Orexin neurons are indispensable for prostaglandin E2-induced fever and defence against environmental cooling in mice

Journal of Physiology

Volumn 591, Issue 22, 2013, Pages 5623-5643

  Takahashi, Yoshiko ^a,b   Zhang, Wei ^c   Sameshima, Kohei ^a   Kuroki, Chiharu ^a,b   Matsumoto, Ami ^a   Sunanaga, Jinko ^a,b   Kono, Yu ^a   Sakurai, Takeshi ^d   Kanmura, Yuichi ^b   Kuwaki, Tomoyuki ^a  

^a Departments of Physiology   (Japan)

^b KAGOSHIMA UNIVERSITY   (Japan)

^c University of Alabama at Birmingham   (United States)

^d KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; OREXIN; PROSTAGLANDIN E2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE DISORDER; BRAIN NERVE CELL; CELL ACTIVATION; COLD EXPOSURE; CONTROLLED STUDY; COOLING; ENVIRONMENTAL TEMPERATURE; FEVER; HEATING; MALE; MEDULLARY RAPHE NUCLEUS,; MOUSE; NONHUMAN; NUCLEUS RAPHE PALLIDUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAPHE NUCLEUS; RECTUM TEMPERATURE; THERMOGENESIS; THERMOREGULATION; WILD TYPE;

ANIMALS; COLD TEMPERATURE; DINOPROSTONE; FEVER; GLUTAMIC ACID; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; NEUROPEPTIDES; OREXIN RECEPTORS; RAPHE NUCLEI; RECEPTORS, GLUTAMATE; THERMOGENESIS;

EID: 84887615250     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.261271     Document Type: Article

References (57)

