Dnmt3a in sim1 neurons is necessary for normal energy homeostasis

Journal of Neuroscience

Volumn 34, Issue 46, 2014, Pages 15288-15296

  Kohno, Daisuke ^a,c,d   Lee, Syann ^a   Harper, Matthew J ^a,b   Kim, Ki Woo ^a,e   Sone, Xhideyuki ^a,f   Sasaki, Tsutomu ^d   Kitamura, Tadahiro ^d   Fan, Guoping ^g   Elmquist, Joel K ^a  

^a Department of Internal Medicine   (United States)

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

^c Advanced Scientific Research Leaders Development Unit   (Japan)

^d GUNMA UNIVERSITY   (Japan)

^e Yonsei University Wonju College of Medicine   (South Korea)

^f UNIVERSITY OF NIIGATA PREFECTURE   (Japan)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA methylation; Dnmt3a; Epigenetics; Feeding; Hypothalamus; Obesity

Indexed keywords

DNA METHYLTRANSFERASE 3A; GALANIN; INSULIN; LEPTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; TYROSINE 3 MONOOXYGENASE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA (CYTOSINE 5) METHYLTRANSFERASE; REPRESSOR PROTEIN; SIM1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DNA METHYLATION; ENERGY EXPENDITURE; ENERGY HOMEOSTASIS; FEMALE; GENE EXPRESSION PROFILING; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; HYPERCHOLESTEROLEMIA; HYPERPHAGIA; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; INSULIN TOLERANCE TEST; LIPID DIET; LOCOMOTION; MALE; MICRO-COMPUTED TOMOGRAPHY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OBESITY; OXYGEN CONSUMPTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SINGLE MINDED 1 NEURON; UPREGULATION; ADIPOSE TISSUE; ANIMAL; BIOSYNTHESIS; BLOOD; COMPLICATION; ENERGY METABOLISM; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADIPOSE TISSUE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CHOLESTEROL, LDL; DIET, HIGH-FAT; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; ENERGY METABOLISM; FEMALE; GALANIN; GENE EXPRESSION PROFILING; GLUCOSE INTOLERANCE; HOMEOSTASIS; HYPERPHAGIA; INSULIN; LEPTIN; MALE; MICE; MICE, KNOCKOUT; NEURONS; OBESITY; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; REPRESSOR PROTEINS; TYROSINE 3-MONOOXYGENASE; UP-REGULATION;

EID: 84909979554     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1316-14.2014     Document Type: Article

References (68)

