Corticosterone Induced the Increase of proBDNF in Primary Hippocampal Neurons Via Endoplasmic Reticulum Stress.
Animals
Anti-Inflammatory Agents
/ pharmacology
Brain-Derived Neurotrophic Factor
/ drug effects
Corticosterone
/ pharmacology
Depressive Disorder, Major
Disks Large Homolog 4 Protein
/ drug effects
Endoplasmic Reticulum Chaperone BiP
Endoplasmic Reticulum Stress
/ drug effects
Follistatin-Related Proteins
/ drug effects
Hippocampus
/ cytology
Mice
Neurons
/ drug effects
Primary Cell Culture
Protein Precursors
/ drug effects
Receptors, N-Methyl-D-Aspartate
/ drug effects
Synaptophysin
/ metabolism
Corticosterone
Depression
Endoplasmic reticulum stress
Primary hippocampal neurons
proBDNF
Journal
Neurotoxicity research
ISSN: 1476-3524
Titre abrégé: Neurotox Res
Pays: United States
ID NLM: 100929017
Informations de publication
Date de publication:
Aug 2020
Aug 2020
Historique:
received:
01
01
2020
accepted:
01
04
2020
revised:
28
03
2020
pubmed:
8
5
2020
medline:
16
6
2021
entrez:
8
5
2020
Statut:
ppublish
Résumé
Major depression disorder is one of the most common psychiatric disorders that greatly threaten the mental health of a large population worldwide. Previous studies have shown that endoplasmic reticulum (ER) stress plays an important role in the pathophysiology of depression, and current research suggests that brain-derived neurotrophic factor precursor (proBDNF) is involved in the development of depression. However, the relationship between ER and proBDNF in the pathophysiology of depression is not well elucidated. Here, we treated primary hippocampal neurons of mice with corticosterone (CORT) and evaluated the relationship between proBDNF and ERS. Our results showed that CORT induced ERS and upregulated the expression of proBDNF and its receptor, Follistatin-like protein 4 (FSTL4), which contributed to significantly decreased neuronal viability and expression of synaptic-related proteins including NR2A, PSD95, and SYN. Anti-proBDNF neutralization and ISRIB (an inhibitor of the ERS) treatment, respective ly, protected neuronal viabilities and increased the expression of synaptic-related proteins in corticosterone-exposed neurons. ISRIB treatment reduced the expression of proBDNF and FSTL4, whereas anti-proBDNF treatment did not affect ERS markers (Grp78, p-PERK, ATF4) expression. Our study presented evidence that CORT-induced ERS negatively regulated the neuronal viability and the level of synaptic-related protein of primary neurons via the proBDNF/FSTL4 pathway.
Identifiants
pubmed: 32378057
doi: 10.1007/s12640-020-00201-4
pii: 10.1007/s12640-020-00201-4
doi:
Substances chimiques
Anti-Inflammatory Agents
0
Brain-Derived Neurotrophic Factor
0
Disks Large Homolog 4 Protein
0
Dlg4 protein, mouse
0
Endoplasmic Reticulum Chaperone BiP
0
Follistatin-Related Proteins
0
Fstl4 protein, mouse
0
Hspa5 protein, mouse
0
NR2A NMDA receptor
0
Protein Precursors
0
Receptors, N-Methyl-D-Aspartate
0
Synaptophysin
0
Syp protein, mouse
0
brain-derived neurotrophic factor precursor
0
Corticosterone
W980KJ009P
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
370-384Subventions
Organisme : National Natural Science Foundation of China (CN)
ID : 31371212
Organisme : National Natural Science Foundation of China (CN)
ID : 81760238
Organisme : National Natural Science Foundation of China
ID : 81571256
Organisme : National Natural Science Foundation of China
ID : 81771354
