Dendritic Peptide Release Mediates Interpopulation Crosstalk between Neurosecretory and Preautonomic Networks

Neuron

Volumn 78, Issue 6, 2013, Pages 1036-1049

  Son, SookJin ^a   Filosa, JessicaA ^a   Potapenko, EvgeniyS ^a   Biancardi, ViniciaC ^a   Zheng, Hong ^b   Patel, KaushikP ^b   Tobin, VickyA ^c   Ludwig, Mike ^c   Stern, JavierE ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; MESSENGER RNA; VASOPRESSIN; VASOPRESSIN V1A RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVE; CONTROLLED STUDY; DENDRITE; GENE EXPRESSION REGULATION; MALE; MOLECULAR INTERACTION; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NEUROSECRETION; NEUROTRANSMISSION; NONHUMAN; OSMOTIC STRESS; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RAT; SYMPATHETIC NERVE CELL; SYMPATHETIC TONE; VASOPRESSIN V1A RECEPTOR GENE;

ANIMALS; DENDRITES; HYPOTHALAMUS; MALE; NERVE NET; NEUROPEPTIDES; NEUROSECRETION; ORGAN CULTURE TECHNIQUES; RATS; RATS, TRANSGENIC; RATS, WISTAR;

EID: 84879258353     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.04.025     Document Type: Article

References (54)

