Orexin and MCH neurons express c-Fos differently after sleep deprivation vs. recovery and bear different adrenergic receptors

European Journal of Neuroscience

Volumn 21, Issue 10, 2005, Pages 2807-2816

  Modirrousta, Mandana ^a   Mainville, Lynda ^a   Jones, Barbara E ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Hypocretin; Hypothalamus; Noradrenaline; Rat; Waking

Indexed keywords

ADRENERGIC RECEPTOR; ALPHA 1A ADRENERGIC RECEPTOR; ALPHA 2 ADRENERGIC RECEPTOR; ALPHA 2A ADRENERGIC RECEPTOR; MELANIN CONCENTRATING HORMONE; NORADRENALIN; OREXIN; PROTEIN C FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SLEEP; SLEEP DEPRIVATION; WAKEFULNESS;

ANIMALS; HYPOTHALAMIC HORMONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MELANINS; NEURONS; NEUROPEPTIDES; PITUITARY HORMONES; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SLEEP; SLEEP DEPRIVATION;

EID: 20644467465     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04104.x     Document Type: Article

References (61)

1. Alam, M.N., Gong, H., Alam, T., Jaganath, R., McGinty, D. & Szymusiak, R. (2002) Sleep-waking discharge patterns of neurons recorded in the rat perifornical lateral hypothalamic area. J. Physiol. (Lond.), 538, 619-631.
2. Aston-Jones, G. & Bloom, F.E. (1981) Activity of norepinephrine- containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J. Neurosci., 1, 876-886.
3. Bayer, L., Eggermann, E., Serafin, M., Grivel, J., Machard, D., Muhtethaler, M. & Jones, B.E. (2005) Opposite effects of noradrenaline and acotylcholine upon hypocretin/orexin versus melanin concentrating hormone neurons in rat hypothalamic slices. Neuroscience, 130, 807-811.
4. Bayer, L., Eggermann, E., Serafin, M., Saint-Mieux, B., Machard, D., Jones, B. & Muhlethaler, M. (2001) Orexins (hypocretins) directly excite tuberomammillary neurones. Eur. J. Neurosci., 14, 1571-1575.
5. Bayer, L., Mairet-Coello, G., Risold, P.Y. & Griffond, B. (2002) Orexin/hypocretin neurons: chemical phenotype and possible interactions with melanin-concentrating hormone neurons. Regul. Pept., 104, 33-39.
6. Bergmann, B.M., Winter, J.B., Rosenberg, R.S. & Rechtschaffen, A. (1987) NREM sleep with low-voltage EEG in the rat. Sleep, 10, 1-11.
7. Bittencourt, J.C., Presse, F., Arias, C., Peto, C., Vaughan, J., Nahon, J.L., Vale, W. & Sawchenko, P.E. (1992) The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J. Comp. Neurol., 319, 218-245.
8. Broberger, C., De Lecea, L., Sutcliffe, J.G. & Hokfelt, T. (1998) Hypocretin/orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J. Comp. Neurol., 402, 460-474.
9. Burlet, S., Tyler, C.J. & Leonard, C.S. (2002) Direct and indirect excitation of laterodorsal tegmental neurons by Hypocretin/Orexin peptides: implications for wakefulness and narcolepsy. J. Neurosci., 22, 2862-2872.
10. Chemelli, R.M., Willie, J.T., Sinton, C.M., Elmquist, J.K., Scammell, T., Lee, C., Richardson, J.A., Williams, S.C., Xiong, Y., Kisanuki, Y., Fitch, T.E., Nakazato, M., Hammer, R.E., Saper, C.B. & Yanagisawa, M. (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell, 98, 437-451.
11. Eggermann, E., Serafin, M., Bayer, L., Machard, D., Saint-Mleux, B., Jones, B.E. & Muhlethaler, M. (2001) Orexins/hypocretins excite basal forebrain cholinergic neurones. Neuroscience, 108, 177-181.
12. Espana, R.A., Plahn, S. & Berridge, C.W. (2002) Circadian-dependent and circadian-independent behavioral actions of hypocretin/orexin. Brain Res., 943, 224-236.
