The laminar position, morphology, and gene expression profiles of cortical astrocytes are influenced by time of birth from ventricular/subventricular progenitors.
astrocyte
cortical development
neural progenitor cell
radial glia
ventricular/subventricular zone
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
09 Jun 2024
09 Jun 2024
Historique:
revised:
06
05
2024
received:
21
07
2023
accepted:
27
05
2024
medline:
9
6
2024
pubmed:
9
6
2024
entrez:
9
6
2024
Statut:
aheadofprint
Résumé
Astrocytes that reside in superficial (SL) and deep cortical layers have distinct molecular profiles and morphologies, which may underlie specific functions. Here, we demonstrate that the production of SL and deep layer (DL) astrocyte populations from neural progenitor cells in the mouse is temporally regulated. Lineage tracking following in utero and postnatal electroporation with PiggyBac (PB) EGFP and birth dating with EdU and FlashTag, showed that apical progenitors produce astrocytes during late embryogenesis (E16.5) that are biased to the SL, while postnatally labeled (P0) astrocytes are biased to the DL. In contrast, astrocytes born during the predominantly neurogenic window (E14.5) showed a random distribution in the SL and DL. Of interest, E13.5 astrocytes birth dated at E13.5 with EdU showed a lower layer bias, while FT labeling of apical progenitors showed no bias. Finally, examination of the morphologies of "biased" E16.5- and P0-labeled astrocytes demonstrated that E16.5-labeled astrocytes exhibit different morphologies in different layers, while P0-labeled astrocytes do not. Differences based on time of birth are also observed in the molecular profiles of E16.5 versus P0-labeled astrocytes. Altogether, these results suggest that the morphological, molecular, and positional diversity of cortical astrocytes is related to their time of birth from ventricular/subventricular zone progenitors.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN-2020-06512
Organisme : National Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN-2024-04539
Organisme : National Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN-2024-05363
Organisme : Canadian Foundation for Innovation (CFI)
ID : 38013
Organisme : Canadian Foundation for Innovation (CFI)
ID : 36661
Organisme : The Connaught Fund Young Investigator Award
Organisme : Christiane and Claudia Hempel Foundation for Regenerative Medicine
Organisme : Jürgen Manchot Foundation
Organisme : Canadian Institutes of Health Research (CIHR)
ID : 420504
Organisme : Canadian Institutes of Health Research (CIHR)
ID : CGS-M
Organisme : The Fonds de recherche du Québec (FRQ) in partnership with Parkinson Québec
Organisme : Ontario Research Fund
Organisme : Canada Research Chairs Program
ID : 950-231616
Organisme : Genome Canada/the Ontario Genomics Institute/the Province of Ontario
Organisme : James and Elisabeth Cloppenburg, Peek and Cloppenburg Düsseldorf Foundation
Informations de copyright
© 2024 The Author(s). GLIA published by Wiley Periodicals LLC.
Références
Bandler, R. C., Vitali, I., Delgado, R. N., Ho, M. C., Dvoretskova, E., Ibarra Molinas, J. S., Frazel, P. W., Mohammadkhani, M., Machold, R., Maedler, S., Liddelow, S. A., Nowakowski, T. J., Fishell, G., & Mayer, C. (2022). Single‐cell delineation of lineage and genetic identity in the mouse brain. Nature, 601(7893), 404–409.
Bayraktar, O. A., Bartels, T., Polioudakis, D., Holmqvist, S., Ben Haim, L., Young, A. M. H., Prakash, K., Brown, A., Paredes, M. F., Kawaguchi, R., Stockley, J., Sabeur, K., Chang, S. M., Huang, E., Hutchinson, P., Ullian, E. M., Geschwind, D. H., Coppola, G., & Rowitch, D. H. (2018). Single‐cell in situ transcriptomic map of astrocyte cortical layer diversity. bioRxiv.
Bayraktar, O. A., Fuentealba, L. C., Alvarez‐Buylla, A., & Rowitch, D. H. (2014). Astrocyte development and heterogeneity. Cold Spring Harbor Perspectives in Biology, 7(1), a020362.
Berry, M., & Rogers, A. W. (1965). The migration of neuroblasts in the developing cerebral cortex. Journal of Anatomy, 99(Pt 4), 691–709.
