Neuroinflammatory reactive astrocyte formation correlates with adverse outcomes in perinatal white matter injury.
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
26 Jun 2024
26 Jun 2024
Historique:
revised:
15
05
2024
received:
07
09
2023
accepted:
20
05
2024
medline:
26
6
2024
pubmed:
26
6
2024
entrez:
26
6
2024
Statut:
aheadofprint
Résumé
Perinatal white matter injury (WMI) is the leading cause of long-term neurological morbidity in infants born preterm. Neuroinflammation during a critical window of early brain development plays a key role in WMI disease pathogenesis. The mechanisms linking inflammation with the long-term myelination failure that characterizes WMI, however, remain unknown. Here, we investigate the role of astrocyte reactivity in WMI. In an experimental mouse model of WMI, we demonstrate that WMI disease outcomes are improved in mutant mice lacking secretion of inflammatory molecules TNF-α, IL-1α, and C1q known, in addition to other roles, to induce the formation of a neuroinflammatory reactive astrocyte substate. We show that astrocytes express molecular signatures of the neuroinflammatory reactive astrocyte substate in both our WMI mouse model and human tissue affected by WMI, and that this gene expression pattern is dampened in injured mutant mice. Our data provide evidence that a neuroinflammatory reactive astrocyte substate correlates with adverse WMI disease outcomes, thus highlighting the need for further investigation of these cells as potential causal players in WMI pathology.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Dr Miriam and Sheldon G Adelson Medical Research Foundation
Organisme : European Research Council Advanced Grant
ID : 789054
Organisme : NIH HHS
ID : P01NS08351
Pays : United States
Organisme : NIH HHS
ID : R00NS117804
Pays : United States
Organisme : SGGG/Bayer Research Grant 2019
Organisme : UniBE Initiator Award 2020
Organisme : Departmental Research Fund, Department of Obstetrics and Gynecology, Inselspital, Bern
Organisme : NINDS NIH HHS
ID : P01 NS083513
Pays : United States
Informations de copyright
© 2024 The Author(s). GLIA published by Wiley Periodicals LLC.
Références
Back, S. A. (2017). White matter injury in the preterm infant: Pathology and mechanisms. Acta Neuropathologica, 134(3), 331–349.
Ben Haim, L., & Rowitch, D. H. (2017). Functional diversity of astrocytes in neural circuit regulation. Nature Reviews Neuroscience, 18(1), 31–41.
Brandebura, A. N., Paumier, A., Onur, T. S., & Allen, N. J. (2023). Astrocyte contribution to dysfunction, risk and progression in neurodegenerative disorders. Nature Reviews. Neuroscience, 24(1), 23–39.
Eggenberger, S., Boucard, C., Schoeberlein, A., Guzman, R., Limacher, A., Surbek, D., & Mueller, M. (2019). Stem cell treatment and cerebral palsy: Systemic review and meta‐analysis. World journal of Stem Cells, 11(10), 891–903.
Foo, L. C., Allen, N. J., Bushong, E. A., Ventura, P. B., Chung, W. S., Zhou, L., Cahoy, J. D., Daneman, R., Zong, H., Ellisman, M. H., & Barres, B. A. (2011). Development of a method for the purification and culture of rodent astrocytes. Neuron, 71(5), 799–811.
Guttenplan, K. A., Stafford, B. K., El‐Danaf, R. N., Adler, D. I., Münch, A. E., Weigel, M. K., Huberman, A. D., & Liddelow, S. A. (2020). Neurotoxic reactive astrocytes drive neuronal death after retinal injury. Cell Reports, 31(12), 107776.
Guttenplan, K. A., Weigel, M. K., Adler, D. I., Couthouis, J., Liddelow, S. A., Gitler, A. D., & Barres, B. A. (2020). Knockout of reactive astrocyte activating factors slows disease progression in an ALS mouse model. Nature Communications, 11(1), 3753.
Guttenplan, K. A., Weigel, M. K., Prakash, P., Wijewardhane, P. R., Hasel, P., Rufen‐Blanchette, U., Münch, A. E., Blum, J. A., Fine, J., Neal, M. C., Bruce, K. D., Gitler, A. D., Chopra, G., Liddelow, S. A., & Barres, B. A. (2021). Neurotoxic reactive astrocytes induce cell death via saturated lipids. Nature, 599(7883), 102–107.
