Abstract
Neurons project axons to local and distal sites and can display heterogeneous morphologies with limited physical dimensions that may influence the structure of large organelles such as mitochondria. Using cryo-electron tomography (cryo-ET), we characterized native environments within axons and presynaptic varicosities to examine whether spatial restrictions within these compartments influence the morphology of mitochondria. Segmented tomographic reconstructions revealed distinctive morphological characteristics of mitochondria residing at the narrowed boundary between presynaptic varicosities and axons with limited physical dimensions (approximately 80 nm), compared to mitochondria in nonspatially restricted environments. Furthermore, segmentation of the tomograms revealed discrete organizations between the inner and outer membranes, suggesting possible independent remodeling of each membrane in mitochondria at spatially restricted axonal/varicosity boundaries. Thus, cryo-ET of mitochondria within axonal subcompartments reveals that spatial restrictions do not obstruct mitochondria from residing within them, but limited available space can influence their gross morphology and the organization of the inner and outer membranes. These findings offer new perspectives on the influence of physical and spatial characteristics of cellular environments on mitochondrial morphology and highlight the potential for remarkable structural plasticity of mitochondria to adapt to spatial restrictions within axons.
Highlights
Neurons are architecturally complex cells that can extend axonal projections with elaborate arborization for several hundreds of millimeters to form synaptic connections with local and distal targets [1,2,3]
Neurons are complex cells that communicate with each other via axons that can extend over distances of a meter or longer
Axons show variable dimensions, sometimes thinning to a diameter significantly smaller than the standard diameter of mitochondria, raising the question of how mitochondrial structures can adapt to the local spatial environment
Summary
Neurons are architecturally complex cells that can extend axonal projections with elaborate arborization for several hundreds of millimeters (and in some cases, meters) to form synaptic connections with local and distal targets [1,2,3]. Tracking through the axons is a well-developed system of microtubules that mediate motor-driven anterograde and retrograde transport of signaling cargoes, protein complexes, and organelles critical for function and homeostasis at distant synapses [10,11]. Transport of these intracellular components creates a spatially and temporally dynamic environment within the axon that can contain a variety of organelles and cargoes of different shapes, sizes, and number [12,13]. Mitochondria are morphologically dynamic organelles that can exist in a variety of shapes and sizes, how mitochondria adapt to the physical constraints presented in axons has not been previously examined
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