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The Journal of Neuroscience, October 1, 1998, 18(19):7962-7971

Presynaptic and Postsynaptic Actions and Modulation of Neuroendocrine Neurons by a New Hypothalamic Peptide, Hypocretin/Orexin

Anthony N. van den Pol1, 2, Xiao-Bing Gao1, Karl Obrietan2, Thomas S. Kilduff2, and Andrei B. Belousov2

1 Department of Neurosurgery, Yale University Medical School, New Haven, Connecticut 06520, and 2 Department of Biological Sciences, Stanford University, Stanford, California 94305

A new orexigenic peptide called hypocretin (orexin) has recently been described in neurons of the lateral hypothalamus and perifornical area. The medial and lateral hypothalamus have been loosely called satiety and feeding centers of the brain, respectively. Approximately one-third of all medial and lateral hypothalamic neurons tested, but not hippocampal neurons, show a striking nanomolar sensitivity to hypocretin. As studied with calcium digital imaging with fura-2, hypocretin raises cytoplasmic calcium via a mechanism based on G-protein enhancement of calcium influx through plasma membrane channels. The peptide has a potent effect at both presynaptic and postsynaptic receptors. Most synaptic activity in hypothalamic circuits is attributable to axonal release of GABA or glutamate. With whole-cell patch-clamp recording, we show that hypocretin, acting directly at axon terminals, can increase the release of each of these amino acid transmitters. Two hypocretin peptides, hypocretin-1 and hypocretin-2, are coded by a single gene; neurons that respond to one peptide also respond to the other. In addition to its effect on feeding, we find that this peptide also regulates the synaptic activity of physiologically identified neuroendocrine neurons studied in hypothalamic slices containing the arcuate nucleus, suggesting a second function of hypocretin in hormone regulation. The widespread distribution of hypocretin axons, coupled with the strong response to the peptide at both presynaptic and postsynaptic sites, suggests that the peptide probably modulates a variety of hypothalamic regulatory systems and could regulate the axonal input to these regions presynaptically.

Key words: hypothalamus; presynaptic; neuroendocrine; neuromodulation; neuropeptide; glutamate; GABA; feeding

