The hypothalamic neuropeptide melanin-concentrating hormone acts in the nucleus accumbens to modulate feeding behavior and forced-swim performance

Journal of Neuroscience

Volumn 25, Issue 11, 2005, Pages 2933-2940

  Georgescu, Dan ^a   Sears, Robert M ^a,b   Hommel, Jonathan D ^a   Barrot, Michel ^a   Bolaños, Carlos A ^c   Marsh, Donald J ^d   Bednarek, Maria A ^d   Bibb, James A ^a   Maratos Flier, Eleftheria ^e   Nestler, Eric J ^a   DiLeone, Ralph J ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Accumbens; Appetite; Depression; Feeding; Lateral hypothalamus; MCH; Neuropeptide; Obesity

Indexed keywords

AMPA RECEPTOR; BINDING PROTEIN; CYCLIC AMP; DOPAMINE; DYNORPHIN; ENKEPHALIN; GLUTAMATE RECEPTOR 1; GLUTAMIC ACID; MELANIN CONCENTRATING HORMONE; NEUROPEPTIDE;

ANIMAL TISSUE; APPETITE; ARTICLE; CHEMICAL ANALYSIS; DEPRESSION; FEEDING BEHAVIOR; FLUORESCENCE IN SITU HYBRIDIZATION; FOOD DEPRIVATION; FORCED SWIMMING TEST; HYPOTHALAMUS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIMBIC CORTEX; MOUSE; NERVE CELL; NONHUMAN; NUCLEUS ACCUMBENS; PHOSPHORYLATION; PRIORITY JOURNAL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BENZAZEPINES; BLOTTING, WESTERN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOPAMINE AGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; DYNORPHINS; EATING; ENKEPHALINS; FEEDING BEHAVIOR; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; HYPOTHALAMIC HORMONES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MELANINS; MICE; MICE, TRANSGENIC; NEURONS; NEUROPEPTIDES; NUCLEUS ACCUMBENS; PITUITARY HORMONES; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, AMPA; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; RECEPTORS, PITUITARY HORMONE; SERINE; SWIMMING; TIME FACTORS;

EID: 20144362544     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1714-04.2005     Document Type: Article

References (66)

