Estrogen-related receptor β deletion modulates whole-body energy balance via estrogen-related receptor γ and attenuates neuropeptide Y gene expression

European Journal of Neuroscience

Volumn 37, Issue 7, 2013, Pages 1033-1047

  Byerly, Mardi S ^a   Al Salayta, Muhannad ^a   Swanson, Roy D ^a   Kwon, Kiwook ^a   Peterson, Jonathan M ^a   Wei, Zhikui ^a   Aja, Susan ^a   Moran, Timothy H ^a   Blackshaw, Seth ^a   Wong, G William ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hindbrain; Meal patterns; Medulla; Metabolism; Mice

Indexed keywords

MESSENGER RNA; NEUROPEPTIDE Y; STEROID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPETITE; ARTICLE; ATTENUATION; BODY COMPOSITION; BODY MASS; BRAIN NERVE CELL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENERGY BALANCE; ENERGY EXPENDITURE; ESTROGEN RELATED RECEPTOR BETA GENE; ESTROGEN RELATED RECEPTOR GAMMA GENE; GENE DELETION; GENE EXPRESSION; INSULIN SENSITIVITY; METABOLIC RATE; MOUSE; NEUROMODULATION; NEUROPEPTIDE Y GENE; NONHUMAN; PHENOTYPE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RHOMBENCEPHALON; SATIETY; SIGNAL TRANSDUCTION;

ANIMALS; BODY WEIGHT; ENERGY METABOLISM; GENE DELETION; GENE EXPRESSION; INSULIN RESISTANCE; MICE; MICE, KNOCKOUT; NEURONS; NEUROPEPTIDE Y; PHENOTYPE; RECEPTORS, ESTROGEN; RHOMBENCEPHALON; SATIATION; SIGNAL TRANSDUCTION;

EID: 84875664465     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12122     Document Type: Article

References (57)

