Regulation of Energy Homeostasis by Bombesin Receptor Subtype-3: Selective Receptor Agonists for the Treatment of Obesity

Cell Metabolism

Volumn 11, Issue 2, 2010, Pages 101-112

  Guan, Xiao Ming ^a   Chen, Howard ^a   Dobbelaar, Peter H ^a   Dong, Yan ^a   Fong, Tung M ^a   Gagen, Karen ^a   Gorski, Judith ^a   He, Shuwen ^a   Howard, Andrew D ^a   Jian, Tianying ^a   Jiang, Michael ^a   Kan, Yanqing ^a   Kelly, Theresa M ^a   Kosinski, Jennifer ^a   Lin, Linus S ^a   Liu, Jian ^a   Marsh, Donald J ^a   Metzger, Joseph M ^a   Miller, Randy ^a   Nargund, Ravi P ^a   Palyha, Oksana ^a   Shearman, Lauren ^a   Shen, Zhu ^a   Stearns, Ralph ^a   Strack, Alison M ^a   Stribling, Sloan ^a   Tang, Yui Sing ^a   Wang, Sheng Ping ^a   White, Amanda ^a   Yu, Hong ^a   Reitman, Marc L ^a   more..

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

HUMDISEASE; MOLNEURO

Indexed keywords

ANTIOBESITY AGENT; BAG 1; BAG 2; BANTAG 1; BOMBESIN ANTAGONIST; BOMBESIN RECEPTOR; BOMBESIN RECEPTOR SUBTYPE 3; CANNABINOID 1 RECEPTOR AGONIST; MELANOCORTIN 4 RECEPTOR; MELANOCORTIN RECEPTOR AGONIST; TARANABANT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG DOSE COMPARISON; DRUG DOSE INCREASE; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG RECEPTOR BINDING; DRUG SCREENING; ENERGY BALANCE; FOOD INTAKE; HUMAN; LOW DRUG DOSE; MALE; METABOLIC RATE; MONOAMINE NERVE CELL; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RAT; RECEPTOR OCCUPANCY; REGULATORY MECHANISM; TACHYPHYLAXIS; WEIGHT REDUCTION;

ANIMALS; ANTI-OBESITY AGENTS; BODY WEIGHT; BRAIN; EATING; ENERGY METABOLISM; HUMANS; LIGANDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OBESITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, BOMBESIN;

BOVINE RESPIRATORY SYNCYTIAL VIRUS; MUS;

EID: 75149160396     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2009.12.008     Document Type: Article

References (65)

