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Journal of Natural Medicines
Published in: Journal of Natural Medicines 4/2016

01-10-2016 | Original Paper

Chemical composition and anti-inflammatory activity of the leaves of Byrsonima verbascifolia

Authors: Aline Aparecida Saldanha, Lucas Fernandes do Carmo, Sara Batista do Nascimento, Natália Alves de Matos, Clarice de Carvalho Veloso, Ana Hortência Fonsêca Castro, Ric C. H. De Vos, André Klein, João Máximo de Siqueira, Carlos Alexandre Carollo, Thalita Vieira do Nascimento, Mônica Cristina Toffoli-Kadri, Adriana Cristina Soares

Published in: Journal of Natural Medicines | Issue 4/2016

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Abstract

An ethnopharmacological survey indicates that the genus Byrsonima has some medicinal species that are commonly found in the Brazilian Cerrado and has been used as an anti-inflammatory and for gastroduodenal disorders. The aim of this study was to evaluate the anti-inflammatory and antioxidant activity along with qualitative chemical characterization of the methanolic extract of the leaves of Byrsonima verbascifolia (BvME) obtained by exhaustive percolation. The data from the chemical analyses by liquid chromatography–mass spectrometry led to tentative identification of 42 compounds belonging to proanthocyanidins, galloyl quinic acid derivatives, flavonoids, and triterpene glycoside derivatives. BvME contain flavonoids and show an antioxidative activity. The methanolic extract administered intraperitoneally at doses of 50, 100, or 300 mg/kg showed a significant reduction in paw edema and modulated the neutrophil influx in a mouse model. Furthermore, the anti-edematogenic activity of the extract provided in smaller doses (12.5 and 25 mg/kg) was also demonstrated in a mouse paw edema model. The extract inhibited NO production by macrophages induced by lipopolysaccharide. We presume that the anti-inflammatory effects of BvME are due to a combination of compounds present in B. verbascifolia, including catechins (procyanidins), flavonoids, and triterpene glycosides and that these anti-inflammatory actions should be mediated, at least partly, through the inhibition of NO production. This study supports and validates the ethnopharmacological uses of B. verbascifolia as an anti-inflammatory.
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Literature
1.
Mendanha DM, Ferreira HD, Felício LP, Silva EM, Pereira DG, Nunes WB, Carvalho S (2010) Modulatory effect of Byrsonima verbascifolia (Malpighiaceae) against damage induced by doxorubicin in somatic cells of Drosophila melanogaster. Genet Mol Res 9:69–77CrossRefPubMed
2.
Falcão HS, Lima IO, Santos VL, Dantas HF, Diniz MFFM, Barbosa-Filho JM, Batista LM (2005) Review of the plants with anti-inflammatory activity studied in Brazil. Braz J Pharmacogn 15:381–391CrossRef
3.
Martínez-Vázquez M, González-Esquinca AR, Luna LC, Gutiérrez MNN, García-Argaéz NA (1999) Antimicrobial activity of Byrsonima crassifolia (L.) H.B.K. J Ethnopharmacol 66:79–82CrossRefPubMed
4.
Pio Côrrea M (1978) Dicionário de Plantas Úteis do Brasil e das Exóticas Cultivadas. Ministério da Agricultura, Rio de Janeiro
5.
Guilhon-Simplicio F, Pereira MDM (2011) Chemical and pharmacological aspects of Byrsonima (Malpighiaceae). Quim Nova 34:1032–1041CrossRef
6.
Moreira LQ, Vilela FC, Orlandi L, Dias DF, Santos ALA, Silva MA, Paiva R, Alves da Silva G, Giusti-Paiva A (2011) Anti-inflammatory effect of extract and fractions from the leaves of Byrsonima intermedia A. Juss. in rats. J Ethnopharmacol 138:610–615CrossRefPubMed
