Bioassay-Guided Fractionation of Acetone and Methanol Extracts of Quercus infectoria Galls with Antimalarial Properties
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Abstract
The antimalarial properties of crude extracts from Quercus infectoria galls were investigated through bioassay-guided fractionation. Acetone (QIA) and methanol (QIM) crude extracts have been reported to have promising antimalarial activity against Plasmodium falciparum (3D7 strain). These extracts were subjected to fractionation using automated preparative high-performance liquid chromatography (prep-HPLC) to identify the most active fractions. Nine fractions were isolated from each extract, of which the fractions QIA11 and QIM16 showed antimalarial activity, with IC50 values of 17.65 ± 1.82 ?g/mL and 24.21 ± 1.88 ?g/mL, respectively. In comparison, the standard antimalarial drug artemisinin has an IC50 value of 0.004 ± 0.001 ?g/mL). Through high-resolution liquid chromatography coupled with mass spectrometry (HR-LCMS) analysis of the fractions, four known compounds were successfully identified: gallic acid, ellagic acid, 1,3,6-tris-o-(3,4,5- trihydroxybenzoyl)-beta-d-glucose and 1-O,6-O-digalloyl-beta-D-glucose.
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References
Abdullah A R, Hapidin H and Abdullah H. (2017). Phytochemical analysis of Quercus infectoria galls extracts using FTIR, LC-MS and MS/MS analysis. Research Journal of Biotechnology 12(12): 55–61.
Alseekh S, Aharoni A, Brotman Y, Contrepois K, D’Auria J, Ewald J, Ewald J C, et al. (2021). Mass spectrometry-based metabolomics: A guide for annotation, quantification and best reporting practices. Nature Methods 18(7): 747–56. https://doi.org/10.1038/s41592-021-01197-1
Abdul Haque A S, Wasim A, Khan M R and Hasan A. (2016). Ethnopharmacology of Quercus infectoria galls: A review. Hippocratic Journal of Unani Medicine 11(3): 105–118.
Arya A, Foko L P K, Chaudhry S, Sharma A and Singh V. (2021). Artemisinin-based combination therapy (ACT) and drug resistance molecular markers: A systematic review of clinical studies from two malaria endemic regions – India and Sub-Saharan Africa. International Journal for Parasitology: Drugs and Drug Resistance 15: 43–56. https://doi.org/10.1016/j.ijpddr.2020.11.006
Atanasov A G, Waltenberger B, Pferschy-Wenzig E M, Linder T, Wawrosch C, Uhrin P, Temml V, et al. (2015). Discovery and resupply of pharmacologically active plantderived natural products: A review. Biotechnology Advances 33(8): 1582–1614. https://doi.org/10.1016/j.biotechadv.2015.08.001
Blades A T, Ikonomou M G and Kebarle P. (1991). Mechanism of electrospray mass spectrometry. electrospray as an electrolysis cell. Analytical Chemistry 63(19): 2109–2114. https://doi.org/10.1021/ac00019a009
Che C T and Zhang H. (2019). Plant natural products for human health. International Journal of Molecular Sciences 20(4): 2–5. https://doi.org/10.3390/ijms20040830
Dash G K, Ansari M T, Sami F and Majeed S. (2016). Proximate analysis and quantitative estimation of gallic acid in Quercus infectoria Oliv. galls by HPTLC. Internasional Journal of Pharmaceutical Sciences and Research 7(11): 4400–4406. https://doi.org/10.13040/IJPSR.0975-8232.7(11).4400-06
Dworkin J P. (2011). Chromatographic co-elution. In: M Gargaud, R Amils, J C Quintanilla, H J (Jim) Cleaves, W M Irvine, D L Pinti and M Viso (eds.), Encyclopedia of astrobiology. Berlin, Heidelberg: Springer Berlin Heidelberg, 302. https://doi.org/10.1007/978-3-642-11274-4_289
Ekasari W, Fatmawati D, Khoiriah S M, Baqiuddin W A, Nisa H Q, Maharupini A A S, Wahyuni T S, Oktarina R D, Suhartono E and Sahu R K.(2022). Antimalarial activity of extract and fractions of Sauropus androgynus (L.) Merr. Scientifica (Cairo) 2022: 3552491. https://doi.org/10.1155/2022/3552491
Fatima S, Farooqi A H A, Kumar R, Kumar T R S and Khanuja S P S. (2001). Antibacterial activity possessed by medicinal plants used in tooth powders. Journal of Medicinal and Aromatic Plant Sciences 22(4a): 187–189.
