Pmch expression during early development is critical for normal energy homeostasis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 3, 2010, Pages

  Mul, Joram D ^a   Yi, Chun Xia ^b   Van Den Berg, Sjoerd A A ^c   Ruiter, Marieke ^c   Toonen, Pim W ^a   Van Der Elst, Martine C J ^d   Voshol, Peter J ^c   Ellenbroek, Bart A ^d   Kalsbeek, Andries ^b,e   La Fleur, Susanne E ^e,f   Cuppen, Edwin ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Childhood obesity; Hypothalamus; Melanin concentrating hormone; Rat knockout model

Indexed keywords

MELANIN CONCENTRATING HORMONE; MELANIN CONCENTRATING HORMONE RECEPTOR 1; PMCH PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ADAPTATION; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY GROWTH; BODY WEIGHT; CONTROLLED STUDY; DEVELOPMENT; DIETARY INTAKE; ENDOCRINE FUNCTION; ENERGY; ENERGY EXPENDITURE; FEEDING; FEEDING BEHAVIOR; GENOTYPE; HOMEOSTASIS; HYPOPHAGIA; KNOCKOUT MOUSE; MALE; METABOLISM; NONHUMAN; OSTEOPOROSIS; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RAT;

ANIMALS; BODY WEIGHT; ENERGY INTAKE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEOSTASIS; HYPOTHALAMIC HORMONES; MELANINS; PITUITARY HORMONES; PROTEIN PRECURSORS; RATS;

EID: 77349114417     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00154.2009     Document Type: Article

References (68)

