Bioactive compounds of pequi pulp and oil extracts modulate antioxidant activity and antiproliferative activity in cocultured blood mononuclear cells and breast cancer cells

  • Renata Brito Programa de Pós-Graduação em Ciência e Tecnologia de Alimentos, Universidade Federal de Santa Maria, Santa Maria, Brazil
  • Milene Teixeira Barcia Programa de Pós-Graduação em Ciência e Tecnologia de Alimentos, Universidade Federal de Santa Maria, Santa Maria, Brazil
  • Carla Andressa Almeida Farias Programa de Pós-Graduação em Ciência e Tecnologia de Alimentos, Universidade Federal de Santa Maria, Santa Maria, Brazil
  • Rui Carlos Zambiazi Centro de Ciências Químicas, Farmacêuticas e de Alimentos, Universidade Federal de Pelotas, Pelotas, Brazil
  • Patrícia Gelli Feres de Marchi Programa de Pós-Graduação em Imunologia e Parasitologia Básicas e Aplicadas, Universidade Federal de Mato Grosso, Campus Universitário do Araguaia, Barra do Garças, Brazil
  • Mahmi Fujimori Programa de Pós-Graduação em Imunologia e Parasitologia Básicas e Aplicadas, Universidade Federal de Mato Grosso, Campus Universitário do Araguaia, Barra do Garças, Brazil
  • Adenilda Cristina Honorio-França Programa de Pós-Graduação em Imunologia e Parasitologia Básicas e Aplicadas, Universidade Federal de Mato Grosso, Campus Universitário do Araguaia, Barra do Garças, Brazil
  • Eduardo Luzia França Programa de Pós-Graduação em Imunologia e Parasitologia Básicas e Aplicadas, Universidade Federal de Mato Grosso, Campus Universitário do Araguaia, Barra do Garças, Brazil
  • Paula Becker Pertuzatti Programa de Pós-Graduação em Imunologia e Parasitologia Básicas e Aplicadas, Universidade Federal de Mato Grosso, Campus Universitário do Araguaia, Barra do Garças, Brazil
DOI: https://doi.org/10.29219/fnr.v66.8282
Keywords: immunomodulatory potential, MCF-7 cells, phenolic compounds, phytosterols, tocopherols

Abstract

Background: Pequi (Caryocar brasiliense Camb.) is a fruit from Brazilian Cerrado rich in bioactive compounds, such as phytosterols and tocopherols, which can modulate the death of cancer cells.

Objective: In the present study, the main bioactive compounds of hydrophilic and lipophilic extracts of pequi oil and pulp were identified and were verified if they exert modulatory effects on oxidative stress of mononuclear cells cocultured with MCF-7 breast cancer cells.

Study design: Identification and quantification of the main compounds and classes of bioactive compounds in pequi pulp and oil, hydrophilic, and lipophilic extracts were performed using spectroscopy and liquid chromatographic methods, while the beneficial effects, such as antioxidant capacity in vitro, were determined using methods based on single electron transfer reaction or hydrogen atom transfer, while for antioxidant and antiproliferative activities ex vivo, 20 healthy volunteers were recruited. Human peripheral blood mononuclear cells (MN) were collected, and cellular viability assay by MTT (3-(4,5-dimethylthiazol-2-yl)-2,5 diphenyltetrazolium bromide), superoxide anion evaluation, and CuZn-superoxide dismutase determination (CuZn-SOD) in MN cells, MCF-7 cells, and coculture of MN cells and MCF-7 cells in the presence and absence of pequi pulp or oil hydrophilic and lipophilic extracts were performed.

Results: In the hydrophilic extract, the pequi pulp presented the highest phenolic content, while in the oil lipophilic extract, it had the highest content of carotenoids. The main phytosterol in pequi oil was β-sitosterol (10.22 mg/g), and the main tocopherol was γ-tocopherol (26.24 μg/g sample). The extracts that had highest content of bioactive compounds stimulated blood mononuclear cells and also improved SOD activity. By evaluating the extracts against MCF-7 cells and coculture, they showed cytotoxic activity.

Conclusion: The results support the anticarcinogenic activity of pequi extracts, in which the pequi pulp hydrophilic extracts presented better immunomodulatory potential.

