IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32230-2.html
   My bibliography  Save this article

Pregnancy-induced maternal microchimerism shapes neurodevelopment and behavior in mice

Author

Listed:
  • Steven Schepanski

    (University Medical Center Hamburg-Eppendorf
    University Medical Center Hamburg-Eppendorf)

  • Mattia Chini

    (University Medical Center Hamburg-Eppendorf)

  • Veronika Sternemann

    (University Medical Center Hamburg-Eppendorf
    University Medical Center Hamburg-Eppendorf)

  • Christopher Urbschat

    (University Medical Center Hamburg-Eppendorf)

  • Kristin Thiele

    (University Medical Center Hamburg-Eppendorf)

  • Ting Sun

    (University Medical Center Hamburg-Eppendorf
    Max Planck Institute for Multidisciplinary Sciences)

  • Yu Zhao

    (University Medical Center Hamburg-Eppendorf)

  • Mareike Poburski

    (University Medical Center Hamburg-Eppendorf
    University Medical Center Hamburg-Eppendorf)

  • Anna Woestemeier

    (University Medical Center Hamburg-Eppendorf)

  • Marie-Theres Thieme

    (University Medical Center Hamburg-Eppendorf)

  • Dimitra E. Zazara

    (University Medical Center Hamburg-Eppendorf)

  • Malik Alawi

    (University Medical Center Hamburg-Eppendorf)

  • Nicole Fischer

    (University Medical Center Hamburg-Eppendorf)

  • Joerg Heeren

    (University Medical Center Hamburg-Eppendorf)

  • Nikita Vladimirov

    (Max Delbrück Center for Molecular Medicine)

  • Andrew Woehler

    (Max Delbrück Center for Molecular Medicine)

  • Victor G. Puelles

    (University Medical Center Hamburg-Eppendorf)

  • Stefan Bonn

    (University Medical Center Hamburg-Eppendorf)

  • Nicola Gagliani

    (University Medical Center Hamburg-Eppendorf)

  • Ileana L. Hanganu-Opatz

    (University Medical Center Hamburg-Eppendorf)

  • Petra C. Arck

    (University Medical Center Hamburg-Eppendorf)

Abstract

Life-long brain function and mental health are critically determined by developmental processes occurring before birth. During mammalian pregnancy, maternal cells are transferred to the fetus. They are referred to as maternal microchimeric cells (MMc). Among other organs, MMc seed into the fetal brain, where their function is unknown. Here, we show that, in the offspring’s developing brain in mice, MMc express a unique signature of sensome markers, control microglia homeostasis and prevent excessive presynaptic elimination. Further, MMc facilitate the oscillatory entrainment of developing prefrontal-hippocampal circuits and support the maturation of behavioral abilities. Our findings highlight that MMc are not a mere placental leak out, but rather a functional mechanism that shapes optimal conditions for healthy brain function later in life.