1. Adan R.A., Vanderschuren L.J., and la Fleur S.E. Anti-obesity drugs and neural circuits of feeding. Trends Pharmacol. Sci. 29 (2008) 208-217
2. Addy C., Wright H., Van Laere K., Gantz I., Erondu N., Musser B.J., Lu K., Yuan J., Sanabria-Bohórquez S.M., Stoch A., et al. The acyclic CB1R inverse agonist taranabant mediates weight loss by increasing energy expenditure and decreasing caloric intake. Cell Metab. 7 (2008) 68-78
3. Ashrafi K., Chang F.Y., Watts J.L., Fraser A.G., Kamath R.S., Ahringer J., and Ruvkun G. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421 (2003) 268-272
4. Bannon A.W., Seda J., Carmouche M., Francis J.M., Norman M.H., Karbon B., and McCaleb M.L. Behavioral characterization of neuropeptide Y knockout mice. Brain Res. 868 (2000) 79-87
5. Blanchet P.J., Grondin R., Bédard P.J., Shiosaki K., and Britton D.R. Dopamine D1 receptor desensitization profile in MPTP-lesioned primates. Eur. J. Pharmacol. 309 (1996) 13-20
6. Boyle R.G., Humphries J., Mitchell T., Showell G.A., Apaya R., Iijima H., Shimada H., Arai T., Ueno H., Usui Y., et al. The design of a new potent and selective ligand for the orphan bombesin receptor subtype 3 (BRS3). J. Pept. Sci. 11 (2005) 136-141
7. Carlton D.L., Collin-Smith L.J., Daniels A.J., Deaton D.N., Goetz A.S., Laudeman C.P., Littleton T.R., Musso D.L., Morgan R.J., Szewczyk J.R., and Zhang C. Discovery of small molecule agonists for the bombesin receptor subtype 3 (BRS-3) based on an omeprazole lead. Bioorg. Med. Chem. Lett. 18 (2008) 5451-5455
8. Chen A.S., Marsh D.J., Trumbauer M.E., Frazier E.G., Guan X.M., Yu H., Rosenblum C.I., Vongs A., Feng Y., Cao L., et al. Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass. Nat. Genet. 26 (2000) 97-102
9. Chen A.S., Metzger J.M., Trumbauer M.E., Guan X.M., Yu H., Frazier E.G., Marsh D.J., Forrest M.J., Gopal-Truter S., Fisher J., et al. Role of the melanocortin-4 receptor in metabolic rate and food intake in mice. Transgenic Res. 9 (2000) 145-154
10. Chen H.Y., Trumbauer M.E., Chen A.S., Weingarth D.T., Adams J.R., Frazier E.G., Shen Z., Marsh D.J., Feighner S.D., Guan X.M., et al. Orexigenic action of peripheral ghrelin is mediated by neuropeptide Y and agouti-related protein. Endocrinology 145 (2004) 2607-2612
11. Cota D., Marsicano G., Tschöp M., Grübler Y., Flachskamm C., Schubert M., Auer D., Yassouridis A., Thöne-Reineke C., Ortmann S., et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J. Clin. Invest. 112 (2003) 423-431
12. De Souza J., Butler A.A., and Cone R.D. Disproportionate inhibition of feeding in A(y) mice by certain stressors: a cautionary note. Neuroendocrinology 72 (2000) 126-132
13. Dong Y., Tyszkiewicz J.P., and Fong T.M. Galanin and galanin-like peptide differentially modulate neuronal activities in rat arcuate nucleus neurons. J. Neurophysiol. 95 (2006) 3228-3234
14. Ebihara K., Ogawa Y., Katsuura G., Numata Y., Masuzaki H., Satoh N., Tamaki M., Yoshioka T., Hayase M., Matsuoka N., et al. Involvement of agouti-related protein, an endogenous antagonist of hypothalamic melanocortin receptor, in leptin action. Diabetes 48 (1999) 2028-2033
15. Erickson J.C., Clegg K.E., and Palmiter R.D. Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 381 (1996) 415-421
16. Erondu N., Gantz I., Musser B., Suryawanshi S., Mallick M., Addy C., Cote J., Bray G., Fujioka K., Bays H., et al. Neuropeptide Y5 receptor antagonism does not induce clinically meaningful weight loss in overweight and obese adults. Cell Metab. 4 (2006) 275-282
