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Research Articles

Genotoxicity mechanism of food preservative propionic acid in the in vivo Drosophila model: gut damage, oxidative stress, cellular immune response and DNA damage

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Pages 327-336 | Received 27 Jun 2022, Accepted 07 Oct 2022, Published online: 24 Oct 2022

References

  • Alaraby M, Demir E, Domenech J, Velazquez A, Hernandez A, Marcos R. 2020. In vivo evaluation of the toxic and genotoxic effects of exposure to cobalt nanoparticles in Drosophila melanogaster. Environ Sci. 7(2):610–622.
  • Al-Lahham S, Rezaee F. 2019. Propionic acid counteracts the inflammation of human subcutaneous adipose tissue: a new avenue for drug development. Daru. 27(2):645–652.
  • Al-Lahham S, Roelofsen H, Rezaee F, Weening D, Hoek A, Vonk R, Venema K. 2012. Propionic acid affects immune status and metabolism in adipose tissue from overweight subjects. Eur J Clin Invest. 42(4):357–364.
  • Al-Lahham SH, Peppelenbosch MP, Roelofsen H, Vonk RJ, Venema K. 2010. Biological effects of propionic acid in humans; metabolism, potential applications and underlying mechanisms. Biochim Biophys Acta. 1801(11):1175–1183.
  • Banerjee U, Girard JR, Goins LM, Spratford CM. 2019. Drosophila as a genetic model for hematopoiesis. Genetics. 211(2):367–417.
  • Bilen J, Bonini NM. 2005. Drosophila as a model for human neurodegenerative disease. Annu Rev Genet. 39:153–171.
  • Bier E. 2005. Drosophila, the golden bug, emerges as a tool for human genetics. Nat Rev Genet. 6(1):9–23.
  • Bolognini D, Tobin AB, Milligan G, Moss C. 2016. The pharmacology and function of short chain fatty acid receptors. Mol Pharmacol. 89(3):388–398.
  • Carrau T, Thümecke S, Silva LMR, Perez-Bravo D, Gärtner U, Taubert A, Hermosilla C, Vilcinskas A, Lee KZ. 2021. The cellular innate immune response of the invasive pest insect Drosophila suzukii against Pseudomonas entomophila involves the release of extracellular traps. Cells. 10(12):3320.
  • Demir E. 2022. Mechanisms and biological impacts of graphene and multi-walled carbon nanotubes on Drosophila melanogaster: oxidative stress, genotoxic damage, phenotypic variations, locomotor behavior, parasitoid resistance, and cellular immune response. J Appl Toxicol. 42(3):450–474.
  • Demir E, Kaya B. 2013. Studies on the genotoxic properties of four benzyl derivatives in the in vivo comet assay using haemocytes of Drosophila melanogaster. Fresenius Environ Bull. 22:1590–1596.
  • Demir E, Marcos R. 2017. Assessing the genotoxic effects of two lipid peroxidation products (4-oxo-2-nonenal and 4-hydroxy-hexenal) in haemocytes and midgut cells of Drosophila melanogaster larvae. Food Chem Toxicol. 105:1–7.
  • Demir E, Marcos R. 2018. Antigenotoxic potential of boron nitride nanotubes. Nanotoxicology. 12(8):868–884.
  • Demir E, Marcos R, Kaya B. 2012. Genotoxicity studies in the ST cross of the Drosophila wing spot test of sunflower and soybean oils before and after frying and boiling procedures. Food Chem Toxicol. 50(10):3619–3624.
  • Demir E, Kocaoğlu S, Kaya B. 2008. Genotoxicity testing of four benzyl derivatives in the Drosophila wing spot test. Food Chem Toxicol. 46(3):1034–1041.
  • Demir E, Turna F, Aksakal S, Kaya B, Marcos R. 2014. Genotoxicity of different sweeteners in Drosophila. Fresenius Environ Bull. 23:3426–3432.
  • Demir E, Turna F, Kaya B, Creus A, Marcos R. 2013. Mutagenic/recombinogenic effects of four lipid peroxidation products in Drosophila. Food Chem Toxicol. 53:221–227.
  • Demir E, Turna Demir F. 2022. Drosophila melanogaster as a dynamic in vivo model organism reveals the hidden effects of interactions between microplastic/nanoplastic and heavy metals. J Appl Toxicol. 2022:4353.
  • Demir ET, Demir F, Marcos R. 2022. Drosophila as a suitable in vivo model in the safety assessment of nanomaterials. Adv Exp Med Biol. 1357:275–301.
  • Depetris-Chauvin A, Galagovsky D, Chevalier C, Maniere G, Grosjean Y. 2017. Olfactory detection of a bacterial short-chain fatty acid acts as an orexigenic signal in Drosophila melanogaster larvae. Sci Rep. 7(1):14230.
  • Dudzic JP, Kondo S, Ueda R, Bergman CM, Lemaitre B. 2015. Drosophila innate immunity: regional and functional specialization of prophenoloxidases. BMC Biol. 13:81.
