Effects of normal aging on myelin sheath ultrastructures in the somatic sensorimotor system of rats

Xie,Fang; Liang,Ping; Fu,Han; Zhang,Jiu‑Cong; Chen,Jun

doi:10.3892/mmr.2014.2228

Effects of normal aging on myelin sheath ultrastructures in the somatic sensorimotor system of rats

Authors:
- Fang Xie
- Ping Liang
- Han Fu
- Jiu‑Cong Zhang
- Jun Chen
View Affiliations

Affiliations: Institute for Biomedical Sciences of Pain, Tangdu Hospital, The Fourth Military Medical University, Xi'an, Shaanxi 710038, P.R. China, School of Pharmacy, The Fourth Military Medical University, Xi'an, Shaanxi 710032, P.R. China, Department of Gastroenterology, Lanzhou General Hospital of Lanzhou Military Command, Lanzhou, Gansu 730050, P.R. China
Published online on: May 9, 2014 https://doi.org/10.3892/mmr.2014.2228
Pages: 459-466

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Previous studies have presented qualitative and quantitative data regarding the morphological changes that occur peripherally in myelin sheaths and nerve fibers of rats during their lifespan. However, studies on ultrastructural features of myelinated fibers (MFs) in the central nervous system (CNS) remain limited. In the present study, morphological analyses of the somatic sensorimotor MFs in rats at time‑points between postnatal day 14 and postnatal month (PNM) 26 were conducted using electron microscopy. Significant alterations in the myelin sheath were observed in the sensorimotor system of aging and aged rats, which became aggravated with age. The ultrastructural pattern of myelin lamellae also exhibited age dependence. The transformation of the myelin intraperiod line from complete to incomplete fusion occurred after PNM 5, leading to an expansion of periodicity in myelin lamellae. These pathological changes in the myelin structure occurred very early and showed a significant correlation with age, indicating that myelin was the part of the CNS with the highest susceptibility to the influence of aging, and may be the main target of aging effects. In addition to the myelin breakdown, continued myelin production and remyelination were observed in the aging sensorimotor system, suggesting the presence of endogenous mechanisms of myelin repair.

