Predator stress-induced depression is associated with inhibition of hippocampal neurogenesis in adult male mice
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摘要
Stress has been suggested to disturb the 5-hydroxytryptamine system and decrease neurogenesis, which contribute to the development of depression. Few studies have investigated the effect of predator stress, a type of psychological stress, on depression and hippocampal neurogenesis in adult mice; we therefore investigated this in the present study. A total of 35 adult male Kunming mice were allocated to a cat stress group, cat odor stress group, cat stress + fluoxetine group, cat odor stress + fluoxetine group, or a control group(no stress/treatment). After 12 days of cat stress or cat odor stress, behavioral correlates of depression were measured using the open field test, elevated plus maze test, and dark-avoidance test. The concentrations of hippocampal 5-hydroxytryptamine and 5-hydroxyindoleacetic acid were measured using high-performance liquid chromatography-electrochemical detection. Neurogenesis was also analyzed using a bromodeoxyuridine and doublecortin double-immunostaining method. Cat stress and cat odor stress induced depression-like behaviors; this effect was stronger in the cat stress model. Furthermore, compared with the control group, cat stress mice exhibited lower 5-hydroxytryptamine concentrations, higher 5-hydroxyindoleacetic acid concentrations, and significantly fewer bromodeoxyuridine+/doublecortin+-labeled cells in the dentate gyrus, which was indicative of less neurogenesis. The changes observed in the cat stress group were not seen in the cat stress + fluoxetine group, which suggests that the effects of predator stress on depression and neurogenesis were reversed by fluoxetine. Taken together, our results indicate that depression-like behaviors induced by predator stress are associated with the inhibition of hippocampal neurogenesis.
Stress has been suggested to disturb the 5-hydroxytryptamine system and decrease neurogenesis, which contribute to the development of depression. Few studies have investigated the effect of predator stress, a type of psychological stress, on depression and hippocampal neurogenesis in adult mice; we therefore investigated this in the present study. A total of 35 adult male Kunming mice were allocated to a cat stress group, cat odor stress group, cat stress + fluoxetine group, cat odor stress + fluoxetine group, or a control group(no stress/treatment). After 12 days of cat stress or cat odor stress, behavioral correlates of depression were measured using the open field test, elevated plus maze test, and dark-avoidance test. The concentrations of hippocampal 5-hydroxytryptamine and 5-hydroxyindoleacetic acid were measured using high-performance liquid chromatography-electrochemical detection. Neurogenesis was also analyzed using a bromodeoxyuridine and doublecortin double-immunostaining method. Cat stress and cat odor stress induced depression-like behaviors; this effect was stronger in the cat stress model. Furthermore, compared with the control group, cat stress mice exhibited lower 5-hydroxytryptamine concentrations, higher 5-hydroxyindoleacetic acid concentrations, and significantly fewer bromodeoxyuridine+/doublecortin+-labeled cells in the dentate gyrus, which was indicative of less neurogenesis. The changes observed in the cat stress group were not seen in the cat stress + fluoxetine group, which suggests that the effects of predator stress on depression and neurogenesis were reversed by fluoxetine. Taken together, our results indicate that depression-like behaviors induced by predator stress are associated with the inhibition of hippocampal neurogenesis.
Stress has been suggested to disturb the 5-hydroxytryptamine system and decrease neurogenesis, which contribute to the development of depression. Few studies have investigated the effect of predator stress, a type of psychological stress, on depression and hippocampal neurogenesis in adult mice; we therefore investigated this in the present study. A total of 35 adult male Kunming mice were allocated to a cat stress group, cat odor stress group, cat stress + fluoxetine group, cat odor stress + fluoxetine group, or a control group(no stress/treatment). After 12 days of cat stress or cat odor stress, behavioral correlates of depression were measured using the open field test, elevated plus maze test, and dark-avoidance test. The concentrations of hippocampal 5-hydroxytryptamine and 5-hydroxyindoleacetic acid were measured using high-performance liquid chromatography-electrochemical detection. Neurogenesis was also analyzed using a bromodeoxyuridine and doublecortin double-immunostaining method. Cat stress and cat odor stress induced depression-like behaviors; this effect was stronger in the cat stress model. Furthermore, compared with the control group, cat stress mice exhibited lower 5-hydroxytryptamine concentrations, higher 5-hydroxyindoleacetic acid concentrations, and significantly fewer bromodeoxyuridine+/doublecortin+-labeled cells in the dentate gyrus, which was indicative of less neurogenesis. The changes observed in the cat stress group were not seen in the cat stress + fluoxetine group, which suggests that the effects of predator stress on depression and neurogenesis were reversed by fluoxetine. Taken together, our results indicate that depression-like behaviors induced by predator stress are associated with the inhibition of hippocampal neurogenesis.
