Target-dependence of sensory neurons: An ultrastructural comparison of axotomised dorsal root ganglion neurons with allowed or denied reinnervation of peripheral targets

Johnson, Ian; Sears, T. A.

doi:10.1016/j.neuroscience.2012.10.015

Cited by 16 publications

(20 citation statements)

References 76 publications

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“…Why does axonal injury result variably in axon regeneration or collateral sprouting, atrophy or cell death (Thuret et al, )? A long‐standing observation is that after axonal injury, “chromatolysis” occurs in central, autonomic, and peripheral neurons (whether injured peripherally or centrally) (Torvik and Heding, ; Lieberman, ; Nathaniel and Nathaniel, ; Egan et al, ; Barron, ; Barron, ; Kobayashi et al, ; Severinsen and Jakobsen, ; Johnson and Sears, ). This catastrophic event involves dramatic whole‐cell morphological changes that are easily visible under the light microscope (e.g., after cresyl violet or toluidine blue staining for Nissl substance).…”

Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

“…Electron microscopy reveals that Nissl bodies are parallel arrays of cisterns of rough endoplasmic reticulum studded with ribosomes; rosettes of free polyribosomes and monoribosomes are found between the cisterns (Fig. ) (Matthews and Raisman, ; Johnson and Sears, ). Each ribosome is a complex of ribosomal RNAs (rRNAs) and proteins that use transfer RNAs (tRNAs) and amino acids to synthesize proteins from mRNAs.…”

Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

“…EM shows that chromatolysis is the fragmentation of stacks of rough endoplasmic reticulum leaving clear areas of cytoplasm lacking Nissl bodies; in some cases (see below) this can be accompanied by the disaggregation and/or disassembly of polyribosomes to leave a fine “dust‐like” powder (Cragg, ; Matthews and Raisman, ; Torvik, ; Barron and Dentinger, ; Dentinger et al, ; Johnson and Sears, ). Ribosomes can be depleted from rough endoplasmic reticulum (Lieberman, ; Barron, ; Baltanas et al, ).…”

Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

“…Ribosomes and fragments of endoplasmic reticulum can also be found in autophagic vacuoles after axotomy (Matthews and Raisman, ; Torvik, ) and during Purkinje cell degeneration (Baltanas et al, ). The cell body response can also involve dispersion to the soma's periphery of any remaining ribonucleoprotein complexes (Cragg, ; Barron and Dentinger, ; Dentinger et al, ; Johnson and Sears, ) (Fig. ) and movement of the nucleus to an eccentric position.…”

Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

“…Alternatively, ribonucleases might cause irreversible cleavage of RNA and ribosomes within hours of injury but the diffusion or dispersion of Nissl substance might take longer. Chromatolytic neurons often revert to a more‐normal phenotype if they regenerate (Matthews and Raisman, ; Johnson and Sears, ). In cultured neurons and organotypic slices, fission of endoplasmic reticulum in dendrites can be followed by fusion (i.e., it is reversible): it does not affect neuronal survival (Kucharz et al, ; Kucharz et al, ).…”

Section: Might Attenuation Of Chromatolysis Be Therapeutically Benefimentioning

confidence: 99%

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Chromatolysis: Do injured axons regenerate poorly when ribonucleases attack rough endoplasmic reticulum, ribosomes and RNA?

Moon

2018

Developmental Neurobiology

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After axonal injury, chromatolysis (fragmentation of Nissl substance) can occur in the soma. Electron microscopy shows that chromatolysis involves fission of the rough endoplasmic reticulum. In CNS neurons (which do not regenerate axons back to their original targets) or in motor neurons or dorsal root ganglion neurons denied axon regeneration (e.g., by transection and ligation), chromatolysis is often accompanied by degranulation (loss of ribosomes from rough endoplasmic reticulum), disaggregation of polyribosomes and degradation of monoribosomes into dust-like particles. Ribosomes and rough endoplasmic reticulum may also be degraded in autophagic vacuoles by ribophagy and reticulophagy, respectively. In other words, chromatolysis is disruption of parts of the protein synthesis infrastructure. Whereas some neurons may show transient or no chromatolysis, severely injured neurons can remain chromatolytic and never again synthesize normal levels of protein; some may atrophy or die. Ribonuclease(s) might cause the following features of chromatolysis: fragmentation and degranulation of rough endoplasmic reticulum, disaggregation of polyribosomes and degradation of monoribosomes. For example, ribonucleases in the EndoU/PP11 family can modify rough endoplasmic reticulum; many ribonucleases can degrade mRNA causing polyribosomes to unchain and disperse, and they can disassemble monoribosomes; Ribonuclease 5 can control rRNA synthesis and degrade tRNA; Ribonuclease T2 can degrade ribosomes, endoplasmic reticulum and RNA within autophagic vacuoles; and Ribonuclease IRE1α acts as a stress sensor within the endoplasmic reticulum. Regeneration might be improved after axonal injury by protecting the protein synthesis machinery from catabolism; targeting ribonucleases using inhibitors can enhance neurite outgrowth and could be a profitable strategy in vivo. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018.

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Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

Section: Injury To Mammalian Axons Can Cause a Transient Or Persistenmentioning

confidence: 99%

Section: Might Attenuation Of Chromatolysis Be Therapeutically Benefimentioning

confidence: 99%

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Chromatolysis: Do injured axons regenerate poorly when ribonucleases attack rough endoplasmic reticulum, ribosomes and RNA?

Moon

2018

Developmental Neurobiology

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Schwann Cell‐Specific Ablation of Beclin 1 Impairs Myelination and Leads to Motor and Sensory Neuropathy in Mice

Gambarotto,

Russo,

Bresolin

et al. 2024

Advanced Science

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The core component of the class III phosphatidylinositol 3‐kinase complex, Beclin 1, takes part in different protein networks, thus switching its role from inducing autophagy to regulating autophagosomal maturation and endosomal trafficking. While assessed in neurons, astrocytes, and microglia, its role is far less investigated in myelinating glia, including Schwann cells (SCs), responsible for peripheral nerve myelination. Remarkably, the dysregulation in endosomal trafficking is emerging as a pathophysiological mechanism underlying peripheral neuropathies, such as demyelinating Charcot‐Marie‐Tooth (CMT) diseases. By knocking out Beclin 1 in SCs here a novel mouse model (Becn1 cKO) is generated, developing a severe and progressive neuropathy, accompanied by involuntary tremors, body weight loss, and premature death. Ultrastructural analysis revealed abated myelination and SCs displaying enlarged cytoplasm with progressive accumulation of intracellular vesicles. Transcriptomic and histological analysis from sciatic nerves of 10‐day and 2‐month‐old mice revealed pro‐mitotic gene deregulation and increased SCs proliferation at both stages with axonal loss and increased immune infiltration in adults, well reflecting the progressive motor and sensory functional impairment that characterizes Becn1 cKO mice, compared to controls. The study establishes a further step in understanding key mechanisms in SC development and points to Beclin 1 and its regulated pathways as targets for demyelinating CMT forms.

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The histomorphological and stereological assessment of rat dorsal root ganglion tissues after various types of sciatic nerve injury

Delibaş,

Kaplan

2023

Histochem Cell Biol

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Peripheral nerve injuries lead to signi cant changes in the dorsal root ganglia, where the cell bodies of the damaged axons are located. The sensory neurons and the surrounding satellite cells rearrange the composition of the intracellular organelles to enhance their plasticity for adaptation to changing conditions and responding to injury. Meanwhile, satellite cells acquire phagocytic properties and work with macrophages to eliminate degenerated neurons. These structural and functional changes are not identical in all injury types. Understanding the cellular response, which varies according to the type of injury involved, is essential in determining the optimal method of treatment. In this research, we investigated the numerical and morphological changes in primary sensory neurons and satellite cells in the dorsal root ganglion 30 days following chronic compression, crush and transection injuries using stereology, high-resolution light microscopy, immunohistochemistry, and behavioral analysis techniques.Electron microscopic methods were employed to evaluate ne structural alterations in cells. Stereological evaluations revealed no statistically signi cant difference in terms of mean sensory neuron numbers (p > 0.05), although a signi cant decrease was observed in sensory neuron volumes in the transection and crush injury groups (p < 0.05). Active caspase-3 immunopositivity increased in the injury groups compared to the sham group (p < 0.05). While crush injury led to desensitization, chronic compression injury caused thermal hyperalgesia. Electromyography parameters exhibited a signi cant decrease in the compression and crush injury groups compared to the sham group (p < 0.05). Macrophage in ltrations were observed in all injury types. Electron microscopic results revealed that the chromatolysis response was triggered in the sensory neuron bodies from the transection injury group. An increase in organelle density was observed in the perikaryon of sensory neurons after crush-type injury. This indicates the presence of a more active regeneration process in crush-type injury than in other types. The effect of chronic compression injury is more devastating than that of crush-type injury, and the edema caused by compression signi cantly inhibits the regeneration process.

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Target-dependence of sensory neurons: An ultrastructural comparison of axotomised dorsal root ganglion neurons with allowed or denied reinnervation of peripheral targets

Cited by 16 publications

References 76 publications

Chromatolysis: Do injured axons regenerate poorly when ribonucleases attack rough endoplasmic reticulum, ribosomes and RNA?

Chromatolysis: Do injured axons regenerate poorly when ribonucleases attack rough endoplasmic reticulum, ribosomes and RNA?

Schwann Cell‐Specific Ablation of Beclin 1 Impairs Myelination and Leads to Motor and Sensory Neuropathy in Mice

The histomorphological and stereological assessment of rat dorsal root ganglion tissues after various types of sciatic nerve injury

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