IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39326-3.html
   My bibliography  Save this article

Defining diurnal fluctuations in mouse choroid plexus and CSF at high molecular, spatial, and temporal resolution

Author

Listed:
  • Ryann M. Fame

    (Boston Children’s Hospital and Harvard Medical School
    Stanford University)

  • Peter N. Kalugin

    (Boston Children’s Hospital and Harvard Medical School
    Harvard Medical School
    Harvard Medical School)

  • Boryana Petrova

    (Boston Children’s Hospital and Harvard Medical School)

  • Huixin Xu

    (Boston Children’s Hospital and Harvard Medical School)

  • Paul A. Soden

    (Boston Children’s Hospital and Harvard Medical School)

  • Frederick B. Shipley

    (Boston Children’s Hospital and Harvard Medical School
    Harvard University)

  • Neil Dani

    (Boston Children’s Hospital and Harvard Medical School)

  • Bradford Grant

    (Boston Children’s Hospital and Harvard Medical School)

  • Aja Pragana

    (Boston Children’s Hospital and Harvard Medical School)

  • Joshua P. Head

    (Boston Children’s Hospital and Harvard Medical School)

  • Suhasini Gupta

    (Boston Children’s Hospital and Harvard Medical School)

  • Morgan L. Shannon

    (Boston Children’s Hospital and Harvard Medical School)

  • Fortunate F. Chifamba

    (Boston Children’s Hospital
    Harvard Medical School)

  • Hannah Hawks-Mayer

    (Boston Children’s Hospital
    Harvard Medical School)

  • Amanda Vernon

    (Department of Brain and Cognitive Sciences, MIT
    Picower Institute for Learning and Memory
    Broad Institute of MIT and Harvard)

  • Fan Gao

    (Department of Brain and Cognitive Sciences, MIT
    Picower Institute for Learning and Memory
    Broad Institute of MIT and Harvard
    Lyterian Therapeutics)

  • Yong Zhang

    (Washington University)

  • Michael J. Holtzman

    (Washington University)

  • Myriam Heiman

    (Department of Brain and Cognitive Sciences, MIT
    Picower Institute for Learning and Memory
    Broad Institute of MIT and Harvard)

  • Mark L. Andermann

    (Harvard Medical School
    Harvard University
    Beth Israel Deaconess Medical Center)

  • Naama Kanarek

    (Boston Children’s Hospital and Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Jonathan O. Lipton

    (Boston Children’s Hospital
    Harvard Medical School)

  • Maria K. Lehtinen

    (Boston Children’s Hospital and Harvard Medical School
    Harvard Medical School
    Harvard University
    Broad Institute of MIT and Harvard)

Abstract

Transmission and secretion of signals via the choroid plexus (ChP) brain barrier can modulate brain states via regulation of cerebrospinal fluid (CSF) composition. Here, we developed a platform to analyze diurnal variations in male mouse ChP and CSF. Ribosome profiling of ChP epithelial cells revealed diurnal translatome differences in metabolic machinery, secreted proteins, and barrier components. Using ChP and CSF metabolomics and blood-CSF barrier analyses, we observed diurnal changes in metabolites and cellular junctions. We then focused on transthyretin (TTR), a diurnally regulated thyroid hormone chaperone secreted by the ChP. Diurnal variation in ChP TTR depended on Bmal1 clock gene expression. We achieved real-time tracking of CSF-TTR in awake TtrmNeonGreen mice via multi-day intracerebroventricular fiber photometry. Diurnal changes in ChP and CSF TTR levels correlated with CSF thyroid hormone levels. These datasets highlight an integrated platform for investigating diurnal control of brain states by the ChP and CSF.

