The protective effect of oleuropein against radiation-induced cytotoxicity, apoptosis, and genetic damage in cultured human lymphocytes

References

• Al-Azzawie HF, Alhamdani M-SS. 2006. Hypoglycemic and antioxidant effect of oleuropein in alloxan-diabetic rabbits. Life Sci. 78(12):1371–1377.
   PubMed Web of Science ®Google Scholar
• Alirezaei M, Dezfoulian O, Neamati S, Rashidipour M, Tanideh N, Kheradmand A. 2012. Oleuropein prevents ethanol-induced gastric ulcers via elevation of antioxidant enzyme activities in rats. J Physiol Biochem. 68(4):583–592.
   PubMed Web of Science ®Google Scholar
• Allahbakhshian-Farsani M, Abdian N, Ghasemi-Dehkordi P, Sadeghiani M, Saffari-Chaleshtori J, Hashemzadeh-Chaleshtori M, Khosravi-Farsani S. 2014. Cytogentic analysis of human dermal fibroblasts (HDFs) in early and late passages using both karyotyping and comet assay techniques. Cytotechnology. 66(5):815–822.
   Google Scholar
• Aminian M, Bakhshandeh M, Allahbakhshian-Farsani M, Bakhshandeh E, Shakeri N. 2017. Comparison of the protection performance in a composite shield and a lead standard shield in terms of biological effects in nuclear medicine. Iran J Nucl Med. 25(2):129–135.
   Google Scholar
• Azzam EI, Jay-Gerin J-P, Pain D. 2012. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 327(1–2):48–60.
   PubMed Web of Science ®Google Scholar
• Begum N, Prasad NR, Kanimozhi G, Hasan AQ. 2012. Apigenin ameliorates gamma-radiation-induced cytogenetic alterations in cultured human blood lymphocytes. Mut Res/Genet Toxicol Env Mutagenesis. 747(1):71–76.
   PubMed Web of Science ®Google Scholar
• Benavente-Garcıa O, Castillo J, Lorente J, Ortuño A, Del Rio JA. 2000. Antioxidant activity of phenolics extracted from Olea europaea L. leaves. Food Chem. 68(4):457–462.
   Web of Science ®Google Scholar
• Bennett CB, Lewis AL, Baldwin KK, Resnick MA. 1993. Lethality induced by a single site-specific double-strand break in a dispensable yeast plasmid. Proc Nat Acad Sci. 90(12):5613–5617.
   PubMed Web of Science ®Google Scholar
• Bordón E, Henríquez-Hernández LA, Lara PC, Ruíz A, Pinar B, Rodríguez-Gallego C, Lloret M. 2010. Prediction of clinical toxicity in locally advanced head and neck cancer patients by radio-induced apoptosis in peripheral blood lymphocytes (PBLs). Radiat Oncol. 5(1):4.
   PubMedGoogle Scholar
• Brown DQ, Pittock JW, Rubinstein JS. 1982. Early results of the screening program for radioprotectors. Int J Rad Oncol Biol Phys. 8(3–4):565–570.
   PubMed Web of Science ®Google Scholar
• Bulotta S, Celano M, Lepore SM, Montalcini T, Pujia A, Russo D. 2014. Beneficial effects of the olive oil phenolic components oleuropein and hydroxytyrosol: focus on protection against cardiovascular and metabolic diseases. J Transl Med. 12(1):219.
   PubMed Web of Science ®Google Scholar
• Cassatt DR, Fazenbaker CA, Bachy CM, Hanson MS. 2002. Preclinical modeling of improved amifostine (Ethyol) use in radiation therapy. Sem Rad Oncol. 12(1):97–102.
   PubMed Web of Science ®Google Scholar
• Cheki M, Shirazi A, Mahmoudzadeh A, Bazzaz JT, Hosseinimehr SJ. 2016. The radioprotective effect of metformin against cytotoxicity and genotoxicity induced by ionizing radiation in cultured human blood lymphocytes. Mutat Res. 809:24–32.
   PubMed Web of Science ®Google Scholar
• Coggle JE. 1983. Biological effects of radiation. London (UK); New York (NY): Taylor & Francis.
