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AMPK Activation of PGC-1α/NRF-1-Dependent SELENOT Gene Transcription Promotes PACAP-Induced Neuroendocrine Cell Differentiation Through Tolerance to Oxidative Stress

  • Houssni Abid
  • Dorthe Cartier
  • Abdallah Hamieh
  • Anne-Marie François-Bellan
  • Christine Bucharles
  • Hugo Pothion
  • Destiny-Love Manecka
  • Jérôme Leprince
  • Sahil Adriouch
  • Olivier Boyer
  • Youssef Anouar
  • Isabelle Lihrmann
Article
  • 77 Downloads

Abstract

Several cues including pituitary adenylate cyclase-activating polypeptide (PACAP), which acts through cAMP stimulation, specify the conversion of sympathoadrenal (SA) precursors toward different cell phenotypes by promoting their survival and differentiation. Selenoprotein T (SELENOT) is a PACAP-stimulated ER oxidoreductase that exerts an essential antioxidant activity and whose up-regulation is associated with SA cell differentiation. In the present study, we investigated the transcriptional cascade elicited by PACAP/cAMP to trigger SELENOT gene transcription during the conversion of PC12 cells from SA progenitor-like cells toward a neuroendocrine phenotype. Unexpectedly, we found that PACAP/cAMP recruits the canonical pathway that regulates mitochondrial function in order to elicit SELENOT gene transcription and the consequent antioxidant response during PC12 cell differentiation. This cascade involves LKB1-mediated AMPK activation in order to stimulate SELENOT gene transcription through the PGC1-α/NRF-1 complex, thus allowing SELENOT to promote PACAP-stimulated neuroendocrine cell survival and differentiation. Our data reveal that a PACAP and cAMP-activated AMPK-PGC-1α/NRF-1 cascade is critical for the coupling of oxidative stress tolerance, via SELENOT gene expression, and mitochondrial biogenesis in order to achieve PC12 cell differentiation. The data further highlight the essential role of SELENOT in cell metabolism during differentiation.

Keywords

cAMP PGC-1α NRF-1 Mitochondriogenesis Oxidative stress 

Notes

Author Contributions

I.L. and Y.A. designed the experiments. H.A., D.C, A.H., A-M.F-B., C.B., H.P., D-L.M. and A.S. performed the experiments; J.L. and O.B. helped to analyze the data, I.L. and Y.A. wrote the manuscript.

Funding

This work was supported by Inserm (U1239), the Conseil Régional de Normandie, the University of Rouen Normandie and the European Union. Europe is involved in Normandie with European Regional Development Fund (ERDF).

Compliance with Ethical Standards

Competing Interests

The authors declare they have no competing interest.

Supplementary material

12035_2018_1352_MOESM1_ESM.doc (64 kb)
ESM 1 (DOC 64.5 kb)
12035_2018_1352_MOESM2_ESM.pdf (23 kb)
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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Houssni Abid
    • 1
    • 2
  • Dorthe Cartier
    • 1
    • 2
  • Abdallah Hamieh
    • 1
    • 2
  • Anne-Marie François-Bellan
    • 3
  • Christine Bucharles
    • 1
    • 2
  • Hugo Pothion
    • 1
    • 2
  • Destiny-Love Manecka
    • 1
    • 2
  • Jérôme Leprince
    • 1
    • 2
  • Sahil Adriouch
    • 2
    • 4
  • Olivier Boyer
    • 2
    • 4
  • Youssef Anouar
    • 1
    • 2
  • Isabelle Lihrmann
    • 1
    • 2
  1. 1.UNIROUEN, Inserm U1239, Neuronal and Neuroendocrine Differentiation and Communication LaboratoryRouen-Normandie UniversityMont-Saint-AignanFrance
  2. 2.Institute for Research and Innovation in BiomedicineRouenFrance
  3. 3.CNRS UMR 7051, Neurophysiopathol InstAix-Marseille University13015 MarseilleFrance
  4. 4.UNIROUEN, Inserm U1234, Pathophysiology and Biotherapy of Inflammatory and Autoimmune DiseasesRouen-Normandie UniversityRouenFrance

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