Ascl1 controls the number and distribution of astrocytes and oligodendrocytes in the gray matter and white matter of the spinal cord

Development (Cambridge)

Volumn 141, Issue 19, 2014, Pages 3721-3731

  Vue, Tou Yia ^a   Parras, Carlos M ^b,d   Guillemot, Francois ^b   Johnson, Jane E ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

Author keywords

Astrocyte heterogeneity; Glial specification; Oligodendrogenesis; Spinal cord gliogenesis

Indexed keywords

TRANSCRIPTION FACTOR MASH1; ASCL1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL COUNT; CELL LINEAGE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; GLIA CELL; GRAY MATTER; MOUSE; NONHUMAN; OLIGODENDROGLIA; PROTEIN EXPRESSION; SPINAL CORD; STEM CELL; WHITE MATTER; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; EMBRYOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; PHYSIOLOGY;

ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINEAGE; FLUORESCENT ANTIBODY TECHNIQUE; MICE; OLIGODENDROGLIA; SPINAL CORD;

EID: 84908099276     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.105270     Document Type: Article

References (51)

1. Bachoo, R. M., Kim, R. S., Ligon, K. L., Maher, E. A., Brennan, C., Billings, N., Chan, S., Li, C., Rowitch, D. H., Wong, W. H. et al. (2004). Molecular diversity of astrocytes with implications for neurological disorders. Proc. Natl. Acad. Sci. USA 101, 8384-8389.
2. Battiste, J., Helms, A. W., Kim, E. J., Savage, T. K., Lagace, D. C., Mandyam, C. D., Eisch, A. J., Miyoshi, G. and Johnson, J. E. (2007). Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 134, 285-293.
3. Borromeo, M. D., Meredith, D. M., Castro, D. S., Chang, J. C., Tung, K.-C., Guillemot, F. and Johnson, J. E. (2014). A transcription factor network specifying inhibitory versus excitatory neurons in the dorsal spinal cord. Development 141, 2803-2812, 3102.
4. Cai, J., Chen, Y., Cai, W.-H., Hurlock, E. C., Wu, H., Kernie, S. G., Parada, L. F. and Lu, Q. R. (2007). A crucial role for Olig2 in white matter astrocyte development. Development 134, 1887-1899.
5. Castro, D. S., Martynoga, B., Parras, C., Ramesh, V., Pacary, E., Johnston, C., Drechsel, D., Lebel-Potter, M., Garcia, L. G., Hunt, C. et al. (2011). A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev. 25, 930-945.
6. Deneen, B., Ho, R., Lukaszewicz, A., Hochstim, C. J., Gronostajski, R. M. and Anderson, D. J. (2006). The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52, 953-968.
7. Fogarty, M., Richardson, W. D. and Kessaris, N. (2005). A subset of oligodendrocytes generated from radial glia in the dorsal spinal cord. Development 132, 1951-1959.
8. Garcia-Marques, J. and Lopez-Mascaraque, L. (2013). Clonal identity determines astrocyte cortical heterogeneity. Cereb. Cortex 23, 1463-1472.
9. 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.
10. Guillemot, F., Lo, L.-C., Johnson, J. E., Auerbach, A., Anderson, D. J. and Joyner, A. L. (1993). Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476.
11. Haas, B., Schipke, C. G., Peters, O., Söhl, G., Willecke, K. and Kettenmann, H. (2006). Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb. Cortex 16, 237-246.
12. Helms, A. W., Battiste, J., Henke, R. M., Nakada, Y., Simplicio, N., Guillemot, F. and Johnson, J. E. (2005). Sequential roles for Mash1 and Ngn2 in the generation of dorsal spinal cord interneurons. Development 132, 2709-2719.
13. Hill, R. A., Patel, K. D., Medved, J., Reiss, A. M. and Nishiyama, A. (2013). NG2 cells in white matter but not gray matter proliferate in response to PDGF. J. Neurosci. 33, 14558-14566.