   Google Scholar
• Coni E, Di Benedetto R, Di Pasquale M, Masella R, Modesti D, Mattei R, Carlini EA. 2000. Protective effect of oleuropein, an olive oil biophenol, on low density lipoprotein oxidizability in rabbits. Lipids. 35(1):45–54.
   PubMed Web of Science ®Google Scholar
• Davari H, Haddad F, Moghimi A, Rahimi MF, Ghavamnasiri MR. 2012. Study of radioprotective effect of green tea against gamma irradiation using micronucleus assay on binucleated human lymphocytes. Iran J Basic Med Sci. 15(5):1026.
   PubMed Web of Science ®Google Scholar
• Delic J, Morange M, Magdelenat H. 1993. Ubiquitin pathway involvement in human lymphocyte gamma-irradiation-induced apoptosis. Mol Cell Biol. 13(8):4875–4883.
   PubMed Web of Science ®Google Scholar
• Di Domenico F, Perluigi M, Foppoli C, Blarzino C, Coccia R, De Marco F, Butterfield DA, Cini C. 2009. Protective effect of ferulic acid ethyl ester against oxidative stress mediated by UVB irradiation in human epidermal melanocytes. Free Radic Res. 43(4):365–375.
   PubMed Web of Science ®Google Scholar
• Dive C, Gregory CD, Phipps DJ, Evans DL, Milner AE, Wyllie AH. 1992. Analysis and discrimination of necrosis and apoptosis (programmed cell death) by multiparameter flow cytometry. Biochim Biophys Acta (BBA)-Mol Cell Res. 1133(3):275–285.
   PubMedGoogle Scholar
• Dizdaroglu M, Jaruga P. 2012. Mechanisms of free radical-induced damage to DNA. Free Radic Res. 46(4):382–419.
   PubMed Web of Science ®Google Scholar
• Eriksson D, Stigbrand T. 2010. Radiation-induced cell death mechanisms. Tumour Biol. 31(4):363–372.
   PubMedGoogle Scholar
• Etebari M, Ghannadi A, Jafarian-Dehkordi A, Ahmadi F. 2012. Genotoxicity evaluation of aqueous extracts of Cotoneaster discolor and Alhagi pseudoalhagi manna by comet assay. Res Pharma Sci. 7(5):149.
   Google Scholar
• Etebari M, Zolfaghari B, Jafarian-Dehkordi A, Rakian R. 2012. Evaluation of DNA damage of hydro-alcoholic and aqueous extract of Echium amoenum and Nardostachys jatamansi. J Res Med Sci. 17(8):782.
   PubMed Web of Science ®Google Scholar
• Evens AM, Prachand S, Shi B, Paniaqua M, Gordon LI, Gartenhaus RB. 2004. Imexon-induced apoptosis in multiple myeloma tumor cells is caspase-8 dependent. Clin Cancer Res. 10(4):1481–1491.
   PubMed Web of Science ®Google Scholar
• Ghoraeian P, Mozdarani H, Akhlaghpoor S. 2005. Effect of famotidine on radiation induced apoptosis in human peripheral blood leukocytes. Iran J Rad Res. 3(1):31–36.
   Google Scholar
• Hall EJ, Giaccia AJ. 2006. Radiobiology for the Radiologist. Philadelphia (PA): Lippincott Williams & Wilkins.
   Google Scholar
• Hassen I, Casabianca H, Hosni K. 2015. Biological activities of the natural antioxidant oleuropein: exceeding the expectation–a mini-review. J Funct Foods. 18:926–940.
   Web of Science ®Google Scholar
• Hertveldt JP, Thierens H, Cornelissen M, Vral A, De Ridder KL. 1997. Technical report flow cytometry as a quantitative and sensitive method to evaluate low dose radiation induced apoptosis in vitro in human peripheral blood lymphocytes. Int J Radiat Biol. 71(4):429–433.
