Cytotoxicity, antiplasmodial and antimalarial effects of the spice and medicinal tree Schinus terebinthifolius

References

• Abubakar AR, Haque M. 2020. Preparation of medicinal plants: basic ­extraction and fractionation procedures for experimental purposes. J Pharm Bioallied Sci. 12(1):1–10. doi: 10.4103/jpbs.JPBS_175_19.
   PubMed Web of Science ®Google Scholar
• Albernaz LC, de Paula JE, Romero GAS, Silva MdRR, Grellier P, Mambu L, Espindola LS. 2010. Investigation of plant extracts in traditional medicine of the Brazilian Cerrado against protozoans and yeasts. J Ethnopharmacol. 131(1):116–121. doi: 10.1016/j.jep.2010.06.011.
   PubMed Web of Science ®Google Scholar
• Allard PM, Péresse T, Bisson J, Gindro K, Marcourt L, Pham VC, Roussi F, Litaudon M, Wolfender JL. 2016. Integration of molecular networking and in-silico MS/MS fragmentation for natural products dereplication. Anal Chem. 88(6):3317–3323. doi: 10.1021/acs.analchem.5b04804.
   PubMed Web of Science ®Google Scholar
• Almeida Barbosa LC, Demuner AJ, Clemente AD, de Paula VF, Ismail FMD. 2007. Seasonal variation in the composition of volatile oils from Schinus terebinthifolius raddi. Quím Nova. 30(8):1959–1965. doi: 10.1590/S0100-40422007000800030.
   Web of Science ®Google Scholar
• Andrade-Neto VF, Brandão MG, Oliveira FQ, Casali VW, Njaine B, Zalis MG, Oliveira LA, Krettli AU. 2004. Antimalarial activity of Bidens pilosa L. (Asteraceae) ethanol extracts from wild plants collected in various ­localities or plants cultivated in humus soil. Phytother Res. 18(8):634–639. doi: 10.1002/ptr.1510.
   PubMed Web of Science ®Google Scholar
• Arnoso BJdM, Da Costa GF, Schmidt B. 2019. Biodisponibilidade e classificação de compostos fenólicos. NB. 18(1):39–48. doi: 10.33233/nb.v18i1.1432.
   Google Scholar
• Arsianti A, Astuti H, Fadilah F, Martin Simadibrata D, Marie Adyasa Z, Amartya D, Bahtiar A, Tanimoto H, Kakiuchi K. 2018. Synthesis and in vitro antimalarial activity of alkyl esters of gallate as a growth inhibitor of Plasmodium falciparum. Orient J Chem. 34(2):655–662. doi: 10.13005/ojc/340207.
   Google Scholar
• Bendaoud H, Romdhane M, Souchard JP, Cazaux S, Bouajila J. 2010. Chemical composition and anticancer and antioxidant activities of Schinus molle L. and Schinus terebinthifolius Raddi berries essential oils. J Food Sci. 75(6):C466–472. doi: 10.1111/j.1750-3841.2010.01711.x.
   PubMed Web of Science ®Google Scholar
• Bézivin C, Tomasi S, Lohézic-Le Dévéhat F, Boustie J. 2003. Cytotoxic activity of some lichen extracts on murine and human cancer cell lines. Phytomedicine. 10(6-7):499–503. doi: 10.1078/094471103322331458.
   PubMed Web of Science ®Google Scholar
• Borenfreund E, Babich H, Martin-Alguacil N. 1988. Comparisons of two in vitro cytotoxicity assays - the neutral red (NR) and tetrazolium MTT tests. Toxicol in Vitro. 2(1):1–6. doi: 10.1016/0887-2333(88)90030-6.
   PubMed Web of Science ®Google Scholar
• Bourdy G, Willcox ML, Ginsburg H, Rasoanaivo P, Graz B, Deharo E. 2008. Ethnopharmacology and malaria: new hypothetical leads or old efficient antimalarials? Int J Parasitol. 38(1):33–41. doi: 10.1016/j.ijpara.2007.07.004.
   PubMed Web of Science ®Google Scholar
• Carvalho MG, Melo AGN, Aragão CFS, Raffin FN, Moura TFAL. 2013. Schinus terebinthifolius Raddi: chemical composition, biological properties and toxicity. Rev Bras Plantas Med. 15(1):158–169. doi: 10.1590/S1516-05722013000100022.
