Diverse subtypes of astrocytes and their development during corticogenesis

Frontiers in Neuroscience

Volumn 9, Issue APR, 2015, Pages

  Tabata, Hidenori ^a  

^a INSTITUTE FOR DEVELOPMENTAL RESEARCH   (Japan)

Author keywords

Astrocyte; Cell specification; Cerebral cortex; Gliogenesis; Oligodendrocyte; Subventricular zone

Indexed keywords

CRE RECOMBINASE; GLIAL FIBRILLARY ACIDIC PROTEIN; HERMES ANTIGEN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR;

ASTROCYTE; ASYMMETRIC CELL DIVISION; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CORTICAL VENTRICULAR ZONE; CORTICOGENESIS; ELECTROPORATION; GENE OVEREXPRESSION; GENE TRANSFER; GLIA CELL; GOLGI STAIN; GRAY MATTER; HUMAN; IMMUNOHISTOCHEMISTRY; NEURAL STEM CELL; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; PROTOPLASMIC ASTROCYTE; SHORT SURVEY; SUBVENTRICULAR ZONE; SYNAPSE; TRANSPOSON; WHITE MATTER;

EID: 84928680622     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00114     Document Type: Short Survey

References (71)

1. Alvarez-Buylla, A., and Garcia-Verdugo, J. M. (2002). Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634.
2. Bandeira, F., Lent, R., and Herculano-Houzel, S. (2009). Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc. Natl. Acad. Sci. U.S.A. 106, 14108-14113. doi: 10.1073/pnas.0804650106
3. Bass, N. H., Hess, H. H., Pope, A., and Thalheimer, C. (1971). Quantitative cytoarchitectonic distribution of neurons, glia, and DNA in rat cerebral cortex. J. Comp. Neurol. 143, 481-490. doi: 10.1002/cne.901430405
4. Burda, J. E., and Sofroniew, M. V. (2014). Reactive gliosis and the multicellular response to CNS damage and disease. Neuron 81, 229-248. doi: 10.1016/j.neuron.2013.12.034
5. Bushong, E. A., Martone, M. E., Jones, Y. Z., and Ellisman, M. H. (2002). Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22, 183-192.
6. Cai, J., Chen, Y., Cai, W.-H., Hurlock, E. C., Wu, H., Kernie, S. G., et al. (2007). A crucial role for Olig2 in white matter astrocyte development. Development 134, 1887-1899. doi: 10.1242/dev.02847
7. Cameron, R. S., and Rakic, P. (1991). Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 4, 124-137. doi: 10.1002/glia.440040204
8. Colombo, J. A., Lipina, S., Yáñez, A., and Puissant, V. (1997). Postnatal development of interlaminar astroglial processes in the cerebral cortex of primates. Int. J. Dev. Neurosci. 15, 823-833. doi: 10.1016/S0736-5748(97)00043-9
9. Colombo, J. A., and Reisin, H. D. (2004). Interlaminar astroglia of the cerebral cortex: a marker of the primate brain. Brain Res. 1006, 126-131. doi: 10.1016/j.brainres.2004.02.003
10. Costa, M. R., Bucholz, O., Schroeder, T., and Götz, M. (2009). Late origin of glia-restricted progenitors in the developing mouse cerebral cortex. Cereb. Cortex 19(Suppl. 1), i135-i143. doi: 10.1093/cercor/bhp046
11. Costa, M. R., Kessaris, N., Richardson, W. D., Götz, M., and Hedin-Pereira, C. (2007). The marginal zone/layer I as a novel niche for neurogenesis and gliogenesis in developing cerebral cortex. J. Neurosci. 27, 11376-11388. doi: 10.1523/JNEUROSCI.2418-07.2007
12. de Azevedo, L. C., Fallet, C. R., Moura-Neto, V., Daumas-Duport, C. R., Hedin-Pereira, C., and Lent, R. (2003). Cortical radial glial cells in human fetuses: depth-correlated transformation into astrocytes. J. Neurobiol. 55, 288-298. doi: 10.1002/neu.10205
13. de los Monteros, A. E., Zhang, M., and De Vellis, J. (1993). O2A progenitor cells transplanted into the neonatal rat brain develop into oligodendrocytes but not astrocytes. Proc. Natl. Acad. Sci. U.S.A. 90, 50-54.