   PubMed Web of Science ®Google Scholar
• Heyder P, Gaipl US, Beyer TD, Voll RE, Kern PM, Stach C, Kalden JR, Herrmann M. 2003. Early detection of apoptosis by staining of acid-treated apoptotic cells with FITC-labeled lectin from Narcissus pseudonarcissus. Cytometry A. 55(2):86–93.
   PubMedGoogle Scholar
• Hoeijmakers JH. 2001. Genome maintenance mechanisms for preventing cancer. Nature. 411(6835):366–374.
   PubMed Web of Science ®Google Scholar
• Hosseinimehr SJ. 2007a. Natural product aspotential radioprotective agents. J Mazandaran Univ Med Sci. 17(61):175–189.
   Google Scholar
• Hosseinimehr SJ. 2007b. Trends in the development of radioprotective agents. Drug Discov Today. 12(19–20):794–805.
   PubMed Web of Science ®Google Scholar
• Hosseinimehr SJ, Mahmoudzadeh A, Azadbakht M, Akhlaghpoor S. 2009. Radioprotective effects of Hawthorn against genotoxicity induced by gamma irradiation in human blood lymphocytes. Radiat Environ Biophys. 48(1):95–98.
   PubMed Web of Science ®Google Scholar
• Huang X, Okafuji M, Traganos F, Luther E, Holden E, Darzynkiewicz Z. 2004. Assessment of histone H2AX phosphorylation induced by DNA topoisomerase I and II inhibitors topotecan and mitoxantrone and by the DNA cross-linking agent cisplatin. Cytometry A. 58(2):99–110.
   PubMedGoogle Scholar
• Islamian JP, Mehrali H. 2015. Lycopene as a carotenoid provides radioprotectant and antioxidant effects by quenching radiation-induced free radical singlet oxygen: an overview. Cell J. 16(4):386.
   PubMed Web of Science ®Google Scholar
• Jagetia GC. 2007. Radioprotective potential of plants and herbs against the effects of ionizing radiation. J Clin Biochem Nutr. 40(2):74–81.
   PubMed Web of Science ®Google Scholar
• Kalman NS, Zhao SS, Anscher MS, Urdaneta AI. 2017. Current status of targeted radioprotection and radiation injury mitigation and treatment agents: a critical review of the literature. Int J Rad Oncol Biol Phys. 98(3):662–682.
   PubMed Web of Science ®Google Scholar
• Kanimozhi G, Prasad NR, Ramachandran S, Pugalendi KV. 2011. Umbelliferone modulates gamma-radiation induced reactive oxygen species generation and subsequent oxidative damage in human blood lymphocytes. Eur J Pharmacol. 672(1–3):20–29.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Kim MH, Byon YY, Park JW, Jee Y, Joo HG. 2007. Radioprotective effects of an acidic polysaccharide of Panax ginseng on bone marrow cells. J Vet Sci. 8(1):39–44.
   PubMed Web of Science ®Google Scholar
• Kmochova A, Tichy A, Zarybnicka L, Sinkorova Z, Vavrova J, Rehacek V, Durisova K, Kubelkova K, Pejchal J, Kuca K, et al. 2016. Modulation of ionizing radiation-induced effects by NU7441, KU55933 and VE821 in peripheral blood lymphocytes. J Appl Biomed. 14(1):19–24.
   Web of Science ®Google Scholar
• Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. 1994. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood. 84(5):1415–1420.
   PubMed Web of Science ®Google Scholar
• Kopjar N, Miocić S, Ramić S, Milić M, Viculin T. 2006. Assessment of the radioprotective effects of amifostine and melatonin on human lymphocytes irradiated with gamma-rays in vitro. Arh Hig Rada Toksikol. 57(2):155.
   PubMedGoogle Scholar
• Lankoff A, Banasik A, Duma A, Ochniak E, Lisowska H, Kuszewski T, Góźdź S, Wojcik A. 2006. A comet assay study reveals that aluminium induces DNA damage and inhibits the repair of radiation-induced lesions in human peripheral blood lymphocytes. Toxicol Lett. 161(1):27–36.
