Fluoxetine increases hippocampal neurogenesis and induces epigenetic factors but does not improve functional recovery after traumatic brain injury

Journal of Neurotrauma

Volumn 28, Issue 2, 2011, Pages 259-268

  Wang, Yonggang ^a,b,c   Neumann, Melanie ^a,b,d   Hansen, Katharina ^a,b   Hong, Shuwhey M ^a,b   Kim, Sharon ^a,b   Noble Haeusslein, Linda J ^b   Liu, Jialing ^a,b  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

controlled cortical impact; histone acetylation; memory; methyl CpG binding domain 1; selective serotonin reuptake inhibitor

Indexed keywords

FLUOXETINE; HISTONE H3; METHYL CPG BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BARNES MAZE TEST; BRAIN CELL; BRAIN CORTEX; BRAIN SURGERY; CATWALK ASSISTED GAIT TEST; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CONVALESCENCE; DENTATE GYRUS; DISEASE SEVERITY; DNA METHYLATION; DRUG EFFICACY; EPIGENETICS; FUNCTION TEST; GAIT; HIPPOCAMPUS; HISTONE ACETYLATION; IMMUNOHISTOCHEMISTRY; LEARNING; MALE; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; PROTEIN INDUCTION; QUANTITATIVE ANALYSIS; STEREOLOGY; TRAUMATIC BRAIN INJURY; WESTERN BLOTTING;

ANIMALS; BRAIN INJURIES; EPIGENESIS, GENETIC; FLUOXETINE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NEUROGENESIS; RECOVERY OF FUNCTION;

EID: 79951698211     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1648     Document Type: Article

References (57)

