Olig2 regulates terminal differentiation and maturation of peripheral olfactory sensory neurons

The bHLH transcription factor Olig2 is required for sequential cell fate determination of both motor neurons and oligodendrocytes and for progenitor proliferation in the central nervous system. However, the role of Olig2 in peripheral sensory neurogenesis remains unknown. We report that Olig2 is tra...

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Published in:	Cellular and molecular life sciences : CMLS Vol. 77; no. 18; pp. 3597 - 3609
Main Authors:	Wang, Ya-Zhou, Fan, Hong, Ji, Yu, Reynolds, Kurt, Gu, Ran, Gan, Qini, Yamagami, Takashi, Zhao, Tianyu, Hamad, Salaheddin, Bizen, Norihisa, Takebayashi, Hirohide, Chen, YiPing, Wu, Shengxi, Pleasure, David, Lam, Kit, Zhou, Chengji J.
Format:	Journal Article
Language:	English
Published:	Cham Springer International Publishing 01-09-2020 Springer Nature B.V
Subjects:	Biochemistry Biomedical and Life Sciences Biomedicine Cell Biology Cell differentiation Cell fate Central nervous system Depletion Differentiation Fate maps Gene mapping Gestation Helix-loop-helix proteins (basic) Life Sciences Mapping Maturation Motor neurons Nervous system Neurogenesis Neurons Olfactory ensheathing cells Olfactory marker protein Olfactory receptor neurons Olfactory system Olig2 protein Oligodendrocytes Original Article Sensory neurons Smell Dcx Sox2 Basic helix–loop–helix (bHLH) transcription factors Fabp7 (Blbp) Peripheral nervous system (PNS) Tuj1
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Abstract	The bHLH transcription factor Olig2 is required for sequential cell fate determination of both motor neurons and oligodendrocytes and for progenitor proliferation in the central nervous system. However, the role of Olig2 in peripheral sensory neurogenesis remains unknown. We report that Olig2 is transiently expressed in the newly differentiated olfactory sensory neurons (OSNs) and is down-regulated in the mature OSNs in mice from early gestation to adulthood. Genetic fate mapping demonstrates that Olig2-expressing cells solely give rise to OSNs in the peripheral olfactory system. Olig2 depletion does not affect the proliferation of peripheral olfactory progenitors and the fate determination of OSNs, sustentacular cells, and the olfactory ensheathing cells. However, the terminal differentiation and maturation of OSNs are compromised in either Olig2 single or Olig1/Olig2 double knockout mice, associated with significantly diminished expression of multiple OSN maturation and odorant signaling genes, including Omp , Gnal , Adcy3 , and Olfr15 . We further demonstrate that Olig2 binds to the E-box in the Omp promoter region to regulate its expression. Taken together, our results reveal a distinctly novel function of Olig2 in the periphery nervous system to regulate the terminal differentiation and maturation of olfactory sensory neurons.
AbstractList	The bHLH transcription factor Olig2 is required for sequential cell fate determination of both motor neurons and oligodendrocytes and for progenitor proliferation in the central nervous system. However, the role of Olig2 in peripheral sensory neurogenesis remains unknown. We report that Olig2 is transiently expressed in the newly differentiated olfactory sensory neurons (OSNs) and is down-regulated in the mature OSNs in mice from early gestation to adulthood. Genetic fate mapping demonstrates that Olig2-expressing cells solely give rise to OSNs in the peripheral olfactory system. Olig2 depletion does not affect the proliferation of peripheral olfactory progenitors and the fate determination of OSNs, sustentacular cells, and the olfactory ensheathing cells. However, the terminal differentiation and maturation of OSNs are compromised in either Olig2 single or Olig1/Olig2 double knockout mice, associated with significantly diminished expression of multiple OSN maturation and odorant signaling genes, including Omp , Gnal , Adcy3 , and Olfr15 . We further demonstrate that Olig2 binds to the E-box in the Omp promoter region to regulate its expression. Taken together, our results reveal a distinctly novel function of Olig2 in the periphery nervous system to regulate the terminal differentiation and maturation of olfactory sensory neurons. The bHLH transcription factor Olig2 is required for sequential cell fate determination of both motor neurons and oligodendrocytes and for progenitor proliferation in the central nervous system. However, the role of Olig2 in peripheral sensory neurogenesis remains unknown. We report that Olig2 is transiently expressed in the newly differentiated olfactory sensory neurons (OSNs) and is down-regulated in the mature OSNs in mice from early gestation to adulthood. Genetic fate mapping demonstrates that Olig2-expressing cells solely give rise to OSNs in the peripheral olfactory system. Olig2 depletion does not affect the proliferation of peripheral olfactory progenitors and the fate determination of OSNs, sustentacular