Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 31558–31568 | Cite as

Micronucleus frequency is correlated with antioxidant enzyme levels in workers occupationally exposed to pesticides

  • Maria del Carmen Xotlanihua-Gervacio
  • Mirna Citlali Guerrero-Flores
  • José Francisco Herrera-Moreno
  • Irma Martha Medina-Díaz
  • Yael Yvette Bernal-Hernández
  • Briscia Socorro Barrón-Vivanco
  • Monserrat Sordo
  • Aurora Elizabeth Rojas-García
Research Article
  • 117 Downloads

Abstract

Oxidative stress can cause DNA damage leading to nuclear anomalies such as micronuclei (MN). Antioxidant enzymes involved in protection against intracellular oxidative stress include glutathione peroxidase (GPx), glutathione reductase (GR), superoxide dismutase (SOD), and catalase (CAT). Pesticide exposure induces oxidative stress and alters antioxidant defense mechanisms, including detoxification and scavenger enzymes. The aim of this study was to evaluate MN frequency in workers occupationally exposed to pesticides and their relationship with antioxidant enzyme activities. A cross-sectional study was conducted in 201 individuals, some of whom were dedicated to the spraying of pesticides. The cytokinesis-block micronucleus (CBMN) assay was conducted, and the activities of GPx, GR, SOD, and CAT were determined. The geometric mean (GM) of MN was 5.4 (1–26 MN). The GM for the antioxidant enzymes was 198.68 U/mL for GPx, 38.96 U/g Hb for GR, 94.78 U/mL for SOD, and 69.77 U/g Hb for CAT. There was a lower MN frequency in males than that in females, and a higher nuclear index. In addition, age affected MN frequency. There was a negative correlation between MN frequency and GPx activity, but a positive one between MN frequency and GR activity. These findings suggest the involvement of GPx in MN frequency.

Keywords

Micronuclei Antioxidant enzymes Pesticides exposure 

Notes

Acknowledgments

The authors would like to thank Rigoberto Zepeda Arce for his technical assistance; Cyndia Azucena González Arias and Norma Elena Pérez Herrera for their critical review of the manuscript; to Leticia Yañez Estrada and the team of the Gender, Health and Environmental Laboratory of the Medicine Faculty, San Luis Potosi Autonomous University, for their help in DAP determination. The authors also would like to thank all study participants.

Funding information

This study was supported by CONACyT-SALUD-Mexico-233803.

Compliance with ethical standards

All participants signed an informed consent at the beginning of the study. This study was approved by the Bioethics Commission of Nayarit State, Mexico (CEBN/0112017).

Conflict of interest

The authors declare that there are no conflicts of interest.

