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Pistachio (Pistacia vera L.) hull samples from Turkey: phenolic compounds, antioxidant properties, and cytotoxic activities against HeLa, MCF-7, OE-33, and ACC-201 cancer cell lines

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Abstract

The phenolic profiles, antioxidant properties, and cytotoxic activities of Pistacia vera L. hull sample extracts were investigated to contribute to the important research being conducted on the potential bioeconomic applications of plants worldwide. The top six compounds revealed by RP-HPLC-DAD in the flavonoid subgroup and phenolic acid extracts of the hull samples were gallic acid (6726 ± 58 µg/gDW), quercetin (2991 ± 96 µg/gDW), catechin (1170 ± 62 µg/gDW), myricetin (940 ± 35 µg/gDW), rutin (563 ± 28 µg/gDW), and protocatechuic acid (539 ± 9.3 µg/gDW). The flavonoids hesperidin, rutin, isorhamnetin, apigenin, and eupatorin and the phenolic acids benzoic acid, o-coumaric acid, ferulic acid, and t-cinnamic acid were determined in P. vera hull samples for the first time in this study. Of the investigated antioxidant properties of the extracts, the DPPH· and HO· scavenging capacities were significant, with the best IC50 values of 2.08 ± 0.11 and 6.11 ± 0.36 ppm, respectively. Cytotoxic effects of the P. vera hull extracts were most commonly exhibited against the MCF-7 cell line, followed by OE-33, HeLa, and ACC-201. The top IC50 values were 25 ± 1.3 ppm for HeLa and MCF-7, 28 ± 2.0 ppm for ACC-201, and 40 ± 3.2 ppm for OE-33. These results suggest that P.vera hulls show promise for applications in food additives and medicine.

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References

  1. M.J. Balunas, A.D. Kinghorn, Life Sci. (2005). https://doi.org/10.1016/j.lfs.2005.09.012

    Article  PubMed  Google Scholar 

  2. F. Shahidi, P. Ambigaipalan, J. Funct. Foods (2015). https://doi.org/10.1016/j.jff.2015.06.018

    Article  Google Scholar 

  3. A.J. Parr, G.P. Bolwell, J. Sci. Food Agric. (2000). https://doi.org/10.1002/(SICI)10970010(20000515)80:-7%3c985::AID-JSFA572%3e3.0.CO;2-7

    Article  Google Scholar 

  4. B. Halliwell, J.M. Gutteridge, C.E. Cross, J. Lab. Clin. Med. (1992). https://doi.org/10.5555/uri:pii:002221439290284r

    Article  PubMed  Google Scholar 

  5. B. Halliwell, J.M. Gutteridge, Free radical biology and medicine (Oxford University Press, Oxford, 2015)

    Book  Google Scholar 

  6. A. Gurib-Fakim, Mol. Aspects Med. (2006). https://doi.org/10.1016/j.mam.2005.07.008

    Article  PubMed  Google Scholar 

  7. M.H. Alma, S. Nitz, H. Kollmannsberger, M. Digrak, F.T. Efe, N. Yilmaz, J. Agric. Food Chem. (2004). https://doi.org/10.1021/jf040014e

    Article  PubMed  Google Scholar 

  8. E. Ros, L.C. Tapsell, J. Sabaté, Curr. Atheroscler. Rep. (2010). https://doi.org/10.1007/s11883-010-0132-5

    Article  PubMed  Google Scholar 

  9. M.L. Dreher, Nutr. Rev. (2012). https://doi.org/10.1111/j.1753-4887.2011.00467.x

    Article  PubMed  Google Scholar 

  10. B.L. Halvorsen, M.H. Carlsen, K.M. Phillips, S.K. Bohn, K. Holte, D.R. Jacobs, R. Blomhoff, Am. J. Clin. Nutr. (2006). https://doi.org/10.1093/ajcn/84.1.95

    Article  PubMed  Google Scholar 

  11. M. Martorana, T. Arcoraci, L. Rizza, M. Cristani, F.P. Bonina, A. Saija, A. Tomaino, Fitoterapia (2013). https://doi.org/10.1016/j.fitote.2012.12.032

    Article  PubMed  Google Scholar 

  12. A. Tsokou, K. Georgopoulou, E. Melliou, P. Magiatis, E. Tsitsa, Molecules (2007). https://doi.org/10.3390/12061233

    Article  PubMed  PubMed Central  Google Scholar 

  13. B.R. Ghalem, B. Mohamed, Afr. J. Pharm. Pharmacol. (2009). https://doi.org/10.5897/AJPP.9000050

    Article  Google Scholar 

  14. H. Hosseinzadeh, S.A.S. Tabassi, N.M. Moghadam, M. Rashedinia, S. Mehri, Iran J. Pharm. Res. (2012). https://doi.org/10.22037/IJPR.2012.1125

