Physiology of spontaneous [Ca(2+)]i oscillations in the isolated vasopressin and oxytocin neurones of the rat supraoptic nucleus
Jazyk angličtina Země Nizozemsko Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
27072326
PubMed Central
PMC4969632
DOI
10.1016/j.ceca.2016.04.001
PII: S0143-4160(16)30038-0
Knihovny.cz E-zdroje
- Klíčová slova
- Ca(2+) oscillations, Dehydration, Electrical activity, Enhanced green fluorescence protein, Fluorescence spectrofluorimetry, Fura-2, Hyper-osmolarity, Hypo-osmolarity, Hypothalamus, Lactation, Magnocellular neurosecretory cells, Monomeric red fluorescence protein, Osmoregulation, Oxytocin, Skewness, Spationtemporal dynamics, Supraoptic nucleus, Transgenic rats, Vasopressin,
- MeSH
- dehydratace MeSH
- neurony metabolismus MeSH
- nucleus supraopticus metabolismus MeSH
- osmolární koncentrace MeSH
- oxytocin metabolismus MeSH
- potkani Wistar MeSH
- vápník metabolismus MeSH
- vápníková signalizace * MeSH
- vasopresiny metabolismus MeSH
- zelené fluorescenční proteiny metabolismus MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- enhanced green fluorescent protein MeSH Prohlížeč
- oxytocin MeSH
- vápník MeSH
- vasopresiny MeSH
- zelené fluorescenční proteiny MeSH
The magnocellular vasopressin (AVP) and oxytocin (OT) neurones exhibit specific electrophysiological behaviour, synthesise AVP and OT peptides and secrete them into the neurohypophysial system in response to various physiological stimulations. The activity of these neurones is regulated by the very same peptides released either somato-dendritically or when applied to supraoptic nucleus (SON) preparations in vitro. The AVP and OT, secreted somato-dendritically (i.e. in the SON proper) act through specific autoreceptors, induce distinct Ca(2+) signals and regulate cellular events. Here, we demonstrate that about 70% of freshly isolated individual SON neurones from the adult non-transgenic or transgenic rats bearing AVP (AVP-eGFP) or OT (OT-mRFP1) markers, produce distinct spontaneous [Ca(2+)]i oscillations. In the neurones identified (through specific fluorescence), about 80% of AVP neurones and about 60% of OT neurones exhibited these oscillations. Exposure to AVP triggered [Ca(2+)]i oscillations in silent AVP neurones, or modified the oscillatory pattern in spontaneously active cells. Hyper- and hypo-osmotic stimuli (325 or 275 mOsmol/l) respectively intensified or inhibited spontaneous [Ca(2+)]i dynamics. In rats dehydrated for 3 or 5days almost 90% of neurones displayed spontaneous [Ca(2+)]i oscillations. More than 80% of OT-mRFP1 neurones from 3 to 6-day-lactating rats were oscillatory vs. about 44% (OT-mRFP1 neurones) in virgins. Together, these results unveil for the first time that both AVP and OT neurones maintain, via Ca(2+) signals, their remarkable intrinsic in vivo physiological properties in an isolated condition.
