Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Research Article

miR-204-5p Plays a Critical Role in the Pathogenesis of Depression and Anti-depression Action of Venlafaxine in the Hippocampus of Mice

Author(s): Wei Guan*, Xin-Yuan Wu, Xiang Jin, Xiao-Ming Sheng and Yan Fan

Volume 31, Issue 22, 2024

Published on: 24 July, 2023

Page: [3412 - 3425] Pages: 14

DOI: 10.2174/0929867330666230623163315

Price: $65

Abstract

Background: Venlafaxine has been demonstrated to treat diseases such as social anxiety disorder and depression. Most of antidepressants including venlafaxine have a certain effect, but significant side effects. Therefore, it is necessary for us to research the development of novel antidepressants for effective treatment in practice. MicroRNA-204 (miR-204) is highly expressed in brain tissue, and plays a critical role in the synaptic plasticity of hippocampal neurons in rats. However, the underlying molecular mechanism of miR-204 remains unclear to date, this study aims to offer unique insights into depression and provide a theoretical basis for clinical physicians.

Methods: A chronic social defeat stress (CSDS) was initially adopted for establishing a mice model of depression in this research and depression-like behaviors were evaluated by a series of behavioral experiments including the sucrose preference test (SPT), the tail suspension test (TST), the forced swim test (FST) and the social interaction test (SIT). Quantitative real-time reverse transcription PCR (qRT-PCR) was also conducted to test the expression levels of miR-204 and BDNF in the hippocampus of mice. Finally, gene interference of miR-204-5p was further adopted to test whether miR-204-5p played an effective role in the antidepressant effects of venlafaxine in mice.

Results: Our data implicated that CSDS significantly increased the miR-204-5p but not miR-204-3p levels in the hippocampus of mice. The treatment of venlafaxine obviously relieved depression- like behaviors of CSDS-induced mice. The usage of venlafaxine abolished the increasing effects on the expression of miR-204-5p but up-regulated the BDNF expression level in CSDS-exposured mice. More importantly, we found that genetic overexpression of miR-204-5p decreased the reverse effects of venlafaxine on depressive-like behaviors and genetic knockdown of hippocampal miR-204-5p relieved the depressive-like behaviors and neurogenesis in CSDS-induced mice.

Conclusion: miR-204-5p played an effective role in the antidepressant effects of venlafaxine in CSDS-induced mice.