Ferguson N. M. (2018). Challenges and opportunities in controlling mosquito-borne infections. Nature 559(7715): 490–497. https://doi.org/10.1038/s41586-018-0318-5
Ferrer Amate C, Unterluggauer H, Fischer R J, Fernández-Alba A R and Masselter S. (2010). Development and validation of a LC–MS/MS method for the simultaneous determination of aflatoxins, dyes and pesticides in spices. Analytical and Bioanalytical Chemistry 397(1): 93–107. https://doi.org/10.1007/s00216-010-3526-x
Goli A H, Barzegar M and Sahari M A. (2005). Antioxidant activity and total phenolic compounds of pistachio (Pistachia vera) hull extracts. Food Chemistry 92(3): 521–525. https://doi.org/10.1016/j.foodchem.2004.08.020
Hamid H, Kaur G, Abdullah S T, Ali M, Athar M and Alam M S. (2005). Two new compounds from the galls of Quercus infectoria with nitric oxide and superoxide inhibiting ability. Pharmaceutical Biology 43(4): 317–323. https://doi.org/10.1080/13880200590951711
Harborne J B. (1998). Phytochemical methods (3rd Ed.). London: Chapman and Hall. Ibrahim N and Abu-Bakar N. (2019). Measurement of pH of the digestive vacuole isolated from the plasmodium falciparum-infected erythrocyte by digitonin permeabilization. International Journal of Pharmaceutical Sciences and Research 10(5): 2587–2593. https://doi.org/10.13040/IJPSR.0975-8232.10(5).2587-93
Imtiyaz S, Ali S J, Tariq M, Chaudhary S S and Aslam M. (2013). Oak galls: The medicinal balls. Journal of Pharmaceutical and Scientific Innovation 1(6): 39–43.
Iylia Arina M Z and Harisun Y. (2019). Effect of extraction temperatures on tannin content and antioxidant activity of Quercus Infectoria (manjakani). Biocatalysis and Agricultural Biotechnology 19(March): 101104. https://doi.org/10.1016/j.bcab.2019.101104
Jonville M C, Kodja H, Humeau L, Fournel J, De Mol P, Cao M, Angenot L and Frédérich M. (2008). Screening of medicinal plants from Reunion Island for antimalarial and cytotoxic activity. Journal of Ethnopharmacology 120(3): 382–386. https://doi.org/10.1016/j.jep.2008.09.005
Joshi D D. (2012). UV–vis. spectroscopy: Herbal drugs and fingerprints. In: D D Joshi (ed.). Herbal drugs and fingerprints: Evidence based herbal drugs. India: Springer India, 101–120. https://doi.org/10.1007/978-81-322-0804-4_6
Kamarudin N A, Nik Salleh N N H and Tan S C. (2021a). Gallotannin-enriched fraction from Quercus infectoria galls as an antioxidant and inhibitory agent against human glioblastoma multiforme. Plants 10(12): 2581. https://doi.org/10.3390/plants10122581
Kamarudin N A, Muhamad N, Nik Salleh N N H and Tan S C. (2021b). Impact of solvent selection on phytochemical content, recovery of tannin and antioxidant activity of Quercus infectoria galls. Pharmacognosy Journal 13(September): 1195–1204. https://doi.org/10.5530/pj.2021.13.153
Kanu A B. (2021). Recent developments in sample preparation techniques combined with high-performance liquid chromatography: A critical review. Journal of Chromatography A 1654: 462444. https://doi.org/10.1016/j.chroma.2021.462444
Kebarle P and Verkerk U H. (2010). On the mechanism of electrospray ionization mass spectrometry (ESIMS). In: Cole R B (ed.), Electrospray and MALDI mass spectrometry: Fundamentals, instrumentation, practicalities, and biological applications. Hoboken, NJ: John Wiley and Sons, 1–48. https://doi.org/10.1002/9780470588901.ch1
Kheirandish F, Delfan B, Mahmoudvand H, Moradi N, Ezatpour B, Ebrahimzadeh F and Rashidipour M. (2016). Antileishmanial, antioxidant, and cytotoxic activities of Quercus infectoria Olivier extract. Biomedicine and Pharmacotherapy 82: 208–215. https://doi.org/10.1016/j.biopha.2016.04.040
Kumar N and Goel N. (2019). Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnology Reports (Amsterdam, Netherlands) 24(December): e00370. https://doi.org/10.1016/j.btre.2019.e00370
Ma S, Qin H, Jiang M, Wang J, Wang W, Guo G, Zhou L, Chen W and Han B. (2020). Identification and comparison of tannins in gall of Rhus chinensis Mill. and gall of Quercus infectoria Oliv. by high-performance liquid chromatography-electrospray mass spectrometry. Journal of Chromatographic Science 58(5): 403–410. https://doi.org/10.1093/chromsci/bmz096
Mamede L, Ledoux A, Jansen O and Frédérich M. (2020). Natural phenolic compounds and derivatives as potential antimalarial agents. Planta Medica 86(9): 585–618. https://doi.org/10.1055/a-1148-9000
Mazid M, Khan T A and Mohammad F. (2011). Role of secondary metabolites in defense mechanisms of plants. Biology and Medicine 3(2): 232–249.
