Alleviative effects of fluoxetine on depressive-like behaviors by epigenetic regulation of BDNF gene transcription in mouse model of post-stroke depression

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Jin, Hui Juan ^a   Pei, Lei ^a,b   Li, Ya Nan ^a   Zheng, Hui ^a   Yang, Shuai ^a   Wan, Yan ^a   Mao, Ling ^a   Xia, Yuan Peng ^a   He, Quan Wei ^a   Li, Man ^a   Yue, Zhen Yu ^c   Hu, Bo ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIDEPRESSANT AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR; FLUOXETINE;

ANIMAL; C57BL MOUSE; CEREBROVASCULAR ACCIDENT; COMPLICATION; DEPRESSION; DISEASE MODEL; DRUG EFFECT; GENETIC EPIGENESIS; GENETICS; HIPPOCAMPUS; MALE; METABOLISM; TRANSCRIPTION INITIATION;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSION; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; FLUOXETINE; HIPPOCAMPUS; MALE; MICE, INBRED C57BL; STROKE; TRANSCRIPTIONAL ACTIVATION;

EID: 85032841491     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-13929-5     Document Type: Article

References (53)

1. Flaster, M., Sharma, A. & Rao, M. Poststroke depression: a review emphasizing the role of prophylactic treatment and synergy with treatment for motor recovery. Topics in stroke rehabilitation 20, 139-150, https://doi.org/10.1310/tsr2002-139 (2013).
2. Hackett, M. L. & Pickles, K. Part I: frequency of depression after stroke: an updated systematic review and meta-analysis of observational studies. International journal of stroke: official journal of the International Stroke Society 9, 1017-1025, https://doi. org/10.1111/ijs.12357 (2014).
3. Fruehwald, S., Gatterbauer, E., Rehak, P. & Baumhackl, U. Early fluoxetine treatment of post-stroke depression-A three-month double-blind placebo-controlled study with an open-label long-term follow up. Journal of neurology 250, 347-351, https://doi. org/10.1007/s00415-003-1014-3 (2003).
4. Wiart, L., Petit, H., Joseph, P. A., Mazaux, J. M. & Barat, M. Fluoxetine in early poststroke depression: a double-blind placebocontrolled study. Stroke; a journal of cerebral circulation 31, 1829-1832 (2000).
5. Castren, E. & Rantamaki, T. The role of BDNF and its receptors in depression and antidepressant drug action: Reactivation of developmental plasticity. Developmental neurobiology 70, 289-297, https://doi.org/10.1002/dneu.20758 (2010).
6. Russo-Neustadt, A. A. & Chen, M. J. Brain-derived neurotrophic factor and antidepressant activity. Current pharmaceutical design 11, 1495-1510 (2005).
7. Hodes, G. E., Hill-Smith, T. E. & Lucki, I. Fluoxetine treatment induces dose dependent alterations in depression associated behavior and neural plasticity in female mice. Neuroscience letters 484, 12-16, https://doi.org/10.1016/j.neulet.2010.07.084 (2010).
8. Jin, L. et al. Long-term Ameliorative Effects of the Antidepressant Fluoxetine Exposure on Cognitive Deficits in 3 x TgAD Mice. Molecular neurobiology, doi:https://doi.org/10.1007/s12035-016-9952-9 (2016).
9. Menke, A. & Binder, E. B. Epigenetic alterations in depression and antidepressant treatment. Dialogues in clinical neuroscience 16, 395-404 (2014).
10. Aid, T., Kazantseva, A., Piirsoo, M., Palm, K. & Timmusk, T. Mouse and rat BDNF gene structure and expression revisited. Journal of neuroscience research 85, 525-535, https://doi.org/10.1002/jnr.21139 (2007).
11. Martinowich, K., Manji, H. & Lu, B. New insights into BDNF function in depression and anxiety. Nature neuroscience 10, 1089-1093, https://doi.org/10.1038/nn1971 (2007).
12. Kang, H. J. et al. Longitudinal associations between BDNF promoter methylation and late-life depression. Neurobiology of aging 36(1764), e1761-1767, https://doi.org/10.1016/j.neurobiolaging.2014.12.035 (2015).
13. Mitchelmore, C. & Gede, L. Brain Derived Neurotrophic Factor: epigenetic regulation in psychiatric disorders. Brain research 1586, 162-172, https://doi.org/10.1016/j.brainres.2014.06.037 (2014).
14. McCarthy, D. M., Brown, A. N. & Bhide, P. G. Regulation of BDNF expression by cocaine. The Yale journal of biology and medicine 85, 437-446 (2012).