Organisme : National Natural Science Foundation of China
ID : 81471106
Organisme : National Natural Science Foundation of China
ID : 81471372
Organisme : National Natural Science Foundation of China
ID : 81901231
Organisme : Natural Science Foundation of Hunan Province
ID : 2018JJ3635
Organisme : Natural Science Foundation of Hunan Province
ID : 2019JJ40369
Organisme : Fundamental Research Funds for Central Universities of the Central South University
ID : 506021710
Organisme : Fundamental Research Funds for Central Universities of the Central South University
ID : 506021717
Références
Bai YY, Ruan CS, Yang CR, Li JY, Kang Z et al (2016) ProBDNF signaling regulates depression-like behaviors in rodents under chronic stress. Neuropsychopharmacology 41:2882–2892
pubmed: 27312407
pmcid: 5061880
Beluche I, Chaudieu I, Norton J, Carriere I, Boulenger JP et al (2009) Persistence of abnormal cortisol levels in elderly persons after recovery from major depression. J Psychiatr Res 43:777–783
pubmed: 19054531
Chen S, Liang T, Zhou FH, Cao Y, Wang C et al (2019) Regular music exposure in juvenile rats facilitates conditioned fear extinction and reduces anxiety after foot shock in adulthood. Biomed Res Int 2019:8740674
pubmed: 31380440
pmcid: 6662454
Cowansage KK, LeDoux JE, Monfils MH (2010) Brain-derived neurotrophic factor: a dynamic gatekeeper of neural plasticity. Curr Mol Pharmacol 3:12–29
pubmed: 20030625
De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M (1998) Brain corticosteroid receptor balance in health and disease. Endocr Rev 19:269–301
pubmed: 9626555
Donoso F, Ramirez VT, Golubeva AV, Moloney GM, Stanton C et al (2019) Naturally derived polyphenols protect against corticosterone-induced changes in primary cortical neurons. Int J Neuropsychopharmacol 22:765–777
pubmed: 31812985
pmcid: 6929673
Drevets WC (2000) Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Prog Brain Res 126:413–431
pubmed: 11105660
Duman RS (2004) Neural plasticity: consequences of stress and actions of antidepressant treatment. Dialogues Clin Neurosci 6:157–169
pubmed: 22034207
pmcid: 3181800
Duman RS, Aghajanian GK, Sanacora G, Krystal JH (2016) Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants. Nat Med 22:238–249
pubmed: 26937618
pmcid: 5405628
Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116–1127
pubmed: 16631126
pmcid: 16631126
Feyissa AM, Chandran A, Stockmeier CA, Karolewicz B (2009) Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog Neuro-Psychopharmacol Biol Psychiatry 33:70–75
Furuse K, Ukai W, Hashimoto E, Hashiguchi H, Kigawa Y, Ishii T, Tayama M, Deriha K, Shiraishi M, Kawanishi C (2019) Antidepressant activities of escitalopram and blonanserin on prenatal and adolescent combined stress-induced depression model: possible role of neurotrophic mechanism change in serum and nucleus accumbens. J Affect Disord 247:97–104
pubmed: 30658246
Geng ZH, Cheng YY, Ma XL, Li ST (2003) Effect of zinc on the corticosterone-induced injury of primary cultured rat hippocampal neurons. Sheng Li Xue Bao 55:736–741
pubmed: 14695494
Gong MJ, Han B, Wang SM, Liang SW, Zou ZJ (2016) Icariin reverses corticosterone-induced depression-like behavior, decrease in hippocampal brain-derived neurotrophic factor (BDNF) and metabolic network disturbances revealed by NMR-based metabonomics in rats. J Pharm Biomed Anal 123:63–73
pubmed: 26874256
Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, Scheimann J, Myers B (2016) Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol 6:603–621