Suggested Citation

  • Steven Schepanski & Mattia Chini & Veronika Sternemann & Christopher Urbschat & Kristin Thiele & Ting Sun & Yu Zhao & Mareike Poburski & Anna Woestemeier & Marie-Theres Thieme & Dimitra E. Zazara & Ma, 2022. "Pregnancy-induced maternal microchimerism shapes neurodevelopment and behavior in mice," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32230-2
    DOI: 10.1038/s41467-022-32230-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32230-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-32230-2?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. Ayal Ben-Zvi & Baptiste Lacoste & Esther Kur & Benjamin J. Andreone & Yoav Mayshar & Han Yan & Chenghua Gu, 2014. "Mfsd2a is critical for the formation and function of the blood–brain barrier," Nature, Nature, vol. 509(7501), pages 507-511, May.
    2. Elisa Gomez Perdiguero & Kay Klapproth & Christian Schulz & Katrin Busch & Emanuele Azzoni & Lucile Crozet & Hannah Garner & Celine Trouillet & Marella F. de Bruijn & Frederic Geissmann & Hans-Reimer , 2015. "Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors," Nature, Nature, vol. 518(7540), pages 547-551, February.
    3. Helen E. Vuong & Geoffrey N. Pronovost & Drake W. Williams & Elena J. L. Coley & Emily L. Siegler & Austin Qiu & Maria Kazantsev & Chantel J. Wilson & Tomiko Rendon & Elaine Y. Hsiao, 2020. "The maternal microbiome modulates fetal neurodevelopment in mice," Nature, Nature, vol. 586(7828), pages 281-286, October.
    4. Patrick Bateson & David Barker & Timothy Clutton-Brock & Debal Deb & Bruno D'Udine & Robert A. Foley & Peter Gluckman & Keith Godfrey & Tom Kirkwood & Marta Mirazón Lahr & John McNamara & Neil B. Metc, 2004. "Developmental plasticity and human health," Nature, Nature, vol. 430(6998), pages 419-421, July.
    5. Timothy Spellman & Mattia Rigotti & Susanne E. Ahmari & Stefano Fusi & Joseph A. Gogos & Joshua A. Gordon, 2015. "Hippocampal–prefrontal input supports spatial encoding in working memory," Nature, Nature, vol. 522(7556), pages 309-314, June.
    6. C. Stremmel & R. Schuchert & F. Wagner & R. Thaler & T. Weinberger & R. Pick & E. Mass & H. C. Ishikawa-Ankerhold & A. Margraf & S. Hutter & R. Vagnozzi & S. Klapproth & J. Frampton & S. Yona & C. Sch, 2018. "Author Correction: Yolk sac macrophage progenitors traffic to the embryo during defined stages of development," Nature Communications, Nature, vol. 9(1), pages 1-3, December.
    7. C. Stremmel & R. Schuchert & F. Wagner & R. Thaler & T. Weinberger & R. Pick & E. Mass & H. C. Ishikawa-Ankerhold & A. Margraf & S. Hutter & R. Vagnozzi & S. Klapproth & J. Frampton & S. Yona & C. Sch, 2018. "Yolk sac macrophage progenitors traffic to the embryo during defined stages of development," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    8. Ina Annelies Stelzer & Christopher Urbschat & Steven Schepanski & Kristin Thiele & Ioanna Triviai & Agnes Wieczorek & Malik Alawi & Denise Ohnezeit & Julian Kottlau & Jiabin Huang & Nicole Fischer & H, 2021. "Vertically transferred maternal immune cells promote neonatal immunity against early life infections," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Nikita Vladimirov & Fabian F. Voigt & Thomas Naert & Gabriela R. Araujo & Ruiyao Cai & Anna Maria Reuss & Shan Zhao & Patricia Schmid & Sven Hildebrand & Martina Schaettin & Dominik Groos & José María, 2024. "Benchtop mesoSPIM: a next-generation open-source light-sheet microscope for cleared samples," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    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. Xiaowei Gu & Anna Heinrich & Shu-Yun Li & Tony DeFalco, 2023. "Testicular macrophages are recruited during a narrow fetal time window and promote organ-specific developmental functions," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Fabrizio Sergio & Giacomo Tavecchia & Julio Blas & Alessandro Tanferna & Fernando Hiraldo & Erkki Korpimaki & Steven R. Beissinger, 2022. "Hardship at birth alters the impact of climate change on a long-lived predator," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Huee Ru Chong & Yadollah Ranjbar-Slamloo & Malcolm Zheng Hao Ho & Xuan Ouyang & Tsukasa Kamigaki, 2023. "Functional alterations of the prefrontal