DOI QR코드

DOI QR Code

Olig2 Transcription Factor in the Developing and Injured Forebrain; Cell Lineage and Glial Development

  • Ono, Katsuhiko (Department of Biology, Kyoto Prefectural University of Medicine) ;
  • Takebayashi, Hirohide (Division of Neurobiology and Bioinformatics, National Institute for Physiological Sciences) ;
  • Ikenaka, Kazuhiro (Division of Neurobiology and Bioinformatics, National Institute for Physiological Sciences)
  • Received : 2009.03.16
  • Accepted : 2009.03.19
  • Published : 2009.04.30

Abstract

Olig2 transcription factor is widely expressed throughout the central nervous system; therefore, it is considered to have multiple functions in the developing, mature and injured brain. In this mini-review, we focus on Olig2 in the forebrain (telencephalon and diencephalon) and discuss the functional significance of Olig2 and the differentiation properties of Olig2-expressing progenitors in the development and injured states. Short- and long-term lineage analysis in the developing forebrain elucidated that not all late Olig2+ cells are direct cohorts of early cells and that Olig2 lineage cells differentiate into neurons or glial cells in a region- and stage-dependent manner. Olig2-deficient mice revealed large elimination of oligodendrocyte precursor cells and a decreased number of astrocyte progenitors in the dorsal cortex, whereas no reduction in the number of GABAergic neurons. In addition to Olig2 function in the developing cortex, Olig2 is also reported to be important for glial scar formation after injury. Thus, Olig2 can be essential for glial differentiation during development and after injury.