1. Antunes V.R., Yao S.T., Pickering A.E., Murphy D., Paton J.F. A spinal vasopressinergic mechanism mediates hyperosmolality-induced sympathoexcitation. J.Physiol. 2006, 576:569-583.
2. Armstrong W.E., Wang L., Li C., Teruyama R. Performance, properties and plasticity of identified oxytocin and vasopressin neurones invitro. J.Neuroendocrinol. 2010, 22:330-342.
3. Biancardi V.C., Campos R.R., Stern J.E. Altered balance of gamma-aminobutyric acidergic and glutamatergic afferent inputs in rostral ventrolateral medulla-projecting neurons in the paraventricular nucleus of the hypothalamus of renovascular hypertensive rats. J.Comp. Neurol. 2010, 518:567-585.
4. Biancardi V.C., Son S.J., Sonner P.M., Zheng H., Patel K.P., Stern J.E. Contribution of central nervous system endothelial nitric oxide synthase to neurohumoral activation in heart failure rats. Hypertension 2011, 58:454-463.
5. Bourque C.W. Central mechanisms of osmosensation and systemic osmoregulation. Nat. Rev. Neurosci. 2008, 9:519-531.
6. Brown C.H., Ludwig M., Leng G. kappa-opioid regulation ofneuronal activity in the rat supraoptic nucleus invivo. J.Neurosci. 1998, 18:9480-9488.
7. Buijs R.M., Van Eden C.G. The integration of stress by the hypothalamus, amygdala and prefrontal cortex: balance between the autonomic nervous system and the neuroendocrine system. Prog. Brain Res. 2000, 126:117-132.
8. Chen X., Pittman Q.J. Vasopressin and amastatin induce V(1)-receptor-mediated suppression of excitatory transmission in the rat parabrachial nucleus. J.Neurophysiol. 1999, 82:1689-1696.
9. Chen Q.H., Toney G.M. AT(1)-receptor blockade in the hypothalamic PVN reduces central hyperosmolality-induced renal sympathoexcitation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 281:R1844-R1853.
10. Cheramy A., Leviel V., Glowinski J. Dendritic release of dopamine in the substantia nigra. Nature 1981, 289:537-542.
11. Cohn J.N., Levine T.B., Olivari M.T., Garberg V., Lura D., Francis G.S., Simon A.B., Rector T. Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure. N.Engl. J. Med. 1984, 311:819-823.
12. de Kock C.P., Burnashev N., Lodder J.C., Mansvelder H.D., Brussaard A.B. NMDA receptors induce somatodendritic secretion in hypothalamic neurones of lactating female rats. J.Physiol. 2004, 561:53-64.
13. de Kock C.P., Cornelisse L.N., Burnashev N., Lodder J.C., Timmerman A.J., Couey J.J., Mansvelder H.D., Brussaard A.B. NMDA receptors trigger neurosecretion of 5-HT within dorsal raphe nucleus of the rat in the absence of action potential firing. J.Physiol. 2006, 577:891-905.
14. Ely D.L. Organization of cardiovascular and neurohumoral responses to stress. Implications for health and disease. Ann. N Y Acad. Sci. 1995, 771:594-608.
15. Esler M.D., Lambert G.W., Ferrier C., Kaye D.M., Wallin B.G., Kalff V., Kelly M.J., Jennings G.L. Central nervous system noradrenergic control of sympathetic outflow in normotensive and hypertensive humans. Clin. Exp. Hypertens. 1995, 17:409-423.
16. Filosa J.A., Bonev A.D., Straub S.V., Meredith A.L., Wilkerson M.K., Aldrich R.W., Nelson M.T. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat. Neurosci. 2006, 9:1397-1403.
17. Fuxe K., Dahlström A., Höistad M., Marcellino D., Jansson A., Rivera A., Diaz-Cabiale Z., Jacobsen K., Tinner-Staines B., Hagman B., et al. From the Golgi-Cajal mapping to the transmitter-based characterization of the neuronal networks leading to two modes of brain communication: wiring and volume transmission. Brain Res. Brain Res. Rev. 2007, 55:17-54.
18. Galarreta M., Hestrin S. Spike transmission and synchronydetection in networks of GABAergic interneurons. Science 2001, 292:2295-2299.
19. Ghamari-Langroudi M., Bourque C.W. Flufenamic acid blocks depolarizing afterpotentials and phasic firing in rat supraoptic neurones. J.Physiol. 2002, 545:537-542.
20. Gouzènes L., Desarménien M.G., Hussy N., Richard P., Moos F.C. Vasopressin regularizes the phasic firing pattern of rat hypothalamic magnocellular vasopressin neurons. J.Neurosci. 1998, 18:1879-1885.
21. Guan J.L., Kageyama H., Wang Q.P., Takenoya F., Kita T., Matsumoto H., Ohtaki T., Shioda S. Electron microscopy examination of galanin-like peptide (GALP)-containing neurons in the rat hypothalamus. Regul. Pept. 2005, 126:73-78.
22. Hatton G.I., Cobbett P., Salm A.K. Extranuclear axon collateralsof paraventricular neurons in the rat hypothalamus: intracellular staining,immunocytochemistry and electrophysiology. Brain Res. Bull. 1985, 14:123-132.
23. Kombian S.B., Mouginot D., Pittman Q.J. Dendritically released peptides act as retrograde modulators of afferent excitation in the supraoptic nucleus invitro. Neuron 1997, 19:903-912.
24. Landgraf R., Neumann I.D. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 2004, 25:150-176.
