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Drosophila melanogaster as model organism for monitoring and analyzing genotoxicity associated with city air pollution

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Abstract

This study evaluated the genotoxic potential of atmospheric pollution associated with urbanization using the model organism Drosophila melanogaster and the Comet assay with hemolymph cells. Larvae were exposed to atmospheric compounds in an urban and a rural area in the municipality of Vitória de Santo Antão, Pernambuco, Brazil, for 6 days (from the embryo stage to the third larval stage) in April 2015 and April 2017. The results were compared to a negative environmental control group exposed to a preserved area (Catimbau National Park) and to a negative control exposed to the laboratory room conditions. The Comet assay demonstrated significant genetic damage in the organisms exposed to the urban area compared with those exposed to the rural area and negative control groups. The evidences were supported by particulate matter analysis showing higher photopeaks of chemical elements such as aluminum, silicon, sulfur, potassium, calcium, titanium, and iron, associated to road dust fraction in urban environment. Once again, the results confirm D. melanogaster an ideal bioindicator organism to monitor genotoxic hazard associated with atmospheric pollution.

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References

  • Alves CA, Evtyugina M, Vicente AMP, Vicente ED, Nunes TV, Silva PMA, Duarte MAC, Pio CA, Amato F, Querol X (2018) Chemical profiling of PM10 from urban road dust. Sci Total Environ 634:41–51

    Article  CAS  Google Scholar 

  • Bajpayee M, Dhawan A (2014) Biomarkers for monitoring adverse health effects of air pollution in humans. J Transl Toxicol 1:46–51

    Google Scholar 

  • Bier E, Mcginnis W (2016) Model organisms in the study of development and disease. In: Epstein's inborn errors of development. Third edition. Oxford University Press. pp. 25–45

  • Billet S, Landkocz Y, Martin PJ, Verdin A, Ledoux F, Lepers C, André V, Cazier F, Sichel F, Shirali P, Gosset P, Courcot D (2018) Chemical characterization of fine and ultrafine PM, direct and indirect genotoxicity of PM and their organic extracts on pulmonary cells. J Environ Sci 71:168–178

    Article  Google Scholar 

  • Bocchi C, Bazzini C, Fontana F, Pinto G, Martino A, Cassoni F (2016) Characterization of urban aerossol: seasonal variation of mutagenicity and genotoxicity of PM2.5, PM1 and semi-volatile organic compounds. Mutat Res 809:16–23

    Article  CAS  Google Scholar 

  • Carneseca EC, Achcar JA, Martinez EZ (2012) Association between particulate matter air pollution and monthly inhalation and nebulization procedures in Ribeirão Preto, São Paulo State, Brazil. Cad Saude Publica 28:1591–1598

    Article  Google Scholar 

  • Cohen AJ, Brauer M, Burnett M et al (2017) Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: an analysis of data from the Global Burden of Diseases Study 2015. Lancet 389:1907–1918

    Article  Google Scholar 

  • Collins A, Koppen G, Valdiglesias V, Dusinska M, Kruszewski M, Møller P, Rojas E, Dhawan A, Benzie I, Coskun E, Moretti M, Speit G, Bonassi S (2014) The comet assay as a tool for human biomonitoring studies: the ComNet project. Mutat Res Rev Mutat Res 759:27–39

    Article  CAS  Google Scholar 

  • Delgado-Rodríguez A, Ortíz-Marttelo R, Villalobos-Pietrini R, Gómez-Arroyo S, Graf U (1999) Genotoxicity of organic extracts of airborne particles in somatic cells of Drosophila melanogaster. Chemosphere 39:33–43

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • DETRAN-PE (Departamento Estadual de Trânsito de Pernambuco), (2018). Estatística da frota de veículos segundo os municípios - Pernambuco. http://www.detran.pe.gov.br/index.php?option=com_content&view=article&id=36&Itemid=72 (Accessed January 2018)

  • Dihl RR, Silva CGA, Amaral VS, Reguly ML, Andrade HHR (2008) Mutagenic and recombinogenic activity of airborne particulates, PM10 and TSP, organic extracts in the Drosophila wing-spot test. Environ Pollut 151:47–52

