Antagonistic interplay between hypocretin and leptin in the lateral hypothalamus regulates stress responses

Nature Communications

Volumn 6, Issue , 2015, Pages

  Bonnavion, Patricia ^a,b   Jackson, Alexander C ^c,d   Carter, Matthew E ^e   De Lecea, Luis ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CONNECTICUT   (United States)

^e WILLIAMS COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; LEPTIN; OREXIN;

ANTAGONISM; INHIBITION; PHYSIOLOGICAL RESPONSE; RODENT;

ANIMAL EXPERIMENT; ARTICLE; CORTICOSTERONE RELEASE; DIET RESTRICTION; DOWN REGULATION; LATERAL HYPOTHALAMUS; MALE; METABOLISM; MOUSE; NERVE CELL; NONHUMAN; PHOTOSTIMULATION; REGULATORY MECHANISM; SENSITIZATION; SIGNAL TRANSDUCTION; STRESS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; FOOD DEPRIVATION; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LIGHT; PHYSIOLOGICAL STRESS; RADIATION RESPONSE;

MUS;

ANIMALS; DOWN-REGULATION; FOOD DEPRIVATION; GABAERGIC NEURONS; HYPOTHALAMIC AREA, LATERAL; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LEPTIN; LIGHT; MALE; METABOLIC NETWORKS AND PATHWAYS; MICE, INBRED C57BL; OREXINS; PITUITARY-ADRENAL SYSTEM; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84923332677     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7266     Document Type: Article

References (69)