引文
Airan RD,Meltzer LA,Roy M,Gong Y,Chen H,Deisseroth K(2007)High-speed imaging reveals neurophysiological links to behavior in an animal model of depression.Science 317:819-823.
Apfelbach R,Blanchard CD,Blanchard RJ,Hayes RA,McGregor IS(2005)The effects of predator odors in mammalian prey species:a review of field and laboratory studies.Neurosci Biobehav Rev29:1123-1144.
Bourin M,Hasco?t M(2003)The mouse light/dark box test.Eur JPharmacol 463:55-65.
Brezun JM,Daszuta A(2000)Serotonin may stimulate granule cell proliferation in the adult hippocampus,as observed in rats grafted with foetal raphe neurons.Eur J Neurosci 12:391-396.
Burgado J,Harrell CS,Eacret D,Reddy R,Barnum CJ,Tansey MG,Miller AH,Wang H,Neigh GN(2014)Two weeks of predatory stress induces anxiety-like behavior with co-morbid depressive-like behavior in adult male mice.Behav Brain Res 275:120-125.
Chen G,Rajkowska G,Du F,Seraji‐Bozorgzad N,Manji HK(2000)Enhancement of hippocampal neurogenesis by lithium.J Neurochem 75:1729-1734.
Cryan JF,Mombereau C(2004)In search of a depressed mouse:utility of models for studying depression-related behavior in genetically modified mice.Mol Psychiatry 9:326-357.
David DJ,Samuels BA,Rainer Q,Wang J-W,Marsteller D,Mendez I,Drew M,Craig DA,Guiard BP,Guilloux JP(2009)Neurogenesis-dependent and-independent effects of fluoxetine in an animal model of anxiety/depression.Neuron 62:479-493.
Drapier D,Bentue-Ferrer D,Laviolle B,Millet B,Allain H,Bourin M,Reymann J-M(2007)Effects of acute fluoxetine,paroxetine and desipramine on rats tested on the elevated plus-maze.Behav Brain Res176:202-209.
Dulawa SC,Hollick KA,Gundersen B,Hen R(2004)Effects of chronic fluoxetine in animal models of anxiety and depression.Neuropsychopharmacology 29:1321-1330.
Duman RS,Malberg J,Thome J(1999)Neural plasticity to stress and antidepressant treatment.Biol Psychiatry 46:1181-1191.
Duric V,Banasr M,Licznerski P,Schmidt HD,Stockmeier CA,Simen AA,Newton SS,Duman RS(2010)A negative regulator of MAP kinase causes depressive behavior.Nat Med 16:1328-1332.
Fleshner M,Campisi J,Amiri L,Diamond DM(2004)Cat exposure induces both intra-and extracellular Hsp72:the role of adrenal hormones.Psychoneuroendocrinology 29:1142-1152.
Gould E,Tanapat P,McEwen BS,Flügge G,Fuchs E(1998)Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress.Proc Natl Acad Sci U S A 95:3168-3171.
Guo X,Ma Z,Du B,Li T,Li W,Xu L,He J,Kang L(2018)Dop1 enhances conspecific olfactory attraction by inhibiting miR-9a maturation in locusts.Nat Commun 9:1193.