Cerrato, V., Parmigiani, E., Figueres‐Oñate, M., Betizeau, M., Aprato, J., Nanavaty, I., Berchialla, P., Luzzati, F., de'Sperati, C., López‐Mascaraque, L., & Buffo, A. (2018). Multiple origins and modularity in the spatiotemporal emergence of cerebellar astrocyte heterogeneity. PLoS Biology, 16(9), e2005513.
Clavreul, S., Abdeladim, L., Hernández‐Garzón, E., Niculescu, D., Durand, J., Ieng, S. H., Barry, R., Bonvento, G., Beaurepaire, E., Livet, J., & Loulier, K. (2019). Cortical astrocytes develop in a plastic manner at both clonal and cellular levels. Nature Communications, 10(1), 4884.
Dimou, L., Simon, C., Kirchhoff, F., Takebayashi, H., & Götz, M. (2008). Progeny of Olig2‐expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. The Journal of Neuroscience, 28(41), 10434–10442.
Endo, F., Kasai, A., Soto, J. S., Yu, X., Qu, Z., Hashimoto, H., Gradinaru, V., Kawaguchi, R., & Khakh, B. S. (2022). Molecular basis of astrocyte diversity and morphology across the CNS in health and disease. Science, 378(6619), eadc9020.
Evers, D. L., Fowler, C. B., Cunningham, B. R., Mason, J. T., & O'Leary, T. J. (2011). The effect of formaldehyde fixation on RNA: Optimization of formaldehyde adduct removal. The Journal of Molecular Diagnostics, 13(3), 282–288.
Fuentealba, L. C., Rompani, S. B., Parraguez, J. I., Obernier, K., Romero, R., Cepko, C. L., & Alvarez‐Buylla, A. (2015). Embryonic origin of postnatal neural stem cells. Cell, 161(7), 1644–1655.
Furutachi, S., Miya, H., Watanabe, T., Kawai, H., Yamasaki, N., Harada, Y., Imayoshi, I., Nelson, M., Nakayama, K. I., Hirabayashi, Y., & Gotoh, Y. (2015). Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells. Nature Neuroscience, 18(5), 657–665.
Gao, P., Postiglione, M. P., Krieger, T. G., Hernandez, L., Wang, C., Han, Z., Streicher, C., Papusheva, E., Insolera, R., Chugh, K., Kodish, O., Huang, K., Simons, B. D., Luo, L., Hippenmeyer, S., & Shi, S. H. (2014). Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell, 159(4), 775–788.
Garcia‐Marques, J., & Lopez‐Mascaraque, L. (2013). Clonal identity determines astrocyte cortical heterogeneity. Cerebral Cortex, 23(6), 1463–1472.
Ge, W. P., Miyawaki, A., Gage, F. H., Jan, Y. N., & Jan, L. Y. (2012). Local generation of glia is a major astrocyte source in postnatal cortex. Nature, 484(7394), 376–380.
Gingrich, E. C., Case, K., & Garcia, A. D. R. (2022). A subpopulation of astrocyte progenitors defined by sonic hedgehog signaling. Neural Development, 17(1), 2.
Govindan, S., Oberst, P., & Jabaudon, D. (2018). In vivo pulse labeling of isochronic cohorts of cells in the central nervous system using FlashTag. Nature Protocols, 13(10), 2297–2311.
Guillemot, F. (2007). Spatial and temporal specification of neural fates by transcription factor codes. Development, 134(21), 3771–3780.
Hochstim, C., Deneen, B., Lukaszewicz, A., Zhou, Q., & Anderson, D. J. (2008). Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell, 133(3), 510–522.
Hofer, T., Busch, K., Klapproth, K., & Rodewald, H.‐R. (2016). Fate mapping and quantitation of hematopoiesis in vivo. Annual Review of Immunology, 34, 449–478.
Huang, W., Zhao, N., Bai, X., Karram, K., Trotter, J., Goebbels, S., Scheller, A., & Kirchhoff, F. (2014). Novel NG2‐CreERT2 knock‐in mice demonstrate heterogeneous differentiation potential of NG2 glia during development. Glia, 62(6), 896–913.
Iacobas, D. A., Iacobas, S., Stout, R. F., & Spray, D. C. (2020). Cellular environment remodels the genomic fabrics of functional pathways in astrocytes. Genes, 11(5), 520.
