Evidence for spontaneous axon degeneration during peripheral nerve maturation

Reier, Paul J.; Hughes, Arthur

doi:10.1002/aja.1001350113

Cited by 46 publications

(12 citation statements)

References 7 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Electron microscopic studies have described degenerating axons in the central nervous system (Hashimoto and Palay, 1965;Mugnaini et al, 1967;Sotelo and Palay, 1971;Leonhardt, 1976), in the neurohypophysis (Dellmann and Rodrfguez, 1970;Baumgarten et al, 1972), in the rodent pineal gland (Matsushima and Reiter, 1977), in the cat carotid sinus (Knoche et al, 1977), and during the development of mouse and rat sciatic nerve (Reier and Hughes, 1972).…”

Section: Discussionmentioning

confidence: 97%

Degeneration and regeneration of autonomic nerve endings in the anterior part of rhesus monkey ciliary muscle

Townes‐Anderson

Raviola

1978

J Neurocytol

View full text Add to dashboard Cite

The autonomic nerve plexus of the ciliary muscle was examined with the electron microscope in normal rhesus monkeys of different ages. In the anterior region of the muscle, at the boundary with the poorly innervated scleral spur and trabecular meshwork, 3.8-7.1% of the axons exhibit either degenerative or regenerative features. The cytoplasm of degenerating axons contains lamellated, dense and multivesicular bodies, vesicles, whorls of filaments, and membranous debris. The plasma membrane is often discontinuous and, on occasion, axonal debris and degenerative organelles are freely dispersed in the connective tissue spaces of the muscle. Degenerating axons contain a granular reaction product when stained for acid phosphatase activity. Regenerating axons are characterized by tightly packed mitochondria, glycogen particles, and aggregates of synaptic vesicles; they synapse with muscle cells and are negative to the acid phosphatase reaction. A quantitative analysis showed that in the anterior region of the ciliary muscle degenerating and regenerating axons increase in number with age, although the total number of axonal profiles remains constant. In the age groups examined, degenerating axons occurred with the same frequency as regenerating axons, thus, the age-dependent increase in axonal degeneration is accompanied by a parallel increase in axonal regeneration. We conclude that autonomic nerve endings in the anterior part of the ciliary muscle undergo a continuous process of renewal that is more prominent in old age.

show abstract

Section: Discussionmentioning

confidence: 97%

Degeneration and regeneration of autonomic nerve endings in the anterior part of rhesus monkey ciliary muscle

Townes‐Anderson

Raviola

1978

J Neurocytol

View full text Add to dashboard Cite

show abstract

“…Possibly the 77-kDa NGF receptor species is derived from neuronal sources. Aside from normal cell death, axons of the sciatic nerve (30) and sympathetic trunk (31) undergo spontaneous degeneration in the postnatal rat. This process commences near birth, and axon numbers stabilize by P6 (31).…”

Section: Discussionmentioning

confidence: 99%

Identification of a truncated form of the nerve growth factor receptor.

DiStefano

Johnson

1988

Proc. Natl. Acad. Sci. U.S.A.

