Melanocortin-4 receptor mRNA expressed in sympathetic outflow neurons to brown adipose tissue: Neuroanatomical and functional evidence

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 2, 2008, Pages

  Song, C Kay ^a   Vaughan, Cheryl H ^a   Keen Rhinehart, Erin ^a   Harris, Ruth B S ^b   Richard, Denis ^c   Bartness, Timothy J ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

In situ hybridization; Melanocortins; Pseudorabies virus; Siberian hamsters; Tract tracing

Indexed keywords

MELANOCORTIN; MELANOCORTIN 4 RECEPTOR; MESSENGER RNA; ALPHA INTERMEDIN; CYCLOPEPTIDE; DRUG DERIVATIVE; MELANOTAN II; MELANOTAN-II;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN THIRD VENTRICLE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; IN SITU HYBRIDIZATION; MALE; NEUROANATOMY; NONHUMAN; PHODOPUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDORABIES HERPETOVIRUS; SYMPATHETIC NERVE CELL; THALAMUS MIDLINE NUCLEUS; THERMOGENESIS; ADRENERGIC SYSTEM; ANIMAL; ANTERIOR HYPOTHALAMUS; DRUG EFFECT; DRUG POTENTIATION; EFFERENT NERVE; GENETICS; HAMSTER; INNERVATION; METABOLISM; METHODOLOGY; MICROINJECTION; STAINING; TIME;

ADIPOSE TISSUE, BROWN; ALPHA-MSH; ANIMALS; CRICETINAE; HERPESVIRUS 1, SUID; IN SITU HYBRIDIZATION; MALE; MICROINJECTIONS; NEURONS, EFFERENT; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PEPTIDES, CYCLIC; PHODOPUS; RECEPTOR, MELANOCORTIN, TYPE 4; RNA, MESSENGER; STAINING AND LABELING; SYMPATHETIC NERVOUS SYSTEM; THERMOGENESIS; TIME FACTORS;

EID: 51149096739     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00174.2008     Document Type: Article

References (60)

