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Antioxidant activity, phytochemical composition of Andricus tomentosus and its antiproliferative effect on Mia-Paca2 cell line

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Abstract

Plant derived products are widely used in cancer treatment. Gall species has been preferred for treatment various diseases in folk medicine, but there are few studies on the anticancer effects of gall species. The present study reports the antioxidant activity and total secondary metabolites of extracts of A. tomentosus galls. The antioxidant potency of galls was carried out using different in-vitro model systems. Their cytotoxic efficacy on Mia-Paca cell line was also explored. Gall extract was found to contain a large amount of phenolic acids. The extract potently scavenged free radicals including DPPH (IC50 9.56 ± 1.08 µg/mL), ABTS (IC50 18.51 ± 0.25 µg/mL). It can be seen as a potential source of antioxidants according to β-carotene/linoleic acid method (%92.58 ± 0.92) and Phosphomolybdenum assays (104.36 ± 4.95 mgAE/g). Gall extract also posses ability of metal chelating (%40.07 ± 2.30) and Fe3+ (184.01 ± 2.83 mgTE/g) and Cu2+ (89.81 ± 0.96 mgTE/g) reducing activity. According to total secondary metabolites tests, gall extract showed high total phenolic, total flavonoid and total tannin amount. HPLC analysis of the extract suggested it to contain caffeic acid (424.068.479 µg/g), ellagic acid (187.696.132 µg/g). XTT assay revealed gall extract to enhance percent survival of Mia-Paca2 cell line exposed A. tomentosus extracts. The best cytotoxic effect was determined in acetone extracts (IC50: 124.7 µM). Expression of some genes (Bax, Bcl-2, FAS, BID, caspase-3, caspase-8, caspase-9, caspase-10, FADD, TRADD) in the apoptosis pathway was determined to invastigate apoptosis inducing activity. These results indicate that A. tomentosus galls possess potent antioxidant activity, when tested both in chemical as well as biological models.

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References

  1. Ugur D, Gunes H, Gunes F, Mammadov R (2017) Cytotoxic activities of certain medicinal plants on different cancer. Iran J Pharm Res 13:299

    Google Scholar 

  2. Tokgun O, Akca H, Mammadov R, Aykurt C, Deniz G (2012) Convolvulus galaticus, Crocus antalyensis, and Lilium candidum extracts show their antitumor activity through induction of p53-mediated apoptosis on human breast cancer cell line MCF-7 cells. J Med Food 15(11):1000–1005. https://doi.org/10.1089/jmf.2012.0050

    Article  PubMed  Google Scholar 

  3. Rezzoug M, Bakchiche B, Gherib A, Roberta A, Kilinçarslan Ö, Mammadov R, Bardaweel SK (2019) Chemical composition and bioactivity of essential oils and ethanolic extracts of Ocimum basilicum L. and Thymus algeriensis Boiss. & Reut. from the Algerian Saharan Atlas. BMC Complement Altern Med 19(1):146. https://doi.org/10.1186/s12906-019-2556-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Elmas L, Secme M, Mammadov R, Fahrioglu U, Dodurga Y (2019) The determination of the potential anticancer effects of Coriandrum sativum in PC-3 and LNCaP prostate cancer cell lines. J Cell Biochem 120(3):3506–3513. https://doi.org/10.1002/jcb.27625

    Article  CAS  PubMed  Google Scholar 

  5. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136(5):E359–E386. https://doi.org/10.1002/ijc.29210

    Article  CAS  PubMed  Google Scholar 

  6. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492

    Article  PubMed  Google Scholar 

  7. Han Y, Ma L, Zhao L, Feng W, Zheng X (2019) Rosmarinic inhibits cell proliferation, invasion and migration via up-regulating miR-506 and suppressing MMP2/16 expression in pancreatic cancer. Biomed Pharmacother 115:108878. https://doi.org/10.1016/j.biopha.2019.108878

