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Chemical composition, antileishmanial and antioxidant activity of Eugenia moraviana (Myrtaceae) fruit extract

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Abstract

Leishmaniasis is a severe disease caused by protozoa of the genus Leishmania. The disease affects millions of people. Treatment is limited to only a few drugs that cause severe side effects. The identification of new compounds to treat leishmaniasis remains a challenge. This study aimed to determine the chemical composition of Eugenia moraviana fruit extract (EmCE) and to investigate its effect on the promastigote and amastigote forms of Leishmania amazonensis, the ultrastructural changes induced by it, its cytotoxicity, and antioxidant effect. Liquid chromatography–high-resolution mass spectrometry was used to identify EmCE components. Amastigote forms (IC50 0.6 µg mL−1) were more sensitive to EmCE treatment than promastigote forms (IC50 77.2 µg mL−1). The cytotoxicity concentration 50% was 187.8 µg mL−1 for J774.A1 macrophages and 190.0 µg mL−1 for murine macrophages, with selectivity index of 313 and 316.7, respectively. EmCE induced 14.7% hemolysis. Promastigotes exposed to EmCE experienced drastic ultrastructural changes, such as intense cytoplasm vacuolization and mitochondrial swelling. The antioxidant activity IC50 for DPPH was 0.78 µg mL−1, inhibition of lipid peroxidation was 56.4%, FRAP assays with 1.19 µM ferrous sulfate/mg sample, and total phenolic acid equivalent was 76.1 µg gallic acid/mg sample.EmCE was not cytotoxic, was highly selective for protozoans, and caused intracellular death of the parasite. The results indicated the potential value of EmCE in the treatment of leishmaniasis. These results are the first report of antileishmanial activity and chemical composition for E. moraviana fruits extract.

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References

  • Alam N, Bristi NJ, Rafiquzzaman (2013) Review on in vivo and in vitro methods evaluation of antioxidant activity. Saudi Pharm J 21:143–152

    PubMed  Google Scholar 

  • Almeida-Souza F, Taniwaki NN, Amaral ACF, Souza CS, Calabrese KS, Abreu-Silva AL (2016) Ultrastructural changes and death of Leishmania infantum promastigotes induced by Morinda citrifolia Linn. fruit (Noni) juice treatment. Evidence-Based Complement Altern Med 2016:5063540

    Google Scholar 

  • Alvar J, Croft SL, Kaye P, Khamesipour A, Sundar S, Reed SG (2013) Case study for a vaccine against leishmaniasis. Vaccine 31:B244–B249

    CAS  PubMed  Google Scholar 

  • Andrade MA, Azevedo CS, Motta FN, Santos ML, Silva C, Santana JM, Bastos IMD (2016) Essential oils: in vitro activity against Leishmania amazonensis, cytotoxicity and chemical composition. BMC Complement Alter Med 16:1–8

    Google Scholar 

  • Angélico EC, Costa JGM, Galvão FFR, Santos FO, Rodrigues OG (2012) Composição química do óleo essencial das folhas de Croton heliotropiifolius Kant (sinônimo C. rhamnifolius): Resultados preliminares. Rev Biol e Farmácia 7:57–61

    Google Scholar 

  • Apel MA, Sobral M (2002) Chemical composition of the essential oils from southern Brazilian Eugenia species. Part IV: section Racemulosae. J Ess Oil Res 14:3–6

    Google Scholar 

  • Asmari AA, Omani SA, Otaibi MA, Abdulaaly AA, Elfaki I, Al K, Arshaduddin M (2014) Gastroprotective effect of minocycline in experimentally induced gastric ulcers in rats. Int J Clin Exp Med 7:586–596

    PubMed  PubMed Central  Google Scholar 

  • Bagetti M, Maria E, Facco P, Piccolo J, Hirsch GE, Rodriguez-Amaya D, Kobori CN, Vizzotto M, Emanuelli T (2011) Physicochemical characterization and antioxidant capacity of pitanga fruits (Eugenia uniflora L.). Ciência e Tecnol Aliment 31:147–154