17. Fathi Z., Corjay M.H., Shapira H., Wada E., Benya R., Jensen R., Viallet J., Sausville E.A., and Battey J.F. BRS-3: a novel bombesin receptor subtype selectively expressed in testis and lung carcinoma cells. J. Biol. Chem. 268 (1993) 5979-5984
18. Fleischmann A., Läderach U., Friess H., Buechler M.W., and Reubi J.C. Bombesin receptors in distinct tissue compartments of human pancreatic diseases. Lab. Invest. 80 (2000) 1807-1817
19. Fong T.M., Guan X.M., Marsh D.J., Shen C.P., Stribling D.S., Rosko K.M., Lao J., Yu H., Feng Y., Xiao J.C., et al. Antiobesity efficacy of a novel cannabinoid-1 receptor inverse agonist, N-[(1S,2S)-3-(4-chlorophenyl)-2-(3-cyanophenyl)-1-methylpropyl]-2-methyl-2-[[5-(trifluoromethyl)pyridin-2-yl]oxy]propanamide (MK-0364), in rodents. J. Pharmacol. Exp. Ther. 321 (2007) 1013-1022
20. Franklin K.B.J., and Paxinos G. The mouse brain in stereotaxic coordinates (1997), Academic Press, New York
21. Fulton S., Pissios P., Manchon R.P., Stiles L., Frank L., Pothos E.N., Maratos-Flier E., and Flier J.S. Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 51 (2006) 811-822
22. Gao Q., and Horvath T.L. Neurobiology of feeding and energy expenditure. Annu. Rev. Neurosci. 30 (2007) 367-398
23. Gatley S.J., Gifford A.N., Volkow N.D., Lan R., and Makriyannis A. 123I-labeled AM251: a radioiodinated ligand which binds in vivo to mouse brain cannabinoid CB1 receptors. Eur. J. Pharmacol. 307 (1996) 331-338
24. Guo L., Ye Z., Ujjainwalla F., Sings H.L., Sebhat I.K., Huber J., Weinberg D.H., Tang R., MacNeil T., Tamvakopoulos C., et al. Synthesis and SAR of potent and orally bioavailable tert-butylpyrrolidine archetype derived melanocortin subtype-4 receptor modulators. Bioorg. Med. Chem. Lett. 18 (2008) 3242-3247
25. Hou X., Wei L., Harada A., and Tatamoto K. Activation of bombesin receptor subtype-3 stimulates adhesion of lung cancer cells. Lung Cancer 54 (2006) 143-148
26. Huszar D., Lynch C.A., Fairchild-Huntress V., Dunmore J.H., Fang Q., Berkemeier L.R., Gu W., Kesterson R.A., Boston B.A., Cone R.D., et al. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88 (1997) 131-141
27. Ishihara A., Kanatani A., Mashiko S., Tanaka T., Hidaka M., Gomori A., Iwaasa H., Murai N., Egashira S., Murai T., et al. A neuropeptide Y Y5 antagonist selectively ameliorates body weight gain and associated parameters in diet-induced obese mice. Proc. Natl. Acad. Sci. USA 103 (2006) 7154-7158
28. Jennings C.A., Harrison D.C., Maycox P.R., Crook B., Smart D., and Hervieu G.J. The distribution of the orphan bombesin receptor subtype-3 in the rat CNS. Neuroscience 120 (2003) 309-324
29. Jensen R.T., Battey J.F., Spindel E.R., and Benya R.V. International Union of Pharmacology. LXVIII. Mammalian bombesin receptors: nomenclature, distribution, pharmacology, signaling, and functions in normal and disease states. Pharmacol. Rev. 60 (2008) 1-42
30. Ladenheim E.E., Hamilton N.L., Behles R.R., Bi S., Hampton L.L., Battey J.F., and Moran T.H. Factors contributing to obesity in bombesin receptor subtype-3-deficient mice. Endocrinology 149 (2008) 971-978
31. Lammerich H.P., Busmann A., Kutzleb C., Wendland M., Seiler P., Berger C., Eickelmann P., Meyer M., Forssmann W.G., and Maronde E. Identification and functional characterization of hemorphins VV-H-7 and LVV-H-7 as low-affinity agonists for the orphan bombesin receptor subtype 3. Br. J. Pharmacol. 138 (2003) 1431-1440
32. Lewis M.M., Watts V.J., Lawler C.P., Nichols D.E., and Mailman R.B. Homologous desensitization of the D1A dopamine receptor: efficacy in causing desensitization dissociates from both receptor occupancy and functional potency. J. Pharmacol. Exp. Ther. 286 (1998) 345-353
