Fruiting increases total content of flavonoids and antiproliferative effects of Cereus jamacaru D.C. cladodes in sarcoma 180 cells in vitro
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摘要
Objective: To evaluate the influence of fruiting phenological stage on total flavonoid content, antioxidant activity, and antiproliferative effects of Cereus jamacaru(C. jamacaru)(mandacaru) cladodes and fruit. Methods: Fruit and cladodes at vegetative and fruiting stage of C. jamacaru were collected. The fruit was dissected and bark, pulp, and seeds were separated. Vegetative and fruiting cladodes, together with bark, pulp, and seeds were used to obtain five hydroalcoholic extracts. The extracts were investigated for total flavonoid content, using AlCl3 colorimetric method, antioxidant activity by 2,2-diphenyl-1-picrylhydrazyl and 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) radical scavenging capacity and Fe~(2+) ion chelating activity, and in vitro antiproliferative effects(sarcoma 180 cells) by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2 H-tetrazolium bromide assay. Results: The extract of C. jamacaru cladodes at the fruiting stage showed higher flavonoid content compared to the other extracts. Seed extracts showed the highest antioxidant activity in 2,2-diphenyl-1-picrylhydrazyl and 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) assays, and the extract of cladodes at vegetative stage showed better antioxidant activity in Fe~(2+) ion chelating activity. The extract of fruiting cladodes promoted higher antiproliferative effects compared to the other extracts. Conclusions: These findings suggest that fruiting increases the content of flavonoids and antiproliferative effects of C. jamacaru cladodes. Data reinforce the potential use of C. jamacaru cladodes and fruits as natural antioxidants and potent anticancer agent.
Objective: To evaluate the influence of fruiting phenological stage on total flavonoid content, antioxidant activity, and antiproliferative effects of Cereus jamacaru(C. jamacaru)(mandacaru) cladodes and fruit. Methods: Fruit and cladodes at vegetative and fruiting stage of C. jamacaru were collected. The fruit was dissected and bark, pulp, and seeds were separated. Vegetative and fruiting cladodes, together with bark, pulp, and seeds were used to obtain five hydroalcoholic extracts. The extracts were investigated for total flavonoid content, using AlCl3 colorimetric method, antioxidant activity by 2,2-diphenyl-1-picrylhydrazyl and 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) radical scavenging capacity and Fe~(2+) ion chelating activity, and in vitro antiproliferative effects(sarcoma 180 cells) by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2 H-tetrazolium bromide assay. Results: The extract of C. jamacaru cladodes at the fruiting stage showed higher flavonoid content compared to the other extracts. Seed extracts showed the highest antioxidant activity in 2,2-diphenyl-1-picrylhydrazyl and 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) assays, and the extract of cladodes at vegetative stage showed better antioxidant activity in Fe~(2+) ion chelating activity. The extract of fruiting cladodes promoted higher antiproliferative effects compared to the other extracts. Conclusions: These findings suggest that fruiting increases the content of flavonoids and antiproliferative effects of C. jamacaru cladodes. Data reinforce the potential use of C. jamacaru cladodes and fruits as natural antioxidants and potent anticancer agent.
Objective: To evaluate the influence of fruiting phenological stage on total flavonoid content, antioxidant activity, and antiproliferative effects of Cereus jamacaru(C. jamacaru)(mandacaru) cladodes and fruit. Methods: Fruit and cladodes at vegetative and fruiting stage of C. jamacaru were collected. The fruit was dissected and bark, pulp, and seeds were separated. Vegetative and fruiting cladodes, together with bark, pulp, and seeds were used to obtain five hydroalcoholic extracts. The extracts were investigated for total flavonoid content, using AlCl3 colorimetric method, antioxidant activity by 2,2-diphenyl-1-picrylhydrazyl and 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) radical scavenging capacity and Fe~(2+) ion chelating activity, and in vitro antiproliferative effects(sarcoma 180 cells) by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2 H-tetrazolium bromide assay. Results: The extract of C. jamacaru cladodes at the fruiting stage showed higher flavonoid content compared to the other extracts. Seed extracts showed the highest antioxidant activity in 2,2-diphenyl-1-picrylhydrazyl and 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulfonic acid) assays, and the extract of cladodes at vegetative stage showed better antioxidant activity in Fe~(2+) ion chelating activity. The extract of fruiting cladodes promoted higher antiproliferative effects compared to the other extracts. Conclusions: These findings suggest that fruiting increases the content of flavonoids and antiproliferative effects of C. jamacaru cladodes. Data reinforce the potential use of C. jamacaru cladodes and fruits as natural antioxidants and potent anticancer agent.