1. Beauquis, J., Roig, P., De Nicola, A.F., and Saravia, F. (2009). Neuronal plasticity and antidepressants in the diabetic brain. Ann. NY Acad. Sci. 1153, 203-208.
2. Berends, H.I., Nijlant, J., van Putten, M., and Movig, K.L. (2009). Single dose of fluoxetine increases muscle activation in chronic stroke patients. Clin. Neuropharmacol. 32, 1-5.
3. Bilgen, M. (2005). A new device for experimental modeling of central nervous system injuries. Neurorehabil. Neural Repair 19, 219-226. (Pubitemid 41216297)
4. Boast, C., Bartolomeo, A.C., Morris, H., and Moyer, J.A. (1999). 5HT antagonists attenuate MK801-impaired radial arm maze performance in rats. Neurobiol. Learn. Mem. 71, 259-271. (Pubitemid 29394848)
5. Boyeson, M.G., Harmon, R.L., and Jones, J.L. (1994). Comparative effects of fluoxetine, amitriptyline and serotonin on functional motor recovery after sensorimotor cortex injury. Am. J. Phys. Med. Rehabil. 73, 76-83. (Pubitemid 24126183)
6. Carli, M., Bonalumi, P., and Samanin, R. (1997). WAY 100635, a 5-HT1A receptor antagonist, prevents the impairment of spatial learning caused by intrahippocampal administration of scopolamine or 7-chloro-kynurenic acid. Brain Res. 774, 167-174. (Pubitemid 28007896)
7. Carli, M., Lazarova, M., Tatarczynska, E., and Samanin, R. (1992). Stimulation of 5-HT1A receptors in the dorsal hippocampus impairs acquisition and performance of a spatial task in a water maze. Brain Res. 595, 50-56.
8. Carli, M., and Samanin, R. (1992). 8-Hydroxy-2-(di-n-propylamino) tetralin impairs spatial learning in a water maze: role of postsynaptic 5-HT1A receptors. Br. J. Pharmacol. 105, 720-726.
9. Cassel, S., Carouge, D., Gensburger, C., Anglard, P., Burgun, C., Dietrich, J.B., Aunis, D., and Zwiller, J. (2006). Fluoxetine and cocaine induce the epigenetic factors MeCP2 and MBD1 in adult rat brain. Mol. Pharmacol. 70, 487-492. (Pubitemid 44092309)
10. Cheng, J.P., Hoffman, A.N., Zafonte, R.D., and Kline, A.E. (2008). A delayed and chronic treatment regimen with the 5- HT1A receptor agonist 8-OH-DPAT after cortical impact injury facilitates motor recovery and acquisition of spatial learning. Behav. Brain Res. 194, 79-85.
11. Chen, Y., Peng, L., Zhang, X., Stolzenburg, J.U., and Hertz, L. (1995). Further evidence that fluoxetine interacts with a 5- HT2C receptor in glial cells. Brain Res. Bull. 38, 153-159.
12. Crosio, C., Heitz, E., Allis, C.D., Borrelli, E., and Sassone-Corsi, P. (2003). Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J. Cell Sci. 116, 4905-4914. (Pubitemid 38016697)
13. Dash, P.K., Orsi, S.A., and Moore, A.N. (2009). Histone deactylase inhibition combined with behavioral therapy enhances learning and memory following traumatic brain injury. Neuroscience 163, 1-8.
14. David, D.J., Samuels, B.A., Rainer, Q., Wang, J.W., Marsteller, D., Mendez, I., Drew, M., Craig, D.A., Guiard, B.P., Guilloux, J.P., Artymyshyn, R.P., Gardier, A.M., Gerald, C., Antonijevic, I.A., Leonardo, E.D., and Hen, R. (2009). Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493.
15. Dulawa, S.C., Holick, K.A., Gundersen, B., and Hen, R. (2004). Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 29, 1321-1330. (Pubitemid 38780655)
16. Encinas, J.M., Vaahtokari, A., and Enikolopov, G. (2006). Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl. Acad. Sci. USA 103, 8233-8238. (Pubitemid 43801081)
17. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., and Tsai, L.H. (2007). Recovery of learning and memory is associated with chromatin remodelling. Nature 447, 178-182. (Pubitemid 46763080)
18. Gao, W.M., Chadha, M.S., Kline, A.E., Clark, R.S., Kochanek, P.M., Dixon, C.E., and Jenkins, L.W. (2006). Immunohistochemical analysis of histone H3 acetylation and methylation-evidence for altered epigenetic signaling following traumatic brain injury in immature rats. Brain Res. 1070, 31-34. (Pubitemid 43247741)
19. Guan, Z., Giustetto, M., Lomvardas, S., Kim, J.H., Miniaci, M.C., Schwartz, J.H., Thanos, D., and Kandel, E.R. (2002). Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111, 483-493. (Pubitemid 35363296)
