MicroRNA sequencing of rat hippocampus and human biofluids identifies acute, chronic, focal and diffuse traumatic brain injuries.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
24 02 2020
24 02 2020
Historique:
received:
01
08
2019
accepted:
29
01
2020
entrez:
26
2
2020
pubmed:
26
2
2020
medline:
12
11
2020
Statut:
epublish
Résumé
High-throughput sequencing technologies could improve diagnosis and classification of TBI subgroups. Because recent studies showed that circulating microRNAs (miRNAs) may serve as noninvasive markers of TBI, we performed miRNA-seq to study TBI-induced changes in rat hippocampal miRNAs up to one year post-injury. We used miRNA PCR arrays to interrogate differences in serum miRNAs using two rat models of TBI (controlled cortical impact [CCI] and fluid percussion injury [FPI]). The translational potential of our results was evaluated by miRNA-seq analysis of human control and TBI (acute and chronic) serum samples. Bioinformatic analyses were performed using Ingenuity Pathway Analysis, miRDB, and Qlucore Omics Explorer. Rat miRNA profiles identified TBI across all acute and chronic intervals. Rat CCI and FPI displayed distinct serum miRNA profiles. Human miRNA profiles identified TBI across all acute and chronic time points and, at 24 hours, discriminated between focal and diffuse injuries. In both species, predicted gene targets of differentially expressed miRNAs are involved in neuroplasticity, immune function and neurorestoration. Chronically dysregulated miRNAs (miR-451a, miR-30d-5p, miR-145-5p, miR-204-5p) are linked to psychiatric and neurodegenerative disorders. These data suggest that circulating miRNAs in biofluids can be used as "molecular fingerprints" to identify acute, chronic, focal or diffuse TBI and potentially, presence of neurodegenerative sequelae.
Identifiants
pubmed: 32094409
doi: 10.1038/s41598-020-60133-z
pii: 10.1038/s41598-020-60133-z
pmc: PMC7040013
doi:
Substances chimiques
MicroRNAs
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3341Références
Maas, A. I. R. et al. Traumatic brain injury: integrated approaches to improve prevention, clinical care, and research. Lancet Neurol 16, 987–1048 (2017).
doi: 10.1016/S1474-4422(17)30371-X
Cohen, J. D. et al. Detection and localization of surgically resectable cancers with a multi-analyte blood test. Science (2018).
Sheinerman, K. S. & Umansky, S. R. Circulating cell-free microRNA as biomarkers for screening, diagnosis and monitoring of neurodegenerative diseases and other neurologic pathologies. Front Cell Neurosci 7, 150 (2013).
doi: 10.3389/fncel.2013.00150
Boehm, M. & Slack, F. J. MicroRNA control of lifespan and metabolism. Cell Cycle 5, 837–840 (2006).
doi: 10.4161/cc.5.8.2688
Salta, E. & De Strooper, B. Non-coding RNAs with essential roles in neurodegenerative disorders. Lancet Neurol 11, 189–200 (2012).
doi: 10.1016/S1474-4422(11)70286-1
Boone, D. K. et al. Evidence linking microRNA suppression of essential prosurvival genes with hippocampal cell death after traumatic brain injury. Sci Rep 7, 6645 (2017).
doi: 10.1038/s41598-017-06341-6
Amberger, J. S., Bocchini, C. A., Schiettecatte, F., Scott, A. F. & Hamosh, A. OMIM.org: Online Mendelian Inheritance in Man (OMIM(R)), an online catalog of human genes and genetic disorders. Nucleic Acids Res 43, D789–798 (2015).
doi: 10.1093/nar/gku1205
Rexach, J., Lee, H., Martinez-Agosto, J. A., Nemeth, A. H. & Fogel, B. L. Clinical application of next-generation sequencing to the practice of neurology. Lancet Neurol 18, 492–503 (2019).
doi: 10.1016/S1474-4422(19)30033-X
Boone, D. R. et al. Traumatic brain injury induces long-lasting changes in immune and regenerative signaling. PLoS One 14 (2019).
doi: 10.1371/journal.pone.0214741
Robertson, C. S. et al. Effect of erythropoietin and transfusion threshold on neurological recovery after traumatic brain injury: a randomized clinical trial. JAMA 312, 36–47 (2014).