1. Abrahamson EE, Leak RK & Moore RY (2001). The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport 12, 435-440.
2. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K & de Lecea L (2007). Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420-424.
3. Arrigoni E, Mochizuki T & Scammell TE (2010). Activation of the basal forebrain by the orexin/hypocretin neurons. Acta Physiol 198, 223-235.
4. Berthoud H-R, Patterson LM, Sutton GM, Morrison C & Zheng H (2005). Orexin inputs to caudal raphé neurons involved in thermal, cardiovascular, and gastrointestinal regulation. Histochem Cell Biol 123, 147-156.
5. Cano G, Passerin AM, Schiltz JC, Card JP, Morrison SF & Sved AF (2003). Anatomical substrates for the central control of sympathetic outflow to interscapular adipose tissue during cold exposure. J Comp Neurol 460, 303-326.
6. Cao W-H & Morrison SF (2006). Glutamate receptors in the raphe pallidus mediate brown adipose tissue thermogenesis evoked by activation of dorsomedial hypothalamic neurons. Neuropharmacology 51, 426-437.
7. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, Fitch TE, Nakazato M, Hammer RE, Saper CB & Yanagisawa M (1999). Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98, 437-451.
8. Cheng SB, Kuchiiwa S, Gao HZ, Kuchiiwa T & Nakagawa S (2003). Morphological study of orexin neurons in the hypothalamus of the Long-Evans rat, with special reference to co-expression of orexin and NADPH-diaphorase or nitric oxide synthase activities. Neurosci Res 46, 53-62.
9. Chou TC, Lee CE, Lu J, Elmquist JK, Hara J, Willie JT, Beuckmann CT, Chemelli RM, Sakurai T, Yanagisawa M, Saper CB & Scammell TE (2001). Orexin (hypocretin) neurons contain dynorphin. J Neurosci 21, RC168.
10. Conte WL, Kamishina H & Reep RL (2009). Multiple neuroanatomical tract-tracing using fluorescent Alexa Fluor conjugates of cholera toxin subunit B in rats. Nature Protocols 4, 1157-1166.
11. Deng B-S, Nakamura A, Zhang W, Yanagisawa M, Fukuda Y & Kuwaki T (2007). Contribution of orexin in hypercapnic chemoreflex: evidence from genetic and pharmacological disruption and supplementation studies in mice. J Appl Physiol 103, 1772-1779.
12. DiMicco JA & Zaretsky DV (2007). The dorsomedial hypothalamus: a new player in thermoregulation. Am J Physiol Regul Integr Comp Physiol 292, R47-63.
13. Elias CF, Saper CB, Maratos-Flier E, Tritos NA, Lee C, Kelly J, Tatro JB, Hoffman GE, Ollmann MM, Barsh GS, Sakurai T, Yanagisawa M & Elmquist JK (1998). Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J Comp Neurol 402, 442-459.
14. Estabrooke IV, McCarthy MT, Ko E, Chou TC, Chemelli RM, Yanagisawa M, Saper CB & Scammell TE (2001). Fos expression in orexin neurons varies with behavioral state. J Neurosci 21, 1656-1662.
15. Fadel J, Bubser M & Deutch AY (2002). Differential activation of orexin neurons by antipsychotic drugs associated with weight gain. J Neurosci 22, 6742-6746.
16. Hakansson M, de Lecea L, Sutcliffe JG, Yanagisawa M & Meister B (1999). Leptin receptor- and STAT3-immunoreactivities in hypocretin/orexin neurones of the lateral hypothalamus. J Neuroendocrinol 11, 653-663.
17. Handler CM, Piliero TC, Geller EB & Adler MW (1994). Effect of ambient temperature on the ability of mu-, kappa- and delta-selective opioid agonists to modulate thermoregulatory mechanisms in the rat. J Pharmacol Exp Ther 268, 847-855.
18. Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM, Sinton CM, 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.
19. Harris GC, Wimmer M & Aston-Jones G (2005). A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437, 556-559.
20. Kayaba Y, Nakamura A, Kasuya Y, Ohuchi T, Yanagisawa M, Komuro I, Fukuda Y & Kuwaki T (2003). Attenuated defense response and low basal blood pressure in orexin knockout mice. Am J Physiol Regul Integr Comp Physiol 285, R581-593.
21. Li Y, Gao X-B, Sakurai T & Pol ANvd (2002). Hypocretin/orexin excites hypocretin neurons via a local glutamate neuron - a potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36, 1169-1181.
22. Madden CJ & Morrison SF (2003). Excitatory amino acid receptor activation in the raphe pallidus area mediates prostaglandin-evoked thermogenesis. Neuroscience 122, 5-15.
23. Madden CJ & Morrison SF (2004). Excitatory amino acid receptors in the dorsomedial hypothalamus mediate prostaglandin-evoked thermogenesis in brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 286, R320-325.
24. McAllen RM, Tanaka M, Ootsuka Y & McKinley MJ (2010). Multiple thermoregulatory effectors with independent central controls. Eur J Appl Physiol 109, 27-33.
25. Mileykovskiy BY, Kiyashchenko LI & Siegel JM (2005). Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46, 787-798.
26. Morrison SF (2011). Central neural pathways for thermoregulatory cold defense. J Appl Physiol 110, 1137-1149.
27. Morrison SF & Nakamura K (2011). Central neural pathways for thermoregulation. Front Biosci 16, 74-104.
28. Nakamura K (2011). Central circuitries for body temperature regulation and fever. Am J Physiol Regul Integr Comp Physiol 301, R1207-1228.