pubmed: 27065163
pmcid: 4867107
Hiester BG, Galati DF, Salinas PC, Jones KR (2013) Neurotrophin and Wnt signaling cooperatively regulate dendritic spine formation. Mol Cell Neurosci 56:115–127
pubmed: 23639831
pmcid: 3793870
Huang EJ, Reichardt LF (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72:609–642
pubmed: 12676795
Jacobson L, Sapolsky R (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118–134
pubmed: 2070776
Jiang Y, Li Z, Liu Y, Liu X, Chang Q, Liao Y, Pan R (2015) Neuroprotective effect of water extract of Panax ginseng on corticosterone-induced apoptosis in PC12 cells and its underlying molecule mechanisms. J Ethnopharmacol 159:102–112
pubmed: 25446601
Joels M, Karst H, Sarabdjitsingh RA (2018) The stressed brain of humans and rodents. Acta Physiol (Oxf) 223:e13066
Keller J, Gomez R, Williams G, Lembke A, Lazzeroni L, Murphy GM Jr, Schatzberg AF (2017) HPA axis in major depression: cortisol, clinical symptomatology and genetic variation predict cognition. Mol Psychiatry 22:527–536
pubmed: 27528460
Kessing LV, Willer IS, Knorr U (2011) Volume of the adrenal and pituitary glands in depression. Psychoneuroendocrinology 36:19–27
pubmed: 20646833
Kim S, Joe Y, Jeong SO, Zheng M, Back SH, Park SW, Ryter SW, Chung HT (2014) Endoplasmic reticulum stress is sufficient for the induction of IL-1beta production via activation of the NF-kappaB and inflammasome pathways. Innate Immun 20:799–815
pubmed: 24217221
Latt HM, Matsushita H, Morino M, Koga Y, Michiue H, Nishiki T, Tomizawa K, Matsui H (2018) Oxytocin inhibits corticosterone-induced apoptosis in primary hippocampal neurons. Neuroscience 379:383–389
pubmed: 29596965
Lee AL, Ogle WO, Sapolsky RM (2002) Stress and depression: possible links to neuron death in the hippocampus. Bipolar Disord 4:117–128
pubmed: 12071509
Lee R, Kermani P, Teng KK, Hempstead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294:1945–1948
pubmed: 11729324
Li J, Chen J, Ma N, Yan D, Wang Y, Zhao X, Zhang Y, Zhang C (2019) Effects of corticosterone on the expression of mature brain-derived neurotrophic factor (mBDNF) and proBDNF in the hippocampal dentate gyrus. Behav Brain Res 365:150–156
pubmed: 30851317
Li J, Xie X, Li Y, Liu X, Liao X et al (2017) Differential behavioral and neurobiological effects of chronic corticosterone treatment in adolescent and adult rats. Front Mol Neurosci 10:25
pubmed: 28210212
pmcid: 5288376
Liu Y, Shen S, Li Z, Jiang Y, Si J, Chang Q, Liu X, Pan R (2014) Cajaninstilbene acid protects corticosterone-induced injury in PC12 cells by inhibiting oxidative and endoplasmic reticulum stress-mediated apoptosis. Neurochem Int 78:43–52
pubmed: 25193317
Liu YM, Hu CY, Shen JD, Wu SH, Li YC, Yi LT (2017) Elevation of synaptic protein is associated with the antidepressant-like effects of ferulic acid in a chronic model of depression. Physiol Behav 169:184–188
pubmed: 27940143
Luo C, Zhong XL, Zhou FH, Li JY, Zhou P, Xu JM, Song B, Li CQ, Zhou XF, Dai RP (2016) Peripheral brain derived neurotrophic factor precursor regulates pain as an inflammatory mediator. Sci Rep 6:27171
pubmed: 27251195
pmcid: 4890020
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
pubmed: 24300695
Malhi GS, Mann JJ (2018) Depression. Lancet 392:2299–2312
pubmed: 30396512
McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904
pubmed: 17615391