1. Adrian, T.E., Allen, J.M., Bloom, S.R., Ghatei, M.A., Rossor, M.N., Roberts, G.W., Crow, T.J., Tatemoto, K. & Polak, J.M. (1983) Neuropeptide Y distribution in human brain. Nature, 306, 584-586.
2. Alaynick, W.A., Kondo, R.P., Xie, W., He, W., Dufour, C.R., Downes, M., Jonker, J.W., Giles, W., Naviaux, R.K., Giguere, V. & Evans, R.M. (2007) ERRgamma directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab., 6, 13-24.
3. Allen Brain Atlas. (2012) Available http://mouse.brain-map.org/.
4. Allen, Y.S., Adrian, T.E., Allen, J.M., Tatemoto, K., Crow, T.J., Bloom, S.R. & Polak, J.M. (1983) Neuropeptide Y distribution in the rat brain. Science, 221, 877-879.
5. Anand, B.K. & Brobeck, J.R. (1984) Nutrition classics. The Yale Journal of Biology and Medicine. Volume XXIV 1951-1952. Hypothalamic control of food intake in rats and cats. Nutr. Rev., 42, 354-356.
6. Baird, J.P., Rios, C., Loveland, J.L., Beck, J., Tran, A. & Mahoney, C.E. (2008) Effects of hindbrain melanin-concentrating hormone and neuropeptide Y administration on licking for water, saccharin, and sucrose solutions. Am. J. Physiol. Regul. Integr. Comp. Physiol., 294, R329-R343.
7. Begriche, K., Levasseur, P.R., Zhang, J., Rossi, J., Skorupa, D., Solt, L.A., Young, B., Burris, T.P., Marks, D.L., Mynatt, R.L. & Butler, A.A. (2011) Genetic dissection of the functions of the melanocortin-3 receptor, a seven-transmembrane G-protein-coupled receptor, suggests roles for central and peripheral receptors in energy homeostasis. J. Biol. Chem., 286, 40771-40781.
8. Bergman, R.N., Ider, Y.Z., Bowden, C.R. & Cobelli, C. (1979) Quantitative estimation of insulin sensitivity. Am. J. Physiol., 236, E667-E677.
9. Bergman, R.N., Phillips, L.S. & Cobelli, C. (1981) Physiologic evaluation of factors controlling glucose tolerance in man: measurement of insulin sensitivity and beta-cell glucose sensitivity from the response to intravenous glucose. J. Clin. Invest., 68, 1456-1467.
10. Berthoud, H.R. & Powley, T.L. (1985) Altered plasma insulin and glucose after obesity-producing bipiperidyl brain lesions. Am. J. Physiol., 248, R46-R53.
11. Berthoud, H.R., Fox, E.A. & Powley, T.L. (1990) Localization of vagal preganglionics that stimulate insulin and glucagon secretion. Am. J. Physiol., 258, R160-R168.
12. Bi, S., Scott, K.A., Kopin, A.S. & Moran, T.H. (2004) Differential roles for cholecystokinin a receptors in energy balance in rats and mice. Endocrinology, 145, 3873-3880.
13. Blackshaw, S. & Snyder, S.H. (1997) Developmental expression pattern of phototransduction components in mammalian pineal implies a light-sensing function. J. Neurosci., 17, 8074-8082.
14. Blackshaw, S., Harpavat, S., Trimarchi, J., Cai, L., Huang, H., Kuo, W.P., Weber, G., Lee, K., Fraioli, R.E., Cho, S.H., Yung, R., Asch, E., Ohno-Machado, L., Wong, W.H. & Cepko, C.L. (2004) Genomic analysis of mouse retinal development. PLoS Biol., 2, E247.
15. Blackshaw, S., Scholpp, S., Placzek, M., Ingraham, H., Simerly, R. & Shimogori, T. (2010) Molecular pathways controlling development of thalamus and hypothalamus: from neural specification to circuit formation. J. Neurosci., 30, 14925-14930.
16. Bookout, A.L., Jeong, Y., Downes, M., Yu, R.T., Evans, R.M. & Mangelsdorf, D.J. (2006) Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell, 126, 789-799.
17. Breda, E., Cavaghan, M.K., Toffolo, G., Polonsky, K.S. & Cobelli, C. (2001) Oral glucose tolerance test minimal model indexes of beta-cell function and insulin sensitivity. Diabetes, 50, 150-158.
18. Briancon, N., McNay, D.E., Maratos-Flier, E. & Flier, J.S. (2010) Combined neural inactivation of suppressor of cytokine signaling-3 and protein-tyrosine phosphatase-1B reveals additive, synergistic, and factor-specific roles in the regulation of body energy balance. Diabetes, 59, 3074-3084.
19. Byerly, M.S., Simon, J., Lebihan-Duval, E., Duclos, M.J., Cogburn, L.A. & Porter, T.E. (2009) Effects of BDNF, T3, and corticosterone on expression of the hypothalamic obesity gene network in vivo and in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol., 296, R1180-R1189.
20. Caumo, A., Bergman, R.N. & Cobelli, C. (2000) Insulin sensitivity from meal tolerance tests in normal subjects: a minimal model index. J. Clin. Endocrinol. Metab., 85, 4396-4402.