doi: 10.1001/jama.2014.6490
Cangelosi, R. & Goriely, A. Component retention in principal component analysis with application to cDNA microarray data. Biol Direct 2, 2 (2007).
doi: 10.1186/1745-6150-2-2
Peixoto, C. A., Oliveira, W. H., Araujo, S. & Nunes, A. K. S. AMPK activation: Role in the signaling pathways of neuroinflammation and neurodegeneration. Exp Neurol 298, 31–41 (2017).
doi: 10.1016/j.expneurol.2017.08.013
Keller, A. et al. Toward the blood-borne miRNome of human diseases. Nat Methods 8, 841–843 (2011).
doi: 10.1038/nmeth.1682
Masel, B. E. & DeWitt, D. S. Traumatic brain injury: a disease process, not an event. J Neurotrauma 27, 1529–1540 (2010).
doi: 10.1089/neu.2010.1358
Lee, B. & Newberg, A. Neuroimaging in traumatic brain imaging. NeuroRx 2, 372–383 (2005).
doi: 10.1602/neurorx.2.2.372
Hamdeh, S. A. et al. Proteomic differences between focal and diffuse traumatic brain injury in human brain tissue. Nature Research Journal (2018).
McAllister, T. W. Genetic factors in traumatic brain injury. Handb Clin Neurol 128, 723–739, https://doi.org/10.1016/B978-0-444-63521-1.00045-5 (2015).
doi: 10.1016/B978-0-444-63521-1.00045-5
pubmed: 25701917
Hebert, S. S. & De, S. B. Alterations of the microRNA network cause neurodegenerative disease. Trends Neurosci 32, 199–206 (2009).
doi: 10.1016/j.tins.2008.12.003
Gandal, M. J. et al. Shared molecular neuropathology across major psychiatric disorders parallels polygenic overlap. Science 359, 693–697 (2018).
doi: 10.1126/science.aad6469
Henshall, D. C. et al. MicroRNAs in epilepsy: pathophysiology and clinical utility. Lancet Neurol 15, 1368–1376 (2016).
doi: 10.1016/S1474-4422(16)30246-0
Kim, Y. et al. Bipolar Disorder Associated microRNA, miR-1908-5p, Regulates the Expression of Genes Functioning in Neuronal Glutamatergic Synapses. Exp Neurobiol 25, 296–306 (2016).
doi: 10.5607/en.2016.25.6.296
Schneider, R. et al. Downregulation of exosomal miR-204-5p and miR-632 as a biomarker for FTD: a GENFI study. J Neurol Neurosurg Psychiatry 89, 851–858 (2018).
doi: 10.1136/jnnp-2017-317492
Shu, P. et al. Opposing Gradients of MicroRNA Expression Temporally Pattern Layer Formation in the Developing Neocortex. Dev Cell (2019).
Schork, A. J. et al. A genome-wide association study of shared risk across psychiatric disorders implicates gene regulation during fetal neurodevelopment. Nat Neurosci 22, 353–361 (2019).
doi: 10.1038/s41593-018-0320-0
Rehfeld, F., Rohde, A. M., Nguyen, D. T. & Wulczyn, F. G. Lin28 and let-7: ancient milestones on the road from pluripotency to neurogenesis. Cell Tissue Res 359, 145–160 (2015).
doi: 10.1007/s00441-014-1872-2
Peipei, L. et al. Epigenetic dysregulation of enhancers in neurons is associated with Alzheimer’s disease pathology and cognitive symptoms. Nature Communications (2019).
Cole, J. H., Leech, R. & Sharp, D. J. Prediction of brain age suggests accelerated atrophy after traumatic brain injury. Ann. Neurol 77, 571–581 (2015).
doi: 10.1002/ana.24367
Sarkar, S. N., Russell, A. E., Engler-Chiurazzi, E. B., Porter, K. N. & Simpkins, J. W. MicroRNAs and the Genetic Nexus of Brain Aging, Neuroinflammation, Neurodegeneration, and Brain Trauma. Aging Dis 10, 329–352 (2019).
doi: 10.14336/AD.2018.0409
Wang, W. et al. Dietary miR-451 protects erythroid cells from oxidative stress via increasing the activity of Foxo3 pathway. Oncotarget 8, 107109–107124 (2017).
pubmed: 29291015
pmcid: 5739800
Roitbak, T. MicroRNAs and Regeneration in Animal Models of CNS Disorders. Neurochem Res (2019).
