Glutamatergic preoptic area neurons that express leptin receptors drive temperature-dependent body weight homeostasis

Journal of Neuroscience

Volumn 36, Issue 18, 2016, Pages 5034-5046

  Yu, Sangho ^a   Qualls Creekmore, Emily ^a   Rezai Zadeh, Kavon ^a   Jiang, Yanyan ^b   Berthoud, Hans Rudolf ^a   Morrison, Christopher D ^a   Derbenev, Andrei V ^b   Zsombok, Andrea ^b   Münzberg, Heike ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Body temperature; Body weight; DREADD; Energy expenditure; Food intake; Thermoregulation

Indexed keywords

CLOZAPINE N OXIDE; LEPTIN RECEPTOR; STAT3 PROTEIN; BETA 3 ADRENERGIC RECEPTOR; GLUTAMIC ACID DERIVATIVE; LEPTIN RECEPTOR, MOUSE;

ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; BODY WEIGHT MAINTENANCE; BROWN ADIPOSE TISSUE; CELL COUNT; CONTROLLED STUDY; ENERGY EXPENDITURE; FEMALE; FOOD INTAKE; GABAERGIC TRANSMISSION; GLUTAMATERGIC SYNAPSE; HOMEOSTASIS; HYPOTHERMIA; IMMUNOHISTOCHEMISTRY; LOCOMOTION; LUNG GAS EXCHANGE; MALE; MICROSCOPY; MOUSE; NONHUMAN; PHARMACOGENETICS; PREOPTIC AREA; PRIORITY JOURNAL; RECTUM TEMPERATURE; THERMOGENESIS; TRAINING; ANIMAL; BIOSYNTHESIS; BODY WEIGHT; CYTOLOGY; DRUG EFFECTS; EATING; ENERGY METABOLISM; GENETICS; NERVE CELL; PHYSIOLOGY; TEMPERATURE; THERMOREGULATION;

ADIPOSE TISSUE, BROWN; ANIMALS; BODY TEMPERATURE; BODY TEMPERATURE REGULATION; BODY WEIGHT; EATING; ENERGY METABOLISM; GLUTAMATES; HOMEOSTASIS; MICE; NEURONS; PREOPTIC AREA; RECEPTORS, ADRENERGIC, BETA-3; RECEPTORS, LEPTIN; TEMPERATURE;

EID: 84965011463     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0213-16.2016     Document Type: Article

References (52)

