Deletion of Mecp2 in Sim1-Expressing Neurons Reveals a Critical Role for MeCP2 in Feeding Behavior, Aggression, and the Response to Stress

Neuron

Volumn 59, Issue 6, 2008, Pages 947-958

  Fyffe, Sharyl L ^a   Neul, Jeff L ^a   Samaco, Rodney C ^a   Chao, Hsiao Tuan ^a   Ben Shachar, Shay ^a   Moretti, Paolo ^a   McGill, Bryan E ^a   Goulding, Evan H ^b   Sullivan, Elinor ^b   Tecott, Laurence H ^b   Zoghbi, Huda Y ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

HUMDISEASE; MOLNEURO; SYSNEURO

Indexed keywords

METHYL CPG BINDING PROTEIN 2;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN MAPPING; BRAIN REGION; CONTROLLED STUDY; FEEDING BEHAVIOR; GENE; GENE DELETION; GENE EXPRESSION; HYPOTHALAMUS; METHYL CPG BINDING PROTEIN 2 GENE; MOUSE; NERVE CELL; NONHUMAN; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; RETT SYNDROME; SIM1 GENE; SOCIAL BEHAVIOR; STRESS;

ADAPTATION, PSYCHOLOGICAL; ADIPOSITY; AGGRESSION; ANIMALS; APPETITE REGULATION; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FEEDING BEHAVIOR; GENE DELETION; GENETIC ENGINEERING; HYPOTHALAMUS; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; NEURONS; REPRESSOR PROTEINS; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 52049126415     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.07.030     Document Type: Article

References (62)

