Antidepressant Acts on Astrocytes Leading to an Increase in the Expression of Neurotrophic/Growth Factors: Differential Regulation of FGF-2 by Noradrenaline

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Kajitani, Naoto ^a,b   Hisaoka Nakashima, Kazue ^a   Morioka, Norimitsu ^a   Okada Tsuchioka, Mami ^b   Kaneko, Masahiro ^a   Kasai, Miho ^a   Shibasaki, Chiyo ^b   Nakata, Yoshihiro ^a   Takebayashi, Minoru ^b  

^a HIROSHIMA UNIVERSITY   (Japan)

^b NATIONAL HOSPITAL ORGANIZATION KURE MEDICAL CENTER AND CHUGOKU CANCER CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; AMITRIPTYLINE; BETA ADRENERGIC RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CLOMIPRAMINE; CYCLOHEXIMIDE; DIAZEPAM; DULOXETINE; FIBROBLAST GROWTH FACTOR 2; FLUVOXAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; HALOPERIDOL; MESSENGER RNA; NERVE GROWTH FACTOR; NORADRENALIN; TRIHEXYPHENIDYL; VASCULOTROPIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN CORTEX; CONTROLLED STUDY; INHIBITION KINETICS; NERVE CELL CULTURE; NERVE CELL STIMULATION; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RAT; REAL TIME POLYMERASE CHAIN REACTION;

AMITRIPTYLINE; ANIMALS; ANTIDEPRESSIVE AGENTS; ASTROCYTES; BIOGENIC MONOAMINES; CELLS, CULTURED; CEREBRAL CORTEX; CYCLOHEXIMIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; HIPPOCAMPUS; NERVE GROWTH FACTORS; NEURONS; NOREPINEPHRINE; PSYCHOTROPIC DRUGS; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, ALPHA; RECEPTORS, ADRENERGIC, BETA; RNA, MESSENGER;

RATTUS;

EID: 84870788182     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051197     Document Type: Article

References (63)

1. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, et al. (2002) Neurobiology of depression. Neuron 34: 13-25.
2. Duman RS, Monteggia LM, (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59: 1116-1127.
3. Chen F, Madsen TM, Wegener G, Nyengaard JR, (2010) Imipramine treatment increases the number of hippocampal synapses and neurons in a genetic animal model of depression. Hippocampus 20: 1376-1384.
4. Malberg JE, (2004) Implications of adult hippocampal neurogenesis in antidepressant action. J Psychiatry Neurosci 29: 196-205.
5. Evans SJ, Choudary PV, Neal CR, Li JZ, Vawter MP, et al. (2004) Dysregulation of the fibroblast growth factor system in major depression. Proc Natl Acad Sci U S A 101: 15506-15511.
6. Chen B, Dowlatshahi D, MacQueen GM, Wang JF, Young LT, (2001) Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biol Psychiatry 50: 260-265.
7. Brunoni AR, Lopes M, Fregni F, (2008) A systematic review and meta-analysis of clinical studies on major depression and BDNF levels: implications for the role of neuroplasticity in depression. Int J Neuropsychopharmacol 11: 1169-1180.
8. Zhang X, Zhang Z, Xie C, Xi G, Zhou H, et al. (2008) Effect of treatment on serum glial cell line-derived neurotrophic factor in depressed patients. Prog Neuropsychopharmacol Biol Psychiatry 32: 886-890.
9. Nibuya M, Morinobu S, Duman RS, (1995) Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15: 7539-7547.
10. Mallei A, Shi B, Mocchetti I, (2002) Antidepressant treatments induce the expression of basic fibroblast growth factor in cortical and hippocampal neurons. Mol Pharmacol 61: 1017-1024.
11. Warner-Schmidt JL, Duman RS, (2007) VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc Natl Acad Sci U S A 104: 4647-4652.
12. Shirayama Y, Chen AC, Nakagawa S, Russell DS, Duman RS, (2002) Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 22: 3251-3261.
13. Turner CA, Gula EL, Taylor LP, Watson SJ, Akil H, (2008) Antidepressant-like effects of intracerebroventricular FGF2 in rats. Brain Res 1224: 63-68.
14. Overstreet DH, Fredericks K, Knapp D, Breese G, McMichael J, (2010) Nerve growth factor (NGF) has novel antidepressant-like properties in rats. Pharmacol Biochem Behav 94: 553-560.
15. Takebayashi M, Hisaoka K, Tsuchioka M (2009) Glial dysfunction in mood disorders: The role of GDNF. In: Shirayama Y, Chaki S, editors. Recent Developments on Depression Research. Kerala, India: Research Signpost. 125-143.
16. Seth P, Koul N, (2008) Astrocyte, the star avatar: redefined. J Biosci 33: 405-421.
17. Azevedo FA, Carvalho LR, Grinberg LT, Farfel JM, Ferretti RE, et al. (2009) Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513: 532-541.
18. Slezak M, Pfrieger FW, (2003) New roles for astrocytes: regulation of CNS synaptogenesis. Trends Neurosci 26: 531-535.
19. Ma DK, Ming GL, Song H, (2005) Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr Opin Neurobiol 15: 514-520.
20. Páv M, Kovárů H, Fiserová A, Havrdová E, Lisá V, (2008) Neurobiological aspects of depressive disorder and antidepressant treatment: role of glia. Physiol Res 57: 151-164.
21. Riva MA, Molteni R, Lovati E, Fumagalli F, Rusnati M, et al. (1996) Cyclic AMP-dependent regulation of fibroblast growth factor-2 messenger RNA levels in rat cortical astrocytes: comparison with fibroblast growth factor-1 and ciliary neurotrophic factor. Mol Pharmacol 49: 699-706.
22. Krzan M, Wu VW, Schwartz JP, (2001) Serotonin regulation of nerve growth factor synthesis in neonatal and adult astrocytes: comparison to the beta-adrenergic agonist isoproterenol. J Neurosci Res 64: 261-267.
23. Yan M, Dai H, Ding T, Dai A, Zhang F, et al. (2011) Effects of dexmedetomidine on the release of glial cell line-derived neurotrophic factor from rat astrocyte cells. Neurochem Int 58: 549-557.
24. Juric DM, Miklic S, Carman-Krzan M, (2006) Monoaminergic neuronal activity up-regulates BDNF synthesis in cultured neonatal rat astrocytes. Brain Res 1108: 54-62.
