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Maternal dietary fat during lactation shapes single nucleus transcriptomic profile of postnatal offspring hypothalamus in a sexually dimorphic manner in mice

Author

Listed:
  • Yi Huang

    (Chinese Academy of Sciences
    Metabolism Program)

  • Anyongqi Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wenjiang Zhou

    (Fudan University)

  • Baoguo Li

    (Chinese Academy of Sciences
    Zhengzhou University)

  • Linshan Zhang

    (Fudan University)

  • Agata M. Rudolf

    (Chinese Academy of Sciences)

  • Zengguang Jin

    (Chinese Academy of Sciences)

  • Catherine Hambly

    (University of Aberdeen)

  • Guanlin Wang

    (Fudan University)

  • John R. Speakman

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Aberdeen
    China Medical University)

Abstract

Maternal overnutrition during lactation predisposes offspring to develop metabolic diseases and exacerbates the relevant syndromes in males more than females in later life. The hypothalamus is a heterogenous brain region that regulates energy balance. Here we combined metabolic trait quantification of mother and offspring mice under low and high fat diet (HFD) feeding during lactation, with single nucleus transcriptomic profiling of their offspring hypothalamus at peak lacation to understand the cellular and molecular alterations in response to maternal dietary pertubation. We found significant expansion in neuronal subpopulations including histaminergic (Hdc), arginine vasopressin/retinoic acid receptor-related orphan receptor β (Avp/Rorb) and agouti-related peptide/neuropeptide Y (AgRP/Npy) in male offspring when their mothers were fed HFD, and increased Npy-astrocyte interactions in offspring responding to maternal overnutrition. Our study provides a comprehensive offspring hypothalamus map at the peak lactation and reveals how the cellular subpopulations respond to maternal dietary fat in a sex-specific manner during development.

Suggested Citation

  • Yi Huang & Anyongqi Wang & Wenjiang Zhou & Baoguo Li & Linshan Zhang & Agata M. Rudolf & Zengguang Jin & Catherine Hambly & Guanlin Wang & John R. Speakman, 2024. "Maternal dietary fat during lactation shapes single nucleus transcriptomic profile of postnatal offspring hypothalamus in a sexually dimorphic manner in mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46589-x
    DOI: 10.1038/s41467-024-46589-x
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    References listed on IDEAS

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    1. Christian Huisman & Hyeyoung Cho & Olivier Brock & Su Jeong Lim & Sung Min Youn & Younjung Park & Sangsoo Kim & Soo-Kyung Lee & Alessio Delogu & Jae W. Lee, 2019. "Single cell transcriptome analysis of developing arcuate nucleus neurons uncovers their key developmental regulators," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    2. Dong Won Kim & Parris Whitney Washington & Zoe Qianyi Wang & Sonia Hao Lin & Changyu Sun & Basma Taleb Ismail & Hong Wang & Lizhi Jiang & Seth Blackshaw, 2020. "The cellular and molecular landscape of hypothalamic patterning and differentiation from embryonic to late postnatal development," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Adam E. Locke & Bratati Kahali & Sonja I. Berndt & Anne E. Justice & Tune H. Pers & Felix R. Day & Corey Powell & Sailaja Vedantam & Martin L. Buchkovich & Jian Yang & Damien C. Croteau-Chonka & Tonu , 2015. "Genetic studies of body mass index yield new insights for obesity biology," Nature, Nature, vol. 518(7538), pages 197-206, February.
    4. Michael Lattke & Robert Goldstone & James K. Ellis & Stefan Boeing & Jerónimo Jurado-Arjona & Nicolás Marichal & James I. MacRae & Benedikt Berninger & Francois Guillemot, 2021. "Extensive transcriptional and chromatin changes underlie astrocyte maturation in vivo and in culture," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    5. Jie Xu & Christopher L. Bartolome & Cho Shing Low & Xinchi Yi & Cheng-Hao Chien & Peng Wang & Dong Kong, 2018. "Genetic identification of leptin neural circuits in energy and glucose homeostases," Nature, Nature, vol. 556(7702), pages 505-509, April.
    6. Michael W. Schwartz & Stephen C. Woods & Daniel Porte & Randy J. Seeley & Denis G. Baskin, 2000. "Central nervous system control of food intake," Nature, Nature, vol. 404(6778), pages 661-671, April.
    7. M. Büttner & J. Ostner & C. L. Müller & F. J. Theis & B. Schubert, 2021. "scCODA is a Bayesian model for compositional single-cell data analysis," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
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