Estrogen therapy increases BDNF expression and improves post-stroke depression in ovariectomy-treated rats

Su,Qiaoer; Cheng,Yifan; Jin,Kunlin; Cheng,Jianhua; Lin,Yuanshao; Lin,Zhenzhen; Wang,Liuqing; Shao,Bei

doi:10.3892/etm.2016.3531

Estrogen therapy increases BDNF expression and improves post-stroke depression in ovariectomy-treated rats

Authors:
- Qiaoer Su
- Yifan Cheng
- Kunlin Jin
- Jianhua Cheng
- Yuanshao Lin
- Zhenzhen Lin
- Liuqing Wang
- Bei Shao
View Affiliations

Affiliations: Department of Pediatrics, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325000, P.R. China, Department of Neurology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325000, P.R. China, University of North Texas Health Science Center, Fort Worth, TX 76107, USA
Published online on: July 19, 2016 https://doi.org/10.3892/etm.2016.3531
Pages: 1843-1848

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The present study investigated the effect of exogenous estrogen on post-stroke depression. Rats were exposed to chronic mild stress following middle cerebral artery occlusion. The occurrence of post‑stroke depression was evaluated according to the changes in preference for sucrose and performance in a forced swimming test. Estrogen therapy significantly improved these neurological symptoms, indicating that estrogen is effective in treating post‑stroke depression. Increased brain‑derived neurotrophic factor (BDNF) expression was reported in the hippocampus of rats that had been treated with estrogen for two weeks, suggesting that BDNF expression may be an important contributor to the improvement of post‑stroke depression that is observed following estrogen therapy.