13. Espana, R.A., Valentino, R.J. & Berridge, C.W. (2003) Fos immunoreactivity in hypocretin-synthesizing and hypocretin-1 receptor-expressing neurons: effects of diurnal and nocturnal spontaneous waking, stress and hypocretin-1 administration. Neuroscience, 121, 201-217.
14. Estabrooke, I.V., McCarthy, M.T., Ko, E., Chou, T.C., Chemelli, R.M., Yanagisawa, M., Saper, C.B. & Scammell, T.E. (2001) Fos expression in orexin neurons varies with behavioral state. J. Neurosci., 21, 1656-1662.
15. Ferguson, A.V. & Samson, W.K. (2003) The orexin/hypocretin system: a critical regulator of neuroendocrine and autonomic function. Front. Neuroendocrinol., 24, 141-150.
16. Flugge, G., van Kampen, M., Meyer, H. & Fuchs, E. (2003) Alpha2A and alpha2C-adrenoceptor regulation in the brain: alpha2A changes persist after chronic stress. Eur. J. Neurosci., 17, 917-928.
17. Fort, P., Khateb, A., Pegna, A., Muhlethaler, M. & Jones, B.E. (1995) Noradrenergic modulation of cholinergic nucleus basalis neurons demonstrated by in vitro pharmacological and immunohistochemical evidence in the guinea pig brain. Eur. J. Neurosci., 7, 1502-1511.
18. Fort, P., Khateb, A., Serafin, M., Muhlethaler, M. & Jones, B.E. (1998) Pharmacological characterization and differentiation of non-cholinergic nucleus basalis neurons in vitro. Neuroreport, 9, 1-5.
19. Fujiki, N., Yoshida, Y., Ripley, B., Honda, K., Mignot, E. & Nishino, S. (2001) Changes in CSF hypocretin-1 (orexin A) levels in rats across 24 hours and in response to food deprivation. Neuroreport, 12, 993-997.
20. Gallopin, T., Fort, P., Eggermann, E., Cauli, B., Luppi, P.H., Rossier, J., Audinat, E., Muhlethaler, M. & Serafin, M. (2000) Identification of sleep-promoting neurons in vitro. Nature, 404, 992-995.
21. Gao, X.B. & van den Pol, A.N. (2001) Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypothalamus. J. Physiol. (Lond.), 533, 237-252.
22. Gritti, I., Mainville, L. & Jones, B.E. (1993) Codistribution of GABA with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J. Comp. Neurol., 329, 438-457.
23. Grivel, J., Tobler, I., Muhlethaler, M. & Serafin, M. (2004) Following sleep deprivation the excitation of hypocretin/orexin neurons by noradrenaline reverses to inhibition. Soc. Neurosci. Abstr., 318.8.
24. Guan, J.L., Uehara, K., Lu, S., Wang, Q.P., Funahashi, H., Sakurai, T., Yanagizawa, M. & Shioda, S. (2002) Reciprocal synaptic relationships between orexin- and melanin-concentrating hormone-containing neurons in the rat lateral hypothalamus: a novel circuit implicated in feeding regulation. Int. J. Obes. Relat. Metab. Disord., 26, 1523-1532.
25. Hairston, I.S., Peyron, C., Denning, D.P., Ruby, N.F., Flores, J., Sapolsky, R.M., Heller, H.C. & O'Hara, B.F. (2004) Sleep deprivation effects on growth factor expression in neonatal rats: a potential role for BDNF in the mediation of delta power. J. Neurophysiol., 91, 1586-1595.
26. Hara, J., Beuckmann, C.T., Nambu, T., Willie, J.T., Chemelli, R.M., Sinton, C.M., Sugiyama, F., Yagami, K., Goto, K., Yanagisawa, M. & Sakurai, T. (2001) Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron, 30, 345-354.
27. Horvath, T.L., Peyron, C., Diano, S., Ivanov, A., Aston-Jones, G., Kilduff, T.S. & van den Pol, A.N. (1999) Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J. Comp. Neurol., 415, 145-159.
28. Ida, T., Nakahara, K., Murakami, T., Hanada, R., Nakazato, M. & Murakami, N. (2000) Possible involvement of orexin in the stress reaction in rats. Biochem. Biophys. Res. Commun., 270, 318-323.
