Peripheral facial nerve axotomy in mice causes sprouting of motor axons into perineuronal central white matter: Time course and molecular characterization

Makwana, Milan; Werner, Alexander; Acosta-Saltos, A; Gonitel, Roman; Pararajasingham, Abirami; Ruff, Crystal A.; Rumajogee, Prakasham; Cuthill, Dan; Galiano, Mathias; Bohatschek, Marion; Wallace, Adam S.; Anderson, Patrick N.; Mayer, Ulríke; Behrens, Axel; Raivich, Gennadij

doi:10.1002/cne.23113

Cited by 4 publications

(5 citation statements)

References 72 publications

(110 reference statements)

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“…Our observation of CD44 expression in the periphery of motor neurons is in agreement with previous studies showing its presence in the plasma membrane of neurons (Jones et al, ). Although the function played by CD44 in motor neurons is not clear, some authors suggest that its presence in regenerative axons may indicate a putative role in regulation of axonal outgrowth (Makwana et al, ). The fact that GFAP‐IL6Tg animals showed less expression of both CD44 and CD49e receptors at the time‐points where the neuronal wrapping and synaptic stripping has been described, lead us to speculate that the increase in neuronal death observed in GFAP‐IL6Tg animals could be due to a deficient attachment of microglia and/or lymphocytes to neurons.…”

Section: Discussionmentioning

confidence: 99%

Effects of astrocyte‐targeted production of interleukin‐6 in the mouse on the host response to nerve injury

Almolda

Villacampa

Manders

et al. 2014

Glia

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Interleukin-6 (IL-6) is a pleiotropic cytokine with a key role in the control of inflammatory/immune responses. In the central nervous system (CNS), an increase in IL-6 occurs in a wide range of pathological conditions such as excitotoxicity and traumatic brain injury. We evaluated the effects of astrocyte-targeted production of IL-6 in the CNS in the sterile-nerve injury model of facial nerve axotomy. To accomplish this, facial nerve transection was performed in transgenic mice (glial fibrillary acidic protein [GFAP]-IL6Tg) with IL-6 production under the GFAP promoter. Neuronal death, glial activation, lymphocyte recruitment, and integrin expression were evaluated by immunohistochemistry and flow cytometry from 3 to 28 days postinjury. Our findings revealed an increase in motor neuron cell death in GFAP-IL6Tg mice correlating with changes in the microglial activation pattern, characterized principally by less attachment to neurons and reduced expression of both CD11b and CD18. We also found a higher CD4(+) T-lymphocyte recruitment in GFAP-IL6Tg mice. In addition, changes in the expression pattern of different integrins and their receptors were observed in transgenic animals. Specifically, alterations in osteopontin expression in motor neurons and its receptors CD44 and CD49e in lymphocytes and microglia, respectively, which may account for the variations related to glial reactivity and lymphocyte infiltration. In conclusion, our results indicated that forced local production of IL-6 has a direct impact on the outcome of nerve injury in the CNS inducing an increase in neurodegeneration, changes in glial response, and lymphocyte recruitment as well as in the expression of different integrins and their receptors.

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Section: Discussionmentioning

confidence: 99%

Effects of astrocyte‐targeted production of interleukin‐6 in the mouse on the host response to nerve injury

Almolda

Villacampa

Manders

et al. 2014

Glia

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“…We have shown that immunostaining with the galanin and NPY antibodies in the dorsal horn can be abolished by pre-incubation with the corresponding peptide [26,28]. It has also been reported that neuronal staining with the galanin antibody is absent in the brains of galanin knock-out mice [52]. The nNOS antibody labels a band of 155 kDa in Western blots of rat hypothalamus, and immunostaining is abolished by pre-incubation in nNOS [41].…”

