Early-life Stress Induces Genome-wide Sex-dependent MiRNA Expression and Correlation Across Limbic Brain Areas in Rats

Overview

Journal Epigenomics

Specialty Genetics

Date 2021 May 19

PMID 34008410

Citations 12

Authors

Lauren A McKibben

Yogesh Dwivedi

Affiliations

Soon will be listed here.

Abstract

The aim of this study was to assess regional- and sex-dependent changes in miRNA expression resulting from early-life stress (ELS). Small RNA sequencing was used to determine sex-dependent changes in miRNAs after maternal separation, a rodent model of ELS, across the prefrontal cortex, amygdala and hippocampus. Maternal separation induced anhedonia and altered miRNA expression in a sex-dependent manner, particularly in the prefrontal cortex and hippocampus. Gene ontology revealed that these miRNAs target genes with brain-specific biological functions. Using a network approach to explore miRNA signaling across the brain after ELS, regional differences were highlighted as key to studying the brain's stress response, which indicates that sex is critical for understanding miRNA-mediated ELS-induced behavior.

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References

Qiu C, Chen G, Cui Q . Towards the understanding of microRNA and environmental factor interactions and their relationships to human diseases. Sci Rep. 2012; 2:318. PMC: 3306023. DOI: 10.1038/srep00318. View

Yoshino Y, Roy B, Dwivedi Y . Altered miRNA landscape of the anterior cingulate cortex is associated with potential loss of key neuronal functions in depressed brain. Eur Neuropsychopharmacol. 2020; 40:70-84. PMC: 7655604. DOI: 10.1016/j.euroneuro.2020.06.004. View

Van der Auwera S, Ameling S, Wittfeld K, dHarcourt Rowold E, Nauck M, Volzke H . Association of childhood traumatization and neuropsychiatric outcomes with altered plasma micro RNA-levels. Neuropsychopharmacology. 2019; 44(12):2030-2037. PMC: 6898678. DOI: 10.1038/s41386-019-0460-2. View

Im H, Kenny P . MicroRNAs in neuronal function and dysfunction. Trends Neurosci. 2012; 35(5):325-34. PMC: 3565236. DOI: 10.1016/j.tins.2012.01.004. View

Linnstaedt S, Rueckeis C, Riker K, Pan Y, Wu A, Yu S . MicroRNA-19b predicts widespread pain and posttraumatic stress symptom risk in a sex-dependent manner following trauma exposure. Pain. 2019; 161(1):47-60. PMC: 6923535. DOI: 10.1097/j.pain.0000000000001709. View

Abkevich V, Camp N, Hensel C, Neff C, Russell D, Hughes D . Predisposition locus for major depression at chromosome 12q22-12q23.2. Am J Hum Genet. 2003; 73(6):1271-81. PMC: 1180393. DOI: 10.1086/379978. View

Hung Y, Wu M, Tsai M, Huang Y, Kang H . Aberrant Expression of Intracellular let-7e, miR-146a, and miR-155 Correlates with Severity of Depression in Patients with Major Depressive Disorder and Is Ameliorated after Antidepressant Treatment. Cells. 2019; 8(7). PMC: 6678487. DOI: 10.3390/cells8070647. View

Makarova J, Shkurnikov M, Wicklein D, Lange T, Samatov T, Turchinovich A . Intracellular and extracellular microRNA: An update on localization and biological role. Prog Histochem Cytochem. 2016; 51(3-4):33-49. DOI: 10.1016/j.proghi.2016.06.001. View

Bertolote J, Fleischmann A . Suicide and psychiatric diagnosis: a worldwide perspective. World Psychiatry. 2006; 1(3):181-5. PMC: 1489848. View

10.

Zhang X, Ke X, Pu Q, Yuan Y, Yang W, Luo X . MicroRNA-410 acts as oncogene in NSCLC through downregulating SLC34A2 via activating Wnt/β-catenin pathway. Oncotarget. 2016; 7(12):14569-85. PMC: 4924736. DOI: 10.18632/oncotarget.7538. View

11.

Zhang J, Zhang J, Liu L, Zhou Y, Li Y, Shao Z . Effects of miR-541 on neurite outgrowth during neuronal differentiation. Cell Biochem Funct. 2011; 29(4):279-86. DOI: 10.1002/cbf.1747. View

12.

Xu X, Dai J, Chen Y, Liu C, Xin F, Zhou X . Intrinsic connectivity of the prefrontal cortex and striato-limbic system respectively differentiate major depressive from generalized anxiety disorder. Neuropsychopharmacology. 2020; 46(4):791-798. PMC: 8027677. DOI: 10.1038/s41386-020-00868-5. View

13.

Timberlake Ii M, Roy B, Dwivedi Y . A Novel Animal Model for Studying Depression Featuring the Induction of the Unfolded Protein Response in Hippocampus. Mol Neurobiol. 2019; 56(12):8524-8536. DOI: 10.1007/s12035-019-01687-6. View

14.

Dickson D, Paulus J, Mensah V, Lem J, Saavedra-Rodriguez L, Gentry A . Reduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress. Transl Psychiatry. 2018; 8(1):101. PMC: 5966454. DOI: 10.1038/s41398-018-0146-2. View

15.

Middeldorp C, Sullivan P, Wray N, Hottenga J, de Geus E, van den Berg M . Suggestive linkage on chromosome 2, 8, and 17 for lifetime major depression. Am J Med Genet B Neuropsychiatr Genet. 2008; 150B(3):352-8. PMC: 2784956. DOI: 10.1002/ajmg.b.30817. View

16.

Yang Y, Cheng Z, Tang H, Jiao H, Sun X, Cui Q . Neonatal Maternal Separation Impairs Prefrontal Cortical Myelination and Cognitive Functions in Rats Through Activation of Wnt Signaling. Cereb Cortex. 2016; 27(5):2871-2884. DOI: 10.1093/cercor/bhw121. View

17.

Cohen H, Matar M, Joseph Z . Animal models of post-traumatic stress disorder. Curr Protoc Neurosci. 2013; Chapter 9:Unit 9.45. DOI: 10.1002/0471142301.ns0945s64. View

18.

Xu J, Wang R, Liu Y, Liu D, Jiang H, Pan F . FKBP5 and specific microRNAs via glucocorticoid receptor in the basolateral amygdala involved in the susceptibility to depressive disorder in early adolescent stressed rats. J Psychiatr Res. 2017; 95:102-113. DOI: 10.1016/j.jpsychires.2017.08.010. View

19.

Belmaker R, Agam G . Major depressive disorder. N Engl J Med. 2008; 358(1):55-68. DOI: 10.1056/NEJMra073096. View

20.

Yang Q, Qiu C, Yang J, Wu Q, Cui Q . miREnvironment database: providing a bridge for microRNAs, environmental factors and phenotypes. Bioinformatics. 2011; 27(23):3329-30. DOI: 10.1093/bioinformatics/btr556. View