1. Amir S. Stimulation of the paraventricular nucleus with glutamate activates interscapular brown adipose tissue thermogenesis in rats. Brain Res 508: 152-155, 1990.
2. 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. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123: 493-505, 2005.
3. Bamshad M, Aoki VT, Adkison MG, Warren WS, Bartness TJ. Central nervous system origins of the sympathetic nervous system outflow to white adipose tissue. Am J Physiol Regul Integr Comp Physiol 275: R291-R299, 1998.
4. Bamshad M, Song CK, Bartness TJ. CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 276: R1569-R1578, 1999.
5. Bartness TJ, Song CK. Brain-adipose tissue neural crosstalk. Physiol Behav 91: :343-351, 2007.
6. Bartness TJ, Song CK. Sympathetic and sensory innervation of white adipose tissue. J Lipid Res 48: 1655-1672, 2007.
7. Bartness TJ, Song CK, Demas GE. Central nervous system innervation of brown adipose tissue. In: Adipose Tissue, edited by Klaus S. Georgetown, TX: Landes Bioscience, 2001, p. 162-200.
8. Berthoud HR, Patterson LM, Sutton GM, Morrison C, Zheng H. Orexin inputs to caudal raphé neurons involved in thermal, cardiovascular, and gastrointestinal regulation. Histochem Cell Biol 123: 147-156, 2005.
9. Billington CJ, Briggs JE, Harker S, Grace M, Levine AS. Neuropeptide Y in hypothalamic paraventricular nucleus: a center coordinating energy metabolism. Am J Physiol Regul Integr Comp Physiol 266: R1765-R1770, 1994.
10. Bowers RR, Festuccia WTL, Song CK, Shi H, Migliorini RH, Bartness TJ. Sympathetic innervation of white adipose tissue and its regulation of fat cell number. Am J Physiol Regul Integr Comp Physiol 286: R1167-R1175, 2004.
11. Brito MN, Brito NA, Baro DJ, Song CK, Bartness TJ. Differential activation of the sympathetic innervation of adipose tissues by melanocortin receptor stimulation. Endocrinology 148: 5339-53347, 2007.
12. Brito NA, Brito MN, Bartness TJ. Differential sympathetic drive to adipose tissues after food deprivation, cold exposure or glucoprivation. Am J Physiol Regul Integr Comp Physiol 294: R1445-R1452, 2008.
13. Cano G, Passerin AM, Schiltz JC, Card JP, Morrison SF, Sved AF. Anatomical substrates for the central control of sympathetic outflow to interscapular adipose tissue during cold exposure. J Comp Neurol 460: 303-326, 2003.
14. Card JP. Practical considerations for the use of pseudorabies virus in transneuronal studies of neural circuitry. Neurosci Biobehav Rev 22: 685-694, 1998.
15. Cinti S. The role of brown adipose tissue in human obesity. Nutr Metab Cardiovasc Dis 16: 569-574, 2006.
16. Collins S, Migliorini RH, Bartness TJ. Mechanisms controlling adipose tissue metabolism by the sympathetic nervous system: anatomical and molecular aspects. In: Handbook of Contemporary Neuropharmacology, edited by Sibley D, Hanin I, Kuhar M, and Skolnick P. New York: Wiley, 2007, p. 785-814.
17. De LB, Monda M, Amaro S, Pellicano MP, Cioffi LA. Lack of diet-induced thermogenesis following lesions of paraventricular nucleus in rats. Physiol Behav 46: 685-691, 1989.
18. Demas GE, Bowers RR, Bartness TJ, Gettys TW. Photoperiodic regulation of gene expression in brown and white adipose tissue of Siberian hamsters (Phodopus sungorus). Am J Physiol Regul Integr Comp Physiol 282: R114-R121, 2002.
19. Ellacott KL, Cone RD. The central melanocortin system and the integration of short- and long-term regulators of energy homeostasis. Recent Prog Horm Res 59: 395-408, 2004.
20. Freeman PH, Wellman PJ. Brown adipose tissue thermogenesis induced by low level electrical stimulation of hypothalamus in rats. Brain Res Bull 18: 7-11, 1987.
21. Giordano A, Frontini A, Castellucci M, Cinti S. Presence and distribution of cholinergic nerves in rat mediastinal brown adipose tissue. J Histochem Cytochem 52: 923-930, 2004.
22. Giordano A, Song CK, Bowers RR, Ehlen JC, Frontini A, Cinti S, Bartness TJ. White adipose tissue lacks significant vagal innervation and immunohistochemical evidence of parasympathetic innervation. Am J Physiol Regul Integr Comp Physiol 291: R1243-R1255, 2006.
23. Giordano A, Song CK, Bowers RR, Ehlen JC, Frontini A, Cinti S, Bartness TJ. No sympathy for the claim of parasympathetic innervation of white adipose tissue. Am J Physiol Regul Integr Comp Physiol 293: R550-R552, 2007.
24. Grill HJ, Ginsberg AB, Seeley RJ, Kaplan JM. Brainstem application of melanocortin receptor ligands produces long-lasting effects on feeding and body weight. J Neurosci 18: 10128-10135, 1998.
25. Grill HJ, Kaplan JM. The neuroanatomical axis for control of energy balance. Front Neuroendocrinol 23: 2-40, 2002.
26. Himms-Hagen J, Melnyk A, Zingaretti MC, Ceresi E, Barbatelli G, Cinti S. Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol 279: C670-C681, 2000.
27. Hollopeter G, Erickson JC, Seeley RJ, Marsh DJ, Palmiter RD. Response of neuropeptide Y-deficient mice to feeding effectors. Regul Pept 75-76: 383-389, 1998.
28. Holt SJ, Wheal HV, York DA. Response of brown adipose tissue to electrical stimulation of hypothalamus centres in intact and adrenalectomized Zucker rats. Neurosci Lett 84: 63-67, 1988.
29. 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. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88: 131-141, 1997.
30. Kim S, Krynyckyi BR, Machac J, Kim CK. Concomitant paravertebral FDG uptake helps differentiate supraclavicular and suprarenal brown fat uptake from malignant uptake when CT coregistration is not available. Clin Nucl Med 31: 127-130, 2006.
