Astrocytes Amplify Neuronal Dendritic Volume Transmission Stimulated by Norepinephrine

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2019 Dec 26

PMID 31875545

Citations 18

Authors

Chun Chen

Zhiying Jiang

Xin Fu

Diankun Yu

Hai Huang

Jeffrey G Tasker

Affiliations

Soon will be listed here.

Abstract

In addition to their support role in neurotransmitter and ion buffering, astrocytes directly regulate neurotransmission at synapses via local bidirectional signaling with neurons. Here, we reveal a form of neuronal-astrocytic signaling that transmits retrograde dendritic signals to distal upstream neurons in order to activate recurrent synaptic circuits. Norepinephrine activates α adrenoreceptors in hypothalamic corticotropin-releasing hormone (CRH) neurons to stimulate dendritic release, which triggers an astrocytic calcium response and release of ATP; ATP stimulates action potentials in upstream glutamate and GABA neurons to activate recurrent excitatory and inhibitory synaptic circuits to the CRH neurons. Thus, norepinephrine activates a retrograde signaling mechanism in CRH neurons that engages astrocytes in order to extend dendritic volume transmission to reach distal presynaptic glutamate and GABA neurons, thereby amplifying volume transmission mediated by dendritic release.

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References

Vahl T, Ulrich-Lai Y, Ostrander M, Dolgas C, Elfers E, Seeley R . Comparative analysis of ACTH and corticosterone sampling methods in rats. Am J Physiol Endocrinol Metab. 2005; 289(5):E823-8. DOI: 10.1152/ajpendo.00122.2005. View

Herman J, Mueller N, Figueiredo H . Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Ann N Y Acad Sci. 2004; 1018:35-45. DOI: 10.1196/annals.1296.004. View

Whitnall M, Smyth D, Gainer H . Vasopressin coexists in half of the corticotropin-releasing factor axons present in the external zone of the median eminence in normal rats. Neuroendocrinology. 1987; 45(5):420-4. DOI: 10.1159/000124768. View

Ulrich-Lai Y, Herman J . Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci. 2009; 10(6):397-409. PMC: 4240627. DOI: 10.1038/nrn2647. View

Mulligan S, MacVicar B . Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature. 2004; 431(7005):195-9. DOI: 10.1038/nature02827. View

Pascual O, Casper K, Kubera C, Zhang J, Revilla-Sanchez R, Sul J . Astrocytic purinergic signaling coordinates synaptic networks. Science. 2005; 310(5745):113-6. DOI: 10.1126/science.1116916. View

Kovacs K, Foldes A, Sawchenko P . Glucocorticoid negative feedback selectively targets vasopressin transcription in parvocellular neurosecretory neurons. J Neurosci. 2000; 20(10):3843-52. PMC: 6772698. View

Yamazaki R, Chen Q, SCHREIBER S, Brinton R . Localization of V1a vasopressin receptor mRNA expression in cultured neurons, astroglia, and oligodendroglia of rat cerebral cortex. Brain Res Mol Brain Res. 1997; 45(1):138-40. DOI: 10.1016/s0169-328x(96)00285-9. View

Day H, Campeau S, Watson Jr S, Akil H . Expression of alpha(1b) adrenoceptor mRNA in corticotropin-releasing hormone-containing cells of the rat hypothalamus and its regulation by corticosterone. J Neurosci. 1999; 19(22):10098-106. PMC: 6782978. View

10.

Cunningham Jr E, Bohn M, Sawchenko P . Organization of adrenergic inputs to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol. 1990; 292(4):651-67. DOI: 10.1002/cne.902920413. View

11.

Paulsen R, Contestabile A, Villani L, Fonnum F . An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J Neurochem. 1987; 48(5):1377-85. DOI: 10.1111/j.1471-4159.1987.tb05674.x. View

12.

Verkhratsky A, Nedergaard M . Physiology of Astroglia. Physiol Rev. 2018; 98(1):239-389. PMC: 6050349. DOI: 10.1152/physrev.00042.2016. View

13.

Ma X, Levy A, Lightman S . Rapid changes in heteronuclear RNA for corticotrophin-releasing hormone and arginine vasopressin in response to acute stress. J Endocrinol. 1997; 152(1):81-9. DOI: 10.1677/joe.0.1520081. View

14.

Tasker J, Dudek F . Electrophysiological properties of neurones in the region of the paraventricular nucleus in slices of rat hypothalamus. J Physiol. 1991; 434:271-93. PMC: 1181417. DOI: 10.1113/jphysiol.1991.sp018469. View

15.

Di S, Popescu I, Tasker J . Glial control of endocannabinoid heterosynaptic modulation in hypothalamic magnocellular neuroendocrine cells. J Neurosci. 2013; 33(46):18331-42. PMC: 3828473. DOI: 10.1523/JNEUROSCI.2971-12.2013. View

16.

Jiang Z, Rajamanickam S, Justice N . Local Corticotropin-Releasing Factor Signaling in the Hypothalamic Paraventricular Nucleus. J Neurosci. 2018; 38(8):1874-1890. PMC: 5824736. DOI: 10.1523/JNEUROSCI.1492-17.2017. View

17.

Fuzesi T, Wittmann G, Liposits Z, Lechan R, Fekete C . Contribution of noradrenergic and adrenergic cell groups of the brainstem and agouti-related protein-synthesizing neurons of the arcuate nucleus to neuropeptide-y innervation of corticotropin-releasing hormone neurons in hypothalamic paraventricular.... Endocrinology. 2007; 148(11):5442-50. DOI: 10.1210/en.2007-0732. View

18.

Sawchenko P, Swanson L . The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res. 1982; 257(3):275-325. DOI: 10.1016/0165-0173(82)90010-8. View

19.

Helmreich D, Itoi K, Akil H, Watson S . Norepinephrine-induced CRH and AVP gene transcription within the hypothalamus: differential regulation by corticosterone. Brain Res Mol Brain Res. 2001; 88(1-2):62-73. DOI: 10.1016/s0169-328x(01)00018-3. View

20.

Bartanusz V, Aubry J, Jezova D, Baffi J, Kiss J . Up-regulation of vasopressin mRNA in paraventricular hypophysiotrophic neurons after acute immobilization stress. Neuroendocrinology. 1993; 58(6):625-9. DOI: 10.1159/000126602. View