   PubMed Web of Science ®Google Scholar
• Lapierre A, Brengues M, Bourgier C, Ozsahin EM, Azria D. 2017. Radiation induced lymphocyte apoptosis assay and predictive breast fibrosis nomogram: first implementation in daily practice in France. Int J Rad Oncol Biol Phys. 99(2):E27–E28.
   Web of Science ®Google Scholar
• Lawenda BD, Kelly KM, Ladas EJ, Sagar SM, Vickers A, Blumberg JB. 2008. Should supplemental antioxidant administration be avoided during chemotherapy and radiation therapy? J Nat Cancer Inst. 100(11):773–783.
   PubMedGoogle Scholar
• Le Caër S. 2011. Water radiolysis: influence of oxide surfaces on H2 production under ionizing radiation. Water. 3(1):235–253.
   Web of Science ®Google Scholar
• Lee-Huang S, Zhang L, Huang PL, Chang Y-T, Huang PL. 2003. Anti-HIV activity of olive leaf extract (OLE) and modulation of host cell gene expression by HIV-1 infection and OLE treatment. Biochem Biophys Res Commun. 307(4):1029–1037.
   PubMed Web of Science ®Google Scholar
• Lobo V, Patil A, Phatak A, Chandra N. 2010. Free radicals, antioxidants and functional foods: impact on human health. Pharmacogn Rev. 4(8):118–126.
   PubMedGoogle Scholar
• Mahvi A, Mardani G, Ghasemi-Dehkordi P, Saffari-Chaleshtori J, Hashemzadeh-Chaleshtori M, Allahbakhshian-Farsani M, Abdian N. 2015. Effects of phenanthrene and pyrene on cytogenetic stability of human dermal fibroblasts using alkaline comet assay technique. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences. 85(4):1055–1063.
   Google Scholar
• Matteucci C, Grelli S, De Smaele E, Fontana C, Mastino A. 1999. Identification of nuclei from apoptotic, necrotic, and viable lymphoid cells by using multiparameter flow cytometry. Cytometry: J Int Soc Anal Cytol. 35(2):145–153.
   PubMedGoogle Scholar
• Maurya DK, Adhikari S, Nair CKK, Devasagayam TPA. 2007. DNA protective properties of vanillin against gamma-radiation under different conditions: possible mechanisms. Mutat Res. 634(1–2):69–80.
   PubMed Web of Science ®Google Scholar
• Mozdarani H, Ghoraeian P. 2008. Modulation of gamma-ray-induced apoptosis in human peripheral blood leukocytes by famotidine and vitamin C. Mut Res/Genet Toxicol Env Mutagen. 649(1–2):71–78.
   PubMed Web of Science ®Google Scholar
• Mozdarani H, Vessal NJ. 1993. CIMETIDINE CAN MODIFY THE EFFECTS OF WHOLE BODY'Y-IRRADIATION ON LY MPHOHEM ATOPOIETIC SYSTEM. Med J Islamic Republic Of Iran. 7(2):95–99.
   Google Scholar
• Nair CK, Parida DK, Nomura T. 2001. Radioprotectors in radiotherapy. J Radiat Res. 42(1):21–37.
   PubMed Web of Science ®Google Scholar
• Nübel T, Damrot J, Roos WP, Kaina B, Fritz G. 2006. Lovastatin protects human endothelial cells from killing by ionizing radiation without impairing induction and repair of DNA double-strand breaks. Clin Cancer Res. 12(3):933–939.
   PubMed Web of Science ®Google Scholar
• Ozsahin M, Ozsahin H, Shi Y, Larsson B, Würgler FE, Crompton NEA. 1997. Rapid assay of intrinsic radiosensitivity based on apoptosis in human CD4 and CD8 T-lymphocytes. Int J Rad Oncol Biol Phys. 38(2):429–440.
   PubMed Web of Science ®Google Scholar
• Patt HM, Mayer SH, Straube RL, Jackson EM. 1953. Radiation dose reduction by cysteine. J Cell Comp Physiol. 42(3):327–341.
   PubMedGoogle Scholar
• Petkov V, Manolov P. 1972. Pharmacological analysis of the iridoid oleuropein. Arzneimittelforschung. 22(9):1476–1486.