    Article  CAS  Google Scholar 

  • Domingues ÉP, Silva GG, Oliveira AB, Mota LM, Santos VSV, Campos EOJ, Pereira BB (2018) Genotoxic effects following exposure to air pollution in street vendors from a high-traffic urban area. Environ Monit Assess 190:215

    Article  Google Scholar 

  • Douki T, Corbière C, Preterre D, Martin PJ, Lecureur V, André V, Landkocz Y, Pottier I, Keravec V, Fardel O, Moreira-Rebelo S, Pottier D, Vendeville C, Dionnet F, Gosset P, Billet S, Monteil C, Sichel F (2018) Comparative study of diesel and biodiesel exhausts on lung oxidative stress and genotoxicity in rats. Environ Pollut 235:514–524

    Article  CAS  Google Scholar 

  • Eom HJ, Liu Y, Kwak GS, Heo M, Song KS, Chung YD, Chon TS, Choi J (2017) Inhalation toxicity of indoor air pollutants in Drosophila melanogaster using integrated transcriptomics and computational behavior analyses. Sci Rep 7:46473

    Article  CAS  Google Scholar 

  • Feretti D et al (2014) Monitoring air pollution effects on children for supporting public health policy: the protocol of the prospective cohort MAPEC study. J Neurointerv Surg 4:1–8

    Google Scholar 

  • Gaivão I, Sierra M (2014) Drosophila comet assay: insights, uses, and future perspectives. Front Genet 5:304

    Article  Google Scholar 

  • Gerber GB, Leonard A, Hantson P (2002) Carcinogenicity, mutagenicity and teratogenicity of manganese compounds. Crit Rev Oncol Hematol 42:25–34

    Article  CAS  Google Scholar 

  • Gómez-Arroyo S, Cortés-Eslava J, Loza-Gómez P, Arenas-Huertero F, Mora MG, Bermea OM (2018) In situ biomonitoring of air quality in rural and urban environments of Mexico Valley through genotoxicity evaluated in wild plants. Atmos Pollut Res 9:119–125

    Article  Google Scholar 

  • IARC (International Agency for Research on Cancer) (1983) Polynuclear aromatic compounds. Iarc monographs on the evaluation of the carcinogenic risk of chemical to humans. Part 1, chemical, environmental and experimental data, v. 32. In: December,1983. Lyon, France

    Google Scholar 

  • IBGE (Instituto Brasileiro de Geografia e Estatística), (2018). https://www.ibge.gov.br (Acessed April 2018)

  • Imanikia S, Galea F, Nagy E, Phillips DH, Stürzenbaum SR, Arlt VM (2016) The application of the comet assay to assess the genotoxicity of environmental pollutants in the nematode Caenorhabditis elegans. Environ Toxicol Pharmacol 45:356–361

    Article  CAS  Google Scholar 

  • Inamdar AA, Masurekar P, Bennett JW (2010) Neurotoxicity of fungal volatile organic compounds in Drosophila melanogaster. Toxicol Sci 117:418–426

    Article  CAS  Google Scholar 

  • Lemos AT, Coronas MV, Rocha JA, Vargas VM (2012) Mutagenicity of particulate matter fractions in areas under the impact of urban and industrial activities. Chemosphere 89:1126–1134

    Article  CAS  Google Scholar 

  • Lenz S, Karsten P, Schulz JB, Voigt A (2013) Drosophila as a screening tool to study human neurodegenerative diseases. J Neurochem 127:453–460

    Article  CAS  Google Scholar 

  • Lima P, Vasconcellos MC, Montenegro RC, Bahia MO, Costa ET, Antunes LM, Burbano RR (2011) Genotoxic effects of aluminum, iron, and manganese in human cells and experimental systems: a review of the literature. Hum Exp Toxicol 30:1435–1444

    Article  CAS  Google Scholar 

  • Lloyd TE, Taylor JP (2010) Flightless flies: Drosophila models of neuromuscular disease. Ann N Y Acad Sci 1184:e1–20