Acknowledgement

Supported by : MEXT, JSPS

References

  1. Anderson, S.A., Eisenstat, D.D., Shi, L., and Rubenstein, J.L. (1997). Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474-476 https://doi.org/10.1126/science.278.5337.474
  2. Islam, M.S., Tatsumi, K., Okuda, H., Shiosaka, S., and Wanaka, A. (2009). Olig2-expressing progenitor cells preferentially differenttiate into oligodendrocytes in cuprizone-induced demyelinated lesions. Neurochem. Int. 54, 192-198 https://doi.org/10.1016/j.neuint.2008.10.011
  3. Levine, J.M., Reynolds, R., and Fawcett, J.W. (2001). The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 24, 39-47 https://doi.org/10.1016/S0166-2236(00)01691-X
  4. 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 https://doi.org/10.1016/0896-6273(93)90311-E
  5. 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 https://doi.org/10.1016/S0092-8674(02)00678-5
  6. Miyoshi, G., Gutt, S.J., Takebayashi, H., and Fishell, G. (2007). Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J. Neurosci. 27, 7786-7798 https://doi.org/10.1523/JNEUROSCI.1807-07.2007
  7. Park, H.C., Mehta, A., Richardson, J.S., and Appel, B. (2002). Olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev. Biol. 248, 356-368 https://doi.org/10.1006/dbio.2002.0738
  8. Petryniak, M.A., Potter, G.B., Rowitch, D.H., and Rubenstein, J.L.R. (2007). Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 55, 417-433 https://doi.org/10.1016/j.neuron.2007.06.036
  9. Rivers, L.E., Young, K.M., Rizzi, M., Jamen, F., Psachoulia, K., Wade, A., Kessaris, N., and Richardson, W.D. (2008). PDGFRa/NG2 glia generates myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci. 11, 1392-1401 https://doi.org/10.1038/nn.2220
  10. Takebayashi, H., Yoshida, S., Sugimori, M., Kosako, H., Kominami, R., Nakafuku, M., and Nabeshima, Y. (2000). Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech. Dev. 99, 143-148 https://doi.org/10.1016/S0925-4773(00)00466-4
  11. Takebayashi, H., Usui, N., Ono, K., and Ikenaka, K. (2008). Tamoxifen modulates apoptosis in multiple modes of action in CreER mice. Genesis 46, 775-781 https://doi.org/10.1002/dvg.20461
  12. Yue, T., Xian, K., Hurlock, E., Xin, M., Kernie, S.G., Parada, L.F., and Lu, Q.R. (2006). A critical role for dorsal progenitors in cortical myelination. J. Neurosci. 26, 1275-1280 https://doi.org/10.1523/JNEUROSCI.4717-05.2006
  13. Zhou, Q., Wang, S., and Anderson, D.J. (2000). Identification of a novel family of oligodendrocyte lineage-specific basic helix-loophelix transcription factors. Neuron 25, 331-343 https://doi.org/10.1016/S0896-6273(00)80898-3
  14. Marti, E., Takada, R., Bumcrot, D.A., Sasaki, H., and McMahon, A.P. (1995). Distribution of sonic hedgehog peptides in the developing chick and mouse embryo. Development 121, 2537-2547
  15. Parras, C.M., Hunt, C., Sugimori, M., Nakafuku, M., Rowitch, D.H., and Guillemot, F. (2007). The proneural gene Mash1 specifies and early population of telencephalic oligodendrocytes. J. Neurosci. 27, 4233-4242 https://doi.org/10.1523/JNEUROSCI.0126-07.2007
  16. Mukouyama, Y., Deneen, B., Lukaszewicz, A., Novitch, B.G., Wichterle, H., Jessell, T.M., and Anderson, D.J. (2006). Olig2+ neuroepithelial motoneuron progenitors are not multipotent stem cells in vivo. Proc. Natl. Acad. Sci. USA 103, 1551-1556 https://doi.org/10.1073/pnas.0510658103
  17. Naruse, M., Nakahira, E., Miyata, T., Hitoshi, S., Ikenaka, K., and Bansal, R. (2006). Induction of oligodendrocyte progenitors in dorsal forebrain by intraventricular microinjection of FGF-2. Dev. Biol. 297, 262-273 https://doi.org/10.1016/j.ydbio.2006.05.017
  18. Nery, S., Wichterle, H., and Fishell, G. (2001). Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128, 527-540
  19. Zhou, Q., and Anderson, D.J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61-73 https://doi.org/10.1016/S0092-8674(02)00677-3
  20. Ligon, K.L., Kesari, S., Kitada, M., Sun, T., Arnett, H.A., Alberta, J.A., Anderson, D.J., Stiles, C.D., and Rowitch, D.H. (2006). Development of G2 neural progenitor cells requires Olig gene function. Proc. Natl. Acad. Sci. USA 103, 7853-7858 https://doi.org/10.1073/pnas.0511001103
  21. Wu, S., Wu, Y., and Capecchi, M.R. (2006). Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development 133, 581-580 https://doi.org/10.1242/dev.02236
  22. Furusho, M., Ono, K., Takebayashi, H., Masahira, N., Kagawa, T., Ikeda, K., and Ikenaka K. (2006). Involvement of the Olig2 tran scription factor in cholinergic neuron development of the basal forebrain. Dev. Biol. 293, 348-357 https://doi.org/10.1016/j.ydbio.2006.01.031
  23. Ivanova, A., Nakahira, E., Kagawa, T., Oba, A.,, Wada, T., Takebayashi, H., Spassky, N., Levine, J., Zalc, B., and Ikenaka, K. (2003). Evidence for a second wave of oligodendrogenesis in the postnatal cerebral cortex of the mouse. J. Neurosci. Res. 73, 581-592 https://doi.org/10.1002/jnr.10717