121

View full text Add to dashboard Cite

Schwann cells express growth factor (NGF) receptors on their cell surface in response to axotomy, a phenomenon that can be demonstrated both in vivo and in vitro. The predominant form of the NGF receptor on Schwann cells exists as an %80-kDa band, as determined by NaDod-S04/PAGE. We demonstrate that cultured Schwann cells shed a truncated (50-kDa) form of the NGF receptor (NGF-Rt) into their medium. Other cell types that shed the NGF-Rt into medium include a rat schwannoma and, to a lesser extent, PC12 cells and superior cervical ganglion neurons. NGF-Rt was not found in media conditioned by mixed neuron/glia cultures from various brain regions, or anterior pituitary cells derived from rat. In vivo, NGF-Rt was present in neonatal rat urine, and its presence was developmentally regulated: levels were high in postnatal day-1 rat urine and declined to low, but detectable, levels by weeks 4 and 8. NGF-Rt was also found in amniotic fluid and in the stomach contents of fetal rats. Maternal urine (pre-and postnatal) had slightly elevated NGF-Rt levels over normal adult urine. NGF-Rt was detected in rat plasma and showed developmental regulation similar to that found for urine. In addition, a 77-kDa receptor species was detected in plasma during early development. Finally, NGF-Rt was significantly elevated in the urine of adult rats with bilateral sciatic nerve lesions. These findings suggest that the developmentally regulated release of NGF-Rt, present in plasma and other body fluids, plays a regulatory role in nervous system development.Nerve growth factor (NGF) exerts its effects on NGFdependent neurons by interacting with specific, high-affinity receptors located on the neuronal cell surface (1-5). NGF receptors have been extensively characterized on peripheral sympathetic neurons (6, 7), neural crest-derived sensory neurons (8), as well as a variety of tumor cell lines (9-11). NGF receptors have also been localized to neurons, predominantly cholinergic, of the central nervous system (12)(13)(14)(15). In addition to their neuronal localization, NGF receptors have recently been identified on cultured ganglionic Schwann cells (16)(17)(18) and on rat peripheral nerve Schwann cells both in vivo and in vitro (19,20). Schwann cells in the distal portion of lesioned adult sciatic nerve increase their NGF receptor content with time after injury (19). Likewise, Schwann cells isolated from neonatal rat sciatic nerve increase their NGF receptor number with time in culture (20). These experiments indicate that Schwann cells express NGF receptors on their cell surface in response to loss of axonal contact. We have proposed that expression of NGF-binding sites on the Schwann cell surface sequesters NGF (which is probably secreted by the Schwann cell) and thus guides NGF-dependent axons during regeneration and possibly development (19, 20).In these studies we have discovered that Schwann cells and, to a lesser extent, PC12 cells and superior cervical ganglion (SCG) neurons, shed a truncated form of the NGF receptor (NGF-R...

show abstract

“…Another way to determine whether axons are lost during development is to count them at different postnatal times. Aguayo et al (1973) investigating descriptions of the spontaneous loss of axons in normal peripheral nerves (Webster and O'Connell, 1970;Reier and Hughes, 1972), noted 16,000 axons in the cervical sympathetic trunk at birth and only 5760 axons 3 weeks later. A decline of similar magnitude was reported by Koppel and Innocenti (1983): 70% of callosal axons present at birth were eliminated by adulthood.…”

Section: Discussionmentioning

confidence: 99%

Postnatal development of the rat dorsal funiculus

Ks¹,

Coggeshall²

1987

J. Neurosci.

View full text Add to dashboard Cite

The present study shows that there are approximately 21,000 axons in the neonatal rat dorsal funiculus, as compared to 26,000 in 2-week-old animals. We attribute this increase primarily to arriving corticospinal fibers. In adult animals, however, there are approximately 15,000 axons. This is a decline of 58% from the 2 week level, and the decrease is proportionately similar in the corticospinal area and the dorsal funiculus proper. Thus, axon numbers decline in later postnatal development, and since the decline seems to be well past the time of the histogenetic death of the cells that give rise to these axons, we propose that the loss is not caused by the death of neurons. This is further evidence that a reduction in axon numbers not accompanied by cell death is a widespread phenomenon in mammalian postnatal neural development. We infer that the mechanism of axon loss is a reduction in axon branching and that its function is to sharpen synaptic connections.

show abstract

Evidence for spontaneous axon degeneration during peripheral nerve maturation

Cited by 46 publications

References 7 publications

Degeneration and regeneration of autonomic nerve endings in the anterior part of rhesus monkey ciliary muscle

Degeneration and regeneration of autonomic nerve endings in the anterior part of rhesus monkey ciliary muscle

Identification of a truncated form of the nerve growth factor receptor.

Postnatal development of the rat dorsal funiculus

Contact Info

Product

Resources

About