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Articles, Cellular/Molecular

Hypothalamic miR-103 Protects from Hyperphagic Obesity in Mice

Ilya A. Vinnikov, Karolina Hajdukiewicz, Jürgen Reymann, Jürgen Beneke, Rafal Czajkowski, Lena C. Roth, Martin Novak, Andreas Roller, Nicole Dörner, Vytaute Starkuviene, Fabian J. Theis, Holger Erfle, Günther Schütz, Valery Grinevich and Witold Konopka
Journal of Neuroscience 6 August 2014, 34 (32) 10659-10674; https://doi.org/10.1523/JNEUROSCI.4251-13.2014
Ilya A. Vinnikov
1Molecular Biology of the Cell I,
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Karolina Hajdukiewicz
3Laboratory of Animal Models, Neurobiology Center, Nencki Institute of Experimental Biology of the Polish Academy of Sciences, 02-093 Warsaw, Poland,
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Jürgen Reymann
5ViroQuant-CellNetworks RNAi Screening Facility, BioQuant and
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Jürgen Beneke
5ViroQuant-CellNetworks RNAi Screening Facility, BioQuant and
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Rafal Czajkowski
3Laboratory of Animal Models, Neurobiology Center, Nencki Institute of Experimental Biology of the Polish Academy of Sciences, 02-093 Warsaw, Poland,
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Lena C. Roth
2Schaller Research Group on Neuropeptides, German Cancer Research Center, 69120 Heidelberg, Germany,
4CellNetworks Cluster of Excellence,
7Department of Molecular Neurobiology, Max Planck Institute for Medical Research, 69120 Heidelberg, Germany,
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Martin Novak
1Molecular Biology of the Cell I,
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Andreas Roller
8Institute for Bioinformatics and Systems Biology, Helmholtz Center Munich, German Research Center for Environmental Health, 85764 Neuherberg, Germany, and
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Nicole Dörner
1Molecular Biology of the Cell I,
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Vytaute Starkuviene
6ViroQuant Screening of Cellular Networks, BioQuant, University of Heidelberg, 69120 Heidelberg, Germany,
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Fabian J. Theis
8Institute for Bioinformatics and Systems Biology, Helmholtz Center Munich, German Research Center for Environmental Health, 85764 Neuherberg, Germany, and
9Department of Mathematics, Technical University Munich, 85748 Garching, Germany
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Holger Erfle
5ViroQuant-CellNetworks RNAi Screening Facility, BioQuant and
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Günther Schütz
1Molecular Biology of the Cell I,
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Valery Grinevich
2Schaller Research Group on Neuropeptides, German Cancer Research Center, 69120 Heidelberg, Germany,
4CellNetworks Cluster of Excellence,
7Department of Molecular Neurobiology, Max Planck Institute for Medical Research, 69120 Heidelberg, Germany,
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Witold Konopka
1Molecular Biology of the Cell I,
3Laboratory of Animal Models, Neurobiology Center, Nencki Institute of Experimental Biology of the Polish Academy of Sciences, 02-093 Warsaw, Poland,
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Abstract

The role of neuronal noncoding RNAs in energy control of the body is not fully understood. The arcuate nucleus (ARC) of the hypothalamus comprises neurons regulating food intake and body weight. Here we show that Dicer-dependent loss of microRNAs in these neurons of adult (DicerCKO) mice causes chronic overactivation of the signaling pathways involving phosphatidylinositol-3-kinase (PI3K), Akt, and mammalian target of rapamycin (mTOR) and an imbalance in the levels of neuropeptides, resulting in severe hyperphagic obesity. Similarly, the activation of PI3K-Akt-mTOR pathway due to Pten deletion in the adult forebrain leads to comparable weight increase. Conversely, the mTORC1 inhibitor rapamycin normalizes obesity in mice with an inactivated Dicer1 or Pten gene. Importantly, the continuous delivery of oligonucleotides mimicking microRNAs, which are predicted to target PI3K-Akt-mTOR pathway components, to the hypothalamus attenuates adiposity in DicerCKO mice. Furthermore, loss of miR-103 causes strong upregulation of the PI3K-Akt-mTOR pathway in vitro and its application into the ARC of the Dicer-deficient mice both reverses upregulation of Pik3cg, the mRNA encoding the catalytic subunit p110γ of the PI3K complex, and attenuates the hyperphagic obesity. Our data demonstrate in vivo the crucial role of neuronal microRNAs in the control of energy homeostasis.

  • Dicer
  • hypothalamus
  • metabolism
  • mice
  • microRNA
  • obesity
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The Journal of Neuroscience: 34 (32)
Journal of Neuroscience
Vol. 34, Issue 32
6 Aug 2014
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Hypothalamic miR-103 Protects from Hyperphagic Obesity in Mice
Ilya A. Vinnikov, Karolina Hajdukiewicz, Jürgen Reymann, Jürgen Beneke, Rafal Czajkowski, Lena C. Roth, Martin Novak, Andreas Roller, Nicole Dörner, Vytaute Starkuviene, Fabian J. Theis, Holger Erfle, Günther Schütz, Valery Grinevich, Witold Konopka
Journal of Neuroscience 6 August 2014, 34 (32) 10659-10674; DOI: 10.1523/JNEUROSCI.4251-13.2014

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Hypothalamic miR-103 Protects from Hyperphagic Obesity in Mice
Ilya A. Vinnikov, Karolina Hajdukiewicz, Jürgen Reymann, Jürgen Beneke, Rafal Czajkowski, Lena C. Roth, Martin Novak, Andreas Roller, Nicole Dörner, Vytaute Starkuviene, Fabian J. Theis, Holger Erfle, Günther Schütz, Valery Grinevich, Witold Konopka
Journal of Neuroscience 6 August 2014, 34 (32) 10659-10674; DOI: 10.1523/JNEUROSCI.4251-13.2014
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Keywords

  • Dicer
  • hypothalamus
  • metabolism
  • mice
  • microRNA
  • obesity

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