    Article  PubMed  PubMed Central  Google Scholar 

  15. M.H. Sehitoglu, H. Han, P. Kalin, İ Gülçin, A. Ozkan, H.Y. Aboul-Enein, J. Enzym. Inhib. Med. Chem. (2015). https://doi.org/10.3109/14756366.2014.915395

    Article  Google Scholar 

  16. C. Gentile, L. Tesoriere, D. Butera, M. Fazzari, M. Monastero, M. Allegra, M.A. Livrea, J. Agric. Food Chem. (2007). https://doi.org/10.1021/jf062533i

    Article  PubMed  Google Scholar 

  17. A. Tomaino, M. Martorana, T. Arcoraci, D. Monteleone, C. Giovinazzo, A. Saija, Biochimie (2010). https://doi.org/10.1016/j.biochi.2010.03.027

    Article  PubMed  Google Scholar 

  18. M. Seifeddinipour, R. Farghadani, F. Namvar, J. Mohamad, H. Abdul Kadir, Molecules (2018). https://doi.org/10.3390/molecules23010110

    Article  Google Scholar 

  19. C. Beres, G.N.S. Costa, I. Cabezudo, N.K. da Silva-James, A.S.C. Teles, A.P.G. Cruz et al., Waste Manage. (2017). https://doi.org/10.1016/j.wasman.2017.07.017

    Article  Google Scholar 

  20. E. Arjeh, H.R. Akhavan, M. Barzegar, Á.A. Carbonell-Barrachina, Trends Food Sci. Technol. (2020). https://doi.org/10.1016/j.tifs.2019.12.031

    Article  Google Scholar 

  21. A. Mokhtarpour, A.A. Naserian, R. Valizadeh, M.D. Mesgaran, F. Pourmollae, Annu. Res. Rev. Biol. (2014). https://doi.org/10.9734/ARRB/2014/7793

    Article  Google Scholar 

  22. H.N. Özbek, F. Halahlih Göğüş, D.K. Yanık, H. Azaizeh, Waste Biomass Valoriz. (2020). https://doi.org/10.1007/s12649-018-0512-6

    Article  Google Scholar 

  23. F. Pellati, S. Benvenuti, M. Melegari, Phytochem. Anal. (2004). https://doi.org/10.1002/pca.771

    Article  PubMed  Google Scholar 

  24. M. Olszewska, J. Pharm. Biomed. Anal. (2008). https://doi.org/10.1016/j.jpba.2008.06.004

    Article  PubMed  Google Scholar 

  25. E.A. Turumtay, F. İslamoğlu, D. Çavuş, H. Şahin, H. Turumtay, B. Vanholme, Ind. Crops Prod. (2014). https://doi.org/10.1016/j.indcrop.2013.11.042

    Article  Google Scholar 

  26. P. Valentão, P.B. Andrade, F. Areias, F. Ferreres, R.M. Seabra, J. Agric. Food Chem. (1999). https://doi.org/10.1021/jf990444i

    Article  PubMed  Google Scholar 

  27. K.H. Kim, R. Tsao, R. Yang, S.W. Cui, Food Chem. (2006). https://doi.org/10.1016/j.foodchem.2005.01.032

    Article  Google Scholar 

  28. A. De Villiers, F. Lynen, A. Crouch, P. Sandra, Chromatographia (2004). https://doi.org/10.1365/s10337-004-0204-1

    Article  Google Scholar 

  29. A. Braca, N. De Tommasi, L. Di Bari, C. Pizza, M. Politi, I. Morelli, J. Nat. Prod. (2001). https://doi.org/10.1021/np0100845

    Article  PubMed  Google Scholar 

  30. B. Halliwell, J.M. Gutteridge, O. Aruoma, Anal. Biochem. (1987). https://doi.org/10.1016/0003-2697(87)90222-3

    Article  PubMed  Google Scholar 

  31. P. Carter, Anal. Biochem. (1971). https://doi.org/10.1016/0003-2697(71)90405-2

    Article  PubMed  Google Scholar 

  32. M. Oyaizu, Jpn. J. Nutr. (1986). https://doi.org/10.5264/eiyogakuzashi.44.307

    Article  Google Scholar 

  33. T. Mosmann, J. Immunol. Methods (1983). https://doi.org/10.1016/0022-1759(83)90303-4

    Article  PubMed  Google Scholar 

  34. M.P. Fabani, L. Luna, M.V. Baroni, M.V. Monferran, M. Ighani, A. Tapia, G.E. Feresin, J. Func. Foods. (2013). https://doi.org/10.1016/j.jff.2013.05.002

    Article  Google Scholar 

  35. D. Barreca, G. Laganà, U. Leuzzi, A. Smeriglio, D. Trombetta, E. Bellocco, Food Chem. (2016). https://doi.org/10.1016/j.foodchem.2015.09.077