引文
[1]de Lucena CM,Alves CAB,Pereira DD,Nunes EN,Costa GM,da Silva Costa GG,et al.Use and knowledge of Cactaceae in Northeastern Brazil.JEthnobiol Ethnomed 2013;9(1):62.
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[3]da Silva Darci DM,Ronielson FR de SC,Gabriel AGM,Peron AP.Cytotoxic action of the stem aqueous extract of the stem of Cereus jamacaru DC.(mandacaru).Rev Cuba Plantas Med 2015;19(2):226-234.
[4]Dutra JCV,Moisés Ferreira J,Pereira PRC,Ben-Hur de Oliveira J,Vitorino Gervásio S,Bernardes Xavier M,et al.Cereus jamacaru DC hydroalcoholic extract promotes anti-cytotoxic and antitumor activity.Pharmaceuticals 2018;11(4):130.
[5]Pretti IR,da Luz AC,Jamal CM,Batitucci MCP.Variation of biochemical and antioxidant activity with respect to the phenological stage of Tithonia diversifolia Hemsl.(Asteraceae)populations.Ind Crops Prod 2018;121:241-249.
[6]dos Santos PC,Dutra JCV,Delarmelina JM,Tose LV,Rom?o W,Jamal CM,et al.Coriandrum sativum grown under organic or chemical fertilizer effectively prevents DNA damage:Preliminary phytochemical screening,flavonoid content,ESI(-)FT-ICR MS,in vitro antioxidant and in vivo(mice bone marrow)antimutagenic activity against cyclophosphamide.Asian Pac JTrop Biomed 2018;8(6):292.
[7]Oliveira JB de,Dutra JCV,Gervásio SV,Xavier MB,Pereira PRC,Mota MM,et al.Bauhinia sp.sob diferentes condi??es de sazonalidade induz atividade anticancer em sarcoma-180 in vitro.In:Natiéli Piovesan VBV(ed).Produ??o e controle de produtos naturais.Atena Editora:Ponta Grossa;2018,p.42-59.
[8]Santos VS,Dutra JCV,Gervásio SV,Pereira PRC,Mota MM,Santos PC,et al.Coriandrum sativum em estádio vegetativo e flora??o induz atividade anticancer in vitro.In:Natiéli Piovesan VBV(ed).Produ??o e controle de produtos naturais.Atena Editora:Ponta Grossa;2018,p.69-82.
[9]Gomes VGN,Quirino ZGM,Araujo HFP.Frugivory and seed dispersal by birds in Cereus jamacaru DC.ssp.jamacaru(Cactaceae)in the Caatinga of Northeastern Brazil.Brazilian J Biol 2014;74(1):32-40.
[10]Fuertes MA,Castilla J,Alonso C,Prez JM.Cisplatin biochemical mechanism of action:From cytotoxicity to induction of cell death through interconnections between apoptotic and necrotic pathways.Curr Med Chem2003;10(3):257-266.
[11]Belcavello L,Dutra JCV,de Freitas JV,Aranha IP,Batitucci MCP.Mutagenicity of ipriflavone in vivo and in vitro.Food Chem Toxicol 2012;50(3-4):996-1000.Doi:10.1016/j.fct.2011.12.013.
[12]Santana AF.Composi??o química e atividades antioxidante e biológica das fra??es clorofórmica e hidrometanólica do extrato da raiz de Cereus jamacaru DC.(Cactaceae).Dissertation Thesis.Feira de Santana State University;2016.