20. Holick, K.A., Lee, D.C., Hen, R., and Dulawa, S.C. (2008). Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33, 406-417. (Pubitemid 350243341)
21. Jin, Y., Lim, C.M., Kim, S.W., Park, J.Y., Seo, J.S., Han, P.L., Yoon, S.H., and Lee, J.K. (2009). Fluoxetine attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. Brain Res. 1281, 108-116.
22. Jones, N.C., Salzberg, M.R., Kumar, G., Couper, A., Morris, M.J., and OBrien, T.J. (2008). Elevated anxiety and depressive-like behavior in a rat model of genetic generalized epilepsy suggesting common causation. Exp. Neurol. 209, 254-260.
23. Jorge, R.E., and Starkstein, S.E. (2005). Pathophysiologic aspects of major depression following traumatic brain injury. J. Head Trauma Rehabil. 20, 475-487. (Pubitemid 41690423)
24. Kennard, L.E., Chumbley, J.R., Ranatunga, K.M., Armstrong, S.J., Veale, E.L., and Mathie, A. (2005). Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. Br. J. Pharmacol. 144, 821-829. (Pubitemid 40516121)
25. Kong, E.K., Peng, L., Chen, Y., Yu, A.C., and Hertz, L. (2002). Up-regulation of 5-HT2B receptor density and receptormediated glycogenolysis in mouse astrocytes by long-term fluoxetine administration. Neurochem. Res. 27, 113-120. (Pubitemid 34242437)
26. Levenson, J.M., and Sweatt, J.D. (2006). Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation. Cell Mol. Life Sci. 63, 1009-1016. (Pubitemid 43800770)
27. Liang, K.C., Tsui, K.Y., Tyan, Y.M., and Chiang, T.C. (1998). Buspirone impaired acquisition and retention in avoidance tasks: involvement of the hippocampus. Chin. J. Physiol. 41, 33-44.
28. Liu, Z., Fan, Y., Won, S.J., Neumann, M., Hu, D., Zhou, L., Weinstein, P.R., and Liu, J. (2007). Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38, 146-152. (Pubitemid 46035620)
29. Li, W.L., Cai, H.H., Wang, B., Chen, L., Zhou, Q.G., Luo, C.X., Liu, N., Ding, X.S., and Zhu, D.Y. (2009). Chronic fluoxetine treatment improves ischemia-induced spatial cognitive deficits through increasing hippocampal neurogenesis after stroke. J. Neurosci. Res. 87, 112-122.
30. Matsumori, Y., Hong, S.M., Fan, Y., Kayama, T., Hsu, C.Y., Weinstein, P.R., and Liu, J. (2006). Enriched environment and spatial learning enhance hippocampal neurogenesis and salvages ischemic penumbra after focal cerebral ischemia. Neurobiol. Dis. 22, 187-198.
31. Maya Vetencourt, J.F., Sale, A., Viegi, A., Baroncelli, L., De Pasquale, R., OLeary, O.F., Castren, E., and Maffei, L. (2008). The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320, 385-388. (Pubitemid 351555663)
32. Meneses, A. (2002). Involvement of 5-HT(2A/2B/2C) receptors on memory formation: simple agonism, antagonism, or inverse agonism? Cell Mol. Neurobiol. 22, 675-688. (Pubitemid 36169216)
33. Meneses, A. (2007). Stimulation of 5-HT1A, 5-HT1B, 5-HT2A/ 2C, 5-HT3 and 5-HT4 receptors or 5-HT uptake inhibition: short- and long-term memory. Behav. Brain Res. 184, 81-90. (Pubitemid 47411590)
34. Miller, C.A., Gavin, C.F., White, J.A., Parrish, R.R., Honasoge, A., Yancey, C.R., Rivera, I.M., Rubio, M.D., Rumbaugh, G., and Sweatt, J.D. (2010). Cortical DNA methylation maintains remote memory. Nat. Neurosci. 13, 664-666.
35. Milman, A., Rosenberg, A., Weizman, R., and Pick, C.G. (2005). Mild traumatic brain injury induces persistent cognitive deficits and behavioral disturbances in mice. J. Neurotrauma 22, 1003-1010. (Pubitemid 41362066)
36. Mostert, J.P., Koch, M.W., Heerings, M., Heersema, D.J., and De Keyser, J. (2008). Therapeutic potential of fluoxetine in neurological disorders. CNS Neurosci. Ther. 14, 153-164. (Pubitemid 351713316)
37. Mowla, A., Mosavinasab, M., and Pani, A. (2007). Does fluoxetine have any effect on the cognition of patients with mild cognitive impairment? A double-blind, placebo-controlled, clinical trial. J. Clin. Psychopharmacol. 27, 67-70. (Pubitemid 46105768)
38. Nahon, E., Israelson, A., Abu-Hamad, S., and Varda, S.B. (2005). Fluoxetine (Prozac) interaction with the mitochondrial voltage- dependent anion channel and protection against apoptotic cell death. FEBS Lett. 579, 5105-5110. (Pubitemid 41242861)