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References


  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394–424. doi: 10.3322/caac.21492

  2. Cimino-Mathews A, Foote J, Emens L. Immune targeting in breast cancer. Oncology 2015; 29(5): 375–85.

  3. de Araújo RL, Savazzi S, Fujimori M, Deluque AL, Honório-França EL, Konda PBP, et al. Effects of mangaba (Hancornia speciosa) fruit extract adsorbed onto PEG microspheres in MCF-7 breast cancer cells co-cultured with blood cells. Asian Pac J Cancer Prev 2019; 20(7): 1995–2001. doi: 10.31557/APJCP.2019.20.7.1995

  4. Savazzi S, Araújo R, Fujimori M, de Marchi PGF, Fagundes DLG, Honório-França AC, et al. Effects of anacardium humile fruit adsorbed on polyethylene glycol microspheres on oxidative stress in mononuclear blood cells co-cultured with MCF-7 breast cancer cells. Wulfenia 2019; 26(9): 35–48.

  5. Ombredane AS, Araujo VHS, Borges CO, Costa PL, Landim MG, Pinheiro AC, et al. Nanoemulsion-based system as a promising approach for enhancing the antitumoral activity of pequi oil (Caryocar brasiliense Cambess.) in breast cancer cells. J Drug Deliv Sci Technol 2020; 58: 101819. doi: 10.1016/j.jddst.2020.101819

  6. Machado MTC, Mello BCBS, Hubinger MD. Study of alcoholic and aqueous extraction of pequi (Caryocar brasiliense Camb.) natural antioxidants and extracts concentration by nanofiltration. J Food Eng 2013; 117(4): 450–7. doi: 10.1016/j.jfoodeng.2012.12.007

  7. Traesel GK, Araújo FHS, Castro LHA, Lima FF, Menegati SELT, Justi PN, et al. Safety assessment of oil from pequi (Caryocar brasiliense Camb.): evaluation of the potential genotoxic and clastogenic effects. J Med Food 2017; 20(8): 804–11. doi: 10.1089/jmf.2017.0021

  8. Torres LRO, Shinagawa FB, Araújo ES, Oropeza MVC, Macedo LFL, Almeida-Muradian LB, et al. Physicochemical and antioxidant properties of the pequi (Caryocar brasiliense Camb.) almond oil obtained by handmade and cold-pressed processes. Int Food Res J 2016; 23(4): 1541–51.

  9. Torres LRO, Santana FC, Torres-Leal FL, Melo ILP, Yoshime LT, Matos-Neto EM, et al. Pequi (Caryocar brasiliense Camb.) almond oil attenuates carbono tetrachloride-induced acute hepatic injury in rats: antioxidant and anti-inflammatory effects. Food Chem Toxicol 2016; 97: 205–16. doi: 10.1016/j.fct.2016.09.009

  10. Faria-Machado AF, Tres A, van Ruth SM, Antoniassi R, Junqueira NTV, Lopes PSN, et al. Discrimination of pulp oil and kernel oil from pequi (Caryocar brasiliense) by fatty acid methyl esters fingerprinting, using GC-FID and multivariate analysis. J Agric Food Chem 2015; 63(45): 10064–9. doi: 10.1021/acs.jafc.5b03699

  11. Playdon MC, Ziegler RG, Sampson JN, Stolzenberg-Solomon R, Thompson HJ, Irwin ML, et al. Nutritional metabolomics and breast cancer risk in a prospective study. Am J Clin Nutr 2017; 106: 637–49. doi: 10.3945/ajcn.116.150912

  12. Shahzad N, Khan W, Md S, Ali A, Saluja SS, Sharma S, et al. Phytosterols as a natural anticancer agent: current status and future perspective. Biomed Pharmacother 2017; 88: 786–94. doi: 10.1016/j.biopha.2017.01.068

  13. Blanco-Vaca F, Cedó L, Julve J. Phytosterols in cancer: from molecular mechanisms to preventive and therapeutic potentials. Curr Med Chem 2019; 26(37): 6735–49. doi: 10.2174/092986732566618060709311

  14. Hutchinson SA, Lianto P, Moore JB, Hughes TA, Thorne JL. Phytosterols inhibit side-chain oxysterol mediated activation of LXR in breast cancer cells. Int J Mol Sci 2019; 20: 3241. doi: 10.3390/ijms20133241

  15. Rodriguez-Amaya DB. A guide to carotenoids analyses in foods. In: Rodriguez-Amaya, DB, eds. General procedure and sources of errors in carotenoid analysis. Washington, DC: E-Publishing Inc.; 2001, pp. 23–33.

