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The evolution of Olig genes and their roles in myelination

Published online by Cambridge University Press:  08 September 2009

Huiliang Li  and
William D. Richardson
Huiliang Li
Affiliation:
Wolfson Institute for Biomedical Research and Research, Department of Cell and Developmental Biology, University College London, London, UK
William D. Richardson*
Affiliation:
Wolfson Institute for Biomedical Research and Research, Department of Cell and Developmental Biology, University College London, London, UK
*
Correspondence should be addressed to: William D. Richardson, Wolfson Institute for Biomedical Research, University College London, Gower Street, London WC1E 6BT, UK phone: +44 (0)20 7679 6729 fax: +44 (0)20 7209 0470 email: w.richardson@ucl.ac.uk
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Abstract

One of the special attributes of vertebrates is their myelinated nervous system. By increasing the conduction velocity of axons, myelin allows for increased body size, rapid movement and a large and complex brain. In the central nervous system (CNS), oligodendrocytes (OLs) are the myelin-forming cells. The transcription factors OLIG1 and OLIG2, master regulators of OL development, presumably also played a seminal role during the evolution of the genetic programme leading to myelination in the CNS. From the available ontogenetic and phylogenetic data we attempt to reconstruct the evolutionary events that led to the emergence of the Olig gene family and speculate about the links between Olig genes, their specific cis-regulatory elements and myelin evolution. In addition, we report a putative myelin basic protein (MBP) ancestor in the lancelet Branchiostoma floridae, which lacks compact myelin. The lancelet ‘Mbp’ gene lacks the OLIG1/2- and SOX10-binding sites that characterize vertebrate Mbp homologs, raising the possibility that insertion of cis-regulatory elements might have been involved in evolution of the myelinating programme.