Section: Methodsmentioning

confidence: 99%

Galanin-Immunoreactivity Identifies a Distinct Population of Inhibitory Interneurons in Laminae I-III of the Rat Spinal Cord

et al. 2011

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BackgroundInhibitory interneurons constitute 30-40% of neurons in laminae I-III and have an important anti-nociceptive role. However, because of the difficulty in classifying them we know little about their organisation. Previous studies have identified 3 non-overlapping groups of inhibitory interneuron, which contain neuropeptide Y (NPY), neuronal nitric oxide synthase (nNOS) or parvalbumin, and have shown that these differ in postsynaptic targets. Some inhibitory interneurons contain galanin and the first aim of this study was to determine whether these form a different population from those containing NPY, nNOS or parvalbumin. We also estimated the proportion of neurons and GABAergic axons that contain galanin in laminae I-III.ResultsGalanin cells were concentrated in laminae I-IIo, with few in laminae IIi-III. Galanin showed minimal co-localisation with NPY, nNOS or parvalbumin in laminae I-II, but most galanin-containing cells in lamina III were nNOS-positive. Galanin cells constituted ~7%, 3% and 2% of all neurons in laminae I, II and III, and we estimate that this corresponds to 26%, 10% and 5% of the GABAergic neurons in these laminae. However, galanin was only found in ~6% of GABAergic boutons in laminae I-IIo, and ~1% of those in laminae IIi-III.ConclusionsThese results show that galanin, NPY, nNOS and parvalbumin can be used to define four distinct neurochemical populations of inhibitory interneurons. Together with results of a recent study, they suggest that the galanin and NPY populations account for around half of the inhibitory interneurons in lamina I and a quarter of those in lamina II.

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“…The parvalbumin antibody was raised against mouse parvalbumin and recognises a single band of 13 kDa in blots of mouse brain homogenates [65]. The galanin antibody detects rat galanin, but not substance P, vasoactive intestinal polypeptide or NPY (manufacturer's specification), and it has been reported that staining with this antibody is absent from the brains of galanin knock-out mice [70]. The mouse monoclonal VGAT antibody (raised against amino acids 75-87 of mouse VGAT) labels a single band of 57 kDa in blots of mouse brain and retina, and immunostaining is blocked by preabsorption with the immunising peptide [71].…”

Section: Characterisation Of Antibodiesmentioning

confidence: 99%

Dynorphin is Expressed Primarily by GABAergic Neurons That Contain Galanin in the Rat Dorsal Horn

et al. 2011

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BackgroundThe opioid peptide dynorphin is expressed by certain neurons in the superficial dorsal horn of the spinal cord, but little is known about the types of cell that contain dynorphin. In this study, we have used an antibody against the dynorphin precursor preprodynorphin (PPD), to reveal the cell bodies and axons of dynorphin-expressing neurons in the rat spinal cord. The main aims were to estimate the proportion of neurons in each of laminae I-III that express dynorphin and to determine whether they are excitatory or inhibitory neurons.ResultsPPD-immunoreactive cells were concentrated in lamina I and the outer part of lamina II (IIo), where they constituted 17% and 8%, respectively, of all neurons. Around half of those in lamina I and 80% of those in lamina II were GABA-immunoreactive. We have previously identified four non-overlapping neurochemical populations of inhibitory interneurons in this region, defined by the presence of neuropeptide Y, galanin, parvalbumin and neuronal nitric oxide synthase. PPD co-localised extensively with galanin in both cell bodies and axons, but rarely or not at all with the other three markers. PPD was present in around 4% of GABAergic boutons (identified by the presence of the vesicular GABA transporter) in laminae I-II.ConclusionsThese results show that most dynorphin-expressing cells in the superficial dorsal horn are inhibitory interneurons, and that they largely correspond to the population that is defined by the presence of galanin. We estimate that dynorphin is present in ~32% of inhibitory interneurons in lamina I and 11% of those in lamina II. Since the proportion of GABAergic boutons that contain PPD in these laminae was considerably lower than this, our findings suggest that these neurons may generate relatively small axonal arborisations.

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Peripheral facial nerve axotomy in mice causes sprouting of motor axons into perineuronal central white matter: Time course and molecular characterization

Cited by 4 publications

References 72 publications

Effects of astrocyte‐targeted production of interleukin‐6 in the mouse on the host response to nerve injury

Effects of astrocyte‐targeted production of interleukin‐6 in the mouse on the host response to nerve injury

Galanin-Immunoreactivity Identifies a Distinct Population of Inhibitory Interneurons in Laminae I-III of the Rat Spinal Cord

Dynorphin is Expressed Primarily by GABAergic Neurons That Contain Galanin in the Rat Dorsal Horn

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