Fluoxetine Enhances Neurogenesis in Aged Rats with Cortical Infarcts, but This is not Reflected in a Behavioral Recovery

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• 作者：Xiaoyu Sun ; Zhike Zhou ; Tingting Liu ; Mei Zhao…
• 关键词：Aging ; Behavioral recovery ; Selective serotonin reuptake inhibitors ; Neurogenesis ; Cerebral ischemia
• 刊名：Journal of Molecular Neuroscience
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：58
• 期：2
• 页码：233-242
• 全文大小：1,438 KB
• 参考文献：Ayerbe L, Ayis S, Crichton S, Wolfe CD, Rudd AG (2014) The long-term outcomes of depression up to 10 years after stroke; the South London Stroke Register. J Neurol Neurosurg Psychiatry 85:514–521CrossRef PubMed
  Badan I, Buchhold B, Hamm A, et al. (2003) Accelerated glial reactivity to stroke in aged rats correlates with reduced functional recovery. J Cereb Blood Flow Metab 23:845–854CrossRef PubMed
  Bondolfi L, Calhoun M, Ermini F, et al. (2002) Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J Neurosci 22:515–522PubMed
  Bondolfi L, Ermini F, Long JM, Ingram DK, Jucker M (2004) Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiol Aging 25:333–340CrossRef PubMed
  Bonita R, Solomon N, Broad JB (1997) Prevalence of stroke and stroke-related disability. Estimates from the Auckland Stroke sTudies Stroke 28:1898–1902CrossRef PubMed
  Brown AW, Marlowe KJ, Bjelke B (2003) Age effect on motor recovery in a post-acute animal stroke model. Neurobiol Aging 24:607–614CrossRef PubMed
  Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 2:894–897CrossRef PubMed
  Chollet F, Tardy J, Albucher JF, et al. (2011) Fluoxetine for motor recovery after acute ischaemic stroke (FLAME): a randomised placebo-controlled trial. Lancet Neurol 10:123–130CrossRef PubMed
  Couillard-Despres S, Wuertinger C, Kandasamy M, et al. (2009) Ageing abolishes the effects of fluoxetine on neurogenesis. Mol Psychiatry 14:856–864CrossRef PubMed
  Cowen DS, Takase LF, Fornal CA, Jacobs BL (2008) Age-dependent decline in hippocampal neurogenesis is not altered by chronic treatment with fluoxetine. Brain Res 1228:14–19CrossRef PubMed
  Dam M, Tonin P, De Boni A, et al. (1996) Effects of fluoxetine and maprotiline on functional recovery in poststroke hemiplegic patients undergoing rehabilitation therapy. Stroke 27:1211–1214CrossRef PubMed
  Darsalia V, Heldmann U, Lindvall O, Kokaia Z (2005) Stroke-induced neurogenesis in aged brain. Stroke 36:1790–1795CrossRef PubMed
  Donnan GA, Fisher M, Macleod M, Davis SM (2008) Stroke. Lancet 371:1612–1623CrossRef PubMed
  Dulawa SC, Holick KA, Gundersen B, Hen R (2004) Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 29:1321–1330CrossRef PubMed
  Encinas JM, Vaahtokari A, Enikolopov G (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A 103:8233–8238PubMedCentral CrossRef PubMed
  Flaster M, Sharma A, Rao M (2013) Poststroke depression: a review emphasizing the role of prophylactic treatment and synergy with treatment for motor recovery. Top Stroke Rehabil 20:139–150CrossRef PubMed
  Gainotti G, Antonucci G, Marra C, Paolucci S (2001) Relation between depression after stroke, antidepressant therapy, and functional recovery. J Neurol Neurosurg Psychiatry 71:258–261PubMedCentral CrossRef PubMed
  Goldstein LB (1997) Influence of common drugs and related factors on stroke outcome. Curr Opin Neurol 10:52–57CrossRef PubMed
  Heine VM, Maslam S, Joels M, Lucassen PJ (2004) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 25:361–375CrossRef PubMed
  Holick KA, Lee DC, Hen R, Dulawa SC (2008) Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33:406–417CrossRef PubMed
  Huang GJ, Bannerman D, Flint J (2008) Chronic fluoxetine treatment alters behavior, but not adult hippocampal neurogenesis, in BALB/cJ mice. Mol Psychiatry 13:119–121CrossRef PubMed
  Jessberger S, Zhao C, Toni N, Clemenson GD Jr., Li Y, Gage FH (2007) Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci 27, 9400–9407.CrossRef PubMed
  Jin K, Minami M, Xie L, et al. (2004) Ischemia-induced neurogenesis is preserved but reduced in the aged rodent brain. Aging Cell 3:373–377CrossRef PubMed
  Jin K, Sun Y, Xie L, et al. (2003) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2:175–183CrossRef PubMed
  Jolkkonen J, Puurunen K, Rantakomi S, Sirvio J, Haapalinna A, Sivenius J (2000) Effects-of fluoxetine on sensorimotor and spatial learning deficits following focal cerebral ischemia in rats. Restor Neurol Neurosci 17:211–216PubMed
  Jorgensen HS, Nakayama H, Raaschou HO, Vive-Larsen J, Stoier M. Olsen TS (1995) Outcome and time course of recovery in stroke. Part I: outcome. The Copenhagen Stroke Study. Arch Phys Med Rehabil 76, 399–405.CrossRef PubMed
  Kelly-Hayes M, Beiser A, Kase CS, Scaramucci A, D’Agostino RB, Wolf PA (2003) The influence of gender and age on disability following ischemic stroke: the Framingham study. J Stroke Cerebrovasc Dis 12:119–126CrossRef PubMed