References

  1. Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezale A (2004) Pesticides and oxidative stress: a review. Med Sci Monit 10:141–147Google Scholar
  2. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefGoogle Scholar
  3. Ali D, Kumar PG, Kumar S, Ahmed M (2014) Evaluation of genotoxic and oxidative stress response to dimethoate in freshwater fishChanna punctatus (Bloch). Chem Speciat Bioavailab 26:111–118CrossRefGoogle Scholar
  4. Banerjee BD, Seth V, Ahmed RS (2001) Pesticide-induced oxidative stress: perspectives and trends. Rev Environ Health 16:1–40CrossRefGoogle Scholar
  5. Barale R, Chelotti L, DelRy S, Andreassi MG, Ballardin M, Bulleri M, He J, Baldacci S, Di Pede F, Gemignani F, Landi S (1998) Sister chromatid exchange and micronucleus frequency in human lymphocytes of 1,650 subjects in an Italian population: II. Contribution of sex, age, and lifestyle. Environ Mol Mutagen 31:228–242CrossRefGoogle Scholar
  6. Barp J, Araújo ASR, Fernandes TRG, Rigatto KV, Llesuy S, Belló-Klein A, Singal P (2002) Myocardial antioxidant and oxidative stress changes due to sex hormones. Braz J Med Biol Res 35:1075–1081CrossRefGoogle Scholar
  7. Benedetti D, Nunes E, Sarmento M, Porto C, Lochims dos Santos CE, Ferraz Dias J, Da Silva J (2013) Genetic damage in soybean workers exposed to pesticides: evaluation with the comet and buccal micronucleus cytome assays. Mutat Res 752:28–33CrossRefGoogle Scholar
  8. Benitez-Trinidad AB, Herrera-Moreno JF, Vázquez-Estrada G, Verdín-Betancourt FA, Sordo M, Ostrosky-Wegman P, Bernal-Hernández YY, Medina-Díaz IM, Barrón-Vivanco BS, Robledo-Marenco MI, Salazar AM, Rojas-García AE (2015) Cytostatic and genotoxic effect of themeohos in human lymphocytes and HepG2 cells. Toxicol in Vitro 29:779–786CrossRefGoogle Scholar
  9. Bolognesi C (2003) Genotoxicity of pesticides: a review of human biomonitoring studies. Mutat Res 543:251–272CrossRefGoogle Scholar
  10. Bolognesi C, Holland N (2016) The use of the lymphocyte cytokinesis-block micronucleus assay for monitoring pesticide-exposed populations. Mutat Res 770:183–203CrossRefGoogle Scholar
  11. Bolognesi C, Abbondandolo A, Barale R, Casalone R, Dalpra L, De Ferri M, Degrassi F, Forni A, Lamberti L, Lando C, Migliore L, Padovani P, Pasquini R, Puntoni R, Sbrana I, Stella M, Bonassi S (1997) Age-related increase of baseline frequencies of sister chromatid exchanges, chromosome aberrations, and micronuclei in human lymphocytes. Cancer Epidemiol Biomark Prev 6:249–256Google Scholar
  12. Bolognesi C, Creus A, Ostrosky-Wegman P, Marcos R (2011) Micronuclei and pesticide exposure. Mutagenesis 26:19–26CrossRefGoogle Scholar
  13. Bonassi S, Znaor A, Ceppi CL, Chang WP, Holland N, Kirsch-Volders M, Zeiger E, Ban S, Barale R, Bigatti MP, Bolognesi C, Cebulska-Wasilewska A, Fabianova E, Fucic A, Hagmar L, Joksic G, Martelli A, Migliore L, Mirkova E, Scarfi MR, Zijno A, Norppa H, Fenech M (2007) An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans. Carcinogenesis 28:625–631CrossRefGoogle Scholar
  14. Cervantes Ríos E, Ortiz Muñiz R, Konigsberg Fainstein M, Graniel Guerrero J, Rodríguez Cruz L (2018) Assessment of micronucleus and oxidative stress in peripheral blood from malnourished children. Nutr Hosp 35:519–526Google Scholar
  15. Cicchetti R, Argentin G (2003) The role of oxidative stress in the in vitro induction of micronuclei by pesticides in mouse lung fibroblasts. Mutagenesis 18:127–132CrossRefGoogle Scholar