Keywords

MyelinOlig genesevolution and development (evo-devo)behaviourmyelin basic protein
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 2 , May 2008 , pp. 129 - 135
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Arnett, H.A., Fancy, S.P., Alberta, J.A., Zhao, C., Plant, S.R., Kaing, S. et al. (2004) bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science 306, 2111–2115.CrossRefGoogle ScholarPubMed
Atchley, W.R. and Fitch, W.M. (1997) A natural classification of the basic helix-loop-helix class of transcription factors. Proceedings of the National Academy of Sciences of the U.S.A. 94, 5172–5176.CrossRefGoogle ScholarPubMed
Braddy, S.J., Poschmann, M. and Tetlie, O.E. (2008) Giant claw reveals the largest ever arthropod. Biology Letters 4, 106–109.CrossRefGoogle ScholarPubMed
Briscoe, J. and Ericson, J. (2001) Specification of neuronal fates in the ventral neural tube. Current Opinion in Neurobiology 11, 43–49.CrossRefGoogle ScholarPubMed
Bronchain, O.J., Pollet, N., Ymlahi-Ouazzani, Q., Dhorne-Pollet, S., Helbling, J.C., Lecarpentier, J.E. et al. (2007) The Olig family: phylogenetic analysis and early gene expression in Xenopus tropicalis. Development, Genes and Evolution 217, 485–497.CrossRefGoogle ScholarPubMed
Bullock, T.H., Moore, J.K. and Fields, R.D. (1984) Evolution of myelin sheaths: both lamprey and hagfish lack myelin. Neuroscience Letters 48, 145–148.CrossRefGoogle ScholarPubMed
Campagnoni, A.T., Pribyl, T.M., Campagnoni, C.W., Kampf, K., mur-Umarjee, S., Landry, C.F. et al. (1993) Structure and developmental regulation of Golli-mbp, a 105-kilobase gene that encompasses the myelin basic protein gene and is expressed in cells in the oligodendrocyte lineage in the brain. Journal of Biological Chemistry 268, 4930–4938.CrossRefGoogle ScholarPubMed
Colman, D., Doyle, J.P., D'Urso, D., Kitagawa, K., Pedraza, M., Yoshida, M. and Fannon, A.M. (1996) Speculations on myelin sheath evolution. In Jessen, K.R. and Richardson, W.D. (eds) Glial Cell Development. BIOS Scientific Publishers Ltd., pp. 85–98.Google Scholar
Davis, A.D., Weatherby, T.M., Hartline, D.K. and Lenz, P.H. (1999) Myelin-like sheaths in copepod axons. Nature 398, 571.CrossRefGoogle ScholarPubMed
Dehal, P. and Boore, J.L. (2005) Two rounds of whole genome duplication in the ancestral vertebrate. Public Library of Science Biology 3, e314.Google ScholarPubMed
Donoghue, P.C., Graham, A. and Kelsh, R.N. (2008) The origin and evolution of the neural crest. Bioessays 30, 530–541.CrossRefGoogle ScholarPubMed
Feng, J.M. (2007) Minireview: expression and function of golli protein in immune system. Neurochemistry Research 32, 273–278.CrossRefGoogle ScholarPubMed
Filippi, A., Tiso, N., Deflorian, G., Zecchin, E., Bortolussi, M. and Argenton, F. (2005) The basic helix-loop-helix olig3 establishes the neural plate boundary of the trunk and is necessary for development of the dorsal spinal cord. Proceedings of the National Academy of Sciences of the U.S.A. 102, 4377–4382.CrossRefGoogle ScholarPubMed
Forey, P. and Janvier, P. (1994) Evolution of the early vertebrates. American Scientist 82, 554–565.Google Scholar
Fors, L., Hood, L. and Saavedra, R.A. (1993) Sequence similarities of myelin basic protein promoters from mouse and shark: implications for the control of gene expression in myelinating cells. Journal of Neurochemistry 60, 513–521.CrossRefGoogle ScholarPubMed
Gokhan, S., Marin-Husstege, M., Yung, S.Y., Fontanez, D., Casaccia-Bonnefil, P. and Mehler, M.F. (2005) Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression. Journal of Neuroscience 25, 8311–8321.CrossRefGoogle ScholarPubMed
Gould, R.M., Morrison, H.G., Gilland, E. and Campbell, R.K. (2005) Myelin tetraspan family proteins but no non-tetraspan family proteins are present in the ascidian (Ciona intestinalis) genome. Biological Bulletin 209, 49–66.CrossRefGoogle ScholarPubMed
Halder, G., Callaerts, P. and Gehring, W.J. (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 1788–1792.CrossRefGoogle ScholarPubMed
Hartline, D.K. and Colman, D.R. (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Current Biology 17, R29–R35.CrossRefGoogle ScholarPubMed
Janvier, P. (1996) The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies. Paleontology 39, 259–287.Google Scholar
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. Nature Neuroscience 9, 173–179.CrossRefGoogle ScholarPubMed
Landry, C.F., Pribyl, T.M., Ellison, J.A., Givogri, M.I., Kampf, K., Campagnoni, C.W. et al. (1998) Embryonic expression of the myelin basic protein gene: identification of a promoter region that targets transgene expression to pioneer neurons. Journal of Neuroscience 18, 7315–7327.CrossRefGoogle ScholarPubMed
Lee, S.K., Lee, B., Ruiz, E.C. and Pfaff, S.L. (2005) Olig2 and Ngn2 function in opposition to modulate gene expression in motor neuron progenitor cells. Genes and Development 19, 282–294.CrossRefGoogle ScholarPubMed