View Figures

View References

1	Hackett ML, Yapa C, Parag V and Anderson CS: Frequency of depression after stroke: A systematic review of observational studies. Stroke. 36:1330–1340. 2005. View Article : Google Scholar : PubMed/NCBI
2	Weimar C, Kurth T, Kraywinkel K, Wagner M, Busse O, Haberl RL and Diener HC: German Stroke Data Bank Collaborators: Assessment of functioning and disability after ischemic stroke. Stroke. 33:2053–2059. 2002. View Article : Google Scholar : PubMed/NCBI
3	Williams LS, Ghose SS and Swindle RW: Depression and other mental health diagnoses increase mortality risk after ischemic stroke. Am J Psychiatry. 161:1090–1095. 2004. View Article : Google Scholar : PubMed/NCBI
4	Sinyor D, Amato P, Kaloupek DG, Becker R, Goldenberg M and Coopersmith H: Post-stroke depression: Relationships to functional impairment, coping strategies, and rehabilitation outcome. Stroke. 17:1102–1107. 1986. View Article : Google Scholar : PubMed/NCBI
5	CarodArtal FJ and Egido JA: Quality of life after stroke: The importance of a good recovery. Cerebrovasc Dis. 27(Suppl 1): 204–214. 2009. View Article : Google Scholar
6	Feibel JH and Springer CJ: Depression and failure to resume social activities after stroke. Arch Phys Med Rehabil. 63:276–277. 1982.PubMed/NCBI
7	Janzing JG, Bouwens JM, Teunisse RJ, Van't Hof MA and Zitman FG: The relationship between depression and mortality in elderly subjects with less severe dementia. Psychol Med. 29:979–983. 1999. View Article : Google Scholar : PubMed/NCBI
8	Bilge C, Koçer E, Koçer A and Türk Börü U: Depression and functional outcome after stroke: The effect of antidepressant therapy on functional recovery. Eur J Phys Rehabil Med. 44:13–18. 2008.PubMed/NCBI
9	Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N and Caleo M: Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci. 24:1850–1856. 2006. View Article : Google Scholar : PubMed/NCBI
10	Peng CH, Chiou SH, Chen SJ, Chou YC, Ku HH, Cheng CK, Yen CJ, Tsai TH, Chang YL and Kao CL: Neuroprotection by Imipramine against lipopolysaccharide-induced apoptosis in hippocampus-derived neural stem cells mediated by activation of BDNF and the MAPK pathway. Eur Neuropsychopharmacol. 18:128–140. 2008. View Article : Google Scholar : PubMed/NCBI
11	Luellen BA, Bianco LE, Schneider LM and Andrews AM: Reduced brain-derived neurotrophic factor is associated with a loss of serotonergic innervation in the hippocampus of aging mice. Genes Brain Behav. 6:482–490. 2007. View Article : Google Scholar : PubMed/NCBI
12	Hall J, Thomas KL and Everitt BJ: Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci. 3:533–535. 2000. View Article : Google Scholar : PubMed/NCBI
13	Duman RS and Monteggia LM: A neurotrophic model for stress-related mood disorders. Biol Psychiatry. 59:1116–1127. 2006. View Article : Google Scholar : PubMed/NCBI
14	Mohajerani MH, Sivakumaran S, Zacchi P, Aguilera P and Cherubini E: Correlated network activity enhances synaptic efficacy via BDNF and the ERK pathway at immature CA3 CA1 connections in the hippocampus. Proc Natl Acad Sci USA. 104:13176–13181. 2007. View Article : Google Scholar : PubMed/NCBI
15	Li Y, Luikart BW, Birnbaum S, Chen J, Kwon CH, Kernie SG, BasselDuby R and Parada LF: TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron. 59:399–412. 2008. View Article : Google Scholar : PubMed/NCBI
16	Bergami M, Rimondini R, Santi S, Blum R, Götz M and Canossa M: Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci USA. 105:15570–15575. 2008. View Article : Google Scholar : PubMed/NCBI
17	Siuciak JA, Lewis DR, Wiegand SJ and Lindsay RM: Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav. 56:131–137. 1997. View Article : Google Scholar : PubMed/NCBI
18	Sen S, Duman R and Sanacora G: Serum brain-derived neurotrophic factor, depression, and antidepressant medications: Meta-analyses and implications. Biol Psychiatry. 64:527–532. 2008. View Article : Google Scholar : PubMed/NCBI
19	Satomura E, Baba H, Nakano Y, Maeshima H, Suzuki T and Arai H: Correlations between brain-derived neurotrophic factor and clinical symptoms in medicated patients with major depression. J Affect Disord. 135:332–335. 2011. View Article : Google Scholar : PubMed/NCBI
20	Dreimüller N, Schlicht KF, Wagner S, Peetz D, Borysenko L, Hiemke C, Lieb K and Tadić A: Early reactions of brain-derived neurotrophic factor in plasma (pBDNF) and outcome to acute antidepressant treatment in patients with Major Depression. Neuropharmacology. 62:264–269. 2012. View Article : Google Scholar : PubMed/NCBI
21	Yang L, Zhang Z, Sun D, Xu Z, Yuan Y, Zhang X and Li L: Low serum BDNF may indicate the development of PSD in patients with acute ischemic stroke. Int J Geriatr Psychiatry. 26:495–502. 2011. View Article : Google Scholar : PubMed/NCBI