14. Hochstim, C., Deneen, B., Lukaszewicz, A., Zhou, Q. and Anderson, D. J. (2008). Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 133, 510-522.
15. Hoffmann, S. A., Hos, D., Kuspert, M., Lang, R. A., Lovell-Badge, R., Wegner, M. and Reiprich, S. (2014). Stem cell factor Sox2 and its close relative Sox3 have differentiation functions in oligodendrocytes. Development 141, 39-50.
16. Horton, S., Meredith, A., Richardson, J. A. and Johnson, J. E. (1999). Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor MASH1. Mol. Cell. Neurosci. 14, 355-369.
17. Jacob, J., Kong, J., Moore, S., Milton, C., Sasai, N., Gonzalez-Quevedo, R., Terriente, J., Imayoshi, I., Kageyama, R., Wilkinson, D. G. et al. (2013). Retinoid acid specifies neuronal identity through graded expression of Ascl1. Curr. Biol. 23, 412-418.
18. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
19. Kang, P., Lee, H. K., Glasgow, S. M., Finley, M., Donti, T., Gaber, Z. B., Graham, B. H., Foster, A. E., Novitch, B. G., Gronostajski, R.M. et al. (2012). Sox9 and NFIA coordinate a transcriptional regulatory cascade during the initiation of gliogenesis. Neuron 74, 79-94.
20. Kim, E. J., Leung, C. T., Reed, R. R. and Johnson, J. E. (2007). In vivo analysis of Ascl1 defined progenitors reveals distinct developmental dynamics during adult neurogenesis and gliogenesis. J. Neurosci. 27, 12764-12774.
21. Kim, E. J., Battiste, J., Nakagawa, Y. and Johnson, J. E. (2008). Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol. Cell. Neurosci. 38, 595-606.
22. Kim, E. J., Ables, J. L., Dickel, L. K., Eisch, A. J. and Johnson, J. E. (2011). Ascl1 (Mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS ONE 6, e18472.
23. Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C. D. and Rowitch, D. H. (2002). Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75-86.
24. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R. et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140.
25. Mizuguchi, R., Kriks, S., Cordes, R., Gossler, A., Ma, Q. and Goulding, M. (2006). Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat. Neurosci. 9, 770-778.
26. Molofsky, A. V., Krenick, R., Ullian, E., Tsai, H.-H., Deneen, B., Richardson, W. D., Barres, B. A. and Rowitch, D. H. (2012). Astrocytes and disease: a neurodevelopmental perspective. Genes Dev. 26, 891-907.
27. Muroyama, Y., Fujiwara, Y., Orkin, S. H. and Rowitch, D. H. (2005). Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature 438, 360-363.
28. Nakatani, H., Martin, E., Hassani, H., Clavairoly, A., Maire, C. L., Viadieu, A., Kerninon, C., Delmasure, A., Frah, M., Weber, M. et al. (2013). Ascl1/Mash1 Promotes Brain Oligodendrogenesis during Myelination and Remyelination. J. Neurosci. 33, 9752-9768.
29. Nishiyama, A., Komitova, M., Suzuki, R. and Zhu, X. (2009). Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10, 9-22.
30. Oberheim, N. A., Goldman, S. A. and Nedergaard, M. (2012). Heterogeneity of astrocytic form and function. Methods Mol. Biol. 814, 23-45.
31. Pacary, E., Heng, J., Azzarelli, R., Riou, P., Castro, D., Lebel-Potter, M., Parras, C., Bell, D. M., Ridley, A. J., Parsons, M. et al. (2011). Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signaling. Neuron 69, 1069-1084.
32. Parras, C. M., Galli, R., Britz, O., Soares, S., Galichet, C., Battiste, J., Johnson, J. E., Nakafuku, M., Vescovi, A. and Guillemot, F. (2004). Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23, 4495-4505.