    Google Scholar 

  • Barreiros ALBS, David JM, David JP (2006) Oxidative stress: Relations between the formation of reactive species and the organism’s defense. Quim Nova 29:113–123

    CAS  Google Scholar 

  • Braga FG, Bouzada MLM, Fabri RL, Matos MO, Moreira FO, Scio E, Coimbra ES (2007) Antileishmanial and antifungal activity of plants used in traditional medicine in Brazil. J Ethnopharmacol 111:396–402

    PubMed  Google Scholar 

  • Brenton AG, Godfrey AR (2010) Accurate mass measurement: terminology and treatment of data. J Am Soc Mass Spectrom 21:1821–35

    CAS  PubMed  Google Scholar 

  • Castro LLD, Sprenger LK, Madrid IM, Oliveira FC, Oliveira PA, Castro LM, Berne MEA, Leite FPL (2019) In vitro and in vivo effect of Eugenia uniflora extracts on gastrointestinal nematode of sheep. Ciência Anim Bras 20:1–12

    Google Scholar 

  • Celli GB, Pereira-Netto AB, Beta T (2011) Comparative analysis of total phenolic content, antioxidante activity,and flavonoids profile of fruits from two varieties of Brazilian cherry (Eugenia uniflora L.) throughout the fruit developmental stages. Food Res Int 44:2442–2451

    CAS  Google Scholar 

  • Cota BB, Siqueira EP, Oliveira DM, Alves TMA, Sobral MEG, Rabello A, Zani CL (2012) Chemical constituents and leishmanicidal activity from leaves of Kielmeyera variabilis. Rev Bras Farmacogn 22:1253–1258

    CAS  Google Scholar 

  • Cunningham AC (2002) Parasitic adaptive mechanisms in infection by Leishmania. Exp Mol Pathol 72:132–141

    CAS  PubMed  Google Scholar 

  • Dagnino APA, Mesquita CS, Dorneles GP, Teixeira VON, Barros FMC, Ccana-Ccapatinta GV, Fonseca SG, Monteiro MC, Júnior LCR, Peres A, Von Poser GL, Roosevelt P, Romão T (2018) Phloroglucinol derivatives from Hypericum species trigger mitochondrial dysfunction in Leishmania amazonensis. Parasitology 14:25–53

    Google Scholar 

  • Ferreira CC, Marochio GG, Partata AK (2012) Estudo sobre a leishmaniose tegumentar americana com enfoque na farmacoterapia. Rev Científica ITPAC 5:2–10

    Google Scholar 

  • Filho VC, Meyre-Silva C, Niero R, Nathália L, Mariano B, Gomes F, Farias IV, Gazoni VF, Silva S, Giménez A, Gutierrez-Yapu D, Salamanca E, Malheiros A (2013) Evaluation of antileishmanial activity of selected brazilian plants and identification of the active principles. Evidence-Based Complement Altern Med 2013:265025

    Google Scholar 

  • Garcia MCF, Soares DC, Santana RC, Saraiva EM, Siani AC, Ramos MFS, Danelli MGM, Souto-Padron TC, Pinto-da-Silva LH (2018) The in vitro antileishmanial activity of essential oil from Aloysia gratissima and guaiol, its major sesquiterpene against Leishmania amazonensis. Parasitology 145:1219–1227

    CAS  PubMed  Google Scholar 

  • Gobbo-Neto L, Lopes NP (2007) Plantas medicinais: fatores de influência no conteúdo de metabólitos secundários. Quim Nov 30:374–381

    CAS  Google Scholar 

  • Govaerts R, Dransfield J, Zona S, Hodel DR, Henderson A (2019) World checklist of Myrtaceae. Facilitated by the Royal Botanic Gardens, Kew, http://wcsp.science.kew.org/

