Toxicological aspect of bioinsecticide pyrethrum extract and expressions of apoptotic gene levels in human hepotacellular carcinoma HepG2 cells

References

• Aşık E, Akpınar Y, Güray NT, İşcan M, Demircigil GÇ, Volkan M. 2016. Cellular uptake, genotoxicity and cytotoxicity of cobalt ferrite magnetic nanoparticles in human breast cells. Toxicol Res. 5(6):1649–1662.
   Web of Science ®Google Scholar
• Benvindo-Souza M, Oliveira EAS, Assis RA, Santos CGA, Borges RE, Silva D de M, Santos LR, de S. 2020. Micronucleus test in tadpole erythrocytes: Trends in studies and new paths. Chemosphere. 240:124910.
   PubMed Web of Science ®Google Scholar
• Birge RB, Boeltz S, Kumar S, Carlson J, Wanderley J, Calianese D, Barcinski M, Brekken RA, Huang X, Hutchins JT, et al. 2016. Phosphatidylserine is a global immunosuppressive signal in efferocytosis, infectious disease, and cancer. Cell Death Differ. 23(6):962–978.
   PubMed Web of Science ®Google Scholar
• Brunelle JK, Letai A. 2009. Control of mitochondrial apoptosis by the Bcl-2 family. J Cell Sci. 122(Pt 4):437–441.
   PubMed Web of Science ®Google Scholar
• Campos VRE, Oliveira de JL, Pascoli M, Lima de R, Fraceto LF. 2016. Neem oil and crop protection: from now to the future. Front Plant Sci. 7:1494.
   PubMed Web of Science ®Google Scholar
• Casida JE, Quistad GB. 1995. Pyrethrum flowers: production, chemistry, toxicology and uses. New York: Oxford University Press, p. 356.
   Google Scholar
• Chen Q, Kang J, Fu C. 2018. The independence of and associations among apoptosis, autophagy, and necrosis. Signal Transduct Target Ther. 3:18.
   PubMed Web of Science ®Google Scholar
• Choo SP, Tan WL, Goh BKP, Tai WM, Zhu AX. 2016. Comparison of hepatocellular carcinoma in eastern versus western populations. Cancer. 122(22):3430–3446.
   PubMed Web of Science ®Google Scholar
• Cox C. 2002. Pyrethrins/pyrethrum insecticide factsheet. J. Pestic. Reform. 2 (1):14–20.
   Google Scholar
• Degterev A, Boyce M, Yuan J. 2003. A decade of caspases. Oncogene. 22(53):8543–8567.
   PubMed Web of Science ®Google Scholar
• Eastmond DA, Tucker JD. 1989. Identification of aneuploidy-inducing agents using cytokinesis-blocked human lymphocytes and antikinetochore antibody. Environ Mol Mutagen. 13(1):34–43.
   PubMed Web of Science ®Google Scholar
• EC 2008. Commission Regulation (EC) No. 889/2008 of 5 September 2008 laying down detailed rules for the implementation of Council Regulation (EC) No. 834/2007 on organic production and labelling of organic products with regard to organic production, labelling and control. Offic. J. Eur. Union OJ L. 250:1–84.
   Google Scholar
• Elmore S. 2007. Apoptosis: A Review of Programmed Cell Death. Toxicol Pathol. 35(4):495–516.
   PubMed Web of Science ®Google Scholar
• Environmental Protection Agency (EPA) 2018. Pyrethrins and Pyrethroids Reregistration and Labeling. EPA-HQ-OPP-2008-0331-0085, 12 Feb 2020.
   Google Scholar
• Fenech M. 2000. The in vitro micronucleus technique. Mutat Res. 455 (1–2):81–95.
