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Protective effects of anthocyanin against apoptosis and oxidative stress induced by arsanilic acid in DF-1 cells

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Abstract

Anthocyanin is a natural plant pigment that acts as an antioxidant and scavenges free radicals. This study aimed to investigate the potential protective role of nightshade anthocyanin (NA), a natural flavonoid compound, against the arsanilic acid (ASA)-induced cell death of DF-1 cells. DF-1 cells were initially exposed to ASA, and then NA was applied to the treated cells. Cell viability, intracellular reactive oxygen species (ROS), mitochondrial membrane potential (MMP), and apoptosis were examined. Results showed that NA inhibited the ASA-induced decrease in cell viability, increase in ROS, and loss of MMP in DF-1 cells. Moreover, caspase-3 activation was inhibited by ASA supplementation and NA attenuated the ASA-induced increase in the percentage of apoptotic cells. In summary, our study suggested that NA can enhance ASA-induced cytotoxicity and apoptosis, thereby providing a basis for the molecular mechanisms of NA-mediated protection.

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References

  1. Adriano DC (2001) Arsenic. Springer, New York

    Google Scholar 

  2. Proudfoot FG, Jackson ED, Hulan HW, Salisbury CD (1991) Arsanilic acid as a growth promoter for chicken broilers when administered via either the feed or drinking water. Can Vet J 71(1):221–226

    CAS  Google Scholar 

  3. Desheng Q, Niya Z (2006) Effect of arsanilic acid on performance and residual of arsenic in tissue of Japanese laying quail. Poult Sci 85(12):2097–2100

    Article  CAS  Google Scholar 

  4. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257

    Article  CAS  Google Scholar 

  5. Yuan H, Gong Z, Yuan IY, Han B, Han HR (2006) In vitro arsanilic acid induction of apoptosis in rat hepatocytes. Asian Australas J Anim Sci 19(9):1328–1334

    Article  CAS  Google Scholar 

  6. Lu Y, Yuan H, Deng S, Wei Q, Guo C, Yi J, Wu J, Li R, Wen L, He Z (2014) Arsanilic acid causes apoptosis and oxidative stress in rat kidney epithelial cells (NRK-52e cells) by the activation of the caspase-9 and -3 signaling pathway. Drug Chem Toxicol 37(1):55–62

    Article  CAS  Google Scholar 

  7. Ming Z, Jing W, Hui Y, Deng SJ, Yuan LY, Guo CZ, Li Z (2011) DNA damage and decrease of cellular oxidase activity in piglet sertoli cells exposed to cadmium. J Vet Med Sci 73(2):199–203

    Article  Google Scholar 

  8. Kim W, Yang HJ, Youn HS, Yun YJ, Seong KM, Youn BH (2018) Myricetin inhibits Akt survival signaling and induces bad-mediated apoptosis in a low dose ultraviolet (UV)-B-irradiated HaCaT human immortalized keratinocytes. J Radiat Res 51(3):285–296

    Article  Google Scholar 

  9. Pan P, Peiffer DS, Huang Y-W, Oshima K, Stoner GD, Wang L-S (2018) Inhibition of the development of N-nitrosomethylbenzylamine-induced esophageal tumors in rats by strawberries and aspirin, alone and in combination. J Berry Res 8(2):137–146. https://doi.org/10.3233/JBR-170291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Jainu M, Devi CS (2006) Antiulcerogenic and ulcer healing effects of Solanum nigrum (L.) on experimental ulcer models: possible mechanism for the inhibition of acid formation. J Ethnopharmacol 104(1–2):156–163

    Article  Google Scholar 

  11. Perez GRM, Perez LJA, Garcia DLM, Sossa MH (1998) Neuropharmacological activity of Solanum nigrum fruit. J Ethnopharmacol 62(1):43–48

    Article  CAS  Google Scholar 

  12. Sun RL, Zhou QX, Sun FH, Jin CX (2007) Antioxidative defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ Exp Bot 60(3):468–476

    Article  CAS  Google Scholar 

  13. Ghosh D, Konishi T (2007) Anthocyanins and anthocyanin-rich extracts: role in diabetes and eye function. Asia Pac J Clin Nutr 16(2):200–208

    CAS  PubMed  Google Scholar 

  14. Rahnastorilla M, Tyni J, Huovinen M, Jarho E, Kulikowicz T, Ravichandran S, Bohr VA, Ferrucci L, Lahtelakakkonen M, Moaddel R (2018) Natural polyphenols as sirtuin 6 modulators. Sci Rep 8(1):4163

    Article  Google Scholar 

  15. Traustadóttir T, Davies SS, Stock AA, Su Y, Heward CB, Roberts LJ, Harman SM (2009) Tart cherry juice decreases oxidative stress in healthy older men and women. J Nutr 139(10):1896–1900

