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The Journal of Neuroscience, September 20, 2006, 26(38):9722-9735; doi:10.1523/JNEUROSCI.1716-06.2006

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Development/Plasticity/Repair
Identification of Sox17 as a Transcription Factor That Regulates Oligodendrocyte Development

Jiho Sohn,^1,3 * JoAnne Natale,^1,2 * Li-Jin Chew,¹ Shibeshih Belachew,⁴ Ying Cheng,² Adan Aguirre,¹ Judith Lytle,^1,5 Brahim Nait-Oumesmar,⁶ Christophe Kerninon,⁶ Masami Kanai-Azuma,⁷ Yoshiakira Kanai,⁷ and Vittorio Gallo¹

Centers for ¹Neuroscience Research and ²Genetic Medicine, Children's National Medical Center, Washington, DC 20010, ³Institute of Biomedical Sciences, Neuroscience Program, George Washington University, Washington, DC 20052, ⁴Center for Cellular and Molecular Neurobiology, University of Liège, 4000 Liège, Belgium, ⁵Department of Neuroscience, Georgetown University Medical School, Washington, DC 20057, ⁶Institut National de la Santé et de la Recherche Médicale, Unité Mixte de Recherche 546 and Université Pierre et Marie Curie, F-75634 Paris, France, and ⁷Department of Veterinary Anatomy, The University of Tokyo, Tokyo 113-8657, Japan

Correspondence should be addressed to Dr. Vittorio Gallo, Center for Neuroscience Research, Children's National Medical Center, 111 Michigan Avenue NW, Washington, DC 20010. Email: vgallo{at}cnmcresearch.org

Microarray analysis of oligodendrocyte lineage cells purified by fluorescence-activated cell sorting (FACS) from 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNP)–enhanced green fluorescent protein (EGFP) transgenic mice revealed Sox17 (SRY-box containing gene 17) gene expression to be coordinately regulated with that of four myelin genes during postnatal development. In CNP–EGFP-positive (CNP–EGFP⁺) cells, Sox17 mRNA and protein levels transiently increased between postnatal days 2 and 15, with white matter O4⁺ preoligodendrocytes expressing greater Sox17 levels than Nkx2.2⁺ (NK2 transcription factor related, locus 2) NG2⁺, or GalC⁺ (galactocerebroside) cells. In spinal cord, Sox17 protein expression was undetectable in the primary motor neuron domain between embryonic days 12.5 and 15.5 but was evident in Nkx2.2⁺ and CC1⁺ cells. In cultured oligodendrocyte progenitor cells (OPCs), Sox17 levels were maximal in O4⁺ cells and peaked during the phenotypic conversion from bipolar to multipolar. Parallel increases in Sox17 and p27 occurred before MBP protein expression, and Sox17 upregulation was prevented by conditions inhibiting differentiation. Sox17 downregulation with small interfering RNAs increased OPC proliferation and decreased lineage progression after mitogen withdrawal, whereas Sox17 overexpression in the presence of mitogen had opposite effects. Sox17 overexpression enhanced myelin gene expression in OPCs and directly stimulated MBP gene promoter activity. These findings support important roles for Sox17 in controlling both oligodendrocyte progenitor cell cycle exit and differentiation.

Key words: gene profiling; cell lineage; CNP–EGFP mouse; cell cycle; myelin genes; cell differentiation

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Received Nov. 21, 2005; revised Aug. 4, 2006; accepted Aug. 4, 2006.

Correspondence should be addressed to Dr. Vittorio Gallo, Center for Neuroscience Research, Children's National Medical Center, 111 Michigan Avenue NW, Washington, DC 20010. Email: vgallo{at}cnmcresearch.org

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