[1]
Edinoff, A.N.; Akuly, H.A.; Hanna, T.A.; Ochoa, C.O.; Patti, S.J.; Ghaffar, Y.A.; Kaye, A.D.; Viswanath, O.; Urits, I.; Boyer, A.G.; Cornett, E.M.; Kaye, A.M. Selective serotonin reuptake inhibitors and adverse effects: A narrative review. Neurol. Int., 2021, 13(3), 387-401.
[http://dx.doi.org/10.3390/neurolint13030038] [PMID: 34449705]
[2]
Zhou, J.; Wang, X.; Feng, L.; Xiao, L.; Yang, R.; Zhu, X.; Shi, H.; Hu, Y.; Chen, R.; Boyce, P.; Wang, G. Venlafaxine vs. fluoxetine in postmenopausal women with major depressive disorder: an 8-week, randomized, single-blind, active-controlled study. BMC Psychiatry, 2021, 21(1), 260.
[http://dx.doi.org/10.1186/s12888-021-03253-8] [PMID: 34011310]
[3]
Thomas Haskins, J.; Moyer, J.A.; Muth, E.A.; Sigg, E.B. DMI, Wy-45,030, Wy-45,881 and ciramadol inhibit locus coeruleus neuronal activity. Eur. J. Pharmacol., 1985, 115(2-3), 139-146.
[http://dx.doi.org/10.1016/0014-2999(85)90684-3] [PMID: 2998818]
[4]
Potter, D.E.; Choudhury, M. Ketamine: repurposing and redefining a multifaceted drug. Drug Discov. Today, 2014, 19(12), 1848-1854.
[http://dx.doi.org/10.1016/j.drudis.2014.08.017] [PMID: 25224017]
[5]
Åkerblom, M.; Jakobsson, J. MicroRNAs as neuronal fate determinants. Neuroscientist, 2014, 20(3), 235-242.
[http://dx.doi.org/10.1177/1073858413497265] [PMID: 23877999]
[6]
Roy, B.; Dunbar, M.; Shelton, R.C.; Dwivedi, Y. Identification of microRNA-124-3p as a putative epigenetic signature of major depressive disorder. Neuropsychopharmacology, 2017, 42(4), 864-875.
[http://dx.doi.org/10.1038/npp.2016.175] [PMID: 27577603]
[7]
O’Connor, R.M.; Grenham, S.; Dinan, T.G.; Cryan, J.F. microRNAs as novel antidepressant targets: Converging effects of ketamine and electroconvulsive shock therapy in the rat hippocampus. Int. J. Neuropsychopharmacol., 2013, 16(8), 1885-1892.
[http://dx.doi.org/10.1017/S1461145713000448] [PMID: 23684180]
[8]
Li, Y.; Fan, C.; Wang, L.; Lan, T.; Gao, R.; Wang, W.; Yu, S.Y. MicroRNA-26a-3p rescues depression-like behaviors in male rats via preventing hippocampal neuronal anomalies. J. Clin. Invest., 2021, 131(16), e148853.
[http://dx.doi.org/10.1172/JCI148853] [PMID: 34228643]
[9]
Guan, W.; Xu, D.W.; Ji, C.H.; Wang, C.N.; Liu, Y.; Tang, W.Q.; Gu, J.H.; Chen, Y.M.; Huang, J.; Liu, J.F.; Jiang, B. Hippocampal miR-206-3p participates in the pathogenesis of depression via regulating the expression of BDNF. Pharmacol. Res., 2021, 174, 105932.
[http://dx.doi.org/10.1016/j.phrs.2021.105932] [PMID: 34628001]
[10]
Yang, W.; Liu, M.; Zhang, Q.; Zhang, J.; Chen, J.; Chen, Q.; Suo, L. Knockdown of miR-124 reduces depression-like behavior by targeting CREB1 and BDNF. Curr. Neurovasc. Res., 2020, 17(2), 196-203.
[http://dx.doi.org/10.2174/1567202617666200319141755] [PMID: 32189593]
[11]
Martinowich, K.; Lu, B. Interaction between BDNF and serotonin: Role in mood disorders. Neuropsychopharmacology, 2008, 33(1), 73-83.
[http://dx.doi.org/10.1038/sj.npp.1301571] [PMID: 17882234]
[12]
Zhu, D.L.; Yan, H.X.; Yue, J.J.; Liu, J.F.; Li, Z.B.; Song, J.F. Effect of inhibiting miR-204 expression on the learning and memory abilities of neonatal rats with intrauterine growth restriction and related mechanism. Zhongguo Dang Dai Er Ke Za Zhi, 2022, 24(12), 1376-1383.
[http://dx.doi.org/10.7499/j.issn.1008-8830.2205140] [PMID: 36544422]
[13]
Micheli, L.; Ceccarelli, M.; D’Andrea, G.; Tirone, F. Depression and adult neurogenesis: Positive effects of the antidepressant fluoxetine and of physical exercise. Brain Res. Bull., 2018, 143, 181-193.
[http://dx.doi.org/10.1016/j.brainresbull.2018.09.002] [PMID: 30236533]
