Division of Biomedical Sciences, School of Medicine, University of California, Riverside, Riverside, California 92521.
Centre for Neuroendocrinology, and Department of Physiology, School of Biomedical Sciences, University of Otago, Dunedin 9054, New Zealand.
J Neurosci. 2024 Jul 10;44(28):e0222242024. doi: 10.1523/JNEUROSCI.0222-24.2024.
Obesity is associated with hypogonadism in males, characterized by low testosterone and sperm number. Previous studies determined that these stem from dysregulation of hypothalamic circuitry that regulates reproduction, by unknown mechanisms. Herein, we used mice fed chronic high-fat diet, which mimics human obesity, to determine mechanisms of impairment at the level of the hypothalamus, in particular gonadotropin-releasing hormone (GnRH) neurons that regulate luteinizing hormone (LH), which then regulates testosterone. Consistent with obese humans, we demonstrated lower LH, and lower pulse frequency of LH secretion, but unchanged pituitary responsiveness to GnRH. LH pulse frequency is regulated by pulsatile GnRH secretion, which is controlled by kisspeptin. Peripheral and central kisspeptin injections, and DREADD-mediated activation of kisspeptin neurons, demonstrated that kisspeptin neurons were suppressed in obese mice. Thus, we investigated regulators of kisspeptin secretion. We determined that the LH response to NMDA was lower in obese mice, corresponding to fewer glutamate receptors in kisspeptin neurons, which may be critical for kisspeptin synchronization. Given that kisspeptin neurons also interact with anorexigenic POMC neurons, which are affected by obesity, we examined their cross talk, and determined that the LH response to either DREADD-mediated activation of POMC neurons or central injection of αMSH, a product of POMC, is abolished in obese mice. This was accompanied by diminished levels of αMSH receptor, MC4R, in kisspeptin neurons. Together, our studies determined that obesity leads to the downregulation of receptors that regulate kisspeptin neurons, which is associated with lower LH pulse frequency, leading to lower LH and hypogonadism.
肥胖与男性的性腺功能减退症有关,其特征是睾丸激素和精子数量低。先前的研究确定,这些是由调节生殖的下丘脑回路失调引起的,但具体机制尚不清楚。在此,我们使用模拟人类肥胖的慢性高脂肪饮食喂养的小鼠,以确定在下丘脑水平上受损的机制,特别是调节黄体生成素 (LH) 的促性腺激素释放激素 (GnRH) 神经元,LH 继而调节睾丸激素。与肥胖的人类一致,我们证明了 LH 降低,LH 分泌的脉冲频率降低,但对 GnRH 的垂体反应不变。LH 脉冲频率受脉冲 GnRH 分泌调节,而脉冲 GnRH 分泌受 kisspeptin 控制。外周和中枢 kisspeptin 注射以及 DREADD 介导的 kisspeptin 神经元激活表明,肥胖小鼠的 kisspeptin 神经元受到抑制。因此,我们研究了 kisspeptin 分泌的调节剂。我们确定,肥胖小鼠对 NMDA 的 LH 反应较低,对应于 kisspeptin 神经元中的谷氨酸受体减少,这对于 kisspeptin 同步可能至关重要。鉴于 kisspeptin 神经元还与受肥胖影响的厌食 POMC 神经元相互作用,我们检查了它们的串扰,并确定对 POMC 神经元的 DREADD 介导的激活或 POMC 的产物 αMSH 的中枢注射的 LH 反应在肥胖小鼠中被消除。这伴随着 kisspeptin 神经元中 αMSH 受体 MC4R 的水平降低。总之,我们的研究确定,肥胖导致调节 kisspeptin 神经元的受体下调,这与较低的 LH 脉冲频率有关,导致 LH 降低和性腺功能减退症。