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Heat treatment and protective potentials of luteolin-7-O-glucoside against cisplatin genotoxic and cytotoxic effects

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Abstract

Cisplatin is an effective chemotherapeutic agent that has pronounced adverse effects. Using flavonoids is currently eliciting considerable interest. During extraction and conditioning, they usually undergo several physical treatments such as heat treatment, although it is not known whether thermal treatment might influence the pharmacological effects of flavonoids such as luteolin-7-O-glucoside (L7G). This study was undertaken to explore the protective role of native and heated L7G against DNA damage and oxidative stress induced by cisplatin. Balb/c mice were administered L7G before a single intraperitoneal injection of cisplatin (10 mg/kg). Animals were sacrificed 24 h after treatment with drugs. The geno-protective role of native and heated L7G was evaluated by comet assay. In addition to monitoring the activities of antioxidant enzymes, levels of malondialdehyde and reduced glutathione were assessed in the liver, kidney, brain, and spleen tissues. The results of the present study demonstrate that both heated and native L7G, at a dose of 40 mg/kg b.w, were able to reduce the genotoxicity of cisplatin. They attenuate the oxidative stress (malondialdehyde, catalase, GPx, SOD, and GSH) and tissue damage (creatinine, IFNγ). Heat treatment did not alter the antigenotoxic effect observed for native L7G and showed similar effects to those of native L7G for all of the evaluated parameters. Our study reveals that L7G attenuates the side effects of anticancer drug and heat treatment did not alter his antigenotoxic and antioxidant the potential.

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References

  • Adeoye BO, Asenuga ER, Oyagbemi AA et al (2017) The protective effect of the ethanol leaf extract of Andrographis paniculata on cisplatin-induced acute kidney injury in rats through nrf2/KIM-1 signalling pathway. Drug Res. https://doi.org/10.1055/s-0043-118179

  • Ahmed EA, Omar HM, elghaffar Sk, et al (2011) The antioxidant activity of vitamin C, DPPD and L-cysteine against cisplatin-induced testicular oxidative damage in rats. Food Chem Toxicol 49:1115–1121. doi: https://doi.org/10.1016/j.fct.2011.02.002

  • Almaghrabi OA (2015) Molecular and biochemical investigations on the effect of quercetin on oxidative stress induced by cisplatin in rat kidney. Saudi J Biol Sci 22:227–231. https://doi.org/10.1016/j.sjbs.2014.12.008

    Article  CAS  Google Scholar 

  • Aly MS, Ashour MB, El Nahas SM, Abo Zeid MAF (2003) Genotoxicity and cytotoxicity of the anticancer drugs gemcitabine and cisplatin, separately and in combination: in vivo studies. J Biol Sci 3:961–972

    Article  Google Scholar 

  • Ansari MA (2017) Sinapic acid modulates Nrf2/HO-1 signaling pathway in cisplatin-induced nephrotoxicity in rats. Biomed Pharmacother 93:646–653. https://doi.org/10.1016/j.biopha.2017.06.085

    Article  CAS  Google Scholar 

  • Anuradha S, Devi KR (2011) Anti-genotoxic effects of crude garlic extract on cisplatin induced toxicity on germ cells and morphology of sperms in in vivo mouse. J Cell Anim Biol 5:279–282

    Google Scholar 

  • Arjumand W, Sultana S (2011) Glycyrrhizic acid: a phytochemical with a protective role against cisplatin-induced genotoxicity and nephrotoxicity. Life Sci 89:422–429. https://doi.org/10.1016/j.lfs.2011.06.016

    Article  CAS  Google Scholar 

  • Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell, Longev

    Google Scholar 

  • Badary OA, Abdel-Maksoud S, Ahmed WA, Owieda GH (2005) Naringenin attenuates cisplatin nephrotoxicity in rats. Life Sci 76:2125–2135. https://doi.org/10.1016/j.lfs.2004.11.005

    Article  CAS  Google Scholar 

  • Barberino RS, Menezes VG, Ribeiro A, Palheta RC Jr, Jiang X, Smitz JEJ, Matos MHT (2017) Melatonin protects against cisplatin-induced ovarian damage in mice via the MT1 receptor and antioxidant activity. Biol Reprod 96:1244–1255. https://doi.org/10.1093/biolre/iox053