14. Eisenbarth, G. S., Walsh, F. S., and Nirenberg, M. (1979). Monoclonal antibody to a plasma membrane antigen of neurons. Proc. Natl. Acad. Sci. U.S.A. 76, 4913-4917.
15. Fujita, S. (1963). The matrix cell and cytogenesis in the developing central nervous system. J. Comp. Neurol. 120, 37-42.
16. Fukuchi-Shimogori, T. (2001). Neocortex patterning by the secreted signaling molecule FGF8. Science 294, 1071-1074. doi: 10.1126/science.1064252
17. Gao, P., Postiglione, M. P., Krieger, T. G., Hernandez, L., Wang, C., Han, Z., et al. (2014). Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell 159, 775-788. doi: 10.1016/j.cell.2014.10.027
18. García-Marques, J., and López-Mascaraque, L. (2013). Clonal identity determines astrocyte cortical heterogeneity. Cereb. Cortex 23, 1463-1472. doi: 10.1093/cercor/bhs134
19. Ge, W.-P., Miyawaki, A., Gage, F. H., Jan, Y. N., and Jan, L. Y. (2012). Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484, 376-380. doi: 10.1038/nature10959
20. Gressens, P., Richelme, C., Kadhim, H. J., Gadisseux, J. F., and Evrard, P. (1992). The germinative zone produces the most cortical astrocytes after neuronal migration in the developing mammalian brain. Biol. Neonate 61, 4-24.
21. Halassa, M. M., Fellin, T., Takano, H., Dong, J.-H., and Haydon, P. G. (2007). Synaptic islands defined by the territory of a single astrocyte. J. Neurosci. 27, 6473-6477. doi: 10.1523/JNEUROSCI.1419-07.2007
22. Han, X., Chen, M., Wang, F., Windrem, M., Wang, S., Shanz, S., et al. (2013). Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Stem Cell 12, 342-353. doi: 10.1016/j.stem.2012.12.015
23. Henneberger, C., Papouin, T., Oliet, S. H. R., and Rusakov, D. A. (2010). Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232-236. doi: 10.1038/nature08673
24. Kawakami, K., and Noda, T. (2004). Transposition of the Tol2 element, an Ac-like element from the Japanese medaka fish Oryzias latipes, in mouse embryonic stem cells. Genetics 166, 895-899. doi: 10.1534/genetics.166.2.895
25. Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., and Richardson, W. D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9, 173-179. doi: 10.1038/nn1620
26. Kucukdereli, H., Allen, N. J., Lee, A. T., Feng, A., Ozlu, M. I., Conatser, L. M., et al. (2011). Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc. Natl. Acad. Sci. U.S.A. 108, E440-E449. doi: 10.1073/pnas.1104977108
27. Levison, S. W., Chuang, C., Abramson, B. J., and Goldman, J. E. (1993). The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development 119, 611-622.
28. Levison, S. W., and Goldman, J. E. (1993). Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10, 201-212.
29. Levitt, P., Cooper, M. L., and Rakic, P. (1981). Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci. 1, 27-39.
30. Marín-Padilla, M. (1995). Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocytes in the human cerebral cortex: a Golgi study. J. Comp. Neurol. 357, 554-572. doi: 10.1002/cne.903570407
31. Marshall, C. A. G., and Goldman, J. E. (2002). Subpallial dlx2-expressing cells give rise to astrocytes and oligodendrocytes in the cerebral cortex and white matter. J. Neurosci. 22, 9821-9830.
32. Marshall, C. A. G., Novitch, B. G., and Goldman, J. E. (2005). Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J. Neurosci. 25, 7289-7298. doi: 10.1523/JNEUROSCI.1924-05.2005
33. Martín-López, E., García-Marques, J., Núñez-Llaves, R., and López-Mascaraque, L. (2013). Clonal astrocytic response to cortical injury. PLoS ONE 8:e74039. doi: 10.1371/journal.pone.0074039
