Estrogens stimulate serotonin neurons to inhibit binge-like eating in mice

Journal of Clinical Investigation

Volumn 124, Issue 10, 2014, Pages 4351-4362

  Cao, Xuehong ^a,b   Xu, Pingwen ^a   Oyola, Mario G ^a   Xia, Yan ^a   Yan, Xiaofeng ^a   Saito, Kenji ^a   Zou, Fang ^a   Wang, Chunmei ^a   Yang, Yongjie ^a   Hinton, Antentor ^a   Yan, Chunling ^a   Ding, Hongfang ^a   Zhu, Liangru ^a,c   Yu, Likai ^a   Yang, Bin ^d   Feng, Yuxin ^e,h   Clegg, Deborah J ^f   Khan, Sohaib ^e   Dimarchi, Richard ^d   Mani, Shaila K ^a   Tong, Qingchun ^g   Xu, Yong ^a   more..

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b WUHAN POLYTECHNIC UNIVERSITY   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d INDIANA UNIVERSITY   (United States)

^e UNIVERSITY OF CINCINNATI   (United States)

^f UNIVERSITY OF TEXAS AT DALLAS   (United States)

^g UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^h SPECTRUM HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; APAMIN; CONJUGATED ESTROGEN; ESTROGEN RECEPTOR ALPHA; GLUCAGON LIKE PEPTIDE 1; SEROTONIN; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; ESTROGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINGE EATING DISORDER; CELL ACTIVATION; CONDITIONED TASTE AVERSION TEST; CONJUGATE; CONTROLLED STUDY; DEPOLARIZATION; DORSAL RAPHE NUCLEUS; DRUG CONJUGATION; DRUG TARGETING; ESTROGEN ACTIVITY; FEMALE; HORMONAL THERAPY; MEMBRANE STEADY POTENTIAL; MOUSE; NONHUMAN; PSYCHOPHARMACOLOGY; PSYCHOPHARMACOTHERAPY; SEROTONINERGIC NERVE CELL; AGONISTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FEEDING BEHAVIOR; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; NERVE CELL; RAPHE NUCLEUS;

ANIMALS; BINGE-EATING DISORDER; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEEDING BEHAVIOR; FEMALE; GLUCAGON-LIKE PEPTIDE 1; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; NEURONS; RAPHE NUCLEI; SEROTONIN;

EID: 84907495482     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI74726     Document Type: Article

References (53)

