Microglia cytoarchitecture in the brain of adenosine A


Journal

The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110

Informations de publication

Date de publication:
03 2020
Historique:
received: 12 03 2019
revised: 10 08 2019
accepted: 15 08 2019
pubmed: 28 8 2019
medline: 22 6 2021
entrez: 28 8 2019
Statut: ppublish

Résumé

Microglia cells exert a critical role in brain development, mainly supported by their immune functions, which predicts an impact on the genesis of psychiatric disorders. In fact, microglia stress during gestation is, for instance, associated with chronic anxiety and cognitive deficits accompanied by long-lasting, region- and sex-specific changes in microglia morphology. We recently reported that the pattern of microglia morphologic plasticity, which is sex-determined, impacts on anxious-like behaviour and cognition. We also reported that the pharmacologic blockade of adenosine A

Identifiants

pubmed: 31454441
doi: 10.1111/ejn.14561
doi:

Substances chimiques

Receptor, Adenosine A2A 0
Adenosine K72T3FS567

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1377-1387

Subventions

Organisme : COMPETE
ID : PTDC/NEU-NMC/4154/2014
Pays : International
Organisme : COMPETE
ID : Project POCI-01-0145-FEDER-007440
Pays : International
Organisme : COMPETE
ID : Strategic project: UID/NEU/04539/2013
Pays : International
Organisme : COMPETE
ID : UID/NEU/04539/2019
Pays : International
Organisme : Santa Casa da Misericórdia, Prémio Maratona da Saúde, and Centro 2020 Regional Operational Programme
ID : CENTRO-01-0145-FEDER-000008: BrainHealth 2020
Pays : International
Organisme : Santa Casa da Misericórdia, Prémio Maratona da Saúde, and Centro 2020 Regional Operational Programme
ID : CENTRO-01-0246-FEDER-000010
Pays : International
Organisme : Portuguese Foundation for Science and Technology
ID : PD/BD/114116/2015
Pays : International
Organisme : Portuguese Foundation for Science and Technology
ID : SFRH/BPD/86830/2012
Pays : International