  • El-Ansary A, Abu-Shmais G, Al-Dbass A. 2013. Neuroprotective effect of creatine against propionic acid toxicity in neuroblastoma SH-SY5Y cells in culture. Afr Biotechnol. 12:4925–4935.
  • El-Ansary AK, Bacha AB, Kotb M. 2012. Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J Neuroinflammation. 9:74.
  • Environment and Climate Change Canada and Health Canada, 2021. 2019. Screening assessment carboxylic acids group. https://www.canada.ca/en/environment-climate change/services/evaluating-existing-substances/screening-assessment-carboxylic-acids group.html.
  • EFSA (European Food Safety Authority). 2014. Scientific opinion on the re-evaluation of propionic acid (E 280), sodium propionate (E 281), calcium propionate (E 282) and potassium propionate (E 283) as food additives. Efsa J. 12:3779.
  • Flecknell P. 2002. Replacement, reduction and refinement. Altex. 19:73–78.
  • FDA (Food and Drug Administration). 2017. Sec. 184.1081 propionic acid. Title 21, Volume 3, Chapter 1, Part 184. 2017. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=184.1081.
  • Frye RE, Rose S, Chacko J, Wynne R, Bennuri SC, Slattery JC, Tippett M, Delhey L, Melnyk S, Kahler SG, et al. 2016. Modulation of mitochondrial function by the microbiome metabolite propionic acid in autism and control cell lines. Transl Psychiatry. 6(10):e927.
  • Gallego-Villar L, Perez-Cerda C, Perez B, Abia D, Ugarte M, Richard E, Desviat LR. 2013. Functional characterization of novel genotypes and cellular oxidative stress studies in propionic acidemia. J Inherit Metab Dis. 36(5):731–740.
  • Ghosh M, Manivannan J, Sinha S, Chakraborty A, Mallick SK, Bandyopadhyay M, Mukherjee A. 2012. In vitro and in vivo genotoxicity of silver nanoparticles. Mutat Res. 749(1–2):60–69.
  • Gold KS, Brückner K. 2015. Macrophages and cellular immunity in Drosophila melanogaster. Semin Immunol. 27(6):357–368.
  • Gonzalez C. 2013. Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics. Nat Rev Cancer. 13(3):172–183.
  • Hartung T, Sabbioni E. 2011. Alternative in vitro assays in nanomaterial toxicology. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 3(6):545–573.
  • Irving P, Ubeda JM, Doucet D, Troxler L, Lagueux M, Zachary D, Hoffmann JA, Hetru C, Meister M. 2005. New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell Microbiol. 7(3):335–350.
  • Jalvingh KM, Chang PL, Nuzhdin SV, Wertheim B. 2014. Genomic changes under rapid evolution: selection for parasitoid resistance. Proc R Soc B. 281:2013–2303.
  • JECFA (Joint FAO/WHO Expert Committee on Food Additives). 2006. Combined compendium of food additive specifications. Monograph 1. [accessed] http://www.fao.org/food/food-safetyquality/scientific-advice/jecfa/jecfa-additives/en/.
  • Jennings BH. 2011. Drosophila-a versatile model in biology & medicine. Mater Today. 14(5):190–195.
  • Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I. 2015. Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients. 7(4):2839–2849.
  • Końca K, Lankoff A, Banasik A, Lisowska H, Kuszewski T, Góźdź S, Koza Z, Wojcik A. 2003. A cross-platform public domain PC image-analysis program for the comet assay. Mutat Res. 534(1–2):15–20.
  • Kraaijeveld AR, Hutcheson KA, Limentani EC, Godfray HCJ. 2001. Costs of counterdefenses to host resistance in a parasitoid of drosophila. Evolution. 55(9):1815–1821.2.0.CO;2]
  • Latouche M, Lasbleiz C, Martin E, Monnier V, Debeir T, Mouatt-Prigent A, Muriel MP, Morel L, Ruberg M, Brice A, et al. 2007. A conditional pan neuronal Drosophila model of spinocerebellar ataxia 7 with a reversible adult phenotype suitable for ıdentifying modifier Genes. J Neurosci. 27(10):2483–2492.
  • Leitão AB, Bian X, Day JP, Pitton S, Demir E, Jiggins FM. 2019. Independent effects on cellular and humoral immune responses underlie genotype-by-genotype interactions between drosophila and parasitoids. PLoS Pathog. 15(10):e1008084.
  • Leitão AB, Sucena E. 2015. Drosophila sessile hemocyte clusters are true hematopoietic tissues that regulate larval blood cell differentiation. eLife. 4:e06166.
  • Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annu Rev Immunol. 25(1):697–743.
  • Letourneau M, Lapraz F, Sharma A, Vanz N, Waltzer L, Crozatier M. 2016. Drosophila hematopoiesis under normal conditions and in response to immune stress. FEBS Lett. 590(22):4034–4051.