1. Abbott CR, Kennedy AR, Wren AM, Rossi M, Murphy KG, Seal LJ, Todd JF, Ghatei MA, Small CJ, Bloom SR (2003) Identification of hypothalamic nuclei involved in the orexigenic effect of melanin-concentrating hormone. Endocrinology 144:3943-3949.
2. Ahima RS, Osei SY (2001) Molecular regulation of eating behavior: new insights and prospects for therapeutic strategies. Trends Mol Med 7:205-213.
3. Anand BK, Brobeck JR (1951) Localization of a "feeding center" in the hypothalamus of the rat. Proc Soc Exp Biol Med 77:323-324.
4. Angulo JA, McEwen BS (1994) Molecular aspects of neuropeptide regulation and function in the corpus striatum and nucleus accumbens. Brain Res Brain Res Rev 19:1-28.
5. Baldo BA, Sadeghian K, Basso AM, Kelley AE (2002) Effects of selective dopamine D1 or D2 receptor blockade within nucleus accumbens sub regions on ingestive behavior and associated motor activity. Behav Brain Res 137:165-177.
6. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, Traynelis SF (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20:89-102.
7. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, Zachariou V, Nestler EJ (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA 99:11435-11440.
8. Bednarek MA, Hreniuk DL, Tan C, Palyha OC, MacNeil DJ, Van der Ploeg LH, Howard AD, Feighner SD (2002) Synthesis and biological evaluation in vitro of selective, high affinity peptide antagonists of human melanin-concentrating hormone action at human melanin-concentrating hormone receptor 1. Biochemistry 41:6383-6390.
9. Borowsky B, Durkin MM, Ogozalek K, Marzabadi MR, DeLeon J, Lagu B, Heurich R, Lichtblau H, Shaposhnik Z, Daniewska I, Blackburn TP, Branchek TA, Gerald C, Vaysse PJ, Forray C (2002) Antidepressant, anxiolytic and anorectic effects of a melanin-concentrating hormone-1 receptor antagonist. Nat Med 8:825-830.
10. Broberger C, De Lecea L, Sutcliffe JG, Hokfelt T (1998) Hypocretin/orexin-and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J Comp Neurol 402:460-474.
11. Bruce HM, Kennedy GC (1951) The central nervous control of food and water intake. Proc R Soc Lond B Biol Sci 138:528-544.
12. Cannon CM, Palmiter RD (2003) Reward without dopamine. J Neurosci 23:10827-10831.
13. Carlezon WA, Pliakas AM, Parow AM, Detke MJ, Cohen BM, Renshaw PF (2002) Antidepressant-like effects of cytidine in the forced swim test in rats. Biol Psychiatry 51:882-889.
14. Carr KD (2002) Augmentation of drug reward by chronic food restriction: behavioral evidence and underlying mechanisms. Physiol Behav 76:353-364.
15. Carr KD, Kim GY, Cabeza de Vaca S (2000) Chronic food restriction in rats augments the central rewarding effect of cocaine and the delta1 opioid agonist, DPDPE, but not the delta2 agonist, deltorphin-II. Psychopharmacology (Berl) 152:200-207.
16. Chambers J, Ames RS, Bergsma D, Muir A, Fitzgerald LR, Hervieu G, Dytko GM, Foley JJ, Martin J, Liu WS, Park J, Ellis C, Ganguly S, Konchar S, Cluderay J, Leslie R, Wilson S, Sarau HM (1999) Melanin-concentrating hormone is the cognate ligand for the orphan G-protein-coupled receptor SLC-1. Nature 400:261-265.
17. Chen Y, Hu C, Hsu CK, Zhang Q, Bi C, Asnicar M, Hsiung HM, Fox N, Slieker LJ, Yang DD, Heiman ML, Shi Y (2002) Targeted disruption of the melanin-concentrating hormone receptor-1 results in hyperphagia and resistance to diet-induced obesity. Endocrinology 143:2469-2477.
18. Corbit LH, Muir JL, Balleine BW (2001) The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell. J Neurosci 21:3251-3260.
19. Cowley MA, Smart JL, Rubinstein M, Cerdan 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.
20. Curran EJ, Watson Jr SJ (1995) Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 361:57-76.
21. Detke MJ, Rickels M, Lucki I (1995) Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl) 121:66-72.
22. DiLeone RJ, Georgescu D, Nestler EJ (2003) Lateral hypothalamic neuropeptides in reward and drug addiction. Life Sci 73:759-768.
23. Elmquist JK (2001) Hypothalamic pathways underlying the endocrine, autonomic, and behavioral effects of leptin. Physiol Behav 74:703-708.
24. Flier JS (2004) Obesity wars: molecular progress confronts an expanding epidemic. Cell 116:337-350.
25. Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763-770.
26. Fulton S, Woodside B, Shizgal P (2000) Modulation of brain reward circuitry by leptin. Science 287:125-128.
27. Georgescu D, Zachariou V, Barrot M, Mieda M, Willie JT, Eisch AJ, Yanagisawa M, Nestler EJ, DiLeone RJ (2003) Involvement of the lateral hypothalamic peptide orexin in morphine dependence and withdrawal. J Neurosci 23:3106-3111.
28. Greengard P (2001) The neurobiology of slow synaptic transmission. Science 294:1024-1030.
29. Hawes BE, Kil E, Green B, O'Neill K, Fried S, Graziano MP (2000) The melanin-concentrating hormone receptor couples to multiple G proteins to activate diverse intracellular signaling pathways. Endocrinology 141:4524-4532.
30. Hyman SE, Malenka RC (2001) Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2:695-703.
31. Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR (1998) Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595-601.
32. Kelley AE, Berridge KC (2002) The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22:3306-3311.
33. Knapp RJ, Goldenberg R, Shuck C, Cecil A, Watkins J, Miller C, Crites G, Malatynska E (2002) Antidepressant activity of memory-enhancing drugs in the reduction of submissive behavior model. Eur J Pharmacol 440:27-35.
34. Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24:97-129.