15. Tai, D. J. et al. MeCP2 SUMOylation rescues Mecp2-mutant-induced behavioural deficits in a mouse model of Rett syndrome. Nature communications 7, 10552, https://doi.org/10.1038/ncomms10552 (2016).
16. Cohen, S. et al. Genome-wide activity-dependent MeCP2 phosphorylation regulates nervous system development and function. Neuron 72, 72-85, https://doi.org/10.1016/j.neuron.2011.08.022 (2011).
17. Zhou, Z. et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269, https://doi.org/10.1016/j.neuron.2006.09.037 (2006).
18. Zeng, B. et al. Involvement of PI3K/Akt/FoxO3a and PKA/CREB Signaling Pathways in the Protective Effect of Fluoxetine Against Corticosterone-Induced Cytotoxicity in PC12 Cells. Journal of molecular neuroscience: MN 59, 567-578, https://doi.org/10.1007/ s12031-016-0779-7 (2016).
19. Santos, M. et al. The neuroanatomical model of post-stroke depression: towards a change of focus? Journal of the neurological sciences 283, 158-162, https://doi.org/10.1016/j.jns.2009.02.334 (2009).
20. Kronenberg, G., Gertz, K., Heinz, A. & Endres, M. Of mice and men: modelling post-stroke depression experimentally. British journal of pharmacology 171, 4673-4689, https://doi.org/10.1111/bph.12775 (2014).
21. O'Keefe, L. M. et al. Social isolation after stroke leads to depressive-like behavior and decreased BDNF levels in mice. Behavioural brain research 260, 162-170, https://doi.org/10.1016/j.bbr.2013.10.047 (2014).
22. Vahid-Ansari, F., Lagace, D. C. & Albert, P. R. Persistent post-stroke depression in mice following unilateral medial prefrontal cortical stroke. Translational psychiatry 6, e863, https://doi.org/10.1038/tp.2016.124 (2016).
23. Lee, B. H. & Kim, Y. K. The roles of BDNF in the pathophysiology of major depression and in antidepressant treatment. Psychiatry investigation 7, 231-235, https://doi.org/10.4306/pi.2010.7.4.231 (2010).
24. Wu, G. F. et al. Antidepressant effect of taurine in chronic unpredictable mild stress-induced depressive rats. Scientific reports 7, 4989, https://doi.org/10.1038/s41598-017-05051-3 (2017).
25. Ikegame, T. et al. DNA methylation of the BDNF gene and its relevance to psychiatric disorders. Journal of human genetics 58, 434-438, https://doi.org/10.1038/jhg.2013.65 (2013).
26. Greer, P. L. & Greenberg, M. E. From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59, 846-860, https://doi.org/10.1016/j.neuron.2008.09.002 (2008).
27. Bhogal, S. K., Teasell, R., Foley, N. & Speechley, M. Lesion location and poststroke depression: systematic review of the methodological limitations in the literature. Stroke; a journal of cerebral circulation 35, 794-802, https://doi.org/10.1161/01. STR.0000117237.98749.26 (2004).
28. Murphy, G. M. Jr. et al. BDNF and CREB1 genetic variants interact to affect antidepressant treatment outcomes in geriatric depression. Pharmacogenetics and genomics 23, 301-313, https://doi.org/10.1097/FPC.0b013e328360b175 (2013).
29. Greenberg, M. E., Xu, B., Lu, B. & Hempstead, B. L. New insights in the biology of BDNF synthesis and release: implications in CNS function. The Journal of neuroscience: the official journal of the Society for Neuroscience 29, 12764-12767, https://doi.org/10.1523/ JNEUROSCI.3566-09.2009 (2009).
30. Krishnan, V. & Nestler, E. J. The molecular neurobiology of depression. Nature 455, 894-902, https://doi.org/10.1038/nature07455 (2008).
31. Karege, F., Vaudan, G., Schwald, M., Perroud, N. & La Harpe, R. Neurotrophin levels in postmortem brains of suicide victims and the effects of antemortem diagnosis and psychotropic drugs. Brain research. Molecular brain research 136, 29-37, https://doi. org/10.1016/j.molbrainres.2004.12.020 (2005).
32. Sales, A. J. et al. Antidepressant-like effect induced by systemic and intra-hippocampal administration of DNA methylation inhibitors. British journal of pharmacology 164, 1711-1721, https://doi.org/10.1111/j.1476-5381.2011.01489.x (2011).
33. Nagahara, A. H. & Tuszynski, M. H. Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nature reviews. Drug discovery 10, 209-219, https://doi.org/10.1038/nrd3366 (2011).
