Abstract
Licania rigida Benth., a Brazilian endemic plant, has been traditionally used for treating inflammation and stomach pain. This work investigates the anti-inflammatory and gastroprotective activities of the ethanolic extract from L. rigida seeds (EELr) by in vitro and in vivo methods. The phytochemical profile was determined and the in vitro antioxidant activity was investigated by radical scavenging and thiobarbituric acid reactive substances methods. The ovalbumin denaturation method was used with sodium diclofenac as standard for the in vitro anti-inflammatory activity assessment. Acetylsalicylic acid was used to induce gastric ulcers in male mice and then to evaluate the preventive and therapeutic gastroprotective effect of EELr, using omeprazole as the reference drug. The extract exhibited relevant amount of phenolic compounds and flavonoids, in particular, demonstrating in vitro antioxidant capacity. EELr was able to inhibit almost 60% of ovalbumin denaturation at a concentration considered low. It also prevented the decrease of biochemical markers for oxidative stress such as superoxide dismutase (SOD) and reduced glutathione (GSH) in the stomach and SOD and catalase (CAT) in the liver. EELr also significantly decreased the number of lesions as well as reduced the ulcerated area when used as therapy. The observed effect may be due to its phenolic compounds, such as chlorogenic acid, caffeic acid and tannins, as previously reported. EELr is a potential source of compounds with anti-inflammatory activity, protects the liver from oxidative damage and improves healing of aspirin-induced ulcers. This work contributes to the knowledge of L. rigida species.
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References
Adinortey MB, Ansah C, Galyuon I, Nyarko A (2013) In vivo models used for evaluation of potential antigastroduodenal ulcer agents. Ulcers. https://doi.org/10.1155/2013/796405
Ağagündüz D, Şahin TÖ, Yılmaz B, Ekenci KD, Şehriban DÖ, Capasso R (2022) Cruciferous vegetables and their bioactive metabolites: from prevention to novel therapies of colorectal cancer. Evid Based Compl Alter Med. 2022:1534083. https://doi.org/10.1155/2022/1534083
Ahmed MAE, Mohanad M, Ahmed AAE, Aboulhoda BE, El-Awdan SA (2021) Mechanistic insights into the protective effects of chlorogenic acid against indomethacin-induced gastric ulcer in rats: Modulation of the cross talk between autophagy and apoptosis signaling. Life Sci 275:119370. https://doi.org/10.1016/j.lfs.2021.119370
Akhter S, Irfan HM, Ullah A, Jahan S, Roman M, Latif MB, Althobaiti YS (2022) Noscapine hydrochloride (benzyl-isoquinoline alkaloid) effectively prevents protein denaturation through reduction of IL-6, NF-kB, COX-2, Prostaglandin-E2 in rheumatic rats. Saudi Pharm J 30(12):1791–1801. https://doi.org/10.1016/j.jsps.2022.10.008
Alencar-araripe GD, Nunes-pinheiro S, Célia D, Costa O, Feitosa S, Almeida GD, Karlo G, Tomé R, Girão C (2014) A clinical trial and oral wound treated by essential oil of lippia sidoides mouthrinse in horses. Acta Sci Vet 42:1249
Anwar S, Almatroudi A, Allemailem KS, Joseph RJ, Khan AA, Rahmani AH (2020) Protective effects of ginger extract against glycation and oxidative stress-induced health complications: An in vitro study. Processes. https://doi.org/10.3390/PR8040468
Beber AP, de Souza P, Boeing T, Somensi LB, Mariano LNB, Cury BJ, Burci LM, da Silva CB, Simionatto E, de Andrade SF, da Silva LM (2018) Constituents of leaves from Bauhinia curvula Benth. exert gastroprotective activity in rodents: role of quercitrin and kaempferol. Inflammopharmacology 26:539–550. https://doi.org/10.1007/s10787-017-0313-8
Beers R Jr, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195(1):133–140
Beretta G, Shala AL (2022) Impact of heat shock proteins in neurodegeneration: possible therapeutical targets. Ann Neurosci 29(1):71–82. https://doi.org/10.1177/09727531211070528