Hasel, P., Rose, I. V. L., Sadick, J. S., Kim, R. D., & Liddelow, S. A. (2021). Neuroinflammatory astrocyte subtypes in the mouse brain. Nature Neuroscience, 24(10), 1475–1487.
Khakh, B. S., & Sofroniew, M. V. (2015). Diversity of astrocyte functions and phenotypes in neural circuits. Nature Neuroscience, 18(7), 942–952.
Liddelow, S. A., Guttenplan, K. A., Clarke, L. E., Bennett, F. C., Bohlen, C. J., Schirmer, L., Bennett, M. L., Münch, A. E., Chung, W. S., Peterson, T. C., Wilton, D. K., Frouin, A., Napier, B. A., Panicker, N., Kumar, M., Buckwalter, M. S., Rowitch, D. H., Dawson, V. L., Dawson, T. M., … Barres, B. A. (2017). Neurotoxic reactive astrocytes are induced by activated microglia. Nature, 541(7638), 481–487.
Nobuta, H., Ghiani, C. A., Paez, P. M., Spreuer, V., Dong, H., Korsak, R. A., Manukyan, A., Li, J., Vinters, H. V., Huang, E. J., Rowitch, D. H., Sofroniew, M. V., Campagnoni, A. T., de Vellis, J., & Waschek, J. A. (2012). STAT3‐mediated astrogliosis protects myelin development in neonatal brain injury. Annals of Neurology, 72(5), 750–765.
Renz, P., Schoeberlein, A., Haesler, V., Maragkou, T., Surbek, D., & Brosius, L. A. (2022). A novel murine multi‐hit model of perinatal acute diffuse white matter injury recapitulates major features of human disease. Biomedicines, 10(11), 2810.
Shiow, L. R., Favrais, G., Schirmer, L., Schang, A. L., Cipriani, S., Andres, C., Wright, J. N., Nobuta, H., Fleiss, B., Gressens, P., & Rowitch, D. H. (2017). Reactive astrocyte COX2‐PGE2 production inhibits oligodendrocyte maturation in neonatal white matter injury. Glia, 65(12), 2024–2037.
Srivastava, T., Sherman, L. S., & Back, S. A. (2020). Dysregulation of Hyaluronan homeostasis during white matter injury. Neurochemical Research, 45(3), 672–683.
Thomi, G., Surbek, D., Haesler, V., Joerger‐Messerli, M., & Schoeberlein, A. (2019). Exosomes derived from umbilical cord mesenchymal stem cells reduce microglia‐mediated neuroinflammation in perinatal brain injury. Stem Cell Research & Therapy, 10(1), 105.
Volpe, J. J. (2019). Dysmaturation of premature brain: Importance, cellular mechanisms, and potential interventions. Pediatric Neurology, 95, 42–66.
Wheeler, M. A., Jaronen, M., Covacu, R., Zandee, S. E. J., Scalisi, G., Rothhammer, V., Tjon, E. C., Chao, C. C., Kenison, J. E., Blain, M., Rao, V. T. S., Hewson, P., Barroso, A., Gutiérrez‐Vázquez, C., Prat, A., Antel, J. P., Hauser, R., & Quintana, F. J. (2019). Environmental control of astrocyte pathogenic activities in CNS inflammation. Cell, 176(3), 581–596.e18.
Yun, S. P., Kam, T. I., Panicker, N., Kim, S. M., Oh, Y., Park, J. S., Kwon, S. H., Park, Y. J., Karuppagounder, S. S., Park, H., Kim, S., Oh, N., Kim, N. A., Lee, S., Brahmachari, S., Mao, X., Lee, J. H., Kumar, M., An, D., … Ko, H. S. (2018). Block of A1 astrocyte conversion by microglia is neuroprotective in models of Parkinson's disease. Nature Medicine, 24(7), 931–938.
Zamanian, J. L., Xu, L., Foo, L. C., Nouri, N., Zhou, L., Giffard, R. G., & Barres, B. A. (2012). Genomic analysis of reactive astrogliosis. The Journal of Neuroscience, 32(18), 6391–6410.