34. McCarthy, M., Turnbull, D. H., Walsh, C. A., and Fishell, G. (2001). Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J. Neurosci. 21, 6772-6781.
35. Miller, R. H., and Raff, M. C. (1984). Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct. J. Neurosci. 4, 585-592.
36. Miyata, T., Kawaguchi, A., Okano, H., and Ogawa, M. (2001). Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727-741. doi: 10.1016/S0896-6273(01)00420-2
37. Molofsky, A. V., Krenick, R., Ullian, E., Tsai, H. H., Deneen, B., Richardson, W. D., et al. (2012). Astrocytes and disease: a neurodevelopmental perspective. Genes Dev. 26, 891-907. doi: 10.1101/gad.188326.112
38. Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R. O., and Pearlman, A. L. (2001). Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 4, 143-150. doi: 10.1038/83967
39. Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., and Kriegstein, A. R. (2001). Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720. doi: 10.1038/35055553
40. Noctor, S. C., Martínez-Cerdeño, V., Ivic, L., and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144. doi: 10.1038/nn1172
41. Oberheim, N. A., Takano, T., Han, X., He, W., Lin, J. H. C., Wang, F., et al. (2009). Uniquely hominid features of adult human astrocytes. J. Neurosci. 29, 3276-3287. doi: 10.1523/JNEUROSCI.4707-08.2009
42. Ogata, K., and Kosaka, T. (2002). Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience 113, 221-233. doi: 10.1016/S0306-4522(02)00041-6
43. Oliet, S. H., Piet, R., and Poulain, D. A. (2001). Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292, 923-926. doi: 10.1126/science.1059162
44. Ono, K., Takebayashi, H., Ikeda, K., Furusho, M., Nishizawa, T., Watanabe, K., et al. (2008). Regional- and temporal-dependent changes in the differentiation of Olig2 progenitors in the forebrain, and the impact on astrocyte development in the dorsal pallium. Dev. Biol. 320, 456-468. doi: 10.1016/j.ydbio.2008.06.001
45. Parnavelas, J. G. (1999). Glial cell lineages in the rat cerebral cortex. Exp. Neurol. 156, 418-429. doi: 10.1006/exnr.1999.7044
46. Pfrieger, F. W. (2010). Role of glial cells in the formation and maintenance of synapses. Brain Res. Rev. 63, 39-46. doi: 10.1016/j.brainresrev.2009.11.002
47. Price, J., and Thurlow, L. (1988). Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development 104, 473-482.
48. Raff, M. C., Abney, E. R., Cohen, J., Lindsay, R., and Noble, M. (1983a). Two types of astrocytes in cultures of developing rat white matter: differences in morphology, surface gangliosides, and growth characteristics. J. Neurosci. 3, 1289-1300.
49. Raff, M. C., Miller, R. H., and Noble, M. (1983b). A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303, 390-396.
50. Richardson, W. D., Kessaris, N., and Pringle, N. (2006). Oligodendrocyte wars. Nat. Rev. Neurosci. 7, 11-18. doi: 10.1038/nrn1826
51. Rivers, L. E., Young, K. M., Rizzi, M., Jamen, F., Psachoulia, K., Wade, A., et al. (2008). PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci. 11, 1392-1401. doi: 10.1038/nn.2220
52. Rothstein, J. D., Dykes-Hoberg, M., Pardo, C. A., Bristol, L. A., Jin, L., Kuncl, R. W., et al. (1996). Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675-686.
53. Saito, T., and Nakatsuji, N. (2001). Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240, 237-246. doi: 10.1006/dbio.2001.0439
54. Sato, Y., Kasai, T., Nakagawa, S., Tanabe, K., Watanabe, T., Kawakami, K., et al. (2007). Stable integration and conditional expression of electroporated transgenes in chicken embryos. Dev. Biol. 305, 616-624. doi: 10.1016/j.ydbio.2007.01.043