   Google Scholar
• Ceravolo IP, Aguiar AC, Adebayo JO, Krettli AU. 2021. Studies on activities and chemical characterization of medicinal plants in search for new antimalarials: a ten year review on ethnopharmacology. Front Pharmacol. 12:734263. doi: 10.3389/fphar.2021.734263.
   PubMed Web of Science ®Google Scholar
• Cos P, Vlietinck AJ, Berghe DV, Maes L. 2006. Anti-infective potential of natural products: how to develop a stronger in vitro ‘proof-of-concept. J Ethnopharmacol. 106(3):290–302. doi: 10.1016/j.jep.2006.04.003.
   PubMed Web of Science ®Google Scholar
• Coutinho JP, Aguiar ACC, dos Santos PA, Lima JC, Rocha MGL, Zani CL, Alves TMA, Santana AEG, Pereira MdM, Krettli AU. 2013. Aspidosperma (Apocynaceae) plant cytotoxicity and activity towards malaria parasites. Part I: Aspidosperma nitidum (Benth) used as a remedy to treat fever and malaria in the Amazon. Mem Inst Oswaldo Cruz. 108(8):974–982. doi: 10.1590/0074-0276130246.
   PubMed Web of Science ®Google Scholar
• da Silva MM, Iriguchi EKK, Kassuya CAL, Vieira MD, Foglio MA, de Carvalho JE, Ruiz ALTG, Souza KD, Formagio SN. 2017. Schinus terebinthifolius: phenolic constituents and in vitro antioxidant, antiproliferative and in vivo anti-inflammatory activities. Rev Bras Farmacogn. 27(4):445–452. doi: 10.1016/j.bjp.2016.12.007.
   Google Scholar
• da Silva JHS, Simas NK, Alviano CS, Alviano DS, Ventura JA, de Lima EJ, Seabra SH, Kuster RM. 2018. Anti-Escherichia coli activity of extracts from Schinus terebinthifolius fruits and leaves. Nat Prod Res. 32(11):1365–1368. doi: 10.1080/14786419.2017.1344657.
   PubMed Web of Science ®Google Scholar
• Da Silva RAD. 1926. Pharmacopeia dos Estados Unidos do Brasil: schinus terebinthifolius Raddi. Nacional.
   Google Scholar
• Dai P, Zhu L, Luo F, Lu L, Li Q, Wang L, Wang Y, Wang X, Hu M, Liu Z. 2015. Triple recycling processes impact systemic and local bioavailability of orally administered flavonoids. Aaps J. 17(3):723–736. doi: 10.1208/s12248-015-9732-x.
   PubMed Web of Science ®Google Scholar
• de Pilla Varotti F, Botelho AC, Andrade AA, de Paula RC, Fagundes EM, Valverde A, Mayer LM, Mendonça JS, de Souza MV, Boechat N, et al. 2008. Synthesis, antimalarial activity, and intracellular targets of MEFAS, a new hybrid compound derived from mefloquine and artesunate. Antimicrob Agents Chemother. 52(11):3868–3874. doi: 10.1128/AAC.00510-08.
   PubMed Web of Science ®Google Scholar
• do Céu de Madureira M, Paula Martins A, Gomes M, Paiva J, Proença da Cunha A, do Rosário V. 2002. Antimalarial activity of medicinal plants used in traditional medicine in S. Tomé and Príncipe islands. J Ethnopharmacol. 81(1):23–29. doi: 10.1016/s0378-8741(02)00005-3.
   PubMed Web of Science ®Google Scholar
• Ennigrou A, Casabianca H, Laarif A, Hanchi B, Hosni K. 2017. Maturation-related changes in phytochemicals and biological activities of the Brazilian pepper tree (Schinus terebinthifolius Raddi) fruits. S Afr J Bot. 108:407–415. doi: 10.1016/j.sajb.2016.09.005.
   Web of Science ®Google Scholar
• Fett Neto AGF, Dicosmo F. 1992. Distribution and amounts of taxol in different shoot parts of Taxus cuspidata. Planta Med. 58(5):464–466. doi: 10.1055/s-2006-961515.
   PubMed Web of Science ®Google Scholar
• Ganesh D, Fuehrer HP, Starzengrüber P, Swoboda P, Khan WA, Reismann JA, Mueller MS, Chiba P, Noedl H. 2012. Antiplasmodial activity of flavonol quercetin and its analogues in Plasmodium falciparum: evidence from clinical isolates in Bangladesh and standardized parasite clones. Parasitol Res. 110(6):2289–2295. doi: 10.1007/s00436-011-2763-z.