1. De Kloet, E. R., Joëls, M. & Holsboer, F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475 (2005).
2. Dallman, M. F., Akana, S. F., Strack, A. M., Hanson, E. S. & Sebastian, R. J. The neural network that regulates energy balance is responsive to glucocorticoids and insulin and also regulates HPA axis responsivity at a site proximal to CRF neurons. Ann. NY Acad. Sci. 771, 730-742 (1995).
3. Koob, G. F. Stress, corticotropin-releasing factor, and drug addiction. Ann. NY Acad. Sci. 897, 27-45 (1999).
4. Adam, T. C. & Epel, E. S. Stress, eating and the reward system. Physiol. Behav. 91, 449-458 (2007).
5. Yamanaka, A. et al. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 38, 701-713 (2003).
6. Berridge, C. W., España, R. A. & Vittoz, N. M. Hypocretin/orexin in arousal and stress. Brain Res. 1314, 91-102 (2010).
7. Winsky-Sommerer, R. et al. Interaction between the corticotropin-releasing factor system and hypocretins (Orexins). J. Neurosci. 24, 11439-11448 (2004).
8. Lee, M. G., Hassani, O. K. & Jones, B. E. Discharge of identified orexin/ hypocretin neurons across the sleep-waking cycle. J. Neurosci. 25, 6716-6720 (2005).
9. Mileykovskiy, B. Y., Kiyashchenko, L. I. & Siegel, J. M. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46, 787-798 (2005).
10. Kuru, M. et al. Centrally administered orexin/hypocretin activates HPA axis in rats. Neuroreport 11, 1977-1980 (2000).
11. Johnson, P. L., Molosh, A., Fitz, S. D., Truitt, W. A. & Shekhar, A. Orexin, stress, and anxiety/panic states. Prog. Brain Res. 198, 133-161 (2012).
12. Jászberényi, M., Bujdosó, E., Pataki, I. & Telegdy, G. Effects of orexins on the hypothalamic-pituitary-adrenal system. J. Neuroendocrinol. 12, 1174-1178 (2000).
13. Russell, S. H. et al. The central effects of orexin-A in the hypothalamic- pituitary-adrenal axis in vivo and in vitro in male rats. J. Neuroendocrinol. 13, 561-566 (2001).
14. Al-Barazanji, K. A., Wilson, S., Baker, J., Jessop, D. S. & Harbuz, M. S. Central orexin-A activates hypothalamic-pituitary-adrenal axis and stimulates hypothalamic corticotropin releasing factor and arginine vasopressin neurones in conscious rats. J. Neuroendocrinol. 13, 421-424 (2001).
15. Samson, W. K., Bagley, S. L., Ferguson, A. V. & White, M. M. Hypocretin/ orexin type 1 receptor in brain: role in cardiovascular control and the neuroendocrine response to immobilization stress. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R382-R387 (2007).
16. Kayaba, Y. et al. Attenuated defense response and low basal blood pressure in orexin knockout mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R581-R593 (2003).
17. Sakurai, T. & Mieda, M. Connectomics of orexin-producing neurons: interface of systems of emotion, energy homeostasis and arousal. Trends Pharmacol. Sci. 32, 451-462 (2011).
18. Van Swieten, M. M., Pandit, R., Adan, R. A. & van der Plasse, G. The neuroanatomical function of leptin in the hypothalamus. J. Chem. Neuroanat. 61-62, 207-220 (2014).
19. Heiman, M. L. et al. Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress. Endocrinology 138, 3859-3863 (1997).
20. Ahima, R. S., Prabakaran, D. & Flier, J. S. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J. Clin. Invest. 101, 1020-1027 (1998).
21. Stephens, T. W. et al. The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature 377, 530-532 (1995).
22. Scott, M. M. et al. Leptin targets in the mouse brain. J. Comp. Neurol. 514, 518-532 (2009).
23. Elmquist, J. K., Maratos-Flier, E., Saper, C. B. & Flier, J. S. Unraveling the central nervous system pathways underlying responses to leptin. Nat. Neurosci. 1, 445-450 (1998).
24. Myers, M. G., Münzberg, H., Leinninger, G. M. & Leshan, R. L. The geometry of leptin action in the brain: more complicated than a simple ARC. Cell Metab. 9, 117-123 (2009).
25. Goforth, P. B., Leinninger, G. M., Patterson, C. M., Satin, L. S. & Myers, M. G. Leptin acts via lateral hypothalamic area neurotensin neurons to inhibit orexin neurons by multiple GABA-independent mechanisms. J. Neurosci. 34, 11405-11415 (2014).
26. Louis, G. W., Leinninger, G. M., Rhodes, C. J. & Myers, M. G. Direct innervation and modulation of orexin neurons by lateral hypothalamic LepRb neurons. J. Neurosci. 30, 11278-11287 (2010).
27. Adamantidis, A. R., Zhang, F., Aravanis, A. M., Deisseroth, K. & de Lecea, L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420-424 (2007).
28. Adamantidis, A. & de Lecea, L. Physiological arousal: a role for hypothalamic systems. Cell. Mol. Life Sci. 65, 1475-1488 (2008).
29. Nader, N., Chrousos, G. P. & Kino, T. Interactions of the circadian CLOCK system and the HPA axis. Trends Endocrinol. Metab. 21, 277-286 (2010).
30. Horvath, T. L. & Gao, X.-B. Input organization and plasticity of hypocretin neurons: possible clues to obesity's association with insomnia. Cell Metab. 1, 279-286 (2005).
31. Lutter, M. et al. Orexin signaling mediates the antidepressant-like effect of calorie restriction. J. Neurosci. 28, 3071-3075 (2008).
32. Dallman, M. F. et al. Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front. Neuroendocrinol. 14, 303-347 (1993).
33. Maffei, M. et al. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat. Med. 1, 1155-1161 (1995).
34. Banks, A. S., Davis, S. M., Bates, S. H. & Myers, M. G. Activation of downstream signals by the long form of the leptin receptor. J. Biol. Chem. 275, 14563-14572 (2000).
35. White, D. W., Kuropatwinski, K. K., Devos, R., Baumann, H. & Tartaglia, L. A. Leptin receptor (OB-R) signaling. Cytoplasmic domain mutational analysis and evidence for receptor homo-oligomerization. J. Biol. Chem. 272, 4065-4071 (1997).