22	Allaman I, Papp M, Kraftsik R, Fiumelli H, Magistretti PJ and Martin JL: Expression of brain-derived neurotrophic factor is not modulated by chronic mild stress in the rat hippocampus and amygdala. Pharmacol Rep. 60:1001–1007. 2008.PubMed/NCBI
23	RomanoTorres M and Fernández-Guasti A: Estradiol valerate elicits antidepressant-like effects in middle-aged female rats under chronic mild stress. Behav Pharmacol. 21:104–111. 2010. View Article : Google Scholar : PubMed/NCBI
24	Herrick SP, Waters EM, Drake CT, McEwen BS and Milner TA: Extranuclear estrogen receptor beta immunoreactivity is on doublecortin-containing cells in the adult and neonatal rat dentate gyrus. Brain Res. 1121:46–58. 2006. View Article : Google Scholar : PubMed/NCBI
25	Walf AA, Rhodes ME and Frye CA: Antidepressant effects of ERbeta-selective estrogen receptor modulators in the forced swim test. Pharmacol Biochem Behav. 78:523–529. 2004. View Article : Google Scholar : PubMed/NCBI
26	Tanapat P, Hastings NB, Reeves AJ and Gould E: Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci. 19:5792–5801. 1999.PubMed/NCBI
27	Crispino M, Stone DJ, Wei M, Anderson CP, Tocco G, Finch CE and Baudry M: Variations of synaptotagmin I, synaptotagmin IV, and synaptophysin mRNA levels in rat hippocampus during the estrous cycle. Exp Neurol. 159:574–583. 1999. View Article : Google Scholar : PubMed/NCBI
28	Li XH, Liu NB, Zhang MH, Zhou YL, Liao JW, Liu XQ and Chen HW: Effects of chronic multiple stress on learning and memory and the expression of Fyn, BDNF, TrkB in the hippocampus of rats. Chin Med J (Engl). 120:669–674. 2007.PubMed/NCBI
29	Sandstrom NJ and Williams CL: Spatial memory retention is enhanced by acute and continuous estradiol replacement. Horm Behav. 45:128–135. 2004. View Article : Google Scholar : PubMed/NCBI
30	Liu F, Day M, Muñiz LC, Bitran D, Arias R, Revilla-Sanchez R, Grauer S, Zhang G, Kelley C, Pulito V, et al: Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci. 11:334–343. 2008. View Article : Google Scholar : PubMed/NCBI
31	Zhao H, Mayhan WG and Sun H: A modified suture technique produces consistent cerebral infarction in rats. Brain Res. 1246:158–166. 2008. View Article : Google Scholar : PubMed/NCBI
32	Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL and Bartkowski H: Rat middle cerebral artery occlusion: Evaluation of the model and development of a neurologic examination. Stroke. 17:472–476. 1986. View Article : Google Scholar : PubMed/NCBI
33	Herrmann N, Black SE, Lawrence J, Szekely C and Szalai JP: The Sunnybrook Stroke Study: A prospective study of depressive symptoms and functional outcome. Stroke. 29:618–624. 1998. View Article : Google Scholar : PubMed/NCBI
34	Berg A, Palomäki H, Lehtihalmes M, Lönnqvist J and Kaste M: Poststroke depression: An 18-month follow-up. Stroke. 34:138–143. 2003. View Article : Google Scholar : PubMed/NCBI
35	Suzuki S, Brown CM and Wise PM: Neuroprotective effects of estrogens following ischemic stroke. Front Neuroendocrinol. 30:201–211. 2009. View Article : Google Scholar : PubMed/NCBI
36	Mazzucco CA, Lieblich SE, Bingham BI, Williamson MA, Viau V and Galea LA: Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience. 141:1793–1800. 2006. View Article : Google Scholar : PubMed/NCBI
37	Alkayed NJ, McCune SK, Crain BJ, Traystman RJ and Hurn PD: Estrogen-enhanced expression of Bcl-2 mRNA in rat brain after experimental stroke. FASEB J. 12:A9541998.
38	Bagetta G, Chiappetta O, Amantea D, Iannone M, Rotiroti D, Costa A, Nappi G and Corasaniti MT: Estradiol reduces cytochrome c translocation and minimizes hippocampal damage caused by transient global ischemia in rat. Neurosci Lett. 368:87–91. 2004. View Article : Google Scholar : PubMed/NCBI
39	Danton GH and Dietrich WD: Inflammatory mechanisms after ischemia and stroke. J Neuropathol Exp Neurol. 62:127–136. 2003. View Article : Google Scholar : PubMed/NCBI
40	Sairanen M, Lucas G, Ernfors P, Castrén M and Castrén 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. 25:1089–1094. 2005. View Article : Google Scholar : PubMed/NCBI
41	Zhou J, Zhang H, Cohen RS and Pandey SC: Effects of estrogen treatment on expression of brain-derived neurotrophic factor and cAMP response element-binding protein expression and phosphorylation in rat amygdaloid and hippocampal structures. Neuroendocrinology. 81:294–310. 2005. View Article : Google Scholar : PubMed/NCBI
42	Yang LC, Zhang QG, Zhou CF, Yang F, Zhang YD, Wang RM and Brann DW: Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS One. 5:e98512010. View Article : Google Scholar : PubMed/NCBI