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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
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