Summary of ssbd-repos-000374

Name
URL
DOI

Title
Dietary Availability Acutely Influences Puberty Onset via Hypothalamic Neural Circuit
Description

Reproduction poses a substantial burden, especially for mammalian females. Puberty onset serves as a vital checkpoint, regulated based on the body’s energy state, to prevent inappropriate reproductive activity under malnutrition. However, the neural basis of this puberty checkpoint remains poorly understood. Here, we demonstrate that peripubertal malnutrition in female mice reduces the synchronous activity episodes of arcuate kisspeptin neurons, which are critical regulators of the gonadotropin axis. Improved dietary availability increased the frequency of this pulsatile activity, facilitating puberty onset. Using a viral-genetic approach, we show that the activity of agouti-related protein neurons in the arcuate nucleus, a hunger center, can bidirectionally regulate the pulsatile activity of kisspeptin neurons and follicular maturation in the ovaries. Collectively, a neural circuit connecting feeding to reproductive centers modulates the frequency of pulsatile kisspeptin neuron activity based on dietary availability, which sheds light on the neural basis of the puberty checkpoint.

Submited Date
2024-08-01
Release Date
2025-02-25
Updated Date
-
License
Funding information
Grants-in-Aid from the Japan Society for the Promotion of Science (JSPS) to Teppei Goto (Nos. 19K16270, 21K15194, and 24K09651) and Kazunari Miyamichi (Nos. 20K20589 and 21H02587), Mitsubishi foundation and a Takeda Life Science grant to Kazunari Miyamichi, and a RIKEN internal fund to Kazunari Miyamichi. Teppei Goto was also supported by RIKEN Special Postdoctoral Researchers Program.
File formats
CSV files
Data size
22.5 GB

Organism
mice
Strain
C57BL/6N
Cell Line
NA
Genes
Kiss1
Proteins
Kisspeptin

GO Molecular Function (MF)
NA
GO Biological Process (BP)
reproductive functions; pulsatile activities for secretion of gonadotrophin
GO Cellular Component (CC)
Neuron
Study Type
neural activity; Ca2+ imaging
Imaging Methods
fiber photometory with GCaMP6s

Method Summary

See detail in Dietary Availability Acutely Influences Puberty Onset via Hypothalamic Neural Circuit. Goto T et al. (2024), BioRxiv

Related paper(s)

Goto, Teppei, Hagihara, Mitsue, Irie, Satsuki, Abe, Takaya, Kiyonari, Hiroshi, Miyamichi, Kazunari, Dietary availability acutely influences puberty onset via a hypothalamic neural circuit, Neuron

Published in Feb. 25, 2025

(Abstract) Reproduction poses a substantial burden, especially for mammalian females. Puberty onset serves as a vital checkpoint, regulated based on the body?s energy state, to prevent inappropriate reproductive activity under malnutrition. However, the neural basis of this puberty checkpoint remains poorly understood. Here, we demonstrate that peripubertal malnutrition in female mice reduces the synchronous activity episodes of arcuate kisspeptin neurons, which are critical regulators of the gonadotropin axis. Improved dietary availability increased the frequency of this pulsatile activity, facilitating puberty onset. Using a viral-genetic approach, we show that the activity of agouti-related protein neurons in the arcuate nucleus, a hunger center, can bidirectionally regulate the pulsatile activity of kisspeptin neurons and follicular maturation in the ovaries. Collectively, a neural circuit connecting feeding to reproductive centers acts as an adjuster of the frequency of pulsatile kisspeptin neuron activity based on dietary availability, contributing to the neural basis of the puberty checkpoint.
Related paper(s)

Goto, Teppei, Hagihara, Mitsue, Irie, Satsuki, Abe, Takaya, Kiyonari, Hiroshi, Miyamichi, Kazunari (2023/01/01), Dietary Availability Acutely Governs Puberty Onset via Hypothalamic Neural Circuit, bioRxiv, 2023.09.15.558025

Published in 2023/01/01

(Abstract) Reproduction poses a substantial burden, especially for mammalian females. Puberty onset serves as a vital checkpoint, regulated based on the body’s energy state, to prevent inappropriate reproductive activity under malnutrition. However, the neural basis of this puberty checkpoint remains poorly understood. Here, we demonstrate that peripubertal malnutrition in female mice reduces the synchronous activity episodes of arcuate kisspeptin neurons (SEskiss), which are critical regulators of the gonadotropin axis. Improved dietary availability boosts SEskiss frequency, facilitating puberty onset. Using a viral-genetic approach, we show that the activating agouti-related protein neurons in the arcuate nucleus (ARCAgrp neurons), a hunger center, suppresses SEskiss, even with enough food. Conversely, loss-of-function of ARCAgrp neurons enhances SEskiss during malnutrition, partly promoting irregular sexual maturation. Collectively, a neural circuit connecting feeding to reproductive centers is responsible for disinhibiting SEskiss frequency based on dietary availability, which sheds light on the neural basis of puberty checkpoint.HighlightsThe pulsatile activity of arcuate kisspeptin neurons emerges and grows before vaginal opening.Pubertal impairment resulting from malnutrition is associated with a reduction in the pulsatile activity of kisspeptin neurons.Pubertal recovery by food availability follows the elevated pulsatile activity of kisspeptin neurons during catch-up growth.The arcuate Agrp neurons suppress the frequency of pulsatile activity of kisspeptin neurons under negative energy balance.Competing Interest StatementThe authors have declared no competing interest.

Contact(s)
Kazunari Miyamichi
Organization(s)
RIKEN , Center for Biosystems Dynamics Research , Lab for comparative connectomics
Image Data Contributors
Teppei Goto
Quantitative Data Contributors

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