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. 2018 Mar 1;162(1):318-326.
doi: 10.1093/toxsci/kfx261.

Exposure to Concentrated Ambient PM2.5 Compromises Spermatogenesis in a Mouse Model: Role of Suppression of Hypothalamus-Pituitary-Gonads Axis

Lianglin Qiu  1   2 , Minjie Chen  1   3 , Xiaoke Wang  1   2 , Xiaobo Qin  1   4 , Sufang Chen  1   5 , Yingyun Qian  2 , Zhenzhen Liu  2 , Qi Cao  6 , Zhekang Ying  1   3
Affiliations

Exposure to Concentrated Ambient PM2.5 Compromises Spermatogenesis in a Mouse Model: Role of Suppression of Hypothalamus-Pituitary-Gonads Axis

Lianglin Qiu et al. Toxicol Sci. .

Abstract

Epidemiological studies link ambient fine particulate matter (PM2.5) pollution to abnormalities in the male reproductive system. However, few toxicological studies have investigated this potentially important adverse effect of PM2.5 pollution. Therefore, in the present study, we analyzed the effects of PM2.5 exposure on spermatogenesis and hypothalamic-pituitary-gonadal (HPG) axis in a murine model. Fourteen male C57BL/6J mice were subjected to a 4-month exposure to filtered air or concentrated ambient PM2.5 (CAP). Their sperm count, testicular histology, spermatogenic parameters, and the major components of HPG axis were assessed. Exposure to CAP significantly reduced sperm count in the epididymis. This was accompanied by Sertoli cell vacuolization, immature germ cell dislocation, and decreases in pachytene spermatocytes and round spermatids of stage VII seminiferous tubules, suggesting a marked impairment of spermatogenesis in these mice. This impairment of spermatogenesis appeared to be attributable to a suppression of HPG axis subsequent to CAP exposure-induced hypothalamic inflammation, as exposure to CAP significantly increased TNFα and IL1b mRNA levels and meanwhile decreased gonadotropin-releasing hormone mRNA expression in the hypothalamus. Moreover, CAP exposure significantly reduced circulating testosterone and follicle-stimulating hormone, testicular testosterone and mRNA expression of follicle-stimulating hormone target gene SHBG and luteinizing hormone target genes P450scc, 17βHSD, and StAR. The present data demonstrate that exposure to ambient PM2.5 impairs spermatogenesis in murine model, raising the concern over effects of ambient PM2.5 pollution on the male reproductive function.

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Figures

Figure 1.
Figure 1.
The effects of CAP exposure on sperm count and organ coefficients. A, Organ coefficient of testis. B, Organ coefficient of epididymis. C, Sperm count. D, Abnormal sperm morphology. A–D, Abnormal sperm head; e: normal sperm; f–m: abnormal sperm; n–q: abnormal sperm tail. E, Normal sperm rate. Bar: 20 μm. The data are expressed as the mean ± SD. n = 7 per group. *p<.05, compared with FA-treated group.
Figure 2.
Figure 2.
The effects of CAP exposure on testicular histology. A, A stage VII seminiferous tubule morphology in testis in control group. B, A stage VII seminiferous tubule morphology in testis in CAP-treated group. C, The magnification image of the selected area from (A). D, The magnification image of the selected area from (B). Black arrow head: immature germ cells. Asterisk: Sertoli cell vacuolization. n = 7 per group. Bar in the upper panel: 100 μm. Bar in the lower panel: 20 μm.
Figure 3.
Figure 3.
The effects of CAP exposure on spermatogenetic parameters. A, Seminiferous tubules diameter. B, Epithelial height. C, Ratio of seminiferous tubules diameter/epithelial height. D, The number of Sertoli cell per stage VII seminiferous tubule. E, The number of spermatogonias per stage VII seminiferous tubule. F, The number of pachytene spermatocyte per stage VII seminiferous tubule. G, The number of round spermatid per stage VII seminiferous tubule. H, The ratio of spermatogonias/Sertoli cell per stage VII seminiferous tubule. I, The ratio of pachytene spermatocyte/Sertoli cell per stage VII seminiferous tubule. J, The ratio of pachytene round spermatid/Sertoli cell per stage VII seminiferous tubule. K, The ratio of total germ cell/Sertoli cell per stage VII seminiferous tubule. The data are expressed as the mean ± SD. n = 7 per group. *p<.05, **p<.01, compared with FA-treated group.
Figure 4.
Figure 4.
The effects of CAP exposure on count of Tra98 or CREM1 positive cells. A, Tra98 positive cells in seminiferous tubule. B, The count of Tra98 positive cells per seminiferous tubule. C, CREM1 positive cells in seminiferous tubule. B, The count of CREM1 positive cells per seminiferous tubule. The data are expressed as the mean ± SD. n = 7 per group. Bar: 100 μm. **p<.01, compared with FA-treated group.
Figure 5.
Figure 5.
The effects of CAP exposure on reproductive related hormones. A, Serum FSH. B, Serum T. C, Serum E2. D, Testicular FSH. E, Testicular T. F, Testicular E2. The data are expressed as the mean ± SD, n = 7 per group. *p<.05, compared with FA-treated group.
Figure 6.
Figure 6.
The effects of CAP exposure on the expressions of testosterone synthesis and function related genes. A, AR. B, P450scc C, CYP17α. D, P450arom. E, 17βHSD. F, 3βHSD. G, StAR. H, SHBG. The data are expressed as the mean ± SD. n = 7 per group. *p<.05, **p<.01, compared with FA-treated group.
Figure 7.
Figure 7.
The effects of CAP exposure on the hypothalamic mRNA expressions of GnRH and inflammatory biomarkers. A, TNFα. B, IL-1β. C, IL-6. The data are expressed as the mean ± SD. n = 7 per group. *p<.05, compared with FA-treated group.
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