A high-resolution morphological and ultrastructural map of anterior sensory cilia and glia in Caenorhabditis elegans.
A high-resolution morphological and ultrastructural map of anterior sensory cilia and glia in Caenorhabditis elegans.
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DOI：
10.7554/elife.01948
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发表时间：
2014-03-25
期刊：
影响因子：
7.7
通讯作者：
Nicastro D
中科院分区：
文献类型：
--
作者：
Doroquez DB;Berciu C;Anderson JR;Sengupta P;Nicastro D
许多初级感觉纤毛表现出独特的结构，对于特定感觉刺激的转导至关重要。虽然基本的纤毛发生机制已被很好地描述，但复杂的纤毛结构是如何产生的仍不清楚。几十年前进行的开创性工作提供了对线虫不同感觉纤毛形态的初步但不完整的描述。为了开始探索产生这些非常复杂的结构的机制，我们利用电子显微镜和断层扫描的进展，以高分辨率重建了线虫成虫两性感觉纤毛的60个中的50个的三维结构。我们描述了新的轴丝微管组织模式，阐明了纤毛底部的结构特征，描述了纤毛-胶质细胞相互作用的新方面，并确定了暗示纤毛蛋白运输新机制的结构。线虫不同纤毛的这种完整的超微结构描述为研究潜在的纤毛发生途径以及确定的纤毛结构对特定神经元功能的贡献提供了基础。Http://dx.doi.org/10.7554/eLife.01948.001为了生存，动物必须不断地收集周围环境的信息，然后决定如何应对。动物依靠被称为感觉神经元的细胞来帮助它们感知和处理这些信息，而大多数动物的这些神经元具有被称为纤毛的更小的结构，帮助它们收集这些信息。这些纤毛的结构可以从简单的毛状杆到复杂的分枝乔木。纤毛缺陷会导致细胞退化和死亡。科学家已经确定并确定了线虫体内60个带有纤毛的感觉神经元的功能。线虫是一种微小的蛔虫，具有简单的神经系统。这些实验表明，这些纤毛的形状非常不同，而且这种形状决定了神经元处理的信息类型。了解更多关于纤毛是如何形成的，以及这些形状如何使它们执行特定的感觉功能，将使科学家更好地理解大脑如何处理感觉信息。Doroquez等人。现在利用成像技术的进步，在线虫鼻子的50个神经元上产生了非常详细的纤毛三维重建。实验包括快速冷冻蠕虫，用防腐剂溶液慢慢取代冻结的水分子，然后将其嵌入树脂中。这允许Doroquez等人。将样品切成非常薄的切片--大约比一张纸薄1400倍--然后用透射电子显微镜和电子断层扫描对它们进行成像。最后，所有这些图像在计算机中组合在一起，产生纤毛的3D模型。这些模型揭示了广泛的纤毛结构，包括一些以前从未详细研究过的结构。Doroquez等人。也能够看到纤毛内的详细结构，包括决定哪些蛋白质应该进入或排除在单个纤毛之外的隔室。这些模型以及之前的研究结果表明，纤毛是由遗传因素决定的，也是与环境相互作用的结果。这种对不同纤毛结构的详细描述现在应该可以让研究人员识别决定其独特形状的基因，并探索特定的形状如何影响特定的感觉功能。DOI：http://dx.doi.org/10.7554/eLife.01948.002
Many primary sensory cilia exhibit unique architectures that are critical for transduction of specific sensory stimuli. Although basic ciliogenic mechanisms are well described, how complex ciliary structures are generated remains unclear. Seminal work performed several decades ago provided an initial but incomplete description of diverse sensory cilia morphologies in C. elegans. To begin to explore the mechanisms that generate these remarkably complex structures, we have taken advantage of advances in electron microscopy and tomography, and reconstructed three-dimensional structures of fifty of sixty sensory cilia in the C. elegans adult hermaphrodite at high resolution. We characterize novel axonemal microtubule organization patterns, clarify structural features at the ciliary base, describe new aspects of cilia–glia interactions, and identify structures suggesting novel mechanisms of ciliary protein trafficking. This complete ultrastructural description of diverse cilia in C. elegans provides the foundation for investigations into underlying ciliogenic pathways, as well as contributions of defined ciliary structures to specific neuronal functions. DOI: http://dx.doi.org/10.7554/eLife.01948.001 To survive, animals must constantly gather information about their surroundings and then decide how to respond. Animals rely on cells called sensory neurons to help them perceive and process this information, and these neurons in most animals have smaller structures called cilia that help them to gather this information. The structures of these cilia can range from simple hair-like rods to complex branched arbors. Defective cilia can lead to cell degeneration and death. Scientists have identified and determined the functions of many of the 60 sensory neurons with cilia in C. elegans, a tiny roundworm with a simple nervous system. These experiments have revealed that the shapes of these cilia are quite diverse, and that the shape determines the type of information the neurons process. Learning more about how cilia are shaped, and how these shapes allow them to perform specific sensory functions, would give scientists a better understanding of how the brain processes sensory information. Doroquez et al. have now taken advantage of advances in imaging technology to generate highly detailed three-dimensional reconstructions of the cilia on 50 neurons in the nose of C. elegans. The experiments involved rapidly freezing the worms, slowly replacing the frozen water molecules with a preservative solution, and then embedding in resin. This allowed Doroquez et al. to slice the samples into very thin sections—some 1400 times thinner than a sheet of paper—and then image them with transmission electron microscopy and electron tomography. Finally, all these images were combined in a computer to produce 3D models of the cilia. The models reveal a wide range of cilia structures, including some that have never been examined in detail before. Doroquez et al. were also able to see detailed structures within the cilia, including compartments that determine which proteins should enter into, or be excluded from, an individual cilium. The models, along with the results of previous studies, suggest that cilia are shaped by genetic factors and also by interactions with the environment. This detailed description of diverse cilia structures should now allow researchers to identify the genes that determine their unique shapes, and explore how specific shapes contribute to specific sensory functions. DOI: http://dx.doi.org/10.7554/eLife.01948.002