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Featured ArticleResearch Articles, Cellular/Molecular

RLN3/RXFP3 Signaling in the PVN Inhibits Magnocellular Neurons via M-like Current Activation and Contributes to Binge Eating Behavior

Alan Kania, Agata Szlaga, Patryk Sambak, Anna Gugula, Ewa Blasiak, Maria Vittoria Micioni Di Bonaventura, Mohammad Akhter Hossain, Carlo Cifani, Grzegorz Hess, Andrew L. Gundlach and Anna Blasiak
Journal of Neuroscience 8 July 2020, 40 (28) 5362-5375; DOI: https://doi.org/10.1523/JNEUROSCI.2895-19.2020
Alan Kania
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, 30-387, Poland
3School of Pharmacy, Pharmacology Unit, University of Camerino, Camerino, 62032, Italy
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Agata Szlaga
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, 30-387, Poland
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Patryk Sambak
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, 30-387, Poland
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Anna Gugula
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, 30-387, Poland
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Ewa Blasiak
2Department of Physical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Krakow, 30-387, Poland
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Maria Vittoria Micioni Di Bonaventura
3School of Pharmacy, Pharmacology Unit, University of Camerino, Camerino, 62032, Italy
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Mohammad Akhter Hossain
4Florey Institute of Neuroscience and Mental Health, and Florey Department of Neuroscience and Mental Health, University of Melbourne, Melbourne, 3010 Victoria, Australia
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Carlo Cifani
3School of Pharmacy, Pharmacology Unit, University of Camerino, Camerino, 62032, Italy
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Grzegorz Hess
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, 30-387, Poland
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Andrew L. Gundlach
4Florey Institute of Neuroscience and Mental Health, and Florey Department of Neuroscience and Mental Health, University of Melbourne, Melbourne, 3010 Victoria, Australia
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Anna Blasiak
1Department of Neurophysiology and Chronobiology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University, Krakow, 30-387, Poland
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Abstract

Binge-eating disorder is the most common eating disorder. Various neuropeptides play important roles in the regulation of feeding behavior, including relaxin-3 (RLN3), which stimulates food intake in rats through the activation of the relaxin-family peptide-3 receptor (RXFP3). Here we demonstrate that a likely mechanism underlying the orexigenic action of RLN3 is RXFP3-mediated inhibition of oxytocin- and arginine-vasopressin-synthesizing paraventricular nucleus (PVN) magnocellular neurosecretory cells. Moreover, we reveal that, in male and female rats, this action depends on M-like potassium conductance. Notably, higher intra- and peri-PVN RLN3 fiber densities were observed in females, which may constitute an anatomic substrate for observed sex differences in binge-eating disorder. Finally, in a model of binge-eating in female rats, RXFP3 blockade within the PVN prevented binge-eating behavior. These data demonstrate a direct RLN3/RXFP3 action in the PVN of male and female rats, identify the associated ionic mechanisms, and reveal that hypothalamic RLN3/RXFP3 signaling regulates binge-eating behavior.

SIGNIFICANCE STATEMENT Binge-eating disorder is the most common eating disorder worldwide, affecting women twice as frequently as men. Various neuropeptides play important roles in the regulation of feeding behavior, including relaxin-3, which acts via the relaxin-family peptide-3 receptor (RXFP3). Using a model of binge-eating, we demonstrated that relaxin-3/RXFP3 signaling in the hypothalamic paraventricular nucleus (PVN) is necessary for the expression of binge-eating behavior in female rats. Moreover, we elucidated the neuronal mechanism of RLN3/RXFP3 signaling in PVN in male and female rats and characterized sex differences in the RLN3 innervation of the PVN. These findings increase our understanding of the brain circuits and neurotransmitters involved in binge-eating disorder pathology and identify RXFP3 as a therapeutic target for binge-like eating disorders.

  • binge eating
  • M-like current
  • paraventricular nucleus of hypothalamus
  • relaxin-3
  • RXFP3

This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The Journal of Neuroscience: 40 (28)
Journal of Neuroscience
Vol. 40, Issue 28
8 Jul 2020
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RLN3/RXFP3 Signaling in the PVN Inhibits Magnocellular Neurons via M-like Current Activation and Contributes to Binge Eating Behavior
Alan Kania, Agata Szlaga, Patryk Sambak, Anna Gugula, Ewa Blasiak, Maria Vittoria Micioni Di Bonaventura, Mohammad Akhter Hossain, Carlo Cifani, Grzegorz Hess, Andrew L. Gundlach, Anna Blasiak
Journal of Neuroscience 8 July 2020, 40 (28) 5362-5375; DOI: 10.1523/JNEUROSCI.2895-19.2020

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RLN3/RXFP3 Signaling in the PVN Inhibits Magnocellular Neurons via M-like Current Activation and Contributes to Binge Eating Behavior
Alan Kania, Agata Szlaga, Patryk Sambak, Anna Gugula, Ewa Blasiak, Maria Vittoria Micioni Di Bonaventura, Mohammad Akhter Hossain, Carlo Cifani, Grzegorz Hess, Andrew L. Gundlach, Anna Blasiak
Journal of Neuroscience 8 July 2020, 40 (28) 5362-5375; DOI: 10.1523/JNEUROSCI.2895-19.2020
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Keywords

  • binge eating
  • M-like current
  • paraventricular nucleus of hypothalamus
  • relaxin-3
  • RXFP3

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