25. Landgraf R., Neumann I., Holsboer F., Pittman Q.J. Interleukin-1 beta stimulates both central and peripheral release of vasopressin and oxytocin in the rat. Eur. J. Neurosci. 1995, 7:592-598.
26. Leng G., Ludwig M. Neurotransmitters and peptides: whispered secrets and public announcements. J.Physiol. 2008, 586:5625-5632.
27. Leng G., Brown C.H., Bull P.M., Brown D., Scullion S., Currie J., Blackburn-Munro R.E., Feng J., Onaka T., Verbalis J.G., et al. Responses ofmagnocellular neurons to osmotic stimulation involves coactivation of excitatory and inhibitory input: an experimental and theoretical analysis. J.Neurosci. 2001, 21:6967-6977.
28. Ludwig M. Dendritic release of vasopressin and oxytocin. J.Neuroendocrinol. 1998, 10:881-895.
29. Ludwig M., Leng G. Autoinhibition of supraoptic nucleus vasopressin neurons invivo: a combined retrodialysis/electrophysiological study in rats. Eur. J. Neurosci. 1997, 9:2532-2540.
30. Ludwig M., Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci. 2006, 7:126-136.
31. 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.
32. McBean G.J. Inhibition of the glutamate transporter and glial enzymes in rat striatum by the gliotoxin, alpha aminoadipate. Br. J. Pharmacol. 1994, 113:536-540.
33. Mens W.B., Witter A., van Wimersma Greidanus T.B. Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): half-times of disappearance of these neuropeptides from CSF. Brain Res. 1983, 262:143-149.
34. Min M.Y., Rusakov D.A., Kullmann D.M. Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion. Neuron 1998, 21:561-570.
35. Oliet S.H., Bourque C.W. Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature 1993, 364:341-343.
36. Petersen O.H. Cation channels: homing in on the elusive CAN channels. Curr. Biol. 2002, 12:R520-R522.
37. Piet R., Vargová L., Syková E., Poulain D.A., Oliet S.H. Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc. Natl. Acad. Sci. USA 2004, 101:2151-2155.
38. Pittman Q.J., Veale W.L., Lederis K. Central neurohypophyseal peptide pathways: interactions with endocrine and other autonomic functions. Peptides 1982, 3:515-520.
39. Pliquett R.U., Fasshauer M., Blüher M., Paschke R. Neurohumoral stimulation in type-2-diabetes as an emerging disease concept. Cardiovasc. Diabetol. 2004, 3:4.
40. Pow D.V., Morris J.F. Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis. Neuroscience 1989, 32:435-439.
41. Salio C., Lossi L., Ferrini F., Merighi A. Neuropeptides as synaptic transmitters. Cell Tissue Res. 2006, 326:583-598.
42. Shi P., Stocker S.D., Toney G.M. Organum vasculosum laminae terminalis contributes to increased sympathetic nerve activity induced by central hyperosmolality. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R2279-R2289.
43. Sonner P.M., Lee S., Ryu P.D., Lee S.Y., Stern J.E. Imbalanced K+ and Ca2+ subthreshold interactions contribute to increased hypothalamic presympathetic neuronal excitability in hypertensive rats. J.Physiol. 2011, 589:667-683.
44. Swanson L.W., Kuypers H.G. The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J.Comp. Neurol. 1980, 194:555-570.
45. Swanson L.W., Sawchenko P.E. Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 1980, 31:410-417.
46. Swanson L.W., Sawchenko P.E., Wiegand S.J., Price J.L. Separate neurons in the paraventricular nucleus project to the median eminence and to the medulla or spinal cord. Brain Res. 1980, 198:190-195.
47. Teruyama R., Armstrong W.E. Calcium-dependent fast depolarizing afterpotentials in vasopressin neurons in the rat supraoptic nucleus. J.Neurophysiol. 2007, 98:2612-2621.
48. Teruyama R., Sakuraba M., Kurotaki H., Armstrong W.E. Transient receptor potential channel m4 and m5 in magnocellular cells in rat supraoptic and paraventricular nuclei. J.Neuroendocrinol. 2011, 23:1204-1213.
49. Tobin V.A., Hashimoto H., Wacker D.W., Takayanagi Y., Langnaese K., Caquineau C., Noack J., Landgraf R., Onaka T., Leng G., et al. An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 2010, 464:413-417.
50. Toney G.M., Stocker S.D. Hyperosmotic activation of CNS sympathetic drive: implications for cardiovascular disease. J.Physiol. 2010, 588:3375-3384.
51. Ueta Y., Fujihara H., Serino R., Dayanithi G., Ozawa H., Matsuda K.-i., 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.
52. Ullrich N.D., Voets T., Prenen J., Vennekens R., Talavera K., Droogmans G., Nilius B. Comparison of functional properties of the Ca2+-activated cation channels TRPM4 and TRPM5 from mice. Cell Calcium 2005, 37:267-278.
53. Xu H.L., Mao L., Ye S., Paisansathan C., Vetri F., Pelligrino D.A. Astrocytes are a key conduit for upstream signaling of vasodilation during cerebral cortical neuronal activation invivo. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H622-H632.
54. Zingg H.H. Vasopressin and oxytocin receptors. Baillieres Clin. Endocrinol. Metab. 1996, 10:75-96.