33. Liu J., Lao Z.J., Zhang J., Schaeffer M.T., Jiang M.M., Guan X.M., Van der Ploeg L.H., and Fong T.M. Molecular basis of the pharmacological difference between rat and human bombesin receptor subtype-3 (BRS-3). Biochemistry 41 (2002) 8954-8960
34. Luquet S., Perez F.A., Hnasko T.S., and Palmiter R.D. NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310 (2005) 683-685
35. Lutter M., and Nestler E.J. Homeostatic and hedonic signals interact in the regulation of food intake. J. Nutr. 139 (2009) 629-632
36. Mantey S.A., Weber H.C., Sainz E., Akeson M., Ryan R.R., Pradhan T.K., Searles R.P., Spindel E.R., Battey J.F., Coy D.H., and Jensen R.T. Discovery of a high affinity radioligand for the human orphan receptor, bombesin receptor subtype 3, which demonstrates that it has a unique pharmacology compared with other mammalian bombesin receptors. J. Biol. Chem. 272 (1997) 26062-26071
37. Mantey S.A., Gonzalez N., Schumann M., Pradhan T.K., Shen L., Coy D.H., and Jensen R.T. Identification of bombesin receptor subtype-specific ligands: effect of N-methyl scanning, truncation, substitution, and evaluation of putative reported selective ligands. J. Pharmacol. Exp. Ther. 319 (2006) 980-989
38. Marsh D.J., Hollopeter G., Kafer K.E., and Palmiter R.D. Role of the Y5 neuropeptide Y receptor in feeding and obesity. Nat. Med. 4 (1998) 718-721
39. Marsh D.J., Hollopeter G., Huszar D., Laufer R., Yagaloff K.A., Fisher S.L., Burn P., and Palmiter R.D. Response of melanocortin-4 receptor-deficient mice to anorectic and orexigenic peptides. Nat. Genet. 21 (1999) 119-122
40. Matsumoto K., and Iijima H. Sibutramine sensitivity assay revealed a unique phenotype of bombesin BB3 receptor-deficient mice. Eur. J. Pharmacol. 473 (2003) 41-46
41. Morrison C.D., and Berthoud H.R. Neurobiology of nutrition and obesity. Nutr. Rev. 65 (2007) 517-534
42. Nakamichi Y., Wada E., Aoki K., Ohara-Imaizumi M., Kikuta T., Nishiwaki C., Matsushima S., Watanabe T., Wada K., and Nagamatsu S. Functions of pancreatic beta cells and adipocytes in bombesin receptor subtype-3-deficient mice. Biochem. Biophys. Res. Commun. 318 (2004) 698-703
43. Ohki-Hamazaki H., Wada E., Matsui K., and Wada K. Cloning and expression of the neuromedin B receptor and the third subtype of bombesin receptor genes in the mouse. Brain Res. 762 (1997) 165-172
44. Ohki-Hamazaki H., Watase K., Yamamoto K., Ogura H., Yamano M., Yamada K., Maeno H., Imaki J., Kikuyama S., Wada E., and Wada K. Mice lacking bombesin receptor subtype-3 develop metabolic defects and obesity. Nature 390 (1997) 165-169
45. Pinto S., Roseberry A.G., Liu H., Diano S., Shanabrough M., Cai X., Friedman J.M., and Horvath T.L. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304 (2004) 110-115
46. Qian S., Chen H., Weingarth D., Trumbauer M.E., Novi D.E., Guan X., Yu H., Shen Z., Feng Y., Frazier E., et al. Neither agouti-related protein nor neuropeptide Y is critically required for the regulation of energy homeostasis in mice. Mol. Cell. Biol. 22 (2002) 5027-5035
47. Rankinen T., Zuberi A., Chagnon Y.C., Weisnagel S.J., Argyropoulos G., Walts B., Pérusse L., and Bouchard C. The human obesity gene map: the 2005 update. Obesity (Silver Spring) 14 (2006) 529-644
48. Ravinet Trillou C., Delgorge C., Menet C., Arnone M., and Soubrié P. CB1 cannabinoid receptor knockout in mice leads to leanness, resistance to diet-induced obesity and enhanced leptin sensitivity. Int. J. Obes. Relat. Metab. Disord. 28 (2004) 640-648
