Skip to main content

Advertisement

SpringerLink
Log in

Modulating Stress Susceptibility and Resilience: Insights from miRNA Manipulation and Neural Mechanisms in Mice

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

This study explored the impact of microRNAs, specifically mmu-miR-1a-3p and mmu-miR-155-5p, on stress susceptibility and resilience in mice of different strains. Previous research had established that C57BL/6J mice were stress-susceptible, while NET-KO and SWR/J mice displayed stress resilience. These strains also exhibited variations in the serum levels of mmu-miR-1a-3p and mmu-miR-155-5p. To investigate this further, we administered antagonistic sequences (Antagomirs) targeting these microRNAs to C57/BL/6J mice and their analogs (Agomirs) to NET-KO and SWR/J mice via intracerebroventricular (i.c.v) injection. The impact of this treatment was assessed using the forced swim test. The results showed that the stress-susceptible C57/BL/6J mice could be transformed into a stress-resilient phenotype through infusion of Antagomirs. Conversely, stress-resilient mice displayed altered behavior when treated with Ago-mmu-miR-1a-3p. The study also examined the expression of mmu-miR-1a-3p in various brain regions, revealing that changes in its expression in the cerebellum (CER) were associated with the stress response. In vitro experiments with the Neuro2a cell line indicated that the Antago/Ago-miR-1a-3p and Antago/Ago-miR-155-5p treatments affected mRNAs encoding genes related to cAMP and Ca2+ signaling, diacylglycerol kinases, and phosphodiesterases. The expression changes of genes such as Dgkq, Bdnf, Ntrk2, and Pde4b in the mouse cerebellum suggested a link between cerebellar function, synaptic plasticity, and the differential stress responses observed in susceptible and resilient mice. In summary, this research highlights the role of mmu-miR-1a-3p and mmu-miR-155-5p in regulating stress susceptibility and resilience in mice and suggests a connection between these microRNAs, cerebellar function, and synaptic plasticity in the context of stress response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The datasets generated during the current study were presented in detailed diagrams in the manuscript or supplementary material and will be available from the corresponding author upon reasonable request. However, when the paper will be published the data will be placed in a public repository https://figshare.com/.

References

  1. McEwen BS, Bowles NP, Gray JD, Hill MN, Hunter RG, Karatsoreos IN, Nasca C (2015) Mechanisms of stress in the brain. Nat Neurosci 18:1353–1363. https://doi.org/10.1038/nn.4086

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Franklin TB, Saab BJ, Mansuy IM (2012) Neural mechanisms of stress resilience and vulnerability. Neuron 75:747–761. https://doi.org/10.1016/j.neuron.2012.08.016

    Article  PubMed  CAS  Google Scholar 

  3. Dziedzicka-Wasylewska M, Faron-Górecka A, Kuśmider M, Drozdowska E, Rogóz Z, Siwanowicz J, Caron MG, Bönisch H (2006) Effect of antidepressant drugs in mice lacking the norepinephrine transporter. Neuropsychopharmacology 31:2424–2432. https://doi.org/10.1038/sj.npp.1301064

    Article  PubMed  CAS  Google Scholar 

  4. Solich J, Palach P, Budziszewska B, Dziedzicka-Wasylewska M (2008) The effect of two behavioral tests on the corticosterone level in plasma of mice lacking the noradrenaline transporter. Eur Neuropsychopharmacol 18:S40–S40. https://doi.org/10.1016/s0924-977x(08)70045-2

    Article  Google Scholar 

  5. Haenisch B, Bilkei-Gorzo A, Caron MG, Bonisch H (2009) Knockout of the norepinephrine transporter and pharmacologically diverse antidepressants prevent behavioral and brain neurotrophin alterations in two chronic stress models of depression. J Neurochem 111:403–416. https://doi.org/10.1111/j.1471-4159.2009.06345.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Szklarczyk K, Korostynski M, Golda S, Piechota M, Ficek J, Przewlocki R (2016) Endogenous opioids regulate glucocorticoid-dependent stress-coping strategies in mice. Neuroscience 330:121–137. https://doi.org/10.1016/j.neuroscience.2016.05.034

    Article  PubMed  CAS  Google Scholar 

  7. Solich J, Kusmider M, Faron-Gorecka A, Pabian P, Kolasa M, Zemla B, Dziedzicka-Wasylewska M (2020) Serum level of miR-1 and miR-155 as potential biomarkers of stress-resilience of NET-KO and SWR/J mice. Cells 9. https://doi.org/10.3390/cells9040917