Informations de copyright

© 2019 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Références

Alliot, F., Godin, I., & Pessac, B. (1999). Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Developmental Brain Research, 117, 145-152. https://doi.org/10.1016/S0165-3806(99)00113-3
Beery, A. K., & Zucker, I. (2011). Sex bias in neuroscience and biomedical research. Neuroscience and Biobehavioral Reviews, 35, 565-572. https://doi.org/10.1016/j.neubiorev.2010.07.002
Bollinger, J. L., Bergeon Burns, C. M., & Wellman, C. L. (2016). Differential effects of stress on microglial cell activation in male and female medial prefrontal cortex. Brain, Behavior, and Immunity, 52, 88-97. https://doi.org/10.1016/j.bbi.2015.10.003
Caetano, L., Pinheiro, H., Patrício, P., Mateus-Pinheiro, A., Alves, N. D., Coimbra, B., … Gomes, C. A. (2017). Adenosine A2A receptor regulation of microglia morphological remodeling-gender bias in physiology and in a model of chronic anxiety. Molecular Psychiatry, 22, 1035-1043. https://doi.org/10.1038/mp.2016.173
Chen, J., Huang, Z., Ma, J., Zhu, J., Moratalla, R., Standaert, D., … Schwarzschild, M. A. (1999). A 2A adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. The Journal of Neuroscience, 19, 9192-9200. https://doi.org/10.1523/JNEUROSCI.19-21-09192.1999
Chen, Z., & Trapp, B. D. (2016). Microglia and neuroprotection. Journal of Neurochemistry, 136, 10-17. https://doi.org/10.1111/jnc.13062
Clark, A. K., & Malcangio, M. (2012). Microglial signalling mechanisms: Cathepsin S and Fractalkine. Experimental Neurology, 234, 283-292. https://doi.org/10.1016/j.expneurol.2011.09.012
Claypoole, L. D., Zimmerberg, B., & Williamson, L. L. (2017). Neonatal lipopolysaccharide treatment alters hippocampal neuroinflammation, microglia morphology and anxiety-like behavior in rats selectively bred for an infantile trait. Brain, Behavior, and Immunity, 59, 135-146. https://doi.org/10.1016/j.bbi.2016.08.017
Conlay, L. A., Conant, J. A., Debros, F., & Wurtman, R. (1997). Caffeine alters plasma adenosine levels [9]. Nature, 389, 136. https://doi.org/10.1038/38160
Cuadros, M. A., Martin, C., Coltey, P., Almendros, A., & Navascués, J. (1993). First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. The Journal of Comparative Neurology, 330, 113-129. https://doi.org/10.1002/cne.903300110
Cunha, R. A. (2016). How does adenosine control neuronal dysfunction and neurodegeneration? Journal of Neurochemistry, 139, 1019-1055. https://doi.org/10.1111/jnc.13724
Dalmau, I., Vela, J. M., González, B., Finsen, B., & Castellano, B. (2003). Dynamics of microglia in the developing rat brain. The Journal of Comparative Neurology, 458, 144-157. https://doi.org/10.1002/cne.10572
Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., … Gan, W.-B. (2005). ATP mediates rapid microglial response to local brain injury in vivo. Nature Neuroscience, 8, 752-758. https://doi.org/10.1038/nn1472
De Vries, G. J., & Forger, N. G. (2015). Sex differences in the brain: A whole body perspective. Biology of Sex Differences, 6, 1-15.
Duarte, J. M., Gaspar, R., Caetano, L., Patrício, P., Soares-Cunha, C., Mateus-Pinheiro, A., … Gomes, C. A. (2018). Region-specific control of microglia by adenosine A 2A receptors: Uncoupling anxiety and associated cognitive deficits in female rats. Glia, 28, S35-S36.
George, J., Gonçalves, F. Q., Cristóvão, G., Rodrigues, L., Meyer Fernandes, J. R., Gonçalves, T., … Gomes, C. A. (2015). Different danger signals differently impact on microglial proliferation through alterations of ATP release and extracellular metabolism. Glia, 63, 1636-1645. https://doi.org/10.1002/glia.22833
Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., … Merad, M. (2010). Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science, 330, 841-845. https://doi.org/10.1126/science.1194637
Gomes, C., Ferreira, R., George, J., Sanches, R., Rodrigues, D. I., Gonçalves, N., & Cunha, R. A. (2013). Activation of microglial cells triggers a release of brain-derived neurotrophic factor (BDNF) inducing their proliferation in an adenosine A2A receptor-dependent manner: A2A receptor blockade prevents BDNF release and proliferation of microglia. Journal of Neuroinflammation, 10, 16.
Grabert, K., Michoel, T., Karavolos, M. H., Clohisey, S., Baillie, J. K., Stevens, M. P., … McColl, B. W. (2016). Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nature Neuroscience, 19, 504-516. https://doi.org/10.1038/nn.4222