   PubMed Web of Science ®Google Scholar
• Gilbert B, Favoreto R. 2011. Schinus terebinthifolius Radii. Rev Fitos. 6(01):43–56. doi: 10.32712/2446-4775.2011.158.
   Google Scholar
• Gomes RBA, Souza ES, Barraqui NSG, Tosta CL, Nunes APF, Schuenck RP, Ruas FG, Ventura JA, Filgueiras PR, Kuster RM. 2020. Residues from the Brazilian pepper tree (Schinus terebinthifolius Raddi) processing industry: chemical profile and antimicrobial activity of extracts against hospital bacteria. Ind Crops Prod. 143:111430. doi: 10.1016/j.indcrop.2019.05.079.
   Web of Science ®Google Scholar
• Horai H, Arita M, Kanaya S, Nihei Y, Ikeda T, Suwa K, Ojima Y, Tanaka K, Tanaka S, Aoshima K, et al. 2010. MassBank: a public repository for sharing mass spectral data for life sciences. J Mass Spectrom. 45(7):703–714. doi: 10.1002/jms.1777.
   PubMed Web of Science ®Google Scholar
• Iwanaga CC, Ferreira LDAO, Bernuci KZ, Fernandez CMM, Lorenzetti FB, Sehaber CC, Vieira Frez FC, Bernardes SS, Panizzon GP, Linde GA, et al. 2019. In vitro antioxidant potential and in vivo effects of Schinus terebinthifolia Raddi leaf extract in diabetic rats and determination of chemical composition by HPLC-ESI-MS/MS. Nat Prod Res. 33(11):1655–1658. doi: 10.1080/14786419.2018.1425848.
   PubMed Web of Science ®Google Scholar
• Johann S, Sá NP, Lima LA, Cisalpino PS, Cota BB, Alves TM, Siqueira EP, Zani CL. 2010. Antifungal activity of schinol and a new biphenyl compound isolated from Schinus terebinthifolius against the pathogenic fungus Paracoccidioides brasiliensis. Ann Clin Microbiol Antimicrob. 9(1):30. doi: 10.1186/1476-0711-9-30.
   PubMedGoogle Scholar
• Krah E, de Kruijf J, Ragno L. 2018. Integrating traditional healers into the health care system: challenges and opportunities in rural Northern Ghana. J Community Health. 43(1):157–163. doi: 10.1007/s10900-017-0398-4.
   PubMed Web of Science ®Google Scholar
• Lahlou M. 2007. Screening of natural products for drug discovery. Expert Opin Drug Discov. 2(5):697–705. doi: 10.1517/17460441.2.5.697.
   PubMed Web of Science ®Google Scholar
• Lambros C, Vanderberg JP. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol. 65(3):418–420. doi: 10.2307/3280287.
   PubMed Web of Science ®Google Scholar
• Liu Y, Murakami N, Ji H, Abreu P, Zhang S. 2007. Antimalarial flavonol glycosides from Euphorbia hirta. Pharm Biol. 45(4):278–281. doi: 10.1080/13880200701214748.
   Web of Science ®Google Scholar
• Maciel AJ, Lacerda CP, Danielli LJ, Bordignon SAL, Fuentefria AM, Apel MA. 2019. Antichemotactic and antifungal action of the essential oils from Cryptocarya aschersoniana, Schinus terebinthifolia, and Cinnamomum amoenum. Chem Biodivers. 16(8):e1900204. doi: 10.1002/cbdv.201900204.
   PubMed Web of Science ®Google Scholar
• Matsuura HN, Malik S, de Costa F, Yousefzadi M, Mirjalili MH, Arroo R, Bhambra AS, Strnad M, Bonfill M, Fett-Neto AG. 2018. Specialized plant metabolism characteristics and impact on target molecule biotechnological production. Mol Biotechnol. 60(2):169–183. doi: 10.1007/s12033-017-0056-1.
   PubMed Web of Science ®Google Scholar
• Mekuria AB, Geta M, Birru EM, Gelayee DA. 2021. Antimalarial activity of seed extracts of Schinus molle against Plasmodium berghei in mice. J Evid Based Integr Med. 26:2515690X20984287. doi: 10.1177/2515690X20984287.
