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Restraint stress of male mice triggers apoptosis in spermatozoa and spermatogenic cells via activating the TNF-α system

Published online by Cambridge University Press:  14 January 2020

Jie Zhang ,
De-Ling Kong ,
Bin Xiao ,
Hong-Jie Yuan ,
Qiao-Qiao Kong ,
Xiao Han ,
Ming-Jiu Luo  and
Jing-He Tan Open the ORCID record for Jing-He Tan [Opens in a new window]
Jie Zhang
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
De-Ling Kong
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Bin Xiao
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Hong-Jie Yuan
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Qiao-Qiao Kong
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Xiao Han
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Ming-Jiu Luo*
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
Jing-He Tan*
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City271018, People’s Republic of China
*
Author for correspondence: Jing-He Tan or Ming-Jiu Luo, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai-an City, Shandong Province271018, People’s Republic of China. Tel: +86 538 8249616. Fax: +86 538 8241419. E-mail: tanjh@sdau.edu.cn or luo9616@163.com
Author for correspondence: Jing-He Tan or Ming-Jiu Luo, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai-an City, Shandong Province271018, People’s Republic of China. Tel: +86 538 8249616. Fax: +86 538 8241419. E-mail: tanjh@sdau.edu.cn or luo9616@163.com
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Summary

Studies have indicated that psychological stress impairs human fertility and that various stressors can induce apoptosis of testicular cells. However, the mechanisms by which psychological stress on males reduces semen quality and stressors induce apoptosis in testicular cells are largely unclear. Using a psychological (restraint) stress mouse model, we tested whether male psychological stress triggers apoptosis of spermatozoa and spermatogenic cells through activating tumour necrosis factor (TNF)-α signalling. Wild-type or TNF-α−/− male mice were restrained for 48 h before examination for apoptosis and expression of TNF-α and TNF receptor 1 (TNFR1) in spermatozoa, epididymis, seminiferous tubules and spermatogenic cells. The results showed that male restraint significantly decreased fertilization rate and mitochondrial membrane potential, while increasing levels of malondialdehyde, active caspase-3, TNF-α and TNFR1 in spermatozoa. Male restraint also increased apoptosis and expression of TNF-α and TNFR1 in caudae epididymides, seminiferous tubules and spermatogenic cells. Sperm quality was also significantly impaired when spermatozoa were recovered 35 days after male restraint. The restraint-induced damage to spermatozoa, epididymis and seminiferous tubules was significantly ameliorated in TNF-α−/− mice. Furthermore, incubation with soluble TNF-α significantly reduced sperm motility and fertilizing potential. Taken together, the results demonstrated that male psychological stress induces apoptosis in spermatozoa and spermatogenic cells through activating the TNF-α system and that the stress-induced apoptosis in spermatogenic cells can be translated into impaired quality in future spermatozoa.

Keywords

ApoptosisPsychological stressSemen qualitySpermatogenesisTNF-α signalling
Type
Research Article
Information
Zygote , Volume 28 , Issue 2 , April 2020 , pp. 160 - 169
Copyright
© Cambridge University Press 2020

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Footnotes

*

Jie Zhang and De-Ling Kong contributed equally to this work.

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