Long-lasting behavioural and molecular alterations induced by early postnatal fluoxetine exposure are restored by chronic fluoxetine treatment in adult mice

European Neuropsychopharmacology

Volumn 19, Issue 2, 2009, Pages 97-108

  Karpova, Nina N ^a   Lindholm, Jesse ^a   Pruunsild, Priit ^b   Timmusk, Tõnis ^b   Castrén, Eero ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b TALLINN UNIVERSITY OF TECHNOLOGY   (Estonia)

Author keywords

Antidepressant drugs; Brain derived neurotrophic factor; Epigenetics; Postnatal development; Serotonin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FLUOXETINE; HISTONE H3; MESSENGER RNA; NEUROTROPHIN; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; DEPRESSION; DRUG RECEPTOR BINDING; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; PERINATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROMOTER REGION; TREATMENT DURATION;

ANIMALS; ANIMALS, NEWBORN; ANXIETY; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN CHEMISTRY; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHROMATIN; DARKNESS; DEPRESSION; EXPLORATORY BEHAVIOR; FLUOXETINE; HIPPOCAMPUS; IMMUNOPRECIPITATION; LIGHT; MALE; MICE; MICE, INBRED C57BL; RECEPTOR, TRKB; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEROTONIN UPTAKE INHIBITORS; SWIMMING;

EID: 57749181777     PISSN: 0924977X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2008.09.002     Document Type: Article

References (74)