  • Hajdu Z, Hohmann J (2012) An ethnopharmacological survey of the traditional medicine utilized in the community of Porvenir, Bajo Paraguá Indian Reservation, Bolivia. J Ethnopharmacol 139:838–857

    PubMed  Google Scholar 

  • Hammi KM, Essid R, Tabbene O, Elkahoui S, Majdoub H, Ksouri R (2019) Antileishmanial activity of Moringa oleifera leaf extracts and potential synergy with amphotericin B. South African J Bot 1–7

  • Iqbal K, Iqbal J, Staerk D, Kongstad KT (2017) Characterization of antileishmanial compounds from Lawsonia inermis L. leaves using semi-high resolution antileishmanial profiling combined with. Front Phamacology 8:1–7

    Google Scholar 

  • Jiménez-Ruiz A, Alzate JF, Macleod ET, Lüder CGK, Fasel N, Hurd H (2010) Apoptotic markers in protozoan parasites. Parasit Vectors 2:1–15

    Google Scholar 

  • Lemos M, Santin JR, Júnior LCK, Niero R, Andrade SF (2011) Gastroprotective activity of hydroalcoholic extract obtained from the leaves of Brassica oleracea var. acephala DC in different animal models. J Ethnopharmacol 138:503–507

    PubMed  Google Scholar 

  • Lunardi I, Peixoto JLB, Silva CC, Shuquel ITA, Basso EA, Vidotti GJ (2001) Triterpenic acids from Eugenia moraviana. J Braz Chem Soc 12:180–183

    CAS  Google Scholar 

  • Magina MA, Gilioli A, Moresco HH, Colla G, Pizzolatti MG, Brighente IMC (2010) Atividade antioxidante de três espécies de Eugenia (Myrtaceae). Lat Am J Pharm 29:2383

    Google Scholar 

  • Mahmoud II, Marzouk MSA, Moharram FA, El-Gindi MR, Hassan AMK (2001) Acylated flavonol glycosides from Eugenia jambolana leaves. Phytochemistry 58:1239–1244

    CAS  PubMed  Google Scholar 

  • Mayer B, Oberbauer R (2003) Mitochondrial regulation of apoptosis. N. Physiol Sci 18:89–94

    CAS  Google Scholar 

  • McConville M, Handman E (2007) The molecular basis of Leishmania pathogenesis. Int J Parasitol 37:1047–1051

    CAS  PubMed  Google Scholar 

  • Mehwish S, Khan H, Rehman AU, Khan AU, Khan MA, Hayat O, Ahmad M, Wadood A, Ullah N (2019) Natural compounds from plants controlling leishmanial growth via DNA damage and inhibiting trypanothione reductase and trypanothione synthetase: an in vitro and in silico approach. 3 Biotech 9:303

    PubMed  Google Scholar 

  • Mello F, Paganelli CJ, Alberton MD (2017) Quantificação de fenóis e flavonóides totais e atividade antioxidante dos extratos de Eugenia catharinensis. I Simpósio Int em Investig Químico-Farmacêuticas, Univali, Itajaí/SC

  • Mittra B, Saha A, Chowdhury AR, Pal C, Mandal S, Mukhopadhyay S, Bandyopadhyay S, Majumder HK (2000) Luteolin, an abundant dietary component is a potent anti-leishmanial agent that acts by inducing topoisomerase II-mediated kinetoplast DNA. Mol Med 6:527–541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Monzote L, Piñón A, Setzer WN (2014) Antileishmanial potential of tropical rainforest plant extracts. Medicines 2:32–55

    Google Scholar 

  • Oliveira AM, Humberto MMS, Silva JM, Rocha RFA, Sant’ana AEG (2006) Estudo fitoquímico e avaliação das atividades moluscicida e larvicida dos extratos da casca do caule e folha de Eugenia malaccensis L. (Myrtaceae). Rev Bras Farmacogn 16:618–624