    Article  CAS  PubMed  Google Scholar 

  8. Bhuyan DJ, Vuong QV, Chalmers AC, Bowyer MC, Scarlett CJ (2018) An array of bioactive compounds from Australian eucalypts and their relevance in pancreatic cancer therapeutics. Pancreas 47(6):690–707. https://doi.org/10.1097/MPA.0000000000001074

    Article  CAS  PubMed  Google Scholar 

  9. Chung KT, Wong TY, Wei CI, Huang YW, Lin Y (1998) Tannins and human health: a review. Crit Rev Food Sci Nutr 38:421–464. https://doi.org/10.1080/10408699891274273

    Article  CAS  PubMed  Google Scholar 

  10. Cai Y, Zhang J, Chen NG, Shi Z, Qiu J, He C, Chen M (2017) Recent advances in anticancer activities and drug delivery systems of Tannins. Med Res Rev 37:665–701. https://doi.org/10.1002/med.21422

    Article  CAS  PubMed  Google Scholar 

  11. Chauhan SS, Shetty AB, Hatami E, Chowdhury P, Yallapu MM (2020) Pectin-tannic acid nano-complexes promote the delivery and bioactivity of drugs in pancreatic cancer cells. Pharmaceutics 12(3):285. https://doi.org/10.3390/pharmaceutics12030285

    Article  CAS  PubMed Central  Google Scholar 

  12. Türkan F, Taslimi P, Saltan FZ (2019) Tannic acid as a natural antioxidant compound: discovery of a potent metabolic enzyme inhibitor for a new therapeutic approach in diabetes and Alzheimer’s disease. J Biochem Mol Toxicol 33(8):e22340. https://doi.org/10.1002/jbt.22340

    Article  CAS  PubMed  Google Scholar 

  13. Claus EP (1962) Pharmacognosy. Acad Med 37(1):79

    Google Scholar 

  14. Sukor N, Jusoh R, Rahim SA, Kamarudin N (2018) Ultrasound assisted methods for enhanced extraction of phenolic acids from Quercus infectoria galls. Mater Today 5(10):21990–21999. https://doi.org/10.1016/j.matpr.2018.07.060

    Article  CAS  Google Scholar 

  15. Azmaz M, Kılınçarslan Aksoy Ö, Katılmış Y, Mammadov M (2020) Investigation of the antioxidant activity and phenolic compounds of Andricus quercustozae gall and host plant (Quercus infectoria). Int J Secondary Metab 7(2):77–87. https://doi.org/10.21448/ijsm.674930

    Article  Google Scholar 

  16. Akbar S (2020) Quercus infectoria G. Olivier (Fagaceae). In: Handbook of 200 medicinal plants. pp. 1505–1511. https://doi.org/10.1007/978-3-030-16807-0_155

  17. Tavakoli M, Melika G, Sadeghi SE, Pénzes Z, Assareh MA, Atkinson R et al (2008) New species of oak gallwasps from Iran (Hymenoptera: Cynipidae: Cynipini). Zootaxa 1699(1):1–64

    Article  Google Scholar 

  18. Azmaz M, Katılmış Y (2017) Cynipidae (Insecta: Hymenoptera) fauna of Istanbul. Mun Ent Zool 12(1):151

    Google Scholar 

  19. Ionescu MA (1957) Insecta: Cynipinae. Editura Academiei Republicii Populare România

  20. Melika G (2006) Gall wasps of Ukraine. Cynipidae Vestnik zoologii 21(1–2):301–644

    Google Scholar 

  21. Kılınçarslan O, Mammadov R (2018) HPLC analysis and antioxidant, antibacterial and cytotoxicity activities of various solvent extracts of Erysimum kotschyanum Gay.(Brassicaceae). J Chem Soc Pak 40(04):707

    Google Scholar 

  22. Amin I, Zamaliah MM, Chin WF (2004) Total antioxidant activity and phenolic content in selected vegetables. Food Chem 87:581–586. https://doi.org/10.1016/j.foodchem.2004.01.010

    Article  CAS  Google Scholar 

  23. Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: specific application to the determination of vitamin E. Anal Biochem 269(29):337–41