[13]Jia ZS,Tang MC,Wu JM.The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals.Food Chem1999;64(4):555-559.
[14]Rufino MSM,Alves RE,Brito ES,Morais SM,Sampaio CG,PérezJiménez J,et al.Comunicado técnico-metodologia científica:Determina??o da atividade antioxidante total em frutas pela captura do radical livre DPPH.Fortaleza:Embrapa 2007;1(1):1-4.
[15]Rufino M,Alves RE,de Brito ES,de Morais SM,Sampaio C de G,Pérez-Jimenez J,et al.Metodologia científica:Determina??o da atividade antioxidante total em frutas pela captura do radical livre ABTS·+.Embrapa Agroindústria Trop Comun Técnico 2007;1(1):1-4.
[16]Soler-Rivas C,Espín JC,Wichers HJ.An easy and fast test to compare total free radical scavenger capacity of foodstuffs.Phytochem Anal An Int J Plant Chem Biochem Tech 2000;11(5):330-338.
[17]Cirak C,Radusiene J,Ivanauskas L,Jakstas V,?ama?N,Kurt D.Phenological changes in the chemical content of wild and greenhousegrown Hypericum pruinatum:Hypericins,gyperforins and phenolic acids.JBot 2015;4(3):37-47.
[18]Okunlola GO,Jimoh MA,Olatunji OA,Olowolaju ED.Comparative study of the phytochemical contents of Cochorus olitorius and Amaranthus hybridus at different stages of growth.Ann West Univ Timisoara Ser Biol 2017;20(1):43.
[19]King AMY,Young G.Characteristics and occurrence of phenolic phytochemicals.J Am Diet Assoc 1999;99(2):213-218.
[20]Arba M,Falisse A,Choukr-Allah R,Sindic M.Effect of irrigation at critical stages on the phenology of flowering and fruiting of the cactus Opuntia spp.Brazilian J Biol 2018;78(4):653-660.
[21]de Sousa Araújo TA,Alencar NL,de Amorim ELC,de Albuquerque UP.A new approach to study medicinal plants with tannins and flavonoids contents from the local knowledge.J Ethnopharmacol 2008;120(1):72-80.
[22]Lima RKB.Caracteriza??o e potencial antioxidante do fruto da palma(Tacinga inamoena)e do mandacaru(Cereus jamacaru).Dissertation Thesis.Federal Rural University of the Semi-Arid;2016.
[23]Genskowsky E,Puente LA,Pérez-álvarez JA,Fernández-López J,Mu?oz LA,Viuda-Martos M.Determination of polyphenolic profile,antioxidant activity and antibacterial properties of maqui[Aristotelia chilensis(Molina)Stuntz]a Chilean blackberry.J Sci Food Agric 2016;96(12):4235-4242.
[24]?í?M,?í?ováH,Denev P,Kratchanova M,Slavov A,Lojek A.Different methods for control and comparison of the antioxidant properties of vegetables.Food Control 2010;21(4):518-523.
[25]Shahidi F,Zhong Y.Measurement of antioxidant activity.J Funct Foods2015;18:757-781.
[26]Torres N,Goicoechea N,Morales F,Antolín MC.Berry quality and antioxidant properties in Vitis vinifera cv.Tempranillo as affected by clonal variability,mycorrhizal inoculation and temperature.Crop Pasture Sci 2016;67(9):961-977.
[27]Sadras VO,Moran MA.Nonlinear effects of elevated temperature on grapevine phenology.Agric For Meteorol 2013;173:107-115.
[28]Kavamura VN,Taketani RG,Lan?oni MD,Andreote FD,Mendes R,de Melo IS.Water regime influences bulk soil and rhizosphere of Cereus jamacaru bacterial communities in the Brazilian Caatinga biome.PLo S One2013;8(9):e73606.
[29]Sumaya-Martínez MT,Cruz-Jaime S,Madrigal-Santillán E,GarcíaParedes JD,Cari?o-Cortés R,Cruz-Cansino N,et al.Betalain,acid ascorbic,phenolic contents and antioxidant properties of purple,red,yellow and white cactus pears.Int J Mol Sci 2011;12(10):6452-6468.