  8. Borghans B, Homberg JR (2015) Animal models for posttraumatic stress disorder: an overview of what is used in research. World J Psychiatry 5:387–396. https://doi.org/10.5498/wjp.v5.i4.387

    Article  PubMed  PubMed Central  Google Scholar 

  9. Komatsu S, Kitai H, Suzuki HI (2023) Network regulation of microRNA biogenesis and target interaction. Cells 12. https://doi.org/10.3390/cells12020306

  10. Bartel DP (2018) Metazoan microRNAs. Cell 173:20–51. https://doi.org/10.1016/j.cell.2018.03.006

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Saini V, Dawar R, Suneja S, Gangopadhyay S, Kaur C (2021) Can microRNA become next-generation tools in molecular diagnostics and therapeutics? A systematic review. Egypt J Med Hum Genet 22:4. https://doi.org/10.1186/s43042-020-00125-w

    Article  Google Scholar 

  12. Truesdell SS, Mortensen RD, Seo M, Schroeder JC, Lee JH, LeTonqueze O, Vasudevan S (2012) MicroRNA-mediated mRNA translation activation in quiescent cells and oocytes involves recruitment of a nuclear microRNP. Sci Rep 2:842. https://doi.org/10.1038/srep00842

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Alshanbayeva A, Tanwar DK, Roszkowski M, Manuella F, Mansuy IM (2021) Early life stress affects the miRNA cargo of epididymal extracellular vesicles in mousedagger. Biol Reprod 105:593–602. https://doi.org/10.1093/biolre/ioab156

    Article  PubMed  Google Scholar 

  14. Roma-Mateo C, Lorente-Pozo S, Marquez-Thibaut L, Moreno-Estelles M, Garces C, Gonzalez D, Lahuerta M, Aguado C et al (2023) Age-related microRNA overexpression in lafora disease male mice provides links between neuroinflammation and oxidative stress. Int J Mol Sci 24. https://doi.org/10.3390/ijms24021089

  15. Zhang W, Wang L, Wang R, Duan Z, Wang H (2022) A blockade of microRNA-155 signal pathway has a beneficial effect on neural injury after intracerebral haemorrhage via reduction in neuroinflammation and oxidative stress. Arch Physiol Biochem 128:1235–1241. https://doi.org/10.1080/13813455.2020.1764047

    Article  PubMed  CAS  Google Scholar 

  16. Thompson JW, Hu R, Huffaker TB, Ramstead AG, Ekiz HA, Bauer KM, Tang WW, Ghazaryan A et al (2023) MicroRNA-155 plays selective cell-intrinsic roles in brain-infiltrating immune cell populations during neuroinflammation. J Immunol 210:926–934. https://doi.org/10.4049/jimmunol.2200478

    Article  PubMed  CAS  Google Scholar 

  17. Cabrera D, Thompson K, Thomas JD, Peacock C, Antonio J, Tartar JL, Tartar A (2023) Dysregulation of miR-155 expression in professional mixed martial arts (MMA) fighters. Cureus 15:e34944. https://doi.org/10.7759/cureus.34944

    Article  PubMed  PubMed Central  Google Scholar 

  18. Baggish AL, Park J, Min PK, Isaacs S, Parker BA, Thompson PD, Troyanos C, D’Hemecourt P, et al. (2014) Rapid upregulation and clearance of distinct circulating microRNAs after prolonged aerobic exercise. J Appl Physiol 116: 522-531. https://doi.org/10.1152/japplphysiol.01141.2013

  19. Hosoya T, Hashiyada M, Funayama M (2016) Acute Physical stress increases serum levels of specific microRNAs. Microrna 5:50–56. https://doi.org/10.2174/2211536605666160602104659

    Article  PubMed  CAS  Google Scholar 

  20. Xu J, Cao D, Zhang D, Zhang Y, Yue Y (2020) MicroRNA-1 facilitates hypoxia-induced injury by targeting NOTCH3. J Cell Biochem. https://doi.org/10.1002/jcb.29663

  21. Korde A, Ahangari F, Haslip M, Zhang X, Liu Q, Cohn L, Gomez JL, Chupp G et al (2020) An endothelial microRNA-1-regulated network controls eosinophil trafficking in asthma and chronic rhinosinusitis. J Allergy Clin Immunol 145:550–562. https://doi.org/10.1016/j.jaci.2019.10.031

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Pegoraro V, Marozzo R, Angelini C (2020) MicroRNAs and HDAC4 protein expression in the skeletal muscle of ALS patients. Clin Neuropathol. https://doi.org/10.5414/NP301233