Lanjakornsiripan, D., Pior, B. J., Kawaguchi, D., Furutachi, S., Tahara, T., Katsuyama, Y., Suzuki, Y., Fukazawa, Y., & Gotoh, Y. (2018). Layer‐specific morphological and molecular differences in neocortical astrocytes and their dependence on neuronal layers. Nature Communications, 9(1), 1623.
Li, X., Liu, G., Yang, L., Li, Z., Zhang, Z., Xu, Z., Cai, Y., du, H., Su, Z., Wang, Z., Duan, Y., Chen, H., Shang, Z., You, Y., Zhang, Q., He, M., Chen, B., & Yang, Z. (2021). Decoding Cortical Glial Cell Development. Neuroscience Bulletin, 37(4), 440–460.
Liu, J., Wu, X., & Lu, Q. (2022). Molecular divergence of mammalian astrocyte progenitor cells at early gliogenesis. Development, 149(5), dev199985.
Luskin, M. B., & McDermott, K. (1994). Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia, 11(3), 211–226.
Magavi, S., Friedmann, D., Banks, G., Stolfi, A., & Lois, C. (2012). Coincident generation of pyramidal neurons and protoplasmic astrocytes in neocortical columns. The Journal of Neuroscience, 32(14), 4762–4772.
Marshall, C. A., & Goldman, J. E. (2002). Subpallial dlx2‐expressing cells give rise to astrocytes and oligodendrocytes in the cerebral cortex and white matter. The Journal of Neuroscience, 22(22), 9821–9830.
Miller, F. D., & Gauthier, A. S. (2007). Timing is everything: Making neurons versus glia in the developing cortex. Neuron, 54(3), 357–369.
Molofsky, A. V., Krenick, R., Ullian, E., Tsai, H. H., Deneen, B., Richardson, W. D., Barres, B. A., & Rowitch, D. H. (2012). Astrocytes and disease: A neurodevelopmental perspective. Genes & Development, 26(9), 891–907.
Molyneaux, B. J., Arlotta, P., Menezes, J. R. L., & Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nature Reviews. Neuroscience, 8(6), 427–437.
Morel, L., Chiang, M. S. R., Higashimori, H., Shoneye, T., Iyer, L. K., Yelick, J., Tai, A., & Yang, Y. (2017). Molecular and functional properties of regional astrocytes in the adult brain. The Journal of Neuroscience, 37(36), 8706–8717.
Nery, S., Fishell, G., & Corbin, J. G. (2002). The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nature Neuroscience, 5(12), 1279–1287.
Noctor, S. C., Martinez‐Cerdeno, V., & Kriegstein, A. R. (2008). Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. The Journal of Comparative Neurology, 508(1), 28–44.
Oberheim, N. A., Takano, T., Han, X., He, W., Lin, J. H. C., Wang, F., Xu, Q., Wyatt, J. D., Pilcher, W., Ojemann, J. G., Ransom, B. R., Goldman, S. A., & Nedergaard, M. (2009). Uniquely hominid features of adult human astrocytes. The Journal of Neuroscience, 29(10), 3276–3287.
Oberst, P., Fièvre, S., Baumann, N., Concetti, C., Bartolini, G., & Jabaudon, D. (2019). Temporal plasticity of apical progenitors in the developing mouse neocortex. Nature, 573(7774), 370–374.
Ojalvo‐Sanz, A. C., & Lopez‐Mascaraque, L. (2021). Gliogenic potential of single pallial radial glial cells in lower cortical layers. Cells, 10(11), 3237.
Ojalvo‐Sanz, A. C., Pernia‐Solanilla, C., & Lopez‐Mascaraque, L. (2024). Spatial organization of astrocyte clones: The role of developmental progenitor timing. Glia, 72, 1290–1303.
Ollion, J., Cochennec, J., Loll, F., Escudé, C., & Boudier, T. (2013). TANGO: A generic tool for high‐throughput 3D image analysis for studying nuclear organization. Bioinformatics, 29(14), 1840–1841.