Guo YS,Kong LD,Wang YM,Huang ZQ(2004)Antidepressant evaluation of polysaccharides from a Chinese herbal medicine Banxia-houpu decoction.Phytother Res 18:204-207.
Hall C,Ballachey EL(1932)A study of the rat’s behavior in a field:a contribution to method in comparative psychology.Los Angeles:University of California Publications in Psychology,USA.
Hogg S(1996)A review of the validity and variability of the elevated plus-maze as an animal model of anxiety.Pharmacol Biochem Behav54:21-30.
Hong CJ,Tsai SJ,Cheng CY,Liao WY,Song HL,Lai HC(1999)Association analysis of the 5-HT6 receptor polymorphism(C267T)in mood disorders.Am J Med Genet 88:601-602.
Imoto Y,Kira T,Sukeno M,Nishitani N,Nagayasu K,Nakagawa T,Kaneko S,Kobayashi K,Segi-Nishida E(2015)Role of the 5-HT 4receptor in chronic fluoxetine treatment-induced neurogenic activity and granule cell dematuration in the dentate gyrus.Mol Brain 8:29.
Jiang XW,Zhang BQ,Qiao L,Liu L,Wang XW,Yu WH(2018)Acetyl-11-keto-β-boswellic acid extracted from Boswellia serrata promotes Schwann cell proliferation and sciatic nerve function recovery.Neural Regen Res 13:484.
Kempermann G(2002)Regulation of adult hippocampal neurogenesis-implications for novel theories of major depression.Bipolar Disord 4:17-33.
Kempermann G,Kronenberg G(2003)Depressed new neurons?Adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression.Biol Psychiatry 54:499-503.
Kendig MD,Bowen MT,Kemp AH,McGregor IS(2011)Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience.Behav Brain Res225:405-414.
Kobayashi K,Ikeda Y,Sakai A,Yamasaki N,Haneda E,Miyakawa T,Suzuki H(2010)Reversal of hippocampal neuronal maturation by serotonergic antidepressants.Proc Natl Acad Sci U S A 107:8434-8439.
Kung JC,Chen TC,Shyu BC,Hsiao S,Huang AC(2010)Anxiety-and depressive-like responses and c-fos activity in preproenkephalin knockout mice:oversensitivity hypothesis of enkephalin deficit-induced posttraumatic stress disorder.J Biomed Sci 17:29.
Lemaire V,Koehl M,Le Moal M,Abrous D(2000)Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus.Proc Natl Acad Sci U S A 97:11032-11037.
Li JP,Lu W,Yang L,Xie MX,He X,Pan AH(2017)Neurons in the hippocampus of chemobrain versus non-chemotherapy brain.Zhongguo Zuzhi Gongcheng Yanjiu 21:4523-4528.
Lu KT,Huang TC,Wang JY,You YS,Chou JL,Chan MW,Wo PY,Amstislavskaya TG,Tikhonova MA,Yang YL(2015)NKCC1 mediates traumatic brain injury-induced hippocampal neurogenesis through CREB phosphorylation and HIF-1αexpression.Pflugers Arch 467:1651-1661.
Mahar I,Bambico FR,Mechawar N,Nobrega JN(2014)Stress,serotonin,and hippocampal neurogenesis in relation to depression and antidepressant effects.Neurosci Biobehav Rev 38:173-192.
Manduca A,Morena M,Campolongo P,Servadio M,Palmery M,Trabace L,Hill MN,Vanderschuren LJMJ,Cuomo V,Trezza V(2015)Distinct roles of the endocannabinoids anandamide and 2-arachidonoylglycerol in social behavior and emotionality at different developmental ages in rats.Eur Neuropsychopharmacol 25:1362-1374.
McEwen BS(1999)Stress and hippocampal plasticity.Annu Rev Neurosci 22:105-122.
Meduri JD,Farnbauch LA,Jasnow AM(2013)Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat.Behav Brain Res 256:580-590.
Mineur YS,Belzung C,Crusio WE(2006)Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice.Behav Brain Res 175:43-50.
Mirescu C,Gould E(2006)Stress and adult neurogenesis.Hippocampus 16:233.