1. Aid T., Kazantseva A., Piirsoo M., Palm K., and Timmusk T. Mouse and rat BDNF gene structure and expression revisited. J. Neurosci. Res. 85 (2007) 525-535
2. Ansorge M.S., Zhou M., Lira A., Hen R., and Gingrich J.A. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 306 (2004) 879-881
3. Ansorge M.S., Hen R., and Gingrich J.A. Neurodevelopmental origins of depressive disorders. Curr. Opin. Pharmacol. 7 (2007) 8-17
4. Ansorge M.S., Morelli E., and Gingrich J.A. Inhibition of serotonin but not norepinephrine transport during development produces delayed, persistent perturbations of emotional behaviors in mice. J. Neurosci. 28 (2008) 199-207
5. Bernstein B.E., Meissner A., and Lander E.S. The mammalian epigenome. Cell 128 (2007) 669-681
6. Berton O., and Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7 (2006) 137-151
7. Cases O., Lebrand C., Giros B., Vitalis T., De Maeyer E., Caron M.G., Price D.J., Gaspar P., and Seif I. Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knock-outs. J. Neurosci. 18 (1998) 6914-6927
8. Castren E. Neurotrophic effects of antidepressant drugs. Curr. Opin. Pharmacol. 4 (2004) 58-64
9. Castren E. Is mood chemistry?. Nat. Rev. Neurosci. 6 (2005) 241-246
10. Castren E., Voikar V., and Rantamaki T. Role of neurotrophic factors in depression. Curr. Opin. Pharmacol. 7 (2007) 18-21
11. Chakrabarti S.K., James J.C., and Mirmira R.G. Quantitative assessment of gene targeting in vitro and in vivo by the pancreatic transcription factor, Pdx1. Importance of chromatin structure in directing promoter binding. J. Biol. Chem. 277 (2002) 13286-13293
12. Chen Z.Y., Jing D., Bath K.G., Ieraci A., Khan T., Siao C.J., Herrera D.G., Toth M., Yang C., McEwen B.S., Hempstead B.L., and Lee F.S. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314 (2006) 140-143
13. Cryan J.F., Markou A., and Lucki I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol. Sci. 23 (2002) 238-245
14. Czeh B., Muller-Keuker J.I., Rygula R., Abumaria N., Hiemke C., Domenici E., and Fuchs E. Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology 32 (2007) 1490-1503
15. D'Souza D.N., Zhang Y., Garcia F., Battaglia G., and Van de Kar L.D. Fluoxetine-induced changes in body weight and 5-HT1A receptor-mediated hormone secretion in rats on a tryptophan-deficient diet. Am. J. Physiol., Regul. Integr. Comp. Physiol. 286 (2004) R390-397
16. Dulawa S.C., and Hen R. Recent advances in animal models of chronic antidepressant effects: the novelty-induced hypophagia test. Neurosci. Biobehav. Rev. 29 (2005) 771-783
17. Duman R.S. Depression: a case of neuronal life and death?. Biol. Psychiatry 56 (2004) 140-145
18. Duman R.S., and Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59 (2006) 1116-1127
19. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., Zaitsev E., Gold B., Goldman D., Dean M., Lu B., and Weinberger D.R. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112 (2003) 257-269
20. Eyal R., and Yaeger D. Poor neonatal adaptation after in utero exposure to duloxetine. Am. J. Psychiatry 165 (2008) 651
21. Felsenfeld G., and Groudine M. Controlling the double helix. Nature 421 (2003) 448-453
22. Ferreira E., Carceller A.M., Agogue C., Martin B.Z., St-Andre M., Francoeur D., and Berard A. Effects of selective serotonin reuptake inhibitors and venlafaxine during pregnancy in term and preterm neonates. Pediatrics 119 (2007) 52-59
23. Gamaro G.D., Prediger M.E., Lopes J., Bassani M.G., and Dalmaz C. Fluoxetine alters feeding behavior and leptin levels in chronically-stressed rats. Pharmacol. Biochem. Behav. 90 (2008) 312-317
24. Gaspar P., Cases O., and Maroteaux L. The developmental role of serotonin: news from mouse molecular genetics. Nat. Rev. Neurosci. 4 (2003) 1002-1012
25. Gentile S. Serotonin reuptake inhibitor-induced perinatal complications. Paediatr. Drugs 9 (2007) 97-106
26. Gingrich J.A., and Hen R. Dissecting the role of the serotonin system in neuropsychiatric disorders using knockout mice. Psychopharmacology (Berl) 155 (2001) 1-10
27. Gross C., and Hen R. The developmental origins of anxiety. Nat. Rev. Neurosci. 5 (2004) 545-552
28. Gross C., Zhuang X., Stark K., Ramboz S., Oosting R., Kirby L., Santarelli L., Beck S., and Hen R. Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature 416 (2002) 396-400
