Govindan J Amaranath, Nadarajan Saravanapriah, Kim Seongseop, Starich Todd A, Greenstein David
Department of Genetics, Cell Biology and Development, University of Minnesota, 6-160 Jackson Hall, 321 Church Street SE, Minneapolis, MN 55455, USA.
Development. 2009 Jul;136(13):2211-21. doi: 10.1242/dev.034595.
Soma-germline interactions control fertility at many levels, including stem cell proliferation, meiosis and gametogenesis, yet the nature of these fundamental signaling mechanisms and their potential evolutionary conservation are incompletely understood. In C. elegans, a sperm-sensing mechanism regulates oocyte meiotic maturation and ovulation, tightly coordinating sperm availability and fertilization. Sperm release the major sperm protein (MSP) signal to trigger meiotic resumption (meiotic maturation) and to promote contraction of the follicle-like gonadal sheath cells that surround oocytes. Using genetic mosaic analysis, we show that all known MSP-dependent meiotic maturation events in the germline require Galpha(s)-adenylate cyclase signaling in the gonadal sheath cells. We show that the MSP hormone promotes the sustained actomyosin-dependent cytoplasmic streaming that drives oocyte growth. Furthermore, we demonstrate that efficient oocyte production and cytoplasmic streaming require Galpha(s)-adenylate cyclase signaling in the gonadal sheath cells, thereby providing a somatic mechanism that coordinates oocyte growth and meiotic maturation with sperm availability. We present genetic evidence that MSP and Galpha(s)-adenylate cyclase signaling regulate oocyte growth and meiotic maturation in part by antagonizing gap-junctional communication between sheath cells and oocytes. In the absence of MSP or Galpha(s)-adenylate cyclase signaling, MSP binding sites are enriched and appear clustered on sheath cells. We discuss these results in the context of a model in which the sheath cells function as the major initial sensor of MSP, potentially via multiple classes of G-protein-coupled receptors. Our findings highlight a remarkable similarity between the regulation of meiotic resumption by soma-germline interactions in C. elegans and mammals.
体细胞与生殖细胞的相互作用在多个层面控制着生育能力，包括干细胞增殖、减数分裂和配子发生，但这些基本信号机制的本质及其潜在的进化保守性仍未完全了解。在秀丽隐杆线虫中，一种精子感知机制调节卵母细胞的减数分裂成熟和排卵，紧密协调精子的可获得性与受精过程。精子释放主要精子蛋白（MSP）信号来触发减数分裂恢复（减数分裂成熟），并促进围绕卵母细胞的卵泡样性腺鞘细胞收缩。通过遗传镶嵌分析，我们发现生殖系中所有已知的依赖MSP的减数分裂成熟事件都需要性腺鞘细胞中的Gα(s)-腺苷酸环化酶信号传导。我们表明，MSP激素促进持续的肌动球蛋白依赖性细胞质流动，从而驱动卵母细胞生长。此外，我们证明有效的卵母细胞产生和细胞质流动需要性腺鞘细胞中的Gα(s)-腺苷酸环化酶信号传导，从而提供了一种体细胞机制，将卵母细胞生长和减数分裂成熟与精子可获得性相协调。我们提供了遗传证据，表明MSP和Gα(s)-腺苷酸环化酶信号传导部分通过拮抗鞘细胞与卵母细胞之间的间隙连接通讯来调节卵母细胞生长和减数分裂成熟。在没有MSP或Gα(s)-腺苷酸环化酶信号传导的情况下，MSP结合位点在鞘细胞上富集并出现聚集。我们在一个模型的背景下讨论这些结果，在该模型中，鞘细胞可能通过多类G蛋白偶联受体作为MSP的主要初始传感器。我们的发现突出了秀丽隐杆线虫和哺乳动物中体细胞与生殖细胞相互作用对减数分裂恢复调节之间的显著相似性。
