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Localization and dynamic changes of neuregulin-1 at C-type synaptic boutons in association with motor neuron injury and repair

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Issue date
2019
Author
Salvany, Sara
Casanovas i Llorens, Anna
Tarabal Mostazo, Olga
Piedrafita Llorens, Lídia
Hernández, Sara
Santafé Martínez, Manel
Soto-Bernardini, María Clara
Calderó i Pardo, Jordi
Schwab, Markus H.
Esquerda Colell, Josep
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Salvany, Sara; Casanovas i Llorens, Anna; Tarabal Mostazo, Olga; Piedrafita Llorens, Lídia; Hernández, Sara; Santafé Martínez, Manel; ... Esquerda Colell, Josep. (2019) . Localization and dynamic changes of neuregulin-1 at C-type synaptic boutons in association with motor neuron injury and repair. FASEB Journal, 2019, vol. 33, num. 7, p. 7833-7851. https://doi.org/10.1096/fj.201802329R.
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Abstract
C-type synaptic boutons (C-boutons) provide cholinergic afferent input to spinal cord motor neurons (MNs), which display an endoplasmic reticulum (ER)–related subsurface cistern (SSC) adjacent to their postsynaptic membrane. A constellation of postsynaptic proteins is clustered at C-boutons, including M2 muscarinic receptors, potassium channels, and s-1 receptors. In addition, we previously found that neuregulin (NRG)1 is associated with C-boutons at postsynaptic SSCs, whereas its ErbB receptors are located in the presynaptic compartment. Cbouton–mediated regulation of MN excitability has been implicated in MN disease, but NRG1-mediated functions and the impact of various pathologic conditions on C-bouton integrity have not been studied in detail. Here, we investigated changes inC-boutons after electrical stimulation,pharmacological treatment, and peripheral nerve axotomy. SSC-linked NRG1 clusters were severely disrupted in acutely stressedMNs and after tunicamycin-induced ER stress. In axotomized MNs, C-bouton loss occurred in concomitance with microglial recruitment and was prevented by the ER stress inhibitor salubrinal.Activatedmicroglia displayed apositive chemotaxis to C-boutons.Analysis of transgenicmice overexpressing NRG1 type I and type III isoforms in MNs indicated that NRG1 type III acts as an organizer of SSC-like structures, whereas NRG1 type I promotes synaptogenesis of presynaptic cholinergic terminals.Moreover,MN-derived NRG1 signals may regulate the activity of perineuronal microglial cells. Together, these data provide new insights into the molecular and cellular pathology of C-boutons in MN injury and suggest that distinct NRG1 isoform–mediated signaling functions regulate the complex matching between pre- and postsynaptic C-bouton elements.
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http://hdl.handle.net/10459.1/67775
DOI
https://doi.org/10.1096/fj.201802329R
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FASEB Journal, 2019, vol. 33, num. 7, p. 7833-7851
European research projects
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  • Articles publicats (IRBLleida) [1083]
  • Publicacions de projectes de recerca del Plan Nacional [2684]

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