1. Akabayashi A, Koenig JI, Watanabe Y, Alexander JT, Leibowitz SF (1994) Galanin-containing neurons in the paraventricular nucleus: a neurochemical marker for fat ingestion and body weight gain. Proc Natl Acad Sci U S A 91:10375–10379.CrossRef Medline
2. Aran D, Sabato S, Hellman A (2013) DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol 14:R21.CrossRef Medline
3. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB (2005) Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123:493–505.CrossRef Medline
4. Bamshad M, Aoki VT, Adkison MG, Warren WS, Bartness TJ (1998) Central nervous system origins of the sympathetic nervous system outflow to white adipose tissue. Am J Physiol 275:R291–R299. Medline
5. Barker DJ (1997) Fetal nutrition and cardiovascular disease in later life. Br Med Bull 53:96-108.CrossRef Medline
6. Barker DJ, Osmond C (1986) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1:1077–1081.CrossRef Medline
7. Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH (1993) Growth in utero and serum cholesterol concentrations in adult life. BMJ 307:1524-1527.CrossRef Medline
8. Bartness TJ, Shrestha YB, Vaughan CH, Schwartz GJ, Song CK (2010) Sensory and sympathetic nervous system control of white adipose tissue lipolysis. Mol Cell Endocrinol 318:34–43.CrossRef Medline
9. Biag J, Huang Y, Gou L, Hintiryan H, Askarinam A, Hahn JD, Toga AW, Dong HW (2012) Cyto- and chemoarchitecture of the hypothalamic paraventricular nucleus in the C57BL/6J male mouse: a study of immunostaining and multiple fluorescent tract tracing. J Comp Neurol 520:6-33.CrossRef Medline
10. Chang GQ, Gaysinskaya V, Karatayev O, Leibowitz SF (2008) Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 28:12107–12119.CrossRef Medline
11. Clément K, Vaisse C, Lahlou N, Cabrol S, Pelloux V, Cassuto D, Gourmelen M, Dina C, Chambaz J, Lacorte JM, Basdevant A, Bougnéres P, Lebouc Y, Froguel P, Guy-Grand B (1998) A mutation in the human leptin receptor gene causes obesity and pituitary dysfunction. Nature 392:398–401.CrossRef Medline
12. Cordero P, Milagro FI, Campion J, Martinez JA (2013) Maternal methyl donors supplementation during lactation prevents the hyperhomocysteinemia induced by a high-fat-sucrose intake by dams. Int J Mol Sci 14:24422–24437.CrossRef Medline
13. Dodge JE, Okano M, Dick F, Tsujimoto N, Chen T, Wang S, Ueda Y, Dyson N, Li E (2005) Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J Biol Chem 280:17986-17991.CrossRef Medline
14. Dudas B, Baker M, Rotoli G, Grignol G, Bohn MC, Merchenthaler I (2010) Distribution and morphology of the catecholaminergic neural elements in the human hypothalamus. Neuroscience 171:187–195.CrossRef Medline
15. Elliott E, Ezra-Nevo G, Regev L, Neufeld-Cohen A, Chen A (2010) Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat Neurosci 13:1351–1353.CrossRef Medline
16. Enriori PJ, Evans AE, Sinnayah P, Jobst EE, Tonelli-Lemos L, Billes SK, Glavas MM, Grayson BE, Perello M, Nillni EA, Grove KL, Cowley MA (2007) Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons. Cell Metab 5:181–194.CrossRef Medline
17. Feil R, Fraga MF (2011) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13:97–109.CrossRef Medline
18. Foster MT, Song CK, Bartness TJ (2010) Hypothalamic paraventricular nucleus lesion involvement in the sympathetic control of lipid mobilization. Obesity (Silver Spring) 18:682-689. CrossRef
19. Fujikawa T, Matsumura S, Yamada H, Inoue K, Fushiki T (2007) Transforming growth factor-beta in the brain enhances fat oxidation via noradrenergic neurons in the ventromedial and paraventricular hypothalamic nucleus. Brain Res 1173:92–101.CrossRef Medline
20. Fyffe SL, Neul JL, Samaco RC, Chao HT, Ben-Shachar S, Moretti P, McGill BE, Goulding EH, Sullivan E, Tecott LH, Zoghbi HY (2008) Deletion of Mecp2 in Sim1-expressing neurons reveals a critical role for MeCP2 in feeding behavior, aggression, and the response to stress. Neuron 59:947-958.CrossRef Medline
21. Grissom N, Bowman N, Reyes TM (2014) Epigenetic programming of reward function in offspring: a role for maternal diet. Mammalian Genome 25:41-48.CrossRef Medline
22. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151–180.CrossRef Medline
23. Hinney A, Vogel CI, Hebebrand J (2010) From monogenic to polygenic obesity: recent advances. Eur Child Adolesc Psychiatry 19:297–310.CrossRef Medline