[30]Korres NE,Norsworthy JK,Tehranchian P,Gitsopoulos TK,Loka DA,Oosterhuis DM,et al.Cultivars to face climate change effects on crops and weeds:A review.Agron Sustain Dev 2016;36(1):12.
[31]Misra A.Studies on biochemical and physiological aspects in relation to phyto-medicinal qualities and efficacy of the active ingredients during the handling,cultivation and harvesting of the medicinal plants.J Med Plants Res 2009;3(13):1140-1146.
[32]Manikandaselvi S,Vadivel V,Brindha P.Studies on physicochemical and nutritional properties of aerial parts of Cassia occidentalis L.J Food Drug Anal 2016;24(3):508-515.
[33]Fiehn O.Metabolomics-the link between genotypes and phenotypes.Plant Mol Biol 2002;48(2):155-171.
[34]Kayesh E,Shangguan L,Korir NK,Sun X,Bilkish N,Zhang Y,et al.Fruit skin color and the role of anthocyanin.Acta Physiol Plant 2013;35(10):2879-2890.
[35]Tanaka Y,Sasaki N,Ohmiya A.Biosynthesis of plant pigments:Anthocyanins,betalains and carotenoids.Plant J 2008;54(4):733-749.
[36]Mc Cann D,Barrett A,Cooper A,Crumpler D,Dalen L,Grimshaw K,et al.Food additives and hyperactive behaviour in 3-year-old and 8/9-yearold children in the community:A randomised,double-blinded,placebocontrolled trial.Lancet 2007;370(9598):1560-1567.
[37]Piccolella S,Crescente G,Pacifico F,Pacifico S.Wild aromatic plants bioactivity:A function of their(poly)phenol seasonality?A case study from Mediterranean area.Phytochem Rev 2018;17(4):785-799.
[38]Dewick PM.The shikimate pathway:Aromatic amino acids and phenylpropanoids.Medicinal natural products:A biosynthetic approach.3rd ed.Nottingham,U.K;John Wiley&Sons;2009,p.137-186.
[39]Vogt T.Phenylpropanoid biosynthesis.Mol Plant 2010;3(1):2-20.
[2]Souza I,Lima MCA,Melo UBC,Higino JS.Antitumour properties of Cereus jamacaru on an experimental model of cancer in vivo.Fund Clin Pharmacol 2001;15(Suppl 1):148.Doi:https://doi.org/10.1046/j.1472-8206.2001.00113.x.
[3]da Silva Darci DM,Ronielson FR de SC,Gabriel AGM,Peron AP.Cytotoxic action of the stem aqueous extract of the stem of Cereus jamacaru DC.(mandacaru).Rev Cuba Plantas Med 2015;19(2):226-234.
[4]Dutra JCV,Moisés Ferreira J,Pereira PRC,Ben-Hur de Oliveira J,Vitorino Gervásio S,Bernardes Xavier M,et al.Cereus jamacaru DC hydroalcoholic extract promotes anti-cytotoxic and antitumor activity.Pharmaceuticals 2018;11(4):130.
[5]Pretti IR,da Luz AC,Jamal CM,Batitucci MCP.Variation of biochemical and antioxidant activity with respect to the phenological stage of Tithonia diversifolia Hemsl.(Asteraceae)populations.Ind Crops Prod 2018;121:241-249.
[6]dos Santos PC,Dutra JCV,Delarmelina JM,Tose LV,Rom?o W,Jamal CM,et al.Coriandrum sativum grown under organic or chemical fertilizer effectively prevents DNA damage:Preliminary phytochemical screening,flavonoid content,ESI(-)FT-ICR MS,in vitro antioxidant and in vivo(mice bone marrow)antimutagenic activity against cyclophosphamide.Asian Pac JTrop Biomed 2018;8(6):292.