Narrow WE,Rae DS,Robins LN,Regier DA(2002)Revised prevalence estimates of mental disorders in the United States:using a clinical significance criterion to reconcile 2 surveys’estimates.Arch Gen Psychiatry 59:115-123.
Post RJ,Dahlborg KM,O’Loughlin LE,Bloom CM(2014)Effects of juvenile exposure to predator odor on adolescent and adult anxiety and pain nociception.Physiol Behav 131:57-61.
Reif A,Fritzen S,Finger M,Strobel A,Lauer M,Schmitt A,Lesch K(2006)Neural stem cell proliferation is decreased in schizophrenia,but not in depression.Mol Psychiatry 11:514-522.
Saboory E,Ahmadzadeh R,Roshan-Milani S(2011)Prenatal exposure to restraint or predator stresses attenuates field excitatory postsynaptic potentials in infant rats.Int J Dev Neurosci 29:827-831.
Sachs BD,Ni JR,Caron MG(2015)Brain 5-HT deficiency increases stress vulnerability and impairs antidepressant responses following psychosocial stress.Proc Natl Acad Sci U S A 112:2557-2562.
Seidenbecher T,Remmes J,Daldrup T,Lesting J,Pape HC(2016)Distinct state anxiety after predictable and unpredictable fear training in mice.Behav Brain Res 304:20-23.
Shioda N,Han F,Morioka M,Fukunaga K(2008)Bis(1-oxy-2-pyridinethiolato)oxovanadium(IV)enhances neurogenesis via phosphatidylinositol 3-kinase/Akt and extracellular signal regulated kinase activation in the hippocampal subgranular zone after mouse focal cerebral ischemia.Neuroscience 155:876-887.
Silva RCB,Brandao ML(2000)Acute and chronic effects of gepirone and fluoxetine in rats tested in the elevated plus-maze:An ethological analysis.Pharmacol Biochem Behav 65:209-216.
Snyder JS,Soumier A,Brewer M,Pickel J,Cameron HA(2011)Adult hippocampal neurogenesis buffers stress responses and depressive behaviour.Nature 476:458-461.
Steenbergen PJ,Richardson MK,Champagne DL(2011)Patterns of avoidance behaviours in the light/dark preference test in young juvenile zebrafish:a pharmacological study.Behav Brain Res 222:15-25.
Takahashi LK,Nakashima BR,Hong H,Watanabe K(2005)The smell of danger:a behavioral and neural analysis of predator odor-induced fear.Neurosci Biobehav Rev 29:1157-1167.
Tashiro A,Sandler VM,Toni N,Zhao C,Gage FH(2006)NMDA-receptor-mediated,cell-specific integration of new neurons in adult dentate gyrus.Nature 442:929-933.
Tawarayama H(2018)Novel function of the chemorepellent draxin as a regulator for hippocampal neurogenesis.Neural Regen Res 13:799-800.
Toledo M,Sandi C(2011)Stress during adolescence increases novelty seeking and risk-taking behavior in male and female rats.Front Behav Neurosci 5:17.
Tsoory M,Cohen H,Richter-Levin G(2007)Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood.Eur Neuropsychopharmacol 17:245-256.
Van Praag H,Kempermann G,Gage FH(1999)Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus.Nat Neurosci2:266.
Wainwright SR,Galea LA(2013)The neural plasticity theory of depression:assessing the roles of adult neurogenesis and PSA-NCAMwithin the hippocampus.Neural Plast 2013:805497.
Walf AA,Frye CA(2007)The use of the elevated plus maze as an assay of anxiety-related behavior in rodents.Nat Protoc 2:322.
Wright LD,Muir KE,Perrot TS(2013)Stress responses of adolescent male and female rats exposed repeatedly to cat odor stimuli,and long‐term enhancement of adult defensive behaviors.Dev Psychobiol 55:551-567.
Yang S,Liu L,Cao C,Song N,Wang Y,Ma S,Zhang Q,Yu N,Ding X,Yang F,Tian S,Zhang K,Sun T,Yang J,Yao Z,Wu S,Shi L(2018)USP52 acts as a deubiquitinase and promotes histone chaperone AS-F1A stabilization.Nat Commun 9:1285.