Gyoneva, S., Swanger, S. A., Zhang, J., Weinshenker, D., & Traynelis, S. F. (2016). Altered motility of plaque-associated microglia in a model of Alzheimer's disease. Neuroscience, 330, 410-420. https://doi.org/10.1016/j.neuroscience.2016.05.061
Hellwig, S., Brioschi, S., Dieni, S., Frings, L., Masuch, A., Blank, T., & Biber, K. (2016). Altered microglia morphology and higher resilience to stress-induced depression-like behavior in CX3CR21-deficient mice. Brain, Behavior, and Immunity, 55, 126-137. https://doi.org/10.1016/j.bbi.2015.11.008
Huang, Q., Wei, C., Yu, L., Coelho, J. E., Shen, H., Kalda, A., … Chen, J. (2006). Adenosine A 2A receptors in bone marrow-derived cells but not in forebrain neurons are important contributors to 3-nitropropionic acid-induced striatal damage as revealed by cell-type-selective inactivation. The Journal of Neuroscience, 26, 11371-11378. https://doi.org/10.1523/JNEUROSCI.1907-06.2006
Kaster, M. P., Machado, N. J., Silva, H. B., Nunes, A., Ardais, A. P., Santana, M., … Cunha, R. A. (2015). Caffeine acts through neuronal adenosine A 2A receptors to prevent mood and memory dysfunction triggered by chronic stress. Proceedings of the National Academy of Sciences, 112, 201423088.
Lenz, K. M., & McCarthy, M. M. (2015). A starring role for microglia in brain sex differences. Neuroscientist, 21, 306-321. https://doi.org/10.1177/1073858414536468
Lenz, K. M., Nugent, B. M., Haliyur, R., & McCarthy, M. M. (2013). Microglia are essential to masculinization of brain and behavior. Journal of Neuroscience, 33, 2761-2772. https://doi.org/10.1523/JNEUROSCI.1268-12.2013
Li, Z., Ma, L., Kulesskaya, N., Võikar, V., & Tian, L. (2014). Microglia are polarized to M1 type in high-anxiety inbred mice in response to lipopolysaccharide challenge. Brain, Behavior, and Immunity, 38, 237-248. https://doi.org/10.1016/j.bbi.2014.02.008
Luders, E., & Toga, A. W. (2010). Sex differences in brain anatomy. In I. Savic (Ed.), Progress in brain research. Elsevier B.V., pp. 2-12.
Luongo, L., Guida, F., Imperatore, R., Napolitano, F., Gatta, L., Cristino, L., … Maione, S. (2014). The A1 adenosine receptor as a new player in microglia physiology. Glia, 62, 122-132. https://doi.org/10.1002/glia.22592
Nelson, L. H., Warden, S., & Lenz, K. M. (2017). Sex differences in microglial phagocytosis in the neonatal hippocampus. Brain, Behavior, and Immunity, 64, 11-22. https://doi.org/10.1016/j.bbi.2017.03.010
Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005). Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Neuroforum, 11, 95-96.
Ohsawa, K., Sanagi, T., Nakamura, Y., Suzuki, E., Inoue, K., & Kohsaka, S. (2012). Adenosine A3 receptor is involved in ADP-induced microglial process extension and migration. Journal of Neurochemistry, 121, 217-227. https://doi.org/10.1111/j.1471-4159.2012.07693.x
Orr, A. G., Hsiao, E. C., Wang, M. M., Ho, K., Kim, D. H., Wang, X., … Mucke, L. (2015). Astrocytic adenosine receptor A2A and Gs-coupled signaling regulate memory. Nature Neuroscience, 18, 423-434. https://doi.org/10.1038/nn.3930
Orr, A. G., Orr, A. L., Li, X.-J., Gross, R. E., & Traynelis, S. F. (2009). Adenosine A2A receptor mediates microglial process retraction. Nature Neuroscience, 12, 872-878. https://doi.org/10.1038/nn.2341
Panzica, G., & Melcangi, R. C. (2016). Structural and molecular brain sexual differences: A tool to understand sex differences in health and disease. Neuroscience and Biobehavioral Reviews, 67, 2-8. https://doi.org/10.1016/j.neubiorev.2016.04.017
Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., … Gross, C. T. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science, 333, 1456-1458. https://doi.org/10.1126/science.1202529
Peri, F., & Nüsslein-Volhard, C. (2008). Live imaging of neuronal degradation by microglia reveals a role for v0-ATPase a1 in phagosomal fusion in vivo. Cell, 133, 916-927. https://doi.org/10.1016/j.cell.2008.04.037
Ribeiro, F. F., Neves-Tomé, R., Assaife-Lopes, N., Santos, T. E., Silva, R. F. M., Brites, D., … Sebastião, A. M. (2016). Axonal elongation and dendritic branching is enhanced by adenosine A2A receptors activation in cerebral cortical neurons. Brain Structure and Function, 221, 2777-2799. https://doi.org/10.1007/s00429-015-1072-1
Santiago, A. R., Baptista, F. I., Santos, P. F., Cristóvão, G., Ambrósio, A. F., Cunha, R. A., & Gomes, C. A. (2014). Role of microglia adenosine A 2A receptors in retinal and brain neurodegenerative diseases. Mediators of Inflammation, 2014, 1-13. https://doi.org/10.1155/2014/465694