Wang, P. et al. Micro-RNA-155 is induced by K-Ras oncogenic signal and promotes ROS stress in pancreatic cancer. Oncotarget 6, 21148–21158 (2015).
pubmed: 26020803
pmcid: 4673256
Gaudet, A. D., Fonken, L. K., Watkins, L. R., Nelson, R. J. & Popovich, P. G. MicroRNAs: Roles in Regulating Neuroinflammation. Neuroscientist (2017).
Wang, W. X. et al. Mitochondria-associated microRNAs in rat hippocampus following traumatic brain injury. Exp. Neurol 265, 84–93 (2015).
doi: 10.1016/j.expneurol.2014.12.018
Yang, Z., Zhong, L., Xian, R. & Yuan, B. MicroRNA-223 regulates inflammation and brain injury via feedback to NLRP3 inflammasome after intracerebral hemorrhage. Mol Immunol 65, 267–276 (2015).
doi: 10.1016/j.molimm.2014.12.018
Harraz, M. M., Eacker, S. M., Wang, X., Dawson, T. M. & Dawson, V. L. MicroRNA-223 is neuroprotective by targeting glutamate receptors. Proc Natl Acad Sci USA 109, 18962–18967 (2012).
doi: 10.1073/pnas.1121288109
Gao, X. et al. MiR-21 functions oppositely in proliferation and differentiation of neural stem/precursor cells via regulating AKT and GSK-3beta. Cell Mol Biol (Noisy-le-grand) 62, 144–149 (2016).
doi: 10.14715/cmb/2016.62.12.24
Agoston, V. A. et al. How to Translate Time: The Temporal Aspects of Rodent and Human Pathobiological Processes in Traumatic Brain Injury. Journal of Neurotrauma 36, 1–14 (2019).
doi: 10.1089/neu.2018.6261
Lu, B., Nagappan, G. & Lu, Y. BDNF and synaptic plasticity, cognitive function, and dysfunction. Handb Exp Pharmacol 220, 223–250 (2014).
doi: 10.1007/978-3-642-45106-5_9
Zhang, J. et al. Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biol Psychiatry 70, 334–342 (2011).
doi: 10.1016/j.biopsych.2011.05.018
Richiardi, J. et al. BRAIN NETWORKS. Correlated gene expression supports synchronous activity in brain networks. Science 348, 1241–1244 (2015).
doi: 10.1126/science.1255905
Chiu, H., Alqadah, A. & Chang, C. The role of microRNAs in regulating neuronal connectivity. Front Cell Neurosci 7, 283 (2014).
doi: 10.3389/fncel.2013.00283
Xuanyao, L., Yang, I. L. & Pritchard, J. K. Trans Effects on Gene Expression Can Drive Omnigenic Inheritance. Cell 177, 1022–1034 (2019).
doi: 10.1016/j.cell.2019.04.014
McInnes, K., Friesen, C. L., MacKenzie, D. E., Westwood, D. A. & Boe, S. G. Mild Traumatic Brain Injury (mTBI) and chronic cognitive impairment: A scoping review. PLoS One 12, e0174847 (2017).
doi: 10.1371/journal.pone.0174847
Stocchetti, N. & Zanier, E. R. Chronic impact of traumatic brain injury on outcome and quality of life: a narrative review. Crit Care 20, 148 (2016).
doi: 10.1186/s13054-016-1318-1
Parikh, R. B., Obermeyer, Z. & Navathe, A. S. Regulation of predictive analytics in medicine. Science 363, 810–812 (2019).
doi: 10.1126/science.aaw0029
Cristofori, I. & Levin, H. S. Traumatic brain injury and cognition. Handb Clin Neurol 128, 579–611 (2015).
doi: 10.1016/B978-0-444-63521-1.00037-6