circuit underlying cognitive aging in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Kevin Boyé & Luiz Henrique Geraldo & Jessica Furtado & Laurence Pibouin-Fragner & Mathilde Poulet & Doyeun Kim & Bryce Nelson & Yunling Xu & Laurent Jacob & Nawal Maissa & Dritan Agalliu & Lena Claess, 2022. "Endothelial Unc5B controls blood-brain barrier integrity," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Shige Song, 2013. "Prenatal malnutrition and subsequent foetal loss risk: Evidence from the 1959-1961 Chinese famine," Demographic Research, Max Planck Institute for Demographic Research, Rostock, Germany, vol. 29(26), pages 707-728.
    7. Shuhui Wang & Kun Wang & Kangkang Song & Zon Weng Lai & Pengfei Li & Dongying Li & Yajie Sun & Ye Mei & Chen Xu & Maofu Liao, 2024. "Structures of the Mycobacterium tuberculosis efflux pump EfpA reveal the mechanisms of transport and inhibition," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Aguilar, Arturo & Vicarelli, Marta, 2022. "El Niño and children: Medium-term effects of early-life weather shocks on cognitive and health outcomes," World Development, Elsevier, vol. 150(C).
    9. Quaranta, Luciana, 2014. "Early life effects across the life course: The impact of individually defined exogenous measures of disease exposure on mortality by sex in 19th- and 20th-century Southern Sweden," Social Science & Medicine, Elsevier, vol. 119(C), pages 266-273.
    10. van Dijk, Ingrid K. & Nilsson, Therese & Quaranta, Luciana, 2024. "Disease exposure in infancy affects women's reproductive outcomes and offspring health in southern Sweden 1905–2000," Social Science & Medicine, Elsevier, vol. 347(C).
    11. Song, Shige, 2013. "Identifying the intergenerational effects of the 1959–1961 Chinese Great Leap Forward Famine on infant mortality," Economics & Human Biology, Elsevier, vol. 11(4), pages 474-487.
    12. Yoav Printz & Pritish Patil & Mathias Mahn & Asaf Benjamin & Anna Litvin & Rivka Levy & Max Bringmann & Ofer Yizhar, 2023. "Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Yann Vanrobaeys & Utsav Mukherjee & Lucy Langmack & Stacy E. Beyer & Ethan Bahl & Li-Chun Lin & Jacob J. Michaelson & Ted Abel & Snehajyoti Chatterjee, 2023. "Mapping the spatial transcriptomic signature of the hippocampus during memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. Paul Gertler & Tadeja Gracner, 2022. "The Sweet Life: The Long-Term Effects of a Sugar-Rich Early Childhood," NBER Working Papers 30799, National Bureau of Economic Research, Inc.
    15. Miki Nagase & Hidetake Kurihara & Atsu Aiba & Morag J Young & Tatsuo Sakai, 2016. "Deletion of Rac1GTPase in the Myeloid Lineage Protects against Inflammation-Mediated Kidney Injury in Mice," PLOS ONE, Public Library of Science, vol. 11(3), pages 1-17, March.
    16. Fanette Fontaine & Sondra Turjeman & Karel Callens & Omry Koren, 2023. "The intersection of undernutrition, microbiome, and child development in the first years of life," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    17. Bhalotra, Sonia & Delavande, Adeline & Font-Gilabert, Paulino & Maselko, Joanna, 2020. "Maternal investments in children: the role of expected effort and returns," ISER Working Paper Series 2020-03, Institute for Social and Economic Research.
    18. Robert Brooks & Alexei Maklakov, 2010. "Sex Differences in Obesity Associated with Total Fertility Rate," PLOS ONE, Public Library of Science, vol. 5(5), pages 1-4, May.
    19. Liang Yong & Yafen Yu & Bao Li & Huiyao Ge & Qi Zhen & Yiwen Mao & Yanxia Yu & Lu Cao & Ruixue Zhang & Zhuo Li & Yirui Wang & Wencheng Fan & Chang Zhang & Daiyue Wang & Sihan Luo & Yuanming Bai & Shir, 2022. "Calcium/calmodulin-dependent protein kinase IV promotes imiquimod-induced psoriatic inflammation via macrophages and keratinocytes in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    20. Chi Nguyen & Hsiang-Ting Lei & Louis Tung Faat Lai & Marc J. Gallenito & Xuelang Mu & Doreen Matthies & Tamir Gonen, 2023. "Lipid flipping in the omega-3 fatty-acid transporter," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    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:13:y:2022:i:1:d:10.1038_s41467-022-32230-2. 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.