7.
Santos RC, Kushima H, Rodrigues CM, Sannomiya M, Rocha LR, Bauab TM, Tamashiro J, Vilegas W, Hiruma-Lima CA (2012) Byrsonmima intermedia A. Juss.: gastric and duodenal anti-ulcer, antimicrobial, and antidiarrheal effects in experimental rodent models. J Ethnopharmacol 140:203–212CrossRefPubMed
8.
Higushi CT, Sannomiya M, Pavan FR, Leite SRA, Sato DN, Franzblau SG, Sacramento LVS, Vilegas W, Leite CQF (2011) Byrsonima fagifolia Niedenzu apolar compounds with anti-tubercular activity. Evid Based Complement Alternat Med 2011:128349
9.
Sannomiya M, Santos LC, Carbone V, Napolitano A, Piacente S, Pizza C, Souza-Brito AR, Vilegas W (2007) Liquid chromatography/electrospray ionization tandem mass spectrometry profiling of compounds from the infusion of Byrsonima fagifolia Niedenzu. Rapid Commun Mass Spectrom 21:1393–1400CrossRefPubMed
10.
Sannomiya M, Montoro P, Piacente S, Pizza C, Brito ARMS, Vilegas W (2005) Application of liquid chromatography/electrospray ionization tandem mass spectrometry to the analysis of polyphenolic compounds from an infusion of Byrsonima crassa Niedenzu. Rapid Commun Mass Spectrom 19:2244–2250CrossRefPubMed
11.
Rastrelli L, Tommasi N, Berger I, Caceres A, Saravia A, Simone F (1997) Glycolipids from Byrsonima crassifolia. Phytochemistry 45:647–650CrossRef
12.
Amarquaye A, Che CT, Bejar E, Malone MH, Fong HHS (1994) A new glycolipid from Byrsonima crassifolia. Planta Med 60:85–86CrossRefPubMed
13.
Aguiar RM, David JP, David JM (2005) Unusual naphthoquinones, catechin and triterpene from Byrsonima microphylla. Phytochemistry 66:2388–2392CrossRefPubMed
14.
Mendes CC, Cruz FG, David JM, Nascimento IP, David JP (1999) Triterpenes esterified with fatty and triterpene acids isolated from Byrsonima microphylla. Quim Nova 22:185–188CrossRef
15.
Panizza S (1998) Plantas que Curam: Cheiro de Mato. IBRASA, São Paulo
16.
Lopez A, Hudson JB, Towers GH (2001) Antiviral and antimicrobial activities of Colombian medicinal plants. J Ethnopharmacol 77:189–196CrossRefPubMed
17.
Khan MT, Ather A, Thompson KD, Gambari R (2005) Extracts and molecules from medicinal plants against herpes simplex viruses. Antiviral Res 67:107–119CrossRefPubMed
18.
Gonçalves CA, Siqueira JM, Carollo CA, Mauro MO, Davi N, Cunha-Laura AL, Monreal AC, Castro AH, Fernandes L, Chagas RR, Auharek SA, Oliveira RJ (2013) Gestational exposure to Byrsonima verbascifolia: teratogenicity, mutagenicity and immunomodulation evaluation in female Swiss mice. J Ethnopharmacol 3:843–850CrossRef
19.
Van der Hooft JJJ, Vervoort J, Bino RJ, de Vos RCH (2012) Spectral trees as a robust annotation tool in LC–MS based metabolomics. Metabolomics 8:691–703CrossRef
20.
Banov D, Baby AR, Del Bosco LM, Kaneko TM, Velasco MVR (2006) Caracterização do Extrato Seco de Ginkgo biloba L. em formulações de uso tópico. Acta Farm Bonaer 25:219–224
21.
Mensor LL, Menezes FS, Leitao GG, Reis AS, dos Santos TC, Coube CS, Leitão SG (2001) Screening of Brazilian plant extracts for antioxidant activity by the use of DPPH free radical method. Phytother Res 15:127–130CrossRefPubMed
22.
23.
Klein A, Talvani A, Silva PM, Martins MA, Wells TN, Proudfoot A, Luckacs NW, Teixeira MM (2001) Stem cell factor-induced leukotriene B4 production cooperates with eotaxin to mediate the recruitment of eosinophils during allergic pleurisy in mice. J Immunol 167:524–531CrossRefPubMed
24.
Moraes JRE, Moraes FR, Engrácia Filho JR (1998) Chloramphenicol restores the polymorphonuclear accumulation in carrageenin-induced pleurisy in diabetic rats. Braz J Vet Res Anim Sci 35:243–245
