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Impact of a gestational exposure to diesel exhaust on offspring gonadal development: experimental study in the rabbit

Published online by Cambridge University Press:  18 June 2018

M. Bourdon
Affiliation:
UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy-en-Josas, France Sorbonne Paris Cité, Faculté de Médecine, Assistance Publique–Hôpitaux de Paris (AP–HP), Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire (CHU) Cochin, Department of Gynaecology Obstetrics and Reproductive Medicine 53, Université Paris Descartes, Paris, France
L. Torres-Rovira
Affiliation:
UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy-en-Josas, France
D. Monniaux
Affiliation:
UMR PRC, INRA, CNRS, Université de Tours, IFCE, Nouzilly, France
C. Faure
Affiliation:
Biologie de la Reproduction – CECOS, Hôpital Tenon, Assistance Publique–Hôpitaux de Paris (AP–HP), Paris, France UMR_S 938 CDR-Saint-Antoine, Faculté de Médecine, Sorbonne Universités UPMC Paris 6, Paris, France
R. Levy
Affiliation:
Biologie de la Reproduction – CECOS, Hôpital Tenon, Assistance Publique–Hôpitaux de Paris (AP–HP), Paris, France UMR_S 938 CDR-Saint-Antoine, Faculté de Médecine, Sorbonne Universités UPMC Paris 6, Paris, France
A. Tarrade
Affiliation:
UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy-en-Josas, France
D. Rousseau-Ralliard
Affiliation:
UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy-en-Josas, France
P. Chavatte-Palmer
Affiliation:
UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy-en-Josas, France PremUp Foundation, Paris, France
G. Jolivet*
Affiliation:
UMR BDR, INRA, ENVA, Université Paris Saclay, Jouy-en-Josas, France
*
Address for correspondence: G. Jolivet, UMR BDR, INRA, ENVA, Université Paris Saclay, 78350, Jouy-en-Josas, France. E-mail: [email protected]

Abstract

The aim of the present work was to address experimentally the possible impact of exposure to air pollution during gestation on the differentiation and function of the gonads of the offspring using a rabbit model. Rabbits were exposed daily to diluted diesel exhaust gas or filtered air from the 3rd until the 27th day of gestation, during which time germ cells migrate in genital ridges and divide, and fetal sex is determined. Offspring gonads were collected shortly before birth (28th day of gestation) or after puberty (7.5 months after birth). The structure of the gonads was analyzed by histological and immunohistological methods. Serum concentrations of testosterone and anti-Müllerian hormone were determined using ELISA. The morphology and the endocrine function of the gonads collected just at the arrest of the exposure were similar in polluted and control animals in both sexes. No differences were observed as well in gonads collected after puberty. Sperm was collected at the head of the epididymis in adults. Sperm motility and DNA fragmentation were measured. Among all parameters analyzed, only the sperm DNA fragmentation rate was increased three-fold in exposed males. Mechanisms responsible for these modifications and their physiological consequences are to be further clarified.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