Suggested Citation

  • Ryann M. Fame & Peter N. Kalugin & Boryana Petrova & Huixin Xu & Paul A. Soden & Frederick B. Shipley & Neil Dani & Bradford Grant & Aja Pragana & Joshua P. Head & Suhasini Gupta & Morgan L. Shannon &, 2023. "Defining diurnal fluctuations in mouse choroid plexus and CSF at high molecular, spatial, and temporal resolution," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39326-3
    DOI: 10.1038/s41467-023-39326-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39326-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39326-3?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. Lauren M. Hablitz & Virginia Plá & Michael Giannetto & Hanna S. Vinitsky & Frederik Filip Stæger & Tanner Metcalfe & Rebecca Nguyen & Abdellatif Benrais & Maiken Nedergaard, 2020. "Circadian control of brain glymphatic and lymphatic fluid flow," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    2. Inmaculada Martínez-Reyes & Navdeep S. Chandel, 2020. "Mitochondrial TCA cycle metabolites control physiology and disease," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Jihwan Myung & Christoph Schmal & Sungho Hong & Yoshiaki Tsukizawa & Pia Rose & Yong Zhang & Michael J. Holtzman & Erik De Schutter & Hanspeter Herzel & Grigory Bordyugov & Toru Takumi, 2018. "The choroid plexus is an important circadian clock component," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    4. Nan Yang & Jack Williams & Vanja Pekovic-Vaughan & Pengbo Wang & Safiah Olabi & James McConnell & Nicole Gossan & Alun Hughes & Julia Cheung & Charles H. Streuli & Qing-Jun Meng, 2017. "Cellular mechano-environment regulates the mammary circadian clock," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    5. 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.
    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. 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.
    2. Tuğçe Beyazay & Kendra S. Belthle & Christophe Farès & Martina Preiner & Joseph Moran & William F. Martin & Harun Tüysüz, 2023. "Ambient temperature CO2 fixation to pyruvate and subsequently to citramalate over iron and nickel nanoparticles," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Per Kristian Eide & Aslan Lashkarivand & Are Pripp & Lars Magnus Valnes & Markus Herberg Hovd & Geir Ringstad & Kaj Blennow & Henrik Zetterberg, 2023. "Plasma neurodegeneration biomarker concentrations associate with glymphatic and meningeal lymphatic measures in neurological disorders," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Rania El-Botty & Ludivine Morriset & Elodie Montaudon & Zakia Tariq & Anne Schnitzler & Marina Bacci & Nicla Lorito & Laura Sourd & Léa Huguet & Ahmed Dahmani & Pierre Painsec & Heloise Derrien & Soph, 2023. "Oxidative phosphorylation is a metabolic vulnerability of endocrine therapy and palbociclib resistant metastatic breast cancers," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Hao Wu & Xiufeng Zhao & Sophia M. Hochrein & Miriam Eckstein & Gabriela F. Gubert & Konrad Knöpper & Ana Maria Mansilla & Arman Öner & Remi Doucet-Ladevèze & Werner Schmitz & Bart Ghesquière & Sebasti, 2023. "Mitochondrial dysfunction promotes the transition of precursor to terminally exhausted T cells through HIF-1α-mediated glycolytic reprogramming," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Marine Lanfranchi & Sozerko Yandiev & Géraldine Meyer-Dilhet & Salma Ellouze & Martijn Kerkhofs & Raphael Dos Reis & Audrey Garcia & Camille Blondet & Alizée Amar & Anita Kneppers & Hélène Polvèche & , 2024. "The AMPK-related kinase NUAK1 controls cortical axons branching by locally modulating mitochondrial metabolic functions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Cesare Granata & Nikeisha J. Caruana & Javier Botella & Nicholas A. Jamnick & Kevin Huynh & Jujiao Kuang & Hans A. Janssen & Boris Reljic & Natalie A. Mellett & Adrienne Laskowski & Tegan L. Stait & A, 2021. "High-intensity training induces non-stoichiometric changes in the mitochondrial proteome of human skeletal muscle without reorganisation of respiratory chain content," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    8. 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.