Zhang XH,Feng ZH,Wang XY(2018)The ROCK pathway inhibitor Y-27632 mitigates hypoxia and oxidative stress-induced injury to retinal Müller cells.Neural Regen Res 13:549.
Apfelbach R,Blanchard CD,Blanchard RJ,Hayes RA,McGregor IS(2005)The effects of predator odors in mammalian prey species:a review of field and laboratory studies.Neurosci Biobehav Rev29:1123-1144.
Bourin M,Hasco?t M(2003)The mouse light/dark box test.Eur JPharmacol 463:55-65.
Brezun JM,Daszuta A(2000)Serotonin may stimulate granule cell proliferation in the adult hippocampus,as observed in rats grafted with foetal raphe neurons.Eur J Neurosci 12:391-396.
Burgado J,Harrell CS,Eacret D,Reddy R,Barnum CJ,Tansey MG,Miller AH,Wang H,Neigh GN(2014)Two weeks of predatory stress induces anxiety-like behavior with co-morbid depressive-like behavior in adult male mice.Behav Brain Res 275:120-125.
Chen G,Rajkowska G,Du F,Seraji‐Bozorgzad N,Manji HK(2000)Enhancement of hippocampal neurogenesis by lithium.J Neurochem 75:1729-1734.
Cryan JF,Mombereau C(2004)In search of a depressed mouse:utility of models for studying depression-related behavior in genetically modified mice.Mol Psychiatry 9:326-357.
David DJ,Samuels BA,Rainer Q,Wang J-W,Marsteller D,Mendez I,Drew M,Craig DA,Guiard BP,Guilloux JP(2009)Neurogenesis-dependent and-independent effects of fluoxetine in an animal model of anxiety/depression.Neuron 62:479-493.
Drapier D,Bentue-Ferrer D,Laviolle B,Millet B,Allain H,Bourin M,Reymann J-M(2007)Effects of acute fluoxetine,paroxetine and desipramine on rats tested on the elevated plus-maze.Behav Brain Res176:202-209.
Dulawa SC,Hollick KA,Gundersen B,Hen R(2004)Effects of chronic fluoxetine in animal models of anxiety and depression.Neuropsychopharmacology 29:1321-1330.
Duman RS,Malberg J,Thome J(1999)Neural plasticity to stress and antidepressant treatment.Biol Psychiatry 46:1181-1191.
Duric V,Banasr M,Licznerski P,Schmidt HD,Stockmeier CA,Simen AA,Newton SS,Duman RS(2010)A negative regulator of MAP kinase causes depressive behavior.Nat Med 16:1328-1332.
Fleshner M,Campisi J,Amiri L,Diamond DM(2004)Cat exposure induces both intra-and extracellular Hsp72:the role of adrenal hormones.Psychoneuroendocrinology 29:1142-1152.
Gould E,Tanapat P,McEwen BS,Flügge G,Fuchs E(1998)Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress.Proc Natl Acad Sci U S A 95:3168-3171.
Guo X,Ma Z,Du B,Li T,Li W,Xu L,He J,Kang L(2018)Dop1 enhances conspecific olfactory attraction by inhibiting miR-9a maturation in locusts.Nat Commun 9:1193.
Guo YS,Kong LD,Wang YM,Huang ZQ(2004)Antidepressant evaluation of polysaccharides from a Chinese herbal medicine Banxia-houpu decoction.Phytother Res 18:204-207.
Hall C,Ballachey EL(1932)A study of the rat’s behavior in a field:a contribution to method in comparative psychology.Los Angeles:University of California Publications in Psychology,USA.
Hogg S(1996)A review of the validity and variability of the elevated plus-maze as an animal model of anxiety.Pharmacol Biochem Behav54:21-30.
Hong CJ,Tsai SJ,Cheng CY,Liao WY,Song HL,Lai HC(1999)Association analysis of the 5-HT6 receptor polymorphism(C267T)in mood disorders.Am J Med Genet 88:601-602.
