High Dietary Salt Amplifies Osmoresponsiveness in Vasopressin-releasing Neurons

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2021 Mar 17

PMID 33730577

Citations 6

Authors

David I Levi

Joshua C Wyrosdic

Amirah-Iman Hicks

Mary Ann Andrade

Glenn M Toney

Masha Prager-Khoutorsky

Charles W Bourque

Affiliations

Soon will be listed here.

Abstract

High dietary salt increases arterial pressure partly through activation of magnocellular neurosecretory cells (MNC) that secrete the antidiuretic and vasoconstrictor hormone vasopressin (VP) into the circulation. Here, we show that the intrinsic and synaptic excitation of MNC caused by hypertonicity are differentially potentiated in two models of salt-dependent hypertension in rats. One model combined salty chow with a chronic subpressor dose of angiotensin II (AngII-salt), the other involved replacing drinking water with 2% NaCl (salt loading, SL). In both models, we observed a significant increase in the quantal amplitude of EPSCs on MNC. However, model-specific changes were also observed. AngII-salt increased the probability of glutamate release by osmoreceptor afferents and increased overall excitatory network drive. In contrast, SL specifically increased membrane stiffness and the intrinsic osmosensitivity of MNC. These results reveal that dietary salt increases the excitability of MNC through effects on the cell-autonomous and synaptic osmoresponsiveness of MNC.

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References

Prager-Khoutorsky M, Khoutorsky A, Bourque C . Unique interweaved microtubule scaffold mediates osmosensory transduction via physical interaction with TRPV1. Neuron. 2014; 83(4):866-78. DOI: 10.1016/j.neuron.2014.07.023. View

Naeini R, Witty M, Seguela P, Bourque C . An N-terminal variant of Trpv1 channel is required for osmosensory transduction. Nat Neurosci. 2005; 9(1):93-8. DOI: 10.1038/nn1614. View

Gardel M, Shin J, MacKintosh F, Mahadevan L, Matsudaira P, Weitz D . Elastic behavior of cross-linked and bundled actin networks. Science. 2004; 304(5675):1301-5. DOI: 10.1126/science.1095087. View

Keck T, Hubener M, Bonhoeffer T . Interactions between synaptic homeostatic mechanisms: an attempt to reconcile BCM theory, synaptic scaling, and changing excitation/inhibition balance. Curr Opin Neurobiol. 2017; 43:87-93. DOI: 10.1016/j.conb.2017.02.003. View

Zhang Z, Kindrat A, Sharif-Naeini R, Bourque C . Actin filaments mediate mechanical gating during osmosensory transduction in rat supraoptic nucleus neurons. J Neurosci. 2007; 27(15):4008-13. PMC: 6672547. DOI: 10.1523/JNEUROSCI.3278-06.2007. View

Gizowski C, Bourque C . Sodium regulates clock time and output via an excitatory GABAergic pathway. Nature. 2020; 583(7816):421-424. DOI: 10.1038/s41586-020-2471-x. View

Ozaki Y, Soya A, Nakamura J, Matsumoto T, Ueta Y . Potentiation by angiotensin II of spontaneous excitatory postsynaptic currents in rat supraoptic magnocellular neurones. J Neuroendocrinol. 2004; 16(11):871-9. DOI: 10.1111/j.1365-2826.2004.01244.x. View

Bicknell R . Optimizing release from peptide hormone secretory nerve terminals. J Exp Biol. 1988; 139:51-65. DOI: 10.1242/jeb.139.1.51. View

Son S, Filosa J, Potapenko E, Biancardi V, Zheng H, Patel K . Dendritic peptide release mediates interpopulation crosstalk between neurosecretory and preautonomic networks. Neuron. 2013; 78(6):1036-49. PMC: 3884642. DOI: 10.1016/j.neuron.2013.04.025. View

10.

McBryde F, Guild S, Barrett C, Osborn J, Malpas S . Angiotensin II-based hypertension and the sympathetic nervous system: the role of dose and increased dietary salt in rabbits. Exp Physiol. 2007; 92(5):831-40. DOI: 10.1113/expphysiol.2007.037473. View

11.

Shi P, Stocker S, Toney G . Organum vasculosum laminae terminalis contributes to increased sympathetic nerve activity induced by central hyperosmolality. Am J Physiol Regul Integr Comp Physiol. 2007; 293(6):R2279-89. PMC: 3575105. DOI: 10.1152/ajpregu.00160.2007. View

12.

Nomura K, Hiyama T, Sakuta H, Matsuda T, Lin C, Kobayashi K . [Na] Increases in Body Fluids Sensed by Central Na Induce Sympathetically Mediated Blood Pressure Elevations via H-Dependent Activation of ASIC1a. Neuron. 2018; 101(1):60-75.e6. DOI: 10.1016/j.neuron.2018.11.017. View

13.

Panatier A, Gentles S, Bourque C, Oliet S . Activity-dependent synaptic plasticity in the supraoptic nucleus of the rat hypothalamus. J Physiol. 2006; 573(Pt 3):711-21. PMC: 1779752. DOI: 10.1113/jphysiol.2006.109447. View

14.

Brown D, Li S, Lawler J, Randall D . Sympathetic control of BP and BP variability in borderline hypertensive rats on high- vs. low-salt diet. Am J Physiol. 1999; 277(3):R650-7. DOI: 10.1152/ajpregu.1999.277.3.R650. View

15.

Sanchez D, Johnson N, Li C, Novak P, Rheinlaender J, Zhang Y . Noncontact measurement of the local mechanical properties of living cells using pressure applied via a pipette. Biophys J. 2008; 95(6):3017-27. PMC: 2527257. DOI: 10.1529/biophysj.108.129551. View

16.

Kim J, Kim W, Kim Y, Lee Y, Kim Y, Shen F . Chronic hyperosmotic stress converts GABAergic inhibition into excitation in vasopressin and oxytocin neurons in the rat. J Neurosci. 2011; 31(37):13312-22. PMC: 6623275. DOI: 10.1523/JNEUROSCI.1440-11.2011. View

17.

Richard D, Bourque C . Synaptic control of rat supraoptic neurones during osmotic stimulation of the organum vasculosum lamina terminalis in vitro. J Physiol. 1995; 489 ( Pt 2):567-77. PMC: 1156780. DOI: 10.1113/jphysiol.1995.sp021073. View

18.

Fink G, Johnson R, Galligan J . Mechanisms of increased venous smooth muscle tone in desoxycorticosterone acetate-salt hypertension. Hypertension. 2000; 35(1 Pt 2):464-9. DOI: 10.1161/01.hyp.35.1.464. View

19.

Zhang Z, Bourque C . Osmometry in osmosensory neurons. Nat Neurosci. 2003; 6(10):1021-2. DOI: 10.1038/nn1124. View

20.

Sudbury J, Ciura S, Sharif-Naeini R, Bourque C . Osmotic and thermal control of magnocellular neurosecretory neurons--role of an N-terminal variant of trpv1. Eur J Neurosci. 2010; 32(12):2022-30. DOI: 10.1111/j.1460-9568.2010.07512.x. View