    Article  CAS  Google Scholar 

  • López ML, Ceppi S, Palancar GG, Olcese LE, Tirao G, Toselli BM (2011) Elemental concentration and source identification of PM10 and PM2.5 by SR-XRF in Córdoba City, Argentina. Atmos Environ 45:5450–5457

    Article  Google Scholar 

  • Meyer S, Schulz J, Jeibmann A, Taleshi MS, Ebert F, Francesconid KA, Schwerdtle T (2014) Arsenic-containing hydrocarbons are toxic in the in vivo model Drosophila melanogaster. Metallomics 6:2010–2014

    Article  CAS  Google Scholar 

  • Møller P, Hemmingsen JG, Jensen DM, Danielsen PH, Karottki DG, Jantzen K, Roursgaard M, Cao Y, Kermanizadeh A, Klingberg H, Christophersen DV, Hersoug LG, Loft S (2015) Applications of the comet assay in particle toxicology: air pollution and engineered nanomaterials exposure. Mutagenesis 30:67–83

    Article  Google Scholar 

  • Moraes-Filho AV, Carvalho CJS, Verçosa CJ, Gonçalves MW, Rohde C, Silva DM, Cunha KS, Chen-Chen L (2017) In vivo genotoxicity evaluation of efavirenz (EFV) and tenofovir disoproxil fumarate (TDF) alone and in their clinical combinations in Drosophila melanogaster. Mutat Res Gen Tox En 820:31–38

    Article  Google Scholar 

  • Nandhakumar S, Parasuraman S, Shanmugam MM, Ramachandra RK, Chand P, Vishnu BB (2011) Evaluation of DNA damage using single-cell gel electrophoresis. J Pharmacol Pharmacother 2:107–111

    Article  CAS  Google Scholar 

  • Nardocci AC, Freitas CU, Leon ACMP, Junger WL, Gouveia NC (2013) Air pollution and respiratory and cardiovascular diseases: a time series study in Cubatão, São Paulo State, Brazil. Cad Saude Publica 29:1867–1876

    Article  Google Scholar 

  • Nascimento LFC, Francisco JB (2013) Particulate matter and hospital admission due to arterial hypertension in a medium-sized Brazilian city. Cad Saude Publica 29:1565–1571

    Article  Google Scholar 

  • Neethu CB, Vardhanan YS (2016) Effect of minerals on free radicals induced damages in Drosophila melanogaster. Int J Toxicol Pharmacol Res 8:346–352

    Google Scholar 

  • Nehr S, Franzen-Reuter I, Kucejko C (2017) New directions: future approaches to the standardized assessment of airborne pollutants affecting environmental quality. Atmos Environ 166:570–572

    Article  CAS  Google Scholar 

  • Noronha EAP (2013) Análise das potencialidades e vulnerabilidades socioambientais decorrentes do processo da industrialização no município de Vitória de Santo Antão - PE. Universidade de Pernambuco, Recife, Dissertation

    Google Scholar 

  • Núňez-Millacura C, Tapia V, Muňoz P, Maccioni R, Núňez M (2002) An oxidative stress-mediated positive feedback iron uptake loop in neuronal cell. J Neurochem 82:240–248

    Article  Google Scholar 

  • Ostling O, Johanson KJ (1984) Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun 123:291–298

    Article  CAS  Google Scholar 

  • Ogawa HI et al (1994) Genotoxic activities in vivo of cobaltous chloride and other metal chlorides as assayed in the Drosophila wing spot test. Mutat Res 320:133–140

    Article  CAS  Google Scholar 

  • Pereira BB, Campos EOJ, Lima EA, Barrozo MA, Morelli S (2014) Biomonitoring air quality during and after a public transportation strike in the center of Uberlândia, Minas Gerais, Brazil by Tradescantia micronucleus bioassay. Environ Sci Pollut Res Int 21:3680–3685

    Article  CAS  Google Scholar 

  • Rainho CR, Corrêa SM, Aiub CAF, Felzenszwalb I (2016) Biomonitoring of tunnel workers exposed to heavy air pollution in Rio de Janeiro, Brazil. Air Qual Atmos Health 9:881–886

    Article  CAS  Google Scholar 

  • Rand MD (2010) Drosophotoxicology: the growing potential for Drosophila in neurotoxicology. Neurotoxicol Teratol 32:74–83