    Google Scholar 

  • Oliveira LFG, Gilbert B, Villa Bôas GK (2013) Potential for innovation in the treatment of leishmaniasis using plants and natural products as sources of new drugs. Rev Fitos 8:33–42

    Google Scholar 

  • Pan American Health Organization (2019) Leishmaniasis: Epidemiological Report of the Americas. Pan American Health Organization, Washington, www.paho.org/leishmaniasis

  • Queiroz JMG, Suzuki MCM, Motta APR, Nogueira JMR, Carvalho EM (2015) Popular and scientific aspects of Eugenia species use as herbal. Rev Fitos 9:73–159

    Google Scholar 

  • Reynertson KA, Yang H, Jiang B, Basile MJ, Kennelly EJ (2008) Quantitative analysis of antiradical phenolic constituents from fourteen edible Myrtaceae fruits. Food Chem 109:883–890

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha VPC, Rocha CQ, Queiroz EF, Marcourt L, Vilegas W, Grimaldi GB, Furrer P, Allémann É, Wolfender JL, Soares MBP (2019) Antileishmanial activity of dimeric flavonoids isolated from Arrabidaea brachypoda. Molecules 24:1–13

    Google Scholar 

  • Rodrigues JCF, Souza W (2008) Ultrastructural alterations in organelles of parasitic protozoa induced by different classes of metabolic inhibitors. Curr Pharm Des 14:925–938

    CAS  PubMed  Google Scholar 

  • Roesler R, Lorencini M, Pastore G (2010) Brazilian cerrado antioxidant sources: cytotoxicity and phototoxicity in vitro. Ciência e Tecnol Aliment 30:814–821

    Google Scholar 

  • Rufino MSM, Alves RE, Brito ES, Filho JM, Moreira AVB (2006a) Metodologia Científica: Determinação da atividade antioxidante total em frutas no sistema β-caroteno/ácido linoléico. Comun Técnico Embrapa 126:1–4

    Google Scholar 

  • Rufino MSM, Alves RE, Brito ES, Morais SM, Sampaio CDG, Pérez-Jiménez J, Saura-Calixto FD (2006b) Metodologia Científica: Determinação da atividade antioxidante total em frutas pelo método de redução do ferro (FRAP). Comun Técnico Embrapa 125:1–4

    Google Scholar 

  • Rufino MSM, Alves RE, Brito ES, Morais SM, Sampaio CG, Pérez-Jiménez J, Saura-Calixto FD (2007) Metodologia Científica: Determinação da atividade antioxidante total em frutas pela captura do radical livre DPPH. Comun Técnico Embrapa 127:1–4

    Google Scholar 

  • Santos AL, Polidoro AS, Cardoso CAL, Vieira C, Jacques RA, Caramão EB (2017) GC×GC/qMS analyses of Campomanesia guazumifolia (Cambess.) O. Berg essential oils and their antioxidant and antimicrobial activity. Nat Prod Res 6419:1–5

    Google Scholar 

  • Silva JKR, Andrade EHA, Barreto LH, Silva NCF, Ribeiro AF, Montenegro RC, Maia GS (2017) Chemical composition of four essential oils of Eugenia from the Brazilian Amazon and their cytotoxic and antioxidant activity. Medicines 4:2–11

    Google Scholar 

  • Simirgiotis MJ, Adachi S, To S, Yang H, Reynertson KA, Basile MJ, Gil RR, Weinstein IB, Kennelly EJ (2008) Cytotoxic chalcones and antioxidants from the fruits of Syzygium samarangense (Wax Jambu). Food Chem 107:813–819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh K, Garg G, Ali V, Ali V (2016) Current therapeutics, their problems and thiol metabolism as potential drug targets in Leishmaniasis. Curr Drug Metab 17:897–919