Zobrazit více v PubMed
Cazalis M., Dayanithi G., Nordmann J.J. The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. J. Physiol. 1985;369:45–60. PubMed PMC
Cazalis M., Dayanithi G., Nordmann J.J. Requirements for hormone release from permeabilized nerve endings isolated from the rat neurohypophysis. J. Physiol. 1987;390:71–91. PubMed PMC
Cazalis M., Dayanithi G., Nordmann J.J. Hormone release from isolated nerve endings of the rat neurohypophysis. J. Physiol. 1987;390:55–70. PubMed PMC
Brethes D., Dayanithi G., Letellier L., Nordmann J.J. Depolarization-induced Ca2+ increase in isolated neurosecretory nerve terminals measured with fura-2. Proc. Natl. Acad. Sci. U. S. A. 1987;84:1439–1443. PubMed PMC
Dayanithi G., Cazalis M., Nordmann J.J. Relaxin affects the release of oxytocin and vasopressin from the neurohypophysis. Nature. 1987;325:813–816. PubMed
Gouzenes L., Sabatier N., Richard P., Moos F.C., Dayanithi G. V1a- and V2-type vasopressin receptors mediate vasopressin-induced Ca2+ responses in isolated rat supraoptic neurones. J. Physiol. 1999;517(Pt 3):771–779. PubMed PMC
Moos F., Gouzenes L., Brown D., Dayanithi G., Sabatier N., Boissin L., Rabie A., Richard P. New aspects of firing pattern autocontrol in oxytocin and vasopressin neurones. Adv. Exp. Med. Biol. 1998;449:153–162. PubMed
Dayanithi G., Widmer H., Richard P. Vasopressin-induced intracellular Ca2+ increase in isolated rat supraoptic cells. J. Physiol. 1996;490(Pt 3):713–727. PubMed PMC
Sabatier N., Richard P., Dayanithi G. L-, N- and T- but neither P- nor Q-type Ca2+ channels control vasopressin-induced Ca2+ influx in magnocellular vasopressin neurones isolated from the rat supraoptic nucleus. J. Physiol. 1997;503(Pt 2):253–268. PubMed PMC
Sabatier N., Richard P., Dayanithi G. Activation of multiple intracellular transduction signals by vasopressin in vasopressin-sensitive neurones of the rat supraoptic nucleus. J. Physiol. 1998;513(Pt 3):699–710. PubMed PMC
Lambert R.C., Dayanithi G., Moos F.C., Richard P. A rise in the intracellular Ca2+ concentration of isolated rat supraoptic cells in response to oxytocin. J. Physiol. 1994;478(Pt 2):275–287. PubMed PMC
Dayanithi G., Sabatier N., Widmer H. Intracellular calcium signalling in magnocellular neurones of the rat supraoptic nucleus: understanding the autoregulatory mechanisms. Exp. Physiol. 2000;85:75s–84s. PubMed
Ludwig M., Sabatier N., Bull P.M., Landgraf R., Dayanithi G., Leng G. Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites. Nature. 2002;418:85–89. PubMed
Komori Y., Tanaka M., Kuba M., Ishii M., Abe M., Kitamura N., Verkhratsky A., Shibuya I., Dayanithi G. Ca2+ homeostasis, Ca2+ signalling and somatodendritic vasopressin release in adult rat supraoptic nucleus neurones. Cell Calcium. 2010;48:324–332. PubMed
Dayanithi G., Forostyak O., Ueta Y., Verkhratsky A., Toescu E.C. Segregation of calcium signalling mechanisms in magnocellular neurones and terminals. Cell Calcium. 2012;51:293–299. PubMed
Oliet S.H., Bourque C.W. Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature. 1993;364:341–343. PubMed
Bourque C.W., Renaud L.P. Activity patterns and osmosensitivity of rat supraoptic neurones in perfused hypothalamic explants. J. Physiol. 1984;349:631–642. PubMed PMC
Prager-Khoutorsky M., Bourque C.W. Osmosensation in vasopressin neurons: changing actin density to optimize function. Trends Neurosci. 2010;33:76–83. PubMed
Mason W.T. Supraoptic neurones of rat hypothalamus are osmosensitive. Nature. 1980;287:154–157. PubMed
Wakerley J.B., Poulain D.A., Brown D. Comparison of firing patterns in oxytocin- and vasopressin-releasing neurones during progressive dehydration. Brain Res. 1978;148:425–440. PubMed
Ueta Y., Dayanithi G., Fujihara H. Hypothalamic vasopressin response to stress and various physiological stimuli: visualization in transgenic animal models. Horm. Behav. 2011;59:221–226. PubMed