    Article  CAS  Google Scholar 

  • Redlarski G, Lewczuk B, Żak A, Koncicki A, Krawczuk M, Piechocki J, Jakubiuk K, Tojza P, Jaworski J, Ambroziak D, Skarbek L, Gradolewski D (2015) The influence of electromagnetic pollution on living organisms: historical trends and forecasting changes. Biomed Res Int 2015:1–18

    Article  Google Scholar 

  • Reiter LT, Potocki L, Chien S, Gribskov M, Bier E (2001) A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 11:1114–1125

    Article  CAS  Google Scholar 

  • Sanders T, Liu Y, Tchounwou PB (2015) Cytotoxic, genotoxic, and neurotoxic effects of Mg, Pb, and Fe on Pheochromocytoma (PC-12) cells. Environ Toxicol 30:1445–1458

    Article  CAS  Google Scholar 

  • Verçosa CJ, Castro IFA, Garcia ACL, Rohde C (2015) An efficient rearing population cage to expose Drosophilids to various environmental agents. Dros Info Service 98:144–145

    Google Scholar 

  • Verçosa CJ, Moraes-Filho AV, Castro IFA, Santos RGD, Cunha KS, Silva DME, Garcia ACL, Navoni JA, Amaral VSD, Rohde C (2017) Validation of Comet assay in Oregon-R and Wild type strains of Drosophila melanogaster exposed to a natural radioactive environment in Brazilian semiarid region. Ecotoxicol Environ Saf 141:148–153

    Article  Google Scholar 

  • Wasserkort R, Koller T (1997) Screening toxic effects of volatile organic compounds using Drosophila melanogaster. J Appl Toxicol 17:119–125

    Article  CAS  Google Scholar 

  • Wilson M, Widdicombe JH, Gohil K, Burtis KC, Reznick AZ, Cross CE, Eiserich JP (2005) Are Drosophila a useful model for understanding the toxicity of inhaled oxidative pollutants: a review. Inhal Toxicol 17:765–774

    Article  CAS  Google Scholar 

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Acknowledgements

Special thanks are due to our colleagues from Laboratory of Genetics for their help in the field sampling.

Funding

This work was supported by Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Pró-Reitoria para Assuntos de Pesquisa e Pós-Graduação (PROPESQ) from Universidade Federal de Pernambuco (UFPE).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Saúde Humana e Meio Ambiente, Centro Acadêmico de Vitória (CAV), Universidade Federal de Pernambuco (UFPE), Vitória de Santo Antão, Pernambuco, Brazil

    Samuel Lima de Santana

  2. Laboratório de Genética, Centro Acadêmico de Vitória, Universidade Federal de Pernambuco, Rua do Alto do Reservatório s/n, Bairro Bela Vista, Vitória de Santo Antão, Pernambuco, CEP 51608-680, Brazil

    Samuel Lima de Santana, Cícero Jorge Verçosa, Ícaro Fillipe de Araújo Castro, Érima Maria de Amorim, André Severino da Silva & Claudia Rohde

  3. Centro Regional de Ciências Nucleares do Nordeste (CRCN-NE), Av. Prof. Luiz Freire, 200, Bairro Cidade Universitária, Recife, CEP 50740-545, Pernambuco, Brazil

    Thiago Moura da Rocha Bastos, Luiz Joaquim da Silva Neto, Thiago Oliveira dos Santos & Elvis Joacir De França

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  1. Samuel Lima de Santana
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  2. Cícero Jorge Verçosa
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  3. Ícaro Fillipe de Araújo Castro
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  5. André Severino da Silva
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  7. Luiz Joaquim da Silva Neto
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  8. Thiago Oliveira dos Santos
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  10. Claudia Rohde
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Correspondence to Claudia Rohde.

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de Santana, S.L., Verçosa, C.J., de Araújo Castro, Í.F. et al. Drosophila melanogaster as model organism for monitoring and analyzing genotoxicity associated with city air pollution. Environ Sci Pollut Res 25, 32409–32417 (2018). https://doi.org/10.1007/s11356-018-3186-5

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