Bouhlali E, Dine T, Hmidani A, Bourkhis B, Khouya T, Ramchoun M, Filali-Zegzouti Y, Alem C (2020) Phenolic profile and anti-inflammatory activity of four Moroccan date (Phoenix dactylifera L) seed varieties. Heliyon. 6:e03436. https://doi.org/10.1016/j.heliyon.2020.e03436
Caesar LK, Cech NB (2019) Synergy and antagonism in natural product extracts: When 1 + 1 does not equal 2. Nat Prod Rep 36:869–888. https://doi.org/10.1039/c9np00011a
Cardoso JC, de Oliveira MEBS, de Cardoso F (2019) Advances and challenges on the in vitro production of secondary metabolites from medicinal plants. Hortic Bras 37:124–132. https://doi.org/10.1590/s0102-053620190201
Castaneda-Arriaga R, Pérez-González A, Reina M, Alvarez-Idaboy JR, Galano A (2018) Comprehensive investigation of the antioxidant and pro-oxidant effects of phenolic compounds: a double-edged sword in the context of oxidative stress. J Phys Chem B 122:6198–6214. https://doi.org/10.1021/acs.jpcb.8b03500
Cerqua I, Neukirch K, Terlizzi M, Granato E, Caiazzo E, Cicala C, Ialenti A, Capasso R, Werz O, Sorrentino R, Seraphin D, Helesbeux JJ, Cirino G, Koeberle A, Roviezzo F, Rossi A (2022) A vitamin E long-chain metabolite and the inspired drug candidate α-amplexichromanol relieve asthma features in an experimental model of allergen sensitization. Pharmacol Res 181:106250. https://doi.org/10.1016/j.phrs.2022.106250
Chy MNU, Adnan M, Chowdhury MR, Pagano E, Kamal AM, Oh KK et al (2021) Central and peripheral pain intervention by Ophiorrhiza rugosa leaves: potential underlying mechanisms and insight into the role of pain modulators. J Ethnopharmacol 276:114182. https://doi.org/10.1016/j.jep.2021.114182
Dirsch VM, Stuppner H, Vollmar AM (1998) The griess assay: Suitable for a bio-guided fractionation of anti- inflammatory plant extracts? Planta Med 64:423–426. https://doi.org/10.1055/s-2006-957473
Domper Arnal MJ, Hijos-Mallada G, Lanas A (2022) Gastrointestinal and cardiovascular adverse events associated with NSAIDs. Expert Opin Drug Saf 21(3):373–384
Farias DF, Souza TM, Viana MP, Soares BM, Cunha AP, Vasconcelos IM, Maria N, Silva P, Michel P, Ferreira P, Maria V, Melo M, Fontenele A, Carvalho U (2013) Antibacterial, antioxidant and anticholinesterase activities of plant seed extracts from brazilian semiarid region. Biomed Res Int 2013:1–9
Fernandes MF, Cardoso D, de Queiroz LP (2020) An updated plant checklist of the Brazilian Caatinga seasonally dry forests and woodlands reveals high species richness and endemism. J Arid Environ 174:104079. https://doi.org/10.1016/j.jaridenv.2019.104079
Fernández J, Silván B, Entrialgo-Cadierno R, Villar CJ, Capasso R, Uranga JA, Lombó F, Abalo R (2021) Antiproliferative and palliative activity of flavonoids in colorectal cancer. Biomed Pharmacother 143:112241. https://doi.org/10.1016/j.biopha.2021.112241
Ferrarini EG, Paes RS, Baldasso GM, de Assis PM, Gouvêa MC, Cicco P, Raposo NRB, Capasso R, Moreira ELG, Dutra RC (2022) Broad-spectrum cannabis oil ameliorates reserpine-induced fibromyalgia model in mice. Biomed Pharmacother 154:113552. https://doi.org/10.1016/j.biopha.2022.113552
Gupta M, Gulati M, Kapoor B, Kumar B, Kumar R, Kumar R, Khurana N, Gupta R, Singh N (2021) Anti-ulcerogenic effect of methanolic extract of Elaeagnus conferta Roxb. Seeds Wistar Rats. J. Ethnopharmacol. 275:114115. https://doi.org/10.1016/j.jep.2021.114115
Haefliger R, Dries LS, Perassolo MS, Cardoso CDO (2022) Neuropsychological assessment after long-term omeprazole treatment. Appl Neuropsychol Adult. https://doi.org/10.1080/23279095.2022.2106570
Kleniewska P, Pawliczak R (2017) Influence of Synbiotics on Selected Oxidative Stress Parameters. Med. Cell. Longev, Oxid. https://doi.org/10.1155/2017/9315375
Liu X, Zhao M, Wang J, Yang B, Jiang Y (2008) Antioxidant activity of methanolic extract of emblica fruit (Phyllanthus emblica L.) from six regions in China. J Food Compos Anal 21(3):219–228. https://doi.org/10.1016/j.jfca.2007.10.001