   PubMed Web of Science ®Google Scholar
• Fenech M, Knasmueller S, Bolognesi C, Bonassi S, Holland N, Migliore L, Palitti F, Natarajan AT, Kirsch-Volders M. 2016. Molecular mechanisms by which in vivo exposure to exogenous chemical genotoxic agents can lead to micronucleus formation in lymphocytes in vivo and ex vivo in humans. Mutat Res Rev Mutat Res. 770(Pt A):12–25.
   PubMed Web of Science ®Google Scholar
• Fridman JS, Lowe SW. 2003. Control of apoptosis by p53. Oncogene. 22(56):9030–9040.
   PubMed Web of Science ®Google Scholar
• Fulda S, Debatin K-M. 2006. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene. 25(34):4798–4811.
   PubMed Web of Science ®Google Scholar
• Giam M, Huang DC, Bouillet P. 2008. BH3-only proteins and their roles in programmed cell death. Oncogene. 27(S1):S128–S136.
   PubMedGoogle Scholar
• Göktürk T. 2017. Pyrethrum ve Bacillus thuringiensis biyopestisitlerinin Pristiphora abietina (Christ, 1791) (Hymenoptera: Tenthredinidae) üzerindeki etkisi. [The effect of Pyrethrum and Bacillus thuringiensis against Pristiphora abietina (Christ, 1791) (Hymenoptera: Tenthredinidae). Artvin Çoruh Üni., Orman Fakültesi Dergisi. 18(1):83–87.
   Google Scholar
• Gokturk T, Mihli A. 2016. The effect of Pyrethrum and Bacillus thuringiensis against Ricania simulans (Walker, 1851) (Hemiptera: ricanidae) in Turkey. Ann Agrar Sci. 14(4):311–314.
   Google Scholar
• Guncan A, Durmusoglu E. 2004. Bitkisel Kökenli Doğal İnsektisitler Üzerine Bir Değerlendirme. HASAD. 233:26–32.
   Google Scholar
• Gupta S, Dikshit AK. 2010. Biopesticides: an ecofriendly approach for pest control. J. Biopestic. 3:186.
   Google Scholar
• Han YH, Kim SH, Kim SZ, Park WH. 2008. Antimycin A as a mitochondrial electron transport inhibitor prevents the growth of human lung cancer A549 cells. Oncol Rep. 20(3):689–693.
   PubMed Web of Science ®Google Scholar
• Hreljac I, Zajc I, Lah T, Filipic M. 2008. Effects of model organophosphorous pesticides on DNA damage and proliferation of HepG2 cells. Environ Mol Mutagen. 49(5):360–367.
   PubMed Web of Science ®Google Scholar
• Igney FH, Krammer PH. 2002. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2(4):277–288.
   PubMed Web of Science ®Google Scholar
• Isman MB. 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol. 51(1):45–66.
   PubMed Web of Science ®Google Scholar
• Kale J, Osterlund EJ, Andrews DW. 2018. BCL-2 family proteins: changing partners in the dance towards death. Cell Death Differ. 25(1):65–80.
   PubMed Web of Science ®Google Scholar
• Kaya-Aksoy E, Cingoz A, Senbabaoglu F, Seker F, Sur-Erdem I, Kayabolen A, Lokumcu T, Sahin GN, Karahuseyinoglu S, Bagci-Onder T. 2019. The pro-apoptotic Bcl-2 family member Harakiri (HRK) induces cell death in glioblastoma multiforme. Cell Death Dis. 5:64.
   Web of Science ®Google Scholar
• Kayhan H, Esmekaya MA, Yar-Saglam AS, Tuysuz MZ, Canseven AG, Yagci AM, Seyhan N. 2016. Does MW radiation affect gene expression, apoptotic level, and cell cycle progression of human SH-SY5Y neuroblastoma cells? Cell Biochem Biophys. 74(2):99–107.
   PubMed Web of Science ®Google Scholar
• Kim K-H, Kabir E, Jahan SA. 2017. Exposure to pesticides and the associated human health effects. Sci Total Environ. 575:525–535.