  23. Sun J, Liu Q, Zhao L, Cui C, Wu H, Liao L, Tang G, Yang S et al (2019) Potential regulation by miRNAs on glucose metabolism in liver of common carp (Cyprinus carpio) at different temperatures. Comp Biochem Physiol Part D Genomics Proteomics 32:100628. https://doi.org/10.1016/j.cbd.2019.100628

    Article  PubMed  CAS  Google Scholar 

  24. Gao J, Liang Z, Zhao F, Liu X, Ma N (2022) Triptolide inhibits oxidative stress and inflammation via the microRNA-155-5p/brain-derived neurotrophic factor to reduce podocyte injury in mice with diabetic nephropathy. Bioengineered 13:12275–12288. https://doi.org/10.1080/21655979.2022.2067293

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Eivani M, Alijanpour S, Arefian E, Rezayof A (2019) Corticolimbic analysis of microRNAs and protein expressions in scopolamine-induced memory loss under stress. Neurobiol Learn Mem 164:107065. https://doi.org/10.1016/j.nlm.2019.107065

    Article  PubMed  CAS  Google Scholar 

  26. Varendi K, Kumar A, Harma MA, Andressoo JO (2014) miR-1, miR-10b, miR-155, and miR-191 are novel regulators of BDNF. Cell Mol Life Sci 71:4443–4456. https://doi.org/10.1007/s00018-014-1628-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Mojtabavi H, Shaka Z, Momtazmanesh S, Ajdari A, Rezaei N (2022) Circulating brain-derived neurotrophic factor as a potential biomarker in stroke: a systematic review and meta-analysis. J Transl Med 20:126. https://doi.org/10.1186/s12967-022-03312-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Xu F, Gainetdinov RR, Wetsel WC, Jones SR, Bohn LM, Miller GW, Wang YM, Caron MG (2000) Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 3:465–471. https://doi.org/10.1038/74839

    Article  PubMed  CAS  Google Scholar 

  29. Zuo X, Lu J, Manaenko A, Qi X, Tang J, Mei Q, Xia Y, Hu Q (2019) MicroRNA-132 attenuates cerebral injury by protecting blood-brain-barrier in MCAO mice. Exp Neurol 316:12–19. https://doi.org/10.1016/j.expneurol.2019.03.017

    Article  PubMed  CAS  Google Scholar 

  30. Porsolt RD, Bertin A, Jalfre M (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327–336

    PubMed  CAS  Google Scholar 

  31. Paxinos G, Franklin KB (2004) The mouse brain in stereotaxic coordinates: compact. Elsevier Academic Press, Amsterdam, Boston

    Google Scholar 

  32. Brown RAM, Epis MR, Horsham JL, Kabir TD, Richardson KL, Leedman PJ (2018) Total RNA extraction from tissues for microRNA and target gene expression analysis: not all kits are created equal. BMC Biotechnol 18:16. https://doi.org/10.1186/s12896-018-0421-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Solich J, Kolasa M, Faron-Gorecka A, Hajto J, Piechota M, Dziedzicka-Wasylewska M (2021) MicroRNA Let-7e in the mouse prefrontal cortex differentiates restraint-stress-resilient genotypes from susceptible genotype. Int J Mol Sci 22. https://doi.org/10.3390/ijms22179439

  34. Andres-Leon E, Gomez-Lopez G, Pisano DG (2017) Prediction of miRNA-mRNA Interactions Using miRGate. Methods Mol Biol 1580:225–237. https://doi.org/10.1007/978-1-4939-6866-4_15

    Article  PubMed  CAS  Google Scholar 

  35. Fan C, Zhu X, Song Q, Wang P, Liu Z, Yu SY (2018) MiR-134 modulates chronic stress-induced structural plasticity and depression-like behaviors via downregulation of Limk1/cofilin signaling in rats. Neuropharmacology 131:364–376. https://doi.org/10.1016/j.neuropharm.2018.01.009

    Article  PubMed  CAS  Google Scholar 

  36. Park J, Lee J, Choi K, Kang HJ (2021) Regulation of behavioral response to stress by microRNA-690. Mol Brain 14:7. https://doi.org/10.1186/s13041-021-00728-3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Chang CH, Kuek EJW, Su CL, Gean PW (2020) MicroRNA-206 regulates stress-provoked aggressive behaviors in post-weaning social isolation mice. Mol Ther Nucleic Acids 20:812–822. https://doi.org/10.1016/j.omtn.2020.05.001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Singh A, Happel C, Manna SK, Acquaah-Mensah G, Carrerero J, Kumar S, Nasipuri P, Krausz KW et al (2013) Transcription factor NRF2 regulates miR-1 and miR-206 to drive tumorigenesis. J Clin Invest 123:2921–2934. https://doi.org/10.1172/JCI66353