Mohd-Zamri N H, Sinin N J and Abu-Bakar N. (2017). Preparation and in vitro characterization of resealed erythrocytes containing Tmr-Dextran for determination of hemoglobin uptake and transfer by the malaria parasite. International Journal of Pharmaceutical Sciences and Research 8(3): 1038–1047. https://doi.org/10.13040/IJPSR.0975-8232.8(3).1038-47
Morales D. (2021). Oak trees (Quercus spp.) as a source of extracts with biological activities: A narrative review. Trends in Food Science and Technology 109(January): 116–125. https://doi.org/10.1016/j.tifs.2021.01.029
Nakalembe L, Kasolo J N, Nyatia E, Lubega A and Bbosa G S. (2019). Analgesic and antiinflammatory activity of total crude leaf extract of Phytolacca dodecandra in Wistar albino rats. Neuroscience and Medicine 10(3): 259–271. https://doi.org/10.4236/nm.2019.103020
Newman D J and Cragg G M. (2020). Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. Journal of Natural Products 83(3): 770–803. https://doi.org/10.1021/acs.jnatprod.9b01285
Nigussie G and Wale M. (2022). Medicinal plants used in traditional treatment of malaria in Ethiopia: A review of ethnomedicine, anti-malarial and toxicity studies. Malaria Journal 21(1): 1–16. https://doi.org/10.1186/s12936-022-04264-w
Nik Mat Zin N N I, Mohamad M N, Roslan K, Sazeli A W, Abdul Moin N I, Alias A, Zakaria Y and Abu-Bakar N. (2020). In vitro antimalarial and toxicological activities of Quercus infectoria (Olivier) gall extracts. Malaysian Journal of Medical Sciences 27(4): 36–50. https://doi.org/10.21315/mjms2020.27.4.4
Nik Mat Zin N N I, Kathap M O, Sul’ain M D and Abu Bakar N. (2019). Evaluation of antimalarial and toxicological activities of methanol and water leaves extracts of Piper sarmentosum. Asian Journal of Medicine and Biomedicine 3(1): 19–24.
Nik Mat Zin N N I, Wan Mohd Rahimi W N A and Abu Bakar N. (2019). A review of Quercus infectoria (Olivier) galls as a resource for anti-parasitic agents: In vitro and in vivo studies. Malaysian Journal of Medical Sciences 26(6): 19–34. https://doi.org/10.21315/mjms2019.26.6.3
Núñez O and Lucci P. (2014). Applications and uses of formic acid in liquid chromatographymass spectrometry analysis. In J C Taylor (ed.), Advances in chemical research, Vol. 20. New York: Nova Science Publishers, 71–86.
Ochieng C O, Midiwo J O and Owuor P O. (2010). Anti-plasmodial and larvicidal effects of surface exudates of Gardenia ternifolia aerial parts. Research Journal of Pharmacology 4: 45–50. https://doi.org/10.3923/rjpharm.2010.45.50
Oldoni T L C, Merlin N, Bicas T C, Prasniewski A, Carpes S T, Ascari J, de Alencar S M, et al. (2021). Antihyperglycemic activity of crude extract and isolation of phenolic compounds with antioxidant activity from Moringa oleifera Lam. leaves grown in Southern Brazil. Food Research International 141: 110082. https://doi.org/10.1016/j.foodres.2020.110082
Othman L, Sleiman A and Abdel-Massih R M. (2019). Antimicrobial activity of polyphenols and alkaloids in Middle Eastern plants. Frontiers in Microbiology 10: 911. https://doi.org/10.3389/fmicb.2019.00911
Ouji M, Augereau J M, Paloque L and Benoit-Vical F. (2018). Plasmodium falciparum resistance to artemisinin-based combination therapies: A sword of damocles in the path toward malaria elimination. Parasite 25(24): 1–12. https://doi.org/10.1051/parasite/2018021
Rasoanaivo P, Ratsimamanga-tjrverg S and Frappier F. (2021). Guidelines for the nonclinical evaluation of the efficacy of traditional antimalarials. In: Willcox M, Bodeker G, Rasoanaivo P and Addae-Kyereme J (eds.),Traditional medicinal plants and malaria. Boca Raton: CRC Press, 324–341. https://doi.org/10.1201/9780203502327-29
Rayleigh L. (1882). XX. On the equilibrium of liquid conducting masses charged with electricity. The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science 14(87): 184–186. https://doi.org/10.1080/14786448208628425
Samuelsson G. (1999). Drug of natural origin a textbook of pharmacognosy. Stockholm, Sweden: Apotekarsocieteten.