29. Holmes A., Yang R.J., Murphy D.L., and Crawley J.N. Evaluation of antidepressant-related behavioral responses in mice lacking the serotonin transporter. Neuropsychopharmacology 27 (2002) 914-923
30. Holmes A., Lit Q., Murphy D.L., Gold E., and Crawley J.N. Abnormal anxiety-related behavior in serotonin transporter null mutant mice: the influence of genetic background. Genes Brain Behav. 2 (2003) 365-380
31. Homberg J.R., Olivier J.D., Smits B.M., Mul J.D., Mudde J., Verheul M., Nieuwenhuizen O.F., Cools A.R., Ronken E., Cremers T., Schoffelmeer A.N., Ellenbroek B.A., and Cuppen E. Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system. Neuroscience 146 (2007) 1662-1676
32. Homberg J.R., Pattij T., Janssen M.C., Ronken E., De Boer S.F., Schoffelmeer A.N., and Cuppen E. Serotonin transporter deficiency in rats improves inhibitory control but not behavioural flexibility. Eur. J. Neurosci. 26 (2007) 2066-2073
33. Koponen E., Rantamaki T., Voikar V., Saarelainen T., MacDonald E., and Castren E. Enhanced BDNF signaling is associated with an antidepressant-like behavioral response and changes in brain monoamines. Cell. Mol. Neurobiol. 25 (2005) 973-980
34. Koren G., Matsui D., Einarson A., Knoppert D., and Steiner M. Is maternal use of selective serotonin reuptake inhibitors in the third trimester of pregnancy harmful to neonates?. CMAJ 172 (2005) 1457-1459
35. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
36. Kumar A., Choi K.H., Renthal W., Tsankova N.M., Theobald D.E., Truong H.T., Russo S.J., Laplant Q., Sasaki T.S., Whistler K.N., Neve R.L., Self D.W., and Nestler E.J. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48 (2005) 303-314
37. LaRoche R.B., and Morgan R.E. Adolescent fluoxetine exposure produces enduring, sex-specific alterations of visual discrimination and attention in rats. Neurotoxicol. Teratol. 29 (2007) 96-107
38. Lebrand C., Cases O., Adelbrecht C., Doye A., Alvarez C., El Mestikawy S., Seif I., and Gaspar P. Transient uptake and storage of serotonin in developing thalamic neurons. Neuron 17 (1996) 823-835
39. Lebrand C., Cases O., Wehrle R., Blakely R.D., Edwards R.H., and Gaspar P. Transient developmental expression of monoamine transporters in the rodent forebrain. J. Comp. Neurol. 401 (1998) 506-524
40. Lira A., Zhou M., Castanon N., Ansorge M.S., Gordon J.A., Francis J.H., Bradley-Moore M., Lira J., Underwood M.D., Arango V., Kung H.F., Hofer M.A., Hen R., and Gingrich J.A. Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Biol. Psychiatry 54 (2003) 960-971
41. Maciag D., Williams L., Coppinger D., and Paul I.A. Neonatal citalopram exposure produces lasting changes in behavior which are reversed by adult imipramine treatment. Eur. J. Pharmacol. 532 (2006) 265-269
42. Martinowich K., and Lu B. Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology 33 (2008) 73-83
43. 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
44. Mattson M.P., Maudsley S., and Martin B. BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 27 (2004) 589-594
45. Maya Vetencourt J.F., Sale A., Viegi A., Baroncelli L., De Pasquale R., O'Leary O.F., Castren E., and Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320 (2008) 385-388
46. Mostert J.P., Koch M.W., Heerings M., Heersema D.J., and De Keyser J. Therapeutic potential of fluoxetine in neurological disorders. CNS Neurosci. Ther. 14 (2008) 153-164
47. Murphy D.L., Li Q., Engel S., Wichems C., Andrews A., Lesch K.P., and Uhl G. Genetic perspectives on the serotonin transporter. Brain Res. Bull. 56 (2001) 487-494
48. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., and Monteggia L.M. Neurobiology of depression. Neuron 34 (2002) 13-25
49. Nibuya M., Morinobu S., and Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 15 (1995) 7539-7547
50. Nishimura H., Tsuda A., Oguchi M., Ida Y., and Tanaka M. Is immobility of rats in the forced swim test "behavioral despair"?. Physiol. Behav. 42 (1988) 93-95
51. Olivier J.D., Van Der Hart M.G., Van Swelm R.P., Dederen P.J., Homberg J.R., Cremers T., Deen P.M., Cuppen E., Cools A.R., and Ellenbroek B.A. A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience 152 (2008) 573-584
52. Onishchenko N., Karpova N., Sabri F., Castren E., and Ceccatelli S. Long-lasting depression-like behavior and epigenetic changes of BDNF gene expression induced by perinatal exposure to methylmercury. J. Neurochem. 106 (2008) 1378-1387
