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

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, Fortunate F. Chifamba, Hannah Hawks-Mayer, Amanda Vernon, Fan Gao, Yong Zhang, Michael J. Holtzman, Myriam Heiman, Mark L. Andermann, Naama Kanarek, Jonathan O. Lipton and Maria K. Lehtinen ()
Additional contact information
Ryann M. Fame: Boston Children’s Hospital and Harvard Medical School
Peter N. Kalugin: Boston Children’s Hospital and 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
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
Hannah Hawks-Mayer: Boston Children’s Hospital
Amanda Vernon: Department of Brain and Cognitive Sciences, MIT
Fan Gao: Department of Brain and Cognitive Sciences, MIT
Yong Zhang: Washington University
Michael J. Holtzman: Washington University
Myriam Heiman: Department of Brain and Cognitive Sciences, MIT
Mark L. Andermann: Harvard Medical School
Naama Kanarek: Boston Children’s Hospital and Harvard Medical School
Jonathan O. Lipton: Boston Children’s Hospital
Maria K. Lehtinen: Boston Children’s Hospital and Harvard Medical School

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-39326-3

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