1. Andersson B, Larsson B (1961) Influence of local temperature changes in the preoptic area and rostral hypothalamus on the regulation of food and water intake. Acta Physiol Scand 52:75-89. CrossRef Medline
2. Andersson B, Ekman L, Gale CC, Sundsten JW (1963) Control of thyrotrophic hormone (Tsh) secretion by the "heat loss center." Acta Physiol Scand 59:12-33. CrossRef Medline
3. Bellefontaine N, Chachlaki K, Parkash J, Vanacker C, Colledge W, d’Anglemont de Tassigny X, Garthwaite J, Bouret SG, Prevot V (2014) Leptin-dependent neuronal NO signaling in the preoptic hypothalamus facilitates reproduction. J Clin Invest 124:2550-2559. CrossRef Medline
4. Boulant JA, Dean JB (1986) Temperature receptors in the central nervous system. Annu Rev Physiol 48:639-654. CrossRef Medline
5. Cannon B, Nedergaard J (2011) Nonshivering thermogenesis and its adequate measurement in metabolic studies. J Exp Biol 214:242-253. CrossRef Medline
6. Cao WH, 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. CrossRef Medline
7. Cao WH, Fan W, Morrison SF (2004) Medullary pathways mediating specific sympathetic responses to activation of dorsomedial hypothalamus. Neuroscience 126:229-240. CrossRef Medline
8. Collins S, Yehuda-Shnaidman E, WangH (2010) Positive and negative control of Ucp1 gene transcription and the role of β-adrenergic signaling networks. Int J Obes (Lond) 34 [Suppl 1]:S28-S33. CrossRef Medline
9. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509-1517. CrossRef Medline
10. Dulloo AG, Jacquet J, Girardier L (1997) Poststarvation hyperphagia and body fat overshooting in humans: a role for feedback signals from lean and fat tissues. Am J Clin Nutr 65:717-723. Medline
11. Enriori PJ, Sinnayah P, Simonds SE, Garcia Rudaz C, Cowley MA (2011) Leptin action in the dorsomedial hypothalamus increases sympathetic tone to brown adipose tissue in spite of systemic leptin resistance. J Neurosci 31:12189-12197. CrossRef Medline
12. Faouzi M, Leshan R, Björnholm M, Hennessey T, Jones J, Münzberg H (2007) Differential accessibility of circulating leptin to individual hypothalamic sites. Endocrinology 148:5414-5423. CrossRef Medline
13. Gao Q, Horvath TL (2007) Neurobiology of feeding and energy expenditure. Annu Rev Neurosci 30:367-398. CrossRef Medline
14. Grujic D, Susulic VS, Harper ME, Himms-Hagen J, Cunningham BA, Corkey BE, Lowell BB (1997) Beta3-adrenergic receptors on white and brown adipocytes mediate beta3-selective agonist-induced effects on energy expenditure, insulin secretion, and food intake. A study using transgenic and gene knockout mice. J Biol Chem 272:17686-17693. CrossRef Medline
15. Hamilton CL, Brobeck JR (1964) Food intake and temperature regulation in rats with rostral hypothalamic lesions. Am J Physiol 207:291-297. Medline
16. Harris RB, Kasser TR, Martin RJ (1986) Dynamics of recovery of body composition after overfeeding, food restriction or starvation of mature female rats. J Nutr 116:2536-2546. Medline
17. Haynes WG, Morgan DA, Walsh SA, Mark AL, Sivitz WI (1997) Receptormediated regional sympathetic nerve activation by leptin. J Clin Invest 100:270-278. CrossRef Medline
18. Jeong JH, Lee DK, Blouet C, Ruiz HH, Buettner C, Chua S Jr, Schwartz GJ, Jo YH (2015) Cholinergic neurons in the dorsomedial hypothalamus regulate mouse brown adipose tissue metabolism. Mol Metab 4:483-492. CrossRef Medline
19. Joly-AmadoA,CansellC,DenisRG,DelbesAS,Castel J,MartinezS,LuquetS (2014) The hypothalamic arcuate nucleus and the control of peripheral substrates. Best Pract Res Clin Endocrinol Metab 28:725-737. CrossRef Medline
20. Kim B (2008) Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate. Thyroid 18:141-144. CrossRef Medline
21. Laque A, Yu S, Qualls-Creekmore E, Gettys S, Schwartzenburg C, Bui K, Rhodes C, Berthoud HR, Morrison CD, Richards BK, Münzberg H (2015) Leptin modulates nutrient reward via inhibitory galanin action on orexin neurons. Mol Metab 4:706-717. CrossRef Medline
22. Leshan RL, Bjornholm M, Munzberg H, Myers MG Jr (2006) Leptin receptor signaling and action in the central nervous system. Obesity (Silver Spring) 14 [Suppl 5]:208S-212S. Medline
23. Leshan RL, Opland DM, Louis GW, Leinninger GM, Patterson CM, Rhodes CJ, Münzberg H, Myers MG Jr (2010) Ventral tegmental area leptin receptor neurons specifically project to and regulate cocaine-and amphetamine-regulated transcript neurons of the extended central amygdala. J Neurosci 30:5713-5723. CrossRef Medline
24. 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-R325. Medline
25. Martelli D, Luppi M, Cerri M, Tupone D, Mastrotto M, Perez E, Zamboni G, Amici R (2014) The direct cooling of the preoptic-hypothalamic area elicits the release of thyroid stimulating hormone during wakefulness but not during REM sleep. PLoS One 9:e87793. CrossRef Medline