    Article  CAS  PubMed  Google Scholar 

  24. Wu C, Chen F, Wang X, Kim HJ, He GQ, Haley-Zitlin V, Huang G (2006) Antioxidant constituents in feverfew (Tanacetum parthenium) extract and their chromatographic quantification. Food Chem 96(2):220–227. https://doi.org/10.1016/j.foodchem.2005.02.024

    Article  CAS  Google Scholar 

  25. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol Med 26:1231–1237. https://doi.org/10.1016/S0891-5849(98)00315-3

    Article  CAS  Google Scholar 

  26. Apak R, Guclu K, Ozyurek M, Karademir SE, Ercag E (2006) The cupric ion reducing antioxidant capacity and polyphenolic content of some herbal teas. Int J Food Sci Nutr 57:292–304. https://doi.org/10.1080/09637480600798132

    Article  CAS  PubMed  Google Scholar 

  27. Apak R, Özyürek M, Güçlü K, Çapanoğlu E (2016) Antioxidant activity/capacity measurement. 1. Classification, physicochemical principles, mechanisms, and electron transfer (ET)-based assays. J Agric Food Chem 64(5):997–1027. https://doi.org/10.1021/acs.jafc.5b04739

    Article  CAS  PubMed  Google Scholar 

  28. Dinis TCP, Madeira VMC, Almeida LM (1994) Action of phenolic derivates (acetoaminophen, salicylate and 5-aminosalycilate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch Biochem Biophys 315:161–169. https://doi.org/10.1006/abbi.1994.1485

    Article  CAS  PubMed  Google Scholar 

  29. Slinkard K, Vernon L, Singleton VL (1977) Total phenol analyses: automation and comparison with manual methods. Am J Enol Viticult 28:49–55

    CAS  Google Scholar 

  30. Arvouet-Grand A, Vennat B, Pourrat A, Legret P (1994) Standardization of propolis extract and identification of principal constituents. J Pharm Belg 49:462–468

    CAS  PubMed  Google Scholar 

  31. Bekir J, Mars M, Souchard JP, Bouajila J (2013) Assessment of antioxidant, anti inflammatory, anti-cholinesterase and cytotoxic activities of pomegranate (Punica granatum) leaves. Food Chem Toxicol 55:470–475. https://doi.org/10.1016/j.fct.2013.01.036

    Article  CAS  PubMed  Google Scholar 

  32. Caponio F, Alloggio V, Gomesb T (1999) Phenolic compounds of virgin olive oil; influence of paste preparation techniques. Food Chem 64:203–209. https://doi.org/10.1016/S0308-8146(98)00146-0

    Article  CAS  Google Scholar 

  33. Fahrioğlu U, Dodurga Y, Elmas L, Seçme M (2016) Ferulic acid decreases cell viability and colony formation while inhibiting migration of MIA PaCa-2 human pancreatic cancer cells in vitro. Gene 576(1):476–482. https://doi.org/10.1016/j.gene.2015.10.061

    Article  CAS  PubMed  Google Scholar 

  34. Ahmad W (2016) Ethnopharmacology of Quercus infectoria olivier galls: a review. Hippocratic J Unani Med 11:105–18

    Google Scholar 

  35. Shrestha S, Kaushik VS, Eshwarappa RS, Subaramaihha SR, Ramanna LM, Lakkappa DB et al (2014) Pharmacognostic studies of insect gall of Quercus infectoria Olivier (Fagaceae). Asian Pac J Trop Biomed 4(1):35–39. https://doi.org/10.1016/S2221-1691(14)60205-7

    Article  PubMed  PubMed Central  Google Scholar 

  36. Zachariah SM, Kumar NM, Darsana K, Gopal D, Thomas N, Ramkumar M et al (2014) Phytochemical screening, formulation and evaluation of dried galls of Quercus infectoria Olivier. Int J Pharm Sci Rev Res 26:125–30

    Google Scholar 

  37. Fathabada AE, Schariatifar N, Mardania K, Pourfard MI (2015) Study on antibacterial and antioxidant activiy of Oak gall Quercus infectoria (extracts from Iran). Int J Curr Scı 14:44–50