    Article  Google Scholar 

  • Baskar AA, Ignacimuthu S, Michael GP, Al Numair KS (2011) Cancer chemopreventive potential of luteolin-7-O-glucoside isolated from Ophiorrhiza mungos Linn. Nutr Cancer 63:130–138

    CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19. https://doi.org/10.1097/WOX.0b013e3182439613

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Camera E, Mastrofrancesco A, Fabbri C et al (2009) Astaxanthin, canthaxanthin and beta-carotene differently affect UVA-induced oxidative damage and expression of oxidative stress-responsive enzymes. Exp Dermatol 18:222–231. https://doi.org/10.1111/j.1600-0625.2008.00790.x

    Article  CAS  Google Scholar 

  • Chaaban H, Ioannou I, Chebil L et al (2017) Effect of heat processing on thermal stability and antioxidant activity of six flavonoids. J Food Process Preserv

  • Cimino GD, Pan CX, Henderson PT (2013) Personalized medicine for targeted and platinum-based chemotherapy of lung and bladder cancer. Bioanalysis 5:369–391. https://doi.org/10.4155/bio.12.325

    Article  CAS  Google Scholar 

  • Clairbone A (1985) Catalase activity. Handbook of methods for oxygen radical research. CRC Press

  • Dasari S, Tchounwou PB (2014) Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol 740:364–378. https://doi.org/10.1016/j.ejphar.2014.07.025

    Article  CAS  Google Scholar 

  • Domitrovic R, Cvijanovic O, Pugel EP et al (2013) Luteolin ameliorates cisplatin-induced nephrotoxicity in mice through inhibition of platinum accumulation, inflammation and apoptosis in the kidney. Toxicology 310:115–123. https://doi.org/10.1016/j.tox.2013.05.015

    Article  CAS  Google Scholar 

  • Dzialo M, Mierziak J, Korzun U et al (2016) The potential of plant phenolics in prevention and therapy of skin disorders. Int J Mol Sci 17:160. https://doi.org/10.3390/ijms17020160

    Article  CAS  Google Scholar 

  • Eke D, Celik A (2016) Curcumin prevents perfluorooctane sulfonate-induced genotoxicity and oxidative DNA damage in rat peripheral blood. Drug Chem Toxicol 39:97–103. https://doi.org/10.3109/01480545.2015.1041601

    Article  CAS  Google Scholar 

  • Ekinci Akdemir FN, Albayrak M, Calik M et al (2017) The protective effects of p-coumaric acid on acute liver and kidney damages induced by cisplatin. Biomedicines 5. https://doi.org/10.3390/biomedicines5020018

  • Erel O (2004) A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37:277–285. https://doi.org/10.1016/j.clinbiochem.2003.11.015

    Article  CAS  Google Scholar 

  • Espinosa-Diez C, Miguel V, Mennerich D, Kietzmann T, Sánchez-Pérez P, Cadenas S, Lamas S (2015) Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol 6:183–197. https://doi.org/10.1016/j.redox.2015.07.008

    Article  CAS  Google Scholar 

  • Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzym 105:114–121

    Article  CAS  Google Scholar 

  • Fouad AA, Refaie MMM, Abdelghany MI (2018) Naringenin palliates cisplatin and doxorubicin gonadal toxicity in male rats. Toxicol Mech Methods:1–7. https://doi.org/10.1080/15376516.2018.1512180

  • Gaweł S, Wardas M, Niedworok E, Wardas P (2004) Malondialdehyde (MDA) as a lipid peroxidation marker. Wiad Lek (Warsaw, Pol 1960) 57:453–455

    Google Scholar 

  • Geyikoglu F, Isikgoz H, Onalan H et al (2017) Impact of high-dose oleuropein on cisplatin-induced oxidative stress, genotoxicity and pathological changes in rat stomach and lung. J Asian Nat Prod Res:1–18. https://doi.org/10.1080/10286020.2017.1317751

  • Giridharan VV, Thandavarayan RA, Bhilwade HN, Ko KM, Watanabe K, Konishi T (2012) Schisandrin B, attenuates cisplatin-induced oxidative stress, genotoxicity and neurotoxicity through modulating NF-kappaB pathway in mice. Free Radic Res 46:50–60. https://doi.org/10.3109/10715762.2011.638291

    Article  CAS  Google Scholar 

  • Hah SS, Stivers KM, de Vere White RW, Henderson PT (2006) Kinetics of carboplatin-DNA binding in genomic DNA and bladder cancer cells as determined by accelerator mass spectrometry. Chem Res Toxicol 19:622–626. https://doi.org/10.1021/tx060058c