33. Parras, C. M., Hunt, C., Sugimori, M., Nakafuku, M., Rowitch, D. and Guillemot, F. (2007). The proneural gene Mash1 specifies an early population of telencephalic oligodendrocytes. J. Neurosci. 27, 4233-4242.
34. Pringle, N. P., Yu, W.-P., Howell, M., Colvin, J. S., Ornitz, D. M. and Richardson, W. D. (2003). Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 130, 93-102.
35. Rowitch, D. H. (2004). Glial specification in the vertebrate neural tube. Nat. Rev. Neurosci. 5, 409-419.
36. Rowitch, D. H. and Kriegstein, A. R. (2010). Developmental genetics of vertebrate glial-cell specification. Nature 468, 214-222.
37. Sephton, C. F., Good, S. K., Atkin, S., Dewey, C. M., Mayer, P., Herz, J. and Yu, G. (2010). TDP-43 is a developmentally regulated protein essential for early embryonic development. J. Biol. Chem. 285, 6826-6834.
38. Sudarov, A., Turnbull, R. K., Kim, E. J., Lebel-Potter, M., Guillemot, F. and Joyner, A. L. (2011). Ascl1 genetics reveals insights into cerebellum local circuit assembly. J. Neurosci. 31, 11055-11069.
39. Sugimori, M., Nagao, M., Bertrand, N., Parras, C. M., Guillemot, F. and Nakafuku, M. (2007). Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 134, 1617-1629.
40. Sugimori, M., Nagao, M., Parras, C. M., Nakatani, H., Lebel, M., Guillemot, F. and Nakafuku, M. (2008). Ascl1 is required for oligodendrocyte development in the spinal cord. Development 135, 1271-1281.
41. Tien, A.-C., Tsai, H.-H., Molofsky, A. V., McMahon, M., Foo, L. C., Kaul, A., Dougherty, J. D., Heintz, N., Gutmann, D. H., Barres, B. A. et al. (2012). Regulated temporal-spatial astrocyte precursor cell proliferation involves BRAF signalling in mammalian spinal cord. Development 139, 2477-2487.
42. Torii, M., Matsuzaki, F., Osumi, N., Kaibuchi, K., Nakamura, S., Casarosa, S., Guillemot, F. and Nakafuku, M. (1999). Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development 126, 443-456.
43. Tsai, H.-H., Li, H., Fuentealba, L. C., Molofsky, A. V., Taveira-Marques, R., Zhuang, H., Tenney, A., Murnen, A. T., Fancy, S. P. J., Merkle, F. et al. (2012). Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337, 358-362.
44. Viganò, F., Möbius, W., Götz, M. and Dimou, L. (2013). Transplantation reveals regional differences in oligodendrocyte differentiation in the adult brain. Nat. Neurosci. 16, 1370-1372.
45. Walther, E. U., Dichgans, M., Maricich, S.M., Romito, R.R., Yang, F., Dziennis, S., Zackson, S., Hawkes, R. and Herrup, K. (1998). Genomic sequences of aldolase C (Zebrin II) direct lacZ expression exclusively in non-neuronal cells of transgenic mice. Proc. Natl. Acad. Sci. USA 95, 2615-2620.
46. Wichterle, H., Lieberam, I., Porter, J. A. and Jessell, T. M. (2002). Directed differentiation of embryonic stem cells into motor neurons. Cell 110, 385-397.
47. Wildner, H., Müller, T., Cho, S.-H., Bröhl, D., Cepko, C. L., Guillemot, F. and Birchmeier, C. (2006). dILA neurons in the dorsal spinal cord are the product of terminal and non-terminal asymmetric progenitor cell divisions, and require Mash1 for their development. Development 133, 2105-2113.
48. Zhou, Q. and Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73.
49. Zhou, Q., Wang, S. and Anderson, D. J. (2000). Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331-343.
50. Zhou, Q., Choi, G. and Anderson, D. J. (2001). The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31, 791-807.
51. Zhu, Q., Whittemore, S. R., Devries, W. H., Zhao, X., Kuypers, N. J. and Qiu, M. (2011). Dorsally-derived oligodendrocytes in the spinal cord contribute to axonal myelination during development and remyelination following focal demyelination. Glia 59, 1612-1621.