1. Pascal, M, Corso, M, Chanel, O, et al. Assessing the public health impacts of urban air pollution in 25 European cities: results of the Aphekom project. Sci Total Environ. 2013; 449, 390400.Google Scholar
2. IARC Working Group. Outdoor Air Pollution. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 2016; p. 109. Lyon: FR.Google Scholar
3. Donaldson, K, Tran, L, Jimenez, L, et al. Combustion-derived nanoparticles: a review of their toxicology following inhalation exposure. Part Fibre Toxicol. 2005; 2, 14. https://doi.org/10.1186/1743-8977-1182-1110.Google Scholar
4. Kelly, F, Fussell, J. Air pollution and public health: emerging hazards and improved understanding of risk. Environ Geochem Health. 2015; 37, 631649.Google Scholar
5. Rubes, J, Selevan, S, Evenson, D, et al. Episodic air pollution is associated with increased DNA fragmentation in human sperm without other changes in semen quality. Hum Reprod. 2005; 20, 27762783.Google Scholar
6. Guven, A, Kayikci, A, Cam, K, et al. Alterations in semen parameters of toll collectors working at motorways: does diesel exposure induce detrimental effects on semen? Andrologia. 2008; 40, 346351.Google Scholar
7. Hammoud, A, Carrell, D, Gibson, M, et al. Decreased sperm motility is associated with air pollution in Salt Lake City. Fertil Steril. 2010; 93, 18751879.Google Scholar
8. Radwan, M, Jurewicz, J, Sobala, W, et al. Human sperm aneuploidy after exposure to polycyclic aromatic hydrocarbons. Reprod Fert Develop. 2016; 28, 13761381.Google Scholar
9. Frutos, V, González-Comadrán, M, Solà, I, et al. Impact of air pollution on fertility: a systematic review. Gynecol Endocrinol. 2015; 31, 713.Google Scholar
10. Nieuwenhuijsen, M, Basagaña, X, Dadvand, P, et al. Air pollution and human fertility rates. Environ Int. 2014; 70, 914.Google Scholar
11. Bowles, J, Koopman, P. Sex determination in mammalian germ cells: extrinsic versus intrinsic factors. Reproduction. 2010; 139, 943958.Google Scholar
12. She, Z-Y, Yang, W-X. Molecular mechanisms involved in mammalian primary sex determination. J Mol Endocrinol. 2014; 53, R21R37.Google Scholar
13. Slama, R, Thiebaugeorges, O, Goua, V, et al. Maternal personal exposure to airborne benzene and intrauterine growth. Environ Health Perspect. 2009; 117, 13131321.Google Scholar
14. Rahmalia, A, Giorgis-Allemand, L, Lepeule, J, et al. Pregnancy exposure to atmospheric pollutants and placental weight: an approach relying on a dispersion model. Environ Int. 2012; 48, 4755.Google Scholar
15. Fowler, P, Childs, A, Courant, F, et al. In utero exposure to cigarette smoke dysregulates human fetal ovarian developmental signalling. Hum Reprod. 2014; 29, 14711489.Google Scholar
16. Hansen, C, Luben, T, Sacks, J, et al. The effect of ambient air pollution on sperm quality. Environ Health Perspect. 2010; 118, 203209.Google Scholar
17. Ono, N, Oshio, S, Niwata, Y, et al. Prenatal exposure to diesel exhaust impairs mouse spermatogenesis. Inhal Toxicol. 2007; 19, 275281.Google Scholar
18. Li, C, Taneda, S, Taya, K, et al. Effects of in utero exposure to nanoparticle-rich diesel exhaust on testicular function in immature male rats. Toxicol Lett. 2009; 185, 18.Google Scholar
19. Kubo-Irie, M, Oshio, S, Niwata, Y, et al. Pre- and postnatal exposure to low-dose diesel exhaust impairs murine spermatogenesis. Inhal Toxicol. 2011; 23, 805813.Google Scholar
20. Ema, M, Naya, M, Horimoto, M, Kato, H. Developmental toxicity of diesel exhaust: a review of studies in experimental animals. Reprod Toxicol. 2013; 42, 117.Google Scholar
21. Veras, M, Damaceno-Rodrigues, N, Guimarães Silva, R, et al. Chronic exposure to fine particulate matter emitted by traffic affects reproductive and fetal outcomes in mice. Environ Res. 2009; 109, 536543.Google Scholar
22. Ogliari, K, Lichtenfels, A, de Marchi, MR, et al. Intrauterine exposure to diesel exhaust diminishes adult ovarian reserve. Fertil Steril. 2013; 99, 16811688.Google Scholar
23. Watanabe, N, Kurita, M. The masculinization of the fetus during pregnancy due to inhalation of diesel exhaust. Environ Health Perspect. 2001; 109, 111119.Google Scholar
24. Camlin N, Sobinoff A, Sutherland J, et al. Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model. Biol Reprod. 2016; 94, 39, 31–12.Google Scholar
25. Camlin, N, Jarnicki, A, Vanders, R, et al. Grandmaternal smoke exposure reduces female fertility in a murine model, with great-grandmaternal smoke exposure unlikely to have an effect. Hum Reprod. 2017; 32, 12701281.Google Scholar
26. Watanabe, N. Decreased number of sperms and Sertoli cells in mature rats exposed to diesel exhaust as fetuses. Toxicol Lett. 2005; 155, 5158.Google Scholar
27. Mackenzie, K, Angevine, D. Infertility in mice exposed in utero to benzo (a) pyrene. Biol Reprod. 1981; 24, 183191.Google Scholar
28. Foote, R, Carney, E. The rabbit as a model for reproductive and developmental toxicity studies. Reprod Toxicol. 2000; 14, 477493.Google Scholar