    Article  CAS  Google Scholar 

  • Hassan I, Chibber S, Naseem I (2010) Ameliorative effect of riboflavin on the cisplatin induced nephrotoxicity and hepatotoxicity under photoillumination. Food Chem Toxicol 48:2052–2058. https://doi.org/10.1016/j.fct.2010.05.004

    Article  CAS  Google Scholar 

  • Hassan SM, Khalaf MM, Sadek SA, Abo-Youssef AM (2017) Protective effects of apigenin and myricetin against cisplatin-induced nephrotoxicity in mice. Pharm Biol 55:766–774. https://doi.org/10.1080/13880209.2016.1275704

    Article  CAS  Google Scholar 

  • Hegarty M, Chisholm D (2002) Chemotherapy and anaesthesia. Curr Anaesth Crit Care 13:168–174

    Article  Google Scholar 

  • Heindel JJ, Blumberg B, Cave M et al (2017) Metabolism disrupting chemicals and metabolic disorders. Reprod Toxicol. https://doi.org/10.1016/j.reprotox.2016.10.001

  • Hou XM, Zhang XH, Wei KJ, Ji C, Dou SX, Wang WC, Li M, Wang PY (2009) Cisplatin induces loop structures and condensation of single DNA molecules. Nucleic Acids Res 37:1400–1410. https://doi.org/10.1093/nar/gkn933

    Article  CAS  Google Scholar 

  • Houmani H, Rodriguez-Ruiz M, Palma JM et al (2016) Modulation of superoxide dismutase (SOD) isozymes by organ development and high long-term salinity in the halophyte Cakile maritima. Protoplasma 253:885–894. https://doi.org/10.1007/s00709-015-0850-1

    Article  CAS  Google Scholar 

  • Hu C, Kitts DD (2004) Luteolin and luteolin-7-O-glucoside from dandelion flower suppress iNOS and COX-2 in RAW264.7 cells. Mol Cell Biochem 265:107–113

    Article  CAS  Google Scholar 

  • Jordan P, Carmo-Fonseca M (2000) Molecular mechanisms involved in cisplatin cytotoxicity. Cell Mol Life Sci 57:1229–1235

    Article  CAS  Google Scholar 

  • Khan R, Khan AQ, Qamar W, Lateef A, Ali F, Rehman MU, Tahir M, Sharma S, Sultana S (2012) Chrysin abrogates cisplatin-induced oxidative stress, p53 expression, goblet cell disintegration and apoptotic responses in the jejunum of Wistar rats. Br J Nutr 108:1574–1585. https://doi.org/10.1017/S0007114511007239

    Article  CAS  Google Scholar 

  • Kilic U, Kilic E, Tuzcu Z et al (2013) Melatonin suppresses cisplatin-induced nephrotoxicity via activation of Nrf-2/HO-1 pathway. Nutr Metab 10:7. https://doi.org/10.1186/1743-7075-10-7

    Article  CAS  Google Scholar 

  • Liao Y, Lu X, Lu C, Li G, Jin Y, Tang H (2008) Selection of agents for prevention of cisplatin-induced hepatotoxicity. Pharmacol Res 57:125–131. https://doi.org/10.1016/j.phrs.2008.01.001

    Article  CAS  Google Scholar 

  • Lin CZ, Zhu CC, Hu M, Wu AZ, Bairu ZD, Kangsa SQ (2014) Structure-activity relationships of antioxidant activity in vitro about flavonoids isolated from Pyrethrum tatsienense. J Intercult Ethnopharmacol 3:123–127. https://doi.org/10.5455/jice.20140619030232

    Article  Google Scholar 

  • Liu HT, Wang TE, Hsu YT et al (2019) Nanoparticulated honokiol mitigates cisplatin-induced chronic kidney injury by maintaining mitochondria antioxidant capacity and reducing caspase 3-associated cellular apoptosis. Antioxidants. https://doi.org/10.3390/antiox8100466

  • Lou SN, Lai YC, De Huang J et al (2015) Drying effect on flavonoid composition and antioxidant activity of immature kumquat. Food Chem. https://doi.org/10.1016/j.foodchem.2014.08.119

  • Ma P, Zhang S, Su X, Qiu G, Wu Z (2015a) Protective effects of icariin on cisplatin-induced acute renal injury in mice. Am J Transl Res 7:2105–2114