   PubMedGoogle Scholar
• Pietta P-G. 2000. Flavonoids as antioxidants. J Nat Prod. 63(7):1035–1042.
   PubMed Web of Science ®Google Scholar
• Radford IR, Murphy TK, Radley JM, Ellis SL. 1994. Radiation response of mouse lymphoid and myeloid cell lines. Part II. Apoptotic death is shown by all lines examined. Int J Radiat Biol. 65(2):217–227.
   PubMed Web of Science ®Google Scholar
• Rao BN, Archana PR, Aithal BK, Rao BSS. 2011. Protective effect of zingerone, a dietary compound against radiation induced genetic damage and apoptosis in human lymphocytes. Eur J Pharmacol. 657(1–3):59–66.
   PubMed Web of Science ®Google Scholar
• Riss TL, Moravec RA, Niles AL, Duellman S, Benink HA, Worcella TJ, Minor L, Sittampalam GS, Grossman A, Brimacombe K, et al. 2016. Cell viability assays. In: Assay guidance manual. Bethesda (MD): Eli Lilly & Company and the National Center for Advancing Translational Sciences.
   Google Scholar
• Saija A, Trombetta D, Tomaino A, Lo Cascio R, Princi P, Uccella N, Bonina F, Castelli F. 1998. In vitro evaluation of the antioxidant activity and biomembrane interaction of the plant phenols oleuropein and hydroxytyrosol. Int J Pharma. 166(2):123–133.
   Web of Science ®Google Scholar
• Saija A, Scalese M, Lanza M, Marzullo D, Bonina F, Castelli F. 1995. Flavonoids as antioxidant agents: importance of their interaction with biomembranes. Free Radical Biol Med. 19(4):481–486.
   PubMed Web of Science ®Google Scholar
• Samarth RM, Panwar M, Kumar M, Soni A, Kumar M, Kumar A. 2008. Evaluation of antioxidant and radical-scavenging activities of certain radioprotective plant extracts. Food Chem. 106(2):868–873.
   Web of Science ®Google Scholar
• Sellins KS, Cohen JJ. 1987. Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes. J Immunol. 139(10):3199–3206.
   PubMed Web of Science ®Google Scholar
• Shiloh Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer. 3(3):155–168.
   PubMed Web of Science ®Google Scholar
• Siddiqi MA, Bothe E. 1987. Single-and double-strand break formation in DNA irradiated in aqueous solution: dependence on dose and OH radical scavenger concentration. Radiat Res. 112(3):449–463.
   PubMed Web of Science ®Google Scholar
• Speroni E, Guerra MC, Minghetti A, Crespi‐Perellino N, Pasini P, Piazza F, Roda A. 1998. Oleuropein evaluated in vitro and in vivo as an antioxidant. Phytother Res. 12(S1):S98–S100.
   Google Scholar
• Stathakis S. 2010. The physics of radiation therapy. Med Phys. 37(3):1374–1375.
   Google Scholar
• Taverna Porro ML, Greenberg MM. 2015. Double-strand breaks from a radical commonly produced by DNA-damaging agents. Chem Res Toxicol. 28(4):810–816.
   PubMed Web of Science ®Google Scholar
• Tice R, Vasquez M. 1998. Protocol for the application of the pH> 13 alkaline single cell gel (SCG) assay to the detection of DNA damage in mammalian cells. Sigma. 503:465–8353.
   Google Scholar
• Trowell OA, Corp MJ, Lush WR. 1957. Paradoxical resistance of thymus lymphocytes to high doses of X-radiation. Radiat Res. 7(2):120–128.
   PubMed Web of Science ®Google Scholar
• Tubiana M, Dutreix J, Wambersie J. 1990. Introduction to radiobiology. London (UK); New York (NY): Taylor & Francis.
   Google Scholar
• Verma A, Prasad KN, Singh AK, Nyati KK, Gupta RK, Paliwal VK. 2010. Evaluation of the MTT lymphocyte proliferation assay for the diagnosis of neurocysticercosis. J Microbiol Meth. 81(2):175–178.