    Article  Google Scholar 

  16. Chun OK, Daeok Kim A, Chang YL (2003) Superoxide radical scavenging activity of the major polyphenols in fresh plums. J Agric Food Chem 51(27):8067–8072

    Article  CAS  Google Scholar 

  17. Galvano F, La FL, Lazzarino G, Fogliano V, Ritieni A, Ciappellano S, Battistini NC, Tavazzi B, Galvano G (2004) Cyanidins: metabolism and biological properties. J Nutr Biochem 15(1):2–11

    Article  CAS  Google Scholar 

  18. Guerra MC, Galvano FL, Speroni E, Costa S, Renzulli C, Cervellati R (2005) Cyanidin-3-O-beta-glucopyranoside, a natural free-radical scavenger against aflatoxin B1- and ochratoxin A-induced cell damage in a human hepatoma cell line (Hep G2) and a human colonic adenocarcinoma cell line (CaCo-2). Br J Nutr 94(2):211–220

    Article  CAS  Google Scholar 

  19. Ullah I, Park HY, Kim MO (2014) Anthocyanins protect against kainic acid-induced excitotoxicity and apoptosis via ROS-activated AMPK pathway in hippocampal neurons. CNS Neurosci Ther 20(4):327–338

    Article  CAS  Google Scholar 

  20. Ye J, Meng X, Yan C, Wang C (2010) Effect of purple sweet potato anthocyanins on beta-amyloid-mediated PC-12 cells death by inhibition of oxidative stress. Neurochem Res 35(3):357–365

    Article  CAS  Google Scholar 

  21. Karlsen A, Retterstã L, Laake P, Paur I, Bøhn SK, Sandvik L, Blomhoff R (2007) Anthocyanins inhibit nuclear factor-κB activation in monocytes and reduce plasma concentrations of pro-inflammatory mediators in healthy adults. J Nutr 137(8):1951–1954

    Article  CAS  Google Scholar 

  22. Choung MG, Baek IY, Kang ST, Han WY, Shin DC, Moon HP, Kang KH (2001) Isolation and determination of anthocyanins in seed coats of black soybean (Glycine max (L.) Merr.). J Agric Food Chem 49(12):5848–5851

    Article  CAS  Google Scholar 

  23. Himly M, Foster DN, Bottoli I, Iacovoni JS, Vogt PK (1998) The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 248(2):295–304

    Article  CAS  Google Scholar 

  24. Foster D (1998) Development of a spontaneously immortalized chicken embryo fibroblastic cell line. Virology 248(2):305–311

    Article  Google Scholar 

  25. Edirisinghe I, Burton-Freeman B (2016) Anti-diabetic actions of Berry polyphenols—review on proposed mechanisms of action. J Berry Res 6(2):237–250

    Article  Google Scholar 

  26. Giampieri F, Gasparrini M (2018) Overexpression of the anthocyanidin synthase gene in strawberry enhances antioxidant capacity and cytotoxic effects on human hepatic cancer cells. J Agric Food Chem 66(3):581–592. https://doi.org/10.1021/acs.jafc.7b04177

    Article  CAS  PubMed  Google Scholar 

  27. Alvarez-Suarez JM, Giampieri F, Gasparrini M, Mazzoni L, Santos-Buelga C, Gonzalez-Paramas AM, Forbes-Hernandez TY, Afrin S, Paez-Watson T, Quiles JL, Battino M (2017) The protective effect of acerola (Malpighia emarginata) against oxidative damage in human dermal fibroblasts through the improvement of antioxidant enzyme activity and mitochondrial functionality. Food Funct 8(9):3250–3258. https://doi.org/10.1039/c7fo00859g

    Article  CAS  PubMed  Google Scholar 

  28. Maciel LG, Mav DC, Azevedo L, Daguer H, Molognoni L, de Almeida MM, Granato D, Rosso ND (2018) Hibiscus sabdariffa anthocyanins-rich extract: chemical stability, in vitro antioxidant and antiproliferative activities. Food Chem Toxicol 113:187–197

    Article  CAS  Google Scholar 

  29. Zhang J, Giampieri F, Afrin S, Battino M, Zheng X, Reboredorodriguez P (2018) Structure-stability relationship of anthocyanins under cell culture condition. Int J Food Sci Nutr. 30:1–9

    CAS  Google Scholar 

  30. Elisia I, Kitts DD (2008) Anthocyanins inhibit peroxyl radical-induced apoptosis in Caco-2 cells. Mol Cell Biochem 312(1–2):139–145

    Article  CAS  Google Scholar 

  31. Wyllie AH, Kerr JF, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68(68):251–306

    Article  CAS  Google Scholar 

  32. Guo X, Disatnik MH, Monbureau M, Shamloo M, Mochlyrosen D, Qi X (2013) Inhibition of mitochondrial fragmentation diminishes Huntington’s disease-associated neurodegeneration. J Clin Invest 123(12):5371–5388