1. Alon T, Friedman JM. Late-onset leanness in mice with targeted ablation of melanin concentrating hormone neurons. J Neurosci 26: 389-397, 2006.
2. Attademo AM, Sanchez-Borzone M, Lasaga M, Celis ME. Intracerebroventricular injection of neuropeptide EI increases serum LH in male and female rats. Peptides 25: 1995-1999, 2004.
3. Bittencourt JC, Presse F, Arias C, Peto C, Vaughan J, Nahon JL, Vale W, Sawchenko PE. The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J Comp Neurol 319: 218-245, 1992.
4. Bohlooly YM, Mahlapuu M, Andersen H, Astrand A, Hjorth S, Svensson L, Tornell J, Snaith MR, Morgan DG, Ohlsson C. Osteoporosis in MCHR1-deficient mice. Biochem Biophys Res Commun 318: 964-969, 2004.
5. Bouret SG, Simerly RB. Developmental programming of hypothalamic feeding circuits. Clin Genet 70: 295-301, 2006.
6. Brownell KD, Wadden TA. Etiology and treatment of obesity: understanding a serious, prevalent, and refractory disorder. J Consult Clin Psychol 60: 505-517, 1992.
7. 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. Melaninconcentrating hormone is the cognate ligand for the orphan G-proteincoupled receptor SLC-1. Nature 400: 261-265, 1999.
8. Chen Y, Hu C, Hsu CK, Zhang Q, Bi C, Asnicar M, Hsiung HM, Fox N, Slieker LJ, Yang DD, Heiman ML, Shi Y. Targeted disruption of the melanin-concentrating hormone receptor-1 results in hyperphagia and resistance to diet-induced obesity. Endocrinology 143: 2469-2477, 2002.
9. Chung S, Hopf FW, Nagasaki H, Li CY, Belluzzi JD, Bonci A, Civelli O. The melanin-concentrating hormone system modulates cocaine reward. Proc Natl Acad Sci USA 106: 6772-6777, 2009.
10. Cuppen E, Gort E, Hazendonk E, Mudde J, van de Belt J, Nijman IJ, Guryev V, Plasterk RH. Efficient target-selected mutagenesis in Caenorhabditis elegans: toward a knockout for every gene. Genome Res 17: 649-658, 2007.
11. Della-Zuana O, Presse F, Ortola C, Duhault J, Nahon JL, Levens N. Acute and chronic administration of melanin-concentrating hormone enhances food intake and body weight in Wistar and Sprague-Dawley rats. Int J Obes Relat Metab Disord 26: 1289-1295, 2002.
12. Even PC, Mokhtarian A, Pele A. Practical aspects of indirect calorimetry in laboratory animals. Neurosci Biobehav Rev 18: 435-447, 1994.
13. Even PC, Rolland V, Roseau S, Bouthegourd JC, Tome D. Prediction of basal metabolism from organ size in the rat: relationship to strain, feeding, age, and obesity. Am J Physiol Regul Integr Comp Physiol 280: R1887-R1896, 2001.
14. Foreyt JP, Goodrick GK. Evidence for success of behavior modification in weight loss and control. Ann Intern Med 119: 698-701, 1993.
15. Francis RM, Peacock M, Aaron JE, Selby PL, Taylor GA, Thompson J, Marshall DH, Horsman A. Osteoporosis in hypogonadal men: role of decreased plasma 1,25-dihydroxyvitamin D, calcium malabsorption, and low bone formation. Bone 7: 261-268, 1986.
16. Georgescu D, Sears RM, Hommel JD, Barrot M, Bolanos CA, Marsh DJ, Bednarek MA, Bibb JA, Maratos-Flier E, Nestler EJ, DiLeone RJ. The hypothalamic neuropeptide melanin-concentrating hormone acts in the nucleus accumbens to modulate feeding behavior and forced-swim performance. J Neurosci 25: 2933-2940, 2005.
17. Gomez F, Dallman MF. Manipulation of androgens causes different energetic responses to cold in 60- and 40-day-old male rats. Am J Physiol Regul Integr Comp Physiol 280: R262-R273, 2001.
18. Gomez F, Houshyar H, Dallman MF. Marked regulatory shifts in gonadal, adrenal, and metabolic system responses to repeated restraint stress occur within a 3-week period in pubertal male rats. Endocrinology 143: 2852-2862, 2002.
19. Gomori A, Ishihara A, Ito M, Mashiko S, Matsushita H, Yumoto M, Tanaka T, Tokita S, Moriya M, Iwaasa H, Kanatani A. Chronic intracerebroventricular infusion of MCH causes obesity in mice. Melaninconcentrating hormone. Am J Physiol Endocrinol Metab 284: E583-E588, 2003.
20. Gonzalez MI, Baker BI, Hole DR, Wilson CA. Behavioral effects of neuropeptide E-I (NEI) in the female rat: interactions with alpha-MSH, MCH and dopamine. Peptides 19: 1007-1016, 1998.
21. Grove KL, Grayson BE, Glavas MM, Xiao XQ, Smith MS. Development of metabolic systems. Physiol Behav 86: 646-660, 2005.
22. Guesdon B, Paradis E, Samson P, Richard D. Effects of intracerebroventricular and intra-accumbens melanin-concentrating hormone agonism on food intake and energy expenditure. Am J Physiol Regul Integr Comp Physiol 296: R469-R475, 2009.
23. Hammer RL, Barrier CA, Roundy ES, Bradford JM, Fisher AG. Calorie-restricted low-fat diet and exercise in obese women. Am J Clin Nutr 49: 77-85, 1989.