1. Hudson JI, Hiripi E, Pope HG, Pope HG Jr, Kessler RC. The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry. 2007;61(3):348-358.
2. Mitchell JE, Mussell MP. Comorbidity and binge eating disorder. Addict Behav. 1995;20(6):725-732.
3. Patrick L. Eating disorders: a review of the literature with emphasis on medical complications and clinical nutrition. Altern Med Rev. 2002;7(3):184-202.
4. Whitaker AH. An epidemiological study of anorectic and bulimic symptoms in adolescent girls: implications for pediatricians. Pediatr Ann. 1992;21(11):752-759.
5. Verri A, Nappi RE, Cecchini AP, Vallero E, Luzi S, Zara C. Eating disorders and Axis I psychiatric comorbidity in amenorrheic women. Int J Eat Disord. 1998;24(2):137-146.
6. Poyastro Pinheiro A, et al. Patterns of menstrual disturbance in eating disorders. Int J Eat Disord. 2007;40(5):424-434.
7. Lester NA, Keel PK, Lipson SF. Symptom fluctuation in bulimia nervosa: relation to menstrualcycle phase and cortisol levels. Psychol Med. 2003;33(1):51-60.
8. Gladis MM, Walsh BT. Premenstrual exacerbation of binge eating in bulimia. Am J Psychiatry. 1987;144(12):1592-1595.
9. Price WA, Torem MS, Di Marzio LR. Premenstrual exacerbation of bulimia. Psychosomatics. 1987;28(7):378-379.
10. Edler C, Lipson SF, Keel PK. Ovarian hormones and binge eating in bulimia nervosa. Psychol Med. 2007;37(1):131-141.
11. Klump KL, Keel PK, Culbert KM, Edler C. Ovarian hormones and binge eating: exploring associations in community samples. Psychol Med. 2008;38(12):1749-1757.
12. Klump KL, Suisman JL, Culbert KM, Kashy DA, Keel PK, Sisk CL. The effects of ovariectomy on binge eating proneness in adult female rats. Horm Behav. 2011;59(4):585-593.
13. Yu Z, Geary N, Corwin RL. Ovarian hormones inhibit fat intake under binge-type conditions in ovariectomized rats. Physiol Behav. 2008;95(3):501-507.
14. Jimerson DC, Lesem MD, Kaye WH, Hegg AP, Brewerton TD. Eating disorders and depression: is there a serotonin connection? Biol Psychiatry. 1990;28(5):443-454.
15. Monteleone P, Brambilla F, Bortolotti F, Maj M. Serotonergic dysfunction across the eating disorders: relationship to eating behaviour, purging behaviour, nutritional status and general psychopathology. Psychol Med. 2000;30(5):1099-1110.
16. Steiger H. Eating disorders and the serotonin connection: state, trait and developmental effects. J Psychiatry Neurosci. 2004;29(1):20-29.
17. Sabine EJ, Yonace A, Farrington AJ, Barratt KH, Wakeling A. Bulimia nervosa: a placebo controlled double-blind therapeutic trial of mianserin. Br J Clin Pharmacol. 1983;15(suppl 2):195S-202S.
18. Pope HG, Pope HG Jr, Hudson JI, Jonas JM, Yurgelun-Todd D. Bulimia treated with imipramine: a placebo-controlled, double-blind study. Am J Psychiatry. 1983;140(5):554-558.
19. Mitchell JE, Groat R. A placebo-controlled, double-blind trial of amitriptyline in bulimia. J Clin Psychopharmacol. 1984;4(4):186-193.
20. Walsh BT, Stewart JW, Roose SP, Gladis M, Glassman AH. Treatment of bulimia with phenelzine. A double-blind, placebo-controlled study. ArchGen Psychiatry. 1984;41(11):1105-1109.
21. Hughes PL, Wells LA, Cunningham CJ, Ilstrup DM. Treating bulimia with desipramine. A double-blind, placebo-controlled study. Arch Gen Psychiatry. 1986;43(2):182-186.
22. Barlow J, Blouin J, Blouin A, Perez E. Treatment of bulimia with desipramine: a doubleblind crossover study. Can J Psychiatry. 1988;33(2):129-133.
23. Rowland NE, Carlton J. Neurobiology of an anorectic drug: fenfluramine. Prog Neurobiol. 1986;27(1):13-62.
24. Stunkard A, Berkowitz R, Tanrikut C, Reiss E, Young L. d-fenfluramine treatment of binge eating disorder. Am J Psychiatry. 1996;153(11):1455-1459.
25. Blouin AG, Blouin JH, Perez EL, Bushnik T, Zuro C, Mulder E. Treatment of bulimia with fenfluramine and desipramine. J Clin Psychopharmacol. 1988;8(4):261-269.
26. Merchenthaler I, Lane MV, Numan S, Dellovade TL. Distribution of estrogen receptor alpha and beta in the mouse central nervous system: in vivo autoradiographic and immunocytochemical analyses. J Comp Neurol. 2004;473(2):270-291.
27. Dalmasso C, Amigone JL, Vivas L. Serotonergic system involvement in the inhibitory action of estrogen on induced sodium appetite in female rats. Physiol Behav. 2011;104(3):398-407.
28. Robichaud M, Debonnel G. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J Neuroendocrinol. 2005;17(3):179-185.
