Regulation of activity‐dependent dendritic vasopressin release from rat supraoptic neurones

Ludwig, Mike; Bull, Philip M.; Tobin, Vicky; Sabatier, Nancy; Landgraf, Rainer; Dayanithi, Govindan; Leng, Gareth

doi:10.1113/jphysiol.2005.083931

Cited by 103 publications

(95 citation statements)

References 41 publications

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“…Importantly and consistent with its described localization with VP in large dense core vesicles (Watson et al, 1982), dynorphin only acts as a retrograde transmitter in VPexpressing neurons and not in neighboring OT-expressing cells. VP itself has been shown to promote dendritic release (Ludwig et al, 2005), suggesting that initial dendritic secretion of dynorphin and VP may act to prime further dendritic release.…”

Section: Discussionmentioning

confidence: 99%

Retrograde Opioid Signaling Regulates Glutamatergic Transmission in the Hypothalamus

Iremonger¹,

Bains²

2009

J. Neurosci.

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Opioid signaling in the CNS is critical for controlling cellular excitability, yet the conditions under which endogenous opioid peptides are released and the precise mechanisms by which they affect synaptic transmission remain poorly understood. The opioid peptide dynorphin is present in the soma and dendrites of vasopressin neurons in the hypothalamus and dynamically controls the excitability of these cells in vivo. Here, we show that dynorphin is released from dendritic vesicles in response to postsynaptic activity and acts in a retrograde manner to inhibit excitatory synaptic transmission. This inhibition, which requires the activation of -opioid receptors, results from a reduction in presynaptic release of glutamate vesicles. The opioid inhibition is downstream of Ca 2ϩ entry and is likely mediated by a direct modulation of presynaptic fusion machinery. These findings demonstrate that neurons may self-regulate their excitability through the dendritic release of opioids to inhibit excitatory synaptic transmission.

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Section: Discussionmentioning

confidence: 99%

Retrograde Opioid Signaling Regulates Glutamatergic Transmission in the Hypothalamus

Iremonger¹,

Bains²

2009

J. Neurosci.

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“…To ascertain that SDF-1 is able to affect AVP release, the autoregulation of AVP release by AVP observed in vivo (20,21) has been reproduced in the in vitro perifusion system described here. Thus, we have used as an autocrine stimulus vasotocin, a structural analog of AVP, because it did not crossreact with the anti-AVP antibody used in the ELISA.…”

Section: Discussionmentioning

confidence: 99%

“…Mature AVP hypothalamic magnocellular neurons are known to autocontrol their electrical activity and release by somatodendritic release of the hormone (18)(19)(20)(21). We have used this specific property of AVP neurons to set up an in vitro perifusion model to induce AVP release physiologically.…”

mentioning

confidence: 99%

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

Callewaere

Banisadr

Desarménien

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Chemokines play a key role in inflammation. They are expressed not only in neuroinflammatory conditions, but also constitutively by different cell types, including neurons in the normal brain, suggesting that they may act as modulators of neuronal functions. Here, we investigated a possible neuroendocrine role of the chemokine stromal cell-derived factor 1 (SDF-1)͞CXCL12. We demonstrated the colocalization of SDF-1 and its receptor CXCR4 with arginine vasopressin (AVP) in the magnocellular neurons of the supraoptic nucleus (SON) and the paraventricular hypothalamic nucleus and on AVP projections to the neurohypophysis. Electrophysiological recordings of SON neurons demonstrated that SDF-1 affects the electrical activity of AVP neurons through CXCR4, resulting in changes in AVP release. We observed that SDF-1 can blunt the autoregulation of AVP release in vitro and counteract angiotensin II-induced plasma AVP release in vivo. Furthermore, a short-term physiological increase in AVP release induced by enhanced plasma osmolarity, which was produced by the administration of 1 M NaCl i.p., was similarly blocked by central injection of SDF-1 through CXCR4. A change in water balance by long-term salt loading induced a decrease in both SDF-1 and CXCR4 parallel to that of AVP immunostaining in SON. From these data, we demonstrate that chemokine actions in the brain are not restricted to inflammatory processes. We propose to add to the known autoregulation of AVP on its own neurons, a second autocrine system induced by SDF-1 able to modulate central AVP neuronal activity and release.dehydration ͉ hypothalamic magnocellular neurons ͉ neuroendocrine ͉ neuromodulation ͉ posterior pituitary A rginine vasopressin (AVP) and oxytocin (OT) are synthesized in the magnocellular neurosecretory neurons of the hypothalamic supraoptic nucleus (SON) and paraventricular nucleus (PVN) and then transported through the median eminence to the posterior lobe of the pituitary gland, where they are secreted into the general blood circulation. AVP is known to be primarily involved in water absorption in the distal nephron of the kidney, thus regulating drinking behavior, whereas the functions of OT during parturition to increase uterine contraction and during suckling have been well described (1).Chemokines are small, secreted molecules (7-14 kDa) with chemoattractant properties whose main accepted role is leukocyte recruitment in inflammatory sites (2, 3). Recent investigations into the possible involvement of chemokines in a number of neurological disorders associated with neuroinflammation have led to the possibility that many chemokines and their respective receptors can be expressed in the brain (4). However, recent data demonstrated that they not only are observed in neuroinflammatory conditions but also are constitutively expressed by different cell types, including neurons in the normal brain (5-7). These data suggest that chemokines may act as modulators of neuronal functions.Among chemokines and chemokine receptors with possible neuromo...

