Adolescence fluoxetine increases serotonergic activity in the raphe-hippocampus axis and improves depression-like behaviors in female rats that experienced neonatal maternal separation

Psychoneuroendocrinology

Volumn 38, Issue 6, 2013, Pages 777-788

  Yoo, Sang Bae ^a   Kim, Bom Taeck ^b   Kim, Jin Young ^a   Ryu, Vitaly ^a   Kang, Dong Won ^c   Lee, Jong Ho ^a   Jahng, Jeong Won ^a  

^a Seoul National University   (South Korea)

^b Ajou University School of Medicine   (South Korea)

^c Kwandong University College of Medicine   (South Korea)

Author keywords

Depression; Eating disorders; Food intake; Neonatal maternal separation; Serotonin; Stress

Indexed keywords

CORTICOSTERONE; FLUOXETINE;

ADOLESCENT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANORECTIC ACTIVITY; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DRUG ACTIVITY; EXPERIMENTAL TEST; FEMALE; FOOD INTAKE; FORCED SWIMMING TEST; HIPPOCAMPUS; HYPOTHALAMUS; MATERNAL DEPRIVATION; MAZE TEST; NEUROCHEMISTRY; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PERINATAL PERIOD; PRIORITY JOURNAL; RAPHE NUCLEUS; RAT; SEROTONINERGIC SYSTEM; SWIMMING; WEIGHT GAIN;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BODY WEIGHT; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DEPRESSION; EATING; EATING DISORDERS; FEMALE; FLUOXETINE; HIPPOCAMPUS; HYPOTHALAMUS; MATERNAL DEPRIVATION; RAPHE NUCLEI; RATS; SEROTONERGIC NEURONS; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SEROTONIN UPTAKE INHIBITORS;

EID: 84877060636     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.08.013     Document Type: Article

References (60)