[14]
D’Sa, C.; Duman, R.S. Antidepressants and neuroplasticity. Bipolar Disord., 2002, 4(3), 183-194.
[http://dx.doi.org/10.1034/j.1399-5618.2002.01203.x] [PMID: 12180273]
[15]
Huang, X.; Mao, Y.S.; Li, C.; Wang, H.; Ji, J.L. Venlafaxine inhibits apoptosis of hippocampal neurons by up-regulating brain-derived neurotrophic factor in a rat depression model. Int. J. Clin. Exp. Pathol., 2014, 7(8), 4577-4586.
[PMID: 25197330]
[16]
Marshe, V.S.; Islam, F.; Maciukiewicz, M.; Fiori, L.M.; Yerko, V.; Yang, J.; Turecki, G.; Foster, J.A.; Kennedy, S.H.; Blumberger, D.M.; Karp, J.F.; Kennedy, J.L.; Mulsant, B.H.; Reynolds, C.F., III; Lenze, E.J.; Müller, D.J. Validation study of microRNAs previously associated with antidepressant response in older adults treated for late-life depression with venlafaxine. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2020, 100, 109867.
[http://dx.doi.org/10.1016/j.pnpbp.2020.109867] [PMID: 31954757]
[17]
Lopez, J.P.; Pereira, F.; Richard-Devantoy, S.; Berlim, M.; Chachamovich, E.; Fiori, L.M.; Niola, P.; Turecki, G.; Jollant, F. Co-variation of peripheral levels of miR-1202 and brain activity and connectivity during antidepressant treatment. Neuropsychopharmacology, 2017, 42(10), 2043-2051.
[http://dx.doi.org/10.1038/npp.2017.9] [PMID: 28079059]
[18]
Guan, W.; Gu, J.H.; Ji, C.H.; Liu, Y.; Tang, W.Q.; Wang, Y.; Jiang, B. Xanthoceraside administration produces significant antidepressant effects in mice through activation of the hippocampal BDNF signaling pathway. Neurosci. Lett., 2021, 757, 135994.
[http://dx.doi.org/10.1016/j.neulet.2021.135994] [PMID: 34058291]
[19]
Mansouri, M.T.; Naghizadeh, B.; Ghorbanzadeh, B.; Amirgholami, N.; Houshmand, G.; Alboghobeish, S. Venlafaxine inhibits naloxone-precipitated morphine withdrawal symptoms: Role of inflammatory cytokines and nitric oxide. Metab. Brain Dis., 2020, 35(2), 305-313.
[http://dx.doi.org/10.1007/s11011-019-00491-4] [PMID: 31630319]
[20]
Li, D.; Lee, J.; Choi, C.; Kim, J.; Kim, S.; Kim, W. The analgesic effect of venlafaxine and its mechanism on oxaliplatin-induced neuropathic pain in mice. Int. J. Mol. Sci., 2019, 20(7), 1652.
[http://dx.doi.org/10.3390/ijms20071652] [PMID: 30987090]
[21]
Kosuge, A.; Kunisawa, K.; Arai, S.; Sugawara, Y.; Shinohara, K.; Iida, T.; Wulaer, B.; Kawai, T.; Fujigaki, H.; Yamamoto, Y.; Saito, K.; Nabeshima, T.; Mouri, A. Heat-sterilized Bifidobacterium breve prevents depression-like behavior and interleukin-1β expression in mice exposed to chronic social defeat stress. Brain Behav. Immun., 2021, 96, 200-211.
[http://dx.doi.org/10.1016/j.bbi.2021.05.028] [PMID: 34062230]
[22]
Si, L.; Wang, Y.; Liu, M.; Yang, L.; Zhang, L. Expression and role of microRNA-212/nuclear factor I-A in depressive mice. Bioengineered, 2021, 12(2), 11520-11532.
[http://dx.doi.org/10.1080/21655979.2021.2009964] [PMID: 34889698]
[23]
Lu, Y.; Yang, J.; Sun, J.; Lu, W.; Wang, J.H. mRNA and miRNA profiles in the nucleus accumbens are associated with psychological stress-induced susceptible and resilient mice. Pharmacol. Biochem. Behav., 2020, 199, 173062.
[http://dx.doi.org/10.1016/j.pbb.2020.173062] [PMID: 33098854]
[24]
Sun, Z.; Zhan, H.; Wang, C.; Guo, P. Shanzhiside methylester protects against depression by inhibiting inflammation via the miRNA-155-5p/SOCS1 axis. Psychopharmacology (Berl), 2022, 239(7), 2201-2213.
[http://dx.doi.org/10.1007/s00213-022-06107-7] [PMID: 35294601]
[25]
Zhao, H.; Mohamed, N.E.; Chan, S.J.; Tan, C.T.; Tao, R.; Yu, V.C.; Wong, P.T.H. Absence of stress response in dorsal raphe nucleus in modulator of apoptosis 1-deficient mice. Mol. Neurobiol., 2019, 56(3), 2185-2201.