[7]Oliveira JB de,Dutra JCV,Gervásio SV,Xavier MB,Pereira PRC,Mota MM,et al.Bauhinia sp.sob diferentes condi??es de sazonalidade induz atividade anticancer em sarcoma-180 in vitro.In:Natiéli Piovesan VBV(ed).Produ??o e controle de produtos naturais.Atena Editora:Ponta Grossa;2018,p.42-59.
[8]Santos VS,Dutra JCV,Gervásio SV,Pereira PRC,Mota MM,Santos PC,et al.Coriandrum sativum em estádio vegetativo e flora??o induz atividade anticancer in vitro.In:Natiéli Piovesan VBV(ed).Produ??o e controle de produtos naturais.Atena Editora:Ponta Grossa;2018,p.69-82.
[9]Gomes VGN,Quirino ZGM,Araujo HFP.Frugivory and seed dispersal by birds in Cereus jamacaru DC.ssp.jamacaru(Cactaceae)in the Caatinga of Northeastern Brazil.Brazilian J Biol 2014;74(1):32-40.
[10]Fuertes MA,Castilla J,Alonso C,Prez JM.Cisplatin biochemical mechanism of action:From cytotoxicity to induction of cell death through interconnections between apoptotic and necrotic pathways.Curr Med Chem2003;10(3):257-266.
[11]Belcavello L,Dutra JCV,de Freitas JV,Aranha IP,Batitucci MCP.Mutagenicity of ipriflavone in vivo and in vitro.Food Chem Toxicol 2012;50(3-4):996-1000.Doi:10.1016/j.fct.2011.12.013.
[12]Santana AF.Composi??o química e atividades antioxidante e biológica das fra??es clorofórmica e hidrometanólica do extrato da raiz de Cereus jamacaru DC.(Cactaceae).Dissertation Thesis.Feira de Santana State University;2016.
[13]Jia ZS,Tang MC,Wu JM.The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals.Food Chem1999;64(4):555-559.
[14]Rufino MSM,Alves RE,Brito ES,Morais SM,Sampaio CG,PérezJiménez J,et al.Comunicado técnico-metodologia científica:Determina??o da atividade antioxidante total em frutas pela captura do radical livre DPPH.Fortaleza:Embrapa 2007;1(1):1-4.
[15]Rufino M,Alves RE,de Brito ES,de Morais SM,Sampaio C de G,Pérez-Jimenez J,et al.Metodologia científica:Determina??o da atividade antioxidante total em frutas pela captura do radical livre ABTS·+.Embrapa Agroindústria Trop Comun Técnico 2007;1(1):1-4.
[16]Soler-Rivas C,Espín JC,Wichers HJ.An easy and fast test to compare total free radical scavenger capacity of foodstuffs.Phytochem Anal An Int J Plant Chem Biochem Tech 2000;11(5):330-338.
[17]Cirak C,Radusiene J,Ivanauskas L,Jakstas V,?ama?N,Kurt D.Phenological changes in the chemical content of wild and greenhousegrown Hypericum pruinatum:Hypericins,gyperforins and phenolic acids.JBot 2015;4(3):37-47.
[18]Okunlola GO,Jimoh MA,Olatunji OA,Olowolaju ED.Comparative study of the phytochemical contents of Cochorus olitorius and Amaranthus hybridus at different stages of growth.Ann West Univ Timisoara Ser Biol 2017;20(1):43.
[19]King AMY,Young G.Characteristics and occurrence of phenolic phytochemicals.J Am Diet Assoc 1999;99(2):213-218.
[20]Arba M,Falisse A,Choukr-Allah R,Sindic M.Effect of irrigation at critical stages on the phenology of flowering and fruiting of the cactus Opuntia spp.Brazilian J Biol 2018;78(4):653-660.
[21]de Sousa Araújo TA,Alencar NL,de Amorim ELC,de Albuquerque UP.A new approach to study medicinal plants with tannins and flavonoids contents from the local knowledge.J Ethnopharmacol 2008;120(1):72-80.