   PubMed Web of Science ®Google Scholar
• Kirsch-Volders M, Bonassi S, Knasmueller S, Holland N, Bolognesi C, Fenech MF. 2014. Commentary: critical questions, misconceptions and a road map for improving the use of the lymphocyte cytokinesis-block micronucleus assay for in vivo biomonitoring of human exposure to genotoxic chemicals-A HUMN project perspective. Mutat Res Rev Mutat Res. 759:49–58.
   PubMed Web of Science ®Google Scholar
• Knasmüller S, Mersch-Sundermann V, Kevekordes S, Darroudi F, Huber WW, Hoelzl C, Bichler J, Majer BJ. 2004. Use of human-derived liver cell lines for the detection of environmental and dietary genotoxicants; current state of knowledge. Toxicology. 198(1–3):315–328.
   PubMed Web of Science ®Google Scholar
• Knasmüller S, Parzefall W, Sanyal R, Ecker S, Schwab C, Uhl M, Mersch-Sundermann V, Williamson G, Hietsch G, Langer T, et al. 1998. Use of metabolically competent human hepatoma cells for the detection of mutagens and antimutagens. Mutat Res. 402(1–2):185–202.
   PubMed Web of Science ®Google Scholar
• Lavrik I, Golks A, Krammer PH. 2005. Death receptor signaling. J Cell Sci. 118(Pt 2):265–267.
   PubMed Web of Science ®Google Scholar
• Livak JK, Schmittgen DT. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 25(4):402–408.
   PubMed Web of Science ®Google Scholar
• Lu C, Liu X, Dong F, Xu J, Song W, Zhang C, Li Y, Zheng Y. 2010. Simultaneous determination of pyrethrins residues in teas by ultra-performance liquid chromatography/tandem mass spectrometry. Anal Chim Acta. 678(1):56–62.
   PubMed Web of Science ®Google Scholar
• Mamur S, Yuzbasioglu D, Yılmaz S, Erikel E, Ünal F. 2018. Assessment of cytotoxic and genotoxic effects of Enniatin-A in vitro. Food Addit. Contam. Part A. 35(8):1633–1644.
   PubMed Web of Science ®Google Scholar
• Marani M, Tenev T, Hancock D, Downward J, Lemoine NR. 2002. Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol Cell Biol. 22(11):3577–3589.
   PubMed Web of Science ®Google Scholar
• Mohammed FA, Elkady AI, Sye FQ, Mirza MB, Hakeem KR, Alkarim S. 2018. Anethum graveolens (dill) – a medicinal herb induces apoptosis and cell cycle arrest in HepG2 cell line. J Ethnopharmacol. 219:15–22.
   PubMed Web of Science ®Google Scholar
• Mosesso P, Bohm L, Pepe G, Fiore M, Carpinelli A, Gäde G, Nagini S, Ottavianelli A, Degrassi F. 2012. Cytogenetic analyses of Azadirachtin reveal absence of genotoxicity but marked antiproliferative effects in human lymphocytes and CHO cells in vitro. Toxicol Lett. 213(3):361–366.
   PubMed Web of Science ®Google Scholar
• Mossman T. 1983. Rapid colometric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65:55–63.
   PubMed Web of Science ®Google Scholar
• Nazir T, Khan S, Qiu D. 2019. Chapter: biological control of insect pest. In: Haouas D, Hufnagel L, editors. Pest Control and Acarology. IntechOpen; p. 1–14.
   Google Scholar
• Obeng E. 2021. Apoptosis (programmed cell death) and its signals – a review Brazilian Journal of Biology. Braz J Biol. 81(4):1133–1143.
   PubMedGoogle Scholar
• OECD (Organisation for Economic Co-operation and Development) 2016. OECD guideline for the testing of chemicals: In vitro mammalian cell micronucleus test, OECD/OCDE TG 487, 29 July 2016.
