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The Effects of Chronic Lead Exposure on Testicular Development of Japanese Quail (Coturnix japonica): Histopathological Damages, Oxidative Stress, Steroidogenesis Disturbance, and Hypothalamus-Pituitary-Testis Axis Disruption

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Abstract

Lead (Pb) becomes a global public health concern for its high toxicology. Birds are sensitive to environmental pollution and Pb contamination exerts multiple negative influences on bird life. Pb also impacts on avian reproductive system. Thus, in this study, we attempted to determine toxicological effects and possible mechanistic pathways of Pb on avian testicular development by using the model species—Japanese quail (Coturnix japonica). Male quail chicks of 1-week-old were exposed to 0, 50, 500, and 1000 ppm Pb concentrations in drinking water for 5 weeks when reaching sexual maturation. The results showed that high Pb doses (500 and 1000 ppm) induced testis atrophy and cloacal gland shrinkage. Microstructural damages of both hypothalamus and testis indicated the disruption of the hypothalamus-pituitary–gonadal (HPG) axis by Pb exposure. The decrease of gonadotropin-releasing hormone (GnRH), luteinizing hormone (LH) and follicle-stimulating hormone (FSH) and testosterone (T) may also imply HPG axis disruption. Moreover, excess testicular oxidative damages featured by increasing reactive oxygen species (ROS) and malondialdehyde (MDA) and decreasing catalase (CAT), glutathione (GSH), superoxide dismutase (SOD), glutathione-S-transferase (GST), and total antioxidant capacity (T-AOC) indicated increasing risks of reproductive dysfunction by Pb. Furthermore, increasing apoptosis and upregulation of gene expression associated with cell death suggested testicular abnormal development. In addition, molecular signaling involved with steroidogenesis in the testis was disturbed by Pb treatment. The study showed that Pb could impair testicular development and reproductive function by morphological and histological injury, hormone suppression, oxidative stress, cell death, and HPG axis disruption.

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Data Availability

Data are available from the corresponding author on reasonable request.

Abbreviations

AR:

Androgen receptors

AST:

Cross-sectional area of the seminiferous tubules

Bcl-2:

B-cell lymphoma-2

CAT:

Catalase

Casp-3:

Caspase-3

Casp-9:

Caspase-9

Cyt-c:

Cytochrome c

DAX-1:

Dosage-sensitive sex reversal adrenal hypoplasia congenita critical region on the X chromosome, gene 1

FSH:

Follicle stimulating hormone

FSHR:

Follicle-stimulating hormone receptor

FCR:

Feed conversion ratio

GSH:

Glutathione

GST:

Glutathione-S-transferase

HPG axis:

Hypothalamus-pituitary–gonadal axis

GnRH:

Gonadotropin-releasing hormone

IL-1β:

Interleukin 1 beta

LH:

Luteinizing hormone

LHR:

Luteinizing hormone receptor

MDA:

Malondialdehyde

NF-κB:

Nuclear factor kappa B

TNF-α:

Tumor necrosis factor alpha

P450scc:

Cytochrome P450 side-chain cleavage enzyme

P450c17:

Cytochrome P450 17α-hydroxylase/17,20-lyase

ROS:

Reactive oxygen species

SET:

Seminiferous epithelial thickness

SF-1:

Steroidogenic factor 1

SLD:

Seminiferous luminal diameter

SOD:

Superoxide dismutase

StAR:

Steroidogenic acute regulatory protein

STD:

Seminiferous tubular diameter

T:

Testosterone

T-AOC:

Total antioxidant capacity

3β-HSD:

3β-Hydroxysteroid dehydrogenase

17β-HSD:

17β-Hydroxysteroid dehydrogenase

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Acknowledgements

We are grateful for Ms. Yuhan Fang for experimental assistance and for Ms. Xuan Li, Ling Wang, and Gaixia Zhang for valuable suggestions about the manuscript.

Funding

The study was supported by the National Natural Science Foundation of China (No. 33372201).

Author information

Authors and Affiliations

  1. College of Life Sciences, Shaanxi Normal University, No. 620, West Chang’an Avenue, Chang’an District, Xi’an, Shaanxi, 710119, People’s Republic of China

    Ying Zheng, Qingyu Zhang, Lingyang Jing, Yifan Fei & Hongfeng Zhao

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  1. Ying Zheng
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  2. Qingyu Zhang
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  3. Lingyang Jing
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  4. Yifan Fei
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  5. Hongfeng Zhao
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Contributions

Zheng Y: Conceptualization, Methodology, Data curation, Writing-Original draft preparation; Zhang QY, Jing LY, and Fei YF: Data curation, Visualization, and Software; Zhao HF: Conceptualization, Methodology, Writing-Original draft preparation, Supervision; All authors reviewed the manuscript.

Corresponding author

Correspondence to Hongfeng Zhao.

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Ethics Approval

Animal care and experiment operations were approved and conducted in accordance with the Animal Care Guidelines of Shaanxi Normal University (No. SNNU52).

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The authors declare no competing interests.

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Supplementary Information

Fig. S1.

Cloacal glands of quails in different Pb-treated groups. (A) control; (B) 50 ppm; (C) 500 ppm; (D) 1000 ppm. (PNG 5136 kb)

High resolution image (TIF 42934 kb)

Table S1

Primer sequences used in RT-PCR analysis for genes expression of male Japanese quails. (DOCX 17 kb)

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Zheng, Y., Zhang, Q., Jing, L. et al. The Effects of Chronic Lead Exposure on Testicular Development of Japanese Quail (Coturnix japonica): Histopathological Damages, Oxidative Stress, Steroidogenesis Disturbance, and Hypothalamus-Pituitary-Testis Axis Disruption. Biol Trace Elem Res 201, 3446–3460 (2023). https://doi.org/10.1007/s12011-022-03436-8

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