26. McKinley MJ, Yao ST, Uschakov A, McAllen RM, Rundgren M, Martelli D (2015) The median preoptic nucleus: front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis. Acta Physiol (Oxf) 214:8-32. CrossRef Medline
27. Morrison SF, Madden CJ, Tupone D (2014) Central neural regulation of brown adipose tissue thermogenesis and energy expenditure. Cell Metab 19:741-756. CrossRef Medline
28. Münzberg H, Morrison CD (2015) Structure, production and signaling of leptin. Metabolism 64:13-23. CrossRef Medline
29. NakamuraK (2011) Central circuitries for body temperature regulation and fever. Am J Physiol Regul Integr Comp Physiol 301:R1207-R1228. CrossRef Medline
30. Nakamura K, Morrison SF (2007) Central efferent pathways mediating skin cooling-evoked sympathetic thermogenesis in brown adipose tissue.AmJ Physiol Regul Integr Comp Physiol 292:R127-R136. Medline
31. Nakamura K, Morrison SF (2008) Preoptic mechanism for cold-defensive responses to skin cooling. J Physiol 586:2611-2620. CrossRef Medline
32. Nakamura K, Matsumura K, Kaneko T, Kobayashi S, Katoh H, Negishi M (2002) The rostral raphe pallidus nucleus mediates pyrogenic transmission from the preoptic area. J Neurosci 22:4600-4610. Medline
33. Nakamura Y, Nakamura K, Matsumura K, Kobayashi S, Kaneko T, Morrison SF (2005) Direct pyrogenic input from prostaglandin EP3 receptorexpressing preoptic neurons to the dorsomedial hypothalamus. Eur J Neurosci 22:3137-3146. CrossRef Medline
34. Nakamura Y, Nakamura K, Morrison SF (2009) Different populations of prostaglandin EP3 receptor-expressing preoptic neurons project to two fever-mediating sympathoexcitatory brain regions. Neuroscience 161:614-620. CrossRef Medline
35. Paxinos G, Franklin KB (2004) The mouse brain in stereotaxic coordinates, compact 2nd ed. Boston: Elsevier Academic.
36. Ravussin Y, Xiao C, Gavrilova O, Reitman ML (2014) Effect of intermittent cold exposure on brown fat activation, obesity, and energy homeostasis in mice. PLoS One 9:e85876. CrossRef Medline
37. Rezai-Zadeh K, Yu S, Jiang Y, Laque A, Schwartzenburg C, Morrison CD, Derbenev AV, Zsombok A, Münzberg H (2014) Leptin receptor neurons in the dorsomedial hypothalamus are key regulators of energy expenditure and body weight, but not food intake. Mol Metab 3:681-693. CrossRef Medline
38. RobertsWW (1988) Differential thermosensor control of thermoregulatory grooming, locomotion, and relaxed postural extension. AnnN Y Acad Sci 525:363-374. CrossRef Medline
39. Rosenbaum M, Leibel RL (2010) Adaptive thermogenesis in humans. Int J Obes (Lond) 34 [Suppl 1]:S47-S55. CrossRef Medline
40. Susulic VS, Frederich RC, Lawitts J, Tozzo E, Kahn BB, Harper ME, Himms-Hagen J, Flier JS, Lowell BB (1995) Targeted disruption of the beta 3-adrenergic receptor gene. J Biol Chem 270:29483-29492. CrossRef Medline
41. Sutton AK, Pei H, Burnett KH, Myers MG Jr, Rhodes CJ, Olson DP (2014) Control of food intake and energy expenditure by Nos1 neurons of the paraventricular hypothalamus. J Neurosci 34:15306-15318. CrossRef Medline
42. Swanson LW (1976) An autoradiographic study of the efferent connections of the preoptic region in the rat. J Comp Neurol 167:227-256. CrossRef Medline
43. Thompson RH, Swanson LW (2003) Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Rev 41:153-202. CrossRef Medline
44. Trayhurn P, Thurlby PL, James WP (1977) Thermogenic defect in preobese ob/ob mice. Nature 266:60-62. CrossRef Medline
45. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ (2009) Coldactivated brown adipose tissue in healthy men. N Engl J Med 360:1500-1508. CrossRef Medline
46. Vong L, Ye C, Yang Z, Choi B, Chua S Jr, Lowell BB (2011) Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71:142-154. CrossRef Medline
47. Xiao C, Goldgof M, Gavrilova O, ReitmanML (2015) Anti-obesity and metabolic efficacy of the beta3-adrenergic agonist, CL316243, in mice at thermoneutrality compared to 22 degrees C. Obesity (Silver Spring) 23:1450-1459. CrossRef Medline
48. Xu Y, Kim ER, Zhao R, Myers MG Jr, Munzberg H, Tong Q (2013) Glutamate release mediates leptin action on energy expenditure. Mol Metab 2:109-115. CrossRef Medline
49. Yoshida K, Li X, Cano G, Lazarus M, Saper CB (2009) Parallel preoptic pathways for thermoregulation. J Neurosci 29:11954-11964. CrossRef Medline
50. Zaretskaia MV, Zaretsky DV, Shekhar A, DiMicco JA (2002) Chemical stimulation of the dorsomedial hypothalamus evokes non-shivering thermogenesis in anesthetized rats. Brain Res 928:113-125. CrossRef Medline
51. Zaretskaia MV, Zaretsky DV, DiMicco JA (2003) Role of the dorsomedial hypothalamus in thermogenesis and tachycardia caused by microinjection of prostaglandin E2 into the preoptic area in anesthetized rats. Neurosci Lett 340:1-4. CrossRef Medline
52. Zhang Y, Kerman IA, Laque A, Nguyen P, Faouzi M, Louis GW, Jones JC, Rhodes C, Münzberg H (2011) Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits. J Neurosci 31:1873-1884. CrossRef Medline