21. Chen, J. & Nathans, J. (2007) Estrogen-related receptor beta/NR3B2 controls epithelial cell fate and endolymph production by the stria vascularis. Dev. Cell, 13, 325-337.
22. Cobelli, C., Toffolo, G.M., Dalla Man, C., Campioni, M., Denti, P., Caumo, A., Butler, P. & Rizza, R. (2007) Assessment of beta-cell function in humans, simultaneously with insulin sensitivity and hepatic extraction, from intravenous and oral glucose tests. Am. J. Physiol. Endocrinol. Metab., 293, E1-E15.
23. Dahlstrom, A. & Fuxe, K. (1964) Localization of monoamines in the lower brain stem. Experientia, 20, 398-399.
24. Dubois, N.C., Hofmann, D., Kaloulis, K., Bishop, J.M. & Trumpp, A. (2006) Nestin-Cre transgenic mouse line Nes-Cre1 mediates highly efficient Cre/loxP mediated recombination in the nervous system, kidney, and somite-derived tissues. Genesis, 44, 355-360.
25. Dumont, Y., Martel, J.C., Fournier, A., St-Pierre, S. & Quirion, R. (1992) Neuropeptide Y and neuropeptide Y receptor subtypes in brain and peripheral tissues. Prog. Neurobiol., 38, 125-167.
26. Dunbar, J.C., Ergene, E. & Barraco, R.A. (1992) Neuropeptide-Y stimulation of insulin secretion is mediated via the nucleus tractus solitarius. Horm. Metab. Res., 24, 103-105.
27. Ertl, P., Rohde, B. & Selzer, P. (2000) Fast calculation of molecular polar surface area as a sum of fragment-based contributions and its application to the prediction of drug transport properties. J. Med. Chem., 43, 3714-3717.
28. Feng, J.Q., Scott, G., Guo, D., Jiang, B., Harris, M., Ward, T., Ray, M., Bonewald, L.F., Harris, S.E. & Mishina, Y. (2008) Generation of a conditional null allele for Dmp1 in mouse. Genesis, 46, 87-91.
29. Fox, E.A. & Byerly, M.S. (2004) A mechanism underlying mature-onset obesity: evidence from the hyperphagic phenotype of brain-derived neurotrophic factor mutants. Am. J. Physiol. Regul. Integr. Comp. Physiol., 286, R994-R1004.
30. Giguere, V. (2008) Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr. Rev., 29, 677-696.
31. Giguere, V., Yang, N., Segui, P. & Evans, R.M. (1988) Identification of a new class of steroid hormone receptors. Nature, 331, 91-94.
32. Gofflot, F., Chartoire, N., Vasseur, L., Heikkinen, S., Dembele, D., Le Merrer, J. & Auwerx, J. (2007) Systematic gene expression mapping clusters nuclear receptors according to their function in the brain. Cell, 131, 405-418.
33. Grill, H.J. (2006) Distributed neural control of energy balance: contributions from hindbrain and hypothalamus. Obesity (Silver Spring), 14(Suppl 5), 216S-221S.
34. Grill, H.J. & Kaplan, J.M. (2002) The neuroanatomical axis for control of energy balance. Front. Neuroendocrin., 23, 2-40.
35. Grill, H.J., Schwartz, M.W., Kaplan, J.M., Foxhall, J.S., Breininger, J. & Baskin, D.G. (2002) Evidence that the caudal brainstem is a target for the inhibitory effect of leptin on food intake. Endocrinology, 143, 239-246.
36. Hayashi, S., Lewis, P., Pevny, L. & McMahon, A.P. (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev., 119(Suppl 1), S97-S101.
37. Hayes, M.R., Skibicka, K.P., Leichner, T.M., Guarnieri, D.J., DiLeone, R.J., Bence, K.K. & Grill, H.J. (2010) Endogenous leptin signaling in the caudal nucleus tractus solitarius and area postrema is required for energy balance regulation. Cell Metab., 11, 77-83.
38. Herzog, B., Cardenas, J., Hall, R.K., Villena, J.A., Budge, P.J., Giguere, V., Granner, D.K. & Kralli, A. (2006) Estrogen-related receptor alpha is a repressor of phosphoenolpyruvate carboxykinase gene transcription. J. Biol. Chem., 281, 99-106.
39. Hetherington, A. & Ranson, S. (1983) Nutrition Classics. The Anatomical Record, Volume 78, 1940: Hypothalamic lesions and adiposity in the rat. Nutr. Rev., 41, 124-127.
40. Kelder, J., Grootenhuis, P.D., Bayada, D.M., Delbressine, L.P. & Ploemen, J.P. (1999) Polar molecular surface as a dominating determinant for oral absorption and brain penetration of drugs. Pharm. Res., 16, 1514-1519.
41. Kopin, A.S., Mathes, W.F., McBride, E.W., Nguyen, M., Al-Haider, W., Schmitz, F., Bonner-Weir, S., Kanarek, R. & Beinborn, M. (1999) The cholecystokinin-A receptor mediates inhibition of food intake yet is not essential for the maintenance of body weight. J. Clin. Invest., 103, 383-391.