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. McEwen BS, Nasca C, Gray JD (2016) Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41:3–23. https://doi.org/10.1038/npp.2015.171

    Article  PubMed  CAS  Google Scholar 

  40. Bains JS, Wamsteeker Cusulin JI, Inoue W (2015) Stress-related synaptic plasticity in the hypothalamus. Nat Rev Neurosci 16:377–388. https://doi.org/10.1038/nrn3881

    Article  PubMed  CAS  Google Scholar 

  41. Solecki WB, Szklarczyk K, Klasa A, Pradel K, Dobrzanski G, Przewlocki R (2017) Alpha(1)-adrenergic receptor blockade in the VTA modulates fear memories and stress responses. Eur Neuropsychopharmacol 27:782–794. https://doi.org/10.1016/j.euroneuro.2017.05.008

    Article  PubMed  CAS  Google Scholar 

  42. Moreno-Rius J (2019) The cerebellum under stress. Front Neuroendocrinol 54:100774. https://doi.org/10.1016/j.yfrne.2019.100774

    Article  PubMed  CAS  Google Scholar 

  43. Fonken LK, Gaudet AD, Gaier KR, Nelson RJ, Popovich PG (2016) MicroRNA-155 deletion reduces anxiety- and depressive-like behaviors in mice. Psychoneuroendocrinology 63:362–369. https://doi.org/10.1016/j.psyneuen.2015.10.019

    Article  PubMed  CAS  Google Scholar 

  44. Baldacara L, Borgio JGF, Araujo C, Nery-Fernandes F, Lacerda ALT, Moraes W, Montano M, Rocha M et al (2012) Relationship between structural abnormalities in the cerebellum and dementia, posttraumatic stress disorder and bipolar disorder. Dement Neuropsychol 6:203–211. https://doi.org/10.1590/S1980-57642012DN06040003

    Article  PubMed  PubMed Central  Google Scholar 

  45. Chin PW, Augustine GJ (2023) The cerebellum and anxiety. Front Cell Neurosci 17:1130505. https://doi.org/10.3389/fncel.2023.1130505

    Article  PubMed  PubMed Central  Google Scholar 

  46. Xia X, Wang Y, Huang Y, Zhang H, Lu H, Zheng JC (2019) Exosomal miRNAs in central nervous system diseases: biomarkers, pathological mediators, protective factors and therapeutic agents. Prog Neurobiol 183:101694. https://doi.org/10.1016/j.pneurobio.2019.101694

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Zhao Z, Zlokovic BV (2017) Remote control of BBB: a tale of exosomes and microRNA. Cell Res 27:849–850. https://doi.org/10.1038/cr.2017.71

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Inaba H, Li H, Kawatake-Kuno A, Dewa KI, Nagai J, Oishi N, Murai T, Uchida S (2023) GPCR-mediated calcium and cAMP signaling determines psychosocial stress susceptibility and resiliency. Sci Adv 9:eade5397. https://doi.org/10.1126/sciadv.ade5397

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Zhang Y, Lu W, Wang Z, Zhang R, Xie Y, Guo S, Jiao L, Hong Y et al (2020) Reduced neuronal cAMP in the nucleus accumbens damages blood-brain barrier integrity and promotes stress vulnerability. Biol Psychiatry 87:526–537. https://doi.org/10.1016/j.biopsych.2019.09.027

    Article  PubMed  CAS  Google Scholar 

  50. Sakai Y, Li H, Inaba H, Funayama Y, Ishimori E, Kawatake-Kuno A, Yamagata H, Seki T et al (2021) Gene-environment interactions mediate stress susceptibility and resilience through the CaMKIIbeta/TARPgamma-8/AMPAR pathway. iScience 24:102504. https://doi.org/10.1016/j.isci.2021.102504

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Ishisaka M, Hara H (2014) The roles of diacylglycerol kinases in the central nervous system: review of genetic studies in mice. J Pharmacol Sci 124:336–343. https://doi.org/10.1254/jphs.13r07cr

    Article  PubMed  CAS  Google Scholar 

  52. Lee D, Kim E, Tanaka-Yamamoto K (2016) Diacylglycerol kinases in the coordination of synaptic plasticity. Front Cell Dev Biol 4:92. https://doi.org/10.3389/fcell.2016.00092