Imoto Y,Kira T,Sukeno M,Nishitani N,Nagayasu K,Nakagawa T,Kaneko S,Kobayashi K,Segi-Nishida E(2015)Role of the 5-HT 4receptor in chronic fluoxetine treatment-induced neurogenic activity and granule cell dematuration in the dentate gyrus.Mol Brain 8:29.
Jiang XW,Zhang BQ,Qiao L,Liu L,Wang XW,Yu WH(2018)Acetyl-11-keto-β-boswellic acid extracted from Boswellia serrata promotes Schwann cell proliferation and sciatic nerve function recovery.Neural Regen Res 13:484.
Kempermann G(2002)Regulation of adult hippocampal neurogenesis-implications for novel theories of major depression.Bipolar Disord 4:17-33.
Kempermann G,Kronenberg G(2003)Depressed new neurons?Adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression.Biol Psychiatry 54:499-503.
Kendig MD,Bowen MT,Kemp AH,McGregor IS(2011)Predatory threat induces huddling in adolescent rats and residual changes in early adulthood suggestive of increased resilience.Behav Brain Res225:405-414.
Kobayashi K,Ikeda Y,Sakai A,Yamasaki N,Haneda E,Miyakawa T,Suzuki H(2010)Reversal of hippocampal neuronal maturation by serotonergic antidepressants.Proc Natl Acad Sci U S A 107:8434-8439.
Kung JC,Chen TC,Shyu BC,Hsiao S,Huang AC(2010)Anxiety-and depressive-like responses and c-fos activity in preproenkephalin knockout mice:oversensitivity hypothesis of enkephalin deficit-induced posttraumatic stress disorder.J Biomed Sci 17:29.
Lemaire V,Koehl M,Le Moal M,Abrous D(2000)Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus.Proc Natl Acad Sci U S A 97:11032-11037.
Li JP,Lu W,Yang L,Xie MX,He X,Pan AH(2017)Neurons in the hippocampus of chemobrain versus non-chemotherapy brain.Zhongguo Zuzhi Gongcheng Yanjiu 21:4523-4528.
Lu KT,Huang TC,Wang JY,You YS,Chou JL,Chan MW,Wo PY,Amstislavskaya TG,Tikhonova MA,Yang YL(2015)NKCC1 mediates traumatic brain injury-induced hippocampal neurogenesis through CREB phosphorylation and HIF-1αexpression.Pflugers Arch 467:1651-1661.
Mahar I,Bambico FR,Mechawar N,Nobrega JN(2014)Stress,serotonin,and hippocampal neurogenesis in relation to depression and antidepressant effects.Neurosci Biobehav Rev 38:173-192.
Manduca A,Morena M,Campolongo P,Servadio M,Palmery M,Trabace L,Hill MN,Vanderschuren LJMJ,Cuomo V,Trezza V(2015)Distinct roles of the endocannabinoids anandamide and 2-arachidonoylglycerol in social behavior and emotionality at different developmental ages in rats.Eur Neuropsychopharmacol 25:1362-1374.
McEwen BS(1999)Stress and hippocampal plasticity.Annu Rev Neurosci 22:105-122.
Meduri JD,Farnbauch LA,Jasnow AM(2013)Paradoxical enhancement of fear expression and extinction deficits in mice resilient to social defeat.Behav Brain Res 256:580-590.
Mineur YS,Belzung C,Crusio WE(2006)Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice.Behav Brain Res 175:43-50.
Mirescu C,Gould E(2006)Stress and adult neurogenesis.Hippocampus 16:233.
Narrow WE,Rae DS,Robins LN,Regier DA(2002)Revised prevalence estimates of mental disorders in the United States:using a clinical significance criterion to reconcile 2 surveys’estimates.Arch Gen Psychiatry 59:115-123.
Post RJ,Dahlborg KM,O’Loughlin LE,Bloom CM(2014)Effects of juvenile exposure to predator odor on adolescent and adult anxiety and pain nociception.Physiol Behav 131:57-61.
