Cui Xuefan, Chen Lu, Tao Binbin, Zhang Xiya, Song Yanlong, Chen Ji, Duan Ming, Li Weiwei, Chen Kuangxin, Pei Yang, Hu Xuerui, Feng Ke, Luo Daji, Luo Hongrui, Qiao Zhixian, Zhou Fang, Zhu Zuoyan, Trudeau Vance L, Hu Wei
State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology, Chinese Academy of Sciences, Hubei Hongshan Laboratory, Wuhan, 430072, China.
College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China.
Sci China Life Sci. 2025 May 8. doi: 10.1007/s11427-025-2917-5.
Olfactory activation of neuroendocrine pathways plays vital roles in many organisms for reproduction and survival. The importance of gonadotropin-releasing hormone (GnRH) neurons for reproduction is well-established but little is known about whether they can directly sense and transmit sex pheromone signals. We have uncovered the migration path and distribution pattern of a new GnRH neuronal population that fulfills this role. GnRH3 neurons arise from the region located beneath olfactory placode, undergo bidirectional migration along the olfactory nerve, and cell bodies lie within the olfactory epithelium, olfactory bulb and hypothalamus. These olfactory epithelial GnRH3 neurons express ora4, the olfactory receptor that detects pheromones. GnRH3-OB neurons with olfactory epithelial GnRH3 neurons ablation failed to respond to the waterborne post-ovulatory sex pheromone prostaglandin F (PGF). GnRH3 neurons in gnrh3 mutants have a reduced basal firing rate leading to abnormal responses to PGF. Male gnrh3 zebrafish exhibit deficiencies in courtship behavior and a decreased capacity to compete and spawn with females. These findings indicate that GnRH3-OE neurons function as crypt sensory neurons transducing sex pheromone-encoded information critical to reproductive success.
神经内分泌途径的嗅觉激活在许多生物体的繁殖和生存中起着至关重要的作用。促性腺激素释放激素（GnRH）神经元对繁殖的重要性已得到充分证实，但对于它们是否能直接感知并传递性信息素信号却知之甚少。我们发现了一个承担此功能的新GnRH神经元群体的迁移路径和分布模式。GnRH3神经元起源于嗅基板下方的区域，沿嗅神经进行双向迁移，其细胞体位于嗅上皮、嗅球和下丘脑内。这些嗅上皮GnRH3神经元表达ora4，即检测信息素的嗅觉受体。嗅觉上皮GnRH3神经元被切除后，GnRH3-OB神经元对水性排卵后性信息素前列腺素F（PGF）不再有反应。gnrh3突变体中的GnRH3神经元基础放电率降低，导致对PGF的反应异常。雄性gnrh3斑马鱼在求偶行为上存在缺陷，与雌性交配和产卵的能力下降。这些发现表明，GnRH3-OE神经元作为隐性感官神经元，转导对繁殖成功至关重要的性信息素编码信息。