  Kodama M, Fujioka T, Duman RS (2004) Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol Psychiatry 56:570–580CrossRef PubMed
  Li WL, Cai HH, Wang B, et al. (2009) Chronic fluoxetine treatment improves ischemia-induced spatial cognitive deficits through increasing hippocampal neurogenesis after stroke. J Neurosci Res 87:112–122CrossRef PubMed
  Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104–9110PubMed
  Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004) Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24:1726–1733CrossRef PubMed
  Mikami K, Jorge RE, Adams Jr HP, et al. (2011) Effect of antidepressants on the course of disability following stroke. Am J Geriatr Psychiatr 19:1007–1015CrossRef
  Nannetti L, Paci M, Pasquini J, Lombardi B, Taiti PG (2005) Motor and functional recovery in patients with post-stroke depression. Disabil Rehabil 27:170–175CrossRef PubMed
  Niv F, Keiner S, Krishna WOW, Lie DC, Redecker C (2012) Aberrant neurogenesis after stroke: a retroviral cell labeling study. Stroke 43:2468–2475CrossRef PubMed
  Ohira K, Miyakawa T (2011) Chronic treatment with fluoxetine for more than 6 weeks decreases neurogenesis in the subventricular zone of adult mice. Mol Brain 4:10PubMedCentral CrossRef PubMed
  Pariente J, Loubinoux I, Carel C, et al. (2001) Fluoxetine modulates motor performance and cerebral activation of patients recovering from stroke. Ann Neurol 50:718–729CrossRef PubMed
  Peters R (2006) Ageing and the brain. Postgrad Med J 82:84–88PubMedCentral CrossRef PubMed
  Pitkanen A (2003) Clinical trials in neuroprotection. 23–25 January 2003, Key biscayne, FL, USA. IDrugs 6:200–202PubMed
  Popa-Wagner A, Buga AM, Kokaia Z (2011) Perturbed cellular response to brain injury during aging. Ageing Res Rev 10:71–79CrossRef PubMed
  Popa-Wagner A, Buga AM, Turner RC, Rosen CL, Toescu E (2012) Cerebrovascular disorders: role of aging. J Aging Res 2012:128146PubMedCentral CrossRef PubMed
  Popa-Wagner A, Carmichael ST, Kokaia Z, Kessler C, Walker LC (2007) The response of the aged brain to stroke: too much, too soon? Curr Neurovasc Res 4:216–227CrossRef PubMed
  Popp A, Jaenisch N, Witte OW, Frahm C (2009) Identification of ischemic regions in a rat model of stroke. PLoS One 4:e4764PubMedCentral CrossRef PubMed
  Possamai F, dos Santos J, Walber T, Marcon JC, dos Santos TS, Lino de Oliveira C (2015) Influence of enrichment on behavioral and neurogenic effects of antidepressants in Wistar rats submitted to repeated forced swim test. Prog Neuro-Psychopharmacol Biol Psychiatry 58:15–21CrossRef
  Qu HL, Zhao M, Zhao SS, et al. (2015) Forced limb-use enhanced neurogenesis and behavioral recovery after stroke in the aged rats. Neuroscience 286:316–324CrossRef PubMed
  Robinson RG (1998) Treatment issues in poststroke depression. Depress Anxiety 8(Suppl 1):85–90CrossRef PubMed
  Rosen CL, Dinapoli VA, Nagamine T, Crocco T (2005) Influence of age on stroke outcome following transient focal ischemia. J Neurosurg 103:687–694CrossRef PubMed
  Santarelli L, Saxe M, Gross C, et al. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805–809CrossRef PubMed
  Schallert T, Kozlowski DA, Humm JL, Cocke RR (1997) Use-dependent structural events in recovery of function. Adv Neurol 73:229–238PubMed
  Schallert T, Lindner MD (1990) Rescuing neurons from trans-synaptic degeneration after brain damage: helpful, harmful, or neutral in recovery of function? Can J Psychol 44:276–292CrossRef PubMed
  Sun X, Liu T, Zhao M, et al. (2015) Fluoxetine enhanced neurogenesis is not translated to functional outcome in stroke rats. Neurosci Lett 603:31–36CrossRef PubMed
  Surget A, Saxe M, Leman S, et al. (2008) Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol Psychiatry 64:293–301CrossRef PubMed
  Thored P, Arvidsson A, Cacci E, et al. (2006) Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24:739–747CrossRef PubMed
  Wang J-W, David DJ, Monckton JE, Battaglia F, Hen R (2008) Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J Neurosci 28:1374–1384CrossRef PubMed
  Wilson MS, Hamm RJ (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 81:364–372CrossRef PubMed
  Windle V, Corbett D (2005) Fluoxetine and recovery of motor function after focal ischemia in rats. Brain Res 1044:25–32CrossRef PubMed
  Zhao CS, Puurunen K, Schallert T, Sivenius J, Jolkkonen J (2005) Effect of cholinergic medication, before and after focal photothrombotic ischemic cortical injury, on histological and functional outcome in aged and young adult rats. Behav Brain Res 156:85–94CrossRef PubMed
  Zhao S, Zhao M, Xiao T, Jolkkonen J, Zhao C (2013) Constraint-induced movement therapy overcomes the intrinsic axonal growth-inhibitory signals in stroke rats. Stroke 44:1698–1705CrossRef PubMed
  
