Human populations living in urban industrial regions of developed countries are exposed to high levels of environmental pollutants. The reproductive consequences of the exposure to air pollution can be monitored through semen analysis and molecular methods. In this study, we tested the possible impact of seasonal changes in the level of air pollution on the semen quality and sperm DNA methylation of 24 men living and working in the industrial agglomeration of Ostrava (Czech Republic). The study participants were healthy non-smokers. The study group was homogeneous regarding their profession, moderate alcohol consumption, no drug abuse and no additional exposure to chemical toxicants. We performed targeted methylation next generation sequencing (NGS) using Agilent SureSelect Human Methyl-Seq and Illumina NextSeq 500 platform to analyze semen samples collected repeatedly from the same men following the season of high (winter) and low (summer) air pollution exposure. We did not detect any adverse effects of the increased exposure on the semen quality; neither we found any difference in average sperm DNA methylation between the two sampling periods. Our search for differentially methylated CpG sites did not reveal any specific CpG methylation change. Our data indicate that the seasonal changes in the level of the air pollution probably do not have any substantial effect on sperm DNA methylation of men living in the highly polluted industrial agglomeration for a long period of time.

Department of Genetics and Reproductive Biotechnologies Central European Institute of Technology Veterinary Research Institute Brno Czech Republic

Zobrazit více v PubMed

Aarabi, M., San Gabriel, M.C., Chan, D., Behan, N.A., Caron, M., Pastinen, T. et al. (2015) High-dose folic acid supplementation alters the human sperm methylome and is influenced by the MTHFR C677T polymorphism. Human Molecular Genetics, 24(22), 6301-6313. https://doi.org/10.1093/hmg/ddv338

Alkhaled, Y., Laqqan, M., Tierling, S., Lo Porto, C., Amor, H. & Hammadeh, M.E. (2018) Impact of cigarette-smoking on sperm DNA methylation and its effect on sperm parameters. Andrologia, 50, e12950. https://doi.org/10.1111/and.12950

Anton, E. & Krawetz, S.A. (2012) Spermatozoa as biomarkers for the assessment of human male infertility and genotoxicity. Systems Biology in Reproductive Medicine, 58(1), 41-50. https://doi.org/10.3109/19396368.2011.637152

Åsenius, F., Danson, A.F. & Marzi, S.J. (2020) DNA methylation in human sperm: a systematic review. Human Reproduction Update, 26(6), 841-873. https://doi.org/10.1093/humupd/dmaa025

Bind, M.-A., Lepeule, J., Zanobetti, A., Gasparrini, A., Baccarelli, A., Coull, B.A. et al. (2014) Air pollution and gene-specific methylation in the normative aging study: association, effect modification, and mediation analysis. Epigenetics, 9(3), 448-458. https://doi.org/10.4161/epi.27584

Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114-2120. https://doi.org/10.1093/bioinformatics/btu170

Carré, J., Gatimel, N., Moreau, J., Parinaud, J. & Léandri, R. (2017) Does air pollution play a role in infertility?: a systematic review. Environmental Health, 16(1), 82. https://doi.org/10.1186/s12940-017-0291-8

Cernikovsky, L., Krejci, B., Blazek, Z. & Volna, V. (2016) Transboundary air-pollution transport in the Czech-Polish border region between the cities of Ostrava and Katowice. Central European Journal of Public Health, 24, S45-S50. https://doi.org/10.21101/cejph.a4532

Consales, C., Toft, G., Leter, G., Bonde, J.P.E., Uccelli, R., Pacchierotti, F. et al. (2016) Exposure to persistent organic pollutants and sperm DNA methylation changes in Arctic and European populations. Environmental and Molecular Mutagenesis, 57(3), 200-209. https://doi.org/10.1002/em.21994

Darbandi, M., Darbandi, S., Agarwal, A., Baskaran, S., Dutta, S., Sengupta, P. et al. (2019) Reactive oxygen species-induced alterations in H19-Igf2 methylation patterns, seminal plasma metabolites, and semen quality. Journal of Assisted Reproduction and Genetics, 36(2), 241-253. https://doi.org/10.1007/s10815-018-1350-y

Denham, J., O'Brien, B.J., Harvey, J.T. & Charchar, F.J. (2015) Genome-wide sperm DNA methylation changes after 3 months of exercise training in humans. Epigenomics, 7(5), 717-731. https://doi.org/10.2217/epi.15.29

Estill, M.S. & Krawetz, S.A. (2016) The epigenetic consequences of paternal exposure to environmental contaminants and reproductive toxicants. Current Environmental Health Reports, 3(3), 202-213. https://doi.org/10.1007/s40572-016-0101-4

