IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46589-x.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46589-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-46589-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    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. 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.
    6. 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.
    7. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jacob Joseph & Chang Liu & Qin Hui & Krishna Aragam & Zeyuan Wang & Brian Charest & Jennifer E. Huffman & Jacob M. Keaton & Todd L. Edwards & Serkalem Demissie & Luc Djousse & Juan P. Casas & J. Micha, 2022. "Genetic architecture of heart failure with preserved versus reduced ejection fraction," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Vikesh Amin & Jere R. Behrman & Jason M. Fletcher & Carlos A. Flores & Alfonso Flores‐Lagunes & Hans‐Peter Kohler, 2021. "Genetic risks, adolescent health, and schooling attainment," Health Economics, John Wiley & Sons, Ltd., vol. 30(11), pages 2905-2920, November.
    3. Lili Liu & Atlas Khan & Elena Sanchez-Rodriguez & Francesca Zanoni & Yifu Li & Nicholas Steers & Olivia Balderes & Junying Zhang & Priya Krithivasan & Robert A. LeDesma & Clara Fischman & Scott J. Heb, 2022. "Genetic regulation of serum IgA levels and susceptibility to common immune, infectious, kidney, and cardio-metabolic traits," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Michael R. Williamson & Stephanie P. Le & Ronald L. Franzen & Nicole A. Donlan & Jill L. Rosow & Mathilda S. Nicot-Cartsonis & Alexis Cervantes & Benjamin Deneen & Andrew K. Dunn & Theresa A. Jones & , 2023. "Subventricular zone cytogenesis provides trophic support for neural repair in a mouse model of stroke," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Trenton Smith, 2009. "Reconciling psychology with economics: Obesity, behavioral biology, and rational overeating," Journal of Bioeconomics, Springer, vol. 11(3), pages 249-282, December.
    6. Jonas Engesser & Robin Khatri & Darius P. Schaub & Yu Zhao & Hans-Joachim Paust & Zeba Sultana & Nariaki Asada & Jan-Hendrik Riedel & Varshi Sivayoganathan & Anett Peters & Anna Kaffke & Saskia-Lariss, 2024. "Immune profiling-based targeting of pathogenic T cells with ustekinumab in ANCA-associated glomerulonephritis," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    7. Myung Chung & Katsutoshi Imanaka & Ziyan Huang & Akiyuki Watarai & Mu-Yun Wang & Kentaro Tao & Hirotaka Ejima & Tomomi Aida & Guoping Feng & Teruhiro Okuyama, 2024. "Conditional knockout of Shank3 in the ventral CA1 by quantitative in vivo genome-editing impairs social memory in mice," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Shaan Khurshid & Julieta Lazarte & James P. Pirruccello & Lu-Chen Weng & Seung Hoan Choi & Amelia W. Hall & Xin Wang & Samuel F. Friedman & Victor Nauffal & Kiran J. Biddinger & Krishna G. Aragam & Pu, 2023. "Clinical and genetic associations of deep learning-derived cardiac magnetic resonance-based left ventricular mass," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    9. Dixon, Padraig & Hollingworth, William & Harrison, Sean & Davies, Neil M. & Davey Smith, George, 2020. "Mendelian Randomization analysis of the causal effect of adiposity on hospital costs," Journal of Health Economics, Elsevier, vol. 70(C).
    10. Cecilia Pessoa Rodrigues & Aindrila Chatterjee & Meike Wiese & Thomas Stehle & Witold Szymanski & Maria Shvedunova & Asifa Akhtar, 2021. "Histone H4 lysine 16 acetylation controls central carbon metabolism and diet-induced obesity in mice," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    11. Jordi Manuello & Joosung Min & Paul McCarthy & Fidel Alfaro-Almagro & Soojin Lee & Stephen Smith & Lloyd T. Elliott & Anderson M. Winkler & Gwenaëlle Douaud, 2024. "The effects of genetic and modifiable risk factors on brain regions vulnerable to ageing and disease," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    12. Wei Zhao & Erin B. Ware & Zihuai He & Sharon L. R. Kardia & Jessica D. Faul & Jennifer A. Smith, 2017. "Interaction between Social/Psychosocial Factors and Genetic Variants on Body Mass Index: A Gene-Environment Interaction Analysis in a Longitudinal Setting," IJERPH, MDPI, vol. 14(10), pages 1-17, September.
    13. Jie Huang & Jennifer E. Huffman & Yunfeng Huang & Ítalo Valle & Themistocles L. Assimes & Sridharan Raghavan & Benjamin F. Voight & Chang Liu & Albert-László Barabási & Rose D. L. Huang & Qin Hui & Xu, 2022. "Genomics and phenomics of body mass index reveals a complex disease network," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    14. Kristina M. Garske & Asha Kar & Caroline Comenho & Brunilda Balliu & David Z. Pan & Yash V. Bhagat & Gregory Rosenberg & Amogha Koka & Sankha Subhra Das & Zong Miao & Janet S. Sinsheimer & Jaakko Kapr, 2023. "Increased body mass index is linked to systemic inflammation through altered chromatin co-accessibility in human preadipocytes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Davide Pisu & Luana Johnston & Joshua T. Mattila & David G. Russell, 2024. "The frequency of CD38+ alveolar macrophages correlates with early control of M. tuberculosis in the murine lung," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    16. Kaya J. E. Matson & Daniel E. Russ & Claudia Kathe & Isabelle Hua & Dragan Maric & Yi Ding & Jonathan Krynitsky & Randall Pursley & Anupama Sathyamurthy & Jordan W. Squair & Boaz P. Levi & Gregoire Co, 2022. "Single cell atlas of spinal cord injury in mice reveals a pro-regenerative signature in spinocerebellar neurons," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    17. Sheng Wang & Hyunseung Kang, 2022. "Weak‐instrument robust tests in two‐sample summary‐data Mendelian randomization," Biometrics, The International Biometric Society, vol. 78(4), pages 1699-1713, December.
    18. Samuel Baker & Pietro Biroli & Hans van Kippersluis & Stephanie von Hinke, 2022. "Beyond Barker: Infant Mortality at Birth and Ischaemic Heart Disease in Older Age," Bristol Economics Discussion Papers 22/765, School of Economics, University of Bristol, UK.
    19. Parsa Akbari & Olukayode A. Sosina & Jonas Bovijn & Karl Landheer & Jonas B. Nielsen & Minhee Kim & Senem Aykul & Tanima De & Mary E. Haas & George Hindy & Nan Lin & Ian R. Dinsmore & Jonathan Z. Luo , 2022. "Multiancestry exome sequencing reveals INHBE mutations associated with favorable fat distribution and protection from diabetes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    20. Viinikainen, Jutta & Bryson, Alex & Böckerman, Petri & Kari, Jaana T. & Lehtimäki, Terho & Raitakari, Olli & Viikari, Jorma & Pehkonen, Jaakko, 2022. "Does better education mitigate risky health behavior? A mendelian randomization study," Economics & Human Biology, Elsevier, vol. 46(C).

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46589-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.