29. Ito, M., Gomori, A., Ishihara, A., Oda, Z., Mashiko, S., Matsushita, H., Yumoto, M., Sano, H., Tokita, S., Moriya, M., Iwaasa, H. & Kanatani, A. (2003) Characterization of MCH-mediated obesity in mice. Am. J. Physiol. Endocrinol. Metab., 284, E940-E945.
30. Jhanwar-Uniyal, M., Roland, C.R. & Leibowitz, S.F. (1986) Diurnal rhythm of alpha 2-noradrenergic receptors in the paraventricular nucleus and other brain areas: relation to circulating corticosterone and feeding behavior. Life Sci., 38, 473-482.
31. Jones, B.E. (2000) Basic mechanisms of sleep-wake states. In Kryger, M.H., Roth, T., & Dement, W.C., (Eds), Principles and Practice of Sleep Medicine. Saunders, Philadelphia, pp. 134-154.
32. Jones, B.E. & Yang, T.-Z. (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J. Comp. Neurol., 242, 56-92.
33. Kennedy, A.R., Todd, J.F., Stanley, S.A., Abbott, C.R., Small, C.J., Ghatei, M.A. & Bloom, S.R. (2001) Melanin-concentrating hormone (MCH) suppresses thyroid stimulating hormone (TSH) release, in vivo and in vitro, via the hypothalamus and the pituitary. Endocrinology, 142, 3265-3268.
34. Kiyashchenko, L.I., Mileykovskiy, B.Y., Maidment, N., Lam, H.A., Wu, M.F., John, J., Peever, J. & Siegel, J.M. (2002) Release of hypocretin (orexin) during waking and sleep states. J. Neurosci., 22, 5282-5286.
35. Koyama, Y., Takahashi, K., Kodama, T. & Kayama, Y. (2003) State-dependent activity of neurons in the perifornical hypothalamic area during sleep and waking. Neuroscience, 119, 1209-1219.
36. Krout, K.E., Mettenleiter, T.C. & Loewy, A.D. (2003) Single CNS neurons link both central motor and cardiosympathetic systems: a double-virus tracing study. Neuroscience, 118, 853-866.
37. de Lecea, L., Kilduff, T.S., Peyron, C., Gao, X., Foye, P.E., Danielson, P.E., Fukuhara, C., Battenberg, E.L., Gautvik, V.T., Bartlett, F.S., 2nd, Frankel, W.N., van den Pol, A.N., Bloom, F.E., Gautvik, K.M. & Sutcliffe, J.G. (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl Acad. Sci. USA, 95, 322-327.
38. Li, Y., Gao, X.B., Sakurai, T. & van den Pol, A.N. (2002) Hypocretin/Orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron, 36, 1169-1181.
39. Lin, L., Faraco, J., Li, R., Kadotani, H., Rogers, W., Lin, X., Qiu, X., de Jong, P.J., Nishino, S. & Mignot, E. (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell, 98, 365-376.
40. Lubkin, M. & Stricker-Krongrad, A. (1998) Independent feeding and metabolic actions of orexins in mice. Biochem. Biophys. Res. Commun., 253, 241-245.
41. Maloney, K.J., Cape, E.G., Gotman, J. & Jones, B.E. (1997) High frequency gamma electroencephalogram activity in association with sleep-wake states and spontaneous behaviors in the rat. Neuroscience, 76, 541-555.
42. Manns, I.D., Lee, M.G., Modirrousta, M., Hou, Y.P. & Jones, B.E. (2003) Alpha 2 adrenergic receptors on GABAergic, putative sleep-promoting basal forebrain neurons. Eur. J. Neurosci., 18, 723-727.
43. Marsh, D.J., Weingarth, D.T., Novi, D.E., Chen, H.Y., Trumbauer, M.E., Chen, A.S., Guan, X.M., Jiang, M.M., Feng, Y., Camacho, R.E., Shen, Z. & Frazier, E.G., Yu, H., Metzger, J.M., Kuca, S.J., Shearman, L.P., Gopal-Truter, S., MacNeil, D.J., Strack, A.M., MacIntyre, D.E., Van der Ploeg, L.H. & Qian, S. (2002) Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc. Natl Acad. Sci. USA, 99, 3240-3245.
44. Modirrousta, M., Mainville, L. & Jones, B.E. (2004) GABAergic neurons with alpha2-adrenergic receptors in basal forebrain and preoptic area express c-Fos during sleep. Neuroscience, 129, 803-810.