1. Axelrod F.B., Chelimsky G.G., and Weese-Mayer D.E. Pediatric autonomic disorders. Pediatrics 118 (2006) 309-321
2. Balthasar N., Dalgaard L.T., Lee C.E., Yu J., Funahashi H., Williams T., Ferreira M., Tang V., McGovern R.A., Kenny C.D., et al. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123 (2005) 493-505
3. Bourin M., and Hascoet M. The mouse light/dark box test. Eur. J. Pharmacol. 463 (2003) 55-65
4. Carson J.P., Thaller C., and Eichele G. A transcriptome atlas of the mouse brain at cellular resolution. Curr. Opin. Neurobiol. 12 (2002) 562-565
5. Carson J.P., Eichele G., and Chiu W. A method for automated detection of gene expression required for the establishment of a digital transcriptome-wide gene expression atlas. J. Microsc. 217 (2005) 275-281
6. Chahrour M., and Zoghbi H.Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 56 (2007) 422-437
7. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., and Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320 (2008) 1224-1229
8. Chang Q., Khare G., Dani V., Nelson S., and Jaenisch R. The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49 (2006) 341-348
9. Chen R.Z., Akbarian S., Tudor M., and Jaenisch R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27 (2001) 327-331
10. Chen W.G., Chang Q., Lin Y., Meissner A., West A.E., Griffith E.C., Jaenisch R., and Greenberg M.E. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302 (2003) 885-889
11. Chen P., Williams S.M., Grove K.L., and Smith M.S. Melanocortin 4 receptor-mediated hyperphagia and activation of neuropeptide Y expression in the dorsomedial hypothalamus during lactation. J. Neurosci. 24 (2004) 5091-5100
12. Cohen D., Lazar G., Couvert P., Desportes V., Lippe D., Mazet P., and Heron D. MECP2 mutation in a boy with language disorder and schizophrenia. Am. J. Psychiatry 159 (2002) 148-149
13. Couvert P., Bienvenu T., Aquaviva C., Poirier K., Moraine C., Gendrot C., Verloes A., Andres C., Le Fevre A.C., Souville I., et al. MECP2 is highly mutated in X-linked mental retardation. Hum. Mol. Genet. 10 (2001) 941-946
14. Gemelli T., Berton O., Nelson E.D., Perrotti L.I., Jaenisch R., and Monteggia L.M. Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biol. Psychiatry 59 (2006) 468-476
15. Glaze D.G. Neurophysiology of Rett syndrome. J. Child Neurol. 20 (2005) 740-746
16. Guan X.M., Yu H., Trumbauer M., Frazier E., Van der Ploeg L.H., and Chen H. Induction of neuropeptide Y expression in dorsomedial hypothalamus of diet-induced obese mice. Neuroreport 9 (1998) 3415-3419
17. Guy J., Hendrich B., Holmes M., Martin J.E., and Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27 (2001) 322-326
18. Hagberg B. Clinical manifestations and stages of Rett syndrome. Ment. Retard. Dev. Disabil. Res. Rev. 8 (2002) 61-65
19. Haskell-Luevano C., and Monck E.K. Agouti-related protein functions as an inverse agonist at a constitutively active brain melanocortin-4 receptor. Regul. Pept. 99 (2001) 1-7
20. 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
21. Kesterson R.A., Huszar D., Lynch C.A., Simerly R.B., and Cone R.D. Induction of neuropeptide Y gene expression in the dorsal medial hypothalamic nucleus in two models of the agouti obesity syndrome. Mol. Endocrinol. 11 (1997) 630-637
22. Kleefstra T., Yntema H.G., Oudakker A.R., Romein T., Sistermans E., Nillessen W., van Bokhoven H., de Vries B.B., and Hamel B.C. De novo MECP2 frameshift mutation in a boy with moderate mental retardation, obesity and gynaecomastia. Clin. Genet. 61 (2002) 359-362
23. Klein M.E., Lioy D.T., Ma L., Impey S., Mandel G., and Goodman R.H. Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat. Neurosci. 10 (2007) 1513-1514
24. Koizumi H., Hashimoto K., and Iyo M. Dietary restriction changes behaviours in brain-derived neurotrophic factor heterozygous mice: role of serotonergic system. Eur. J. Neurosci. 24 (2006) 2335-2344
25. Kublaoui B.M., Holder Jr. J.L., Tolson K.P., Gemelli T., and Zinn A.R. SIM1 overexpression partially rescues agouti yellow and diet-induced obesity by normalizing food intake. Endocrinology 147 (2006) 4542-4549
26. Lu X.Y., Barsh G.S., Akil H., and Watson S.J. Interaction between alpha-melanocyte-stimulating hormone and corticotropin-releasing hormone in the regulation of feeding and hypothalamo-pituitary-adrenal responses. J. Neurosci. 23 (2003) 7863-7872
27. Lubrano-Berthelier C., Dubern B., Lacorte J.M., Picard F., Shapiro A., Zhang S., Bertrais S., Hercberg S., Basdevant A., Clement K., and Vaisse C. Melanocortin 4 receptor mutations in a large cohort of severely obese adults: prevalence, functional classification, genotype-phenotype relationship, and lack of association with binge eating. J. Clin. Endocrinol. Metab. 91 (2006) 1811-1818
28. Lyons W.E., Mamounas L.A., Ricaurte G.A., Coppola V., Reid S.W., Bora S.H., Wihler C., Koliatsos V.E., and Tessarollo L. Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc. Natl. Acad. Sci. USA 96 (1999) 15239-15244
29. Martinowich K., Hattori D., Wu H., Fouse S., He F., Hu Y., Fan G., and Sun Y.E. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302 (2003) 890-893
30. McGill B.E., Bundle S.F., Yaylaoglu M.B., Carson J.P., Thaller C., and Zoghbi H.Y. Enhanced anxiety and stress-induced corticosterone release are associated with increased Crh expression in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. USA 103 (2006) 18267-18272
31. Moretti P., and Zoghbi H.Y. MeCP2 dysfunction in Rett syndrome and related disorders. Curr. Opin. Genet. Dev. 16 (2006) 276-281
32. Moretti P., Bouwknecht J.A., Teague R., Paylor R., and Zoghbi H.Y. Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum. Mol. Genet. 14 (2005) 205-220
33. Motil K.J., Schultz R.J., Browning K., Trautwein L., and Glaze D.G. Oropharyngeal dysfunction and gastroesophageal dysmotility are present in girls and women with Rett syndrome. J. Pediatr. Gastroenterol. Nutr. 29 (1999) 31-37