Lopes Neto JJ, de Almeida TS, de Medeiros JL, Vieira LR, Moreira TB, Maia AIV, Ribeiro PRV, de Brito ES, Farias DF, Carvalho AFU (2017) Impact of bioaccessibility and bioavailability of phenolic compounds in biological systems upon the antioxidant activity of the ethanolic extract of Triplaris gardneriana seeds. Biomed Pharmacother 88:999–1007. https://doi.org/10.1016/j.biopha.2017.01.109
Lu C, Wei Z, Jiang N, Chen Y, Wang Y, Li S, Wang Q, Fan B, Liu X, Wang F (2022) Soy isoflavones protects against cognitive deficits induced by chronic sleep deprivation via alleviating oxidative stress and suppressing neuroinflammation. Phytother Res 36(5):2072–2080. https://doi.org/10.1002/ptr.7354
Macedo JGF, de Menezes IRA, Ribeiro DA, de Santos M (2018) Analysis of the variability of therapeutic indications of medicinal species in the northeast of Brazil : comparative study. Evidence-Based Complement Altern Med 2018:28
Mahmoud YI, Abd El-Ghffar EA (2019) Spirulina ameliorates aspirin-induced gastric ulcer in albino mice by alleviating oxidative stress and inflammation. Biomed Pharmacother 109:314–321. https://doi.org/10.1016/j.biopha.2018.10.118
Mitra S, Das R, Emran TB, Labib RK, Noor-E-Tabassum IF, Sharma R, Ahmad I, Nainu F, Chidambaram K, Alhumaydhi FA, Chandran D, Capasso R, Wilairatana P (2022) Diallyl disulfide: a bioactive garlic compound with anticancer potential. Front Pharmacol 13:943967. https://doi.org/10.3389/fphar.2022.943967
Mohapatra TK, Nayak RR, Subudhi BB (2019) Exploration of anti-inflammatory and hepatoprotective effect of curcumin on co-administration with acetylsalicylic acid. J Pharm Pharmacogn Res 7:310–322
Nani A, Murtaza B, Sayed Khan A, Khan NA, Hichami A (2021) Antioxidant and Anti-Inflammatory Potential of Polyphenols. Molecules 26:1–15
Paseban M, Niazmand S, Soukhtanloo M, Meibodi NT (2020) The preventive effect of Nigella sativa seed on gastric ulcer induced by indomethacin in rat. J Herbmed Pharmacol 9:12–19. https://doi.org/10.15171/JHP.2020.02
Pessoa IP (2015) Caracterização Química, atividade antioxidante e segurança de uso de sementes de Licania rigida benth. Universidade Federal do Ceará. Available in: http://www.repositorio.ufc.br/handle/riufc/19393
Pessoa IP, Joaquim J, Neto L, Almeida TSD, Farias DF, Vieira LR, Medeiros JLD, Boligon AA (2016) Polyphenol composition, antioxidant activity and cytotoxicity of seeds from two underexploited Wild Licania species: L rigida and L tomentosa. Molecules. https://doi.org/10.3390/molecules21121755
Rodrigues PA, de Morais SM, Souza CM, Magalhães DV, Vieira ÍGP, Andrade GM, Rao VS, Santos FA (2012) Gastroprotective effect of Byrsonima sericea DC leaf extract against ethanol-induced gastric injury and its possible mechanisms of action. An Acad Bras Cienc 84:113–122. https://doi.org/10.1590/S0001-37652012005000011
Sabir SM, Rocha JBT (2008) Antioxidant and hepatoprotective activity of aqueous extract of Solanum fastigiatum (false “Jurubeba”) against paracetamol-induced liver damage in mice. J Ethnopharmacol 120:226–232. https://doi.org/10.1016/j.jep.2008.08.017
Saharan P, Sadh PK, Duhan S, Duhan JS (2020) Bio-enrichment of phenolic, flavonoids content and antioxidant activity of commonly used pulses by solid-state fermentation. J Food Meas Charact 14:1497–1510. https://doi.org/10.1007/s11694-020-00399-z
Sales PF, De Almeida Nóbrega P, Do Nascimento AA, Brito Corrêa FRF, De Veiga Cabral GN, Da Silva EG (2019) Antiulcerogenic activity of the ethanolic extract of Licania macrophylla Benth. Mundo Da Saude 43:814–833. https://doi.org/10.15343/0104-7809.20194304814833
Sandu N, Chilom CG, Popescu AI (2021) Structural and molecular aspects of flavonoids as ligands for serum transferrin Spectrochim Acta Part A Mol. Biomol Spectrosc 254:119600. https://doi.org/10.1016/j.saa.2021.119600