24. Iwata N, Kobayashi K, Sasaoka T, Hidaka H, Nagatsu T (1992) Structure of the mouse tyrosine hydroxylase gene. Biochem Biophys Res Commun 182:348-354.CrossRef Medline
25. Jirtle RL, Skinner MK (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8:253–262.CrossRef Medline
26. Kamei Y, Suganami T, Ehara T, Kanai S, Hayashi K, Yamamoto Y, Miura S, Ezaki O, Okano M, Ogawa Y (2010) Increased expression ofDNAmethyltransferase 3a in obese adipose tissue: studies with transgenic mice. Obesity (Silver Spring) 18:314-321.CrossRef Medline
27. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H (2004) Essential role for de novoDNAmethyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900-903.CrossRef Medline
28. Kim KW, Donato J Jr, Berglund ED, Choi YH, Kohno D, Elias CF, Depinho RA, Elmquist JK (2012) FOXO1 in the ventromedial hypothalamus regulates energy balance. J Clin Invest 122:2578-2589.CrossRef Medline
29. Kofler B, Liu ML, Jacoby AS, Shine J, Iismaa TP (1996) Molecular cloning and characterisation of the mouse preprogalanin gene. Gene 182:71–75.CrossRef Medline
30. Krude H, Biebermann H, Luck W, Horn R, Brabant G, Grüters A (1998) Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat Genet 19:155–157.CrossRef Medline
31. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827–1830.CrossRef Medline
32. LaPlant Q, Vialou V, Covington HE III, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, Iñiguez SD, Koo JW, Mouzon E, Renthal W, Hollis F, Wang H, Noonan MA, Ren Y, Eisch AJ, Bolaños CA, Kabbaj M, et al. (2010) Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 13:1137–1143.CrossRef Medline
33. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204-220.CrossRef Medline
34. Leibowitz SF (1978) Paraventricular nucleus: a primary site mediating adrenergic stimulation of feeding and drinking. Pharmacol Biochem Behav 8:163–175.CrossRef Medline
35. Leibowitz SF, Roland CR, Hor L, Squillari V (1984) Noradrenergic feeding elicited via the paraventricular nucleus is dependent upon circulating corticosterone. Physiol Behav 32:857-864.CrossRef Medline
36. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133–140.CrossRef Medline
37. Meguid MM, Fetissov SO, Varma M, Sato T, Zhang L, Laviano A, Rossi- Fanelli F (2000) Hypothalamic dopamine and serotonin in the regulation of food intake. Nutrition 16:843-857.CrossRef Medline
38. Meister B, Elde R (1993) Dopamine transportermRNAin neurons of the rat hypothalamus. Neuroendocrinology 58:388-395.CrossRef Medline
39. Misawa K, Kanazawa T, Misawa Y, Uehara T, Imai A, Takahashi G, Takebayashi S, Cole A, Carey TE, Mineta H (2013) Galanin has tumor suppressor activity and is frequently inactivated by aberrant promoter methylation in head and neck cancer. Transl Oncol 6:338-346.CrossRef Medline
40. Montague CT, Farooqi IS, Whitehead JP, Soos MA, Rau H, Wareham NJ, Sewter CP, Digby JE, Mohammed SN, Hurst JA, Cheetham CH, Earley AR, Barnett AH, Prins JB, O’Rahilly S (1997) Congenital leptin deficiency is associated with severe early-onset obesity in humans. Nature 387:903–908.CrossRef Medline
41. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmühl Y, Fischer D, Holsboer F, Wotjak CT, Almeida OF, Spengler D (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12:1559-1566.CrossRef Medline
42. Okuse K, Matsuoka I, Kurihara K (1997) Tissue-specific methylation occurs in the essential promoter element of the tyrosine hydroxylase gene. Brain Res Mol Brain Res 46:197–207.CrossRef Medline
43. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
44. Perez-Tilve D, Hofmann SM, Basford J, Nogueiras R, Pfluger PT, Patterson JT, Grant E, Wilson-Perez HE, Granholm NA, Arnold M, Trevaskis JL, Butler AA, Davidson WS, Woods SC, Benoit SC, Sleeman MW, DiMarchi RD, Hui DY, Tschöp MH (2010) Melanocortin signaling in the CNS directly regulates circulating cholesterol. Nat Neurosci 13:877-882.CrossRef Medline
45. Plagemann A, Harder T, Lindner R, Melchior K, Rake A, Rittel F, Rohde W, Dörner G (1998) Alterations of hypothalamic catecholamines in the newborn offspring of gestational diabetic mother rats. Brain Res Dev Brain Res 109:201–209.CrossRef Medline