53. Owens M.J., and Nemeroff C.B. The serotonin transporter and depression. Depress. Anxiety 8 (1998) 5-12 Suppl 1
54. Porsolt R.D., Le Pichon M., and Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 266 (1977) 730-732
55. Rantamaki T., Hendolin P., Kankaanpaa A., Mijatovic J., Piepponen P., Domenici E., Chao M.V., Mannisto P.T., and Castren E. Pharmacologically diverse antidepressants rapidly activate brain-derived neurotrophic factor receptor TrkB and induce phospholipase-Cgamma signaling pathways in mouse brain. Neuropsychopharmacology 32 (2007) 2152-2162
56. Russo-Neustadt A., Beard R.C., and Cotman C.W. Exercise, antidepressant medications, and enhanced brain derived neurotrophic factor expression. Neuropsychopharmacology 21 (1999) 679-682
57. Saarelainen T., Hendolin P., Lucas G., Koponen E., Sairanen M., MacDonald E., Agerman K., Haapasalo A., Nawa H., Aloyz R., Ernfors P., and Castren E. Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J. Neurosci. 23 (2003) 349-357
58. Sairanen M., Lucas G., Ernfors P., Castren M., and Castren E. Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J. Neurosci. 25 (2005) 1089-1094
59. Sairanen M., O'Leary O.F., Knuuttila J.E., and Castren E. Chronic antidepressant treatment selectively increases expression of plasticity-related proteins in the hippocampus and medial prefrontal cortex of the rat. Neuroscience 144 (2007) 368-374
60. Schule C., Zill P., Baghai T.C., Eser D., Zwanzger P., Wenig N., Rupprecht R., and Bondy B. Brain-derived neurotrophic factor Val66Met polymorphism and dexamethasone/CRH test results in depressed patients. Psychoneuroendocrinology 31 (2006) 1019-1025
61. Silhol M., Bonnichon V., Rage F., and Tapia-Arancibia L. Age-related changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats. Neuroscience 132 (2005) 613-624
62. Tao X., Finkbeiner S., Arnold D.B., Shaywitz A.J., and Greenberg M.E. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20 (1998) 709-726
63. Ter Horst P.G., Jansman F.G., van Lingen R.A., Smit J.P., de Jong-van den Berg L.T., and Brouwers J.R. Pharmacological aspects of neonatal antidepressant withdrawal. Obstet. Gynecol. Surv. 63 (2008) 267-279
64. Tervonen T.A., Ajamian F., De Wit J., Verhaagen J., Castren E., and Castren M. Overexpression of a truncated TrkB isoform increases the proliferation of neural progenitors. Eur. J. Neurosci. 24 (2006) 1277-1285
65. Tsankova N.M., Berton O., Renthal W., Kumar A., Neve R.L., and Nestler E.J. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9 (2006) 519-525
66. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., and Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 7 (2004) 847-854
67. West A.P. Neurobehavioral studies of forced swimming: the role of learning and memory in the forced swim test. Prog. Neuropsychopharmacol. Biol. Psychiatry 14 (1990) 863-877
68. Westbroek I., Waarsing J.H., van Leeuwen J.P., Waldum H., Reseland J.E., Weinans H., Syversen U., and Gustafsson B.I. Long-term fluoxetine administration does not result in major changes in bone architecture and strength in growing rats. J. Cell. Biochem. 101 (2007) 360-368
69. Whitaker-Azmitia P.M. Serotonin and brain development: role in human developmental diseases. Brain Res. Bull. 56 (2001) 479-485
70. Vitalis T., Cases O., Callebert J., Launay J.M., Price D.J., Seif I., and Gaspar P. Effects of monoamine oxidase A inhibition on barrel formation in the mouse somatosensory cortex: determination of a sensitive developmental period. J. Comp. Neurol. 393 (1998) 169-184
71. Vogel G., Neill D., Hagler M., and Kors D. A new animal model of endogenous depression: a summary of present findings. Neurosci. Biobehav. Rev. 14 (1990) 85-91
72. Yan W., Wilson C.C., and Haring J.H. 5-HT1a receptors mediate the neurotrophic effect of serotonin on developing dentate granule cells. Brain Res. Dev. Brain Res. 98 (1997) 185-190
73. Yan W., Wilson C.C., and Haring J.H. Effects of neonatal serotonin depletion on the development of rat dentate granule cells. Brain Res. Dev. Brain Res. 98 (1997) 177-184
74. Yen T.T., Wong D.T., and Bemis K.G. Reduction of food consumption and body weight of normal and obese mice by chronic treatment with fluoxetine: a serotonin reuptake inhibitor. Drug Dev. Res. 10 (1987) 37-47