Schwarz KB, Arey BJ, Tolman K, Mahanty S (1988) Iron chelation as a possible mechanism for aspirin-induced malondialdehyde production by mouse liver microsomes and mitochondria. J Clin Invest 81:165–170. https://doi.org/10.1172/JCI113289
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205. https://doi.org/10.1016/0003-2697(68)90092-4
Shovo MARB, Tona MR, Mouah J, Islam F, Chowdhury MHU, Das T, Paul A, Ağagündüz D, Rahman MM, Emran TB, Capasso R, Simal-Gandara J (2021) Computational and pharmacological studies on the antioxidant, thrombolytic, anti-inflammatory, and analgesic activity of Molineria capitulata. Curr Issues Mol Biol 43(2):434–456. https://doi.org/10.3390/cimb43020035
Singh SK, Patra A (2018) Evaluation of phenolic composition, antioxidant, anti-inflammatory and anticancer activities of polygonatum verticillatum (L.). J Integr Med 16:273–282. https://doi.org/10.1016/j.joim.2018.04.005
Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and Antioxidants by means of Folin-Ciocalteu Reagent. Methods Enzymol 299:152–178
Valli M, Russo HM, Bolzani VS (2018) The potential contribution of the natural products from Brazilian biodiversity to bioeconomy. An Acad Bras Cienc 90:763–778
Vasconcelos PCP, Andreo MA, Vilegas W, Hiruma-Lima CA, Pellizzon CH (2010) Effect of Mouriri pusa tannins and flavonoids on prevention and treatment against experimental gastric ulcer. J Ethnopharmacol 131:146–153. https://doi.org/10.1016/j.jep.2010.06.017
Verma MK, Jaiswal A, Sharma P, Kumar P, Singh AN (2019) Oxidative stress and biomarker of TNF-α, MDA and FRAP in hypertension. J Med Life 12:253–259. https://doi.org/10.25122/jml-2019-0031
Viana AFSC, Fernandes HB, Silva FV, Oliveira IS, Freitas FFBP, Machado FDF, Costa CLS, Arcanjo DDR, Chaves MH, Oliveira FA, Oliveira RCM (2013) Gastroprotective activity of cenostigma macrophyllum Tul. var. acuminata Teles Freire leaves on experimental ulcer models. J Ethnopharmacol 150:316–323. https://doi.org/10.1016/j.jep.2013.08.047
Zhang CY, Tan B (1996) Hypotensive activity of aqueous extract of Andrographis paniculata in rats. Clin Exp Pharmacol Physiol 23:675–678. https://doi.org/10.1111/j.1440-1681.1996.tb01756.x
Zhang W, Qi S, Xue X, Al Naggar Y, Wu L, Wang K (2021) Understanding the Gastrointestinal protective effects of polyphenols using foodomics-based approaches. Front Immunol 12:1–18. https://doi.org/10.3389/fimmu.2021.671150
Acknowledgements
The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES), the Federal University of Ceará and the Nucleus for Studies in Microscopy and Image Processing (NEMPI).
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This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
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JFR Writing—Original draft, Conceptualization, Methodology, Investigation; LCV Methodology, Formal Analysis, Investigation; Visualization; LCPAF Resources, Methodology, Formal Analysis, Conceptualization, Validation; TSA Formal analysis, Validation, Writing–Review and Editing; JJLN Formal analysis, Conceptualization; VVN Methodology, Formal Analysis; PMST Resources, Formal Analysis; DCSN-P Formal analysis, Investigation, Visualization, Resources; VCCG-C Methodology, Formal analysis, Investigation, Visualization; AFUC Writing- Review and Editing, Supervision, Project administration; EFM Writing- Review and Editing, Supervision, Project administration, Validation and Visualization.
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de Freitas Rocha, J., de Castro Viana, L., Filho, L.C.P.A. et al. In vitro anti-inflammatory activity and ameliorative effects on gastric ulcers of Licania rigida benth seed extract. Inflammopharmacol 31, 2631–2640 (2023). https://doi.org/10.1007/s10787-023-01283-0
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DOI: https://doi.org/10.1007/s10787-023-01283-0