25. Furukawa S, Furukawa Y, Satoyoshi E, Hayashi K, (1987) Regulation of nerve growth factor synthesis/secretion by catecholamine in cultured mouse astroglial cells. Biochem Biophys Res Commun 147: 1048-1054.
26. Tsuchioka M, Takebayashi M, Hisaoka K, Maeda N, Nakata Y, (2008) Serotonin (5-HT) induces glial cell line-derived neurotrophic factor (GDNF) mRNA expression via the transactivation of fibroblast growth factor receptor 2 (FGFR2) in rat C6 glioma cells. J Neurochem 106: 244-257.
27. Rajkowska G, Miguel-Hidalgo JJ, (2007) Gliogenesis and glial pathology in depression. CNS Neurol Disord Drug Targets 6: 219-233.
28. Ongür D, Drevets WC, Price JL, (1998) Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 95: 13290-13295.
29. Rajkowska G, Miguel-Hidalgo JJ, Wei J, Dilley G, Pittman SD, et al. (1999) Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 45: 1085-1098.
30. Banasr M, Duman RS, (2008) Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol Psychiatry 64: 863-870.
31. Chen Y, Peng L, Zhang X, Stolzenburg JU, Hertz L, (1995) Further evidence that fluoxetine interacts with a 5-HT2C receptor in glial cells. Brain Res Bull 38: 153-159.
32. Kim Y, Kim SH, Kim YS, Lee YH, Ha K, et al. (2011) Imipramine activates glial cell line-derived neurotrophic factor via early growth response gene 1 in astrocytes. Prog Neuropsychopharmacol Biol Psychiatry 35: 1026-1032.
33. Mercier G, Lennon AM, Renouf B, Dessouroux A, Ramaugé M, et al. (2004) MAP kinase activation by fluoxetine and its relation to gene expression in cultured rat astrocytes. J Mol Neurosci 24: 207-216.
34. Hisaoka K, Takebayashi M, Tsuchioka M, Maeda N, Nakata Y, et al. (2007) Antidepressants increase glial cell line-derived neurotrophic factor production through monoamine-independent activation of protein tyrosine kinase and extracellular signal-regulated kinase in glial cells. J Pharmacol Exp Ther 321: 148-157.
35. Czéh B, Di Benedetto B (2012) Antidepressants act directly on astrocytes: Evidences and functional consequences. Eur Neuropsychopharmacol.
36. Sugimoto T, Morioka N, Sato K, Hisaoka K, Nakata Y, (2011) Noradrenergic regulation of period1 expression in spinal astrocytes is involved in protein kinase A, c-Jun N-terminal kinase and extracellular signal-regulated kinase activation mediated by α1- and β2-adrenoceptors. Neuroscience 185: 1-13.
37. Fuchikami M, Morinobu S, Kurata A, Yamamoto S, Yamawaki S, (2009) Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus. Int J Neuropsychopharmacol 12: 73-82.
38. Iwata M, Shirayama Y, Ishida H, Hazama GI, Nakagome K, (2011) Hippocampal astrocytes are necessary for antidepressant treatment of learned helplessness rats. Hippocampus 21: 877-884.
39. Sørensen V, Nilsen T, Wiedłocha A, (2006) Functional diversity of FGF-2 isoforms by intracellular sorting. Bioessays 28: 504-514.
40. Numakawa T, Yamagishi S, Adachi N, Matsumoto T, Yokomaku D, et al. (2002) Brain-derived neurotrophic factor-induced potentiation of Ca(2+) oscillations in developing cortical neurons. J Biol Chem 277: 6520-6529.
41. Audigier S, Guiramand J, Prado-Lourenco L, Conte C, Gonzalez-Herrera IG, et al. (2008) Potent activation of FGF-2 IRES-dependent mechanism of translation during brain development. RNA 14: 1852-1864.
42. Moffett J, Kratz E, Myers J, Stachowiak EK, Florkiewicz RZ, et al. (1998) Transcriptional regulation of fibroblast growth factor-2 expression in human astrocytes: implications for cell plasticity. Mol Biol Cell 9: 2269-2285.
43. Shinozaki Y, Koizumi S, Ishida S, Sawada J, Ohno Y, et al. (2005) Cytoprotection against oxidative stress-induced damage of astrocytes by extracellular ATP via P2Y1 receptors. Glia 49: 288-300.
44. Morishima T, Aoyama M, Iida Y, Yamamoto N, Hirate H, et al. (2008) Lactic acid increases aquaporin 4 expression on the cell membrane of cultured rat astrocytes. Neurosci Res 61: 18-26.
