Age-related quantitative changes in mitochondria of satellite cell sheaths enveloping spinal ganglion neurons in the rabbit

Abstract

We studied mitochondria in the satellite cell sheaths which envelope the spinal ganglion neurons of rabbits aged 12, 42, and 79 months. While the mean cytoplasmic volume of satellite cell sheaths did not change significantly with age, the mean percentage of cytoplasmic volume occupied by mitochondria decreased with age. This decrease is mainly due to a reduction in the total mitochondrial mass and only in minor part is a consequence of lipofuscin accumulation. Mitochondrial structure did not change, while mitochondrial size increased with age. Comparison between mitochondria in nerve cell bodies and those in satellite cell sheaths showed that: (1) the mean percentage of cytoplasmic volume occupied by mitochondria was greater in nerve cell bodies than satellite cell sheaths and the ratio between these two percentages remained constant with advancing age; (2) the total mitochondrial mass was much greater in nerve cell bodies than satellite cell sheaths and the ratio between these two values increased with age; (3) the extent of increase of mitochondrial size with age was similar in nerve cell bodies and satellite cell sheaths. The results of the present study suggest that: (1) the ability of satellite cell sheaths to produce energy decreases with age; (2) the decreased ability of sensory neurons in old animals to meet high energy demands may be partly due to the diminished contribution of their associated satellite cell sheaths.

Mitochondria in Perineuronal Satellite Cell Sheaths of Rabbit Spinal Ganglia: Quantitative Changes during Life

“…This new finding shows that in studies on aging it is advisable to examine extremely old animals in order to obtain complete information on the aging process. In a previous study, the mean mitochondrial size increased significantly with age [Martinelli et al, 2003], and our present results reveal that this increase continues into extremely advanced age. Mitochondrial size also rises with age in the nerve cell bodies of rabbit spinal ganglia [Martinelli et al, 2006].…”

“…In our previous study on mitochondria of the rabbit SCSs [Martinelli et al, 2003], three age groups were studied. The mean cytoplasmic volume of these sheaths did not significantly change from young to old rabbits.…”

“…The percentage of cytoplasmic volume occupied by mitochondria and the size of mitochondria were determined using the stereological method described previously [Martinelli et al, 2003]. This method ensures that all SCSs have the same chance of being sampled, irrespective of their size and the size of the nerve cell bodies with which they are associated.…”

“…In spinal ganglia, each nerve cell body is usually enveloped by its own satellite cell sheath (SCS), thus constituting a structural and probably also a metabolic unit [for reviews, see Pannese, 1981Pannese, , 1994. Because of the close interaction between the spinal ganglion neuron and its SCS, we have previously performed studies on age-related changes in the former and similar studies in the latter [Martinelli et al, 2003]. We have now resumed our investigations on age-related changes in mitochondria of rabbit spinal ganglion SCSs, extending our study to more specimens of the previously considered age groups and also examining animals of extremely advanced age.…”

Optical Analysis of Mitochondrial Function and Heterogeneity in Cultured Hippocampal Astrocytes

“…It is questionable whether filamentous mitochondria differ from granular mitochondria in more than just length. Functional differences were suggested due to a higher occurrence of long filamentous mitochondria in cells with compromised energy metabolism, e. g. in aged cells (Karbowski et al 1997, Bertoni-Freddari et al 2003, Martinelli et al 2003. Long mitochondria probably develop from fusion of shorter ones (Mouli et al 2009) and disturbance of this process leads to poor cellular health in vitro supporting the idea of functional differences (Chen et al 2005).…”