29. Czyzyk TA, Sahr AE, Statnick MA. A model of binge-like eating behavior in mice that does not require food deprivation or stress. Obesity (Silver Spring). 2010;18(9):1710-1717.
30. Feng Y, Manka D, Wagner KU, Khan SA. Estrogen receptor-alpha expression in the mammary epithelium is required for ductal and alveolar morphogenesis in mice. Proc Natl Acad Sci U S A. 2007;104(37):14718-14723.
31. Finan B, et al. Targeted estrogen delivery reverses the metabolic syndrome. Nat Med. 2012;18(12):1847-1856.
32. Gu G, Roland B, Tomaselli K, Dolman CS, Lowe C, Heilig JS. Glucagon-like peptide-1 in the rat brain: Distribution of expression and functional implication. J Comp Neurol. 2013;521(10):2235-2261.
33. Adelman JP, Maylie J, Sah P. Small-conductance Ca2+-activated K+ channels: form and function. Annu Rev Physiol. 2012;74:245-269.
34. Pagadala P, et al. Loss of NR1 subunit of NMDARs in primary sensory neurons leads to hyperexcitability and pain hypersensitivity: involvement of Ca (2+)-activated small conductance potassium channels. J Neurosci. 2013;33(33):13425-13430.
35. Asarian L, Geary N. Estradiol enhances cholecystokinin-dependent lipid-induced satiation and activates estrogen receptor-alpha-expressing cells in the nucleus tractus solitarius of ovariectomized rats. Endocrinology. 2007;148(12):5656-5666.
36. Drucker DJ. Minireview: the glucagon-like peptides. Endocrinology. 2001;142(2):521-527.
37. Dossat AM, Bodell LP, Williams DL, Eckel LA, Keel PK. Preliminary examination of glucagonlike peptide-1 levels in women with purging disorder and bulimia nervosa [published online ahead of print March 4, 2014]. Int J Eat Disord. doi:10.1002/eat.22264.
38. Naessen S, Carlstrom K, Holst JJ, Hellstrom PM, Hirschberg AL. Women with bulimia nervosa exhibit attenuated secretion of glucagonlike peptide 1, pancreatic polypeptide, and insulin in response to a meal. Am J Clin Nutr. 2011;94(4):967-972.
39. Santollo J, Wiley MD, Eckel LA. Acute activation of ER alpha decreases food intake, meal size, and body weight in ovariectomized rats. Am J Physiol Regul Integr Comp Physiol. 2007;293(6):R2194-R2201.
40. Santollo J, Katzenellenbogen BS, Katzenellenbogen JA, Eckel LA. Activation of ERα is necessary for estradiol's anorexigenic effect in female rats. Horm Behav. 2010;58(5):872-877.
41. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS. Increased adipose tissue in male and female estrogen receptor-α knockout mice. Proc Natl Acad Sci U S A. 2000;97(23):12729-12734.
42. Xu Y, et al. Distinct hypothalamic neurons mediate estrogenic effects on energy homeostasis and reproduction. Cell Metab. 2011;14(4):453-465.
43. Zhu L, et al. Steroid receptor coactivator-1 mediates estrogenic actions to prevent body weight gain in female mice. Endocrinology. 2013;154(1):150-158.
44. Xu Y, et al. PI3K signaling in the ventromedial hypothalamic nucleus is required for normal energy homeostasis. Cell Metab. 2010;12(1):88-95.
45. Cannon CM, Scannell CA, Palmiter RD. Mice lacking dopamine D1 receptors express normal lithium chloride-induced conditioned taste aversion for salt but not sucrose. Eur J Neurosci. 2005;21(9):2600-2604.
46. Oyola MG, et al. Anxiolytic effects and neuroanatomical targets of estrogen receptor-β (ERβ) activation by a selective ERβ agonist in female mice. Endocrinology. 2012;153(2):837-846.
47. Flaisher-Grinberg S, Einat H. A possible utilization of the mice forced swim test for modeling manic-like increase in vigor and goaldirected behavior. J Pharmacol Toxicol Methods. 2009;59(3):141-145.
48. Pechnick RN, Chesnokova VM, Kariagina A, Price S, Bresee CJ, Poland RE. Reduced immobility in the forced swim test in mice with a targeted deletion of the leukemia inhibitory factor (LIF) gene. Neuropsychopharmacology. 2004;29(4):770-776.
49. Poleszak E, et al. NMDA/glutamate mechanism of antidepressant-like action of magnesium in forced swim test in mice. Pharmacol Biochem Behav. 2007;88(2):158-164.
50. Hill JW, et al. Acute effects of leptin require PI3K signaling in hypothalamic proopiomelanocortin neurons in mice. J Clin Invest. 2008;118(5):1796-1805.
51. Ren H, et al. FoxO1 target Gpr17 activates AgRP neurons to regulate food intake. Cell. 2012;149(6):1314-1326.
52. Pinto S, et al. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science. 2004;304(5667):110-115.
53. Merlo S, Frasca G, Canonico PL, Sortino MA. Differential involvement of estrogen receptor alpha and estrogen receptor beta in the healing promoting effect of estrogen in human keratinocytes. J Endocrinol. 2009;200(2):189-197.