    Google Scholar 

  38. Arina MI, Harisun Y (2019) Effect of extraction temperatures on tannin content and antioxidant activity of Quercus infectoria (Manjakani). Biocatal Agric Biotechnol 19:101104. https://doi.org/10.1016/j.bcab.2019.101104

    Article  Google Scholar 

  39. Kaur G, Athar M, Alam MS (2008) Quercus infectoria galls possess antioxidant activity and abrogates oxidative stress-induced functional alterations in murine macrophages. Chem Biol Interact 171:272–282. https://doi.org/10.1016/j.cbi.2007.10.002

    Article  CAS  PubMed  Google Scholar 

  40. Doğan Abdioğlu M (2019) Bazı meşe gallerinin kolinesteraz, tirozinaz ve üreaz enzim inhibisyonu ile antioksidan aktivitesinin belirlenmesi. Master’s thesis, Batman Üniversitesi Fen Bilimleri Enstitüsü, Türkiye

  41. Shahin S, Ahmad N (2014) Antioxidant properties and total phenolic content of herbs used in post partum diet therapy in Patna (Bihar), India. J Pharm Biol Sci 9:17–20

    Google Scholar 

  42. Sukor NF, Jusoh R, Kamarudin NS, Halim NA, Sulaiman AZ, Abdullah SB (2020) Synergistic effect of probe sonication and ionic liquid for extraction of phenolic acids from oak galls. Ultrason Sonochem 62:104876. https://doi.org/10.1016/j.ultsonch.2019.104876

    Article  CAS  PubMed  Google Scholar 

  43. Aydin Ç, Rakhimzhanova A, Kilinçarslan Ö, Mammadov R (2020) Antioxidant and phenolic characterization with HPLC of various extract of Verbascum glomeratum Linneus. J Chem Soc Pak 42(2):222

    CAS  Google Scholar 

  44. Hasmah A, Nurazila Z, Chow CY, Rina R, Rafiquzzaman M (2010) Cytotoxic effects of Quercus infectoria extracts towards cervical (Hela) and Ovarian (Caov-3) cancer cell lines. Health Environ J 1(2):17–23

    Google Scholar 

  45. Gao J, Yang X, Yin W, Li M (2018) Gallnuts: a potential treasure in anticancer drug discovery. Evid Based Complement Altern Med 2018:4930371

    Google Scholar 

  46. Jalill RDA (2018) Chemical analysis and anticancer effects of Juniperus polycarpos and oak gall plants extracts. Res J Pharm Technol 11(6):2372–2387

    Article  Google Scholar 

  47. Abdalan S, Baghbani-Arani F, Sadat Shandiz SA (2018) Evaluation of anticancer effect of aqueous and hydroalcoholic extracts of Quercusin fectoria leaf against colon cancer HT29 cell line. J Arak Univ Med Sci 21(4):48–57

    Google Scholar 

  48. Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radical Biol Med 49(11):1603–1616. https://doi.org/10.1016/j.freeradbiomed.2010.09.006

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful for the financial support from the Pamukkale University Scientific Research Projects Coordination Unit (Project No: 2018FEBE062).

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Authors and Affiliations

  1. Department of Biology, Science & Art Faculty, Pamukkale University, Denizli, Turkey

    Özge Kılınçarslan Aksoy

  2. Department of Molecular Biology an Genetic, Muğla Sıtkı Koçman University, Mugla, Turkey

    Ramazan Mammadov

  3. Department of Medical Biology, Medicine Faculty, TurkeyPamukkale University, Denizli, Turkey

    Mücahit Seçme

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Kılınçarslan Aksoy, Ö., Mammadov, R. & Seçme, M. Antioxidant activity, phytochemical composition of Andricus tomentosus and its antiproliferative effect on Mia-Paca2 cell line. Mol Biol Rep 47, 7633–7641 (2020). https://doi.org/10.1007/s11033-020-05833-5

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