[http://dx.doi.org/10.1007/s12035-018-1205-7] [PMID: 30003515]
[26]
Ghanbari, S.; Salimi, A.; Rahmani, S.; Nafissi, N.; Sharifi-Zarchi, A.; Mowla, S.J. miR-361-5p as a promising qRT-PCR internal control for tumor and normal breast tissues. PLoS One, 2021, 16(6), e0253009.
[http://dx.doi.org/10.1371/journal.pone.0253009] [PMID: 34101749]
[27]
Kim, I.B.; Park, S.C. The entorhinal cortex and adult neurogenesis in major depression. Int. J. Mol. Sci., 2021, 22(21), 11725.
[http://dx.doi.org/10.3390/ijms222111725] [PMID: 34769155]
[28]
Wang, J.L.; Wang, Y.; Gao, T.T.; Liu, L.; Wang, Y.J.; Guan, W.; Chen, T.T.; Zhao, J.; Zhang, Y.; Jiang, B. Venlafaxine protects against chronic stress-related behaviors in mice by activating the mTORC1 signaling cascade. J. Affect. Disord., 2020, 276, 525-536.
[http://dx.doi.org/10.1016/j.jad.2020.07.096] [PMID: 32871684]
[29]
Duman, R.S.; Deyama, S.; Fogaça, M.V. Role of BDNF in the pathophysiology and treatment of depression: Activity-dependent effects distinguish rapid-acting antidepressants. Eur. J. Neurosci., 2021, 53(1), 126-139.
[http://dx.doi.org/10.1111/ejn.14630] [PMID: 31811669]
[30]
Gudasheva, T.A.; Povarnina, P.; Tarasiuk, A.V.; Seredenin, S.B. The low molecular weight brain-derived neurotrophic factor mimetics with antidepressant-like activity. Curr. Pharm. Des., 2019, 25(6), 729-737.
[http://dx.doi.org/10.2174/1381612825666190329122852] [PMID: 30931847]
[31]
Peng, S.; Li, W.; Lv, L.; Zhang, Z.; Zhan, X. BDNF as a biomarker in diagnosis and evaluation of treatment for schizophrenia and depression. Discov. Med., 2018, 26(143), 127-136.
[PMID: 30586536]
[32]
Zhu, Y.; Wei, M.; Zhou, X.; Deng, L.H.; Qiu, J.; Li, G.; Zhou, S.Q.; Xie, H.; Li, D.S.; Wang, C.D. Progress on miRNA in giant panda (Ailuropoda melanoleuca). Yi Chuan, 2021, 43(9), 849-857.
[PMID: 34702698]
[33]
Konishi, H.; Sato, H.; Takahashi, K.; Fujiya, M. Tumor-progressive mechanisms mediating miRNA–protein interaction. Int. J. Mol. Sci., 2021, 22(22), 12303.
[http://dx.doi.org/10.3390/ijms222212303] [PMID: 34830186]
[34]
Celik, N.; Kim, M.H.; Hayes, D.J.; Ozbolat, I.T. miRNA induced co-differentiation and cross-talk of adipose tissue-derived progenitor cells for 3D heterotypic pre-vascularized bone formation. Biofabrication, 2021, 13(4), 044107.
[http://dx.doi.org/10.1088/1758-5090/ac23ae] [PMID: 34479220]
[35]
Garcia, G.; Pinto, S.; Cunha, M.; Fernandes, A.; Koistinaho, J.; Brites, D. Neuronal dynamics and mirna signaling differ between SH-SY5Y APPSwe and PSEN1 mutant iPSC-derived AD models upon modulation with miR-124 mimic and inhibitor. Cells, 2021, 10(9), 2424.
[http://dx.doi.org/10.3390/cells10092424] [PMID: 34572073]
[36]
Tavakolizadeh, J.; Roshanaei, K.; Salmaninejad, A.; Yari, R.; Nahand, J.S.; Sarkarizi, H.K.; Mousavi, S.M.; Salarinia, R.; Rahmati, M.; Mousavi, S.F.; Mokhtari, R.; Mirzaei, H. MicroRNAs and exosomes in depression: Potential diagnostic biomarkers. J. Cell. Biochem., 2018, 119(5), 3783-3797.
[http://dx.doi.org/10.1002/jcb.26599] [PMID: 29236313]
[37]
Manna, I.; Quattrone, A.; De Benedittis, S.; Vescio, B.; Iaccino, E.; Quattrone, A. Exosomal miRNA as peripheral biomarkers in Parkinson’s disease and progressive supranuclear palsy: A pilot study. Parkinsonism Relat. Disord., 2021, 93, 77-84.
[http://dx.doi.org/10.1016/j.parkreldis.2021.11.020] [PMID: 34839044]
[38]
Lan, T.; Li, Y.; Fan, C.; Wang, L.; Wang, W.; Chen, S.; Yu, S.Y. MicroRNA-204-5p reduction in rat hippocampus contributes to stress-induced pathology via targeting RGS12 signaling pathway. J. Neuroinflammation, 2021, 18(1), 243.