    CAS  Google Scholar 

  • Ma T, Sun X, Tian C et al (2015b) Enrichment and purification of polyphenol extract from sphallerocarpus gracilis stems and leaves and in vitro evaluation of DNA damage-protective activity and inhibitory effects of α-amylase and α-glucosidase. Molecules. https://doi.org/10.3390/molecules201219780

  • Maatouk M, Mustapha N, Mokdad-Bzeouich I, Chaaban H, Abed B, Iaonnou I, Ghedira K, Ghoul M, Ghedira LC (2017) Thermal treatment of luteolin-7-O-β-glucoside improves its immunomodulatory and antioxidant potencies. Cell Stress Chaperones 22:775–785. https://doi.org/10.1007/s12192-017-0808-7

    Article  CAS  Google Scholar 

  • MacDonald P (2012) Supportive care. Emergencies in Pediatric Oncology. Springer, In, pp 121–141

    Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  Google Scholar 

  • Murakami M, Yamaguchi T, Takamura H, Atoba TM (2004) Effects of thermal treatment on radical-scavenging activity of single and mixed polyphenolic compounds. J Food Sci 69:FCT7–FCT10

    Article  CAS  Google Scholar 

  • Nagy M, Krizkova L, Mucaji P et al (2009) Antimutagenic activity and radical scavenging activity of water infusions and phenolics from ligustrum plants leaves. Molecules 14:509–518. https://doi.org/10.3390/molecules14010509

    Article  CAS  Google Scholar 

  • Naqshbandi A, Khan MW, Rizwan S, Rehman SU, Khan F (2012) Studies on the protective effect of dietary fish oil on cisplatin induced nephrotoxicity in rats. Food Chem Toxicol 50:265–273. https://doi.org/10.1016/j.fct.2011.10.039

    Article  CAS  Google Scholar 

  • Nho JH, Jung HK, Lee MJ, Jang JH, Sim MO, Jeong DE, Cho HW, Kim JC (2018) Beneficial effects of cynaroside on cisplatin-induced kidney injury in vitro and in vivo. Toxicol Res 34:133–141. https://doi.org/10.5487/TR.2018.34.2.133

    Article  CAS  Google Scholar 

  • Orhan F, Çeker S, Anar M et al (2016) Protective effects of three luteolin derivatives on aflatoxin B1-induced genotoxicity on human blood cells. Med Chem Res 25:2567–2577

    Article  CAS  Google Scholar 

  • Pan H, Shen K, Wang X, Meng H, Wang C, Jin B (2014) Protective effect of metalloporphyrins against cisplatin-induced kidney injury in mice. PLoS One 9:e86057. https://doi.org/10.1371/journal.pone.0086057

    Article  CAS  Google Scholar 

  • Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Med Cell Longev 2:270–278. https://doi.org/10.4161/oxim.2.5.9498

    Article  Google Scholar 

  • Pereira JA, Pereira AP, Ferreira IC, Valentão P, Andrade PB, Seabra R, Estevinho L, Bento A (2006) Table olives from Portugal: phenolic compounds, antioxidant potential, and antimicrobial activity. J Agric Food Chem 54:8425–8431. https://doi.org/10.1021/jf061769j

    Article  CAS  Google Scholar 

  • Perry JJP, Shin DS, Getzoff ED, Tainer JA (2010) The structural biochemistry of the superoxide dismutases. Biochim Biophys Acta (BBA)-Proteins Proteomics 1804:245–262

    Article  CAS  Google Scholar 

  • Perše M, Večerić-Haler Ž (2018) Cisplatin-induced rodent model of kidney injury: characteristics and challenges. Biomed Res. Int.

  • Qiusheng Z, Xiling S, Gang L et al (2004) Protective effects of luteolin-7-glucoside against liver injury caused by carbon tetrachloride in rats. Die Pharm Int J Pharm Sci 59:286–288

    Google Scholar 

  • Rajakrishnan R, Lekshmi R, Benil PB, Thomas J, AlFarhan A, Rakesh V, Khalaf S (2017) Phytochemical evaluation of roots of Plumbago zeylanica L. and assessment of its potential as a nephroprotective agent. Saudi J Biol Sci 24:760–766. https://doi.org/10.1016/j.sjbs.2017.01.001

