Riboul Danielle V, Crill Sarah, Oliva Carlos D, Restifo Maria Gabriela, Joseph Reggie, Joseph Kerdes, Nguyen Ken C Q, Hall David H, Fily Yaouen, Macleod Gregory T
Integrative Biology & Neuroscience Graduate Program, Florida Atlantic University, Boca Raton, Florida, USA.
Wilkes Honors College, Florida Atlantic University, Jupiter, Florida, USA.
J Comp Neurol. 2024 Dec;532(12):e70002. doi: 10.1002/cne.70002.
Neurons rely on mitochondria for an efficient supply of ATP and other metabolites. However, while neurons are highly elongated, mitochondria are discrete and limited in number. Due to the slow rates of metabolite diffusion over long distances, it follows that neurons would benefit from an ability to control the distribution of mitochondria to sites of high metabolic activity such as synapses. Ultrastructural data over substantial portions of a neuron's extent that would allow for tests of such hypotheses are scarce. Here, we mined the Caenorhabditis elegans' electron micrographs of John White and Sydney Brenner and found systematic differences in average mitochondrial length (ranging from 1.3 to 2.4 µm), diameter (0.18-0.24 µm) and volume density (3.7%-6.5%) between neurons of different function and neurotransmitter type, but found limited differences in mitochondrial length, diameter, and density between axons and dendrites of the same neurons. In analyses of mitochondrial distribution, mitochondria were found to be distributed randomly with respect to presynaptic sites. Presynaptic sites were primarily localized to varicosities, but mitochondria were no more likely to be found in synaptic varicosities than non-synaptic varicosities. Consistently, mitochondrial volume density was no greater in synaptic varicosities than non-synaptic varicosities. Therefore, beyond the capacity to disperse mitochondria throughout their length, at least in C. elegans, fine caliber neurons manifest limited subcellular control of mitochondrial size and distribution.
神经元依赖线粒体来高效供应三磷酸腺苷(ATP)和其他代谢物。然而,尽管神经元高度细长,但线粒体数量有限且呈离散分布。由于代谢物在长距离上的扩散速度较慢,因此神经元若能将线粒体分布控制到高代谢活性位点(如突触),将从中受益。能用于检验此类假设的、覆盖神经元大部分区域的超微结构数据十分匮乏。在此,我们挖掘了约翰·怀特(John White)和悉尼·布伦纳(Sydney Brenner)拍摄的秀丽隐杆线虫的电子显微照片,发现不同功能和神经递质类型的神经元之间,线粒体的平均长度(范围为1.3至2.4微米)、直径(0.18 - 0.24微米)和体积密度(3.7% - 6.5%)存在系统性差异,但同一神经元的轴突和树突之间,线粒体长度、直径和密度的差异有限。在线粒体分布分析中,发现线粒体相对于突触前位点呈随机分布。突触前位点主要定位于膨体,但线粒体在突触膨体中出现的可能性并不比非突触膨体更高。同样,突触膨体中的线粒体体积密度并不比非突触膨体更大。因此,至少在秀丽隐杆线虫中,除了能在线粒体全长范围内进行分散外,细口径神经元对线粒体大小和分布的亚细胞控制有限。