  16. Eastmond DA, Tucker JD (1989) Identification of aneuploidy-inducing agents using cytokinesis-blocked human lymphocytes and an antikinetochore antibody. Environ Mol Mutagen 1989:34–43CrossRefGoogle Scholar
  17. Fenech M (2010) Dietary reference values of individual micronutrients and nutriomes for genome damage prevention; current status and a road map to the future. Am J Clin Nutr 91(suppl):1438S–1454SCrossRefGoogle Scholar
  18. Fenech M, Bonassi S (2011) The effect of age, gender, diet and lifestyle on DNA damage measured using micronucleus frequency in human peripheral blood lymphocytes. Mutagenesis 26:43–49CrossRefGoogle Scholar
  19. Fenech M, Chang WP, Kirsch-Volders M, Holland N, Bonassi S, Zeiger E (2003) HUMN project: detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutat Res 534:65–75CrossRefGoogle Scholar
  20. Fenech M, Kirsch-Volders M, Natarajan AT, Surralles J, Crott JW, Parry J, Norppa H, Eastmond DA, Tucker JD, Thomas P (2011) Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis 26:125–132CrossRefGoogle Scholar
  21. Giergiel M, Lopucki M, Stachowicz N, Kankofer M (2012) The influence of age and gender on antioxidant enzyme activities in humans and laboratory animals. Aging Clin Exp Res 24:561–569Google Scholar
  22. Haff T, Raderschall E, Reddy G, Ward DC, Radding CM, Golub EI (1999) Sequestration of mammalian Rad51-recombination protein into micronuclei. J Cell Biol 144:11–20CrossRefGoogle Scholar
  23. Hai-Yang Y, Ruo F, Jing L, Hai-Yu W, Ya-Dong W (2014) Increased frequency of micronuclei in binucleated lymphocytes among occupationally pesticide-exposed populations: a meta-analysis. Asian Pac J Cancer Prev 15:6955–6960CrossRefGoogle Scholar
  24. Halliwell B (2002) Effect of diet on cancer development: is oxidative DNA damage a biomarker? Free Radic Biol Med 32:968–974CrossRefGoogle Scholar
  25. Hanawalt PC, Gee P, Ho L, Hsu RK, Kane CJM (1992) Genomic heterogeneity of DNA repair. Role in aging? Ann N Y Acad Sci 663:17–25CrossRefGoogle Scholar
  26. Hernández AF, Lacasaña M, Gil F, Rodriguez-Barranco M, Pla A, López-Guarnido O (2013) Evaluation of pesticide-induced oxidative stress from a gene-environment interaction perspective. Toxicology 307:95–102CrossRefGoogle Scholar
  27. Iarmarcovai G, Bonassi S, Sari-Minodier I, Baciuchka-Palmaro M, Botta A, Orsiere T (2007) Exposure to genotoxic agents, host factors, and lifestyle influence the number of centromeric signals in micronuclei: a pooled re-analysis. Mutat Res 615:18–27CrossRefGoogle Scholar
  28. Ide T, Tsutsui H, Ohashi N, Hayashidani S, Suematsu N, Tsuchihashi M, Tamai H, Takaeshita A (2002) Greater oxidative stress in healthy young men compare with premenopausal women. Arterioscler Thromb Vasc Biol 22:438–442CrossRefGoogle Scholar
  29. Jonnalagadda PR, Jahan P, Venkatasubramanian S, Khan IA, Prasad AYE, Reddy KA, Rao MV, Venkaiah K, Hasan Q (2012) Genotoxicity in agricultural farmers from Guntur district of South India—a case study. Hum Exp Toxicol 31:741–747CrossRefGoogle Scholar
  30. Jurkovič S, Osredkar J, Marc J (2008) Molecular impact of glutathione peroxidases in antioxidant processes. Biochem Med (Zagreb) 18:162–174CrossRefGoogle Scholar
  31. Kander MC, Cui Y, Liu Z (2017) Gender difference in oxidative stress: a new look at the mechanisms for cardiovascular diseases. J Cell Mol Med 21:1024–1032CrossRefGoogle Scholar
  32. Khayat CB, Costa EO, Gonçalves MW, da Cruz e Cunha DM, da Cruz AS, de Araújo Melo CO, Bastos RP, da Cruz AD, de Melo e Silva D (2013) Assessment of DNA damage in Brazilian workers occupationally exposed to pesticides: a study from Central Brazil. Environ Sci Pollut Res 20:7334–7340CrossRefGoogle Scholar