  24. Tatsumi, K., Takebayashi, H., Manabe, T., Tanaka, K.F., Makinodan, M., Yamauchi, T., Makinodan, E., Matsuyoshi, H., Okuda, H., Ikenaka K., et al. (2008). Genetic fate mapping of Olig2 progenitors in the injured adult cerebral cortex reveals preferential differentiation into astrocyte. J. Neurosci. Res. 86, 3494-3502 https://doi.org/10.1002/jnr.21862
  25. Marshall, C.A., Novitch, B.G., and Goldman, J.E. (2005). Olig2 directs astrocyte and oligodendrocyte formation in postnatal subVZ cells. J. Neurosci. 25, 7289-7298 https://doi.org/10.1523/JNEUROSCI.1924-05.2005
  26. Lytle, J.M., Chittajallu, R., Wrathall, J.R., and Gallo, V. (2009). NG2 cell response in the CNP-EGFP mouse after contusive spinal cord injury. Glia 57, 270-825 https://doi.org/10.1002/glia.20755
  27. 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 https://doi.org/10.1242/dev.02847
  28. Ligon, K.L., Huillard, E., Mehta, S., Kesari, S., Liu, H., Alberta, J.A., Bachoo, R.M., Kane, M., Louis, D.N., DePinho, R.A., et al. (2007). Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 53, 503-517 https://doi.org/10.1016/j.neuron.2007.01.009
  29. Zhu, X., Bergles, D.E., and Nishiyama, A. (2008). NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145-157 https://doi.org/10.1242/dev.004895
  30. Takebayashi, H., Nabeshima, Y., Yoshida, S., Chisaka, O., Ikenaka, K., and Nabeshima, Y. (2002). The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr. Biol. 12, 1157-1163 https://doi.org/10.1016/S0960-9822(02)00926-0
  31. Ono, K., Takebayashi, H., Ikeda, K., Furusho, M., Nishizawa, T., Watanabe, K., and Ikenaka, K. (2008). Spacio-temporal 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 https://doi.org/10.1016/j.ydbio.2008.06.001
  32. Tan, A.M., Zhang, W., and Levine, J.M. (2005). NG2: a component of the glial scar that inhibits axon growth. J. Anat. 207, 717-725 https://doi.org/10.1111/j.1469-7580.2005.00452.x
  33. Xin, M., Yue, T., Ma, Z., Wi, F.F., Gow, A., and Lu, Q.R. (2005). Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. J. Neurosci. 25, 1354-1365 https://doi.org/10.1523/JNEUROSCI.3034-04.2005
  34. Fogarty, M., Grist, M., Gelman, D., Marin, O., Pachnis, V., and Kessaris, N. (2007). Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27, 10935-10946 https://doi.org/10.1523/JNEUROSCI.1629-07.2007
  35. Lu, Q.R., Yuk, D., Alberta, J.A., Zhu, Z., Pawlitzky, I., Chan, J., McMahon, A.P., Stiles, C.D., and Rowitch, D.H. (2000). Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317-329 https://doi.org/10.1016/S0896-6273(00)80897-1
  36. Nishiyama, A., Komitova, M., Suzuki, R., and Zhu, X. (2008). Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10, 9-22 https://doi.org/10.1038/nrn2495
  37. 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 https://doi.org/10.1038/nn1620
  38. Olsson, M., Bjorklund, A., and Campbell, K. (1998). Early specification of striatal projection neurons and interneuronal subtypes in the lateral and medial ganglionic eminence. Neuroscience 84, 867-876 https://doi.org/10.1016/S0306-4522(97)00532-0
  39. Vue, T.Y., Aaker, J., Taniguchi, A., Kazemzadeh, C., Skidmore, J.M., Martin, D.M., Martin, J.F., Treier, M., and Nakagawa, Y. (2007). Characterization of progenitor domains in the developing mouse thalamus. J. Comp. Neurol. 505, 73-91 https://doi.org/10.1002/cne.21467
  40. Tekki-Kessaris, N., Woodruff, R., Hall, A.C., Gaffield, W., Kimura, S., Stiles, C.D., and Rowitch, D.H. (2001). Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 128, 2545-2554
  41. Masahira, N., Takebayashi, H., Ono, K., Watanabe, K., Ding, L., Furusho, M., Ogawa, Y., Nabeshima, Y., Alvarez-Buylla, A., Shimizu, K., et al. (2006). Olig2-positive progenitors in the embryonic spinal cord give rise not only to motoneurons and oligodendrocytes, but also to a subset of astrocytes and ependymal cells. Dev. Biol. 293, 358-269 https://doi.org/10.1016/j.ydbio.2006.02.029
  42. Dimou, L., Simon, C., Kirchhoff, F., Takebayashi, H., and Gotz, M. (2008). Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J. Neurosci. 28, 10434-10442 https://doi.org/10.1523/JNEUROSCI.2831-08.2008
  43. Chen, Y., Miles, D.K., Hoang, T.-N., Shi, J., Hurlock, E., Kernie, S., and Lu, Q.R. (2008). The basic helix-loop-helix transcription factor Olig2 is critical for reactive astrocyte proliferation after cortical injury. J. Neurosci. 28, 10983-10989 https://doi.org/10.1523/JNEUROSCI.3545-08.2008
  44. Nakahira, E., Kagawa, T., Shimizu, T., Goulding, M.D., and Ikenaka, K. (2006). Direct evidence that ventral forebrain cells migrate to the cortex and contribute to the generation of cortical myelinating oligodendrocytes. Dev. Biol. 291, 123-131 https://doi.org/10.1016/j.ydbio.2005.12.010
  45. Buffo, A., Vosko, M.R., Erturk, D., Hamann, G.F., Jucker, M., Rowitch, D., and Gotz, M. (2005). Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc. Natl. Acad. Sci. USA 102, 18183-18188 https://doi.org/10.1073/pnas.0506535102