49. Rousseau G., Nantel F., and Bouvier M. Distinct receptor domains determine subtype-specific coupling and desensitization phenotypes for human beta1- and beta2-adrenergic receptors. Mol. Pharmacol. 49 (1996) 752-760
50. Ryan R.R., Weber H.C., Mantey S.A., Hou W., Hilburger M.E., Pradhan T.K., Coy D.H., and Jensen R.T. Pharmacology and intracellular signaling mechanisms of the native human orphan receptor BRS-3 in lung cancer cells. J. Pharmacol. Exp. Ther. 287 (1998) 366-380
51. Sano H., Feighner S.D., Hreniuk D.L., Iwaasa H., Sailer A.W., Pan J., Reitman M.L., Kanatani A., Howard A.D., and Tan C.P. Characterization of the bombesin-like peptide receptor family in primates. Genomics 84 (2004) 139-146
52. Seeley R.J., Yagaloff K.A., Fisher S.L., Burn P., Thiele T.E., van Dijk G., Baskin D.G., and Schwartz M.W. Melanocortin receptors in leptin effects. Nature 390 (1997) 349
53. Shan L., Emanuel R.L., Dewald D., Torday J.S., Asokanathan N., Wada K., Wada E., and Sunday M.E. Bombesin-like peptide receptor gene expression, regulation, and function in fetal murine lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 286 (2004) L165-L173
54. Tan Y.R., Qi M.M., Qin X.Q., Xiang Y., Li X., Wang Y., Qu F., Liu H.J., and Zhang J.S. Wound repair and proliferation of bronchial epithelial cells enhanced by bombesin receptor subtype 3 activation. Peptides 27 (2006) 1852-1858
55. Thakur G.A., Nikas S.P., and Makriyannis A. CB1 cannabinoid receptor ligands. Mini Rev. Med. Chem. 5 (2005) 631-640
56. Weber H.C., Hampton L.L., Jensen R.T., and Battey J.F. Structure and chromosomal localization of the mouse bombesin receptor subtype 3 gene. Gene 211 (1998) 125-131
57. Weber D., Berger C., Eickelmann P., Antel J., and Kessler H. Design of selective peptidomimetic agonists for the human orphan receptor BRS-3. J. Med. Chem. 46 (2003) 1918-1930
58. Whitley J.C., Moore C., Giraud A.S., and Shulkes A. Molecular cloning, genomic organization and selective expression of bombesin receptor subtype 3 in the sheep hypothalamus and pituitary. J. Mol. Endocrinol. 23 (1999) 107-116
59. Yadav V.K., Oury F., Suda N., Liu Z.W., Gao X.B., Confavreux C., Klemenhagen K.C., Tanaka K.F., Gingrich J.A., Guo X.E., et al. A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell 138 (2009) 976-989
60. Yamada K., Wada E., Imaki J., Ohki-Hamazaki H., and Wada K. Hyperresponsiveness to palatable and aversive taste stimuli in genetically obese (bombesin receptor subtype-3-deficient) mice. Physiol. Behav. 66 (1999) 863-867
61. Yamada K., Ohki-Hamazaki H., and Wada K. Differential effects of social isolation upon body weight, food consumption, and responsiveness to novel and social environment in bombesin receptor subtype-3 (BRS-3) deficient mice. Physiol. Behav. 68 (2000) 555-561
62. Yamada K., Santo-Yamada Y., Wada E., and Wada K. Role of bombesin (BN)-like peptides/receptors in emotional behavior by comparison of three strains of BN-like peptide receptor knockout mice. Mol. Psychiatry 7 (2002) 113-117
63. Yoshimatsu H. Hypothalamic neuronal histamine regulates body weight through the modulation of diurnal feeding rhythm. Nutrition 24 (2008) 827-831
64. Zhang L., Nothacker H.P., Wang Z., Bohn L.M., and Civelli O. Pharmacological characterization of a selective agonist for bombesin receptor subtype-3. Biochem. Biophys. Res. Commun. 387 (2009) 283-288
65. Zimmer A., Zimmer A.M., Hohmann A.G., Herkenham M., and Bonner T.I. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl. Acad. Sci. USA 96 (1999) 5780-5785