HDAC1 and HDAC2 control the specification of neural crest cells into peripheral glia

Claire Jacob, Pirmin Lötscher, Stefanie Engler, Arianna Baggiolini, Sandra Varum Tavares, Valérie Brügger, Nessy John, Stine Büchmann-Møller, Paige L. Snider, Simon Conway, Teppei Yamaguchi, Patrick Matthias, Lukas Sommer, Ned Mantei, Ueli Suter

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

Schwann cells, the myelinating glia of the peripheral nervous system (PNS), originate from multipotent neural crest cells that also give rise to other cells, including neurons, melanocytes, chondrocytes, and smooth muscle cells. The transcription factor Sox10 is required for peripheral glia specification. However, all neural crest cells express Sox10 and the mechanisms directing neural crest cells into a specific lineage are poorly understood. We show here that histone deacetylases 1 and 2 (HDAC1/2) are essential for the specification of neural crest cells into Schwann cell precursors and satellite glia, which express the early determinants of their lineage myelin protein zero (P0) and/or fatty acid binding protein 7 (Fabp7). In neural crest cells, HDAC1/2 induced expression of the transcription factor Pax3 by binding and activating the Pax3 promoter. In turn, Pax3 was required to maintain high Sox10 levels and to trigger expression of Fabp7. In addition, HDAC1/2 were bound to the P0 promoter and activated P0 transcription. Consistently, in vivo genetic deletion of HDAC1/2 in mouse neural crest cells led to strongly decreased Sox10 expression, no detectable Pax3, virtually no satellite glia, and no Schwann cell precursors in dorsal root ganglia and peripheral nerves. Similarly, in vivo ablation of Pax3 in the mouse neural crest resulted in strongly reduced expression of Sox10 and Fabp7. Therefore, by controlling the expression of Pax3 and the concerted action of Pax3 and Sox10 on their target genes, HDAC1/2 direct the specification of neural crest cells into peripheral glia.

Original languageEnglish
Pages (from-to)6112-6122
Number of pages11
JournalJournal of Neuroscience
Volume34
Issue number17
DOIs
StatePublished - 2014

Fingerprint

Neural Crest
Neuroglia
Histone Deacetylases
Schwann Cells
Transcription Factors
Myelin P0 Protein
Melanocytes
Peripheral Nervous System
Spinal Ganglia
Chondrocytes
Peripheral Nerves
Smooth Muscle Myocytes
Neurons

Keywords

  • Histone deacetylases
  • Neural crest cells
  • Peripheral glia specification
  • Transcriptional control

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Jacob, C., Lötscher, P., Engler, S., Baggiolini, A., Tavares, S. V., Brügger, V., ... Suter, U. (2014). HDAC1 and HDAC2 control the specification of neural crest cells into peripheral glia. Journal of Neuroscience, 34(17), 6112-6122. https://doi.org/10.1523/JNEUROSCI.5212-13.2014

HDAC1 and HDAC2 control the specification of neural crest cells into peripheral glia. / Jacob, Claire; Lötscher, Pirmin; Engler, Stefanie; Baggiolini, Arianna; Tavares, Sandra Varum; Brügger, Valérie; John, Nessy; Büchmann-Møller, Stine; Snider, Paige L.; Conway, Simon; Yamaguchi, Teppei; Matthias, Patrick; Sommer, Lukas; Mantei, Ned; Suter, Ueli.

In: Journal of Neuroscience, Vol. 34, No. 17, 2014, p. 6112-6122.

Research output: Contribution to journalArticle

Jacob, C, Lötscher, P, Engler, S, Baggiolini, A, Tavares, SV, Brügger, V, John, N, Büchmann-Møller, S, Snider, PL, Conway, S, Yamaguchi, T, Matthias, P, Sommer, L, Mantei, N & Suter, U 2014, 'HDAC1 and HDAC2 control the specification of neural crest cells into peripheral glia', Journal of Neuroscience, vol. 34, no. 17, pp. 6112-6122. https://doi.org/10.1523/JNEUROSCI.5212-13.2014
Jacob C, Lötscher P, Engler S, Baggiolini A, Tavares SV, Brügger V et al. HDAC1 and HDAC2 control the specification of neural crest cells into peripheral glia. Journal of Neuroscience. 2014;34(17):6112-6122. https://doi.org/10.1523/JNEUROSCI.5212-13.2014
Jacob, Claire ; Lötscher, Pirmin ; Engler, Stefanie ; Baggiolini, Arianna ; Tavares, Sandra Varum ; Brügger, Valérie ; John, Nessy ; Büchmann-Møller, Stine ; Snider, Paige L. ; Conway, Simon ; Yamaguchi, Teppei ; Matthias, Patrick ; Sommer, Lukas ; Mantei, Ned ; Suter, Ueli. / HDAC1 and HDAC2 control the specification of neural crest cells into peripheral glia. In: Journal of Neuroscience. 2014 ; Vol. 34, No. 17. pp. 6112-6122.
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AU - Lötscher, Pirmin

AU - Engler, Stefanie

AU - Baggiolini, Arianna

AU - Tavares, Sandra Varum

AU - Brügger, Valérie

AU - John, Nessy

AU - Büchmann-Møller, Stine

AU - Snider, Paige L.

AU - Conway, Simon

AU - Yamaguchi, Teppei

AU - Matthias, Patrick

AU - Sommer, Lukas

AU - Mantei, Ned

AU - Suter, Ueli

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N2 - Schwann cells, the myelinating glia of the peripheral nervous system (PNS), originate from multipotent neural crest cells that also give rise to other cells, including neurons, melanocytes, chondrocytes, and smooth muscle cells. The transcription factor Sox10 is required for peripheral glia specification. However, all neural crest cells express Sox10 and the mechanisms directing neural crest cells into a specific lineage are poorly understood. We show here that histone deacetylases 1 and 2 (HDAC1/2) are essential for the specification of neural crest cells into Schwann cell precursors and satellite glia, which express the early determinants of their lineage myelin protein zero (P0) and/or fatty acid binding protein 7 (Fabp7). In neural crest cells, HDAC1/2 induced expression of the transcription factor Pax3 by binding and activating the Pax3 promoter. In turn, Pax3 was required to maintain high Sox10 levels and to trigger expression of Fabp7. In addition, HDAC1/2 were bound to the P0 promoter and activated P0 transcription. Consistently, in vivo genetic deletion of HDAC1/2 in mouse neural crest cells led to strongly decreased Sox10 expression, no detectable Pax3, virtually no satellite glia, and no Schwann cell precursors in dorsal root ganglia and peripheral nerves. Similarly, in vivo ablation of Pax3 in the mouse neural crest resulted in strongly reduced expression of Sox10 and Fabp7. Therefore, by controlling the expression of Pax3 and the concerted action of Pax3 and Sox10 on their target genes, HDAC1/2 direct the specification of neural crest cells into peripheral glia.

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