• 作者单位：Xiaoyu Sun (1)
  Zhike Zhou (1)
  Tingting Liu (1)
  Mei Zhao (2)
  Shanshan Zhao (1)
  Ting Xiao (3) (4)
  Jukka Jolkkonen (5)
  Chuansheng Zhao (1)
  
  1. Neurology, The First Hospital of China Medical University, No.155, North Nanjing Street, Heping District, Shenyang, Liaoning, 110001, China
  2. Cardiology, Shengjing Hospital of China Medical University, Shenyang, China
  3. Dermatology, The First Hospital of China Medical University, Shenyang, China
  4. Key Laboratory of Immunodermatology, Ministry of Health, Ministry of Education, Shenyang, China
  5. Institute of Clinical Medicine – Neurology, University of Eastern Finland, P. O. Box 1627, 70211, Kuopio, Finland
  
• 刊物主题：Neurosciences; Neurochemistry; Cell Biology; Proteomics; Neurology;
• 出版者：Springer US
• ISSN：1559-1166

文摘

Age is associated with poor outcome and impaired functional recovery after stroke. Fluoxetine, which is widely used in clinical practice, can regulate hippocampal neurogenesis in young rodents. As the rate of neurogenesis is dramatically reduced during aging, we studied the effect of post-stroke fluoxetine treatment on neurogenesis in the subventricular zone (SVZ) and subgranular zone (SGZ) of dentate gyrus (DG) and whether this would be associated with any behavioral recovery after the cortical infarct in aged rats. Aged rats were randomly assigned to four groups: sham-operated rats, sham-operated rats treated with fluoxetine, rats subjected to cerebral ischemia, and rats with ischemia treated with fluoxetine. Focal cortical ischemia was induced by intracranial injection of vasoconstrictive peptide, endothelin-1 (ET-1). Fluoxetine was administered in the drinking water for 3 weeks starting 1 week after ischemia at a dose of 18 mg/kg/day. Behavioral recovery was evaluated on post-stroke days 29 to 31 after which the survival rate and fate of proliferating cells in the SVZ and DG were assessed by immunohistochemistry. Apoptosis was measured with the TUNEL assay. The results indicated that chronic fluoxetine treatment after stroke enhanced the proliferation of newborn neurons in the SVZ, but not in SGZ, and it suppressed perilesional apoptosis. Fluoxetine treatment did not affect the survival or differentiation of newly generated cells in the SVZ i.e., the enhanced neurogenesis was not translated into a behavioral outcome. Keywords Aging Behavioral recovery Selective serotonin reuptake inhibitors Neurogenesis Cerebral ischemia