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The Journal of Neuroscience, December 12, 2007, 27(50):13822-13834; doi:10.1523/JNEUROSCI.4119-07.2007

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

Yu-Feng Wang and Glenn I. Hatton

Department of Cell Biology and Neuroscience, University of California, Riverside, California 92521

Correspondence should be addressed to Yu-Feng Wang, Department of Cell Biology and Neuroscience, University of California, Riverside, CA 92521. Email: yufengw{at}ucr.edu

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.

Key words: coimmunoprecipitation; electrophysiology; immunocytochemistry; signal transduction; supraoptic nucleus; Western blots

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Received Oct. 5, 2006; revised Oct. 14, 2007; accepted Oct. 25, 2007.

Correspondence should be addressed to Yu-Feng Wang, Department of Cell Biology and Neuroscience, University of California, Riverside, CA 92521. Email: yufengw{at}ucr.edu

This article has been cited by other articles:

				Y.-F. Wang and G. I. Hatton Astrocytic Plasticity and Patterned Oxytocin Neuronal Activity: Dynamic Interactions J. Neurosci., February 11, 2009; 29(6): 1743 - 1754. [Abstract] [Full Text] [PDF]

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