    9. Tao Zhang & Sarah E. Noll & Jesus T. Peng & Amman Klair & Abigail Tripka & Nathan Stutzman & Casey Cheng & Richard N. Zare & Alexandra J. Dickinson, 2023. "Chemical imaging reveals diverse functions of tricarboxylic acid metabolites in root growth and development," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    10. Chujiao Lin & Qiyuan Yang & Dongsheng Guo & Jun Xie & Yeon-Suk Yang & Sachin Chaugule & Ngoc DeSouza & Won-Taek Oh & Rui Li & Zhihao Chen & Aijaz A. John & Qiang Qiu & Lihua Julie Zhu & Matthew B. Gre, 2022. "Impaired mitochondrial oxidative metabolism in skeletal progenitor cells leads to musculoskeletal disintegration," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Zaher ElBeck & Mohammad Bakhtiar Hossain & Humam Siga & Nikolay Oskolkov & Fredrik Karlsson & Julia Lindgren & Anna Walentinsson & Dominique Koppenhöfer & Rebecca Jarvis & Roland Bürli & Tanguy Jamier, 2024. "Epigenetic modulators link mitochondrial redox homeostasis to cardiac function in a sex-dependent manner," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    12. Le Tran Phuc Khoa & Wentao Yang & Mengrou Shan & Li Zhang & Fengbiao Mao & Bo Zhou & Qiang Li & Rebecca Malcore & Clair Harris & Lili Zhao & Rajesh C. Rao & Shigeki Iwase & Sundeep Kalantry & Stephani, 2024. "Quiescence enables unrestricted cell fate in naive embryonic stem cells," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    13. Susana Lozano-Tovar & Yaneth Rodríguez-Agudelo & David José Dávila-Ortiz de Montellano & Blanca Estela Pérez-Aldana & Alberto Ortega-Vázquez & Nancy Monroy-Jaramillo, 2023. "Relationship between APOE , PER2 , PER3 and OX2R Genetic Variants and Neuropsychiatric Symptoms in Patients with Alzheimer’s Disease," IJERPH, MDPI, vol. 20(5), pages 1-14, March.
    14. Elisabeth Lambert & Ahmad Reza Mehdipour & Alexander Schmidt & Gerhard Hummer & Camilo Perez, 2022. "Evidence for a trap-and-flip mechanism in a proton-dependent lipid transporter," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    15. Xu, Yan & Gu, Changgui & Wang, Jiangsheng & Wang, Man & Wang, Haiying & Yang, Huijie & Song, Yuxuan, 2023. "Goodwin oscillator model explains different response of circadian rhythms to constant light," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 618(C).
    16. Lanqi Gong & Jie Luo & Yu Zhang & Yuma Yang & Shanshan Li & Xiaona Fang & Baifeng Zhang & Jiao Huang & Larry Ka-Yue Chow & Dittman Chung & Jinlin Huang & Cuicui Huang & Qin Liu & Lu Bai & Yuen Chak Ti, 2023. "Nasopharyngeal carcinoma cells promote regulatory T cell development and suppressive activity via CD70-CD27 interaction," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    17. Fabiola Diniz & Nguyen Yen Nhi Ngo & Mariel Colon-Leyva & Francesca Edgington-Giordano & Sylvia Hilliard & Kevin Zwezdaryk & Jiao Liu & Samir S. El-Dahr & Giovane G. Tortelote, 2023. "Acetyl-CoA is a key molecule for nephron progenitor cell pool maintenance," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    18. Debasmita Bhattacharya & Vicky Shah & Oreoluwa Oresajo & Anthony Scimè, 2021. "p107 mediated mitochondrial function controls muscle stem cell proliferative fates," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    19. Benjamin P. Hurrell & Doumet Georges Helou & Emily Howard & Jacob D. Painter & Pedram Shafiei-Jahani & Arlene H. Sharpe & Omid Akbari, 2022. "PD-L2 controls peripherally induced regulatory T cells by maintaining metabolic activity and Foxp3 stability," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Davide G. Franchina & Henry Kurniawan & Melanie Grusdat & Carole Binsfeld & Luana Guerra & Lynn Bonetti & Leticia Soriano-Baguet & Anouk Ewen & Takumi Kobayashi & Sophie Farinelle & Anna Rita Minafra , 2022. "Glutathione-dependent redox balance characterizes the distinct metabolic properties of follicular and marginal zone B cells," Nature Communications, Nature, vol. 13(1), pages 1-21, 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:14:y:2023:i:1:d:10.1038_s41467-023-39326-3. 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.