36. Leinninger, G. M. & Myers, M. G. LRb signals act within a distributed network of leptin-responsive neurones to mediate leptin action. Acta Physiol. (Oxf.) 192, 49-59 (2008).
37. Leinninger, G. M. et al. Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab. 10, 89-98 (2009).
38. Barlow, S. M., Morrison, P. J. & Sullivan, F. M. Effects of acute and chronic stress on plasma corticosterone levels in the pregnant and non-pregnant mouse. J. Endocrinol. 66, 90-9 (1975).
39. Carter, M. E., Adamantidis, A., Ohtsu, H., Deisseroth, K. & De Lecea, L. Sleep homeostasis modulates hypocretin-mediated sleep-to-wake transitions. J. Neurosci. 29, 10939-10949 (2009).
40. Rolls, A. et al. Optogenetic disruption of sleep continuity impairs memory consolidation. Proc. Natl Acad. Sci. USA 108, 13305-13310 (2011).
41. Peyron, C. et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18, 9996-10015 (1998).
42. Ulrich-Lai, Y. M. & Herman, J. P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10, 397-409 (2009).
43. Carter, M. E. et al. Mechanism for Hypocretin-mediated sleep-to-wake transitions. Proc. Natl Acad. Sci. USA 109, E2635-E2644 (2012).
44. Hagan, J. J. et al. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc. Natl Acad. Sci. USA 96, 10911-10916 (1999).
45. España, R. A., Baldo, B. A., Kelley, A. E. & Berridge, C. W. Wake-promoting and sleep-suppressing actions of hypocretin (orexin): Basal forebrain sites of action. Neuroscience 106, 699-715 (2001).
46. Sears, R. M. et al. Orexin/hypocretin system modulates amygdala-dependent threat learning through the locus coeruleus. Proc. Natl Acad. Sci. USA 110, 20260-20265 (2013).
47. Nakamura, T. et al. Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res. 873, 181-187 (2000).
48. Adamantidis, A. R. et al. Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J. Neurosci. 31, 10829-10835 (2011).
49. Hassani, O. K., Lee, M. G. & Jones, B. E. Melanin-concentrating hormone neurons discharge in a reciprocal manner to orexin neurons across the sleep-wake cycle. Proc. Natl Acad. Sci. USA 106, 2418-2422 (2009).
50. Li, Y., Gao, X. B., Sakurai, T. & van den Pol, A. N. Hypocretin/Orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36, 1169-1181 (2002).
51. Takahashi, K., Lin, J. S. & Sakai, K. Neuronal activity of orexin and non-orexin waking-active neurons during wake-sleep states in the mouse. Neuroscience 153, 860-870 (2008).
52. Schöne, C. et al. Optogenetic probing of fast glutamatergic transmission from hypocretin/orexin to histamine neurons in situ. J. Neurosci. 32, 12437-12443 (2012).
53. Schöne, C., Apergis-Schoute, J., Sakurai, T., Adamantidis, A. & Burdakov, D. Coreleased orexin and glutamate evoke nonredundant spike outputs and computations in histamine neurons. Cell Rep. 7, 697-704 (2014).
54. Johnson, P. L. et al. A key role for orexin in panic anxiety. Nat. Med. 16, 111-115 (2010).
55. Burdakov, D. Electrical signaling in central orexin/hypocretin circuits: tuning arousal and appetite to fit the environment. Neuroscientist 10, 286-291 (2004).
56. López, M. et al. Leptin regulation of prepro-orexin and orexin receptor mRNA levels in the hypothalamus. Biochem. Biophys. Res. Commun. 269, 41-45 (2000).
57. Leinninger, G. M. et al. Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab. 14, 313-323 (2011).
58. Kempadoo, K. A. et al. Hypothalamic neurotensin projections promote reward by enhancing glutamate transmission in the VTA. J. Neurosci. 33, 7618-7626 (2013).
59. Laque, A. et al. Leptin receptor neurons in the mouse hypothalamus are colocalized with the neuropeptide galanin and mediate anorexigenic leptin action. Am. J. Physiol. Endocrinol. Metab. 304, E999-1011 (2013).
60. Steininger, T. L., Alam, M. N., Gong, H., Szymusiak, R. & McGinty, D. Sleep-waking discharge of neurons in the posterior lateral hypothalamus of the albino rat. Brain Res. 840, 138-147 (1999).
61. Hassani, O. K., Henny, P., Lee, M. G. & Jones, B. E. GABAergic neurons intermingled with orexin and MCH neurons in the lateral hypothalamus discharge maximally during sleep. Eur. J. Neurosci. 32, 448-457 (2010).
62. Karnani, M. M., Szabó, G., Erdélyi, F. & Burdakov, D. Lateral hypothalamic GAD65 neurons are spontaneously firing and distinct from orexin- and melanin-concentrating hormone neurons. J. Physiol. 591, 933-953 (2013).
63. Wilding, J. P., Gilbey, S. G., Lambert, P. D., Ghatei, M. A. & Bloom, S. R. Increases in neuropeptide Y content and gene expression in the hypothalamus of rats treated with dexamethasone are prevented by insulin. Neuroendocrinology 57, 581-587 (1993).
64. Stricker-Krongrad, A., Richy, S. & Beck, B. Orexins/hypocretins in the ob/ob mouse: hypothalamic gene expression, peptide content and metabolic effects. Regul. Pept. 104, 11-20 (2002).
65. Hanson, E. S. & Dallman, M. F. Neuropeptide Y (NPY) may integrate responses of hypothalamic feeding systems and the hypothalamo-pituitary-adrenal axis. J. Neuroendocrinol. 7, 273-279 (1995).
66. Baskin, D. G., Hahn, T. M. & Schwartz, M. W. Leptin sensitive neurons in the hypothalamus. Horm. Metab. Res. 31, 345-350 (1999).
67. Gavrila, A. et al. Diurnal and ultradian dynamics of serum adiponectin in healthy men: Comparison with leptin, circulating soluble leptin receptor, and cortisol patterns. J. Clin. Endocrinol. Metab. 88, 2838-2843 (2003).
68. Belle, M. D. et al. Acute suppressive and long-term phase modulation actions of orexin on the mammalian circadian clock. J. Neurosci. 34, 3607-3621 (2014).
69. Leshan, R. L., Björnholm, M., Münzberg, H. & Myers, M. G. Leptin receptor signaling and action in the central nervous system. Obesity (Silver Spring) 14(Suppl 5): 208S-212S (2006).