[http://dx.doi.org/10.1186/s12974-021-02299-5] [PMID: 34674723]
[39]
Hung, Y.Y.; Huang, Y.L.; Chang, C.; Kang, H.Y. Deficiency in androgen receptor aggravates the depressive-like behaviors in chronic mild stress model of depression. Cells, 2019, 8(9), 1021.
[http://dx.doi.org/10.3390/cells8091021] [PMID: 31480771]
[40]
Clark, C.T.; Sit, D.K.; Zumpf, K.B.; Ciolino, J.D.; Yang, A.; Fisher, S.D.; Wisner, K.L. A comparison of symptoms of bipolar and unipolar depression in postpartum women. J. Affect. Disord., 2022, 303, 82-90.
[http://dx.doi.org/10.1016/j.jad.2022.01.064] [PMID: 35041868]
[41]
Duman, R.S. Ketamine and rapid-acting antidepressants: A new era in the battle against depression and suicide. F1000 Res., 2018, 7, 659.
[http://dx.doi.org/10.12688/f1000research.14344.1] [PMID: 29899972]
[42]
Chen, H.; Vandorpe, D.H.; Xie, X.; Alper, S.L.; Zeidel, M.L.; Yu, W. Disruption of Cav1.2-mediated signaling is a pathway for ketamine-induced pathology. Nat. Commun., 2020, 11(1), 4328.
[http://dx.doi.org/10.1038/s41467-020-18167-4] [PMID: 32859919]
[43]
Ikert, H.; Craig, P.M. Chronic exposure to venlafaxine and increased water temperature reversibly alters microRNA in zebrafish gonads (Danio rerio). Comp. Biochem. Physiol. Part D Genomics Proteomics, 2020, 33, 100634.
[http://dx.doi.org/10.1016/j.cbd.2019.100634] [PMID: 31715506]
[44]
Luu, I.; Ikert, H.; Craig, P.M. Chronic exposure to anthropogenic and climate related stressors alters transcriptional responses in the liver of zebrafish (Danio rerio) across multiple generations. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2021, 240, 108918.
[http://dx.doi.org/10.1016/j.cbpc.2020.108918] [PMID: 33141083]
[45]
Weisz, H.A.; Kennedy, D.; Widen, S.; Spratt, H.; Sell, S.L.; Bailey, C.; Sheffield-Moore, M.; DeWitt, D.S.; Prough, D.S.; Levin, H.; Robertson, C.; Hellmich, H.L. MicroRNA sequencing of rat hippocampus and human biofluids identifies acute, chronic, focal and diffuse traumatic brain injuries. Sci. Rep., 2020, 10(1), 3341.
[http://dx.doi.org/10.1038/s41598-020-60133-z] [PMID: 32094409]
[46]
Szuhany, K.L.; Otto, M.W. Assessing BDNF as a mediator of the effects of exercise on depression. J. Psychiatr. Res., 2020, 123, 114-118.
[http://dx.doi.org/10.1016/j.jpsychires.2020.02.003] [PMID: 32065946]
[47]
Wang, H.; Tan, Y.Z.; Mu, R.H.; Tang, S.S.; Liu, X.; Xing, S.Y.; Long, Y.; Yuan, D.H.; Hong, H.; Takeda, G. Takeda G protein–coupled receptor 5 modulates depression-like behaviors via hippocampal CA3 pyramidal neurons afferent to dorsolateral septum. Biol. Psychiatry, 2021, 89(11), 1084-1095.
[http://dx.doi.org/10.1016/j.biopsych.2020.11.018] [PMID: 33536132]
[48]
Morel, C.; Montgomery, S.E.; Li, L.; Durand-de Cuttoli, R.; Teichman, E.M.; Juarez, B.; Tzavaras, N.; Ku, S.M.; Flanigan, M.E.; Cai, M.; Walsh, J.J.; Russo, S.J.; Nestler, E.J.; Calipari, E.S.; Friedman, A.K.; Han, M.H. Midbrain projection to the basolateral amygdala encodes anxiety-like but not depression-like behaviors. Nat. Commun., 2022, 13(1), 1532.
[http://dx.doi.org/10.1038/s41467-022-29155-1] [PMID: 35318315]
[49]
Oskotsky, T.; Marić, I.; Tang, A.; Oskotsky, B.; Wong, R.J.; Aghaeepour, N.; Sirota, M.; Stevenson, D.K. Mortality risk among patients with covid-19 prescribed selective serotonin reuptake inhibitor antidepressants. JAMA Netw. Open, 2021, 4(11), e2133090.
[http://dx.doi.org/10.1001/jamanetworkopen.2021.33090] [PMID: 34779847]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy