Selvaraj Vimal, Asano Atsushi, Buttke Danielle E, Sengupta Prabuddha, Weiss Robert S, Travis Alexander J
Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, USA.
J Cell Physiol. 2009 Mar;218(3):522-36. doi: 10.1002/jcp.21624.
We demonstrate for the first time that a stable, micron-scale segregation of focal enrichments of sterols exists at physiological temperature in the plasma membrane of live murine and human sperm. These enrichments of sterols represent microheterogeneities within this membrane domain overlying the acrosome. Previously, we showed that cholera toxin subunit B (CTB), which binds the glycosphingolipid, G(M1), localizes to this same domain in live sperm. Interestingly, the G(M1) undergoes an unexplained redistribution upon cell death. We now demonstrate that G(M1) is also enriched in the acrosome, an exocytotic vesicle. Transfer of lipids between this and the plasma membrane occurs at cell death, increasing G(M1) in the plasma membrane without apparent release of acrosomal contents. This finding provides corroborative support for an emerging model of regulated exocytosis in which membrane communications might occur without triggering the "acrosome reaction." Comparison of the dynamics of CTB-bound endogenous G(M1) and exogenous BODIPY-G(M1) in live murine sperm demonstrate that the sub-acrosomal ring (SAR) functions as a specialized diffusion barrier segregating specific lipids within the sperm head plasma membrane. Our data show significant differences between endogenous lipids and exogenous lipid probes in terms of lateral diffusion. Based on these studies, we propose a hierarchical model to explain the segregation of this sterol- and G(M1)-enriched domain in live sperm, which is positioned to regulate sperm fertilization competence and mediate interactions with the oocyte. Moreover, our data suggest potential origins of subtypes of membrane raft microdomains enriched in sterols and/or G(M1) that can be separated biochemically.
我们首次证明,在生理温度下,活的小鼠和人类精子的质膜中存在稳定的、微米级的固醇局部富集区隔。这些固醇富集区代表了顶体上方该膜结构域内的微异质性。此前,我们表明,结合糖鞘脂G(M1)的霍乱毒素亚基B(CTB)定位于活精子的同一结构域。有趣的是,G(M1)在细胞死亡时会发生无法解释的重新分布。我们现在证明,G(M1)在顶体(一种胞吐小泡)中也有富集。在细胞死亡时,脂质在顶体和质膜之间转移,增加了质膜中的G(M1),而顶体内容物没有明显释放。这一发现为一种新兴的调节性胞吐模型提供了确证支持,在该模型中,膜通讯可能在不触发“顶体反应”的情况下发生。对活小鼠精子中CTB结合的内源性G(M1)和外源性BODIPY-G(M1)动力学的比较表明,顶体下环(SAR)作为一种特殊的扩散屏障,将精子头部质膜内的特定脂质分隔开来。我们的数据显示,内源性脂质和外源性脂质探针在侧向扩散方面存在显著差异。基于这些研究,我们提出了一个分层模型来解释活精子中这个富含固醇和G(M1)的结构域的区隔,该结构域的定位是调节精子的受精能力并介导与卵母细胞的相互作用。此外,我们的数据表明了富含固醇和/或G(M1)的膜筏微结构域亚型的潜在起源,这些亚型可以通过生化方法分离。