    Article  CAS  Google Scholar 

  33. Tsai HD, Hsieh YY, Hsieh JN, Chang CC, Yang CY, Yang JG, Cheng WL, Tsai FJ, Liu CS (2010) Mitochondria DNA deletion and copy numbers of cumulus cells associated with in vitro fertilization outcomes. J Reprod Med 55(11–12):491–497

    CAS  PubMed  Google Scholar 

  34. Ly JD, Grubb DR, Lawen A (2003) The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 8(2):115–128

    Article  CAS  Google Scholar 

  35. Amicarelli F, Colafarina S, Cattani F, Cimini A, Di IC, Ceru MP, Miranda M (2003) Scavenging system efficiency is crucial for cell resistance to ROS-mediated methylglyoxal injury. Free Radic Biol Med 35(8):856–871

    Article  CAS  Google Scholar 

  36. Semenza GL (2000) Cellular and molecular dissection of reperfusion injury ROS within and without. Circ Res 86(2):117–118

    Article  CAS  Google Scholar 

  37. Uchiyama M (2005) The mechanism of the cell death induced by cadmium and arsenic. Pharm Bull Fukuoka Univ 5:75–76

    Google Scholar 

  38. Redza-Dutordoir M, Averill-Bates DA (2016) Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta 1863(12):2977–2992

    Article  CAS  Google Scholar 

  39. Sinha K, Das J, Pal PB, Sil PC (2013) Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87(7):1157–1180

    Article  CAS  Google Scholar 

  40. Circu ML, Aw TY (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48(6):749–762

    Article  CAS  Google Scholar 

  41. Andreyev AY, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 70(2):200–214

    CAS  PubMed  Google Scholar 

  42. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120(4):483–495

    Article  CAS  Google Scholar 

  43. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417(Pt 1):1–13

    Article  CAS  Google Scholar 

  44. Turrens J (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552(2):335–344

    Article  CAS  Google Scholar 

  45. Huang W, Wu H, Li D, Song J, Xiao Y, Liu C, Zhou J, Sui Z (2018) Protective effects of blueberry anthocyanins against H2O2-induced oxidative injury in human retinal pigment epithelial cells. J Agric Food Chem 66(7):1638–1648

    Article  CAS  Google Scholar 

  46. Kader F, Rovel B, Girardin M, Metche M (2015) Mechanism of browning in fresh highbush blueberry fruit (Vaccinium corymbosum L.). Role of blueberry polyphenol oxidase, chlorogenic acid and anthocyanins. J Sci Food Agric 74(1):31–34

    Article  Google Scholar 

  47. Li X, Liu H, Lv L, Yan H, Yuan Y (2017) Antioxidant activity of blueberry anthocyanin extracts and their protective effects against acrylamide-induced toxicity in HepG2 cells. Int J Food Sci Technol 53(1):147–155. https://doi.org/10.1111/ijfs.13568

    Article  CAS  Google Scholar 

  48. Wu H, Hutabarat RP, Huang WY (2018) Modeling of H2O2-induced damage in retinal pigment epithelial cells and protective effects of blueberry anthocyanin. Chin Pharmacol Bull 34(2):274–279

    Google Scholar 

  49. Kim A, Kwon OS, Kim SO, He L, Bae EY, Lee MS, Jeong SJ, Shim JH, Yoon DY, Kim CH (2010) Caspase-3 activation as a key factor for HBx-transformed cell death. Cell Prolif 41(5):755–774

    Article  Google Scholar 

  50. Putt KS, Chen GW, Pearson JM, Sandhorst JS, Hoagland MS, Kwon JT, Hwang SK, Jin H, Churchwell MI, Cho MH (2006) Small-molecule activation of procaspase-3 to caspase-3 as a personalized anticancer strategy. Nat Chem Biol 2(10):543–550

    Article  CAS  Google Scholar 

  51. Stennicke HR, Jürgensmeier JM, Shin H, Deveraux Q, Wolf BB, Yang X, Zhou Q, Ellerby HM, Ellerby LM, Bredesen D (1998) Pro-caspase-3 is a major physiologic target of caspase-8. J Biol Chem 273(42):27084–27090

    Article  CAS  Google Scholar 

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Acknowledgements

The project was supported by the National Key R&D Program (2016YFD0501208, 2016YFD0501007), National Nature Science Foundation of China (No. 31872535), Shandong Natural Science Foundation of China (ZR2018MC027, ZR2016CQ29) and Funds of Shandong “Double Tops” Program.

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Correspondence to Yongxia Liu or Jianzhu Liu.

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Xie, N., Geng, N., Zhou, D. et al. Protective effects of anthocyanin against apoptosis and oxidative stress induced by arsanilic acid in DF-1 cells. Mol Biol Rep 46, 301–308 (2019). https://doi.org/10.1007/s11033-018-4472-5

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  • DOI: https://doi.org/10.1007/s11033-018-4472-5

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