Copyright © 1998 Society for Neuroscience  0270-6474/98/18197962-10$05.00/0


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A. N van den Pol, P. K Ghosh, R.-j. Liu, Y. Li, G. K Aghajanian, and X.-B. Gao
Hypocretin (orexin) enhances neuron activity and cell synchrony in developing mouse GFP-expressing locus coeruleus
J. Physiol., May 15, 2002; 541(1): 169 - 185.
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S. Burlet, C. J. Tyler, and C. S. Leonard
Direct and Indirect Excitation of Laterodorsal Tegmental Neurons by Hypocretin/Orexin Peptides: Implications for Wakefulness and Narcolepsy
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A. L. Kirchgessner
Orexins in the Brain-Gut Axis
Endocr. Rev., February 1, 2002; 23(1): 1 - 15.
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I O Ebrahim, R S Howard, M D Kopelman, M K Sharief, and A J Williams
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K. S. Eriksson, O. Sergeeva, R. E. Brown, and H. L. Haas
Orexin/Hypocretin Excites the Histaminergic Neurons of the Tuberomammillary Nucleus
J. Neurosci., December 1, 2001; 21(23): 9273 - 9279.
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L.-L. Hwang, C.-T. Chen, and N. J Dun
Mechanisms of orexin-induced depolarizations in rat dorsal motor nucleus of vagus neurones in vitro
J. Physiol., December 1, 2001; 537(2): 511 - 520.
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G. Mazzocchi, L. K. Malendowicz, F. Aragona, P. Rebuffat, L. Gottardo, and G. G. Nussdorfer
Human Pheochromocytomas Express Orexin Receptor Type 2 Gene and Display an in Vitro Secretory Response to Orexins A and B
J. Clin. Endocrinol. Metab., October 1, 2001; 86(10): 4818 - 4821.
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T. L. Horvath, S. Diano, P. Sotonyi, M. Heiman, and M. Tschop
Minireview: Ghrelin and the Regulation of Energy Balance--A Hypothalamic Perspective
Endocrinology, October 1, 2001; 142(10): 4163 - 4169.
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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
T. Shirasaka, S. Miyahara, T. Kunitake, Q.-H. Jin, K. Kato, M. Takasaki, and H. Kannan
Orexin depolarizes rat hypothalamic paraventricular nucleus neurons
Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2001; 281(4): R1114 - R1118.
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W. K. Samson and M. M. Taylor
Hypocretin/orexin suppresses corticotroph responsiveness in vitro
Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2001; 281(4): R1140 - R1145.
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Y.-F. Wang, X.-B. Gao, and A. N. van den Pol
Membrane Properties Underlying Patterns of GABA-Dependent Action Potentials in Developing Mouse Hypothalamic Neurons
J Neurophysiol, September 1, 2001; 86(3): 1252 - 1265.
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Z.-L. Huang, W.-M. Qu, W.-D. Li, T. Mochizuki, N. Eguchi, T. Watanabe, Y. Urade, and O. Hayaishi
Arousal effect of orexin A depends on activation of the histaminergic system
PNAS, August 1, 2001; (2001) 181330998.
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M. Blanco, M. Lopez, T. GarcIa-Caballero, R. Gallego, A. Vazquez-Boquete, G. Morel, R. SenarIs, F. Casanueva, C. Dieguez, and A. Beiras
Cellular Localization of Orexin Receptors in Human Pituitary
J. Clin. Endocrinol. Metab., July 1, 2001; 86(7): 3444 - 3447.
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X.-B. Gao and A. N van den Pol
Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypothalamus
J. Physiol., May 15, 2001; 533(1): 237 - 252.
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L. I. Kiyashchenko, B. Y. Mileykovskiy, Y.-Y. Lai, and J. M. Siegel
Increased and Decreased Muscle Tone With Orexin (Hypocretin) Microinjections in the Locus Coeruleus and Pontine Inhibitory Area
J Neurophysiol, May 1, 2001; 85(5): 2008 - 2016.
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M. Blanco, M. López, T. GarcÍa-Caballero, R. Gallego, A. Vázquez-Boquete, G. Morel, R. SeñarÍs, F. Casanueva, C. Diéguez, and A. Beiras
Cellular Localization of Orexin Receptors in Human Pituitary
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T. S. Kilduff
Sleepy Dogs Don't Lie: A Genetic Disorder Informative About Sleep
Genome Res., April 1, 2001; 11(4): 509 - 511.
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G. Mazzocchi, L. K. Malendowicz, L. Gottardo, F. Aragona, and G. G. Nussdorfer
Orexin A Stimulates Cortisol Secretion from Human Adrenocortical Cells through Activation of the Adenylate Cyclase-Dependent Signaling Cascade
J. Clin. Endocrinol. Metab., February 1, 2001; 86(2): 778 - 782.
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P. Bourgin, S. Huitron-Resendiz, A. D. Spier, V. Fabre, B. Morte, J. R. Criado, J. G. Sutcliffe, S. J. Henriksen, and L. de Lecea
Hypocretin-1 Modulates Rapid Eye Movement Sleep through Activation of Locus Coeruleus Neurons
J. Neurosci., October 15, 2000; 20(20): 7760 - 7765.
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J.-Y. Li, S. Finniss, Y.-K. Yang, Q. Zeng, S.-Y. Qu, G. Barsh, C. Dickinson, and I. Gantz
Agouti-Related Protein-Like Immunoreactivity: Characterization of Release from Hypothalamic Tissue and Presence in Serum
Endocrinology, June 1, 2000; 141(6): 1942 - 1950.
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C.-T. Chen, L.-L. Hwang, J.-K. Chang, and N. J. Dun
Pressor effects of orexins injected intracisternally and to rostral ventrolateral medulla of anesthetized rats
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2000; 278(3): R692 - R697.
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T. Shirasaka, M. Nakazato, S. Matsukura, M. Takasaki, and H. Kannan
Sympathetic and cardiovascular actions of orexins in conscious rats
Am J Physiol Regulatory Integrative Comp Physiol, December 1, 1999; 277(6): R1780 - R1785.
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J. J. Hagan, R. A. Leslie, S. Patel, M. L. Evans, T. A. Wattam, S. Holmes, C. D. Benham, S. G. Taylor, C. Routledge, P. Hemmati, et al.
Orexin A activates locus coeruleus cell firing and increases arousal in the rat
PNAS, September 14, 1999; 96(19): 10911 - 10916.
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P. J Emmerson and R. J Miller
Pre- and postsynaptic actions of opioid and orphan opioid agonists in the rat arcuate nucleus and ventromedial hypothalamus in vitro
J. Physiol., June 1, 1999; 517(2): 431 - 445.
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A. N. van den Pol
Hypothalamic Hypocretin (Orexin): Robust Innervation of the Spinal Cord
J. Neurosci., April 15, 1999; 19(8): 3171 - 3182.
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T. L. Horvath, S. Diano, and A. N. van den Pol
Synaptic Interaction between Hypocretin (Orexin) and Neuropeptide Y Cells in the Rodent and Primate Hypothalamus: A Novel Circuit Implicated in Metabolic and Endocrine Regulations
J. Neurosci., February 1, 1999; 19(3): 1072 - 1087.
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C. Peyron, D. K. Tighe, A. N. van den Pol, L. de Lecea, H. C. Heller, J. G. Sutcliffe, and T. S. Kilduff
Neurons Containing Hypocretin (Orexin) Project to Multiple Neuronal Systems
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P.-E. Lund, R. Shariatmadari, A. Uustare, M. Detheux, M. Parmentier, J. P. Kukkonen, and K. E. O. Akerman
The Orexin OX1 Receptor Activates a Novel Ca2+ Influx Pathway Necessary for Coupling to Phospholipase C
J. Biol. Chem., September 29, 2000; 275(40): 30806 - 30812.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
Z.-L. Huang, W.-M. Qu, W.-D. Li, T. Mochizuki, N. Eguchi, T. Watanabe, Y. Urade, and O. Hayaishi
Arousal effect of orexin A depends on activation of the histaminergic system
PNAS, August 14, 2001; 98(17): 9965 - 9970.
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