Petrelli, F., Dallérac, G., Pucci, L., Calì, C., Zehnder, T., Sultan, S., Lecca, S., Chicca, A., Ivanov, A., Asensio, C. S., Gundersen, V., Toni, N., Knott, G. W., Magara, F., Gertsch, J., Kirchhoff, F., Déglon, N., Giros, B., Edwards, R. H., … Bezzi, P. (2020). Dysfunction of homeostatic control of dopamine by astrocytes in the developing prefrontal cortex leads to cognitive impairments. Molecular Psychiatry, 25(4), 732–749.
Sanchez‐Gonzalez, R., Bribian, A., & Lopez‐Mascaraque, L. (2020). Cell fate potential of NG2 progenitors. Scientific Reports, 10(1), 9876.
Scott, E. Y., Safarian, N., Casasbuenas, D. L., Dryden, M., Tockovska, T., Ali, S., Peng, J., Daniele, E., Nie Xin Lim, I., Bang, K. W. A., Tripathy, S., Yuzwa, S. A., Wheeler, A. R., & Faiz, M. (2024). Integrating single‐cell and spatially resolved transcriptomic strategies to survey the astrocyte response to stroke in male mice. Nature Communications, 15(1), 1584.
Stolt, C. C., Lommes, P., Sock, E., Chaboissier, M. C., Schedl, A., & Wegner, M. (2003). The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes & Development, 17(13), 1677–1689.
Sun, W., Cornwell, A., Li, J., Peng, S., Osorio, M. J., Aalling, N., Wang, S., Benraiss, A., Lou, N., Goldman, S. A., & Nedergaard, M. (2017). SOX9 is an astrocyte‐specific nuclear marker in the adult brain outside the neurogenic regions. The Journal of Neuroscience, 37(17), 4493–4507.
Tabata, H. (2015). Diverse subtypes of astrocytes and their development during corticogenesis. Frontiers in Neuroscience, 9, 114.
Tabata, H., & Nakajima, K. (2001). Efficient in utero gene transfer system to the developing mouse brain using electroporation: Visualization of neuronal migration in the developing cortex. Neuroscience, 103(4), 865–872.
Tabata, H., Sasaki, M., Agetsuma, M., Sano, H., Hirota, Y., Miyajima, M., Hayashi, K., Honda, T., Nishikawa, M., Inaguma, Y., Ito, H., Takebayashi, H., Ema, M., Ikenaka, K., Nabekura, J., Nagata, K. I., & Nakajima, K. (2022). Erratic and blood vessel‐guided migration of astrocyte progenitors in the cerebral cortex. Nature Communications, 13(1), 6571.
Tatsumi, K., Isonishi, A., Yamasaki, M., Kawabe, Y., Morita‐Takemura, S., Nakahara, K., Terada, Y., Shinjo, T., Okuda, H., Tanaka, T., & Wanaka, A. (2018). Olig2‐lineage astrocytes: A distinct subtype of astrocytes that differs from GFAP astrocytes. Frontiers in Neuroanatomy, 12, 8.
Tsai, H. H., Li, H., Fuentealba, L. C., Molofsky, A. V., Taveira‐Marques, R., Zhuang, H., Tenney, A., Murnen, A. T., Fancy, S. P., Merkle, F., Kessaris, N., Alvarez‐Buylla, A., Richardson, W. D., & Rowitch, D. H. (2012). Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science, 337(6092), 358–362.
Wang, J., Xu, J., Zang, G., Zhang, T., Wu, Q., Zhang, H., Chen, Y., Wang, Y., Qin, W., Zhao, S., Qin, E., Qiu, J., Zhang, X., Wen, L., Wang, Y., & Wang, G. (2022). Trans‐2‐enoyl‐CoA reductase Tecr‐driven lipid metabolism in endothelial cells protects against transcytosis to maintain blood‐brain barrier homeostasis. Research (Wash D C), 2022, 9839368.
Zerlin, M., & Goldman, J. E. (1997). Interactions between glial progenitors and blood vessels during early postnatal corticogenesis: Blood vessel contact represents an early stage of astrocyte differentiation. The Journal of Comparative Neurology, 387(4), 537–546.
Zhou, J., Vitalia, I., Roig‐Puiggros, S., Javed, A., Jaboudon, D., Mayer, C., & Bocchi, R. (2023). Dual lineage origins of neocortical astrocytes. bioRxiv.