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Melanin-concentrating hormone regulates beat frequency of ependymal cilia and ventricular volume

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Abstract

Ependymal cell cilia help move cerebrospinal fluid through the cerebral ventricles, but the regulation of their beat frequency remains unclear. Using in vitro, high-speed video microscopy and in vivo magnetic resonance imaging in mice, we found that the metabolic peptide melanin-concentrating hormone (MCH) positively controlled cilia beat frequency, specifically in the ventral third ventricle, whereas a lack of MCH receptor provoked a ventricular size increase.

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Figure 1: MCH increases ependymal cell CBF in the v3V, where MCH fibers and MCHR1 are present in close apposition.
Figure 2: Stimulation of MCH neurons in brain slices increases CBF in neighboring ependymal cells along the v3V.
Figure 3: In vivo assessment of ventricle enlargement in Mchr1−/− mice.

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Acknowledgements

We thank J.M. Friedman (Rockefeller University) for Pmch-CFP mice, J. Boutin (Institut de Recherche Servier) for the MCHR1 antagonists, F. Kober and T. Troalen for cine phase-contrast MRI tests, A. Le Troter for assistance in three-dimensional reconstruction of brain MRI, C. Houdayer for laser-capture dissections, V. Thieffin for animal care, I. Larre for help with immunoassays, F. Aguila for artwork, J. Chabry and P. Mollard for discussions, G. Agarwal for help with Matlab, and S. Rasika and P. Haghighi for corrections and remarks on the manuscript. Supported by the Agence Nationale de la Recherche (ANR; ANR-08-MNPS-018-01 to J.-L.N., ANR Gliodiabesity project to V.P. and ANR-09-BLAN-0267 to V.P.), the CNRS Institut National des Sciences Biologiques (INSB), European Union 6th Framework Program STREPS/NEST-APES 28594 (J.L.N.), Projets Exploratoires Premier Soutien (INSB; A.G. and J.-L.N.), the Fondation de la Recherche Médicale (J.-L.N.), and postdoctoral fellowships from the ANR-08-MNPS-018-01 and CNRS (INSB) and awards from the Société Française de Nutrition 2011 and the Institut Danone 2012 (G.C.). A.A. was supported by the Douglas Foundation, McGill University, Canadian Fund for Innovation, Research Chair (Tier 2), and Institute for Health Research and the Natural Science and Engineering Council of Canada.

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Author notes

  1. Grégory Conductier, Frédéric Brau and Angèle Viola: These authors contributed equally to this work.

  2. Vincent Prévot, Olivier Meste, Jean-Louis Nahon and Alice Guyon: These authors jointly directed this work.

Authors and Affiliations

  1. Institut de Pharmacologie Moléculaire et Cellulaire, UMR 7275 Centre National de la Recherche Scientifique (CNRS), Valbonne, France

    Grégory Conductier, Frédéric Brau, Thibault Lemaire, Raphaël Chapot, Laurianne Lucas, Carole Rovère, Priscilla Maitre, Salma Hosseiny, Agnès Petit-Paitel, Jean-Louis Nahon & Alice Guyon

  2. University of Nice Sophia Antipolis, Nice, France

    Grégory Conductier, Frédéric Brau, Navean Ramkumar, Thibault Lemaire, Raphaël Chapot, Laurianne Lucas, Carole Rovère, Priscilla Maitre, Salma Hosseiny, Agnès Petit-Paitel, Olivier Meste, Jean-Louis Nahon & Alice Guyon

  3. Aix-Marseille Université, Centre de Résonance Magnétique Biologique et Médicale, UMR 7339 CNRS, Faculté de Médecine la Timone, Marseille, France

    Angèle Viola

  4. INSERM U837/University of Lille 2, Lille, France

    Fanny Langlet, Bénédicte Dehouck & Vincent Prévot

  5. I3S, UMR 7271 CNRS, Sophia Antipolis, France

    Navean Ramkumar & Olivier Meste

  6. Douglass Mental Health University Intitute, Montreal, Quebec, Canada

    Antoine Adamantidis

  7. University of Liège, GIGA-Neurosciences, Liège, Belgium

    Bernard Lakaye

  8. Laboratoire d'Histologie, EA3922, SFR FED 4234, Faculté de Médecine et de Pharmacie, Besançon, France

    Pierre-Yves Risold

  9. Station de Primatologie, UPS 846 CNRS, Rousset sur Arc, France

    Jean-Louis Nahon

Authors
  1. Grégory Conductier
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  2. Frédéric Brau
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  3. Angèle Viola
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  4. Fanny Langlet
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  5. Navean Ramkumar
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  6. Bénédicte Dehouck
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  7. Thibault Lemaire
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  9. Laurianne Lucas
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  10. Carole Rovère
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  11. Priscilla Maitre
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  12. Salma Hosseiny
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  13. Agnès Petit-Paitel
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  14. Antoine Adamantidis
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  15. Bernard Lakaye
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  17. Vincent Prévot
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  18. Olivier Meste
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  19. Jean-Louis Nahon
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  20. Alice Guyon
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Contributions

G.C., F.B., A.V., F.L., B.D., V.P., L.L., C.R., P.M., S.H., P.-Y.R., A.P.-P. and A.G. performed the experiments. N.R. and O.M. engineered analytical tools. A.A. and B.L. engineered Mchr1−/− mice. G.C., A.V., V.P., T.L., R.C., P.-Y.R., J.-L.N. and A.G. analyzed the data. G.C., J.-L.N. and A.G. wrote the paper.

Corresponding authors

Correspondence to Jean-Louis Nahon or Alice Guyon.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8 and Supplementary Table 1 (PDF 1370 kb)

Supplementary Movie 1

Representative video recording of the CBF of ciliated ependymal cells in the third ventricle. (AVI 1727 kb)

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Conductier, G., Brau, F., Viola, A. et al. Melanin-concentrating hormone regulates beat frequency of ependymal cilia and ventricular volume. Nat Neurosci 16, 845–847 (2013). https://doi.org/10.1038/nn.3401

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