25.
Ding AH, Nathan CF, Stuehr DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal-macrophages—comparison of activating cytokines and evidence for independent production. J Immunol 141:2407–2412PubMed
26.
Mabry TJ, Markham KR, Thomas MB (1970) The systematic identification of flavonoids. Springer, New YorkCrossRef
27.
Van der Hooft JJJ, Vervoort J, Bino RJ, Beekwilder J, de Vos RCH (2011) Polyphenol identification based on systematic and robust high-resolution accurate mass spectrometry fragmentation. Anal Chem 83:409–416CrossRefPubMed
28.
Fabre N, Rustan I, Hoffmann E, Quetin-Leclercq J (2001) Determination of flavone, flavonol, and flavanone aglycones by negative ion liquid chromatography electrospray ion trap mass spectrometry. J Am Soc Mass Spectrom 12:707–715CrossRefPubMed
29.
Gu L, Kelm MA, Hammerstone JF, Zhang Z, Beecher G, Holden J, Haytowitz D, Prior RL (2003) Liquid chromatographic/electrospray ionization mass spectrometric studies of proanthocyanidins in foods. J Mass Spectrom 38:1272–1280CrossRefPubMed
30.
Li HJ, Deinzer ML (2006) Structural identification and distribution of proanthocyanidins in 13 different hops. J Agric Food Chem 54:4048–4056CrossRefPubMed
31.
Wagner H, Bladt S (2001) Plant drug analyses—a thin layer chromatography atlas. Springer, Berlin
32.
Dosseh C, Moretti C, Tessier AM, Delaveau P (1980) Chemical study on the leaves of Byrsonima verbascifolia Rich. ex Juss. J Plantes Med Phytother 14:136–142
33.
Lu CN, Yuan ZG, Zhang XL, Yan R, Zhao YQ, Liao M, Chen JX (2012) Saikosaponin a and its epimer saikosaponin d exhibit anti-inflammatory activity by suppressing activation of NF-κB signaling pathway. Int Immunopharmacol 14:121–126CrossRefPubMed
34.
An HJ, Kim IT, Park HJ, Kim HM, Choi JH, Lee KT (2011) Tormentic acid, a triterpenoid saponin, isolated from Rosa rugosa, inhibited LPS-induced iNOS, COX-2, and TNF-α expression through inactivation of the nuclear factor-κb pathway in RAW 264.7 macrophages. Int Immunopharmacol 11:504–510CrossRefPubMed
35.
Comalada M, Camuesco D, Sierra S, Ballester I, Xaus J, Gálvez J, Zarzuelo A (2005) In vivo quercitrin anti-inflammatory effect involves release of quercetin, which inhibits inflammation through down-regulation of the NF-κß pathway. Eur J Immunol 35:584–592CrossRefPubMed
36.
Sannomiya M, Fonseca VB, Silva MA, Rocha LR, Santos LC, Hiruma-Lima CA, Souza Brito AR, Vilegas W (2005) Flavonoids and anti-ulcerogenic activity from Byrsonima crassa leaves extracts. J Ethnopharmacol 97:1–6CrossRefPubMed
37.
Nardi GM, Felippi R, DalBó S, Siqueira-Junior JM, Arruda DC, Delle Monache F, Timbola AK, Pizzolatti MG, Ckless K, Ribeiro-do-valle RM (2003) Anti-inflammatory and antioxidant effects of Croton celtidifolius bark. Phytomedicine 10:176–184CrossRefPubMed
38.
Ibrahim T, Cunha JM, Madi K, Fonseca LM, Costa SS, Gonçalves KVL (2002) Immunomodulatory and anti-inflammatory effects of Kalanchoe brasiliensis. Int Immunopharmacol 2:875–883CrossRefPubMed
39.
Bispo MD, Mourão RHV, Franzotti EM, Bomfim KBR, Arrigoni-Blank MDF, Moreno MP, Marchioro M, Antoniolli AR (2001) Antinociceptive and anti-edematogenic effects of the aqueous extract of Hyptis pectinata leaves in experimental animals. J Ethnopharmacol 76:81–86CrossRefPubMed
40.
Schapoval EE, Vargas MR, Chaves CG, Bridi R, Zuanazzi JA, Henriques AT (1998) Anti-inflammatory and antinociceptive activities of extracts and isolated compounds from Stachytarpheta cayennensis. J Ethnopharmacol 60:53–59CrossRefPubMed
41.