45. Monda, M., Viggiano, A. & De Luca, V. (2003) Paradoxical [correction of parodoxical] effect of orexin A: hypophagia induced by hyperthermia. Brain Res., 961, 220-228.
46. Peyron, C., Faraco, J., Rogers, W., Ripley, B., Overeem, S., Charnay, Y., Nevsimalova, S., Aldrich, M., Reynolds, D., Albin, R., Li, R., Hungs, M., Pedrazzoli, M., Padigaru, M., Kucherlapati, M., Fan, J., Maki, R., Lammers, G.J., Bouras, C., Kucherlapati, R., Nishino, S. & Mignot, E. (2000) A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nature Med., 6, 991-997.
47. Peyron, C., Tighe, D.K., van den Pol, A.N., de Lecea, L., Heller, H.C., Sutcliffe, J.G. & Kilduff, T.S. (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci., 18, 9996-10015.
48. van den Pol, A.N. (1999) Hypothalamic hypocretin (orexin): robust innervation of the spinal cord. J. Neurosci., 19, 3171-3182.
49. van den Pol, A.N., Gao, X.B., Obrietan, K., Kilduff, T.S. & Belousov, A.B. (1998) Presynaptic and postsynaptic actions and modulation of neuroendocrine neurons by a new hypothalamic peptide, hypocretin/orexin. J. Neurosci., 18, 7962-7971.
50. Shearman, L.P., Camacho, R.E., Sloan Stribling, D., Zhou, D., Bednarek, M.A., Hreniuk, D.L., Feighner, S.D., Tan, C.P., Howard, A.D., Van der Ploeg, L.H., MacIntyre, D.E., Hickey, G.J. & Strack, A.M. (2003) Chronic MCH-1 receptor modulation alters appetite, body weight and adiposity in rats. Eur. J. Pharmacol., 475, 37-47.
51. Shimada, M., Tritos, N.A., Lowell, B.B., Flier, J.S. & Maratos-Flier, E. (1998) Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature, 396, 670-674.
52. Shirasaka, T., Nakazato, M., Matsukura, S., Takasaki, M. & Kannan, H. (1999) Sympathetic and cardiovascular actions of orexins in conscious rats. Am. J. Physiol., 277, R1780-R1785.
53. Steininger, T.L., Alam, M.N., Gong, H., Szymusiak, R. & McGinty, D. (1999) Sleep-waking discharge of neurons in the posterior lateral hypothalamus of the albino rat. Brain Res., 840, 138-147.
54. Thannickal, T.C., Moore, R.Y., Nienhuis, R., Ramanathan, L., Gulyani, S., Aldrich, M., Cornford, M. & Siegel, J.M. (2000) Reduced number of hypocretin neurons in human narcolepsy. Neuron, 27, 469-414.
55. Verret, L., Goutagny, R., Fort, P., Cagnon, L., Salvert, D., Leger, L., Boissard, R., Salin, P., Peyron, C. & Luppi, P.H. (2003) A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neurosci., 4, 19.
56. Williams, G., Cai, X.J., Elliott, J.C. & Harrold, J.A. (2004) Anabolic neuropeptides. Physiol. Behav., 81, 211-222.
57. Yamanaka, A., Beuckmann, C.T., Willie, J.T., Hara, J., Tsujino, N., Mieda, M., Tominaga, M., Yagami, K., Sugiyama, F., Goto, K., Yanagisawa, M. & Sakurai, T. (2003) Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron, 38, 701-713.
58. Yamuy, J., Fung, S.J., Xi, M. & Chase, M.H. (2004) Hypocretinergic control of spinal cord motoneurons. J. Neurosci., 24, 5336-5345.
59. Yoshida, Y., Fujiki, N., Nakajima, T., Ripley, B., Matsumura, H., Yoneda, H., Mignot, E. & Nishino, S. (2001) Fluctuation of extracellular hypocretin-1 (orexin A) levels in the rat in relation to the light-dark cycle and sleep-wake activities. Eur. J. Neurosci., 14, 1075-1081.
60. Zeitzer, J.M., Buckmaster, C.L., Parker, K.J., Hauck, C.M., Lyons, D.M. & Mignot, E. (2003) Orcadian and homeostatic regulation of hypocretin in a primate model: implications for the consolidation of wakefulness. J. Neurosci., 23, 3555-3560.
61. Zhou, D., Shen, Z., Strack, A.M., Marsh, D.J. & Shearman, L.P (2005) Enhanced running wheel activity of both Mch1r- and Pmch-deficient mice. Regul. Pept., 124, 53-63.