Hackett, J.A. & Surani, M.A. (2013) DNA methylation dynamics during the mammalian life cycle. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1609), 20110328. https://doi.org/10.1098/rstb.2011.0328

Hammoud, A., Carrell, D.T., Gibson, M., Sanderson, M., Parker-Jones, K. & Peterson, C.M. (2010) Decreased sperm motility is associated with air pollution in Salt Lake City. Fertility and Sterility, 93(6), 1875-1879. https://doi.org/10.1016/j.fertnstert.2008.12.089

Jenkins, T.G., James, E.R., Alonso, D.F., Hoidal, J.R., Murphy, P.J., Hotaling, J.M. et al. (2017) Cigarette smoking significantly alters sperm DNA methylation patterns. Andrology, 5(6), 1089-1099. https://doi.org/10.1111/andr.12416

Jiang, R., Jones, M.J., Sava, F., Kobor, M.S. & Carlsten, C. (2014) Short-term diesel exhaust inhalation in a controlled human crossover study is associated with changes in DNA methylation of circulating mononuclear cells in asthmatics. Particle and Fibre Toxicology, 11, 71. https://doi.org/10.1186/s12989-014-0071-3

Jirik, V., Machaczka, O., Miturova, H., Tomasek, I., Slachtova, H., Janoutova, J. et al. (2016) Air pollution and potential health risk in Ostrava region-a review. Central European Journal of Public Health, 24, S4-S17. https://doi.org/10.21101/cejph.a4533

Jones, M.J., Goodman, S.J. & Kobor, M.S. (2015) DNA methylation and healthy human aging. Aging Cell, 14(6), 924-932. https://doi.org/10.1111/acel.12349

Kabukçu, C., Çil, N., Turan, T., Özlülerden, Y., Çabuş, Ü. & Mete, G.A. (2020) Do seasonal variations in ambient temperature, humidity and daylight duration affect semen parameters? A retrospective analysis over eight years. Andrologia, 52(10), e13777. https://doi.org/10.1111/and.13777

Kerachian, M.A., Javadmanesh, A., Azghandi, M., Mojtabanezhad Shariatpanahi, A., Yassi, M., Shams Davodly, E. et al. (2020) Crosstalk between DNA methylation and gene expression in colorectal cancer, a potential plasma biomarker for tracing this tumor. Scientific Reports, 10(1), 2813. https://doi.org/10.1038/s41598-020-59690-0

Krueger, F. & Andrews, S.R. (2011) Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics, 27(11), 1571-1572. https://doi.org/10.1093/bioinformatics/btr167

Lafuente, R., García-Blàquez, N., Jacquemin, B. & Checa, M.A. (2016) Outdoor air pollution and sperm quality. Fertility and Sterility, 106(4), 880-896. https://doi.org/10.1016/j.fertnstert.2016.08.022

Laqqan, M., Tierling, S., Alkhaled, Y., Porto, C.L., Solomayer, E.F. & Hammadeh, M.E. (2017) Aberrant DNA methylation patterns of human spermatozoa in current smoker males. Reproductive Toxicology, 71, 126-133. https://doi.org/10.1016/j.reprotox.2017.05.010

Levitas, E., Lunenfeld, E., Weisz, N., Friger, M. & Har-Vardi, I. (2013) Seasonal variations of human sperm cells among 6455 semen samples: a plausible explanation of a seasonal birth pattern. American Journal of Obstetrics and Gynecology, 208(5), 406.e1-406.e6. https://doi.org/10.1016/j.ajog.2013.02.010

Ma, Y., Lu, Z., Wang, L. & Qiang, M. (2019) Correlation of internal exposure levels of polycyclic aromatic hydrocarbons to methylation of imprinting genes of sperm DNA. International Journal of Environmental Research and Public Health, 16(14), 2606. https://doi.org/10.3390/ijerph16142606

Mao, H., Feng, L. & Yang, W.-X. (2017) Environmental factors contributed to circannual rhythm of semen quality. Chronobiology International, 34(3), 411-425. https://doi.org/10.1080/07420528.2017.1280046

Martin, E.M. & Fry, R.C. (2018) Environmental influences on the epigenome: exposure- associated DNA methylation in human populations. Annual Review of Public Health, 39, 309-333. https://doi.org/10.1146/annurev-publhealth-040617-014629

Mayer, W., Niveleau, A., Walter, J., Fundele, R. & Haaf, T. (2000) Demethylation of the zygotic paternal genome. Nature, 403(6769), 501-502. https://doi.org/10.1038/35000656

Meng, H., Cao, Y., Qin, J., Song, X., Zhang, Q., Shi, Y. et al. (2015) DNA methylation, its mediators and genome integrity. International Journal of Biological Sciences, 11(5), 604-617. https://doi.org/10.7150/ijbs.11218

