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Associations between sperm quality, DNA damage, and CYP1A1, GSTT1 and GSTM1 polymorphisms with 1-hydroxypyrene urinary levels in men occupationally exposed to polycyclic aromatic hydrocarbons

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Abstract

Purpose

During recent decades, several reports have suggested a decrease in semen quality and DNA damage due in part to environmental toxicants and industrial chemicals. Among these xenobiotics, polycyclic aromatic hydrocarbons (PAHs) are of particular concern because of their remarkable mutagenic and carcinogenic properties and because several experimental and epidemiological studies have reported adverse effects of PAHs on male reproductive health and DNA structure. The aim of the study was to evaluate the association between 1-hydroxypyrene (1-OHP) urinary levels and sperm quality, DNA damage and the frequency of CYP1A1, GSTT1, and GSTM1 polymorphisms.

Methods

Semen, urine and blood samples were taken for sperm-quality assessment, 1-OHP urinary level measurement, DNA damage evaluation and polymorphism frequency analysis of three genes implicated in PAH metabolism in a total of 70 Mexican subjects exposed and nonexposed to PAHs.

Results

A significant decrease in sperm quality and increased DNA damage were registered in occupationally exposed volunteers. Polymorphisms modified the 1-OHP urinary levels; however, no associations were found between them. Inverse associations were registered between the sperm concentration/mL and 1-OHP levels and between tail lengths and the GSMT1 null genotype.

Conclusions

Our data showed an inverse association between 1-OHP urinary levels and both sperm quality and the DNA integrity. Additionally, the heterozygote variants of CYP1A1-m1 and CYP1A1-m2 significantly increased the urinary excretion of 1-OHP, and the GSTM1 null variant was inversely associated with the comet parameters evaluated.

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References

  • Agarwal A, Said TM (2003) Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update 9:331–345

    Article  CAS  Google Scholar 

  • Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3(9):2303–2308

    Article  CAS  Google Scholar 

  • Boström CE, Gerde P, Hanberg A, Jernstrom B, Johansson C, Kyrklund T et al (2002) Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ Health Perspect 110(Suppl 3):451–488

    Article  Google Scholar 

  • Cascorbi I, Brock Möller J, Roots I (1996) A C4887A polymorphism in exon 7 of human CYP1A1: population frequency, mutation linkages, and impact on lung cancer susceptibility. Cancer Res 56(21):4965–4969

    CAS  Google Scholar 

  • Chatterjee S, Chakrabarti S, Sengupta B, Poddar S et al (2009) Prevalence of CYP1A1 and GST polymorphisms in the population of northeastern India and susceptibility of oral cancer. Oncol Res 17(9):397–403

    Article  CAS  Google Scholar 

  • Chen B, Hu Y, Jin T, Lu D, Shao M, Zheng L, Wang Q, Shen Y, Liu H, Liu Y, Zhou Y (2007) The influence of metabolic gene polymorphisms on urinary 1-hydroxypyrene concentrations in Chinese coke oven workers. Sci Total Environ 381(1–3):38–46. https://doi.org/10.1016/j.scitotenv.2007.02.021

    Article  CAS  Google Scholar 

  • Choosong T, Phakthongsuk P, Tekasakul S, Tekasakul P (2014) Urinary 1-hydroxypyrene levels in workers exposed to polycyclic aromatic hydrocarbon from rubber wood burning. Saf Health Work 5(2):86–90. https://doi.org/10.1016/j.shaw.2014.03.004

    Article  Google Scholar 

  • Chuang CY, Chang CC (2007) Urinary 1-hydroxypyrene level relative to vehicle exhaust exposure mediated by metabolic enzyme polymorphisms. J Occup Health 49(2):140–151

    Article  CAS  Google Scholar 

  • Concha-Barrientos M, Steenland K, Plunnet L (2006) The contribution of occupational risks to global burden of diseases: summary and next steps. Medlav 97(2):313–321

    Google Scholar 

  • Finotti AC, Costa E, Silva RC, Bordin BM, Silva CT, Moura KK (2009) Glutathione S-transferase M1 and T1 polymorphism in men with idiopathic infertility. Genet Mol Res 8(3):1093–1098. https://doi.org/10.4238/vol8-3gmr642