   PubMed Web of Science ®Google Scholar
• Vermes I, Haanen C, Reutelingsperger C. 2000. Flow cytometry of apoptotic cell death. J Immunol Meth. 243(1–2):167–190.
   PubMed Web of Science ®Google Scholar
• Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. 1995. A novel assay for apoptosis flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J Immunol Meth. 184(1):39–51.
   PubMed Web of Science ®Google Scholar
• Vilasová Z, Rezácová M, Vávrová J, Tichý A, Vokurková D, Zoelzer F, Reháková Z, Osterreicher J, Lukásová E. 2008. Changes in phosphorylation of histone H2A. X and p53 in response of peripheral blood lymphocytes to gamma irradiation. Acta Biochim Pol. 55(2):381–390.
   PubMed Web of Science ®Google Scholar
• Visioli F, Galli C. 1994. Oleuropein protects low density lipoprotein from oxidation. Life Sci. 55(24):1965–1971.
   PubMed Web of Science ®Google Scholar
• Waddick KG, Song CW, Souza L, Uckun FM. 1991. Comparative analysis of the in vivo radioprotective effects of recombinant granulocyte colony-stimulating factor (G-CSF), recombinant granulocyte-macrophage CSF, and their combination. Blood. 77(11):2364–2371.
   PubMed Web of Science ®Google Scholar
• Ward J. 1990. The yield of DNA double-strand breaks produced intracellularly by ionizing radiation: a review. Int J Radiat Biol. 57(6):1141–1150.
   PubMed Web of Science ®Google Scholar
• Whitnall MH, Wilhelmsen CL, McKinney L, Miner V, Seed TM, Jackson WE. 2002. Radioprotective efficacy and acute toxicity of 5-androstenediol after subcutaneous or oral administration in mice. Immunopharmacol Immunotoxicol. 24(4):595–626.
   PubMed Web of Science ®Google Scholar
• Wilkins RC, Kutzner BC, Truong M, Sanchez-Dardon J, McLean JRN. 2002. Analysis of radiation-induced apoptosis in human lymphocytes: flow cytometry using Annexin V and propidium iodide versus the neutral comet assay. Cytometry. 48(1):14–19.
   PubMedGoogle Scholar
• Wlodkowic D, Telford W, Skommer J, Darzynkiewicz Z. 2011. Apoptosis and beyond: cytometry in studies of programmed cell death. Methods Cell Biol. 103:55–98.
   PubMed Web of Science ®Google Scholar
• Wojcikowski K, Stevenson L, Leach D, Wohlmuth H, Gobe G. 2007. Antioxidant capacity of 55 medicinal herbs traditionally used to treat the urinary system: a comparison using a sequential three-solvent extraction process. J Altern Complement Med. 13(1):103–109.
   PubMed Web of Science ®Google Scholar
• Yamini K, Gopal V. 2010. Natural radioprotective agents against ionizing radiation–an overview. Int J PharmTech Res. 2(2):1421–1426.
   Google Scholar
• Yang F, Zhou B-R, Zhang P, Zhao Y-F, Chen J, Liang Y. 2007. Binding of ferulic acid to cytochrome c enhances stability of the protein at physiological pH and inhibits cytochrome c-induced apoptosis. Chem Biol Interact. 170(3):231–243.
   PubMed Web of Science ®Google Scholar
• Zamai L, Falcieri E, Zauli G, Cataldi A, Vitale M. 1993. Optimal detection of apoptosis by flow cytometry depends on cell morphology. Cytometry. 14(8):891–897.
   PubMedGoogle Scholar
• Zhang G, Gurtu V, Kain SR, Yan G. 1997. Early detection of apoptosis using a fluorescent conjugate of annexin V. Biotechniques. 23(3):525–531.
   PubMed Web of Science ®Google Scholar
• Zhang HM, Nie JS, Li X, Niu Q. 2012. Characteristic analysis of peripheral blood mononuclear cell apoptosis in coke oven workers. J Occup Health. 54(1):44–50.
   PubMed Web of Science ®Google Scholar