Leptin action in the dorsomedial hypothalamus increases sympathetic tone to brown adipose tissue in spite of systemic leptin resistance

Journal of Neuroscience

Volumn 31, Issue 34, 2011, Pages 12189-12197

  Enriori, Pablo J ^a   Sinnayah, Puspha ^b   Simonds, Stephanie E ^a   Rudaz, Cecilia Garcia ^a   Cowley, Michael A ^a  

^a MONASH UNIVERSITY   (Australia)

^b VICTORIA UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN; LEPTIN RECEPTOR; MELANOCORTIN; MELANOCORTIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; BRAIN NERVE CELL; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; HORMONE ACTION; HORMONE RESISTANCE; HYPERLEPTINEMIA; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; SYMPATHETIC NERVE; SYMPATHETIC TONE; THERMOGENESIS; THERMOREGULATION;

ADIPOSE TISSUE, BROWN; ANIMALS; BODY TEMPERATURE; DISEASE MODELS, ANIMAL; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; DRUG RESISTANCE; LEPTIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; OBESITY; RECEPTORS, LEPTIN; SYMPATHETIC NERVOUS SYSTEM; THERMOGENESIS;

EID: 80052156758     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2336-11.2011     Document Type: Article

References (46)

1. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB (2005) Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123:493-505
2. Barnes MJ, Lapanowski K, Conley A, Rafols JA, Jen KL, Dunbar JC (2003) High fat feeding is associated with increased blood pressure, sympathetic nerve activity and hypothalamic mu opioid receptors. Brain Res Bull 61:511-519
3. Bartness TJ, Vaughan CH, Song CK (2010) Sympathetic and sensory innervation of brown adipose tissue. Int J Obes (Lond) 34 [Suppl 1]:S36-S42.
4. Billes SK, Cowley MA (2008) Catecholamine reuptake inhibition causes weight loss by increasing locomotor activity and thermogenesis. Neuropsychopharmacology 33:1287-1297
5. Boston BA, Blaydon KM, Varnerin J, Cone RD (1997) Independent and additive effects of central POMC and leptin pathways on murine obesity. Science 278:1641-1644
6. Butler AA (2006) The melanocortin system and energy balance. Peptides 27:281-290
7. Butler AA, Kozak LP (2010) A recurring problem with the analysis of energy expenditure in genetic models expressing lean and obese phenotypes. Diabetes 59:323-329
8. Commins SP, Watson PM, Levin N, Beiler RJ, Gettys TW (2000) Central leptin regulates the UCP1 and ob genes in brown and white adipose tissue via different beta-adrenoceptor subtypes. J Biol Chem 275:33059-33067
9. Cone RD (2006) Studies on the physiological functions of the melanocortin system. Endocr Rev 27:736-749
10. Correia ML, Haynes WG, Rahmouni K, Morgan DA, Sivitz WI, Mark AL (2002) The concept of selective leptin resistance: evidence from agouti yellow obese mice. Diabetes 51:439-442
11. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, Cone RD, Low MJ (2001) Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480-484
12. Dimicco JA, Zaretsky DV (2007) The dorsomedial hypothalamus: a new player in thermoregulation. Am J Physiol Regul Integr Comp Physiol 292:R47-R63.
13. Eikelis N, Schlaich M, Aggarwal A, Kaye D, Esler M (2003) Interactions between leptin and the human sympathetic nervous system. Hypertension 41:1072-1079
14. Enriori PJ, Evans AE, Sinnayah P, Jobst EE, Tonelli-Lemos L, Billes SK, Glavas MM, Grayson BE, Perello M, Nillni EA, Grove KL, Cowley MA (2007) Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons. Cell Metab 5:181-194
15. Galletti F, D'Elia L, Barba G, Siani A, Cappuccio FP, Farinaro E, Iacone R, Russo O, De Palma D, Ippolito R, Strazzullo P (2008) High-circulating leptin levels are associated with greater risk of hypertension in men independently of body mass and insulin resistance: results of an eight-year follow-up study. J Clin Endocrinol Metab 93:3922-3926
16. Gautron L, Lazarus M, Scott MM, Saper CB, Elmquist JK (2010) Identifying the efferent projections of leptin-responsive neurons in the dorsomedial hypothalamus using a novel conditional tracing approach. J Comp Neurol 518:2090-2108
17. Greenfield JR, Miller JW, Keogh JM, Henning E, Satterwhite JH, Cameron GS, Astruc B, Mayer JP, Brage S, See TC, Lomas DJ, O'Rahilly S, Farooqi IS (2009) Modulation of blood pressure by central melanocortinergic pathways. N Engl J Med 360:44-52
18. Hall JE, da Silva AA, do Carmo JM, Dubinion J, Hamza S, Munusamy S, Smith G, Stec DE (2010) Obesity-induced hypertension: role of sympa-thetic nervous system, leptin, and melanocortins. J Biol Chem 285: 17271-17276
19. Harkin A, O'Donnell JM, Kelly JP (2002) A study of VitalView for behavioural and physiological monitoring in laboratory rats. Physiol Behav 77:65-77
20. Haynes WG, Morgan DA, Djalali A, Sivitz WI, Mark AL (1999) Interactions between the melanocortin system and leptin in control of sympathetic nerve traffic. Hypertension 33:542-547