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“…Once triggered, dendritic peptide release can be self-sustaining and hence long-lasting [67]. Other agents that mobilize intracellular calcium stores, such as thapsigargin, can also evoke dendritic release of neuropeptides [67,68,92].…”

Section: (G) Intracellular Calcium Storesmentioning

confidence: 99%

Multiple signalling modalities mediated by dendritic exocytosis of oxytocin and vasopressin

Ludwig

Stern

2015

Phil. Trans. R. Soc. B

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The mammalian hypothalamic magnocellular neurons of the supraoptic and paraventricular nuclei are among the best understood of all peptidergic neurons. Through their anatomical features, vasopressin-and oxytocincontaining neurons have revealed many important aspects of dendritic functions. Here, we review our understanding of the mechanisms of somato-dendritic peptide release, and the effects of autocrine, paracrine and hormone-like signalling on neuronal networks and behaviour. Of secret messages and public announcementsForms of information processing and intercellular communication in the brain may be classified, at least in part, according to distinct spatio-temporal features. At one end of the spectrum is classical chemical synaptic transmission. Chemical synapses are structurally organized units with a well-defined physical substrate and have evolved to transfer information between pairs of neurons efficiently, in a precise, spatially constrained and rapid manner. The strength and time course of this 'hard-wired' communication is dependent on the probability of presynaptic transmitter release, the affinity of the postsynaptic receptors for the transmitter, the density of postsynaptic receptors clustered at highly specialized sites, and the rate of diffusion/uptake of the neurotransmitter at/from the synaptic cleft [1][2][3][4].At the opposite end of the spatio-temporal spectrum, paracrine or hormonelike signalling modalities mediate transfer of information between entire populations of neurons, which in some cases may be located relatively distant from each other, acting in a more diffuse, less spatially constrained manner and on a slower time scale. In the hard-wired chemical synapse, the 'secrecy' of the communication is largely determined by the spatially constrained structure of the synapse. Conversely, in paracrine transmission, specificity is solely determined by the specificity of the signal -receptor interaction. Examples of signalling mechanisms acting at more distant sites include release of catecholamines and acetylcholine from en passant boutons on axonal segments [5], and gaseous neurotransmitters, including nitric oxide and carbon monoxide [6]. However, the prototypes for hormone-like signalling within the brain are many neuropeptides, including vasopressin and oxytocin, released from their somata and dendrites. They are public announcements; they are messages not from one cell to another, but rather a message that is directed from one population of neurons to another [7][8][9].2. The hypothalamo-neurohypophysial axis: a model system to study dendritic peptide releaseThe dendrites of magnocellular neurons (MCNs) of the hypothalamic supraoptic nucleus (SON) and paraventricular nucleus (PVN) have some unique characteristics compared with other neurons in the central nervous system. They are aspiny, branch sparsely, in many cases are aggregated in bundles, and are

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Regulation of activity‐dependent dendritic vasopressin release from rat supraoptic neurones

Cited by 103 publications

References 41 publications

Retrograde Opioid Signaling Regulates Glutamatergic Transmission in the Hypothalamus

Retrograde Opioid Signaling Regulates Glutamatergic Transmission in the Hypothalamus

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

Multiple signalling modalities mediated by dendritic exocytosis of oxytocin and vasopressin

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