   PubMed Web of Science ®Google Scholar
• Morais TR, da Costa-Silva TA, Tempone AG, Borborema SE, Scotti MT, de Sousa RM, Araujo AC, de Oliveira A, de Morais SA, Sartorelli P, et al. 2014. Antiparasitic activity of natural and semi-synthetic tirucallane triterpenoids from Schinus terebinthifolius (Anacardiaceae): structure/activity relationships. Molecules. 19(5):5761–5776. doi: 10.3390/molecules19055761.
   PubMed Web of Science ®Google Scholar
• Morton JF. 1978. Brazilian pepper—its impact on people, animals and the environment. Econ Bot. 32(4):353–359. doi: 10.1007/BF02907927.
   Web of Science ®Google Scholar
• Moura-Costa GF, Nocchi SR, Ceole LF, de Mello JC, Nakamura CV, Dias Filho BP, Temponi LG, Ueda-Nakamura T. 2012. Antimicrobial activity of plants used as medicinals on an indigenous reserve in Rio das Cobras, Paraná, Brazil. J Ethnopharmacol. 143(2):631–638. doi: 10.1016/j.jep.2012.07.016.
   PubMed Web of Science ®Google Scholar
• Nocchi SR, Companhoni MV, de Mello JC, Dias Filho BP, Nakamura CV, Carollo CA, Silva DB, Ueda-Nakamura T. 2017. Antiviral activity of crude hydroethanolic extract from Schinus terebinthifolia against Herpes simplex Virus Type 1. Planta Med. 83(6):509–518. doi: 10.1055/s-0042-117774.
   PubMed Web of Science ®Google Scholar
• Oduola AM, Milhous WK, Weatherly NF, Bowdre JH, Desjardins RE. 1988. Plasmodium falciparum: induction of resistance to mefloquine in cloned strains by continuous drug exposure in vitro. Exp Parasitol. 67(2):354–360. doi: 10.1016/0014-4894(88)90082-3.
   PubMed Web of Science ®Google Scholar
• Oliveira D, Bastos DHM. 2011. Biodisponibilidade de ácidos fenólicos. Quím Nova. 34(6):1051–1056. doi: 10.1590/S0100-40422011000600023.
   Google Scholar
• Oliveira MBS, Valentim IB, Rocha TS, Santos JC, Pires KSN, Tanabe ELL, Borbely KSC, Borbely AU, Goulart MOF. 2020. Schinus terebenthifolius Raddi extracts: from sunscreen activity toward protection of the placenta to Zika virus infection, new uses for a well-known medicinal plant. Ind Crops Prod. 152:112503. doi: 10.1016/j.indcrop.2020.112503.
   PubMed Web of Science ®Google Scholar
• Penna-Coutinho J, Aguiar AC, Krettli AU. 2018. Commercial drugs containing flavonoids are active in mice with malaria and in vitro against chloroquine-resistant Plasmodium falciparum. Mem Inst Oswaldo Cruz. 113(12):e180279. doi: 10.1590/0074-02760180279.
   PubMed Web of Science ®Google Scholar
• Peters W. 1965. Drug resistance in Plasmodium berghei Vincke and Lips, 1948. I. Chloroquine Resistance. Exp Parasitol. 17(1):80–89. doi: 10.1016/0014-4894(65)90012-3.
   PubMed Web of Science ®Google Scholar
• Pires OC, Taquemasa AVC, Akisue G, Oliveira F, Araújo CEP. 2004. Análise preliminar da toxicidade aguda e dose letal mediana (DL50) ­comparativa entre os frutos de Pimenta-do-Reino do Brasil (Schinus terebinthifolius Raddi) e Pimenta do Reino Rangel ET. 2010. Atividade antiprotozoária, antifúngica e citotóxica de extratos de Plantas do bioma Cerrado, com ênfase em Leishmania (Leishmania) chagasi [doctoral thesis]. Brasília (DF): Universidade de Brasília.
   Google Scholar
• Rangel ET. 2010. Atividade antiprotozoária, antifúngica e citotóxica de extratos de Plantas do bioma Cerrado, com ênfase em Leishmania (Leishmania) chagasi. , Brasília, Brazil: Universidade de Brasília.
   Google Scholar
• Rasoanaivo P, Ramanitrahasimbola D, Rafatro H, Rakotondramanana D, Robijaona B, Rakotozafy A, Ratsimamanga-Urverg S, Labaïed M, Grellier P, Allorge L, et al. 2004. Screening extracts of Madagascan plants in search of antiplasmodial compounds. Phytother Res. 18(9):742–747. doi: 10.1002/ptr.1533.