29. Nakamura K & Morrison SF (2007). Central efferent pathways mediating skin cooling-evoked sympathetic thermogenesis in brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 292, R127-136.
30. Nakamura K & Morrison SF (2011). Central efferent pathways for cold-defensive and febrile shivering. J Physiol 589, 3641-3658.
31. Nakamura Y, Nakamura K, Matsumura K, Kobayashi S, Kaneko T & Morrison SF (2005). Direct pyrogenic input from prostaglandin EP3 receptor-expressing preoptic neurons to the dorsomedial hypothalamus. Eur J Neurosci 22, 3137-3146.
32. Nambu T, Sakurai T, Mizukami K, Hosoya Y, Yanagisawa M & Goto K (1999). Distribution of orexin neurons in the adult rat brain. Brain Res 827, 243-260.
33. Oldfield BJ, Giles ME, Watson A, Anderson C, Colvill LM & Mckinley MJ (2002). The neurochemical characterisation of hypothalamic pathways projecting polysynaptically to brown adipose tissue in the rat. Neuroscience 110, 515-526.
34. Paxinos G & Franklin KBJ (2001). The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, Tokyo.
35. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG & Kilduff TS (1998). Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18, 9996-10015.
36. Rathner J, Madden C & Morrison S (2008). Central pathway for spontaneous and prostaglandin E2-evoked cutaneous vasoconstriction. Am J Physiol Regul Integr Comp Physiol 295, R343-354.
37. Rosin DL, Weston MC, Sevigny CP, Stornetta RL & Guyenet PG (2003). Hypothalamic orexin (hypocretin) neurons express vesicular glutamate transporters VGLUT1 or VGLUT2. J Comp Neurol 465, 593-603.
38. Rusyniak DE, Zaretskya DV, Zaretskaiaa MV & DiMiccob JA (2011). The role of orexin-1 receptors in physiologic responses evoked by microinjection of PgE2 or muscimol into the medial preoptic area. Neurosci Lett 498, 162-166.
39. Sakurai T (2007). The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8, 171-181.
40. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richarson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ & Yanagisawa M (1998). Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behaviour. Cell 92, 573-585.
41. Samuels BC, Zaretsky DV & DiMicco JA (2004). Dorsomedial hypothalamic sites where disinhibition evokes tachycardia correlate with location of raphe-projecting neurons. Am J Physiol Regul Integr Comp Physiol 287, R472-478.
42. Schöne C, Cao ZFH, Apergis-Schoute J, Adamantidis A, Sakurai T & Burdakov D (2012). Optogenetic probing of fast glutamatergic transmission from hypocretin/orexin to histamine neurons in situ. J Neurosci 32, 12437-12443.
43. Sellayah D, Bharaj P & Sikder D (2011). Orexin is required for brown adipose tissue development, differentiation, and function. Cell Metab 14, 478-490.
44. Steiner AA, Antunes-Rodrigues J, McCann SM & Branco LG (2002). Antipyretic role of the NO-cGMP pathway in the anteroventral preoptic region of the rat brain. Am J Physiol Regul Integr Comp Physiol 282, R584-593.
45. 2 activates orexin-containing neurons in mice. Respir Physiol Neurobiol 166, 184-186.
46. Takahashi K, Lin JS & Sakai K (2008). Neuronal activity of orexin and non-orexin waking-active neurons during wake-sleep states in the mouse. Neuroscience 153, 860-870.
47. Terada J, Nakamura A, Zhang W, Yanagisawa M, Kuriyama T, Fukuda Y & Kuwaki T (2008). Ventilatory long-term facilitation in mice can be observed both during sleep and wake periods and depends on orexin. J Appl Physiol 104, 499-507.
48. Torrealba F, Yanagisawa M & Saper CB (2003). Colocalization of orexin A and glutamate immunoreactivity in axon terminals in the tuberomammillary nucleus in rats. Neuroscience 119, 1033-1044.
49. Toyama S, Sakurai T, Tatsumi K & Kuwaki T (2009). Attenuated phrenic long-term facilitation in orexin neuron-ablated mice. Respir Physiol Neurobiol 168, 295-302.
50. Tupone D, Madden CJ, Cano G & Morrison SF (2011). An orexinergic projection from perifornical hypothalamus to raphe pallidus increases rat brown adipose tissue thermogenesis. J Neurosci 31, 15944-15955.
51. Vinkers CH, Groenink L, van Bogaert MJV, Westphal KGC, Kalkman CJ, van Oorschot R, Oosting RS, Olivier B & Korte SM (2009). Stress-induced hyperthermia and infection-induced fever: two of a kind Physiol Behav 98, 37-43.
52. Watanabe S, Kuwaki T, Yanagisawa M, Fukuda Y & Shimoyama M (2005). Persistent pain and stress activate pain-inhibitory orexin pathways. Neuroreport 16, 5-8.
53. Yamanaka A, Beuckmann CT, Willie JT, 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.
54. Yoshida K, Li X, Cano G, Lazarus M & Saper CB (2009). Parallel preoptic pathways for thermoregulation. J Neurosci 29, 11954-11964.
55. Zhang W, Sakurai T, Fukuda Y & Kuwaki T (2006). Orexin neuron-mediated skeletal muscle vasodilation and shift of baroreflex during defense response in mice. Am J Physiol Regul Integr Comp Physiol 290, R1654-1663.
56. Zhang W, Sunanaga J, Takahashi Y, Mori T, Sakurai T, Kanmura Y & Kuwaki T (2010). Orexin neurons are indispensable for stress-induced thermogenesis in mice. J Physiol 588, 4117-4129.
57. Zhang W, Zhang N, Sakurai T & Kuwaki T (2009). Orexin neurons in the hypothalamus mediate cardiorespiratory responses induced by disinhibition of the amygdala and bed nucleus of the stria terminalis. Brain Res 1262, 25-37.