21. Huszar D, Lynch CA, Fairchild-Huntress V, Dunmore JH, Fang Q, Berkemeier LR, Gu W, Kesterson RA, Boston BA, Cone RD, Smith FJ, Campfield LA, Burn P, Lee F (1997) Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88:131-141
22. Liu H, Kishi T, Roseberry AG, Cai X, Lee CE, Montez JM, Friedman JM, Elmquist JK (2003) Transgenic mice expressing green fluorescent protein under the control of the melanocortin-4 receptor promoter. J Neurosci 23:7143-7154
23. Marsh AJ, Fontes MA, Killinger S, Pawlak DB, Polson JW, Dampney RA (2003) Cardiovascular responses evoked by leptin acting on neurons in the ventromedial and dorsomedial hypothalamus. Hypertension 42: 488-493
24. Marsh DJ, Hollopeter G, Huszar D, Laufer R, Yagaloff KA, Fisher SL, Burn P, Palmiter RD (1999) Response of melanocortin-4 receptor-deficient mice to anorectic and orexigenic peptides. Nat Genet 21:119-122
25. Morgan DA, Thedens DR, Weiss R, Rahmouni K (2008) Mechanisms mediating renal sympathetic activation to leptin in obesity. Am J Physiol Regul Integr Comp Physiol 295:R1730-R1736.
26. Morrison SF, Nakamura K, Madden CJ (2008) Central control of thermogenesis in mammals. Exp Physiol 93:773-797
27. Mountjoy KG, Mortrud MT, Low MJ, Simerly RB, Cone RD (1994) Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol Endocrinol 8:1298-1308
28. Münzberg H, Flier JS, Bjørbaek C (2004) Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 145:4880-4889
29. Nedergaard J, Cannon B (2010) The changed metabolic world with human brown adipose tissue: therapeutic visions. Cell Metab 11:268-272
30. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
31. Pierroz DD, Ziotopoulou M, Ungsunan L, Moschos S, Flier JS, Mantzoros CS (2002) Effects of acute and chronic administration of the melanocortin agonist MTII in mice with diet-induced obesity. Diabetes 51:1337-1345
32. Rahmouni K, Morgan DA, Morgan GM, Mark AL, Haynes WG (2005) Role of selective leptin resistance in diet-induced obesity hypertension. Diabetes 54:2012-2018
33. Salomon G, Niv-Spector L, Gussakovsky EE, Gertler A (2006) Large-scale preparation of biologically active mouse and rat leptins and their L39A/D40A/F41A muteins which act as potent antagonists. Protein Expr Purif 47:128-136
34. Satoh N, Ogawa Y, Katsuura G, Numata Y, Masuzaki H, Yoshimasa Y, Nakao K (1998) Satiety effect and sympathetic activation of leptin are mediated by hypothalamic melanocortin system. Neurosci Lett 249:107-110
35. Scarpace PJ, Matheny M (1998) Leptin induction of UCP1 gene expression is dependent on sympathetic innervation. Am J Physiol 275:E259-E264.
36. Shi H, Akunuru S, Bierman JC, Hodge KM, Mitchell MC, Foster MT, Seeley RJ, Reizes O (2009) Diet-induced obese mice are leptin insufficient after weight reduction. Obesity (Silver Spring) 17:1702-1709
37. Song CK, Vaughan CH, Keen-Rhinehart E, Harris RB, Richard D, Bartness TJ (2008) Melanocortin-4 receptor mRNA expressed in sympathetic outflow neurons to brown adipose tissue: neuroanatomical and functional evidence. Am J Physiol Regul Integr Comp Physiol 295:R417-R428.
38. Ste Marie L, Miura GI, Marsh DJ, Yagaloff K, Palmiter RD (2000) A metabolic defect promotes obesity in mice lacking melanocortin-4 receptors. Proc Natl Acad Sci U S A 97:12339-12344
39. Voss-Andreae A, Murphy JG, Ellacott KL, Stuart RC, Nillni EA, Cone RD, Fan W (2007) Role of the central melanocortin circuitry in adaptive thermogenesis of brown adipose tissue. Endocrinology 148:1550-1560
40. Williams DL, Bowers RR, Bartness TJ, Kaplan JM, Grill HJ (2003) Brainstem melanocortin 3/4 receptor stimulation increases uncoupling protein gene expression in brown fat. Endocrinology 144:4692-4697
41. Xiao XQ, Williams SM, Grayson BE, Glavas MM, Cowley MA, Smith MS, Grove KL (2007) Excess weight gain during the early postnatal period is associated with permanent reprogramming of brown adipose tissue adaptive thermogenesis. Endocrinology 148:4150-4159
42. Zaretskaia MV, Zaretsky DV, Sarkar S, Shekhar A, DiMicco JA (2008) Induction of Fos-immunoreactivity in the rat brain following disinhibition of the dorsomedial hypothalamus. Brain Res 1200:39-50
43. Zhang J, Matheny MK, Tümer N, Mitchell MK, Scarpace PJ (2007) Leptin antagonist reveals that the normalization of caloric intake and the thermic effect of food after high-fat feeding are leptin dependent. Am J Physiol Regul Integr Comp Physiol 292:R868-R874.
44. Zhang Y, Scarpace PJ (2006) The role of leptin in leptin resistance and obesity. Physiol Behav 88:249-256
45. Zhang Y, Kilroy GE, Henagan TM, Prpic-Uhing V, Richards WG, Bannon AW, Mynatt RL, Gettys TW (2005) Targeted deletion of melanocortin receptor subtypes 3 and 4, but not CART, alters nutrient partitioning and compromises behavioral and metabolic responses to leptin. FASEB J 19:1482-1491
46. 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.