The melanocortin-3 receptor is required for entrainment to meal intake

Journal of Neuroscience

Volumn 28, Issue 48, 2008, Pages 12946-12955

  Sutton, Gregory M ^a   Perez Tilve, Diego ^b   Nogueiras, Ruben ^b,c   Fang, Jidong ^d   Kim, Jason K ^d   Cone, Roger D ^e   Gimble, Jeffrey M ^a   Tschöp, Matthias H ^b,c   Butler, Andrew A ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d PENN STATE COLLEGE OF MEDICINE   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Arousal; Circadian rhythms; Entrainment; Food; Neuropeptide; POMC; Proopiomelanocortin; Rhythm; Sleep; Waking

Indexed keywords

MELANOCORTIN 3 RECEPTOR; NEURONAL PAS DOMAIN 2; PER2 PROTEIN; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENERGY EXPENDITURE; ENERGY METABOLISM; FEEDING BEHAVIOR; FOOD INTAKE; GENE EXPRESSION; HYPOTHALAMUS; LOCOMOTION; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN FUNCTION; WAKEFULNESS;

ANIMALS; APPETITE; APPETITE REGULATION; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN; CELL CYCLE PROTEINS; CEREBRAL CORTEX; CIRCADIAN RHYTHM; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; HYPOTHALAMUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PRO-OPIOMELANOCORTIN; RECEPTOR, MELANOCORTIN, TYPE 3; TRANSCRIPTION FACTORS; WAKEFULNESS;

EID: 58149379032     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3615-08.2008     Document Type: Article

References (44)