Li, H., Lu, Y., Smith, H.K. and Richardson, W.D. (2007) Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. Journal of Neuroscience 27, 14375–14382.CrossRefGoogle ScholarPubMed
Liu, Z., Li, H., Hu, X., Yu, L., Liu, H., Han, R. et al. (2008) Control of precerebellar neuron development by Olig3 bHLH transcription factor. Journal of Neuroscience 28, 10124–10133.CrossRefGoogle ScholarPubMed
Lowe, C.J., Tagawa, K., Humphreys, T., Kirschner, M. and Gerhart, J. (2004) Hemichordate embryos: procurement, culture, and basic methods. Methods in Cell Biology 74, 171–194.CrossRefGoogle ScholarPubMed
Lowe, C.J., Terasaki, M., Wu, M., Freeman, R.M. Jr., Runft, L., Kwan, K. et al. (2006) Dorsoventral patterning in hemichordates: insights into early chordate evolution. Public Library of Science Biology 4, e291.Google ScholarPubMed
Lu, Q.R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C.D. et al. (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109, 75–86.CrossRefGoogle ScholarPubMed
Lu, Q.R., Yuk, D., Alberta, J.A., Zhu, Z., Pawlitzky, I., Chan, J. et al. (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317–329.CrossRefGoogle ScholarPubMed
Lynch, V.J. and Wagner, G.P. (2008) Resurrecting the role of transcription factor change in developmental evolution. Evolution 62, 2131–2154.CrossRefGoogle ScholarPubMed
Morgenstern, B. and Atchley, W.R. (1999) Evolution of bHLH transcription factors: modular evolution by domain shuffling? Molecular Biology and Evolution 16, 1654–1663.CrossRefGoogle ScholarPubMed
Park, H.C., Mehta, A., Richardson, J.S. and Appel, B. (2002) olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Developmental Biology 248, 356–368.CrossRefGoogle ScholarPubMed
Park, M., Lewis, C., Turbay, D., Chung, A., Chen, J.N., Evans, S. et al. (1998) Differential rescue of visceral and cardiac defects in Drosophila by vertebrate tinman-related genes. Proceedings of the National Academy of Sciences of the U.S.A. 95, 9366–9371.CrossRefGoogle ScholarPubMed
Ranganayakulu, G., Elliott, D.A., Harvey, R.P. and Olson, E.N. (1998) Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development 125, 3037–3048.CrossRefGoogle ScholarPubMed
Richardson, W.D., Kessaris, N. and Pringle, N. (2006) Oligodendrocyte wars. Nature Reviews Neuroscience 7, 11–18.CrossRefGoogle ScholarPubMed
Richardson, W.D., Pringle, N.P., Yu, W.P. and Hall, A.C. (1997) Origins of spinal cord oligodendrocytes: possible developmental and evolutionary relationships with motor neurons. Developmental Neuroscience 19, 58–68.CrossRefGoogle ScholarPubMed
Richardson, W.D., Smith, H.K., Sun, T., Pringle, N.P., Hall, A. and Woodruff, R. (2000) Oligodendrocyte lineage and the motor neuron connection. Glia 29, 136–142.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Roots, B.I. (1993) The evolution of myelin. Advances in Neural Science 1, 187–213.Google Scholar
Schweigreiter, R., Roots, B.I., Bandtlow, C.E. and Gould, R.M. (2006) Understanding myelination through studying its evolution. International Reviews of Neurobiology 73, 219–273.CrossRefGoogle ScholarPubMed
Storm, R., Cholewa-Waclaw, J., Reuter, K., Brohl, D., Sieber, M., Treier, M. et al. (2009) The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei. Development 136, 295–305.CrossRefGoogle ScholarPubMed
Sun, T., Pringle, N.P., Hardy, A.P., Richardson, W.D. and Smith, H.K. (1998) Pax6 influences the time and site of origin of glial precursors in the ventral neural tube. Molecular and Cellular Neuroscience 12, 228–239.CrossRefGoogle ScholarPubMed
Takebayashi, H., Nabeshima, Y., Yoshida, S., Chisaka, O., Ikenaka, K. and Nabeshima, Y. (2002a) The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Current Biology 12, 1157–1163.CrossRefGoogle ScholarPubMed
Takebayashi, H., Ohtsuki, T., Uchida, T., Kawamoto, S., Okubo, K., Ikenaka, K. et al. (2002b) Non-overlapping expression of Olig3 and Olig2 in the embryonic neural tube. Mechanisms of Development 113, 169–174.CrossRefGoogle ScholarPubMed
Wagner, G.P. and Lynch, V.J. (2008) The gene regulatory logic of transcription factor evolution. Trends in Ecology and Evolution 23, 377–385.CrossRefGoogle ScholarPubMed
Wegner, M. and Stolt, C.C. (2005) From stem cells to neurons and glia: a Soxist's view of neural development. Trends in Neurosciences 28, 583–588.CrossRefGoogle Scholar
Xin, M., Yue, T., Ma, Z., Wu, F.F., Gow, A. and Lu, Q.R. (2005) Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. Journal of Neuroscience 25, 1354–1365.CrossRefGoogle ScholarPubMed
Zalc, B. and Colman, D.R. (2000) Origins of vertebrate success. Science 288, 271–272.CrossRefGoogle ScholarPubMed
Zalc, B., Goujet, D. and Colman, D. (2008) The origin of the myelination program in vertebrates. Curent Biology 18, R511–R512.CrossRefGoogle ScholarPubMed
Zhou, Q. and Anderson, D.J. (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61–73.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Zimmer, C. (2000) Evolution. In search of vertebrate origins: beyond brain and bone. Science 287, 1576–1579.CrossRefGoogle ScholarPubMed

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