Shah G M, Abbasi A M, Khan N, Guo X, Khan M A, Hussain M, Bibi S, Nazir A and Adnan Tahir A. (2014). Traditional uses of medicinal plants against malarial disease by the tribal communities of lesser Himalayas-Pakistan. Journal of Ethnopharmacology 155(1): 450–462. https://doi.org/10.1016/j.jep.2014.05.047
Shrestha S, Kaushik V S, Eshwarappa, R S B, Subaramaihha S R, Ramanna L M and D B. (2014). Pharmacognostic studies of insect gall of Quercus infectoria Olivier (Fagaceae). Asian Pacific Journal of Tropical Biomedicine 4(1): 35–39. https://doi.org/10.1016/S2221-1691(14)60205-7
Shukla R, Dubey A, Pandey V, Golhani D and Jain A P. (2017). Chromophore: An utility in UV spectrophotometer. Inventi Rapid: Pharm Analysis and Quality Assurance 2012(3): 1–4.
Snyder L R and Dolan J W. (2007). High-performance gradient elution: The practical application of the linear-solvent-strength model. Hoboken, NJ: John Wiley and Sons. https://doi.org/10.1002/0470055529
Tahir A H, Hussain Z, Yousuf H, Fazal F, Tahir M A and Kashif M. (2022). Traditional herbal medicine and its clinical relevance: A need to preserve the past for the future. Journal of Biosciences and Medicines 10(7): 64–75. https://doi.org/10.4236/jbm.2022.107005
Tajuddeen N and Van Heerden F R. (2019). Antiplasmodial natural products: An update. Malaria Journal 18(1): 1–62. https://doi.org/10.1186/s12936-019-3026-1
Tayel A A, El-Sedfy M A, Ibrahim A I and Moussa S H. (2018). Application of Quercus infectoria extract as a natural antimicrobial agent for chicken egg decontamination. Revista Argentina de Microbiologia 50(4): 391–397. https://doi.org/10.1016/j.ram.2017.12.003
Tu Y. (2011). The discovery of Artemisinin (Qinghaosu) and gifts from chinese medicine. Nature Medicine 17(10): 1217–1220. https://doi.org/10.1038/nm.2471
Uzor P F, Onyishi C K, Omaliko A P, Nworgu S A, Ugwu O H and Nwodo N J. (2021). Study of the antimalarial activity of the leaf extracts and fractions of Persea americana and Dacryodes edulis and their HPLC analysis. Evidence-Based Complementary and Alternative Medicine 2021: 218294. https://doi.org/10.1155/2021/5218294
Vink H. (1972). Resolution and column efficiency in chromatography. Journal of Chromatography A 69(2): 237–242. https://doi.org/10.1016/S0021-9673(00)92891-7
Walker J M. (2009). Natural products isolation: Methods and protocols. Life Sciences 531.
Wan Nor Amilah W A W, Mohamad A N, Noor Izani N J and Arizam M F. (2022). Antimicrobial activities of Quercus infectoria gall extracts: A scoping review. Journal of Herbal Medicine 32(June 2021): 100543. https://doi.org/10.1016/j.hermed.2022.100543
WHO. (2021). World malaria report 2021. Geneva: World Health Organization.
Wu Z, Gao W, Phelps M A, Wu D, Miller D D and Dalton J T. (2004). Favorable effects of weak acids on negative-ion electrospray ionization mass spectrometry. Analytical Chemistry 76(3): 839–847. https://doi.org/10.1021/ac0351670
Yuan H, Ma Q, Ye L and Piao G. (2016). The traditional medicine and modern medicine from natural products. Molecules 21(5): 559. https://doi.org/10.3390/molecules21050559
Zhang Q W, Lin L G and Ye W C. (2018). Techniques for extraction and isolation of natural products: A comprehensive review. Chinese Medicine 13: 20. https://doi.org/10.1186/s13020-018-0177-x