  16. Nakbi A, Issaoui M, Dabbou S, Koubaa N, Echbili A, Hammami M, et al. Evaluation of antioxidant activities of phenolic compounds from two extra virgin olive oils. J Food Compos Anal 2010; 23(7): 711–15. doi: 10.1016/j.jfca.2010.05.003

  17. Singleton VL, Orthofer R, Lamuela-Raventós RM. Analysis of total phenols and others oxidation substrates and antioxidants by means of Folin-Ciocaulteau reagent. Method Enzymol 1999; 299: 152–78. doi: 10.1016/S0076-6879(99)99017-1

  18. Arvouet-Grand A, Vennat B, Pourrat A, Legret P. Standardization d’une extrait de propolis et identification des principaux constituents. J Pharm Belg 1994; 49(6): 462–8.

  19. Quatrin A, Pauletto R, Maurer LH, Minuzzi N, Nichelle SM, Carvalho JFC, et al. Characterization and quantification of tannins, flavanols, anthocyanins and matrix-bound polyphenols from jaboticaba fruit peel: a comparison between Myrciaria trunciflora and M. jaboticaba. J Food Compos Anal 2019; 78: 59–74. doi: 10.1016/j.jfca.2019.01.018

  20. Pertuzatti PB, Barcia MT, Jacques AC, Vizzotto M, Godoy HT, Zambiazi R. Quantification of several bioactive compounds and antioxidant activities of six cultivars of Brazilian blueberry. The Nat Prod 2012; 2(3): 188–95. doi: 10.2174/2210315511202030188

  21. Brand-Williams W, Cuvelier ME, Berset C. Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 1995; 28: 25–30. doi: 10.1016/S0023-6438(95)80008-5

  22. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Bio Med 1999; 26: 1231–7. doi: 10.1016/s0891-5849(98)00315-3

  23. Benzie IF, Strain JJ. The Ferric Reducing Ability of Plasma (FRAP) as a measure of ‘antioxidant power’: the FRAP assay. Anal Biochem 1996; 239(1): 70–6. doi: 10.1006/abio.1996.0292

  24. Ou B, Hampsch-Woodill M, Prior RL. Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe. J Agr Food Chem 2001; 49(10): 4619–26. doi: 10.1021/jf010586o

  25. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J lmmunol Methods 1983; 65(1–2): 55–63. doi: 10.1016/0022-1759(83)90303-4

  26. Cilla A, Rodrigo MJ, Zacarías L, Ancos B, Sánchez-Moreno C, Barberá R, et al. Protective effect of bioaccessible fractions of citrus fruit pulps against H2O2-induced oxidative stress in Caco-2 cells. Food Res Int 2018; 103: 335–44. doi: 10.1016/j.foodres.2017.10.066

  27. Pick E, Mizel D. Rapid microassay for the measurement of superoxide and hydrogen peroxide production by macrophages in culture using na automatic enzyme immunoassay reader. J Immunol Methods 1981; 46(2): 211–26. doi: 10.1016/0022-1759(81)90138-1

  28. Van Hoed V. Phenolic compounds in seed oils. Lipid Technol 2010; 22(11): 247–9. doi: 10.1002/lite.201000063

  29. Magalhães FS, Cardoso VL, Reis MHM. Sequential process with bioadsorbents and microfiltration for clarification of pequi (Caryocar brasiliense Camb.) fruit extract. Food Bioprod Process 2018; 108: 105–16. doi: 10.1016/j.fbp.2018.02.003

  30. Duan J, Guo H, Fang Y, Zhou G. The mechanisms of wine phenolic compounds for preclinical anticancer therapeutics. Food Nutr Res 2021; 65: 6507 doi: 10.29219/fnr.v65.6507

  31. Biazotto KR, Mesquita LMS, Neves BV, Braga ARC, Tangerina M, Vilegas W, et al. Brazilian biodiversity fruits: discovering bioactive compounds from underexplored sources. J Agric Food Chem 2019; 67(7): 1860–76. doi: 10.1021/acs.jafc.8b05815

  32. Rodriguez-Amaya DB. Update on natural food pigments – a mini-review on carotenoids, anthocyanins, and betalains. Food Res Int 2019; 124: 200–5. doi: 10.1016/j.foodres.2018.05.028

  33. Pinto MRMR, Paula DA, Alves AI, Rodrigues MZ, Vieira ENR, Fontes EAF, et al. Encapsulation of carotenoid extracts from pequi (Caryocar brasiliense Camb.) by emulsification (O/W) and foam-mat drying. Powder Technol 2018; 339: 939–46. doi: 10.1016/j.powtec.2018.08.076