cells, and the olfactory ensheathing cells. However, the terminal differentiation and maturation of OSNs are compromised in either Olig2 single or Olig1/Olig2 double knockout mice, associated with significantly diminished expression of multiple OSN maturation and odorant signaling genes, including Omp, Gnal, Adcy3, and Olfr15. We further demonstrate that Olig2 binds to the E-box in the Omp promoter region to regulate its expression. Taken together, our results reveal a distinctly novel function of Olig2 in the periphery nervous system to regulate the terminal differentiation and maturation of olfactory sensory neurons. The bHLH transcription factor Olig2 is required for sequential cell fate determination of both motor neurons and oligodendrocytes and for progenitor proliferation in the central nervous system. However, the role of Olig2 in peripheral sensory neurogenesis remains unknown. We report that Olig2 is transiently expressed in the newly differentiated olfactory sensory neurons (OSNs) and is downregulated in the mature OSNs in mice from early gestation to adulthood. Genetic fate mapping demonstrates that Olig2-expressing cells solely give rise to OSNs in the peripheral olfactory system. Olig2 depletion does not affect the proliferation of peripheral olfactory progenitors and the fate determination of OSNs, sustentacular cells, and the olfactory ensheathing cells (OECs). However, the terminal differentiation and maturation of OSNs are compromised in either Olig2 single or Olig1/Olig2 double knockout mice, associated with significantly diminished expression of multiple OSN maturation and odorant signaling genes, including Omp, Gnal, Adcy3, and Olfr15. We further demonstrate that Olig2 binds to the E-box in the Omp promoter region to regulate its expression. Taken together, our results reveal a distinctly novel function of Olig2 in the periphery nervous system to regulate the terminal differentiation and maturation of olfactory sensory neurons.
Author	Gu, Ran Gan, Qini Wang, Ya-Zhou Bizen, Norihisa Pleasure, David Zhao, Tianyu Ji, Yu Hamad, Salaheddin Yamagami, Takashi Chen, YiPing Takebayashi, Hirohide Fan, Hong Reynolds, Kurt Wu, Shengxi Lam, Kit Zhou, Chengji J.
AuthorAffiliation	3 Department of Biochemistry and Molecular Medicine, University of California at Davis, School of Medicine, 2425 Stockton Blvd., Sacramento, California 95817, USA 4 Division of Neurobiology and Anatomy, Graduate School of Medical and Dental Sciences, Niigata University, Asahimachi Chuo-ku, Niigata 951-8510, Japan 2 Institute for Pediatric Regenerative Medicine of Shriners Hospitals for Children, University of California at Davis, School of Medicine, 2425 Stockton Blvd., Sacramento, California 95817, USA 1 Department of Neurobiology and Collaborative Innovation Center for Brain Science, School of Basic Medicine, Fourth Military Medical University, 169 Chang Le Xi Road, Xi’an, Shaanxi 710032, China 5 Department of Cell and Molecular Biology, Tulane University, New Orleans, Louisiana 70118, USA
AuthorAffiliation_xml	– name: 5 Department of Cell and Molecular Biology, Tulane University, New Orleans, Louisiana 70118, USA – name: 4 Division of Neurobiology and Anatomy, Graduate School of Medical and Dental Sciences, Niigata University, Asahimachi Chuo-ku, Niigata 951-8510, Japan – name: 1 Department of Neurobiology and Collaborative Innovation Center for Brain Science, School of Basic Medicine, Fourth Military Medical University, 169 Chang Le Xi Road, Xi’an, Shaanxi 710032, China – name: 3 Department of Biochemistry and Molecular Medicine, University of California at Davis, School of Medicine, 2425 Stockton Blvd., Sacramento, California 95817, USA – name: 2 Institute for Pediatric Regenerative Medicine of Shriners Hospitals for Children, University of California at Davis, School of Medicine, 2425 Stockton Blvd., Sacramento, California 95817, USA
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Keywords	Dcx Sox2 Basic helix–loop–helix (bHLH) transcription factors Fabp7 (Blbp) Peripheral nervous system (PNS) Tuj1
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Snippet	The bHLH transcription factor Olig2 is required for sequential cell fate determination of both motor neurons and oligodendrocytes and for progenitor...
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SubjectTerms	Biochemistry Biomedical and Life Sciences Biomedicine Cell Biology Cell differentiation Cell fate Central nervous system Depletion Differentiation Fate maps Gene mapping Gestation Helix-loop-helix proteins (basic) Life Sciences Mapping Maturation Motor neurons Nervous system Neurogenesis Neurons Olfactory ensheathing cells Olfactory marker protein Olfactory receptor neurons Olfactory system Olig2 protein Oligodendrocytes Original Article Sensory neurons Smell
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Title	Olig2 regulates terminal differentiation and maturation of peripheral olfactory sensory neurons
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