McKinnon MC, Yucel K, Nazarov A, MacQueen GM (2009) A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J Psychiatry Neurosci 34:41–54
pubmed: 19125212
pmcid: 2612082
Meller WH, Kathol RG, Samuelson SD, Gehris TL, Carroll BT, Pitts AF, Clayton PJ (1995) CRH challenge test in anxious depression. Biol Psychiatry 37:376–382
pubmed: 7772646
Murphy BE (1991) Steroids and depression. J Steroid Biochem Mol Biol 38:537–559
pubmed: 1645586
Nakatani Y, Tsuji M, Amano T, Miyagawa K, Miyagishi H, Saito A, Imai T, Takeda K, Ishii D, Takeda H (2014) Neuroprotective effect of yokukansan against cytotoxicity induced by corticosterone on mouse hippocampal neurons. Phytomedicine 21:1458–1465
pubmed: 25022209
Ngoupaye GT, Yassi FB, Bahane DAN, Bum EN (2018) Combined corticosterone treatment and chronic restraint stress lead to depression associated with early cognitive deficits in mice. Metab Brain Dis 33:421–431
pubmed: 29199383
Nitta A, Zheng WH, Quirion R (2004) Insulin-like growth factor 1 prevents neuronal cell death induced by corticosterone through activation of the PI3k/Akt pathway. J Neurosci Res 76:98–103
pubmed: 15048933
Oakes SA, Papa FR (2015) The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol 10:173–194
pubmed: 25387057
Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306:487–491
pubmed: 15486301
Pavitt GD, Ron D (2012) New insights into translational regulation in the endoplasmic reticulum unfolded protein response. Cold Spring Harb Perspect Biol 4
Peng R, Dai W, Li Y (2018) Neuroprotective effect of a physiological ratio of testosterone and estradiol on corticosterone-induced apoptosis in PC12 cells via Traf6/TAK1 pathway. Toxicol in Vitro 50:257–263
pubmed: 29625166
Rao ML, Vartzopoulos D, Fels K (1989) Thyroid function in anxious and depressed patients. Pharmacopsychiatry 22:66–70
pubmed: 2497474
Robinson SA, Brookshire BR, Lucki I (2016) Corticosterone exposure augments sensitivity to the behavioral and neuroplastic effects of fluoxetine in C57BL/6 mice. Neurobiol Stress 3:34–42
pubmed: 26844246
pmcid: 4730790
Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10:423–433
pubmed: 19469026
Sharma D, Barhwal KK, Biswal SN, Srivastava AK, Bhardwaj P, Kumar A, Chaurasia OP, Hota SK (2019) Hypoxia-mediated alteration in cholesterol oxidation and raft dynamics regulates BDNF signalling and neurodegeneration in hippocampus. J Neurochem 148:238–251
pubmed: 30308090
Shen LL, Mañucat-Tan NB, Gao SH, Li WW, Zeng F, Zhu C, Wang J, Bu XL, Liu YH, Gao CY, Xu ZQ, Bobrovskaya L, Lei P, Yu JT, Song W, Zhou HD, Yao XQ, Zhou XF, Wang YJ (2018) The ProNGF/p75NTR pathway induces tau pathology and is a therapeutic target for FTLD-tau. Mol Psychiatry 23:1813–1824
pubmed: 29867188
Sidrauski C, Acosta-Alvear D, Khoutorsky A, Vedantham P, Hearn BR, Li H, Gamache K, Gallagher CM, Ang KKH, Wilson C, Okreglak V, Ashkenazi A, Hann B, Nader K, Arkin MR, Renslo AR, Sonenberg N, Walter P (2013) Pharmacological brake-release of mRNA translation enhances cognitive memory. Elife 2:e00498
pubmed: 23741617
pmcid: 3667625
Smith K (2014) Mental health: a world of depression. Nature 515:181
pubmed: 25391942
Sterner EY, Kalynchuk LE (2010) Behavioral and neurobiological consequences of prolonged glucocorticoid exposure in rats: relevance to depression. Prog Neuro-Psychopharmacol Biol Psychiatry 34:777–790
Sun C, Liu N, Li H, Zhang M, Liu S et al (2004) Experimental study of effect of corticosterone on primary cultured hippocampal neurons and their Ca2+/CaMKII expression. J Huazhong Univ Sci Technolog Med Sci 24:543–546