55. Schmechel, D. E., and Rakic, P. (1979). A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat. Embryol. 156, 115-152.
56. Schnitzer, J., and Schachner, M. (1982). Cell type specificity of a neural cell surface antigen recognized by the monoclonal antibody A2B5. Cell Tissue Res. 224, 625-636. doi: 10.1007/BF00213757
57. Siddiqi, F., Chen, F., Aron, A. W., Fiondella, C. G., Patel, K., and LoTurco, J. J. (2014). Fate mapping by PiggyBac transposase reveals that neocortical GLAST+ progenitors generate more astrocytes than nestin+ progenitors in rat neocortex. Cereb. Cortex 24, 508-520. doi: 10.1093/cercor/bhs332.
58. Simard, M., Arcuino, G., Takano, T., Liu, Q. S., and Nedergaard, M. (2003). Signaling at the gliovascular interface. J. Neurosci. 23, 9254-9262.
59. Sloan, S. A., and Barres, B. A. (2014). Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders. Curr. Opin. Neurobiol. 27, 75-81. doi: 10.1016/j.conb.2014.03.005
60. Sosunov, A. A., Wu, X., Tsankova, N. M., Guilfoyle, E., McKhann, G. M., and Goldman, J. E. (2014). Phenotypic heterogeneity and plasticity of isocortical and hippocampal astrocytes in the human brain. J. Neurosci. 34, 2285-2298. doi: 10.1523/JNEUROSCI.4037-13.2014
61. Tabata, H., and 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, 865-872. doi: 10.1016/S0306-4522(01)00016-1
62. Takano, T., Tian, G.-F., Peng, W., Lou, N., Libionka, W., Han, X., et al. (2005). Astrocyte-mediated control of cerebral blood flow. Nat. Neurosci. 9, 260-267. doi: 10.1038/nn1623
63. Tsai, H.-H., Li, H., Fuentealba, L. C., Molofsky, A. V., Taveira-Marques, R., Zhuang, H., et al. (2012). Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337, 358-362. doi: 10.1126/science.1222381
64. Uwechue, N. M., Marx, M.-C., Chevy, Q., and Billups, B. (2012). Activation of glutamate transport evokes rapid glutamine release from perisynaptic astrocytes. J. Physiol. 590, 2317-2331. doi: 10.1113/jphysiol.2011.226605
65. Voigt, T. (1989). Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol. 289, 74-88. doi: 10.1002/cne.902890106
66. Windrem, M. S., Nunes, M. C., Rashbaum, W. K., Schwartz, T. H., Goodman, R. A., McKhann, G., et al. (2004). Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat. Med. 10, 93-97. doi: 10.1038/nm974
67. Windrem, M. S., Schanz, S. J., Guo, M., Tian, G.-F., Washco, V., Stanwood, N., et al. (2008). Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2, 553-565. doi: 10.1016/j.stem.2008.03.020
68. Windrem, M. S., Schanz, S. J., Morrow, C., Munir, J., Chandler-Militello, D., Wang, S., et al. (2014). A competitive advantage by neonatally engrafted human glial progenitors yields mice whose brains are chimeric for human glia. J. Neurosci. 34, 16153-16161. doi: 10.1523/JNEUROSCI.1510-14.2014
69. Yoshida, A., Yamaguchi, Y., Nonomura, K., Kawakami, K., Takahashi, Y., and Miura, M. (2010). Simultaneous expression of different transgenes in neurons and glia by combining in utero electroporation with the Tol2 transposon-mediated gene transfer system. Genes Cells 15, 501-512. doi: 10.1111/j.1365-2443.2010.01397.x
70. Zhu, X., Bergles, D. E., and Nishiyama, A. (2007). NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145-157. doi: 10.1242/dev.004895
71. Zhu, X., Zuo, H., Maher, B. J., Serwanski, D. R., LoTurco, J. J., Lu, Q. R., et al. (2012). Olig2-dependent developmental fate switch of NG2 cells. Development 139, 2299-2307. doi: 10.1242/dev.078873