45. Allaman I, Fiumelli H, Magistretti PJ, Martin JL, (2011) Fluoxetine regulates the expression of neurotrophic/growth factors and glucose metabolism in astrocytes. Psychopharmacology (Berl) 216: 75-84.
46. Liu Q, Li B, Zhu HY, Wang YQ, Yu J, et al. (2009) Clomipramine treatment reversed the glial pathology in a chronic unpredictable stress-induced rat model of depression. Eur Neuropsychopharmacol 19: 796-805.
47. Uchida S, Hara K, Kobayashi A, Otsuki K, Yamagata H, et al. (2011) Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 69: 359-372.
48. Sergent-Tanguy S, Michel DC, Neveu I, Naveilhan P, (2006) Long-lasting coexpression of nestin and glial fibrillary acidic protein in primary cultures of astroglial cells with a major participation of nestin(+)/GFAP(-) cells in cell proliferation. J Neurosci Res 83: 1515-1524.
49. Bachis A, Mallei A, Cruz MI, Wellstein A, Mocchetti I, (2008) Chronic antidepressant treatments increase basic fibroblast growth factor and fibroblast growth factor-binding protein in neurons. Neuropharmacology 55: 1114-1120.
50. Jarosik J, Legutko B, Werner S, Unsicker K, von Bohlen Und Halbach O, (2011) Roles of exogenous and endogenous FGF-2 in animal models of depression. Restor Neurol Neurosci 29: 153-165.
51. Elsayed M, Banasr M, Duric V, Fournier NM, Licznerski P, et al. (2012) Antidepressant effects of fibroblast growth factor-2 in behavioral and cellular models of depression. Biol Psychiatry 72: 258-265.
52. Li AJ, Suzuki S, Suzuki M, Mizukoshi E, Imamura T, (2002) Fibroblast growth factor-2 increases functional excitatory synapses on hippocampal neurons. Eur J Neurosci 16: 1313-1324.
53. Mudò G, Bonomo A, Di Liberto V, Frinchi M, Fuxe K, et al. (2009) The FGF-2/FGFRs neurotrophic system promotes neurogenesis in the adult brain. J Neural Transm 116: 995-1005.
54. Nelson AD, Svendsen CN, (2006) Low concentrations of extracellular FGF-2 are sufficient but not essential for neurogenesis from human neural progenitor cells. Mol Cell Neurosci 33: 29-35.
55. Biesiada E, Razandi M, Levin ER, (1996) Egr-1 activates basic fibroblast growth factor transcription. Mechanistic implications for astrocyte proliferation. J Biol Chem 271: 18576-18581.
56. Luo X, Zhang X, Shao W, Yin Y, Zhou J, (2009) Crucial roles of MZF-1 in the transcriptional regulation of apomorphine-induced modulation of FGF-2 expression in astrocytic cultures. J Neurochem 108: 952-961.
57. Hisaoka K, Tsuchioka M, Yano R, Maeda N, Kajitani N, et al. (2011) Tricyclic antidepressant amitriptyline activates fibroblast growth factor receptor signaling in glial cells: involvement in glial cell line-derived neurotrophic factor production. J Biol Chem 286: 21118-21128.
58. Prouty RW, Anderson WH, (1990) The forensic science implications of site and temporal influences on postmortem blood-drug concentrations. J Forensic Sci 35: 243-270.
59. Baumann P, Gaillard JM, Jonzier-Perey M, Gerber C, Bouras C, (1984) Evaluation of the levels of free and total amitriptyline and metabolites in the plasma and brain of the rat after long-term administration of doses used in receptor studies. Psychopharmacology (Berl) 84: 489-495.
60. Glotzbach RK, Preskorn SH, (1982) Brain concentrations of tricyclic antidepressants: single-dose kinetics and relationship to plasma concentrations in chronically dosed rats. Psychopharmacology (Berl) 78: 25-27.
61. Miyake K, Fukuchi H, Kitaura T, Kimura M, Sarai K, et al. (1990) Pharmacokinetics of amitriptyline and its demethylated metabolite in serum and specific brain regions of rats after acute and chronic administration of amitriptyline. J Pharm Sci 79: 288-291.
62. O'Donnell JM, Shelton RC (2011) Drug Therapy of Depression and Anxiety Disorders. In: Brunton LL, editor. Goodman & Gilman's The Pharmacological Basis of Therapeutics. 12 ed. New York: McGraw-Hill Book Companies. 397-415.
63. Chen MJ, Nguyen TV, Pike CJ, Russo-Neustadt AA, (2007) Norepinephrine induces BDNF and activates the PI-3K and MAPK cascades in embryonic hippocampal neurons. Cell Signal 19: 114-128.