Okonechnikov, K., Conesa, A. & García-Alcalde, F. (2016) Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics, 32(2), 292-294. https://doi.org/10.1093/bioinformatics/btv566

Ooi, S.K.T., O'Donnell, A.H. & Bestor, T.H. (2009) Mammalian cytosine methylation at a glance. Journal of Cell Science, 122(16), 2787-2791. https://doi.org/10.1242/jcs.015123

Park, Y. & Wu, H. (2016) Differential methylation analysis for BS-seq data under general experimental design. Bioinformatics, 32(10), 1446-1453. https://doi.org/10.1093/bioinformatics/btw026

Pilsner, J.R., Shershebnev, A., Medvedeva, Y.A., Suvorov, A., Wu, H., Goltsov, A. et al. (2018) Peripubertal serum dioxin concentrations and subsequent sperm methylome profiles of young Russian adults. Reproductive Toxicology, 78, 40-49. https://doi.org/10.1016/j.reprotox.2018.03.007

Rubes, J., Selevan, S.G., Evenson, D.P., Zudova, D., Vozdova, M., Zudova, Z. et al. (2005) Episodic air pollution is associated with increased DNA fragmentation in human sperm without other changes in semen quality. Human Reproduction, 20(10), 2776-2783. https://doi.org/10.1093/humrep/dei122

Santi, D., Magnani, E., Michelangeli, M., Grassi, R., Vecchi, B., Pedroni, G. et al. (2018) Seasonal variation of semen parameters correlates with environmental temperature and air pollution: a big data analysis over 6 years. Environmental Pollution, 235, 806-813. https://doi.org/10.1016/j.envpol.2018.01.021

Selevan, S.G., Borkovec, L., Slott, V.L., Zudova, Z., Rubes, J., Evenson, D.P. et al. (2000) Semen quality and reproductive health of young Czech men exposed to seasonal air pollution. Environmental Health Perspectives, 108(9), 887-894.

Sharpe, R.M. (2010) Environmental/lifestyle effects on spermatogenesis. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1546), 1697-1712. https://doi.org/10.1098/rstb.2009.0206

Surani, M.A., Hayashi, K. & Hajkova, P. (2007) Genetic and epigenetic regulators of pluripotency. Cell, 128(4), 747-762. https://doi.org/10.1016/j.cell.2007.02.010

Svedova, B., Raclavska, H., Kucbel, M., Ruzickova, J., Raclavsky, K., Koliba, M. et al. (2020) Concentration variability of water-soluble ions during the acceptable and exceeded pollution in an industrial region. International Journal of Environmental Research and Public Health, 17(10), 3447. https://doi.org/10.3390/ijerph17103447

Tomaskova, H., Tomasek, I., Slachtova, H., Polaufova, P., Splichalova, A., Michalik, J. et al. (2016) PM10 air pollution and acute hospital admissions for cardiovascular and respiratory causes in Ostrava. Central European Journal of Public Health, 24(Suppl), S33-S39. https://doi.org/10.21101/cejph.a4538

Vecoli, C., Montano, L. & Andreassi, M.G. (2016) Environmental pollutants: genetic damage and epigenetic changes in male germ cells. Environmental Science and Pollution Research, 23(23), 23339-23348. https://doi.org/10.1007/s11356-016-7728-4

Wang, X., Tian, X., Ye, B., Zhang, Y., Zhang, X., Huang, S. et al. (2020) The association between ambient temperature and sperm quality in Wuhan, China. Environmental Health, 19(1), 44. https://doi.org/10.1186/s12940-020-00595-w

World Health Organization. (2010) WHO laboratory manual for the examination and processing of human semen, 5th edition. Geneva, Switzerland: World Health Organization Press.

Wu, H., Estill, M.S., Shershebnev, A., Suvorov, A., Krawetz, S.A., Whitcomb, B.W. et al. (2017) Preconception urinary phthalate concentrations and sperm DNA methylation profiles among men undergoing IVF treatment: a cross-sectional study. Human Reproduction (Oxford, England), 32(11), 2159-2169. https://doi.org/10.1093/humrep/dex283

Yauk, C., Polyzos, A., Rowan-Carroll, A., Somers, C.M., Godschalk, R.W., van Schooten, F.J. et al. (2008) Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proceedings of the National Academy of Sciences of the United States of America, 105(2), 605-610. https://doi.org/10.1073/pnas.0705896105

Zhang, J., Cai, Z., Ma, C., Xiong, J. & Li, H. (2020) Impacts of outdoor air pollution on human semen quality: a meta-analysis and systematic review. BioMed Research International, 2020, 7528901. https://doi.org/10.1155/2020/7528901