  33. Lee C-H, Kamijima M, Kim H, Shibata E, Ueyama J, Suzuki T, Takagi K, Saito I, Gotoh M, Hibi H, Naito H, Nakajima T (2006) 8-Hydroxydeoxyguanosine levels in human leukocyte and urine according to exposure to organophosphorus pesticides and paraoxonase 1genotype. Int Arch Occup Environ Health 80:217–227CrossRefGoogle Scholar
  34. Lukaszewicz-Hussain A (2010) Role of oxidative stress in organophosphate insecticide toxicity—short review. Pestic Biochem Physiol 98:145–150CrossRefGoogle Scholar
  35. Luzhna L, Kathiria P, Kovalchuk O (2013) Micronuclei in genotoxicity assessment: from genetics to epigenetics and beyond. Front Genet 4:1–17CrossRefGoogle Scholar
  36. Matarrese P, Colasanti T, Ascione B, Margutti P, Franconi F, Alessandri C, Conti F, Riccieri V, Rosano G, Ortona E, Malorni W (2011) Gender disparity in susceptibility to oxidative stress and apoptosis induced by autoantibodies specific to RLIP76 in vascular cells. Antioxid Redox Signal 15:2825–2836CrossRefGoogle Scholar
  37. Mateuca R, Lombaert N, Aka PV, Decordier L, Kirsch-Volders M (2006) Chromosomal changes: induction, detection methods and applicability in human biomonitoring. Biochimie 88:1515–1531CrossRefGoogle Scholar
  38. Mostafalou S, Abdollahi M (2013) Pesticides and human chronic diseases evidences, mechanisms and perspectives. Toxicol Appl Pharmacol 268:157–177CrossRefGoogle Scholar
  39. Muniz JF, McCauley L, Scherer J, Lasarev M, Koshy M, Kow YW, Nazar-Stewart V, Kisby GE (2008) Biomarkers of oxidative stress and DNA damage in agricultural workers: a pilot study. Toxicol Appl Pharmacol 227:97–107CrossRefGoogle Scholar
  40. Pajović SB, Saičić ZS (2008) Modulation of antioxidant enzyme activities by sexual steroid hormones. Physiol Res 57:801–811Google Scholar
  41. Possamai FP, Fortunato JJ, Feier G, Agostinho FR, Quevedo J, Filho DW, Dal-Pizzol F (2007) Oxidative stress after acute and sub-chronic malathion intoxication in Wistar rats. Environ Toxicol Pharmacol 23:198–204CrossRefGoogle Scholar
  42. Prakasam A, Sethupathy S, Lalitha S (2001) Plasma and RBCs antioxidant status in occupational male pesticides sprayers. Clin Chim Acta 310:107–112CrossRefGoogle Scholar
  43. Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, Dhama K (2014) Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int 2014:1–19CrossRefGoogle Scholar
  44. Ramírez-Jiménez R, Mejía-Saucedo R, Calderón-Hernández J, Montero-Montoya R, Yáñez-Estrada L (2014) Concentraciones urinarias de metabolitos de plaguicidas organofosforados en niños y adolescentes de una zona agrícola de México. Revista Iberoamericana de Ciencias 1:87–94Google Scholar
  45. Richard F, Aurias A, Couturier J, Dutrillaux AM, Flury-Herard A, Gerbautl-Seureau M, Hoffschir F, Lamoliatte E, Lefrancois D, Lombard M, Muleris M, Prieur M, Ricoul M, Sabatier L, Viegas-Péquignot E, Volobouev V, Dutrillaux B (1993) Aneuploidy in human lymphocytes: an extensive study of eight individuals of various ages. Mutat Res 295:71–80CrossRefGoogle Scholar
  46. Rojas-García AE, Sordo M, Vega L, Quintanilla-Vega B, Solis-Heredia M, Ostrosky-Wegman P (2009) The role of paraoxonase polymorphisms in the induction of micronucleus in paraoxon-treated human lymphocytes. Environ Mol Mutagen 50:823–829CrossRefGoogle Scholar
  47. Sandström BE, Marklund SL (1990) Effects of variation in glutathione peroxidase activity on DNA damage and cell survival in human cells exposed to hydrogen peroxide and t-butyl hydroperoxide. Biochem J 271:17–23CrossRefGoogle Scholar