46. Püschel GP (2004) Control of hepatocyte metabolism by sympathetic and parasympathetic hepatic nerves. Anat Rec A Discov Mol Cell Evol Biol 280:854–867. Medline
47. Ravelli GP, Stein ZA, Susser MW (1976) Obesity in young men after famine exposure in utero and early infancy. N Eng J Med 295:349-353.CrossRef Medline
48. Ruggiero DA, Baker H, Joh TH, Reis DJ (1984) Distribution of catecholamine neurons in the hypothalamus and preoptic region of mouse. J Comp Neurol 223:556-582.CrossRef Medline
49. Sandovici I, Smith NH, Nitert MD, Ackers-Johnson M, Uribe-Lewis S, Ito Y, Jones RH, Marquez VE, Cairns W, Tadayyon M, O’Neill LP, Murrell A, Ling C, Constância M, Ozanne SE (2011) Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc Natl Acad Sci U S A 108:5449-5454.CrossRef Medline
50. Sharma D, Bhave S, Gregg E, Uht R (2013) Dexamethasone induces a putative repressor complex and chromatin modifications in the CRH promoter. Mol Endocrinol 27:1142–1152.CrossRef Medline
51. Shi YC, Lau J, Lin Z, Zhang H, Zhai L, Sperk G, Heilbronn R, Mietzsch M, Weger S, Huang XF, Enriquez RF, Baldock PA, Zhang L, Sainsbury A, Herzog H, Lin S (2013) Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN. Cell Metab 17:236-248.CrossRef Medline
52. Stanley BG, Schwartz DH, Hernandez L, Hoebel BG, Leibowitz SF (1989) Patterns of extracellular norepinephrine in the paraventricular hypothalamus: relationship to circadian rhythm and deprivation-induced eating behavior. Life Sci 45:275–282. Medline
53. Stanley S, Pinto S, Segal J, Pérez CA, Viale A, DeFalco J, Cai X, Heisler LK, Friedman JM (2010) Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically. Proc Natl Acad Sci U S A 107:7024-7029.CrossRef Medline
54. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN (1988) Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37:1163–1167.CrossRef Medline
55. Swanson LW, Sawchenko PE (1980) Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 31:410–417.CrossRef Medline
56. Tatton-Brown K, Seal S, Ruark E, Harmer J, Ramsay E, Del Vecchio Duarte S, Zachariou A, Hanks S, O’Brien E, Aksglaede L, Baralle D, Dabir T, Gener B, Goudie D, Homfray T, Kumar A, Pilz DT, Selicorni A, Temple IK, Van Maldergem L, et al. (2014) Mutations in the DNA methyltransferase gene DNMT3A cause an overgrowth syndrome with intellectual disability. Nat Genet 46:385–388.CrossRef Medline
57. Vaisse C, Clement K, Durand E, Hercberg S, Guy-Grand B, Froguel P (2000) Melanocortin-4 receptor mutations are a frequent and heterogeneous cause of morbid obesity. J Clin Invest 106:253–262.CrossRef Medline
58. Volkow ND, Wang GJ, Baler RD (2011) Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci 15:37-46.CrossRef Medline
59. Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM (2010) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151:4756–4764.CrossRef Medline
60. Vucetic Z, Carlin JL, Totoki K, Reyes TM (2012) Epigenetic dysregulation of the dopamine system in diet-induced obesity. J Neurochem 120:891-898.CrossRef Medline
61. Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23:5293-5300.CrossRef Medline
62. Wiench M, John S, Baek S, Johnson TA, Sung MH, Escobar T, Simmons CA, Pearce KH, Biddie SC, Sabo PJ, Thurman RE, Stamatoyannopoulos JA, Hager GL (2011) DNA methylation status predicts cell type-specific enhancer activity. EMBO J 30:3028-3039.CrossRef Medline
63. Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329:444–448.CrossRef Medline
64. Xu Y, Jones JE, Kohno D, Williams KW, Lee CE, Choi MJ, Anderson JG, Heisler LK, Zigman JM, Lowell BB, Elmquist JK (2008) 5-HT2CRs expressed by pro-opiomelanocortin neurons regulate energy homeostasis. Neuron 60:582–589.CrossRef Medline
65. Yeo GS, Heisler LK (2012) Unraveling the brain regulation of appetite: lessons from genetics. Nat Neurosci 15:1343–1349.CrossRef Medline
66. Yeo GS, Farooqi IS, Aminian S, Halsall DJ, Stanhope RG, O’Rahilly S (1998) A frameshift mutation in MC4R associated with dominantly inherited human obesity. Nat Genet 20:111–112.CrossRef Medline
67. Yura S, Itoh H, Sagawa N, Yamamoto H, Masuzaki H, Nakao K, Kawamura M, Takemura M, Kakui K, Ogawa Y, Fujii S (2005) Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab 1:371–378.CrossRef Medline
68. Zhou QY, Palmiter RD (1995) Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 83:1197–1209.CrossRef Medline