Costa G, Francisco V, Lopes MC, Cruz MT, Batista MT (2012) Intracellular signaling pathways modulated by phenolic compounds: application for new anti-inflammatory drugs discovery. Curr Med Chem 19:2876–2900CrossRefPubMed
42.
Byun EB, Yang MS, Choi HG, Sung NY, Song DS, Sin SJ, Byun EH (2013) Quercetin negatively regulates TLR4 signaling induced by lipopolysaccharide through Tollip expression. Biochem Biophys Res Commun 431:698–705CrossRefPubMed
43.
Tuñón MJ, García-Mediavilla MV, Sánchez-Campos S, González-Gallego J (2009) Potential of flavonoids as anti-inflammatory agents: modulation of pro-inflammatory gene expression and signal transduction pathways. Curr Drug Metab 10:256–271CrossRefPubMed
44.
García-Mediavilla V, Crespo I, Collado PS, Esteller A, Sánchez-Campos S, Tuñón MJ, González-Gallego J (2007) The anti-inflammatory flavones quercetin and kaempferol cause inhibition of inducible nitric oxide synthase, cyclooxygenase-2 and reactive C-protein, and down-regulation of the nuclear factor kappaB pathway in Chang Liver cells. Eur J Pharmacol 557:221–229CrossRefPubMed
45.
Tang LQ, Wei W, Wang XY (2007) Effects and mechanisms of catechin for adjuvant arthritis in rats. Adv Ther 24:679–690CrossRefPubMed
46.
Terra X, Valls J, Vitrac X, Mérrilon JM, Arola L, Ardevol A, Bladé C, Fernandez-Larrea J, Pujadas G, Salvadó J, Blay M (2007) Grape-seed procyanidins act as anti-inflammatory agents in endotoxin-stimulated RAW 264.7 macrophages by inhibiting NFkB signaling pathway. J Agric Food Chem 55:4357–4365CrossRefPubMed
47.
Halliwell B, Rafter J, Jenner A (2005) Health promotion by flavonoids, tocopherols, tocotrienols, and other phenols: direct or indirect effects? Antioxidant or not? Am J Clin Nutr 81:268S–276SPubMed
48.
Azevedo MI, Pereira AF, Nogueira RB, Rolim FE, Brito GAC, Wong DVT, Lima Júnior RCP, Ribeiro RA, Vale ML (2013) The antioxidant effects of the flavonoids rutin and quercetin inhibit oxaliplatin-induced chronic painful peripheral neuropathy. Mol Pain 9:53CrossRefPubMedPubMedCentral
49.
Jung HJ, Nam JH, Choi J, Lee KT, Park HJ (2005) 19-Alpha-hydroxyursane-typetriterpenoids: anti-nociceptive anti-inflammatory principles of the roots of Rosa rugosa. Biol Pharm Bull 28:101–104CrossRefPubMed
50.
Francisco V, Figueirinha A, Neves BM, García-Rodríguez C, Lopes MC, Cruz MT, Batista MT (2011) Cymbopogon citratus as source of new and safe anti-inflammatory drugs: bio-guided assay using lipopolysaccharide-stimulated macrophages. J Ethnopharmacol 133:818–827CrossRefPubMed
51.
De Stefano D, Maiuri MC, Simeon V, Grassia G, Soscia A, Cinelli MP, Carnuccio R (2007) Lycopene, quercetin and tyrosol prevent macrophage activation induced by gliadin and IFN-gamma. Eur J Pharmacol 566:192–199CrossRef
52.
Saldanha AA, Soares AC (2015) Compostos químicos e aspectos botânicos, etnobotânicos e farmacológicos da Byrsonima verbascifolia Rich ex. A. Juss. Rev Bras Plantas Med 17:1000–1006CrossRef
Metadata
Title
Chemical composition and anti-inflammatory activity of the leaves of Byrsonima verbascifolia
Authors
Aline Aparecida Saldanha
Lucas Fernandes do Carmo
Sara Batista do Nascimento
Natália Alves de Matos
Clarice de Carvalho Veloso
Ana Hortência Fonsêca Castro
Ric C. H. De Vos
André Klein
João Máximo de Siqueira
Carlos Alexandre Carollo
Thalita Vieira do Nascimento
Mônica Cristina Toffoli-Kadri
Adriana Cristina Soares
Publication date
01-10-2016
Publisher
Springer Japan
Published in
Journal of Natural Medicines / Issue 4/2016
Print ISSN: 1340-3443
Electronic ISSN: 1861-0293
DOI
https://doi.org/10.1007/s11418-016-1011-3

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