35. Lembo PM, Grazzini E, Cao J, Hubatsch DA, Pelletier M, Hoffert C, St-Onge S, Pou C, Labrecque J, Groblewski T, O'Donnell D, Payza K, Ahmad S, Walker P (1999) The receptor for the orexigenic peptide melanin-concentrating hormone is a G-protein-coupled receptor. Nat Cell Biol 1:267-271.
36. Li X, Tizzano JP, Griffey K, Clay M, Lindstrom T, Skolnick P (2001) Antidepressant-like actions of an AMPA receptor potentiator (LY392098). Neuropharmacology 40:1028-1033.
37. Ludwig DS, Tritos NA, Mastaitis JW, Kulkarni R, Kokkotou E, Elmquist J, Lowell B, Flier JS, Maratos-Flier E (2001) Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 107:379-386.
38. Maldonado-Irizarry CS, Swanson CJ, Kelley AE (1995) Glutamate receptors in the nucleus accumbens shell control feeding behavior via the lateral hypothalamus. J Neurosci 15:6779-6788.
39. Marsh DJ, Weingarth DT, Novi DE, Chen HY, Trumbauer ME, Chen AS, Guan XM, Jiang MM, Feng Y, Camacho RE, Shen Z, Frazier EG, Yu H, Metzger JM, Kuca SJ, Shearman LP, Gopal-Truter S, MacNeil DJ, Strack AM, MacIntyre DE, et al. (2002) Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc Natl Acad Sci USA 99:3240-3245.
40. Nestler EJ (2001) Molecular neurobiology of addiction. Am J Addict 10:201-217.
41. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002) Neurobiology of depression. Neuron 34:13-25.
42. Nowend KL, Arizzi M, Carlson BB, Salamone JD (2001) D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption. Pharmacol Biochem Behav 69:373-382.
43. Ortiz J, Fitzgerald LW, Lane S, Terwilliger R, Nestler EJ (1996) Biochemical adaptations in the mesolimbic dopamine system in response to repeated stress. Neuropsychopharmacology 14:443-452.
44. Paxinos G, Watson GC (2004) The rat brain in stereotaxic coordinates, Ed 5. New York: Academic. Pissios P, Trombly DJ, Tzameli I, Maratos-Flier E (2003) Melanin-concentrating hormone receptor 1 activates extracellular signal-regulated kinase and synergizes with G(s)-coupled pathways. Endocrinology 144:3514-3523.
45. Porsolt RD, Le Pichon M, Jalfre M (1977a) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730-732.
46. Porsolt RD, Bertin A, Jalfre M (1977b) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327-336.
47. Qu D, Ludwig DS, Gammeltoft S, Piper M, Pelleymounter MA, Cullen MJ, Mathes WF, Przypek R, Kanarek R, Maratos-Flier E (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380:243-247.
48. Roche KW, O'Brien RJ, Mammen AL, Bernhardt J, Huganir RL (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16:1179-1188.
49. Saito Y, Nothacker HP, Wang Z, Lin SH, Leslie F, Civelli O (1999) Molecular characterization of the melanin-concentrating-hormone receptor. Nature 400:265-269.
50. Salamone JD, Correa M, Mingote S, Weber SM (2003) Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 305:1-8.
51. Saper CB, Chou TC, Elmquist JK (2002) The need to feed: homeostatic and hedonic control of eating. Neuron 36:199-211.
52. Schwartz MW, Woods SC, Porte Jr D, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661-671.
53. Segal-Lieberman G, Bradley RL, Kokkotou E, Carlson M, Trombly DJ, Wang X, Bates S, Myers Jr MG, Flier JS, Maratos-Flier E (2003) Melanin-concentrating hormone is a critical mediator of the leptin-deficient phenotype. Proc Natl Acad Sci USA 100:10085-10090.
54. Shaw-Lutchman TZ, Barrot M, Wallace T, Gilden L, Zachariou V, Impey S, Duman RS, Storm D, Nestler EJ (2002) Regional and cellular mapping of cAMP response element-mediated transcription during naltrexone-precipitated morphine withdrawal. J Neurosci 22:3663-3672.
55. Shimada M, Tritos NA, Lowell BB, Flier JS, Maratos-Flier E (1998) Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature 396:670-674.
56. Snyder GL, Allen PB, Fienberg AA, Valle CG, Huganir RL, Nairn AC, Greengard P (2000) Regulation of phosphorylation of the GluR1 AMPA receptor in the neostriatum by dopamine and psychostimulants in vivo. J Neurosci 20:4480-4488.
57. Stratford TR, Kelley AE (1997) GABA in the nucleus accumbens shell participates in the central regulation of feeding behavior. J Neurosci 17:4434-4440.
58. Stratford TR, Kelley AE (1999) Evidence of a functional relationship between the nucleus accumbens shell and lateral hypothalamus subserving the control of feeding behavior. J Neurosci 19:11040-11048.
59. Svenningsson P, Tzavara ET, Witkin JM, Fienberg AA, Nomikos GG, Greengard P (2002) Involvement of striatal and extrastriatal DARPP-32 in biochemical and behavioral effects of fluoxetine (Prozac). Proc Natl Acad Sci USA 99:3182-3187.
60. Szczypka MS, Kwok K, Brot MD, Marck BT, Matsumoto AM, Donahue BA, Palmiter RD (2001) Dopamme production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron 30:819-828.
61. Takekawa S, Asami A, Ishihara Y, Terauchi J, Kato K, Shimomura Y, Mori M, Murakoshi H, Suzuki N, Nishimura O, Fujino M (2002) T-226296: a novel, orally active and selective melanin-concentrating hormone receptor antagonist. Eur J Pharmacol 438:129-135.
62. Thome J, Sakai N, Shin K, Steifen C, Zhang YJ, Impey S, Storm D, Duman RS (2000) cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment. J Neurosci 20:4030-4036.
63. Walsh BT, Roose SP, Classman AH, Gladis M, Sadik C (1985) Bulimia and depression. Psychosom Med 47:123-131.
64. Wise RA, Hoffman DC (1992) Localization of drug reward mechanisms by intracranial injections. Synapse 10:247-263.
65. Zhang M, Kelley AE (1997) Opiate agonists microinjected into the nucleus accumbens enhance sucrose drinking in rats. Psychopharmacology (Berl) 132:350-360.
66. Zhou QY, Palmiter RD (1995) Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 83:1197-1209.