View Figures

View References

1	Asou H, Hamada K and Sakota T: Visualization of a single myelination process of an oligodendrocyte in culture by video microscopy. Cell Struct Funct. 20:59–70. 1995. View Article : Google Scholar : PubMed/NCBI
2	Fields RD: White matter matters. Sci Am. 298:42–49. 2008.
3	Waxman SG: Conduction in myelinated, unmyelinated, and demyelinated fibers. Arch Neurol. 34:585–589. 1977. View Article : Google Scholar : PubMed/NCBI
4	Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H and Ullén F: Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci. 8:1148–1150. 2005. View Article : Google Scholar : PubMed/NCBI
5	Fields RD: Myelination: an overlooked mechanism of synaptic plasticity? Neuroscientist. 11:528–531. 2005. View Article : Google Scholar : PubMed/NCBI
6	Bartzokis G: Age-related myelin breakdown: a development modal of cognitive decline and Alzheimer’s disease. Neurobiol Aging. 25:5–18. 2004.
7	Albert M: Neuropsychological and neurophysiological changes in healthy adult humans across the age range. Neurobiol Aging. 14:623–625. 1993. View Article : Google Scholar : PubMed/NCBI
8	Peters A: The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol. 31:581–593. 2002. View Article : Google Scholar : PubMed/NCBI
9	Peters A, Sethares C and Killiany RJ: Effects of age on the thickness of myelin sheaths in monkey primary visual cortex. J Comp Neurol. 435:241–248. 2001. View Article : Google Scholar : PubMed/NCBI
10	Hinman JD and Abraham CR: What’s behind the decline? The role of white matter in brain aging. Neurochem Res. 32:2023–2031. 2007.
11	Peters A and Kemper T: A review of the structal alterations in the cerebral hemispheres of the aging rhesus monkey. Neurobiol Aging. 33:2357–2372. 2012. View Article : Google Scholar : PubMed/NCBI
12	Black JA, Foster RE and Waxman SG: Rat optic nerve: freeze-fracture studies during development of myelinated axons. Brain Res. 250:1–20. 1982. View Article : Google Scholar : PubMed/NCBI
13	Chase MH, Engelhardt JK, Adinolfi AM and Chirwa SS: Age-dependent changes in cat masseter nerve: an electrophysiological and morphological study. Brain Res. 586:279–288. 1992. View Article : Google Scholar : PubMed/NCBI
14	Majeed SK: Survey on spontaneous peripheral neuropathy in aging rats. Arzneimittelforschung. 42:986–990. 1992.PubMed/NCBI
15	Sharma AK, Bajada S and Thomas PK: Age changes in the tibial and plantar nerves of the rat. J Anat. 130:417–428. 1980.PubMed/NCBI
16	Stanmore A, Bradbury S and Weddell AG: A quantitative study of peripheral nerve fibres in the mouse following the administration of drugs. 1 Age changes in untreated CBA mice from 3 to 21 months of age. J Anat. 127:101–115. 1978.PubMed/NCBI
17	Navarro X and Kennedy WR: The effects of ageing on regeneration and sprouting of unmyelinated axons. Peripheral Nerve Changes in the Elderly. New Issues in Neurosciences. Thomas PK: 1. Wiley & Sons; New York, NY: pp. 125–134. 1989
18	Verdú E, Butí M and Navarro X: Functional changes of the peripheral nervous system with aging in the mouse. Neurobiol Aging. 17:73–77. 1996.
19	Coleman P, Finch C and Joseph J: The need for multiple time points in aging studies. Neurobiol Aging. 25:3–4. 2004. View Article : Google Scholar : PubMed/NCBI
20	Jernigan TL and Fennema-Notestine C: White matter mapping is needed. Neurobiol Aging. 25:37–39. 2004. View Article : Google Scholar : PubMed/NCBI
21	Coleman PD: How old is old? Neurobiol Aging. 25:12004. View Article : Google Scholar
22	Ceballos D, Cuadras J, Verdú E and Navarro X: Morphometric and ultrastructural changes with ageing in mouse peripheral nerve. J Anat. 195:563–576. 1999. View Article : Google Scholar : PubMed/NCBI
23	Behse F: Morphometric studies on the human sural nerve. Acta Neurol Scand Suppl. 132:1–38. 1990.PubMed/NCBI
24	Arbuthnott ER, Boyd IA and Kalu KU: Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity. J Physiol. 308:125–157. 1980. View Article : Google Scholar : PubMed/NCBI
25	Friede RL and Samorajski T: Myelin formation in the sciatic nerve of the rat. A quantitative electron microscopic, histochemical and radioautographic study. J Neuropathol Exp Neurol. 27:546–570. 1968. View Article : Google Scholar
26	Xie F, Fu H, Hou JF, Jiao K, Costigan M and Chen J: High energy diets-induced metabolic and prediabetic painful polyneuropathy in rats. PLoS One. 8:e574272013. View Article : Google Scholar : PubMed/NCBI
27	Fancy SP, Baranzini SE, Zhao C, et al: Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 23:1571–1585. 2009. View Article : Google Scholar : PubMed/NCBI
28	La Marca R, Cerri F, Horiuchi K, et al: TACE (ADAM17) inhibits Schwann cell myelination. Nat Neurosci. 14:857–865. 2011.PubMed/NCBI
29	Makinodan M, Rosen KM, Ito S and Corfas G: A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science. 337:1357–1360. 2012. View Article : Google Scholar : PubMed/NCBI
30	Knox CA, Kokmen E and Dyck PJ: Morphometric alteration of rat myelinated fibers with aging. J Neuropathol Exp Neurol. 48:119–139. 1989. View Article : Google Scholar : PubMed/NCBI
31	Thomas PK, King RH and Sharma AK: Changes with age in the peripheral nerves of the rat. An ultrastructural study. Acta Neuropathol. 52:1–6. 1980. View Article : Google Scholar : PubMed/NCBI
32	Peters A: The effects of normal aging on nerve fibers and neuroglia in the central nervous system. Brain Aging: Models, Methods, and Mechanisms. Riddle DR: CRC Press; Boca Raton, FL: pp. 97–125. 2007, View Article : Google Scholar : PubMed/NCBI
33	Peters A: The effects of normal aging on myelinated nerve fibers in monkey central nervous system. Front Neuroanat. 3:112009. View Article : Google Scholar : PubMed/NCBI
34	Krinke G, Froehlich E, Herrmann M, et al: Adjustment of the myelin sheath to axonal atrophy in the rat spinal root by the formation of infolded myelin loops. Acta Anat (Basel). 131:182–187. 1988. View Article : Google Scholar : PubMed/NCBI
35	Luebke J, Barbas H and Peters A: Effects of normal aging on prefrontal area 46 in the rhesus monkey. Brain Res Rev. 62:212–232. 2010. View Article : Google Scholar : PubMed/NCBI
36	Sugiyama I, Tanaka K, Akita M, Yoshida K, Kawase T and Asou H: Ultrastructural analysis of the paranodal junction of myelinated fibers in 31-month-old-rats. J Neurosci Res. 70:309–317. 2002. View Article : Google Scholar : PubMed/NCBI
37	Peters A and Sethares C: Is there remyelination during aging of the primate central nervous system? J Comp Neurol. 460:238–254. 2003. View Article : Google Scholar : PubMed/NCBI