Chemosensory and hyperoxia circuits in C. elegans males influence sperm navigational capacity.
Chemosensory and hyperoxia circuits in C. elegans males influence sperm navigational capacity.
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DOI：
10.1371/journal.pbio.2002047
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发表时间：
2017-06
期刊：
影响因子：
9.8
通讯作者：
Miller MA
中科院分区：
文献类型：
--
作者：
Hoang HD;Miller MA
精子的关键功能是定位并与成熟的卵母细胞融合。在实验室条件下，秀丽隐杆线虫精子在雌雄同体的生殖道中导航和定位卵母细胞方面非常有效。在这里，我们确定了影响精子导航能力的化学感受和氧感电路。多种丝氨酸受体B（SR B）化学感受受体调节味觉感觉神经元中的Gα通路，味觉感觉神经元将纤毛延伸通过男性鼻子。在这些感觉神经元中，SRB信号传导是影响精子运动参数所必需和充分的。神经肽Y途径与SRB-13共同作用，对抗GCY-35高氧传感器对精子发生的负面影响。SRB化学感受器在低氧条件下对精子导航不是必需的，C。优雅的人更喜欢。在周围氧气环境中，SRB-13信号传导影响精子发生和精子线粒体期间的基因表达，从而增加迁移速度并抑制两性子宫内的逆转。SRB-13转录组高度富集与病原体防御有关的基因，其中许多基因在不同组织中表达。我们发现，SRB-13信号的关键时间段是精母细胞分化之前。我们的结果支持了年轻的C.雄性秀丽线虫能感知外部环境和氧气压力，从而触发持续时间较长的下游信号事件，影响精子的线粒体和导航能力。男性生命早期的环境暴露可能会改变精子功能和生育能力。栖息地丧失、疾病、气候变化和污染被认为对动物繁殖力产生负面影响。精子是一个潜在的靶点，但分子机制尚不清楚。线虫C.线虫是研究环境与雄性育性关系的一个强有力的遗传模型。雌雄同体的透明表皮允许直接观察迁移的雄性精子和受精过程。在这项研究中，我们确定了多个蛇形受体B（SR B）的化学感受器，在两栖动物的感觉神经元，延长纤毛通过男性的鼻子。这些SRB化学感受器是产生精子所必需的，这些精子能够有效地将雌雄同体的生殖道导航到受精部位。我们发现SRB-13信号抵消了GCY-35 O2传感器活性的负面影响，从而在高氧条件下维持精子线粒体功能和导航能力。特别令人感兴趣的是，SRB-13在睾丸成熟之前的早期幼虫阶段雄性中起作用。我们认为，年轻男性通过改变SRB神经回路来应对特定的压力环境，这反过来又会影响精子线粒体功能和活力。这种化学感受机制可能是C.雄性线虫对外界环境和氧气水平的反应。
The sperm’s crucial function is to locate and fuse with a mature oocyte. Under laboratory conditions, Caenorhabditis elegans sperm are very efficient at navigating the hermaphrodite reproductive tract and locating oocytes. Here, we identify chemosensory and oxygen-sensing circuits that affect the sperm’s navigational capacity. Multiple Serpentine Receptor B (SRB) chemosensory receptors regulate Gα pathways in gustatory sensory neurons that extend cilia through the male nose. SRB signaling is necessary and sufficient in these sensory neurons to influence sperm motility parameters. The neuropeptide Y pathway acts together with SRB-13 to antagonize negative effects of the GCY-35 hyperoxia sensor on spermatogenesis. SRB chemoreceptors are not essential for sperm navigation under low oxygen conditions that C. elegans prefers. In ambient oxygen environments, SRB-13 signaling impacts gene expression during spermatogenesis and the sperm’s mitochondria, thereby increasing migration velocity and inhibiting reversals within the hermaphrodite uterus. The SRB-13 transcriptome is highly enriched in genes implicated in pathogen defense, many of which are expressed in diverse tissues. We show that the critical time period for SRB-13 signaling is prior to spermatocyte differentiation. Our results support the model that young C. elegans males sense external environment and oxygen tension, triggering long-lasting downstream signaling events with effects on the sperm’s mitochondria and navigational capacity. Environmental exposures early in male life may alter sperm function and fertility. Habitat loss, disease, climate change, and pollution are thought to negatively affect animal fertility. Sperm are a potential target, but the molecular mechanisms are not understood. The nematode C. elegans is a powerful genetic model to investigate the relationship between environment and male fertility. The hermaphrodite’s transparent epidermis permits the direct visualization of migrating male sperm and fertilization. In this study, we identified multiple serpentine receptor B (SRB) chemosensory receptors that are expressed in amphid sensory neurons, which extend cilia through the male nose. These SRB chemoreceptors are necessary to produce sperm that are efficient at navigating the hermaphrodite reproductive tract to the fertilization site. We show that SRB-13 signaling counteracts the negative effect of GCY-35 O2 sensor activity, thereby maintaining sperm mitochondrial function and navigational capacity in hyperoxic conditions. Of particular interest, SRB-13 acts in early larval stage males prior to testis maturation. We propose that young males respond to specific stressful environments by altering SRB neural circuits, which in turn impact sperm mitochondrial function and motility. This chemosensory mechanism may be part of a systemic response in C. elegans males to external environment and oxygen levels.