34. Zhou, Z. et al. Decreased serum brain-derived neurotrophic factor (BDNF) is associated with post-stroke depression but not with BDNF gene Val66Met polymorphism. Clinical chemistry and laboratory medicine: CCLM / FESCC 49, 185-189, https://doi. org/10.1515/CCLM.2011.039 (2011).
35. Li, J. et al. Serum Brain-derived neurotrophic factor levels in post-stroke depression. Journal of affective disorders 168, 373-379, https://doi.org/10.1016/j.jad.2014.07.011 (2014).
36. Yang, L. et al. Low serum BDNF may indicate the development of PSD in patients with acute ischemic stroke. International journal of geriatric psychiatry 26, 495-502, https://doi.org/10.1002/gps.2552 (2011).
37. Naert, G. et al. Involvement of Endogenous Brain-Derived Neurotrophic Factor in Hypothalamic-Pituitary-Adrenal Axis Activity. Journal of neuroendocrinology 27, 850-860, https://doi.org/10.1111/jne.12324 (2015).
38. Moore, L. D., Le, T. & Fan, G. DNA methylation and its basic function. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology 38, 23-38, https://doi.org/10.1038/npp.2012.112 (2013).
39. Nelson, E. D., Kavalali, E. T. & Monteggia, L. M. Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. The Journal of neuroscience: the official journal of the Society for Neuroscience 28, 395-406, https:// doi.org/10.1523/JNEUROSCI.3796-07.2008 (2008).
40. Martinowich, K. et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science (New York, N.Y.) 302, 890-893, https://doi.org/10.1126/science.1090842 (2003).
41. Gavin, D. P. & Akbarian, S. Epigenetic and post-transcriptional dysregulation of gene expression in schizophrenia and related disease. Neurobiology of disease 46, 255-262, https://doi.org/10.1016/j.nbd.2011.12.008 (2012).
42. Autry, A. E. & Monteggia, L. M. Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacological reviews 64, 238-258, https://doi.org/10.1124/pr.111.005108 (2012).
43. Karpova, N. N. Role of BDNF epigenetics in activity-dependent neuronal plasticity. Neuropharmacology 76 Pt C, 709-718, https:// doi.org/10.1016/j.neuropharm.2013.04.002 (2014).
44. Lu, B. Pro-region of neurotrophins: role in synaptic modulation. Neuron 39, 735-738 (2003).
45. Sakata, K., Jin, L. & Jha, S. Lack of promoter IV-driven BDNF transcription results in depression-like behavior. Genes, brain, and behavior 9, 712-721, https://doi.org/10.1111/j.1601-183X.2010.00605.x (2010).
46. Mayr, B. & Montminy, M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nature reviews. Molecular cell biology 2, 599-609, https://doi.org/10.1038/35085068 (2001).
47. Qi, X. et al. Fluoxetine increases the activity of the ERK-CREB signal system and alleviates the depressive-like behavior in rats exposed to chronic forced swim stress. Neurobiology of disease 31, 278-285, https://doi.org/10.1016/j.nbd.2008.05.003 (2008).
48. Yoo, Y. K. et al. Ultra-sensitive detection of brain-derived neurotrophic factor (BDNF) in the brain of freely moving mice using an interdigitated microelectrode (IME) biosensor. Scientific reports 6, 33694, https://doi.org/10.1038/srep33694 (2016).
49. Labat-gest, V. & Tomasi, S. Photothrombotic ischemia: a minimally invasive and reproducible photochemical cortical lesion model for mouse stroke studies. Journal of visualized experiments: JoVE, https://doi.org/10.3791/50370 (2013).
50. Boltze, J. et al. Experimental treatment of stroke in spontaneously hypertensive rats by CD34 + and CD34-cord blood cells. German medical science: GMS e-journal 3, Doc09 (2005).
51. Porsolt, R. D., Bertin, A. & Jalfre, M. Behavioral despair in mice: a primary screening test for antidepressants. Archives internationales de pharmacodynamie et de therapie 229, 327-336 (1977).
52. Hong, S. et al. Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats. Physiology & behavior 105, 269-275, https://doi.org/10.1016/j.physbeh.2011.08.036 (2012).
53. Hashikawa-Hobara, N. et al. Calcitonin gene-related peptide pre-administration acts as a novel antidepressant in stressed mice. Scientific reports 5, 12559, https://doi.org/10.1038/srep12559 (2015).