24. Handlon AL, Zhou H. Melanin-concentrating hormone-1 receptor antagonists for the treatment of obesity. J Med Chem 49: 4017-4022, 2006.
25. Hervieu G, Nahon JL. Pro-melanin concentrating hormone messenger ribonucleic acid and peptides expression in peripheral tissues of the rat. Neuroendocrinology 61: 348-364, 1995.
26. Hill JO, Sparling PB, Shields TW, Heller PA. Effects of exercise and food restriction on body composition and metabolic rate in obese women. Am J Clin Nutr 46: 622-630, 1987.
27. Homberg JR, Olivier JD, Smits BM, Mul JD, Mudde J, Verheul M, Nieuwenhuizen OF, Cools AR, Ronken E, Cremers T, Schoffelmeer AN, Ellenbroek BA, Cuppen E. Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system. Neuroscience 146: 1662-1676, 2007.
28. Ito M, Gomori A, Ishihara A, Oda Z, Mashiko S, Matsushita H, Yumoto M, Sano H, Tokita S, Moriya M, Iwaasa H, Kanatani A. Characterization of MCH-mediated obesity in mice. Am J Physiol Endocrinol Metab 284: E940-E945, 2003.
29. Keays DA, Clark TG, Flint J. Estimating the number of coding mutations in genotypic- and phenotypic-driven N-ethyl-N-nitrosourea (ENU) screens. Mamm Genome 17: 230-238, 2006.
30. Khosla T, Billewicz WZ. Measurement of change in body-weight. Br J Nutr 18: 227-239, 1964.
31. Kokkotou E, Jeon JY, Wang X, Marino FE, Carlson M, Trombly DJ, Maratos-Flier E. Mice with MCH ablation resist diet-induced obesity through strain-specific mechanisms. Am J Physiol Regul Integr Comp Physiol 289: R117-R124, 2005.
32. Kokkotou EG, Tritos NA, Mastaitis JW, Slieker L, Maratos-Flier E. Melanin-concentrating hormone receptor is a target of leptin action in the mouse brain. Endocrinology 142: 680-686, 2001.
33. 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. The receptor for the orexigenic peptide melaninconcentrating hormone is a G-protein-coupled receptor. Nat Cell Biol 1: 267-271, 1999.
34. Leser MS, Yanovski SZ, Yanovski JA. A low-fat intake and greater activity level are associated with lower weight regain 3 years after completing a very-low-calorie diet. J Am Diet Assoc 102: 1252-1256, 2002.
35. Ludwig DS, Tritos NA, Mastaitis JW, Kulkarni R, Kokkotou E, Elmquist J, Lowell B, Flier JS, Maratos-Flier E. Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 107: 379-386, 2001.
36. Luthin DR. Anti-obesity effects of small molecule melanin-concentrating hormone receptor 1 (MCHR1) antagonists. Life Sci 81: 423-440, 2007.
37. Mardon J, Zangarelli A, Walrand S, Davicco MJ, Lebecque P, Demigne C, Horcajada MN, Boirie Y, Coxam V. Impact of energy and casein or whey protein intake on bone status in a rat model of age-related bone loss. Br J Nutr 99: 764-772, 2008.
38. 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, Van der Ploeg LH, Qian S. Melaninconcentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc Natl Acad Sci USA 99: 3240-3245, 2002.
39. Mashiko S, Ishihara A, Gomori A, Moriya R, Ito M, Iwaasa H, Matsuda M, Feng Y, Shen Z, Marsh DJ, Bednarek MA, MacNeil DJ, Kanatani A. Antiobesity effect of a melanin-concentrating hormone 1 receptor antagonist in diet-induced obese mice. Endocrinology 146: 3080-3086, 2005.
40. McMillen IC, Adam CL, Muhlhausler BS. Early origins of obesity: programming the appetite regulatory system. J Physiol 565: 9-17, 2005.
41. Nahon JL, Presse F, Bittencourt JC, Sawchenko PE, Vale W. The rat melanin-concentrating hormone messenger ribonucleic acid encodes multiple putative neuropeptides coexpressed in the dorsolateral hypothalamus. Endocrinology 125: 2056-2065, 1989.
42. Nair SG, Adams-Deutsch T, Pickens CL, Smith DG, Shaham Y. Effects of the MCH1 receptor antagonist SNAP 94847 on high-fat foodreinforced operant responding and reinstatement of food seeking in rats. Psychopharmacology (Berl) 205: 129-140. 2009.
43. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA 295: 1549-1555, 2006.
44. Oscai LB, McGarr JA. Evidence that the amount of food consumed in early life fixes appetite in the rat. Am J Physiol Regul Integr Comp Physiol 235: R141-R144, 1978.
45. Palani A, Shapiro S, McBriar MD, Clader JW, Greenlee WJ, Spar B, Kowalski TJ, Farley C, Cook J, van Heek M, Weig B, O'Neill K, Graziano M, Hawes B. Biaryl ureas as potent and orally efficacious melanin concentrating hormone receptor 1 antagonists for the treatment of obesity. J Med Chem 48: 4746-4749, 2005.
46. Pissios P, Bradley RL, Maratos-Flier E. Expanding the scales: the multiple roles of MCH in regulating energy balance and other biological functions. Endocr Rev 27: 606-620, 2006.