    Article  CAS  Google Scholar 

  • Sabuncuoglu S, Eken A, Aydin A et al (2015) Cofactor metals and antioxidant enzymes in cisplatin-treated rats: effect of antioxidant intervention. Drug Chem Toxicol 38:375–382

    Article  CAS  Google Scholar 

  • Serpeloni JM, Grotto D, Mercadante AZ, de Lourdes Pires Bianchi M, Antunes LM (2010) Lutein improves antioxidant defense in vivo and protects against DNA damage and chromosome instability induced by cisplatin. Arch Toxicol 84:811–822. https://doi.org/10.1007/s00204-010-0576-y

    Article  CAS  Google Scholar 

  • Serpeloni JM, Grotto D, Aissa AF, Mercadante AZ, Bianchi Mde L, Antunes LM (2011) An evaluation, using the comet assay and the micronucleus test, of the antigenotoxic effects of chlorophyll b in mice. Mutat Res 725:50–56. https://doi.org/10.1016/j.mrgentox.2011.06.009

    Article  CAS  Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  CAS  Google Scholar 

  • Soliman AM, Desouky S, Marzouk M, Sayed AA (2016) Origanum majorana attenuates nephrotoxicity of cisplatin anticancer drug through ameliorating oxidative stress. Nutrients 8. https://doi.org/10.3390/nu8050264

  • Song Z, Chang H, Han N et al (2017) He-Wei granules (HWKL) combat cisplatin-induced nephrotoxicity and myelosuppression in rats by inhibiting oxidative stress, inflammatory cytokines and apoptosis. RSC Adv 7:19794–19807

    Article  CAS  Google Scholar 

  • Vallverdu-Queralt A, Regueiro J, de Alvarenga JF et al (2015) Carotenoid profile of tomato sauces: effect of cooking time and content of extra virgin olive oil. Int J Mol Sci 16:9588–9599. https://doi.org/10.3390/ijms16059588

    Article  CAS  Google Scholar 

  • Waly MI, Ali BH, Al-Lawati I, Nemmar A (2013) Protective effects of emodin against cisplatin-induced oxidative stress in cultured human kidney (HEK 293) cells. J Appl Toxicol 33:626–630. https://doi.org/10.1002/jat.1788

    Article  CAS  Google Scholar 

  • Wang Y, Lv J, Ma X et al (2010) Specific hemosiderin deposition in spleen induced by a low dose of cisplatin: altered iron metabolism and its implication as an acute hemosiderin formation model. Curr Drug Metab 11:507–515

    Article  CAS  Google Scholar 

  • Weijl NI, Elsendoorn TJ, Lentjes EG, Hopman GD, Wipkink-Bakker A, Zwinderman AH, Cleton FJ, Osanto S (2004) Supplementation with antioxidant micronutrients and chemotherapy-induced toxicity in cancer patients treated with cisplatin-based chemotherapy: a randomised, double-blind, placebo-controlled study. Eur J Cancer 40:1713–1723. https://doi.org/10.1016/j.ejca.2004.02.029

    Article  CAS  Google Scholar 

  • Yu J, Ahmedna M, Goktepe I (2005) Effects of processing methods and extraction solvents on concentration and antioxidant activity of peanut skin phenolics. Food Chem. https://doi.org/10.1016/j.foodchem.2004.03.04

  • Yuan Y, Wang H, Wu Y, Zhang B, Wang N, Mao H, Xing C (2015) P53 contributes to cisplatin induced renal oxidative damage via regulating P66shc and MnSOD. Cell Physiol Biochem 37:1240–1256. https://doi.org/10.1159/000430247

    Article  CAS  Google Scholar 

  • Žemlička L, Fodran P, Lukeš V et al (2014) Physicochemical and biological properties of luteolin-7-O-β-d-glucoside (cynaroside) isolated from Anthriscus sylvestris (L.) Hoffm. Monatshefte für Chemie-Chemical Mon 145:1307–1318

    Article  Google Scholar 

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The authors would like to thank the “Ministère Tunisien de l’enseignement supérieur et de la recherche scientifique” for financial support of this study.

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Correspondence to Mouna Maatouk.

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Maatouk, M., Abed, B., Bouhlel, I. et al. Heat treatment and protective potentials of luteolin-7-O-glucoside against cisplatin genotoxic and cytotoxic effects. Environ Sci Pollut Res 27, 13417–13427 (2020). https://doi.org/10.1007/s11356-020-07900-7

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