   Google Scholar
• Oliveira CR, Garcia TD, Franco-Belussi L, Salla RF, Souza BFS, Melo de NFS, Irazusta SP, Jones-Costa M, Silva-Zacarin ECM, Fraceto LF. 2019. Pyrethrum extract encapsulated in nanoparticles: toxicity studies based on genotoxic and hematological effects in bullfrog tadpoles. Environ Pollut. 253:1009–1020.
   PubMed Web of Science ®Google Scholar
• Pascua-Maestro R, Corraliza-Gomez M, Diez-Hermano S, Perez-Segurado C, Ganfornina MD, Sanchez D. 2018. The MTT-formazan assay: complementary technical approaches and in vivo validation in Drosophila larvae. Acta Histochem. 120(3):179–186. Epub 2018 Feb 1.
   PubMed Web of Science ®Google Scholar
• Pfeil R. 2003. Pesticide residues in food – 2003 – Joint FAO/WHO Meeting on Pesticide Residues (JMPR), PYRETHRINS (addendum), IPCS Inchem Home, (http://192.82.104.231/documents/jmpr/jmpmono/v2003pr11.htm#tox). p. 187–188.
   Google Scholar
• Price RJ, Walters DG, Finch JM, Gabriel KL, Capen CC, Osimitz TG, Lake BG. 2007. A mode of action for induction of liver tumors by Pyrethrins in the rat. Toxicol Appl Pharmacol. 218(2):186–195.
   PubMed Web of Science ®Google Scholar
• Rodríguez-López MI, Mercader-Ros MT, Pellicer JA, Gómez-López VM, Martínez-Romero D, Núñez-Delicado E, Gabaldón JA. 2020. Evaluation of monoterpene-cyclodextrin complexes as bacterial growth effective hurdles. Food Control. 108:106814.
   Web of Science ®Google Scholar
• Romero A, Ares I, Ramos E, Castellano V, Martínez M, Martínez-Larranaga MR, Anadon A, Martínez MA. 2015. Evidence for dose-additive effects of a type II pyrethroid mixture. In vitro assessment. Environ Res. 138:58–66.
   PubMed Web of Science ®Google Scholar
• Schleier JJ, Peterson RKD. 2011. Pyrethrins and pyrethroid insecticides. In: Lopez O, Fernandez-Bolanos Green J. (Eds.), Trends in insect control. Publishing, vol. 3. London: Burlington House, p. 94–131.
   Google Scholar
• Smith ML, Chen IT, Zhan Q, Bae I, Chen CY, Gilmer TM, Kastan MB, O'Connor PM, Fornace AJ. Jr. 1994. Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science. 266(5189):1376–1380.
   PubMed Web of Science ®Google Scholar
• Son Y, An Y, Jung J, Shin S, Park I, Gwak J, Ju BG, Chung Y, Na M, Oh S. 2019. Protopine isolated from Nandina domestica induces apoptosis and autophagy in colon cancer cells by stabilizing p53. Phytother Res. 33(6):1689–1696.
   PubMed Web of Science ®Google Scholar
• Srivastava P, Yadav N, Lella R, Schneider A, Jones A, Marlowe T, Lovett G, O'Loughlin K, Minderman H, Gogada R, et al. 2012. Neem oil limonoids induces p53-independent apoptosis and autophagy. Carcinogenesis. 33(11):2199–2207.
   PubMed Web of Science ®Google Scholar
• Stern A, Rotter A, Novak M, Filipic M, Zegura B. 2019. Genotoxic effects of the cyanobacterial pentapeptide nodularin in HepG2 Cells. Food Chem Toxicol. 124:349–358.
   PubMed Web of Science ®Google Scholar
• Sumit JS, Paul WS. 2005. Tocotrienol-induced cytotoxicity is unrelated to mitochondrial stress apoptotic signaling in neoplastic mammary epithelial cells. Biochem. Cell Biol. 2007 (83):86–95.
