Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance
Abstract Background Energy balance is closely related to reproductive function, wherein hypothalamic kisspeptin mediates regulation of the energy balance. However, the central mechanism of kisspeptin in the regulation of male reproductive function under different energy balance states is unclear. He...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2021-01-01
|
Series: | Reproductive Biology and Endocrinology |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12958-021-00698-0 |
id |
doaj-2506b63d4ad24497987ab0de6f6df4b3 |
---|---|
record_format |
Article |
spelling |
doaj-2506b63d4ad24497987ab0de6f6df4b32021-01-24T12:10:00ZengBMCReproductive Biology and Endocrinology1477-78272021-01-0119111310.1186/s12958-021-00698-0Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balanceBo Chang0Chenglin Song1Haining Gao2Tie Ma3Tao Li4Qianhe Ma5Tingting Yao6Meng Wang7Jing Li8Xuejie Yi9Donghui Tang10Shicheng Cao11Exercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityExercise and Health Research Center/Department of Kinesiology, Shenyang Sport UniversityPE College of Beijing Normal UniversityDepartment of Sports Medicine, School of Public and Basic Sciences, China Medical UniversityAbstract Background Energy balance is closely related to reproductive function, wherein hypothalamic kisspeptin mediates regulation of the energy balance. However, the central mechanism of kisspeptin in the regulation of male reproductive function under different energy balance states is unclear. Here, high-fat diet (HFD) and exercise were used to change the energy balance to explore the role of leptin and inflammation in the regulation of kisspeptin and the hypothalamic-pituitary-testis (HPT) axis. Methods Four-week-old male C57BL/6 J mice were randomly assigned to a normal control group (n = 16) or an HFD (n = 49) group. After 10 weeks of HFD feeding, obese mice were randomly divided into obesity control (n = 16), obesity moderate-load exercise (n = 16), or obesity high-load exercise (n = 17) groups. The obesity moderate-load exercise and obesity high-load exercise groups performed exercise (swimming) for 120 min/day and 120 min × 2 times/day (6 h interval), 5 days/week for 8 weeks, respectively. Results Compared to the mice in the normal group, in obese mice, the mRNA and protein expression of the leptin receptor, kiss, interleukin-10 (IL-10), and gonadotropin-releasing hormone (GnRH) decreased in the hypothalamus; serum luteinizing hormone (LH), follicle-stimulating hormone (FSH), and testosterone levels and sperm quality decreased; and serum leptin, estradiol, and tumor necrosis factor-α (TNF-α) levels and sperm apoptosis increased. Moderate- and high-load exercise effectively reduced body fat and serum leptin levels but had the opposite effects on the hypothalamus and serum IL-10 and TNF-α levels. Moderate-load exercise had anti-inflammatory effects accompanied by increased mRNA and protein expression of kiss and GnRH in the hypothalamus and increased serum FSH, LH, and testosterone levels and improved sperm quality. High-load exercise also promoted inflammation, with no significant effect on the mRNA and protein expression of kiss and GnRH in the hypothalamus, serum sex hormone level, or sperm quality. Moderate-load exercise improved leptin resistance and inflammation and reduced the inhibition of kisspeptin and the HPT axis in obese mice. The inflammatory response induced by high-load exercise may counteract the positive effect of improving leptin resistance on kisspeptin and HPT. Conclusion During changes in energy balance, leptin and inflammation jointly regulate kisspeptin expression on the HPT axis.https://doi.org/10.1186/s12958-021-00698-0Energy balanceInflammationLeptinKisspeptinHypogonadotropic hypogonadism |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Bo Chang Chenglin Song Haining Gao Tie Ma Tao Li Qianhe Ma Tingting Yao Meng Wang Jing Li Xuejie Yi Donghui Tang Shicheng Cao |
spellingShingle |
Bo Chang Chenglin Song Haining Gao Tie Ma Tao Li Qianhe Ma Tingting Yao Meng Wang Jing Li Xuejie Yi Donghui Tang Shicheng Cao Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance Reproductive Biology and Endocrinology Energy balance Inflammation Leptin Kisspeptin Hypogonadotropic hypogonadism |
author_facet |
Bo Chang Chenglin Song Haining Gao Tie Ma Tao Li Qianhe Ma Tingting Yao Meng Wang Jing Li Xuejie Yi Donghui Tang Shicheng Cao |
author_sort |
Bo Chang |
title |
Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance |
title_short |
Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance |
title_full |
Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance |
title_fullStr |
Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance |
title_full_unstemmed |
Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance |
title_sort |
leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance |
publisher |
BMC |
series |
Reproductive Biology and Endocrinology |
issn |
1477-7827 |
publishDate |
2021-01-01 |
description |
Abstract Background Energy balance is closely related to reproductive function, wherein hypothalamic kisspeptin mediates regulation of the energy balance. However, the central mechanism of kisspeptin in the regulation of male reproductive function under different energy balance states is unclear. Here, high-fat diet (HFD) and exercise were used to change the energy balance to explore the role of leptin and inflammation in the regulation of kisspeptin and the hypothalamic-pituitary-testis (HPT) axis. Methods Four-week-old male C57BL/6 J mice were randomly assigned to a normal control group (n = 16) or an HFD (n = 49) group. After 10 weeks of HFD feeding, obese mice were randomly divided into obesity control (n = 16), obesity moderate-load exercise (n = 16), or obesity high-load exercise (n = 17) groups. The obesity moderate-load exercise and obesity high-load exercise groups performed exercise (swimming) for 120 min/day and 120 min × 2 times/day (6 h interval), 5 days/week for 8 weeks, respectively. Results Compared to the mice in the normal group, in obese mice, the mRNA and protein expression of the leptin receptor, kiss, interleukin-10 (IL-10), and gonadotropin-releasing hormone (GnRH) decreased in the hypothalamus; serum luteinizing hormone (LH), follicle-stimulating hormone (FSH), and testosterone levels and sperm quality decreased; and serum leptin, estradiol, and tumor necrosis factor-α (TNF-α) levels and sperm apoptosis increased. Moderate- and high-load exercise effectively reduced body fat and serum leptin levels but had the opposite effects on the hypothalamus and serum IL-10 and TNF-α levels. Moderate-load exercise had anti-inflammatory effects accompanied by increased mRNA and protein expression of kiss and GnRH in the hypothalamus and increased serum FSH, LH, and testosterone levels and improved sperm quality. High-load exercise also promoted inflammation, with no significant effect on the mRNA and protein expression of kiss and GnRH in the hypothalamus, serum sex hormone level, or sperm quality. Moderate-load exercise improved leptin resistance and inflammation and reduced the inhibition of kisspeptin and the HPT axis in obese mice. The inflammatory response induced by high-load exercise may counteract the positive effect of improving leptin resistance on kisspeptin and HPT. Conclusion During changes in energy balance, leptin and inflammation jointly regulate kisspeptin expression on the HPT axis. |
topic |
Energy balance Inflammation Leptin Kisspeptin Hypogonadotropic hypogonadism |
url |
https://doi.org/10.1186/s12958-021-00698-0 |
work_keys_str_mv |
AT bochang leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT chenglinsong leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT haininggao leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT tiema leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT taoli leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT qianhema leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT tingtingyao leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT mengwang leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT jingli leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT xuejieyi leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT donghuitang leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance AT shichengcao leptinandinflammatoryfactorsplayasynergisticroleintheregulationofreproductioninmalemicethroughhypothalamickisspeptinmediatedenergybalance |
_version_ |
1724326270263623680 |