Plasticity of neurohypophysial terminals with increased hormonal release during dehydration: Ultrastructural and biochemical analyses

Abstract

Arginine vasopressin- (AVP) and oxytocin- (OXT) secreting magnocellular neurons undergo gross structural changes with chronic physiological stimulation. Here, we investigated subcellular aspects of plasticity in rat neurohypophysial terminals during dehydration. Ultrastructural analyses demonstrated that chronic dehydration by 2% NaCl drinking for 7 days significantly decreased the numbers of neurosecretory granules and microvesicles but not the numbers of mitochondria. Moreover, in dehydrated rats, terminals making neurovascular contacts enlarged, whereas terminals in apposition to astrocytes, i.e., neuroglial contacts, became smaller. Western blot analyses demonstrated significant decreases in the levels of F3 and Thy-1 together with those of AVP- and OXT-neurophysin, but the levels of synaptophysin, SNAP-25, and GAP-43 were unchanged. Both F3 and Thy-1 were recovered in the buffer-insoluble pellet, and phosphatidyl inositol-specific phospholipase C treatment released both molecules from the crude membrane fraction, indicating that they are attached to terminal membranes by glycosylphosphatidyl inositol anchors. Confocal microscopic observations demonstrated that F3 colocalized with Thy-1 in the same terminals of magnocellular neurons. In contrast, the level of calretinin, a Ca(2+) binding protein was significantly increased with chronic dehydration. Thus, the present results suggest that enhancement of neurovascular contacts results from rearrangement of terminal-astrocyte and terminal-vessel contacts rather than enlargement or sprouting of magnocellular terminals themselves. The down-regulation of F3 and Thy-1 may contribute to enhancement of neurovascular contacts that accompany increased peptide release during dehydration.

Transcription Factor Expression in the Hypothalamo-Neurohypophyseal System of the Dehydrated Rat: Upregulation of Gonadotrophin Inducible Transcription Factor 1 mRNA Is Mediated by cAMP-Dependent Protein Kinase A

“…A plethora of activity-dependent changes in the morphology, electrical properties, and biosynthetic and secretory activity of the HNS have been described (Sharman et al, 2004). For example, alterations in the relationship between MCNs and glia, the extent of terminal contact with the basal lamina in the neurohypophysis, the type and weight of synaptic inputs, and the extent of electrotonic coupling between MCNs have all been documented (Tanaka et al, 1999;Yang and Hatton, 1999;Miyata et al, 2001a;Miyata and Hatton, 2002;Tasker et al, 2002). The response of the HNS to dehydration represents a unique and tractable model for understanding the processes whereby changes in gene expression mediate neuronal plasticity (Sharman et al, 2004), but the molecular mechanics of these processes remain to be elucidated.…”

A comprehensive description of the transcriptome of the hypothalamoneurohypophyseal system in euhydrated and dehydrated rats

“…15), all of which might contribute to the facilitation of hormone production and delivery and, hence, the survival of the organism. For example, alterations in the relationship between MCNs and glia, the extent of terminal contact with the basal lamina in the neurohypophysis, the type and weight of synaptic inputs, and the extent of electrotonic coupling between MCNs have all been documented (16)(17)(18)(19)(20). This plasticity appears to be governed by a complex and dynamic interplay between the intrinsic properties of the MCN, interactions between MCNs, interactions with glia, and the influences of extrinsic synaptic inputs.…”

VEGF-dependent and PDGF-dependent dynamic neurovascular reconstruction in the neurohypophysis of adult mice

“…Moreover, the withdrawal of AZD2171 treatment increased the number of BrdU-labeled endothelial cells and rapidly returned to the control level, while such dramatic rebound proliferation was not observed after the withdrawal of the PDGFR inhibitor STI571. There is no doubt that the surface of the vascular basement membrane is important for neurosecretion to interact with axonal terminals of AVP-and OXT-containing neurons (Tweedle & Hatton 1987, Miyata et al 2001, Miyata & Hatton 2002. Thus, these experiments demonstrate that VEGF signaling is a crucial mediator for proliferation and apoptosis of endothelial cells, indicating the presence of VEGF-dependent regulatory mechanism to control the vascular density in the NH of adult mice.…”

“…Under unstimulated conditions, pituicytes or neurohypophysial astrocytes generally enclose axonal terminals, while the chronic physiological stimulations increase direct contact of axonal terminals with vascular basement membrane (Miyata et al 2001, Miyata & Hatton 2002. This structural reconstruction has been considered to be caused mainly by shape conversion of pituicytes via the b-adrenergic receptor (Smithson et al 1990).…”