   Google Scholar
• U.S. Environmental Protection Agency – USEPA 2006. Registration eligibility decision for pyrethrins. Disponível em: http://www.epa.gov/oppsrrd1/REDs/pyrethrins_red.pdf., 122016.
   Google Scholar
• Uhl M, Helma C, Knasmüller S. 2000. Evaluation of the single cell gel electrophoresis assay with human hepatoma (HepG2) cells. Mutat. Res. 468 (2):213–225.
   PubMed Web of Science ®Google Scholar
• Usta J, Kreydiyyeh S, Knio K, Barnabe P, Bou-Moughlabay Y, Dagher S. 2009. Linalool decreases HepG2 viability by inhibiting mitochondrial complexes I and II, increasing reactive oxygen species and decreasing ATP and GSH levels. Chem Biol Interact. 180(1):39–46.
   PubMed Web of Science ®Google Scholar
• Van Maele-Fabry G, Lantin AC, Hoet P, Lison D. 2010. Childhood leukaemia and parental occupational exposure to pesticides: a systematic review and meta-analysis. Cancer Causes Control. 21 (6):787–809.
   PubMed Web of Science ®Google Scholar
• Wajant H. 2002. The Fas signaling pathway: more than a paradigm. Science. 296 (5573):1635–1636.
   PubMed Web of Science ®Google Scholar
• Wang J, Xue T, Ye H, Sang C, Wu S, Li S. 2021. Study of the common activating mechanism of apoptosis and epithelial-to-mesenchymal transition in alveolar type II epithelial cells. Respir Physiol Neurobiol. 284:103584.
   PubMed Web of Science ®Google Scholar
• Wang S, El-Deiry WS. 2003. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene. 22(53):8628–8633.
   PubMed Web of Science ®Google Scholar
• Wang Y, Tjandra N. 2013. Structural insights of tBid, the caspase-8-activated Bid, and Its BH3 domain. J Biol Chem. 288(50):35840–35851.
   PubMed Web of Science ®Google Scholar
• Weinzierl R, Henn T. 1991. Alternatives in insect management biological and biorational approaches. North Central Regional Extensions Publication. 401:73.
   Google Scholar
• Wlodkowic D, Skommer J, Darzynkiewicz Z. 2012. Cytometry of apoptosis. Historical perspective and new advances. Exp Oncol. 34(3):255–262.
   PubMedGoogle Scholar
• Xie Q, Liu Y, Li X. 2020. The interaction mechanism between autophagy and apoptosis in colon cancer. Transl Oncol. 13(12):100871.
   PubMed Web of Science ®Google Scholar
• Xu Z, Lu M, Yang M, Xu W, Gao J, Zhang Y, Yang Y, Tao L. 2017. Pyrethrum-extract induced autophagy in insect cells: a new target? Pestic. Biochem. Phys. 137:21–26.
   Google Scholar
• Yang Y, Gao J, Zhang Y, Xu W, Hao Y, Xu Z, Tao L. 2018. Natural pyrethrins induce autophagy of HepG2 cells through the activation of AMPK/mTOR pathway. Environ Pollut. 241:1091–1097.
   PubMed Web of Science ®Google Scholar
• Yang Y, Zong M, Xu W, Zhang Y, Wang B, Yang M, Tao L. 2017. Natural pyrethrins induces apoptosis in human hepatocyte cells via Bax- and Bcl-2-mediated mitochondrial pathway. Chem Biol Interact. 262:38–45.
   PubMed Web of Science ®Google Scholar
• Zeljezic D, Mladinic M, Zunec S, Vrdoljak AL, Kasuba V, Tariba B, Zivkovic T, Marjanovic AM, Pavicic I, Milic M, et al. 2016. Cytotoxic, genotoxic and biochemical markers of insecticide toxicity evaluated in human peripheral blood lymphocytes and an HepG2 cell line. Food Chem. Toxicol. 96:90–106.
   PubMed Web of Science ®Google Scholar