31. Kishi T, Aschkenasi CJ, Lee CE, Mountjoy KG, Saper CB, Elmquist JK. Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J Comp Neurol 457: 213-235, 2003.
32. Lean ME, James WP, Jennings G, Trayhurn P. Brown adipose tissue in patients with phaeochromocytoma. Int J Obes 10: 219-227, 1986.
33. Lean MEJ, James WPT. Brown adipose tissue in man. In: Brown Adipose Tissue, edited by Trayhurn P and Nicholls DG. London: Edward Arnold, 1986, p. 339-365.
34. Liu H, Kishi T, Roseberry AG, Cai X, Lee CE, Montez JM, Friedman JM, Elmquist JK. Transgenic mice expressing green fluorescent protein under the control of the melanocortin-4 receptor promoter. J Neurosci 23: 7143-7154, 2003.
35. Mack SO, Wu M, Kc P, Haxhiu MA. Stimulation of the hypothalamic paraventricular nucleus modulates cardiorespiratory responses via oxytocinergic innervation of neurons in pre-Botzinger complex. J Appl Physiol 102: 189-199, 2007.
36. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293: E444-E452, 2007.
37. Nogueiras R, Wiedmer P, Perez-Tilve D, Veyrat-Durebex C, Keogh JM, Sutton GM, Pfluger PT, Castaneda TR, Neschen S, Hofmann SM, Howles PN, Morgan DA, Benoit SC, Szanto I, Schrott B, Schurmann A, Joost HG, Hammond C, Hui DY, Woods SC, Rahmouni K, Butler AA, Farooqi IS, O'Rahilly S, Rohner-Jeanrenaud F, Tschop MH. The central melanocortin system directly controls peripheral lipid metabolism. J Clin Invest 117: 3475-3488, 2007.
38. Oldfield BJ, Allen AM, Davern P, Giles ME, Owens NC. Lateral hypothalamic 'command neurons' with axonal projections to regions involved in both feeding and thermogenesis. Eur J Neurosci 25: 2404-2412, 2007.
39. Oldfield BJ, Giles ME, Watson A, Anderson C, Colvill LM, McKinley MJ. The neurochemical characterisation of hypothalamic pathways projecting polysynaptically to brown adipose tissue in the rat. Neuroscience 110: 515-526, 2002.
40. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. New York: Academic, 2007.
41. Peever JH, Necakov A, Duffin J. Nucleus raphé obscurus modulates hypoglossal output of neonatal rat in vitro transverse brain stem slices. J Appl Physiol 90: 269-279, 2001.
42. Pritchard LE, Turnbull AV, White A. Pro-opiomelanocortin processing in the hypothalamus: impact on melanocortin signalling and obesity. J Endocrinol 172: 411-421, 2002.
43. Raposinho PD, White RB, Aubert ML. The melanocortin agonist melanotan-II reduces the orexigenic and adipogenic effects of neuropeptide Y (NPY) but does not affect the NPY-driven suppressive effects on the gonadotropic and somatotropic axes in the male rat. J Neuroendocrinol 15: 173-181, 2003.
44. Rathner JA, Owens NC, McAllen RM. Cold-activated raphé-spinal neurons in rats. J Physiol 535: 841-854, 2001.
45. Richard D. Energy expenditure: a critical determinant of energy balance with key hypothalamic controls. Minerva Endocrinol 32: 173-183, 2007.
46. Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature 281: 31-35, 1979.
47. Saito M, Minokoshi Y, Shimazu T. Accelerated norepinephrine turnover in peripheral tissues after ventromedial hypothalamic stimulation in rats. Brain Res 481: 298-303, 1989.
48. Shi H, Bartness TJ. Neurochemical phenotype of sympathetic nervous system outflow from brain to white fat. Brain Res Bull 54: 375-385, 2001.
49. Shi H, Bowers RR, Bartness TJ. Norepinephrine turnover in brown and white adipose tissue after partial lipectomy. Physiol Behav 81: 535-543, 2004.
50. Skibicka KP, Grill HJ. Energetic responses are triggered by caudal brainstem melanocortin receptor stimulation and mediated by local sympathetic effector circuits. Endocrinology. In Press.
51. Song CK, Bartness TJ. CNS sympathetic outflow neurons to white fat that express melatonin receptors may mediate seasonal adiposity. Am J Physiol Regul Integr Comp Physiol 281: R666-R672, 2001.
52. Song CK, Enquist LW, Bartness TJ. New developments in viral tracings of neural circuits. Virus Res 11: 235-249, 2005.
53. Song CK, Jackson RX, Harris RBS, Richard D, Bartness TJ. Melanocortin-4 receptor mRNA is expressed in sympathetic nervous system outflow neurons to white adipose tissue. Am J Physiol Regul Integr Comp Physiol 289: R1467-R1476, 2005.
54. Sun QJ, Minson J, Llewellyn-Smith IJ, Arnolda L, Chalmers J, Pilowsky P. Botzinger neurons project towards bulbospinal neurons in the rostral ventrolateral medulla of the rat. J Comp Neurol 388: 23-31, 1997.
55. Vaisse C, Clement K, Guy-Grand B, Froguel P. A frameshift mutation in human MC4R is associated with a dominant form of obesity. Nat Genet 20: 113-114, 1998.
56. Voss-Andreae A, Murphy JG, Ellacott KL, Stuart RC, Nillni EA, Cone RD, Fan W. Role of the central melanocortin circuitry in adaptive thermogenesis of brown adipose tissue. Endocrinology 148: 1550-1560, 2007.
57. Williams DL, Bowers RR, Bartness TJ, Kaplan JM, Grill HJ. Brainstem melanocortin 3/4 receptor stimulation increases uncoupling protein gene expression in brown fat. Endocrinology 144: 4692-4697, 2003.
58. Yasuda T, Masaki T, Kakuma T, Yoshimatsu H. Hypothalamic melanocortin system regulates sympathetic nerve activity in brown adipose tissue. Exp Biol Med (Maywood) 229: 235-239, 2004.
59. Yeo GS, Lank EJ, Farooqi IS, Keogh J, Challis BG, O'Rahilly S. Mutations in the human melanocortin-4 receptor gene associated with severe familial obesity disrupts receptor function through multiple molecular mechanisms. Hum Mol Genet 12: 561-574, 2003.
60. Yoshimatsu H, Egawa M, Bray GA. Sympathetic nerve activity after discrete hypothalamic injections of L-glutamate. Brain Res 601: 121-128, 1993.