1. Ansorge M.S., Morelli E., Gingrich J.A. Inhibition of serotonin but not norepinephrine transport during development produces delayed, persistent perturbations of emotional behaviors in mice. J. Neurosci. 2008, 28:199-207.
2. Barna I., Bálint E., Baranyi J., Bakos N., Makara G.B., Haller J. Gender-specific effect of maternal deprivation on anxiety and corticotrophin-releasing hormone mRNA expression in rats. Brain Res. Bull. 2003, 62:85-91.
3. Benekareddy M., Vadodaria K.C., Nair A.R., Vaidya V.A. Postnatal serotonin type 2 receptor blockade prevents the emergence of anxiety behavior, dysregulated stress-induced immediate early gene responses, and specific transcriptional changes that arise following early life stress. Biol. Psychiatry 2011, 70:1024-1032.
4. Bhagwagar Z., Whale R., Cowen P.J. State and trait abnormalities in serotonin function in major depression. Br. J. Psychiatry 2002, 180:24-28.
5. Branchi I. The double edged sword of neural plasticity: increasing serotonin levels leads to both greater vulnerability to depression and improved capacity to recover. Psychoneuroendocrinology 2011, 36:339-351.
6. Choi S.H., Kwon B.S., Lee S., Houpt T.A., Lee H.T., Jahng J.W. Systemic 5-hydroxy-l-tryptophan down-regulates the arcuate CART mRNA level in rats. Regul. Pept. 2003, 115:73-80.
7. Daniels W.M., Pietersen C.Y., Carstens M.E., Stein D.J. Maternal separation in rats lead to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab. Brain Dis. 2004, 19:3-14.
8. Dedic N., Touma C., Romanowski C.P., Schieven M., Kühne C., Ableitner M., Lu A., Holsboer F., Wurst W., Kimura M., Deussing J.M. Assessing behavioural effects of chronic HPA axis activation using conditional CRH-overexpressing mice. Cell. Mol. Neurobiol. 2012, 32:815-828.
9. Desbonnet L., Garrett L., Daly E., McDermott K.W., Dinan T.G. Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain. Int. J. Dev. Neurosci. 2008, 26:259-268.
10. Dulawa S.C., Holick K.A., Gundersen B., Hen R. Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 2004, 29:1321-1330.
11. Fairburn C.G., Harrison P.J. Eating disorders. Lancet 2003, 361:407-416.
12. Gluck M.E., Geliebter A., Lorence M. Cortisol stress response is positively correlated with central obesity in obese women with binge eating disorder (BED) before and after cognitive-behavioral treatment. Ann. N. Y. Acad. Sci. 2004, 1032:202-207.
13. Goodman W.K., Murphy T.K., Storch E.A. Risk of adverse behavioral effects with pediatric use of antidepressants. Psychopharmacology 2007, 191:87-96.
14. Goossens L., Braet C., Van Vlierberghe L., Mels S. Loss of control over eating in overweight youngsters: the role of anxiety, depression and emotional eating. Eur. Eat. Disord. Rev. 2009, 17:68-78.
15. Halbreich U., Kahn L. Atypical depression, somatic depression and anxious depression in women: are they gender-preferred phenotypes?. J. Affect. Disord. 2007, 102:245-258.
16. Heisler L.K., Jobst E.E., Sutton G.M., Zhou L., Borok E., Thornton-Jones Z., Liu H.Y., Zigman J.M., Balthasar N., Kishi T., Lee C.E., Aschkenasi C.J., Zhang C.Y., Yu J., Boss O., Mountjoy K.G., Clifton P.G., Lowell B.B., Friedman J.M., Horvath T., Butler A.A., Elmquist J.K., Cowley M.A. Serotonin reciprocally regulates melanocortin neurons to modulate food intake. Neuron 2006, 51:239-249.
17. Howland R.H. Induction of mania with serotonin reuptake inhibitors. J. Clin. Psychopharmacol. 1996, 16:425-427.
18. Iwasaki S., Inoue K., Kiriike N., Hikiji K. Effect of maternal separation on feeding behavior of rats in later life. Physiol. Behav. 2000, 70:551-556.
19. Jahng J.W. Animal model of eating disorders associated with stressful experience in early life. Horm. Behav. 2011, 59:213-220.
20. Jahng J.W., Houpt T.A., Joh T.H., Son J.H. Differential expression of monoamine oxidase A, serotonin transporter, tyrosine hydroxylase and norepinephrine transporter mRNA by anorexia mutation and food deprivation. Dev. Brain Res. 1998, 107:241-246.
21. Jahng J.W., Ryu V., Yoo S.B., Noh S.J., Kim J.Y., Lee J.H. Mesolimbic dopaminergic activity responding to acute stress is blunted in adolescent rats that experienced neonatal maternal separation. Neuroscience 2010, 171:144-152.
22. Javaras K.N., Pope H.G., Lalonde J.K., Roberts J.L., Nillni Y.I., Laird N.M., Bulik C.M., Crow S.J., McElroy S.L., Walsh B.T., Tsuang M.T., Rosenthal N.R., Hudson J.I. Co-occurrence of binge eating disorder with psychiatric and mental disorders. J. Clin. Psychiatry 2008, 69:266-273.
23. Kalinichev M., Easterling K.W., Plotsky P.M., Holtzman S.G. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharm. Biochem. Behav. 2002, 73:131-140.
24. Khoury A.E., Gruber S.H.M., Mork A., Mathe A.A. Adult life behavioral consequences of early maternal separation are alleviated by escitalopram treatment in a rat model of depression. Prog. Neuro-Psychopharmacol. Biol. Psychiatr. 2006, 30:535-540.
25. Kim H.J., Lee J.H., Choi S.H., Lee Y.S., Jahng J.W. Fasting-induced increases of arcuate NPY mRNA and plasma corticosterone are blunted in the rat experienced neonatal maternal separation. Neuropeptides 2005, 39:587-594.
26. Kobayashi K., Ikeda Y., Haneda E., Suzuki H. Chronic fluoxetine bidirectionally modulates potentiating effects of serotonin on the hippocampal mossy fiber synaptic transmission. J. Neurosci. 2008, 28:6272-6280.
27. Kobayashi K., Ikeda Y., Sakai A., Yamasaki N., Haneda E., Miyakawa T., Suzuki H. Reversal of hippocampal neuronal maturation by serotonergic antidepressants. Proc. Natl. Acad. Sci. USA 2010, 107:8434-8439.
28. Kobayashi K., Ikeda Y., Suzuki H. Behavioral destabilization induced by the selective serotonin reuptake inhibitor fluoxetine. Mol. Brain 2011, 4(12). 10.1186/1756-6606-4-12.