Schwarz, J. M., Sholar, P. W., & Bilbo, S. D. (2012). Sex differences in microglial colonization of the developing rat brain. Journal of Neurochemistry, 120, 948-963.
Shen, H.-Y., Canas, P. M., Garcia-Sanz, P., Lan, J.-Q., Boison, D., Moratalla, R., … Chen, J.-F. (2013). Adenosine A2A receptors in striatal glutamatergic terminals and GABAergic neurons oppositely modulate psychostimulant action and DARPP-32 phosphorylation. PLoS ONE, 8, e80902. https://doi.org/10.1371/journal.pone.0080902
Silva, C. G., Metin, C., Fazeli, W., Machado, N. J., Darmopil, S., Launay, P.-S., … Bernard, C. (2013). Adenosine receptor antagonists including caffeine alter fetal brain development in mice. Science Translational Medicine, 5, 197ra104-197ra104.
Thion, M. S., & Garel, S. (2017). On place and time: Microglia in embryonic and perinatal brain development. Current Opinion in Neurobiology, 47, 121-130. https://doi.org/10.1016/j.conb.2017.10.004
Tremblay, M.-È., Lowery, R. L., & Majewska, A. K. (2010). Microglial interactions with synapses are modulated by visual experience. PLoS Biology, 8(11), e1000527. https://doi.org/10.1371/journal.pbio.1000527
van Berckel, B. N., Bossong, M. G., Boellaard, R., Kloet, R., Schuitemaker, A., Caspers, E., … Kahn, R. S. (2008). Microglia activation in recent-onset schizophrenia: A quantitative (R)-[11C]PK11195 positron emission tomography study. Biological Psychiatry, 64, 820-822. https://doi.org/10.1016/j.biopsych.2008.04.025
Van den Eynde, K., Missault, S., Fransen, E., Raeymaekers, L., Willems, R., Drinkenburg, W., … Dedeurwaerdere, S. (2014). Hypolocomotive behaviour associated with increased microglia in a prenatal immune activation model with relevance to schizophrenia. Behavioral Brain Research, 258, 179-186. https://doi.org/10.1016/j.bbr.2013.10.005
Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S., & Nabekura, J. (2009). Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. Journal of Neuroscience, 29, 3974-3980. https://doi.org/10.1523/JNEUROSCI.4363-08.2009
Yu, L., Huang, Z., Mariani, J., Wang, Y., Moskowitz, M., & Chen, J. (2004). Selective inactivation or reconstitution of adenosine A 2A receptors in bone marrow cells reveals their significant contribution to the development of ischemic brain injury. Nature Medicine, 10, 1081-1088. https://doi.org/10.1038/nm1103
Yu, L., Shen, H.-Y., Coelho, J. E., Araújo, I. M., Huang, Q.-Y., Day, Y.-J., … Chen, J.-F. (2008). Adenosine A 2A receptor antagonists exert motor and neuroprotective effects by distinct cellular mechanisms. Annals of Neurology, 63, 338-346. https://doi.org/10.1002/ana.21313
Zhao, D., Mokhtari, R., Pedrosa, E., Birnbaum, R., Zheng, D., & Lachman, H. M. (2017). Transcriptome analysis of microglia in a mouse model of Rett syndrome: Differential expression of genes associated with microglia/macrophage activation and cellular stress. Molecular Autism, 8, 17. https://doi.org/10.1186/s13229-017-0134-z

Auteurs

Carla Simões-Henriques (C)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.

Miguel Mateus-Pinheiro (M)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.

Rita Gaspar (R)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.

Helena Pinheiro (H)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.

Joana Mendes Duarte (J)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.

Filipa I Baptista (FI)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.

Paula M Canas (PM)

Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.
Center for Neuroscience and Cell Biology (CNC), University of Coimbra, Coimbra, Portugal.

Carlos Alberto Fontes-Ribeiro (CA)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.
Faculty of Medicine, Institute of Pharmacology and Experimental Therapeutics, University of Coimbra, Coimbra, Portugal.

Rodrigo A Cunha (RA)

Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.
Center for Neuroscience and Cell Biology (CNC), University of Coimbra, Coimbra, Portugal.

António F Ambrósio (AF)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.

Catarina A Gomes (CA)

Faculty of Medicine, Coimbra Institute for Clinical and Biomedical Research (iCBR), University of Coimbra, Coimbra, Portugal.
Center for Innovative Biomedicine and Biotechnology, University of Coimbra, Coimbra, Portugal.
CNC.IBILI, University of Coimbra, Coimbra, Portugal.
Faculty of Medicine, Institute of Pharmacology and Experimental Therapeutics, University of Coimbra, Coimbra, Portugal.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH