Reduction in nerve growth factor availability leads to a conditioning lesion‐like effect in sympathetic neurons

Shoemaker, S.E.; Sachs, H. Hyatt; Vaccariello, Stacey A.; Zigmond, Richard E.

doi:10.1002/neu.20297

Cited by 15 publications

(12 citation statements)

References 113 publications

(135 reference statements)

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“…Subsequently, it was found that a prior lesion in vivo also increased the rate of neurite outgrowth observed in vitro in explants of sensory ganglia and in cultures of dissociated sensory neurons (Hu-Tsai et al, 1994; Edstrom et al, 1996). Similar increases in neurite outgrowth have recently been shown to occur in sympathetic neurons both in ganglion explants and in dissociated cell cultures (Shoemaker et al, 2005; 2006). …”

Section: Introductionsupporting

confidence: 74%

The conditioning lesion effect on sympathetic neurite outgrowth is dependent on gp130 cytokines

Sachs¹,

Rohrer²,

Zigmond³

2010

Experimental Neurology

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Sympathetic neurons, like sensory neurons, increase neurite outgrowth after a conditioning lesion. Studies in leukemia inhibitory factor (LIF) knockout animals showed that the conditioning lesion effect in sensory neurons is dependent in part on this cytokine; however, similar studies on sympathetic neurons revealed no such effect. Comparable studies with sensory neurons taken from mice lacking the related cytokine interleukin-6 (IL-6) have yielded conflicting results. LIF and IL-6 belong to a family of cytokines known as the gp130 family because they act on receptors containing the subunit gp130. In sympathetic ganglia, axotomy leads to increases in mRNA for four of these cytokines (LIF, IL-6, IL-11, and on-costatin M). To test the role of this family of cytokines as a whole in the conditioning lesion response in sympathetic neurons, mice in which gp130 was selectively eliminated in noradrenergic neurons were studied. The postganglionic axons of the SCG were transected, and seven days later the ganglia were removed and neurite outgrowth was measured in explant and dissociated cell cultures. In both systems, neurons from wild type animals showed enhanced growth after a conditioning lesion. In contrast, no enhancement occurred in neurons from mutant animals. This lack of stimulation of outgrowth occurred despite an increase in expression of activating transcription factor 3 (ATF3) in the mutant mice. These studies demonstrate that stimulation of enhanced growth of sympathetic neurons after a conditioning lesion is dependent on gp130 cytokine signaling and is blocked in the absence of signaling by these cytokines in spite of an increase in ATF3.

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Section: Introductionsupporting

confidence: 74%

The conditioning lesion effect on sympathetic neurite outgrowth is dependent on gp130 cytokines

Sachs¹,

Rohrer²,

Zigmond³

2010

Experimental Neurology

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“…Nevertheless, the expression of BDNF, unlike that of NGF, is not upregulated by IL-1β (Meyer et al, 1992). Most availableevidence suggests that endogenous NGF does not promote regeneration (Diamond et al, 1987; Gloster and Diamond, 1992; Shoemaker et al, 2006; Lankford et al, 2013). On the other hand, heterozygote knockout animals indicate that endogenous BDNF and NT3 in non-neuronal cells do promote regeneration (Sahenk et al, 2008; Takemura et al, 2012).…”

Section: The Biology Of Wallerian Degenerationmentioning

confidence: 99%

The neuroimmunology of degeneration and regeneration in the peripheral nervous system

et al. 2015

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Peripheral nerves regenerate following injury due to the effective activation of the intrinsic growth capacity of the neurons and the formation of a permissive pathway for outgrowth due to Wallerian degeneration. Wallerian degeneration and subsequent regeneration are significantly influenced by various immune cells and the cytokines they secrete. Although macrophages have long been known to play a vital role in the degenerative process, recent work has pointed to their importance in influencing the regenerative capacity of peripheral neurons. In this review, we focus on the various immune cells, cytokines, and chemokines that make regeneration possible in the peripheral nervous system, with specific attention placed on the role macrophages play in this process.

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“…Using ELISA, Nagata and colleagues (1987) showed a decrease in total NGF protein in the rat SCG following both 24 hour and 7 day axotomy. Likewise, in another NGF ELISA study, a significant decrease in NGF in the mouse SCG was observed following a 7 day axotomy (Shoemaker et al, 2006). Though it is not clear exactly which NGF species were actually measured in these ELISA experiments, the decreases may be the result of reductions in the 22–24 kDa NGF species.…”

Section: Discussionmentioning

confidence: 79%

Changes in NGF and NT-3 protein species in the superior cervical ganglion following axotomy of postganglionic axons

et al. 2009

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Mature sympathetic neurons in the superior cervical ganglion (SCG) are regulated by target-derived neurotrophins such as nerve growth factor (NGF) and neurotrophin-3 (NT-3). High molecular weight NGF species and mature NT-3 are the predominant NGF and NT-3 protein isoforms in the SCG, yet it is unknown whether the presence of these species is dependent on intact connection with the target tissues. In an attempt to determine the role of peripheral targets in regulating the neurotrophin species found in the SCG, we investigated the NGF and NT-3 protein species present in the SCG following axotomy (transection) or injury of the post-ganglionic axons. Following a 7 day axotomy, the 22-24 kDa NGF species and the mature 14 kDa NT-3 species in the SCG were significantly reduced by 99% and 66% respectively, suggesting that intact connection with the target is necessary for the expression of these protein species. As expected, tyrosine hydroxylase (TH) protein in the SCG was significantly reduced by 80% at 7 days following axotomy. In order to distinguish between the effects of injury and loss of target connectivity, the SCG was examined following compression injury to the post-ganglionic nerves. Following injury, no reduction in the 22-24 kDa NGF or 14 kDa mature NT-3 species was observed in the SCG. TH protein was slightly, yet significantly, decreased in the SCG following injury. The findings of this study suggest that the presence of the 22-24 kDa NGF and mature 14 kDa NT-3 species in the SCG is dependent on connection with peripheral targets and may influence, at least in part, TH protein expression in adult sympathetic neurons.

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Reduction in nerve growth factor availability leads to a conditioning lesion‐like effect in sympathetic neurons

Cited by 15 publications

References 113 publications

The conditioning lesion effect on sympathetic neurite outgrowth is dependent on gp130 cytokines

The conditioning lesion effect on sympathetic neurite outgrowth is dependent on gp130 cytokines

The neuroimmunology of degeneration and regeneration in the peripheral nervous system

Changes in NGF and NT-3 protein species in the superior cervical ganglion following axotomy of postganglionic axons

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