29. Kohl Z., Winner B., Ubhi K., Rockenstein E., Mante M., Münch M., Barlow C., Carter T., Masliah E., Winkler J. Fluoxetine rescues impaired hippocampal neurogenesis in a transgenic A53T synuclein mouse model. Eur. J. Neurosci. 2012, 35:10-19.
30. Lajud N., Roque A., Cajero M., Gutiérrez-Ospina G., Torner L. Periodic maternal separation decreases hippocampal neurogenesis without affecting basal corticosterone during the stress hyporesponsive period, but alters HPA axis and coping behavior in adulthood. Psychoneuroendocrinology 2012, 37:410-420.
31. Leibowitz S.F., Alexander J.T. Hypothalamic serotonin in control of eating behavior, meal size, and body weight. Biol. Psychiatry 1998, 44:851-864.
32. Lee J.H., Cha M.J., Choi S.H., Hwang S.J., Kim D., Jahng J.W. Neuropeptide Y immunoreactivity and corticotropin-releasing hormone mRNA level are increased in the hypothalamus of mouse bearing a human oral squamous cell carcinoma. Neuropeptides 2004, 38:345-350.
33. Lee J.H., Kim H.J., Kim J.G., Ryu V., Kim B.T., Kang D.W., Jahng J.W. Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci. Res. 2007, 58:32-39.
34. Lehmann J., Pryce C.R., Bettschen D., Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 1999, 64:705-715.
35. Lowry C.A., Hale M.W., Plant A., Windle R.J., Shanks N., Wood S.A., Ingram C.D., Renner K.J., Lightman S.L., Summers C.H. Fluoxetine inhibits corticotropin-releasing factor (CRF)-induced behavioural responses in rats. Stress 2009, 12:225-239.
36. Lowy M.T., Reder A.T., Antel J.P., Meltzer H.Y. Glucocorticoid resistance in depression: the dexamethasone suppression test and lymphocyte sensitivity to dexamethasone. Am. J. Psychiatry 1984, 141:1365-1370.
37. Lukkes J.L., Watt M.J., Lowry C.A., Foster G.L. Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front. Behav. Neurosci. 2009, 3:18.
38. MacMillan H.L., Fleming J.E., Streiner D.L., Lin E., Boyle M.H., Jamieson E., Duku E.K., Walsh C.A., Wong M.Y., Beardslee W.R. Childhood abuse and lifetime psychopathology in a community sample. Am. J. Psychiatry 2001, 158:1878-1883.
39. Maniam J., Morris M.J. Voluntary exercise and palatable high-fat diet both improve behavioral profile and stress response in male rats exposed to early life stress: role of hippocampus. Psychoneuroendocrinology 2010, 35:1553-1564.
40. Maniam J., Morris M.J. Palatable cafeteria diet ameliorates anxiety and depression-like symptoms following an adverse early environment. Psychoneuroendocrinology 2010, 35:717-728.
41. Matthews K., Dalley J.W., Matthews C., Tsai T.H., Robbins T.W. Periodic maternal separation of neonatal rats produces region- and gender-specific effects on biogenic amine content in postmortem adult brain. Synapse 2001, 40:1-10.
42. Mclntosh J., Animan H., Merali Z. Short- and long periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res. Dev. Brain Res. 1999, 113:97-106.
43. Myung C.S., Kim B.T., Choi S.H., Song G.Y., Lee S.Y., Jahng J.W. Role of neuropeptide Y and proopiomelanocortin in fluoxetine-induced anorexia. Arch. Pharm. Res. 2005, 28:716-721.
44. Nutt D.J. Neurobiological mechanisms in generalized anxiety disorder. J. Clin. Psychiatry 2001, 62(Suppl. 11):22-27.
45. Oh J.E., Zupan B., Gross S., Toth M. Paradoxical anxiogenic response of juvenile mice to fluoxetine. Neuropsychopharmacology 2009, 34:2197-2207.
46. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinate 1986, Academic Press, New York.
47. Peeters F., Nicolson N.A., Berkhof J. Levels and variability of daily life cortisol secretion in major depression. Psychiatry Res. 2004, 126:1-13.
48. Placidi R.J., Chandler P.C., Oswald K.D., Maldonado C., Wauford P.K., Boggiano M.M. Stress and hunger alter the anorectic efficacy of fluoxetine in binge-eating rats with a history of caloric restriction. Int. J. Eat. Disord. 2004, 36:328-341.
49. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
50. Putignano P., Dubini A., Toja P., Invitti C., Bonfanti S., Redaelli G., Zappulli D., Cavagnini F. Salivary cortisol measurement in normal-weight, obese and anorexic women: comparison with plasma cortisol. Eur. J. Endocrinol. 2001, 145:165-171.
51. Renard G.M., Rivarola M.A., Suarez M.M. Sexual dimorphism in rats: effects of early maternal separation and variable chronic stress on pituitary-adrenal axis and behavior. Int. J. Dev. Neurosci. 2007, 25:373-379.
52. Rüedi-Bettschen D., Feldon J., Pryce C.R. Circadian- and temperature-specific effects of early deprivation on rat maternal care and pup development: short-term markers for long-term effects?. Dev. Psychobiol. 2004, 45:59-71.
53. Ryu V., Lee J.H., Yoo S.B., Gu X.F., Moon Y.W., Jahng J.W. Sustained hyperphagia in adolescent rats that experienced neonatal maternal separation. Int. J. Obes. 2008, 32:1355-1362.
54. Ryu V., Yoo S.B., Kang D.W., Lee J.H., Jahng J.W. Post-weaning isolation promotes food intake and body weight gain in rats that experienced neonatal maternal separation. Brain Res. 2009, 1295:127-134.
55. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
56. Shea A., Walsh C., Macmillan H., Steiner M. Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 2005, 30:162-178.
57. Slotten H.A., Kalinichev M., Hagan J.J., Marsden C.A., Fone K.C.F. Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Res. 2006, 1097:123-132.
58. Vazquez D.M., Lopez J.F., van Hoers H., Watson S.J., Levin S. Maternal deprivation regulates serotonin 1A and 2A receptors in the infant rat. Brain Res. 2000, 855:76-82.
59. Ward A.S., Comer S.D., Haney M., Fischman M.W., Foltin R.W. Fluoxetine-maintained obese humans: effect on food intake and body weight. Physiol. Behav. 1999, 66:815-821.
60. Yoo S.B., Ryu V., Park E.Y., Kim B.T., Kang D.W., Lee J.H., Jahng J.W. The arcuate NPY, POMC, and CART expressions responding to food deprivation are exaggerated in young female rats that experienced neonatal maternal separation. Neuropeptides 2011, 45:343-349.