    Article  CAS  Google Scholar 

  • Han X, Zhou N, Cui Z, Ma M, Li L et al (2011) Association between urinary polycyclic aromatic hydrocarbon metabolites and sperm DNA damage: a population study in Chongqing, China. Environ Health Perspect 119(5):652–657. https://doi.org/10.1289/ehp.1002340

    Article  CAS  Google Scholar 

  • Hayashi SI, Watanabe J, Nakachi K, Kawajiri K (1991) PCR detection of an A/G polymorphism within exon 7 of the CYP1A1 gene. Nucleic Acids Res 19(17):4797

    Article  CAS  Google Scholar 

  • Hsu PC, Chen IY, Pan CH, Wu KY, Pan MH et al (2006) Sperm DNA damage correlates with polycyclic aromatic hydrocarbons biomarker in coke-oven workers. Int Arch Occup Environ Health 79(5):349–356. https://doi.org/10.1007/s00420-005-0066-3

    Article  CAS  Google Scholar 

  • International Agency for Research on Cancer (IARC) (2015) Monographs on the evaluation of carcinogenic risks to humans. Outdoor air pollution 109 France

  • Izawa H, Kohara M, Watanabe G, Taya K, Sagai M (2006) Effects of diesel exhaust particles on the male reproductive system in strains of mice with different aryl hydrocarbon receptor responsiveness. J Reprod Dev 53(6):1191–1197

    Article  Google Scholar 

  • Jeng HA, Yu L (2008) Alteration of sperm quality and hormone levels by polycyclic aromatic hydrocarbons on airborne particulate particles. J Environ Sci Health A Tox Hazard Subst Environ Eng 43(7):675–681. https://doi.org/10.1080/10934520801959815

    Article  CAS  Google Scholar 

  • Jeng HA, Pan CH, Chao MR, Chiu CC, Zhou G, Chou CK, Lin WY (2016) Sperm quality and DNA integrity of coke oven workers exposed to polycyclic aromatic hydrocarbons. Int J Occup Med Environ Health 29(6):915–926. https://doi.org/10.13075/ijomeh.1896.00598

    Article  Google Scholar 

  • Kim YD, Todoroki H, Oyama T, Isse T, Matsumoto A, Yamaguchi T, Kim H, Uchiyama I, Kawamoto T (2004) Identification of cytochrome P450 isoforms involved in 1-hydroxylation of pyrene. Environ Res 94(3):262–266

    Article  CAS  Google Scholar 

  • Klöslová Z, Drímal M, Balog K, Koppová K, Dubajová J (2016) The relations between polycyclic aromatic hydrocarbons exposure and 1-OHP levels as a biomarker of the exposure. Cent Eur J Public Health 24(4):302–307. https://doi.org/10.21101/cejph.a4179

    Article  Google Scholar 

  • Kuusimaki L, Peltonen Y, Mutanen P, Peltonen K et al (2004) Urinary hydroxy-metabolites of naphthalene, phenanthrene and pyrene as markers of exposure to diesel exhaust. Int Arch Occup Environ Health 77(1):23–30. https://doi.org/10.1007/s00420-003-0477-y

    Article  CAS  Google Scholar 

  • Menzie CA, Potocki BB, Santodonato J (1992) Exposure to carcinogenic PAHs in the environment. Environ Sci Technol 26:1278–1284

    Article  CAS  Google Scholar 

  • Moretti M, Dell’Omo M, Villarini M, Pastorelli R et al (2007) Primary DNA damage and genetic polymorphisms for CYP1A1, EPHX and GSTM1 in workers at a graphite electrode manufacturing plant. BMC Public Health 7:270. https://doi.org/10.1186/1471-2458-7-270

    Article  CAS  Google Scholar 

  • Nie JS, Zhang HM, Sun JY, Zeng P, Zhang L, Niu Q (2009) Relationship between CYP1A1 gene polymorphisms and urinary 1-hydroxypyrene levels in coke oven workers. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi (5):270–275

  • Olive PL, Banáth JP, Durand RE (1990) Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the “comet” assay. Radiat Res 122(1):86–94

