobiol. 2017;157:188–211. doi:10.1016/j.pneurobio.2015.12.008
35. Muchtaridi M, Dermawan D, Yusuf M. Molecular docking, 3D structure-based pharmacophore modeling, and ADME prediction of alpha mangostin and its derivatives against estrogen receptor alpha. J Young Pharm. 2018;10(3):252–9. doi:10.5530/jyp.2018.10.58
36. Rettberg J, Yao J, Brnton R. Estrogen: A master regulator of bioenergetic systems in the brain and body. Front Neuroendocrinol. 2014;35(1):515–25. doi:10.1016/j.yfrne.2013.08.001
37. Tang Y, Le W. Differential Roles of M1 and M2 Microglia in Neurodegenerative Diseases. Mol Neurobiol. 2016;53(2):1181–94. doi:10.1007/s12035-014-9070-5
38. Papageorgiou IE, Lewen A, Galow LV, Cesetti T, Scheffel J, Regen T, et al. TLR4-activated microglia require IFN-γ to induce severe neuronal dysfunction and death in situ. Proc Natl Acad Sci U S A. 2016;113(1):212-7. doi:10.1073/pnas.1513853113
39. Cherry JD, Olschowka JA, O’Banion MK. Neuroinflammation and M2 microglia: The good, the bad, and the inflamed. J Neuroinflammation. 2014;11:98. doi:10.1186/1742-2094-11-98
40. Shih RH, Wang CY, Yang CM. NF-kappaB signaling pathways in neurological inflammation: A mini review. Front Mol Neurosci. 2015;8:77. doi:10.3389/fnmol.2015.00077
41. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR, Lee DH, et al. Hormones and endocrine-disrupting chemicals: Low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012;33(3):378–455. doi:10.1210/er.2011-1050
42. Lagarde F, Beausoleil C, Belcher SM, Belzunces LP, Emond C, Guerbet M, et al. Non-monotonic dose-response relationships and endocrine disruptors: A qualitative method of assessment. Environ Health. 2015;14:13. doi:10.1186/1476-069x-14-13
43. Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal. 2016;6(2):71–9. doi:10.1016/j.jpha.2015.11.005
44. Lu J, Muhmood A, Czekała W, Mazurkiewicz J, Dach J, Dong R. Untargeted metabolite profiling for screening bioactive compounds in digestate of manure under anaerobic digestion. Water. 2019;11(11):2420. doi:10.3390/w11112420
45. Duarte AJ, Ribeiro D, Moreira L, Amaral O. In silico analysis of missense mutations as a first step in functional studies: Examples from two sphingolipidoses. Int J Mol Sci. 2018;19(11):3409. doi:10.3390/ijms19113409
46. Aditama APR, Ma’arif B, Mirza DM, Laswati H, Agil M. In vitro and in silico analysis on the bone formation activity of N-hexane fraction of Semanggi (Marsilea crenata Presl.). Syst Rev Pharm. 2020;11(11):837–49.
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Authors
1.
Ma’arif B, Muslikh FA, Amalia D, Mahardiani A, Muchlasi LA, Riwanti P, Taek MM, Laswati H, Agil M. Metabolite Profiling of the Environmental-Controlled Growth of Marsilea crenata Presl. and Its In Vitro and In Silico Antineuroinflammatory Properties. Borneo J Pharm [Internet]. 2022Aug.31 [cited 2025Apr.7];5(3):209-28. Available from: https://journal.umpr.ac.id/index.php/bjop/article/view/3262
Copyright (c) 2022 Burhan Ma'arif, Faisal Akhmal Muslikh, Dilla Amalia, Anisah Mahardiani, Luthfi Achmad Muchlasi, Pramudita Riwanti, Maximus Markus Taek, Hening Laswati, Mangestuti Agil
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