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The evolution of Olig genes and their roles in myelination

  • Huiliang Li (a1) and William D. Richardson (a1)
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.

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Corresponding author
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
References
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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, 21112115.
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, 51725176.
Braddy, S.J., Poschmann, M. and Tetlie, O.E. (2008) Giant claw reveals the largest ever arthropod. Biology Letters 4, 106109.
Briscoe, J. and Ericson, J. (2001) Specification of neuronal fates in the ventral neural tube. Current Opinion in Neurobiology 11, 4349.
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, 485497.
Bullock, T.H., Moore, J.K. and Fields, R.D. (1984) Evolution of myelin sheaths: both lamprey and hagfish lack myelin. Neuroscience Letters 48, 145148.
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, 49304938.
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. 8598.
Davis, A.D., Weatherby, T.M., Hartline, D.K. and Lenz, P.H. (1999) Myelin-like sheaths in copepod axons. Nature 398, 571.
Dehal, P. and Boore, J.L. (2005) Two rounds of whole genome duplication in the ancestral vertebrate. Public Library of Science Biology 3, e314.
Donoghue, P.C., Graham, A. and Kelsh, R.N. (2008) The origin and evolution of the neural crest. Bioessays 30, 530541.
Feng, J.M. (2007) Minireview: expression and function of golli protein in immune system. Neurochemistry Research 32, 273278.
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, 43774382.
Forey, P. and Janvier, P. (1994) Evolution of the early vertebrates. American Scientist 82, 554565.
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, 513521.
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, 83118321.
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, 4966.
Halder, G., Callaerts, P. and Gehring, W.J. (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 17881792.
Hartline, D.K. and Colman, D.R. (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Current Biology 17, R29R35.
Janvier, P. (1996) The dawn of the vertebrates: characters versus common ascent in the rise of current vertebrate phylogenies. Paleontology 39, 259287.
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, 173179.
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, 73157327.
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, 282294.
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, 1437514382.
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, 1012410133.
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, 171194.
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.
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, 7586.
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, 317329.
Lynch, V.J. and Wagner, G.P. (2008) Resurrecting the role of transcription factor change in developmental evolution. Evolution 62, 21312154.
Morgenstern, B. and Atchley, W.R. (1999) Evolution of bHLH transcription factors: modular evolution by domain shuffling? Molecular Biology and Evolution 16, 16541663.
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, 356368.
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, 93669371.
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, 30373048.
Richardson, W.D., Kessaris, N. and Pringle, N. (2006) Oligodendrocyte wars. Nature Reviews Neuroscience 7, 1118.
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, 5868.
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, 136142.
Roots, B.I. (1993) The evolution of myelin. Advances in Neural Science 1, 187213.
Schweigreiter, R., Roots, B.I., Bandtlow, C.E. and Gould, R.M. (2006) Understanding myelination through studying its evolution. International Reviews of Neurobiology 73, 219273.
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, 295305.
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, 228239.
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, 11571163.
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, 169174.
Wagner, G.P. and Lynch, V.J. (2008) The gene regulatory logic of transcription factor evolution. Trends in Ecology and Evolution 23, 377385.
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, 583588.
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, 13541365.
Zalc, B. and Colman, D.R. (2000) Origins of vertebrate success. Science 288, 271272.
Zalc, B., Goujet, D. and Colman, D. (2008) The origin of the myelination program in vertebrates. Curent Biology 18, R511R512.
Zhou, Q. and Anderson, D.J. (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 6173.
Zhou, Q., Choi, G. and Anderson, D.J. (2001) The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31, 791807.
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, 331343.
Zimmer, C. (2000) Evolution. In search of vertebrate origins: beyond brain and bone. Science 287, 15761579.
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