Vasopressin Secretion: Osmotic and Hormonal Regulation by the Lamina Terminalis

Abstract

The lamina terminalis, located in the anterior wall of the third ventricle, is comprised of the subfornical organ, median preoptic nucleus (MnPO) and organum vasculosum of the lamina terminalis (OVLT). The subfornical organ and OVLT are two of the brain's circumventricular organs that lack the blood-brain barrier, and are therefore exposed to the ionic and hormonal environment of the systemic circulation. Previous investigations in sheep and rats show that this region of the brain has a crucial role in osmoregulatory vasopressin secretion and thirst. The effects of lesions of the lamina terminalis, studies of immediate-early gene expression and electrophysiological data show that all three regions of the lamina terminalis are involved in osmoregulation. There is considerable evidence that physiological osmoreceptors subserving vasopressin release are located in the dorsal cap region of the OVLT and possibly also around the periphery of the subfornical organ and in the MnPO. The circulating peptide hormones angiotensin II and relaxin also have access to peptide specific receptors (AT(1) and LGR7 receptors, respectively) in the subfornical organ and OVLT, and both angiotensin II and relaxin act on the subfornical organ to stimulate water drinking in the rat. Studies that combined neuroanatomical tracing and detection of c-fos expression in response to angiotensin II or relaxin suggest that both of these circulating peptides act on neurones within the dorsal cap of the OVLT and the periphery of the subfornical organ to stimulate vasopressin release.

The chemokine SDF-1/CXCL12 modulates the firing pattern of vasopressin neurons and counteracts induced vasopressin release through CXCR4

“…These CVOs, located in the walls of the brain ventricular system and forming the lamina terminalis, are highly vascularized structures lacking the blood-brain barrier (28). Not only do neurons of the lamina terminalis detect changes in plasma tonicity and send this information to the AVP-secreting neurons in SON and PVN, they also are the prime cerebral targets for AII to mediate AVP secretion (29,30). Thus, CXCR4 receptors may play an essential role in the neuroendocrine interconnection between circulating hormones and central brain structures, and they can be added to the numerous peptidergic G protein-coupled receptors found in the CVOs (31).…”

Osmoregulatory fluid intake but not hypovolemic thirst is intact in mice lacking angiotensin

“…Diaminobenzidine was used as the chromogen to visualize the final reaction product. Counts were made of cell nuclei exhibiting Fos-immunoreactivity (Fos-IR) in five osmoregulatory regions of the brain (8,30,33), the supraoptic nucleus (SON), hypothalamic paraventricular nucleus (PVN), organum vasculosum laminae terminalis (OVLT), the subfornical organ (SFO), and the median preoptic nucleus (MnPO) in each brain. Using an eyepiece fitted with a graticule to avoid repeat counting, we averaged the counts of cell nuclei exhibiting Fos-IR in three sections for each specific region, using corresponding rostrocaudal stereotaxic levels for the C57BL6 mouse brain (16) for the particular nuclei in each brain.…”

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

“…The antidiuretic hormone vasopressin (VP) is synthesized as part of a prepropeptide precursor in the cell bodies of SON and PVN MCNs (Brownstein et al, 1980;de Bree, 2000). This precursor is processed during anterograde axonal transportation to terminals in the posterior pituitary gland, in which biologically active VP is stored until mobilized for secretion; a rise in plasma osmolality is detected by intrinsic MCN osmoreceptor mechanisms (Bourque et al, 2002;Zhang and Bourque, 2003) and by specialized osmoreceptive neurons in the circumventricular organs that project to the MCNs (Bourque et al, 1994;Bourque, 1998;McKinley et al, 1999;Anderson et al, 2000;McKinley et al, 2004) that provide direct excitatory inputs (van den Pol et al, 1990) to shape the firing activity of MCNs (Hu and Bourque, 1992;Nissen et al, 1994) for hormone secretion (Dyball et al, 1995;Onaka and Yagi, 2001). On release, VP travels through the blood stream to specific receptor targets located in the kidney in which it increases the permeability of the collecting ducts to water, reducing the renal excretion of water, thus promoting water conservation.…”