   PubMed Web of Science ®Google Scholar
• Rasoanaivo P, Wright CW, Willcox ML, Gilbert B. 2011. Whole plant extracts versus single compounds for the treatment of malaria: synergy and positive interactions. Malar J. 10(Suppl 1):S4. doi: 10.1186/1475-2875-10-S1-S4.
   PubMed Web of Science ®Google Scholar
• Salem MZM, El-Hefny M, Ali HM, Elansary HO, Nasser RA, El-Settawy AAA, El Shanhorey N, Ashmawy NA, Salem AZM. 2018. Antibacterial activity of extracted bioactive molecules of Schinus terebinthifolius ripened fruits against some pathogenic bacteria. Microb Pathog. 120:119–127. doi: 10.1016/j.micpath.2018.04.040.
   PubMed Web of Science ®Google Scholar
• Schmourlo G, Mendonça-Filho RR, Alviano CS, Costa SS. 2005. Screening of antifungal agents using ethanol precipitation and bioautography of medicinal and food plants. J Ethnopharmacol. 96(3):563–568. doi: 10.1016/j.jep.2004.10.007.
   PubMed Web of Science ®Google Scholar
• Siqueira EP, Ceravolo IP, Kohlhoff M, Krettli AU, Zani CL. 2018. Synthesis and antiplasmodial activity of 2-methyl-3-carboxyl-naphtho [2, 3-B] furan quinone derivatives. J Med Chem Drug Des. 1(2). doi: 10.16966/2578-9589.108.
   Google Scholar
• Smilkstein M, Sriwilaijaroen N, Kelly JX, Wilairat P, Riscoe M. 2004. Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob Agents Chemother. 48(5):1803–1806. doi: 10.1128/AAC.48.5.1803-1806.2004.
   PubMed Web of Science ®Google Scholar
• Somsak V, Damkaew A, Onrak P. 2018. Antimalarial activity of kaempferol and its combination with chloroquine in Plasmodium berghei infection in mice. J Pathog. 2018:3912090–3912097. doi: 10.1155/2018/3912090.
   PubMedGoogle Scholar
• Tasdemir D, Lack G, Brun R, Rüedi P, Scapozza L, Perozzo R. 2006. Inhibition of Plasmodium falciparum fatty acid biosynthesis: evaluation of FabG, FabZ, and FabI as drug targets for flavonoids. J Med Chem. 49(11):3345–3353. doi: 10.1021/jm0600545.
   PubMed Web of Science ®Google Scholar
• Trager W, Jensen JB. 1976. Human malaria parasites in continuous culture. Science. 193(4254):673–675. doi: 10.1126/science.781840.
   PubMed Web of Science ®Google Scholar
• Varela-Barca FN, Agnez-Lima LF, de Medeiros SR. 2007. Base excision repair pathway is involved in the repair of lesions generated by flavonoid-enriched fractions of pepper tree (Schinus terebinthifolius, Raddi) stem bark. Environ Mol Mutagen. 48(8):672–681. doi: 10.1002/em.20334.
   PubMed Web of Science ®Google Scholar
• WHO. 2018. Global Malaria Programme, Status report: artemisinin and artemisinin-based combination therapy resistance. Available from: https://apps.who.int/iris/handle/10665/274362.
   Google Scholar
• WHO. 2019a. Geneva: global report on traditional and complementary medicine, ISBN 9789241515436. Available from: https://apps.who.int/iris/handle/10665/312342.
   Google Scholar
• WHO. 2019b. World malaria report 2019. Available from: https://www.who.int/publications/i/item/9789241565721.
   Google Scholar
• WHO. 2021. World malaria report 2021. Available from: https://www.who.int/publications/i/item/9789240015791.
   Google Scholar
• WHO. 2023. World malaria report 2023. Available from: https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2023.
   Google Scholar
• Willcox ML, Bodeker G. 2004. Traditional herbal medicines for malaria. BMJ. 329(7475):1156–1159. doi: 10.1136/bmj.329.7475.1156.
   PubMedGoogle Scholar
• Yendo ACA, De Costa F, Fleck JD, Gosmann G, Fett-Neto AG. 2015. Irradiance-based treatments of Quillaja brasiliensis leaves (A. St.-Hil. & Tul.) Mart. as means to improve immunoadjuvant saponin yield. Ind Crops Prod. 74:228–233. doi: 10.1016/j.indcrop.2015.04.052.
   Web of Science ®Google Scholar