Zhang Yu Ting, Liu Dong Teng, Zhu Yong, Chen Shi Xi, Hong Wan Shu
College of Ocean and Earth Sciences, Xiamen University, Fujian 361005, PR China.
College of Ocean and Earth Sciences, Xiamen University, Fujian 361005, PR China; Department of Biology, Howell Science Complex, East Carolina University, 1000 E, 5th Street, Greenville, NC 27858-4553, USA.
Gen Comp Endocrinol. 2016 May 1;230-231:87-102. doi: 10.1016/j.ygcen.2016.03.029. Epub 2016 Mar 24.
Our previous studies suggested that 17α,20β-dihydroxy-4-pregnen-3-one (DHP), an oocyte maturation inducing progestin, also acts as a sex pheromone in Chinese black sleeper Bostrichthys sinensis, a fish species that inhabits intertidal zones and mates and spawns inside a muddy burrow. The electro-olfactogram response to DHP increased during the breeding season. In the present study, we cloned the cDNAs of the nine progestin receptors (pgr, paqr5, 6, 7(a, b), 8, 9, pgrmc1, 2) from B. sinensis, analyzed their tissue distribution, and determined the expression in the olfactory rosette during the reproductive cycle in female and male fish. The deduced amino acid sequences of the nine progestin receptors share high sequence identities with those of other fish species and relatively lower homology with their mammalian counterparts, and phylogenetic analyses classified the nine B. sinensis progestin receptors into their respective progestin receptor groups. Tissue distribution of B. sinensis progestin receptors showed differential expression patterns, but all these nine genes were expressed in the olfactory rosette. Interestingly, paqr5 mRNA was found in the intermediate and basal parts of the olfactory epithelium but not in the central core using in situ hybridization, and its expression level was the highest in the olfactory rosette among the tissues examined. These results suggested Paqr5 may have an important role for transmitting progestin signaling in the olfactory system. The expression levels of paqr7a and paqr7b, pgr and pgrmc2 mRNA peaked around the mid meiotic stage, and that of paqr8 peaked at late meiotic stage in the olfactory rosette in males, while the olfactory expression of paqr5 decreased gradually as spermatogenesis progressed. In contrast, the expression of the progestin receptors did not change significantly during the development of the ovary in the olfactory rosette in females, except that of pgr. Interestingly, the changes of paqr8 expression in the olfactory rosette in males mirrored the changes of plasma DHP levels in females during the reproductive cycle, suggesting the Paqr8 may also be important for deciphering progestin signaling released by female. To our knowledge, this is the first time to demonstrate the presence of all known progestin receptors in a teleost olfactory rosette, and to show different expressions between the males and females during the reproductive cycle. This study provides the first evidence on changes of all purported progestin receptors during a reproductive cycle in teleost olfactory rosette, and suggests that distinct olfactory sensitivities to DHP may be due to the changes and compositions of each progestin receptor in B. sinensis.
我们之前的研究表明,17α,20β - 二羟基 - 4 - 孕烯 - 3 - 酮(DHP),一种诱导卵母细胞成熟的孕激素,在中国黑鲷(Bostrichthys sinensis)中也作为一种性信息素发挥作用。中国黑鲷是一种栖息于潮间带、在泥洞中交配和产卵的鱼类。在繁殖季节,对DHP的电嗅图反应增强。在本研究中,我们克隆了中国黑鲷的9种孕激素受体(pgr、paqr5、6、7(a,b)、8、9、pgrmc1、2)的cDNA,分析了它们的组织分布,并确定了雌雄鱼在生殖周期中嗅觉叶中的表达情况。这9种孕激素受体推导的氨基酸序列与其他鱼类的序列具有高度的同源性,与哺乳动物的同源性相对较低,系统发育分析将这9种中国黑鲷孕激素受体归类到各自的孕激素受体组中。中国黑鲷孕激素受体的组织分布呈现出不同的表达模式,但所有这9个基因均在嗅觉叶中表达。有趣的是,通过原位杂交发现paqr5 mRNA存在于嗅觉上皮的中间和基部,但在中央核心区域未发现,并且在所检测的组织中其在嗅觉叶中的表达水平最高。这些结果表明Paqr5可能在嗅觉系统中传递孕激素信号方面发挥重要作用。在雄性的嗅觉叶中,paqr7a和paqr7b、pgr和pgrmc2 mRNA的表达水平在减数分裂中期左右达到峰值,而paqr8的表达在减数分裂后期达到峰值,同时随着精子发生的进行,paqr5在嗅觉中的表达逐渐降低。相比之下,在雌性的嗅觉叶中,除了pgr外,孕激素受体在卵巢发育过程中的表达没有显著变化。有趣的是,雄性嗅觉叶中paqr8表达的变化反映了雌性在生殖周期中血浆DHP水平的变化,这表明Paqr8可能对于解读雌性释放的孕激素信号也很重要。据我们所知,这是首次在硬骨鱼的嗅觉叶中证明所有已知孕激素受体的存在,并展示了在生殖周期中雌雄之间的不同表达。本研究首次提供了硬骨鱼嗅觉叶中所有假定的孕激素受体在生殖周期中变化的证据,并表明对DHP不同的嗅觉敏感性可能归因于中国黑鲷中每种孕激素受体的变化和组成。