    Article  PubMed  Google Scholar 

  36. P. Reboredo-Rodríguez, C. González-Barreiro, B. Cancho-Grande, J. Simal-Gándara, F. Giampieri, T.Y. Forbes-Hernández, M. Battino, J. Funct. Foods (2018). https://doi.org/10.1016/j.jff.2018.03.045

    Article  Google Scholar 

  37. S. Lalegani, H.A. Gavlighi, M.H. Azizi, R.A. Sarteshnizi, Food Res. Int. (2018). https://doi.org/10.1016/j.foodres.2017.11.003

    Article  PubMed  Google Scholar 

  38. S. Erşan, Ö.G. Üstündağ, R. Carle, R.M. Schweiggert, J. Food Comp. Anal. (2017). https://doi.org/10.1016/j.jfca.2017.04.013

    Article  Google Scholar 

  39. A. Rajaei, M. Barzegar, A.M. Mobarez, M.A. Sahari, Z.H. Esfahani, Food Chem. Toxicol. (2010). https://doi.org/10.1016/j.fct.2009.09.023

    Article  PubMed  Google Scholar 

  40. H.N. Özbek, D.K. Yanık, S. Fadıloğlu, H.K. Çavdar, F. Göğüş, Grasas Aceites (2018). https://doi.org/10.3989/gya.0217181

    Article  Google Scholar 

  41. J.S. Giftson, S. Jayanthi, N. Nalini, Invest New Drugs (2010). https://doi.org/10.1007/s10637-009-9241-9

    Article  PubMed  Google Scholar 

  42. J.E.N. Dolatabadi, S. Kashanian, Food Res. Int. (2010). https://doi.org/10.1016/j.foodres.2010.03.026

    Article  Google Scholar 

  43. F. Dahooee, A.S. Fatemi, A. Mandegary, F. Sharififar, Int. J. Clin. Pharmacol. Ther. (2016). https://doi.org/10.19070/2167-910X-1600033

    Article  Google Scholar 

  44. M. Leopoldini, N. Russo, S. Chiodo, M. Toscano, J. Agric. Food Chem. (2006). https://doi.org/10.1021/jf060986h

    Article  PubMed  Google Scholar 

  45. Ş Sungur, A. Uzar, Spectrochim. Acta A Mol. Biomol. Spectrosc. (2008). https://doi.org/10.1016/j.saa.2007.03.038

    Article  PubMed  Google Scholar 

  46. Z. Hawula, E. Secondes, D. Wallace, G. Rishi, V.N. Subramaniam, Biosci. Rep. (2021). https://doi.org/10.1042/BSR20210720

  47. B. Badhani, N. Sharma, R. Kakkar, RSC Adv. (2015). https://doi.org/10.1039/C5RA01911G

    Article  Google Scholar 

  48. M. Behgar, S. Ghasemi, A. Naserian, A. Borzoie, H. Fatollahi, Radiat. Phys. Chem. (2011). https://doi.org/10.1016/j.radphyschem.2011.04.016

    Article  Google Scholar 

  49. E.K. Akkol, F.N. Yalcin, D. Kaya, I. Calis, E. Yesilada, T. Ersoz, J. Ethnopharmacol. (2008). https://doi.org/10.1016/j.jep.2008.04.001

    Article  PubMed  Google Scholar 

  50. M. Abotaleb, A. Liskova, P. Kubatka, D. Büsselberg, Biomolecules (2020). https://doi.org/10.3390/biom10020221

    Article  PubMed  PubMed Central  Google Scholar 

  51. L. Ouyang, Z. Shi, S. Zhao, F.T. Wang, T.T. Zhou, B. Liu, J.K. Bao, Cell Prolif. (2012). https://doi.org/10.1111/j.1365-2184.2012.00845.x

    Article  PubMed  PubMed Central  Google Scholar 

  52. E. Oskoueian, N. Abdullah, W.Z. Saad, A.R. Omar, S. Ahmad, W.B. Kuan, Y.W. Ho, J. Med. Plant Res. (2011). https://doi.org/10.5897/JMPR.9000229

    Article  Google Scholar 

  53. E. Safarzadeh, S.S. Shotorbani, B. Baradaran, Adv. Pharm. Bull. (2014). https://doi.org/10.5681/apb.2014.062

    Article  PubMed  PubMed Central  Google Scholar 

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Karaoglu, E.C., Tarhan, L. Pistachio (Pistacia vera L.) hull samples from Turkey: phenolic compounds, antioxidant properties, and cytotoxic activities against HeLa, MCF-7, OE-33, and ACC-201 cancer cell lines. Food Measure 16, 2300–2313 (2022). https://doi.org/10.1007/s11694-022-01316-2

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