34. Motil K.J., Schultz R.J., Abrams S., Ellis K.J., and Glaze D.G. Fractional calcium absorption is increased in girls with Rett syndrome. J. Pediatr. Gastroenterol. Nutr. 42 (2006) 419-426
35. Mount R.H., Charman T., Hastings R.P., Reilly S., and Cass H. The Rett Syndrome Behaviour Questionnaire (RSBQ): refining the behavioural phenotype of Rett syndrome. J. Child Psychol. Psychiatry 43 (2002) 1099-1110
36. Nicholson J.R., Peter J.C., Lecourt A.C., Barde Y.A., and Hofbauer K.G. Melanocortin-4 receptor activation stimulates hypothalamic brain-derived neurotrophic factor release to regulate food intake, body temperature and cardiovascular function. J. Neuroendocrinol. 19 (2007) 974-982
37. Nuber U.A., Kriaucionis S., Roloff T.C., Guy J., Selfridge J., Steinhoff C., Schulz R., Lipkowitz B., Ropers H.H., Holmes M.C., and Bird A. Up-regulation of glucocorticoid-regulated genes in a mouse model of Rett syndrome. Hum. Mol. Genet. 14 (2005) 2247-2256
38. Oswal A., and Yeo G.S. The leptin melanocortin pathway and the control of body weight: lessons from human and murine genetics. Obes. Rev. 8 (2007) 293-306
39. Rios M., Fan G., Fekete C., Kelly J., Bates B., Kuehn R., Lechan R.M., and Jaenisch R. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol. Endocrinol. 15 (2001) 1748-1757
40. Samaco R.C., Fryer J.D., Ren J., Fyffe S., Chao H.T., Sun Y., Greer J.J., Zoghbi H.Y., and Neul J.L. A partial loss of function allele of methyl-CpG-binding protein predicts a human neurodevelopmental syndrome. Hum. Mol. Genet. 17 (2008) 1718-1727
41. Schwartz M.W., Seeley R.J., Woods S.C., Weigle D.S., Campfield L.A., Burn P., and Baskin D.G. Leptin increases hypothalamic pro-opiomelanocortin mRNA expression in the rostral arcuate nucleus. Diabetes 46 (1997) 2119-2123
42. Shahbazian M., Young J., Yuva-Paylor L., Spencer C., Antalffy B., Noebels J., Armstrong D., Paylor R., and Zoghbi H. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35 (2002) 243-254
43. Shahbazian M.D., Sun Y., and Zoghbi H.Y. Balanced X chromosome inactivation patterns in the Rett syndrome brain. Am. J. Med. Genet. 111 (2002) 164-168
44. Spencer C.M., Alekseyenko O., Serysheva E., Yuva-Paylor L.A., and Paylor R. Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav. 4 (2005) 420-430
45. Spencer C.M., Serysheva E., Yuva-Paylor L.A., Oostra B.A., Nelson D.L., and Paylor R. Exaggerated behavioral phenotypes in Fmr1/Fxr2 double knockout mice reveal a functional genetic interaction between Fragile X-related proteins. Hum. Mol. Genet. 15 (2006) 1984-1994
46. Stephens T.W., Basinski M., Bristow P.K., Bue-Valleskey J.M., Burgett S.G., Craft L., Hale J., Hoffmann J., Hsiung H.M., Kriauciunas A., et al. The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature 377 (1995) 530-532
47. Takagi N. The role of X-chromosome inactivation in the manifestation of Rett syndrome. Brain Dev. 23 Suppl 1 (2001) S182-S185
48. Tsao D., Thomsen H.K., Chou J., Stratton J., Hagen M., Loo C., Garcia C., Sloane D.L., Rosenthal A., and Lin J.C. TrkB agonists ameliorate obesity and associated metabolic conditions in mice. Endocrinology 149 (2008) 1038-1048
49. Unger T.J., Calderon G.A., Bradley L.C., Sena-Esteves M., and Rios M. Selective deletion of Bdnf in the ventromedial and dorsomedial hypothalamus of adult mice results in hyperphagic behavior and obesity. J. Neurosci. 27 (2007) 14265-14274
50. Visel A., Thaller C., and Eichele G. GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res. 32 (2004) D552-D556
51. Wade J.M., Juneja P., MacKay A.W., Graham J., Havel P.J., Tecott L.H., and Goulding E.H. Synergistic impairment of glucose homeostasis in ob/ob mice lacking functional serotonin 2C receptors. Endocrinology 149 (2008) 955-961
52. Wang C., Bomberg E., Billington C., Levine A., and Kotz C.M. Brain-derived neurotrophic factor in the hypothalamic paraventricular nucleus reduces energy intake. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R1003-R1012
53. Weaving L.S., Williamson S.L., Bennetts B., Davis M., Ellaway C.J., Leonard H., Thong M.K., Delatycki M., Thompson E.M., Laing N., and Christodoulou J. Effects of MECP2 mutation type, location and X-inactivation in modulating Rett syndrome phenotype. Am. J. Med. Genet. A. 118A (2003) 103-114
54. Weaving L.S., Ellaway C.J., Gecz J., and Christodoulou J. Rett syndrome: clinical review and genetic update. J. Med. Genet. 42 (2005) 1-7
55. Williamson S.L., and Christodoulou J. Rett syndrome: new clinical and molecular insights. Eur. J. Hum. Genet. 14 (2006) 896-903
56. Xu B., Goulding E.H., Zang K., Cepoi D., Cone R.D., Jones K.R., Tecott L.H., and Reichardt L.F. Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor. Nat. Neurosci. 6 (2003) 736-742
57. Yasui D.H., Peddada S., Bieda M.C., Vallero R.O., Hogart A., Nagarajan R.P., Thatcher K.N., Farnham P.J., and Lasalle J.M. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl. Acad. Sci. USA 104 (2007) 19416-19421
58. Yaylaoglu M.B., Titmus A., Visel A., Alvarez-Bolado G., Thaller C., and Eichele G. Comprehensive expression atlas of fibroblast growth factors and their receptors generated by a novel robotic in situ hybridization platform. Dev. Dyn. 234 (2005) 371-386
59. Young D., Nagarajan L., de Klerk N., Jacoby P., Ellaway C., and Leonard H. Sleep problems in Rett syndrome. Brain Dev. 29 (2007) 609-616
60. Zappella M., Meloni I., Longo I., Hayek G., and Renieri A. Preserved speech variants of the Rett syndrome: molecular and clinical analysis. Am. J. Med. Genet. 104 (2001) 14-22
61. Zhou Z., Hong E.J., Cohen S., Zhao W.N., Ho H.Y., Schmidt L., Chen W.G., Lin Y., Savner E., Griffith E.C., et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52 (2006) 255-269
62. Zoghbi H.Y. MeCP2 dysfunction in humans and mice. J. Child Neurol. 20 (2005) 736-740