39. Narushima, K., Paradiso, S., Moser, D.J., Jorge, R., and Robinson, R.G. (2007). Effect of antidepressant therapy on executive function after stroke. Br. J. Psychiatry 190, 260-265. (Pubitemid 46384011)
40. Neumann, M., Wang, Y., Kim, S., Hong, S.M., Jeng, L., Bilgen, M., and Liu, J. (2009). Assessing gait impairment following experimental traumatic brain injury in mice. J. Neurosci. Methods 176, 34-44.
41. Ouardouz, M., Zamponi, G.W., Barr, W., Kiedrowski, L., and Stys, P.K. (2005). Protection of ischemic rat spinal cord white matter: Dual action of KB-R7943 on Na+/Ca2+ exchange and L-type Ca2+ channels. Neuropharmacology 48, 566-575. (Pubitemid 40332414)
42. Pariente, J., Loubinoux, I., Carel, C., Albucher, J.F., Leger, A., Manelfe, C., Rascol, O., and Chollet, F. (2001). Fluoxetine modulates motor performance and cerebral activation of patients recovering from stroke. Ann. Neurol. 50, 718-729. (Pubitemid 33116131)
43. Patterson, D.E., Braverman, S.E., and Belandres, P.V. (1997). Speech dysfunction due to trazodone-fluoxetine combination in traumatic brain injury. Brain Inj. 11, 287-291. (Pubitemid 27153786)
44. Porsolt, R.D., Bertin, A., and Jalfre, M. (1977b). Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229, 327-336. (Pubitemid 8225714)
45. Porsolt, R.D., Le Pichon, M., and Jalfre, M. (1977a). Depression: a new animal model sensitive to antidepressant treatments. Nature 266, 730-732. (Pubitemid 8073804)
46. Richardson-Jones, J.W., Craige, C.P., Guiard, B.P., Stephen, A., Metzger, K.L., Kung, H.F., Gardier, A.M., Dranovsky, A., David, D.J., Beck, S.G., Hen, R., and Leonardo, E.D. (2010). 5- HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 65, 40-52.
47. Rola, R., Mizumatsu, S., Otsuka, S., Morhardt, D.R., Noble- Haeusslein, L.J., Fishman, K., Potts, M.B., and Fike, J.R. (2006). Alterations in hippocampal neurogenesis following traumatic brain injury in mice. Exp. Neurol. 202, 189-199. (Pubitemid 44344260)
48. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C., and Hen, R. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809. (Pubitemid 36962615)
49. Shapira, M., Licht, A., Milman, A., Pick, C.G., Shohami, E., and Eldar-Finkelman, H. (2007). Role of glycogen synthase kinase- 3beta in early depressive behavior induced by mild traumatic brain injury. Mol. Cell Neurosci. 34, 571-577. (Pubitemid 46483079)
50. Shimizu, S., Narita, M., and Tsujimoto, Y. (1999). Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399, 483-487. (Pubitemid 29258855)
51. Singh, R.P., Shiue, K., Schomberg, D., and Zhou, F.C. (2009). Cellular epigenetic modifications of neural stem cell differentiation. Cell Transplant. 18, 1197-1211.
52. Svenningsson, P., Nairn, A.C., and Greengard, P. (2005). DARPP-32 mediates the actions of multiple drugs of abuse. Aaps J. 7, E353-E360. (Pubitemid 43078600)
53. Wang, J.W., David, D.J., Monckton, J.E., Battaglia, F., and Hen, R. (2008). Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J. Neurosci. 28, 1374-1384. (Pubitemid 351231535)
54. Wilson, M.S., and Hamm, R.J. (2002). Effects of fluoxetine on the 5-HT1A receptor and recovery of cognitive function after traumatic brain injury in rats. Am. J. Phys. Med. Rehabil. 81, 364-372. (Pubitemid 34412073)
55. Yu, T.S., Zhang, G., Liebl, D.J., and Kernie, S.G. (2008). Traumatic brain injury-induced hippocampal neurogenesis requires activation of early nestin-expressing progenitors. J. Neurosci. 28, 12901-12912.
56. Zhang, B., West, E.J., Van, K.C., Gurkoff, G.G., Zhou, J., Zhang, X.M., Kozikowski, A.P., and Lyeth, B.G. (2008). HDAC inhibitor increases histone H3 acetylation and reduces microglia inflammatory response following traumatic brain injury in rats. Brain Res. 1226, 181-191.
57. Zhang, X., Peng, L., Chen, Y., and Hertz, L. (1993). Stimulation of glycogenolysis in astrocytes by fluoxetine, an antidepressant acting like 5-HT. Neuroreport 4, 1235-1238. (Pubitemid 23289201)