[22]Lima RKB.Caracteriza??o e potencial antioxidante do fruto da palma(Tacinga inamoena)e do mandacaru(Cereus jamacaru).Dissertation Thesis.Federal Rural University of the Semi-Arid;2016.
[23]Genskowsky E,Puente LA,Pérez-álvarez JA,Fernández-López J,Mu?oz LA,Viuda-Martos M.Determination of polyphenolic profile,antioxidant activity and antibacterial properties of maqui[Aristotelia chilensis(Molina)Stuntz]a Chilean blackberry.J Sci Food Agric 2016;96(12):4235-4242.
[24]?í?M,?í?ováH,Denev P,Kratchanova M,Slavov A,Lojek A.Different methods for control and comparison of the antioxidant properties of vegetables.Food Control 2010;21(4):518-523.
[25]Shahidi F,Zhong Y.Measurement of antioxidant activity.J Funct Foods2015;18:757-781.
[26]Torres N,Goicoechea N,Morales F,Antolín MC.Berry quality and antioxidant properties in Vitis vinifera cv.Tempranillo as affected by clonal variability,mycorrhizal inoculation and temperature.Crop Pasture Sci 2016;67(9):961-977.
[27]Sadras VO,Moran MA.Nonlinear effects of elevated temperature on grapevine phenology.Agric For Meteorol 2013;173:107-115.
[28]Kavamura VN,Taketani RG,Lan?oni MD,Andreote FD,Mendes R,de Melo IS.Water regime influences bulk soil and rhizosphere of Cereus jamacaru bacterial communities in the Brazilian Caatinga biome.PLo S One2013;8(9):e73606.
[29]Sumaya-Martínez MT,Cruz-Jaime S,Madrigal-Santillán E,GarcíaParedes JD,Cari?o-Cortés R,Cruz-Cansino N,et al.Betalain,acid ascorbic,phenolic contents and antioxidant properties of purple,red,yellow and white cactus pears.Int J Mol Sci 2011;12(10):6452-6468.
[30]Korres NE,Norsworthy JK,Tehranchian P,Gitsopoulos TK,Loka DA,Oosterhuis DM,et al.Cultivars to face climate change effects on crops and weeds:A review.Agron Sustain Dev 2016;36(1):12.
[31]Misra A.Studies on biochemical and physiological aspects in relation to phyto-medicinal qualities and efficacy of the active ingredients during the handling,cultivation and harvesting of the medicinal plants.J Med Plants Res 2009;3(13):1140-1146.
[32]Manikandaselvi S,Vadivel V,Brindha P.Studies on physicochemical and nutritional properties of aerial parts of Cassia occidentalis L.J Food Drug Anal 2016;24(3):508-515.
[33]Fiehn O.Metabolomics-the link between genotypes and phenotypes.Plant Mol Biol 2002;48(2):155-171.
[34]Kayesh E,Shangguan L,Korir NK,Sun X,Bilkish N,Zhang Y,et al.Fruit skin color and the role of anthocyanin.Acta Physiol Plant 2013;35(10):2879-2890.
[35]Tanaka Y,Sasaki N,Ohmiya A.Biosynthesis of plant pigments:Anthocyanins,betalains and carotenoids.Plant J 2008;54(4):733-749.
[36]Mc Cann D,Barrett A,Cooper A,Crumpler D,Dalen L,Grimshaw K,et al.Food additives and hyperactive behaviour in 3-year-old and 8/9-yearold children in the community:A randomised,double-blinded,placebocontrolled trial.Lancet 2007;370(9598):1560-1567.
[37]Piccolella S,Crescente G,Pacifico F,Pacifico S.Wild aromatic plants bioactivity:A function of their(poly)phenol seasonality?A case study from Mediterranean area.Phytochem Rev 2018;17(4):785-799.
[38]Dewick PM.The shikimate pathway:Aromatic amino acids and phenylpropanoids.Medicinal natural products:A biosynthetic approach.3rd ed.Nottingham,U.K;John Wiley&Sons;2009,p.137-186.
[39]Vogt T.Phenylpropanoid biosynthesis.Mol Plant 2010;3(1):2-20.