29. Fischer, B, Chavatte-Palmer, P, Viebahn, C, Navarrete Santos, A, Duranthon, V. Rabbit as a reproductive model for human health. Reproduction. 2012; 144, 110.Google Scholar
30. US EPA. Teratologic Effects of Long Term Exposure to Diesel Exhaust Emissions in Rabbits, EPA-600/1-80-011, 1980. Washington, DC: US EPA.Google Scholar
31. Pepelko, WE, Peirano, WB. Health effects of exposure to diesel engine emissions: a summary of animal studies conducted by the US Environmental Protection Agency’s Health Effects. J Am Coll Toxicol. 1983; 2, 253306.Google Scholar
32. de Nazelle, A, Bode, O, Orjuela, JP. Comparison of air pollution exposures in active vs. passive travel modes in European cities: a quantitative review. Environ Int. 2017; 99, 151160.Google Scholar
33. Daniel-Carlier, N, Harscoët, E, Thépot, D, et al. Gonad differentiation in the rabbit: evidence of species-specific features. PLoS ONE. 2013; 8, e60451.Google Scholar
34. Chretien, FC. Etude de l’origine, de la migration et de la multiplication des cellules germinales chez l’embryon de lapin. J Embryol Exp Morphol. 1966; 16, 591607.Google Scholar
35. Valentino, SA, Tarrade, A, Aioun, J, et al. Maternal exposure to diluted diesel engine exhaust alters placental function and induces intergenerational effects in rabbits. Part Fibre Toxicol. 2016; 13, 39.Google Scholar
36. Lundy, T, Smith, P, O’Connel, A, Hudson, NL, McNatty, KP. Populations of granulosa cells in small follicles of the sheep ovary. J Reprod Fertil. 1999; 115, 251262.Google Scholar
37. Bodensteiner, K, Sawyer, H, Moeller, C, et al. Chronic exposure to dibromoacetic acid, a water disinfection byproduct, diminishes primordial follicle populations in the rabbit. Toxicol Sci. 2004; 80, 8391.Google Scholar
38. Dupont, C, Ralliard-Rousseau, D, Tarrade, A, et al. Impact of maternal hyperlipidic hypercholesterolaemic diet on male reproductive organs and testosterone concentration in rabbits. J Dev Orig Health Dis. 2014; 5, 183188.Google Scholar
39. World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th edn, 2010. Cambridge University Press: Cambridge.Google Scholar
40. Rico, C, Drouilhet, L, Salvetti, P, et al. Determination of anti-Müllerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm. Reprod Fertil Dev. 2012; 24, 932944.Google Scholar
41. Maga, G, Hübscher, U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci. 2003; 116, 30513060.Google Scholar
42. Rogakou, EP, Pilch, DR, Orr, AH, Ivanova, VS, Bonner, WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 1998; 273, 58585868.Google Scholar
43. Mahadevaiah, SK, Turner, JMA, Baudat, Fdr, et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet. 2001; 27, 271276.Google Scholar
44. Monniaux D, Clément F, Dalbiès-Tran R, et al. The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link? Biol Reprod. 2014; 90, 85, 81–11.Google Scholar
45. Younglai, EV, Moor, BC, Dimond, P. Effects of sexual activity on luteinizing hormone and testosterone levels in the adult male rabbit. J Endocrinol. 1976; 69, 183191.Google Scholar
46. Theau-Clément, M, Bolet, G, Sanchez, A, Saleil, G, Brun, J. Some factors that influence semen characteristics in rabbits. Anim Reprod Sci. 2015; 157, 3338.Google Scholar
47. Sakkas, D, Alvarez, J. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010; 93, 10271036.Google Scholar
48. Bungum, M, Bungum, L, Giwercman, A. Sperm chromatin structure assay (SCSA): a tool in diagnosis and treatment of infertility. Asian J Androl. 2011; 13, 6975.Google Scholar
49. Rathke, C, Baarends, WM, Awe, S, Renkawitz-Pohl, R. Chromatin dynamics during spermiogenesis. Biochim Biophs Acta. 2014; 1839, 155168.Google Scholar
50. Evgeni, E, Lymberopoulos, G, Touloupidis, S, Asimakopoulos, B. Sperm nuclear DNA fragmentation and its association with semen quality in Greek men. Andrologia. 2015; 47, 11661174.Google Scholar
51. Gunes, S, Al-Sadaan, M, Agarwal, A. Spermatogenesis, DNA damage and DNA repair mechanisms in male infertility. Reprod Biomed Online. 2015; 31, 309319.Google Scholar
52. Manke, A, Wang, L, Rojanasakul, Y. Mechanisms of nanoparticle-induced oxidative stress and toxicity. BioMed Research Int. 2013; 2013, 942916.Google Scholar
53. Aitken, JR, Baker, MA, Sawyer, D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod Biomed Online. 2003; 7, 6570.Google Scholar
54. Drost, JB, Lee, WR. Biological basis of germline mutation: comparisons of spontaneous germline mutation rates among drosophila, mouse, and human. Environ Mol Mutagen. 1995; 25, 4864.Google Scholar
55. Russel, WL, Brauch Russel, L, Kelly, EM. Radiation dose rate and mutation frequency. Science. 1958; 128, 15461550.Google Scholar
56. Meseguer, M, Santiso, R, Garrido, N, et al. Effect of sperm DNA fragmentation on pregnancy outcome depends on oocyte quality. Fertil Steril. 2011; 95, 124128.Google Scholar
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