Reif A,Fritzen S,Finger M,Strobel A,Lauer M,Schmitt A,Lesch K(2006)Neural stem cell proliferation is decreased in schizophrenia,but not in depression.Mol Psychiatry 11:514-522.
Saboory E,Ahmadzadeh R,Roshan-Milani S(2011)Prenatal exposure to restraint or predator stresses attenuates field excitatory postsynaptic potentials in infant rats.Int J Dev Neurosci 29:827-831.
Sachs BD,Ni JR,Caron MG(2015)Brain 5-HT deficiency increases stress vulnerability and impairs antidepressant responses following psychosocial stress.Proc Natl Acad Sci U S A 112:2557-2562.
Seidenbecher T,Remmes J,Daldrup T,Lesting J,Pape HC(2016)Distinct state anxiety after predictable and unpredictable fear training in mice.Behav Brain Res 304:20-23.
Shioda N,Han F,Morioka M,Fukunaga K(2008)Bis(1-oxy-2-pyridinethiolato)oxovanadium(IV)enhances neurogenesis via phosphatidylinositol 3-kinase/Akt and extracellular signal regulated kinase activation in the hippocampal subgranular zone after mouse focal cerebral ischemia.Neuroscience 155:876-887.
Silva RCB,Brandao ML(2000)Acute and chronic effects of gepirone and fluoxetine in rats tested in the elevated plus-maze:An ethological analysis.Pharmacol Biochem Behav 65:209-216.
Snyder JS,Soumier A,Brewer M,Pickel J,Cameron HA(2011)Adult hippocampal neurogenesis buffers stress responses and depressive behaviour.Nature 476:458-461.
Steenbergen PJ,Richardson MK,Champagne DL(2011)Patterns of avoidance behaviours in the light/dark preference test in young juvenile zebrafish:a pharmacological study.Behav Brain Res 222:15-25.
Takahashi LK,Nakashima BR,Hong H,Watanabe K(2005)The smell of danger:a behavioral and neural analysis of predator odor-induced fear.Neurosci Biobehav Rev 29:1157-1167.
Tashiro A,Sandler VM,Toni N,Zhao C,Gage FH(2006)NMDA-receptor-mediated,cell-specific integration of new neurons in adult dentate gyrus.Nature 442:929-933.
Tawarayama H(2018)Novel function of the chemorepellent draxin as a regulator for hippocampal neurogenesis.Neural Regen Res 13:799-800.
Toledo M,Sandi C(2011)Stress during adolescence increases novelty seeking and risk-taking behavior in male and female rats.Front Behav Neurosci 5:17.
Tsoory M,Cohen H,Richter-Levin G(2007)Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood.Eur Neuropsychopharmacol 17:245-256.
Van Praag H,Kempermann G,Gage FH(1999)Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus.Nat Neurosci2:266.
Wainwright SR,Galea LA(2013)The neural plasticity theory of depression:assessing the roles of adult neurogenesis and PSA-NCAMwithin the hippocampus.Neural Plast 2013:805497.
Walf AA,Frye CA(2007)The use of the elevated plus maze as an assay of anxiety-related behavior in rodents.Nat Protoc 2:322.
Wright LD,Muir KE,Perrot TS(2013)Stress responses of adolescent male and female rats exposed repeatedly to cat odor stimuli,and long‐term enhancement of adult defensive behaviors.Dev Psychobiol 55:551-567.
Yang S,Liu L,Cao C,Song N,Wang Y,Ma S,Zhang Q,Yu N,Ding X,Yang F,Tian S,Zhang K,Sun T,Yang J,Yao Z,Wu S,Shi L(2018)USP52 acts as a deubiquitinase and promotes histone chaperone AS-F1A stabilization.Nat Commun 9:1285.
Zhang XH,Feng ZH,Wang XY(2018)The ROCK pathway inhibitor Y-27632 mitigates hypoxia and oxidative stress-induced injury to retinal Müller cells.Neural Regen Res 13:549.