Three-dimensional analysis of mouse rod and cone mitochondrialcristae architecture: Bioenergetic and functional implications

[摘要] Purpose: Comparative studies of structure related to function offera promising means of understanding the significance of differences incytoarchitecture. Mitochondrial crista structure is linked tightly tomitochondrial function. Non-foveal cone photoreceptors of primatescontain considerably more inner segment mitochondria and have higheroxidative enzyme activity than do rods. In addition, it is suggestedthat light-adapted cones have a higher aerobic ATP demand thanlight-adapted rods. Therefore, we investigated the oxidative metabolismand three-dimensional membrane architecture of mouse rod and cone innersegment mitochondria.Methods: We determined the number, size, cytochrome c oxidase (CO)reactivity, and membrane architecture of rod and middlewavelength-sensitive (M) cone inner segment mitochondria from 21 day oldlight-adapted C57BL/6 mice using conventional electron microscopy andthe three-dimensional approach of single- and double-tilt electronmicroscope tomography. Fourteen different measurements of mitochondrialsubstructures were analyzed. Photoreceptor oxygen consumption wasdetermined in dark- and light-adapted retinas.Results: Rod and cone mitochondria displayed an orthodoxconformation. Cone inner segments, compared to rods, contained 2-foldmore mitochondria and were more CO reactive. Rod and cone mitochondriahad similar outer-inner membrane width, contact site width, diameter anddensity, crista width, number of cristae/volume, number of cristaesegments/volume, and fraction of cristae with multiple segments. Incontrast, cone mitochondria had narrower crista junctions, greatercristae connectivity, and approximately 3-fold more cristae membranesurface area compared to rods. The increased cristae membrane surfacearea in cones was accomplished by connecting more cristae segmentstogether, rather than by creating more cristae.Conclusions: These results demonstrate that middle wavelength (M)cones have a different bioenergetic signature than do rods and suggestthat the aerobic ATP demand and production is greater in light-adaptedcones than in light-adapted rods. Cones utilize two complimentarystrategies to increase their aerobic ATP production: increase the numberof mitochondria and increase the cristae surface membrane area. Thegreater ATP generation by cones may also provide increased protectionagainst metabolic insults and apoptosis compared to rods.

[学科分类] 生物化学/生物物理