Jamen F., Alonso G., Shibuya I., Widmer H., Vacher C.M., Calas A., Bockaert J., Brabet P., Dayanithi G. Impaired somatodendritic responses to pituitary adenylate cyclase-activating polypeptide (PACAP) of supraoptic neurones in PACAP type I—receptor deficient mice. J. Neuroendocrinol. 2003;15:871–881. PubMed
Sabatier N., Shibuya I., Dayanithi G. Intracellular calcium increase and somatodendritic vasopressin release by vasopressin receptor agonists in the rat supraoptic nucleus: involvement of multiple intracellular transduction signals. J. Neuroendocrinol. 2004;16:221–236. PubMed
Ueta Y., Fujihara H., Serino R., Dayanithi G., Ozawa H., Matsuda K., Kawata M., Yamada J., Ueno S., Fukuda A., Murphy D. Transgenic expression of enhanced green fluorescent protein enables direct visualization for physiological studies of vasopressin neurons and isolated nerve terminals of the rat. Endocrinology. 2005;146:406–413. PubMed
Katoh A., Fujihara H., Ohbuchi T., Onaka T., Hashimoto T., Kawata M., Suzuki H., Ueta Y. Highly visible expression of an oxytocin-monomeric red fluorescent protein 1 fusion gene in the hypothalamus and posterior pituitary of transgenic rats. Endocrinology. 2011;152:2768–2774. PubMed
Viero C., Shibuya I., Kitamura N., Verkhratsky A., Fujihara H., Katoh A., Ueta Y., Zingg H.H., Chvatal A., Sykova E., Dayanithi G. Review: Oxytocin: crossing the bridge between basic science and pharmacotherapy. CNS Neurosci. Ther. 2010;16:e138–156. PubMed PMC
Moriya T., Shibasaki R., Kayano T., Takebuchi N., Ichimura M., Kitamura N., Asano A., Hosaka Y.Z., Forostyak O., Verkhratsky A., Dayanithi G., Shibuya I. Full-length transient receptor potential vanilloid 1 channels mediate calcium signals and possibly contribute to osmoreception in vasopressin neurones in the rat supraoptic nucleus. Cell Calcium. 2015;57:25–37. PubMed
Grynkiewicz G., Poenie M., Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985;260:3440–3450. PubMed
Dayanithi G., Mechaly I., Viero C., Aptel H., Alphandery S., Puech S., Bancel F., Valmier J. Intracellular Ca2+ regulation in rat motoneurons during development. Cell Calcium. 2006;39:237–246. PubMed
Viero C., Mechaly I., Aptel H., Puech S., Valmier J., Bancel F., Dayanithi G. Rapid inhibition of Ca2+ influx by neurosteroids in murine embryonic sensory neurones. Cell Calcium. 2006;40:383–391. PubMed
Forostyak O., Romanyuk N., Verkhratsky A., Sykova E., Dayanithi G. Plasticity of calcium signaling cascades in human embryonic stem cell-derived neural precursors. Stem Cells Dev. 2013;22:1506–1521. PubMed PMC
Oliet S.H., Bourque C.W. Properties of supraoptic magnocellular neurones isolated from the adult rat. J. Physiol. 1992;455:291–306. PubMed PMC
Trudel E., Bourque C.W. Circadian modulation of osmoregulated firing in rat supraoptic nucleus neurones. J. Neuroendocrinol. 2012;24:577–586. PubMed
Knight W.D., Ji L.L., Little J.T., Cunningham J.T. Dehydration followed by sham rehydration contributes to reduced neuronal activation in vasopressinergic supraoptic neurons after water deprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010;299:R1232–1240. PubMed PMC
Nordmann J.J., Cazalis M., Dayanithi G., Castanas E., Giraud P., Legros J.J., Louis F. Are opioid peptides co-localized with vasopressin or oxytocin in the neural lobe of the rat? Cell Tissue Res. 1986;246:177–182. PubMed
Huang W.C., Ploth D.W., Navar L.G. Angiotensin-mediated alterations in nephron function in goldblatt hypertensive rats. Am. J. Physiol. 1982;243:F553–F560. PubMed
Moos F.C., Rossi K., Richard P. Activation of N-methyl-d-aspartate receptors regulates basal electrical activity of oxytocin and vasopressin neurons in lactating rats. Neuroscience. 1997;77:993–1002. PubMed
Chevaleyre V., Dayanithi G., Moos F.C., Desarmenien M.G. Developmental regulation of a local positive autocontrol of supraoptic neurons. J. Neurosci. 2000;20:5813–5819. PubMed PMC
Ludwig M., Bull P.M., Tobin V.A., Sabatier N., Landgraf R., Dayanithi G., Leng G. Regulation of activity-dependent dendritic vasopressin release from rat supraoptic neurones. J. Physiol. 2005;564:515–522. PubMed PMC