Articlehybrid2007

Interaction of Extracellular Signal-Regulated Protein Kinase 1/2 with Actin Cytoskeleton in Supraoptic Oxytocin Neurons and Astrocytes: Role in Burst Firing

51 citations0/0 files storedJournal of Neuroscience

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Neuroendocrine regulation and behavior Neuroscience and Neuropharmacology Research Protein Kinase Regulation and GTPase Signaling

Abstract

Neuronal firing patterns determine the manner of neurosecretion, the underlying mechanisms of which are poorly understood. Using supraoptic nuclei in brain slices from lactating rats, we examined the involvement of extracellular signal-regulated protein kinase 1/2 (ERK1/2) and filamentous actin (F-actin) in burst generation by oxytocin (OT) neurons. Blocking phosphorylation of ERK1/2 (pERK1/2) decreased miniature EPSCs and blocked OT-evoked bursts, as did intracellularly loading an antibody against pERK1/2. OT (10 pM) increased cytosolic pERK1/2 close to the cell membrane within the first 5 min, subsiding by 30 min, whereas OT elicited pERK1/2 nuclear translocation in closely associated supraoptic astrocytes. The increased pERK1/2 was tightly correlated with spatiotemporal actin dynamics. In OT neurons, OT initially increased F-actin, particularly at membrane subcortical areas, and then decreased it after 30 min. Both polymerization and depolymerization of actin cytoskeleton were associated with bursts, but only polymerization facilitated OT-evoked bursts. Blocking ERK1/2 activation blocked OT-evoked actin polymerization, whereas depolymerizing F-actin increased pERK1/2 expression. These changes were further identified in vivo. In intact animals, suckling increased ERK1/2 activation in the cytosol and membrane subcortical area F-actin formation in OT neurons, whereas it increased F-actin concentration in astrocytic somata. Coimmunoprecipitation showed that suckling increased molecular interactions between pERK1/2 and actin. Finally, two different blockers of ERK1/2 kinase injected intracerebroventricularly reduced suckling-evoked milk ejections. This is the first demonstration that OT mediation of suckling-evoked bursts/milk ejections is via interactions between pERK1/2 and actin cytoskeleton.

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References

2001The Oxytocin Receptor System: Structure, Function, and Regulation 1990Emerging concepts of structure-function dynamics in adult brain: The hypothalamo-neurohypophysial system 1995Morphological and electrophysiological classification of hypothalamic supraoptic neurons 1984Electrophysiological evidence for facilitatory control of oxytocin neurones by oxytocin during suckling in the rat.1992Neurochemical Regulation of Oxytocin Secretion in Lactation*1982Magnocellular neuropeptidergic neurons in hypothalamus: Increases in membrane apposition and number of specialized synapses from pregnancy to lactation 1994An oxytocin receptor antagonist infused into the supraoptic nucleus attenuates intranuclear and peripheral release of oxytocin during suckling in conscious rats 1981Excitatory effects of intraventricular injections of oxytocin on the milk ejection reflex in the rat

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