Ultrastructural Analysis Reveals Mitochondrial Placement Independent of Synapse Placement in Fine Caliber <i>C. elegans</i> Neurons

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.

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Publication Details

Journal
The Journal of Comparative Neurology
Published
2024-12-01
DOI
https://doi.org/10.1002/cne.70002
Citations
2
Primary Topic
Genetics, Aging, and Longevity in Model Organisms
Type
article
Field-Weighted Citation Impact
0.46

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article

Ultrastructural Analysis Reveals Mitochondrial Placement Independent of Synapse Placement in Fine Caliber C. elegans Neurons

Danielle V. Riboul, Yaouen Fily, David H. Hall, Sarah Crill et al.
2 citations
The Journal of Comparative Neurology
Genetics, Aging, and Longevity in Model Organisms
0.46
article

Ultrastructural Analysis Reveals Mitochondrial Placement Independent of Synapse Placement in Fine Caliber C. elegans Neurons

Danielle V. Riboul, Yaouen Fily, David H. Hall, Sarah Crill, Carlos D. Oliva, Ken C. Q. Nguyen, Maria Gabriela Restifo, K. Simmy Joseph, Gregory T. Macleod, Reggie Joseph
article en
2 citations

Abstract

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.

The Journal of Comparative NeurologyVol. 532(12)
Tulane University (US), Albert Einstein College of Medicine (US), Jupiter (United States) (US), Florida Atlantic University (US)
Tulane University, National Institutes of Health, Medical Research Council, National Institute of Neurological Disorders and Stroke
Openalex Percentile: Top 37%
Genetics, Aging, and Longevity in Model Organisms
0.46
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