42. Lein, E.S., Hawrylycz, M.J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A.F., Boguski, M.S., Brockway, K.S., Byrnes, E.J., Chen, L., Chen, T.M., Chin, M.C., Chong, J., Crook, B.E., Czaplinska, A., Dang, C.N., Datta, S., Dee, N.R., Desaki, A.L., Desta, T., Diep, E., Dolbeare, T.A., Donelan, M.J., Dong, H.W., Dougherty, J.G., Duncan, B.J., Ebbert, A.J., Eichele, G., Estin, L.K., Faber, C., Facer, B.A., Fields, R., Fischer, S.R., Fliss, T.P., Frensley, C., Gates, S.N., Glattfelder, K.J., Halverson, K.R., Hart, M.R., Hohmann, J.G., Howell, M.P., Jeung, D.P., Johnson, R.A., Karr, P.T., Kawal, R., Kidney, J.M., Knapik, R.H., Kuan, C.L., Lake, J.H., Laramee, A.R., Larsen, K.D., Lau, C., Lemon, T.A., Liang, A.J., Liu, Y., Luong, L.T., Michaels, J., Morgan, J.J., Morgan, R.J., Mortrud, M.T., Mosqueda, N.F., Ng, L.L., Ng, R., Orta, G.J., Overly, C.C., Pak, T.H., Parry, S.E., Pathak, S.D., Pearson, O.C., Puchalski, R.B., Riley, Z.L., Rockett, H.R., Rowland, S.A., Royall, J.J., Ruiz, M.J., Sarno, N.R., Schaffnit, K., Shapovalova, N.V., Sivisay, T., Slaughterbeck, C.R., Smith, S.C., Smith, K.A., Smith, B.I., Sodt, A.J., Stewart, N.N., Stumpf, K.R., Sunkin, S.M., Sutram, M., Tam, A., Teemer, C.D., Thaller, C., Thompson, C.L., Varnam, L.R., Visel, A., Whitlock, R.M., Wohnoutka, P.E., Wolkey, C.K., Wong, V.Y., Wood, M., Yaylaoglu, M.B., Young, R.C., Youngstrom, B.L., Yuan, X.F., Zhang, B., Zwingman, T.A. & Jones, A.R. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature, 445, 168-176.
43. Luo, J., Sladek, R., Bader, J.A., Matthyssen, A., Rossant, J. & Giguere, V. (1997) Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature, 388, 778-782.
44. Luo, J., Sladek, R., Carrier, J., Bader, J.A., Richard, D. & Giguere, V. (2003) Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol. Cell. Biol., 23, 7947-7956.
45. Mayer, J. (1953) Glucostatic mechanism of regulation of food intake. N. Engl. J. Med., 249, 13-16.
46. Muniyappa, R.L.S., Chen, H. & Quon, M.J. (2008) Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. Am. J. Physiol. Endocrinol. Metab., 294, 15-26.
47. Onishi, A., Peng, G.H., Poth, E.M., Lee, D.A., Chen, J., Alexis, U., de Melo, J., Chen, S. & Blackshaw, S. (2010) The orphan nuclear hormone receptor ERRbeta controls rod photoreceptor survival. Proc. Natl. Acad. Sci. USA, 107, 11579-11584.
48. Ritter, S., Dinh, T.T. & Zhang, Y. (2000) Localization of hindbrain glucoreceptive sites controlling food intake and blood glucose. Brain Res., 856, 37-47.
49. Ritter, S., Dinh, T.T. & Li, A.J. (2006) Hindbrain catecholamine neurons control multiple glucoregulatory responses. Physiol. Behav., 89, 490-500.
50. Rushing, P.A., Houpt, T.A., Henderson, R.P. & Gibbs, J. (1997) High lick rate is maintained throughout spontaneous liquid meals in freely feeding rats. Physiol. Behav., 62, 1185-1188.
51. Shimogori, T., Lee, D.A., Miranda-Angulo, A., Yang, Y., Wang, H., Jiang, L., Yoshida, A.C., Kataoka, A., Mashiko, H., Avetisyan, M., Qi, L., Qian, J. & Blackshaw, S. (2010) A genomic atlas of mouse hypothalamic development. Nat. Neurosci., 13, 767-775.
52. Smith, G.P. (1996) The direct and indirect controls of meal size. Neurosci. Biobehav. Rev., 20, 41-46.
53. Trapp, T. & Holsboer, F. (1996) Nuclear orphan receptor as a repressor of glucocorticoid receptor transcriptional activity. J. Biol. Chem., 271, 9879-9882.
54. Tronche, F., Kellendonk, C., Kretz, O., Gass, P., Anlag, K., Orban, P.C., Bock, R., Klein, R. & Schutz, G. (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet., 23, 99-103.
55. Vanacker, J.M., Pettersson, K., Gustafsson, J.A. & Laudet, V. (1999) Transcriptional targets shared by estrogen receptor- related receptors (ERRs) and estrogen receptor (ER) alpha, but not by ERbeta. EMBO J., 18, 4270-4279.
56. Visel, A., Thaller, C. & Eichele, G. (2004) GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res., 32, D552-D556.
57. Yu, D.D. & Forman, B.M. (2005) Identification of an agonist ligand for estrogen-related receptors ERRbeta/gamma. Bioorg. Med. Chem. Lett., 15, 1311-1313.