1. Bagnol D, Lu XY, Kaelin CB, Day HE, Ollmann M, Gantz I, Akil H, Barsh GS, Watson SJ (1999) Anatomy of an endogenous antagonist: relationship between Agouti- related protein and proopiomelanocortin in brain. J Neurosci 19:RC26.
2. Butler AA (2006) The melanocortin system and energy balance. Peptides 27:281-290.
3. Butler AA, Kesterson RA, Khong K, Cullen MJ, Pelleymounter MA, Dekoning J, Baetscher M, Cone RD (2000) A unique metabolic syndrome causes obesity in the melanocortin-3 receptor-deficient mouse. Endocrinology 141:3518-3521.
4. Butler AA, Marks DL, Fan W, Kuhn CM, Bartolome M, Cone RD (2001) Melanocortin-4 receptor is required for acute homeostatic responses to increased dietary fat. Nat Neurosci 4:605-611.
5. Chen AS, Marsh DJ, Trumbauer ME, Frazier EG, Guan XM, Yu H, Rosenblum CI, Vongs A, Feng Y, Cao L, Metzger JM, Strack AM, Camacho RE, Mellin TN, Nunes CN, Min W, Fisher J, Gopal-Truter S, MacIntyre DE, Chen HY, et al. (2000) Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass. Nat Genet 26:97-102.
6. Choi S, Wong LS, Yamat C, Dallman MF (1998) Hypothalamic ventromedial nuclei amplify circadian rhythms: do they contain a food-entrained endogenous oscillator? J Neurosci 18:3843-3852.
7. Chou TC, Scammell TE, Gooley JJ, Gaus SE, Saper CB, Lu J (2003) Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci 23:10691-10702.
8. Cone RD (2005) Anatomy and regulation of the central melanocortin system. Nat Neurosci 8:571-578.
9. Cone RD (2006) Studies on the physiological functions of the melanocortin system. Endocr Rev 27:736-749.
10. Dudley CA, Erbel-Sieler C, Estill SJ, Reick M, Franken P, Pitts S, McKnight SL (2003) Altered patterns of sleep and behavioral adaptability in NPAS2-deficient mice. Science 301:379-383.
11. Duez H, Staels B (2007) Rev-erbalpha gives a time cue to metabolism. FEBS Lett.
12. Elia M, Livesey G (1988) Theory and validity of indirect calorimetry during net lipid synthesis. Am J Clin Nutr 47:591-607.
13. Ellacott KL, Murphy JG, Marks DL, Cone RD (2007) Obesity-induced inflammation in white adipose tissue is attenuated by loss of melanocortin-3 receptor signaling. Endocrinology 148:6186-6194.
14. Feillet CA, Ripperger JA, Magnone MC, Dulloo A, Albrecht U, Challet E (2006) Lack of food anticipation in Per2 mutant mice. Curr Biol 16:2016-2022.
15. Fekete C, Marks DL, Sarkar S, Emerson CH, Rand WM, Cone RD, Lechan RM (2004) Effect of Agouti-related protein in regulation of the hypothalamic-pituitary-thyroid axis in the melanocortin 4 receptor knockout mouse. Endocrinology 145:4816-4821.
16. Fuller PM, Lu J, Saper CB (2008) Differential rescue of light- and food-entrainable circadian rhythms. Science 320:1074-1077.
17. Gooley JJ, Schomer A, Saper CB (2006) The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci 9:398-407.
18. Haskell-Luevano C, Chen P, Li C, Chang K, Smith MS, Cameron JL, Cone RD (1999) Characterization of the neuroanatomical distribution of agouti-related protein immunoreactivity in the rhesus monkey and the rat. Endocrinology 140:1408-1415.
19. Hill JO (2006) Understanding and addressing the epidemic of obesity: an energy balance perspective. Endocr Rev 27:750-761.
20. Johnstone LE, Fong TM, Leng G (2006) Neuronal activation in the hypothalamus and brainstem during feeding in rats. Cell Metab 4:313-321.
21. King BM (2006) The rise, fall, and resurrection of the ventromedial hypothalamus in the regulation of feeding behavior and body weight. Physiol Behav 87:221-244.
22. Kohsaka A, Bass J (2007) A sense of time: how molecular clocks organize metabolism. Trends Endocrinol Metab 18:4-11.
23. Kornmann B, Schaad O, Bujard H, Takahashi JS, Schibler U (2007) System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 5:e34.
24. Landry GJ, Simon MM, Webb IC, Mistlberger RE (2006) Persistence of a behavioral food-anticipatory circadian rhythm following dorsomedial hypothalamic ablation in rats. Am J Physiol Regul Integr Comp Physiol 290:R1527-1534.
25. Landry GJ, Yamakawa GR, Webb IC, Mear RJ, Mistlberger RE (2007) The dorsomedial hypothalamic nucleus is not necessary for the expression of circadian food-anticipatory activity in rats. J Biol Rhythms 22:467-478.
26. Laposky A, Easton A, Dugovic C, Walisser J, Bradfield C, Turek F (2005) Deletion of the mammalian circadian clock gene BMAL1/Mop3 alters baseline sleep architecture and the response to sleep deprivation. Sleep 28:395-409.
27. Liu C, Li S, Liu T, Borjigin J, Lin JD (2007) Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 447:477-481.
28. 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.
29. Mieda M, Williams SC, Richardson JA, Tanaka K, Yanagisawa M (2006) The dorsomedial hypothalamic nucleus as a putative food-entrainable circadian pacemaker. Proc Natl Acad Sci U S A 103:12150-12155.
30. Mistlberger RE (1994) Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci Biobehav Rev 18:171-195.
31. Rahmouni K, Haynes WG, Morgan DA, Mark AL (2003) Role of melanocortin-4 receptors in mediating renal sympathoactivation to leptin and insulin. J Neurosci 23:5998-6004.
32. Reick M, Garcia JA, Dudley C, McKnight SL (2001) NPAS2: an analog of clock operative in the mammalian forebrain. Science 293:506-509.
33. Roselli-Rehfuss L, Mountjoy KG, Robbins LS, Mortrud MT, Low MJ, Tatro JB, Entwistle ML, Simerly RB, Cone RD (1993) Identification of a receptor for gamma melanotropin and other proopiomelanocortin peptides in the hypothalamus and limbic system. Proc Natl Acad Sci U S A 90:8856-8860.
34. Rossi M, Kim MS, Morgan DG, Small CJ, Edwards CM, Sunter D, Abusnana S, Goldstone AP, Russell SH, Stanley SA, Smith DM, Yagaloff K, Ghatei MA, Bloom SR (1998) A C-terminal fragment of Agouti-related protein increases feeding and antagonizes the effect of alpha-melanocyte stimulating hormone in vivo. Endocrinology 139:4428-4431.
35. Rutter J, Reick M, McKnight SL (2002) Metabolism and the control of circadian rhythms. Annu Rev Biochem 71:307-331.
36. Saper CB, Lu J, Chou TC, Gooley J (2005) The hypothalamic integrator for circadian rhythms. Trends Neurosci 28:152-157.
37. Singru PS, Sánchez E, Fekete C, Lechan RM (2007) Importance of melanocortin signaling in refeeding-induced neuronal activation and satiety. Endocrinology 148:638-646.
38. Staels B (2006) When the Clock stops ticking, metabolic syndrome explodes. Nat Med 12:54-55; discussion 55.
39. Stephan FK (2002) The "other" circadian system: food as a Zeitgeber. J Biol Rhythms 17:284-292.
40. Sutton GM, Trevaskis JL, Hulver MW, McMillan RP, Markward NJ, Babin MJ, Meyer EA, Butler AA (2006) Diet-genotype interactions in the development of the obese, insulin-resistant phenotype of C57BL/6J mice lacking melanocortin-3 or -4 receptors. Endocrinology 147:2183-2196.
41. Tolle V, Low MJ (2008) In vivo evidence for inverse agonism of Agouti-related peptide in the central nervous system of proopiomelanocortin- deficient mice. Diabetes 57:86-94.
42. Trevaskis JL, Butler AA (2005) Double leptin (Lepob) and melanocortin-4 receptor (Mc4r) gene mutations have an additive effect on fat mass, and are associated with reduced effects of leptin on weight loss and food intake. Endocrinology 146:4257-4265.
43. van den Top M, Lee K, Whyment AD, Blanks AM, Spanswick D (2004) Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7:493-494.
44. 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.