  34. Niranjana R, Gayathri R, Mol SN, Sugawara T, Hirata T, Miyashita K, et al. Carotenoids modulate the hallmarks of cancer cells. J Funct Foods 2015; 18: 968–85. doi: 10.1016/j.jff.2014.10.017

  35. Tan CX. Virgin avocado oil: an emerging source of functional fruit oil. J Funct Food 2019; 54: 381–92. doi: 10.1016/j.jff.2018.12.031

  36. Liu Y, Wang Y, Xia Z, Wang Y, Wu Y, Gong Z. Rapid determination of phytosterols by NIRS and chemometric methods. Spectrochim Acta A 2019; 211: 336–41. doi: 10.1016/j.saa.2018.12.030

  37. Granato D, Shahidi F, Wrolstad R, Kilmartin P, Melton LD, Hidalgo FJ, et al. Antioxidant activity, total phenolics and flavonoids contents: should we ban in vitro screening methods? Food Chem 2018; 264: 471–5. doi: 10.1016/j.foodchem.2018.04.012

  38. Cruz MB, Oliveira WS, Araújo RL, Honório França AC, Pertuzatti PB. Buriti (Mauritia Flexuosa L.) pulp oil as na immunomodulator against enteropathogenic Escherichia coli. Ind Crops Prod 2020; 149: 112330. doi: 10.1016/j.indcrop.2020.112330

  39. Ferreira LM, Gehrcke M, Cervi VF, Bitencourt PER, da Silveira EF, Azambuja JH, et al. Pomegranate seed oil nanoemulsions with selective antiglioma activity: optimization and evaluation of citotoxicity, genotoxicity and oxidative effects on mononuclear cells. Pharm Biol 2016; 54(12): 2968–77. doi: 10.1080/13880209.2016.1199039

  40. Gloria NF, Soares N, Brand C, Oliveira FL, Borojevic R, Teodoro AJ. Lycopene and beta-carotene induce cell-cycle arrest and apoptosis in human breast cancer cell lines. Anticancer Res 2014; 34(3): 1377–86.

  41. Barizão EC, Visentainer JV, Almeida VC, Ribeiro D, Chisté RC, Fernandes E. Citharexylum solanaceum fruit extracts: profiles of phenolic compounds and carotenoids and their relation with ROS and RNS scavenging capacities. Food Res Int 2016; 86: 24–33. doi: 10.1016/j.foodres.2016.05.007

  42. Taysan Z, Kayali HA. Flavonoids showed anticancer effects on the ovarian cancer cells: involvement of reactive oxygen species, apoptosis, cell cycle and invasion. Biomed Pharmacother 2019; 116: 109004. doi: 10.1016/j.biopha.2019.109004

  43. Li R, Zhou X, Liu D, Feng W. Enhancing the activity and stability of Mn-superoxide dismutase by one-byone ligation to catalase. Free Radical Bio Med 2018; 129: 138–45. doi: 10.1016/j.freeradbiomed.2018.09.018

  44. Baptista A, Gonçalves RV, Bressan J, Pelúzio MCG. Antioxidant and antimicrobial activities of crude extracts and fractions of cashew (Anacardium occidentale L.), cajui (Anacardium microcarpum), and pequi (Caryocar brasiliense C.): a systematic review. Oxid Med Cell Longev 2018; 3753562. doi: 10.1155/2018/3753562

  45. Yin Y, Liu X, Liu J, Cai E, Zhu H, Li H, et al. Beta-sitosterol and its derivatives repress lipopolysaccharide/d galactosamine-induced acute hepatic injury by inhibiting the oxidation and inflammation in mice. Bioorg Med Chem Lett 2018; 28(9): 1525–33. doi: 10.1016/j.bmcl.2018.03.073

Published
2022-01-27
How to Cite
Brito R., Barcia M. T., Farias C. A. A., Zambiazi R. C., Feres de Marchi P. G., Fujimori M., Honorio-França A. C., França E. L., & Becker Pertuzatti P. (2022). Bioactive compounds of pequi pulp and oil extracts modulate antioxidant activity and antiproliferative activity in cocultured blood mononuclear cells and breast cancer cells. Food & Nutrition Research, 66. https://doi.org/10.29219/fnr.v66.8282
Issue
Vol 66 (2022)
Section
Original Articles
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