  • Lind H, Jonsson H, Schnurer J. 2005. Antifungal effect of dairy propionibacteria–contribution of organic acids. Int J Food Microbiol. 98(2):157–165.
  • Maier E, Kurz K, Jenny M, Schennach H, Ueberall F, Fuchs D. 2010. Food preservatives sodium benzoate and propionic acid and colorant curcumin suppress Th1-type immune response in vitro. Food Chem Toxicol. 48(7):1950–1956.
  • Meister M, Lagueux M. 2003. Drosophila blood cells. Cell Microbiol. 5(9):573–580.
  • Micalizzi EW, Golshani A, Smith ML. 2021. Propionic acid disrupts endocytosis, cell cycle, and cellular respiration in yeast. BMC Res Notes. 14(1):335.
  • Micalizzi EW, Mack JN, White GP, Avis TJ, Smith ML. 2017. Microbial inhibitors of the fungus Pseudogymnoascus destructans, the causal agent of whitenose syndrome in bats. PLoS One. 12(6):e0179770.
  • Micalizzi EW, Smith ML. 2020. Volatile organic compounds kill the white-nose syndrome fungus, Pseudogymnoascus destructans, in hibernaculum sediment. Can J Microbiol. 66:1–7.
  • Moloney A, Sattelle DB, Lomas DA, Crowther DC. 2010. Alzheimer’s disease: insights from Drosophila melanogaster models. Trends Biochem Sci. 35(4):228–235.
  • Mukhopadhyay I, Chowdhuri DK, Bajpayee M, Dhawan A. 2004. Evaluation of in vivo genotoxicity of cypermethrin in Drosophila melanogaster using the alkaline comet assay. Mutagenesis. 19(2):85–90.
  • Nankova BB, Agarwal R, MacFabe DF, La Gamma EF. 2014. Enteric bacterial metabolites propionic and butyric acid modulate gene expression, including CREB-dependent catecholaminergic neurotransmission, in PC12 cells–possible relevance to autism spectrum disorders. PLoS One. 9(8):e103740.
  • Ormsby MJ, Johnson SA, Carpena N, Meikle LM, Goldstone RJ, McIntosh A, Wessel HM, Hulme HE, McConnachie CC, Connolly JPR, et al. 2020. Propionic acid promotes the virulent phenotype of crohn’s disease-associated adherent-invasive Escherichia coli. Cell Rep. 30(7):2297–2305.e5.
  • Pappus SA, Ekka B, Sahu S, Sabat D, Dash P, Mishra M. 2017. A toxicity assessment of hydroxyapatite nanoparticles on development and behaviour of Drosophila melanogaster. J Nanoparticle Res. 19:136.
  • Pham CH, Lee JE, Yu J, Lee SH, Yu KR, Hong J, Cho N, Kim S, Kang D, Lee S, et al. 2021. Anticancer effects of propionic acid inducing cell death in cervical cancer cells. Molecules. 26(16):4951.
  • Quitmann H, Fan R, Czermak P. 2014. Acidic organic compounds in beverage, food, and feed production. Adv Biochem Eng Biotechnol. 143:91–141.
  • Rajak P, Dutta M, Roy S. 2015. Altered differential hemocyte count in 3rd instar larvae of Drosophila melanogaster as a response to chronic exposure of Acephate. Interdiscip Toxicol. 8(2):84–88.
  • 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(1):184–191.
  • Stinson AM, Zidack NK, Strobel GA, Jacobsen BJ. 2003. Mycofumigation with Muscodor albus and Muscodor roseus for control of seedling diseases of sugar beet and verticillium wilt of eggplant. Plant Dis. 87(11):1349–1354.
  • Strober W. 2001. Trypan blue exclusion test of cell viability. Current protocols in immunology 2001; Appendix 3: Appendix 3B. Hoboken (NJ): John Wiley & Sons.
  • Turna Demir F. 2022. In vivo effects of 1, 4-dioxane on genotoxic parameters and behavioral alterations in Drosophila melanogaster. J Toxicol Environ Health A. 85(10):414–430.
  • Turna Demir F, Yavuz M. 2020. Heavy metal accumulation and genotoxic effects in levant vole (Microtus guentheri) collected from contaminated areas due to mining activities. Environ Pollut. 256:113378.
  • Wajner M, Latini A, Wyse ATS, Dutra-Filho S. 2004. The role of oxidative damage in the neuropathology of organic acidurias: insights from animal studies. J Inherit Metab Dis. 27(4):427–448.
  • Wolf MJ, Amrein H, Izatt JA, Choma MA, Reedy MC, Rockman HA. 2006. From the Cover: Drosophila as a model for the identification of genes causing adult human heart disease. Proc Natl Acad Sci U S A. 103(5):1394–1399.
  • Yun J, Lee DG. 2016. A novel fungal killing mechanism of propionic acid. FEMS Yeast Res. 16(7):fow089.
  • Zhang Y, Wolosker MB, Zhao Y, Ren H, Lemos B. 2020. Exposure to microplastics cause gut damage, locomotor dysfunction, epigenetic silencing, and aggravate cadmium (Cd) toxicity in Drosophila. Sci Total Environ. 744:140979.

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