    CAS  PubMed  Google Scholar 

  • Tasdemir D, Kaiser M, Brun R, Yardley V, Schmidt TJ, Tosun F, Ruedi P (2006) Antitrypanosomal and antileishmanial activities of flavonoids and their analogues: in vitro, in vivo, structure-activity relationship, and quantitative structure-activity relationship studies. Antimicrob Agents Chemother 50:1352–1364

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tomborelli PM, Oliveira ML, Oliveira M, Costa DLMG (2018) Atividade antioxidante de extrato de Eugenia dysenterica a partir de diferente frações de solventes. São Luís/MA. 58° Congr Bras Química

  • Valdez RH, Tonin LTD, Ueda-Nakamura T, Filho BPD, Morgado-Diaz JA, Sarragiotto MH, Nakamura CV (2009) Biological activity of 1,2,3,4-tetrahydro-β-carboline-3-carboxamides against Trypanosoma cruzi. Acta Trop 110:7–14

    CAS  PubMed  Google Scholar 

  • Viegas FPD, Ferreira PF, Oliver JC, Silva NC, Dias ALT, Marques MJ, Soares MG (2019) Leishmanicidal and antimicrobial activity of primin and primin-containing extracts from Miconia willdenowii. Fitoterapia 138:104297

    CAS  PubMed  Google Scholar 

  • Vila-Nova NS, Morais SM, Falcão MJC, Bevilaqua CML, Rondon FCM, Wilson ME, Vieira IGP, Andrade HF (2012) Leishmanicidal and cholinesterase inhibiting activities of phenolic compounds of Dimorphandra gardneriana and Platymiscium ϔloribundum, native plants from Caatinga biome. Pesqui Veterinária Bras 32:1164–1168

    Google Scholar 

  • Viuda-Martos M, Navajas YR, Zapata ES, Fernández-López J, Pérez-Álvarez JA (2010) Antioxidant activity of essential oils of five spice plants widely used in a Mediterranean diet. Flavour Fragr J 25:13–19

    CAS  Google Scholar 

Download references

Acknowledgements

This study was financed in part by Fundação Araucária the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) Finance Code 001 and Complexo de Centrais de Apoio a Pesquisa (COMCAP).

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Authors and Affiliations

  1. Postgraduate Program in Health Sciences, Maringá State University, Maringá, Paraná, Brazil

    Fabiana Borges Padilha Ferreira, Áquila Carolina Fernandes Herculano Ramos-Milaré, Thaís Gomes Verzignassi Silveira & Maria Valdrinez Campana Lonardoni

  2. Postgraduate Program in Pharmaceutical Sciences, Maringá State University, Maringá, Paraná, Brazil

    Márcia Regina Pereira Cabral

  3. Department of Health Sciences, Laboratory of Innovation in Drug and Cosmetic Development, Maringá State University, Maringá, Paraná, Brazil

    Danielle Lazarin-Bidóia & Celso Vataru Nakamura

  4. Postgraduate Program in Chemistry, Maringá State University, Maringá, Paraná, Brazil

    Maria Helena Sarragiotto

  5. Postgraduate Program in Biotechnology Applied to Agriculture, University of Paranaense UNIPAR, Umuarama, Paraná State, Brazil

    Wanessa de Campos Bortolucci, Carla Maria Mariano Fernandez & Zilda Cristiani Gazim

  6. Federal University of Santa Catarina, Florianópolis, Santa Catarina State, Brazil

    Izabel Galhardo Demarchi

  7. Department of Clinical Analysis and Biomedicine, Maringá State University, Maringá, Paraná, Brazil

    Thaís Gomes Verzignassi Silveira & Maria Valdrinez Campana Lonardoni

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  1. Fabiana Borges Padilha Ferreira
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Ferreira, F.B.P., Ramos-Milaré, Á.C.F.H., Cabral, M.R.P. et al. Chemical composition, antileishmanial and antioxidant activity of Eugenia moraviana (Myrtaceae) fruit extract. Med Chem Res 29, 1621–1631 (2020). https://doi.org/10.1007/s00044-020-02588-3

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