    Article  PubMed  PubMed Central  Google Scholar 

  53. McEwen BS (2000) The neurobiology of stress: from serendipity to clinical relevance. Brain Res 886:172–189. https://doi.org/10.1016/s0006-8993(00)02950-4

    Article  PubMed  CAS  Google Scholar 

  54. Christoffel DJ, Golden SA, Russo SJ (2011) Structural and synaptic plasticity in stress-related disorders. Rev Neurosci 22:535–549. https://doi.org/10.1515/RNS.2011.044

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Lee CW, Fang YP, Chu MC, Chung YJ, Chi H, Tang CW, So EC, Lin HC et al (2021) Differential mechanisms of synaptic plasticity for susceptibility and resilience to chronic social defeat stress in male mice. Biochem Biophys Res Commun 562:112–118. https://doi.org/10.1016/j.bbrc.2021.05.064

    Article  PubMed  CAS  Google Scholar 

  56. Iu ECY, Chan CB (2022) Is brain-derived neurotrophic factor a metabolic hormone in peripheral tissues? Biology (Basel) 11. https://doi.org/10.3390/biology11071063

  57. D’Mello C, Swain MG (2011) Liver-brain inflammation axis. Am J Physiol Gastrointest Liver Physiol 301:G749–G761. https://doi.org/10.1152/ajpgi.00184.2011

    Article  PubMed  CAS  Google Scholar 

  58. Sen S, Duman R, Sanacora G (2008) Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications. Biol Psychiatry 64:527–532. https://doi.org/10.1016/j.biopsych.2008.05.005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Pan W, Banks WA, Fasold MB, Bluth J, Kastin AJ (1998) Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 37:1553–1561. https://doi.org/10.1016/s0028-3908(98)00141-5

    Article  PubMed  CAS  Google Scholar 

  60. Alcala-Barraza SR, Lee MS, Hanson LR, McDonald AA, Frey WH 2nd, McLoon LK (2010) Intranasal delivery of neurotrophic factors BDNF, CNTF, EPO, and NT-4 to the CNS. J Drug Target 18:179–190. https://doi.org/10.3109/10611860903318134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Wiescholleck V, Manahan-Vaughan D (2012) PDE4 inhibition enhances hippocampal synaptic plasticity in vivo and rescues MK801-induced impairment of long-term potentiation and object recognition memory in an animal model of psychosis. Transl Psychiatry 2:e89. https://doi.org/10.1038/tp.2012.17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Tibbo AJ, Baillie GS (2020) Phosphodiesterase 4B: master regulator of brain signaling. Cells 9. https://doi.org/10.3390/cells9051254

  63. Stornetta RL, Zhu JJ (2011) Ras and Rap signaling in synaptic plasticity and mental disorders. Neuroscientist 17:54–78. https://doi.org/10.1177/1073858410365562

    Article  PubMed  CAS  Google Scholar 

  64. Greenwood MP, Greenwood M, Mecawi AS, Antunes-Rodrigues J, Paton JF, Murphy D (2016) Rasd1, a small G protein with a big role in the hypothalamic response to neuronal activation. Mol Brain 9:1. https://doi.org/10.1186/s13041-015-0182-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank Beata Zemła and Monika Niemczyk for technical support.

Funding

This study was supported by the National Science Centre Poland Grant No. 2016/23/B/NZ4/01086 and Statutory Activity of Maj Institute of Pharmacology Polish Academy of Sciences.

Author information

Authors and Affiliations

  1. Maj Institute of Pharmacology Polish Academy of Sciences, Smętna Street 12, 31-343, Kraków, Poland

    J. Solich, M. Kolasa, A. Faron-Górecka, P. Pabian, K. Latocha, A. Korlatowicz & M. Dziedzicka-Wasylewska

Authors
  1. J. Solich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Kolasa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Faron-Górecka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Pabian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. Latocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Korlatowicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Dziedzicka-Wasylewska
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S J and DWM contributed to the study conception and design. The methodology development and material preparation was carried out by SJ, PP, LK, and KA. Data collection and analysis were performed by SJ, KM, and FGA. The first draft of the manuscript was written by SJ and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to J. Solich.

Ethics declarations

Ethics Approval

This study was performed in line with the principles of the National Ethical Committee for Animal Experiments in Poland. Approval was granted by the Minister of Environment (no. 156/2019) and the 2nd Local Institutional Animal Care and Use Committee (IACUC) (199/2017).

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Solich, J., Kolasa, M., Faron-Górecka, A. et al. Modulating Stress Susceptibility and Resilience: Insights from miRNA Manipulation and Neural Mechanisms in Mice. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-03922-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12035-024-03922-1

Keywords

Search

Navigation