    Article  CAS  Google Scholar 

  • Oliveira-Galvão MF, Queiroz JD, Duarte ES, Hoelzemann JJ, André PA, Saldiva PH, Menezes Filho JA, Batistuzzo de Medeiros SR (2017) Characterization of the particulate matter and relationship between buccal micronucleus and urinary 1-hydroxypyrene levels among cashew nut roasting workers. Environ Pollut (Pt A):659–671. https://doi.org/10.1016/j.envpol.2016.10.024

  • Olshan AF, Luben TJ, Hanley NM, Perreault SD, Chan RL, Herring AH, Basta PV, DeMarini DM (2010) Preliminary examination of polymorphisms of GSTM1, GSTT1, and GSTZ1 in relation to semen quality. Mutat Res 688(1–2):41–46. https://doi.org/10.1016/j.mrfmmm.2010.03.002

    Article  CAS  Google Scholar 

  • Petchpoung K, Kaojarern S, Yoovathaworn K, Sura T, Sirivarasai J (2011) The influence of metabolic gene polymorphisms on urinary 1-hydroxypyrene concentration in Thai bus drivers. Environ Toxicol Pharmacol 31(1):160–164. https://doi.org/10.1016/j.etap.2010.10.006

    Article  CAS  Google Scholar 

  • Raychoudhury SS, Kubinski D (2003) Polycyclic aromatic hydrocarbon-induced cytotoxicity in cultured rat Sertoli cells involves differential apoptotic response. Environ Health Perspect 111(1):33–38. https://doi.org/10.1289/ehp.5458

    Article  CAS  Google Scholar 

  • Rodríguez I, Sandra GA, Rafael VP, Carmen MV, Josefina CE, del Carmen CE, Rocio GM, Francisco AH, Elena CS (2012) Evaluation of 8-hydroxy-2′-deoxyguanosine (8-OHdG) adduct levels and DNA strand breaks in human peripheral blood lymphocytes exposed in vitro to polycyclic aromatic hydrocarbons with or without animal metabolic activation. Toxicol Mech Methods 22(3):170–183. https://doi.org/10.3109/15376516.2011.623330

    Article  CAS  Google Scholar 

  • Sakkas D, Alvarez JG (2010) Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 93:1027–1036

    Article  CAS  Google Scholar 

  • Sanguinetti CJ, Dias Nieto E, Simpson AJ (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17(5):914–921

    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. https://doi.org/10.1016/0014-4827(88)90265-0

    Article  CAS  Google Scholar 

  • Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35(3):206–221

    Article  CAS  Google Scholar 

  • Wang L, Zhao Y, Liu X, Huang T, Wang Y, Gao H, Ma J (2015) Cancer risk of petrochemical workers exposed to airborne PAHs in industrial Lanzhou City, China. Environ Sci Pollut Res Int 22(24):19793–19803. https://doi.org/10.1007/s11356-015-5203-2

    Article  CAS  Google Scholar 

  • World Health Organization (WHO) (2010) Reference values for human semen characteristics, 5th edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Xia Y, Han Y, Zhu P, Wang S, Gu A et al (2009) Relation between urinary metabolites of polycyclic aromatic hydrocarbons and human semen quality. Environ Sci Technol 43(12):4567–4573

    Article  CAS  Google Scholar 

  • http://www.ncbi.nlm.nih.gov/projects/SNP/snp_ref.cgi?rs=4646903; rs=1048943. Accessed 27 July 2017

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Acknowledgements

This work was supported by the University of Coahuila, Mexico.

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Correspondence to Rogelio Recio-Vega or Edgar Olivas-Calderon.

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The study has been conducted in accordance with the ethical standards established in the Declaration of Helsinki of 1964 and its subsequent amendments or comparable ethical standards.

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The authors declare that they have no conflicts of interest.

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Recio-Vega, R., Olivas-Calderon, E., Michel-Ramirez, G. et al. Associations between sperm quality, DNA damage, and CYP1A1, GSTT1 and GSTM1 polymorphisms with 1-hydroxypyrene urinary levels in men occupationally exposed to polycyclic aromatic hydrocarbons. Int Arch Occup Environ Health 91, 725–734 (2018). https://doi.org/10.1007/s00420-018-1320-9

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