pubmed: 15791835
Sun Y, Lim Y, Li F, Liu S, Lu JJ, Haberberger R, Zhong JH, Zhou XF (2012) ProBDNF collapses neurite outgrowth of primary neurons by activating. RhoA PLoS One 7:e35883
pubmed: 22558255
Suzuki R, Fujikawa A, Komatsu Y, Kuboyama K, Tanga N, Noda M (2018) Enhanced extinction of aversive memories in mice lacking SPARC-related protein containing immunoglobulin domains 1 (SPIG1/FSTL4). Neurobiol Learn Mem 152:61–70
pubmed: 29783061
Tafet GE, Nemeroff CB (2016) The links between stress and depression: psychoneuroendocrinological, genetic, and environmental interactions. J Neuropsychiatry Clin Neurosci 28:77–88
pubmed: 26548654
Teng HK, Teng KK, Lee R, Wright S, Tevar S et al (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 25:5455–5463
pubmed: 15930396
pmcid: 6724992
Tennant C (2002) Life events, stress and depression: a review of recent findings. Aust N Z J Psychiatry 36:173–182
pubmed: 11982537
Tu BX, Wang LF, Zhong XL, Hu ZL, Cao WY, Cui YH, Li SJ, Zou GJ, Liu Y, Zhou SF, Zhang WJ, Su JZ, Yan XX, Li F, Li CQ (2019) Acute restraint stress alters food-foraging behavior in rats: taking the easier way while suffered. Brain Res Bull 149:184–193
pubmed: 31034944
Willner P, Scheel-Kruger J, Belzung C (2013) The neurobiology of depression and antidepressant action. Neurosci Biobehav Rev 37:2331–2371
pubmed: 23261405
Woo NH, Teng HK, Siao CJ, Chiaruttini C, Pang PT, Milner TA, Hempstead BL, Lu B (2005) Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 8:1069–1077
pubmed: 16025106
Yang B, Ren Q, Zhang JC, Chen QX, Hashimoto K (2017) Altered expression of BDNF, BDNF pro-peptide and their precursor proBDNF in brain and liver tissues from psychiatric disorders: rethinking the brain-liver axis. Transl Psychiatry 7:e1128
pubmed: 28509900
pmcid: 5534963
Yang B, Yang C, Ren Q, Zhang JC, Chen QX, Shirayama Y, Hashimoto K (2016) Regional differences in the expression of brain-derived neurotrophic factor (BDNF) pro-peptide, proBDNF and preproBDNF in the brain confer stress resilience. Eur Arch Psychiatry Clin Neurosci 266:765–769
pubmed: 27094192
Zhang WJ, Cao WY, Huang YQ, Cui YH, Tu BX, Wang LF, Zou GJ, Liu Y, Hu ZL, Hu R, Li CQ, Xing XW, Li F (2019) The role of miR-150 in stress-induced anxiety-like behavior in mice. Neurotox Res 35:160–172
pubmed: 30120712
Zhao G, Zhang C, Chen J, Su Y, Zhou R et al (2017) Ratio of mBDNF to proBDNF for differential diagnosis of major depressive disorder and bipolar depression. Mol Neurobiol 54:5573–5582
pubmed: 27613282
Zheng J, Yin F, Jin G, Zhang X, Zhang L et al (2018) In vitro neuroprotection of rat hippocampal neurons by manninotriose and astragaloside IV against corticosterone-induced toxicity. Molecules 23
Zhong F, Liu L, Wei JL, Hu ZL, Li L et al (2018) Brain-derived neurotrophic factor precursor in the hippocampus regulates both depressive and anxiety-like behaviors in rats. Front Psychiatry 9:776
pubmed: 30740068
Zhou B, Tan J, Zhang C, Wu Y (2018) Neuroprotective effect of polysaccharides from Gastrodia elata blume against corticosterone-induced apoptosis in PC12 cells via inhibition of the endoplasmic reticulum stress-mediated pathway. Mol Med Rep 17:1182–1190
pubmed: 29115511
Zhou L, Xiong J, Lim Y, Ruan Y, Huang C, Zhu Y, Zhong JH, Xiao Z, Zhou XF (2013) Upregulation of blood proBDNF and its receptors in major depression. J Affect Disord 150:776–784
pubmed: 23537780