47. Pissios P, Frank L, Kennedy AR, Porter DR, Marino FE, Liu FF, Pothos EN, Maratos-Flier E. Dysregulation of the mesolimbic dopamine system and reward in MCH-/- mice. Biol Psychiatry 64: 184-191, 2008.
48. Pissios P, Ozcan U, Kokkotou E, Okada T, Liew CW, Liu S, Peters JN, Dahlgren G, Karamchandani J, Kudva YC, Kurpad AJ, Kennedy RT, Maratos-Flier E, Kulkarni RN. Melanin concentrating hormone is a novel regulator of islet function and growth. Diabetes 56: 311-319, 2007.
49. Presse F, Hervieu G, Imaki T, Sawchenko PE, Vale W, Nahon JL. Rat melanin-concentrating hormone messenger ribonucleic acid expression: marked changes during development and after stress and glucocorticoid stimuli. Endocrinology 131: 1241-1250, 1992.
50. Qu D, Ludwig DS, Gammeltoft S, Piper M, Pelleymounter MA, Cullen MJ, Mathes WF, Przypek R, Kanarek R, Maratos-Flier E. A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380: 243-247, 1996.
51. Remmers F, Fodor M, Delemarre-van de Waal HA. Neonatal food restriction permanently alters rat body dimensions and energy intake. Physiol Behav 95: 208-215, 2008.
52. Robinson MF, Watson PE. Day-to-day variations in body-weight of young women. Br J Nutr 19: 225-235, 1965.
53. Rossi M, Choi SJ, O'Shea D, Miyoshi T, Ghatei MA, Bloom SR. Melanin-concentrating hormone acutely stimulates feeding, but chronic administration has no effect on body weight. Endocrinology 138: 351-355, 1997.
54. Sailer AW, Sano H, Zeng Z, McDonald TP, Pan J, Pong SS, Feighner SD, Tan CP, Fukami T, Iwaasa H, Hreniuk DL, Morin NR, Sadowski SJ, Ito M, Ito M, Bansal A, Ky B, Figueroa DJ, Jiang Q, Austin CP, MacNeil DJ, Ishihara A, Ihara M, Kanatani A, Van der Ploeg LH, Howard AD, Liu Q. Identification and characterization of a second melanin-concentrating hormone receptor, MCH-2R. Proc Natl Acad Sci USA 98: 7564-7569, 2001.
55. Saito Y, Cheng M, Leslie FM, Civelli O. Expression of the melaninconcentrating hormone (MCH) receptor mRNA in the rat brain. J Comp Neurol 435: 26-40, 2001.
56. Saito Y, Nothacker HP, Wang Z, Lin SH, Leslie F, Civelli O. Molecular characterization of the melanin-concentrating-hormone receptor. Nature 400: 265-269, 1999.
57. Sanchez M, Baker BI, Celis M. Melanin-concentrating hormone (MCH) antagonizes the effects of alpha-MSH and neuropeptide E-I on grooming and locomotor activities in the rat. Peptides 18: 393-396, 1997.
58. Shearman LP, Camacho RE, Sloan Stribling D, Zhou D, Bednarek MA, Hreniuk DL, Feighner SD, Tan CP, Howard AD, Van der Ploeg LH, MacIntyre DE, Hickey GJ, Strack AM. Chronic MCH-1 receptor modulation alters appetite, body weight and adiposity in rats. Eur J Pharmacol 475: 37-47, 2003.
59. Shimada M, Tritos NA, Lowell BB, Flier JS, Maratos-Flier E. Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature 396: 670-674, 1998.
60. Sita LV, Elias CF, Bittencourt JC. Connectivity pattern suggests that incerto-hypothalamic area belongs to the medial hypothalamic system. Neuroscience 148: 949-969, 2007.
61. Smits BM, Mudde JB, van de Belt J, Verheul M, Olivier J, Homberg J, Guryev V, Cools AR, Ellenbroek BA, Plasterk RH, Cuppen E. Generation of gene knockouts and mutant models in the laboratory rat by ENU-driven target-selected mutagenesis. Pharmacogenet Genomics 16: 159-169, 2006.
62. Steffens AB. Influence of reversible obesity on eating behavior, blood glucose, and insulin in the rat. Am J Physiol 228: 1738-1744, 1975.
63. Stepan JJ, Lachman M, Zverina J, Pacovsky V, Baylink DJ. Castrated men exhibit bone loss: effect of calcitonin treatment on biochemical indices of bone remodeling. J Clin Endocrinol Metab 69: 523-527, 1989.
64. Sugden MC, Grimshaw RM, Holness MJ. Caloric restriction leads to regional specialisation of adipocyte function in the rat. Biochim Biophys Acta 1437: 202-213, 1999.
65. Tadayyon M, Welters HJ, Haynes AC, Cluderay JE, Hervieu G. Expression of melanin-concentrating hormone receptors in insulin-producing cells: MCH stimulates insulin release in RINm5F and CRI-G1 cell-lines. Biochem Biophys Res Commun 275: 709-712, 2000.
66. van Boxtel R, Toonen PW, van Roekel HS, Verheul M, Smits BM, Korving J, de Bruin A, Cuppen E. Lack of DNA mismatch repair protein MSH6 in the rat results in hereditary non-polyposis colorectal cancer-like tumorigenesis. Carcinogenesis 29: 1290-1297, 2008.
67. van Dale D, Saris WH, ten Hoor F. Weight maintenance and resting metabolic rate 18-40 months after a diet/exercise treatment. Int J Obes 14: 347-359, 1990.
68. Wing RR, Hill JO. Successful weight loss maintenance. Annu Rev Nutr 21: 323-341, 2001.