  48. Sedelnikova OA, Redon CE, Dickey JS, Nakamura AJ, Georgakilas AG, Bonner WM (2010) Role of oxidatively induced DNA lesions in human pathogenesis. Mutat Res 704:152–159CrossRefGoogle Scholar
  49. Shadnia S, Azizi E, Hosseini R, Khoei S, Fouladdel S, Pajoumand A, Jalali N, Abdollahi M (2005) Evaluation of oxidative stress and genotoxicity in organophosphorus insecticide formulators. Hum Exp Toxicol 24:439–445CrossRefGoogle Scholar
  50. Sokoloff K, Frase W, Arbuckle TE, Fisher M, Gaudreau E, LeBlanc A, Morisset A-S, Bouchard MF (2016) Determinants of urinary concentrations of dialkyl phosphates among pregnant women in Canada—results from the MIREC study. Environ Int 94:133–140CrossRefGoogle Scholar
  51. Valcke M, Samuel O, Bouchard M, Dumas P, Belleville D, Tremblay C (2006) Biological monitoring of exposure to organophosphate pesticides in children living in periurban areas of the province of Quebec, Canada. Int Arch Occup Environ Health 79:568–577CrossRefGoogle Scholar
  52. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40CrossRefGoogle Scholar
  53. Verstraeten VLRM, Peckham LA, Olive M, Capell BC, Collins FS, Nabel EG, Young SG, Fong LG, Lammerding J (2011) Protein farnesylation inhibitors cause donut-shaped cell nuclei attributable to a centrosome separation defect. PNAS 108:4997–5002CrossRefGoogle Scholar
  54. Wang X, Thomas P, Xue J, Fenech M (2004) Folate deficiency induces aneuploidy in human lymphocytes in vitro-evidence using cytokinesis-blocked cells and probes specific for chromosomes 17 and 21. Mutat Res 55:167–180CrossRefGoogle Scholar
  55. WHO (2006) World Health Organization. BMI classification. Global database on body mass index. http://apps.who.int/bmi/index.jsp?introPage=intro_3.html
  56. WHO (2009) World Health Organization. The WHO recommended classification of pesticides by hazard and guidelines to classification. http://apps.who.int/iris/bitstream/10665/44271/1/9789241547963_eng.pdf
  57. Yan F, Mu Y, Yan G, Liu J, Shen J, Luo G (2010) Antioxidant enzyme mimics with synergism. Mini-Rev Med Chem 10:342–356CrossRefGoogle Scholar
  58. Yuzhalin AE, Kutikhin AG (2012) Inherited variations in the SOD and GPX gene families and cancer risk. Free Radic Res 46:581–599CrossRefGoogle Scholar
  59. Zeng H (2009) Selenium as an essential micronutrient: roles in cell cycle and apoptosis. Molecules 14:1263–1278CrossRefGoogle Scholar
  60. Zepeda-Arce R, Rojas-García AE, Benitez-Trinidad A, Herrera-Moreno JF, Medina-Díaz IM, Barrón-Vivanco BS, Pier Villegas G, Hernández-Ochoa I, Sólis Heredia MJ, Bernal-Hernández YY (2017) Oxidative stress and genetic damage among workers exposed primarily to organophosphate and pyrethroid pesticides. Environ Toxicol 32:1754–1764CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Maria del Carmen Xotlanihua-Gervacio
    • 1
    • 2
  • Mirna Citlali Guerrero-Flores
    • 1
  • José Francisco Herrera-Moreno
    • 1
    • 2
  • Irma Martha Medina-Díaz
    • 1
  • Yael Yvette Bernal-Hernández
    • 1
  • Briscia Socorro Barrón-Vivanco
    • 1
  • Monserrat Sordo
    • 3
  • Aurora Elizabeth Rojas-García
    • 1
  1. 1.Laboratorio de Contaminación y Toxicología Ambiental. Secretaría de Investigación y PosgradoUniversidad Autónoma de NayaritTepicMexico
  2. 2.Posgrado en Ciencias Biológico Agropecuarias|Unidad Académica de AgriculturaXaliscoMexico
  3. 3.Instituto de Investigaciones BiomédicasUNAMMéxico DFMexico

Personalised recommendations