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

by Fame, Ryann M. , Pragana, Aja , Andermann, Mark L. , Chifamba, Fortunate F. , Soden, Paul A. , Shannon, Morgan L. , Hawks-Mayer, Hannah , Kanarek, Naama , Grant, Bradford , Xu, Huixin , Head, Joshua P. , Lipton, Jonathan O. , Shipley, Frederick B. , Gupta, Suhasini , Kalugin, Peter N. , Vernon, Amanda , Petrova, Boryana , Lehtinen, Maria K. , Heiman, Myriam , Holtzman, Michael J. , Dani, Neil , Gao, Fan , Zhang, Yong

in 13/51 / 14/19 / 147/143 / 38 / 38/35 / 45 / 45/88 / 45/91 / 59 / 59/78 / 631/378/1341 / 631/378/1385/2640 / 631/378/340 / 64/60 / Animals / Biological Transport / Blood / Blood-brain barrier / Blood-Brain Barrier - metabolism / BMAL1 protein / Brain / Brain - metabolism / Cerebrospinal fluid / Choroid plexus / Choroid Plexus - metabolism / Circadian rhythms / Clock gene / Composition / Diurnal variations / Epithelial cells / Epithelium / Gene expression / Humanities and Social Sciences / Male / Metabolites / Metabolomics / Mice / multidisciplinary / Photometry / Prealbumin - genetics / Prealbumin - metabolism / Science / Science (multidisciplinary) / Temporal resolution / Thyroid / Thyroid gland / Thyroid Hormones - metabolism / Time of use / Transthyretin

2023

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

2023

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2023

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Journal Article

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

Fame, Ryann M.,

Pragana, Aja,

Andermann, Mark L.,

Chifamba, Fortunate F.,

Soden, Paul A.,

Shannon, Morgan L.,

Hawks-Mayer, Hannah,

Kanarek, Naama,

Grant, Bradford,

Xu, Huixin,

Head, Joshua P.,

Lipton, Jonathan O.,

Shipley, Frederick B.,

Gupta, Suhasini,

Kalugin, Peter N.,

Vernon, Amanda,

Petrova, Boryana,

Lehtinen, Maria K.,

Heiman, Myriam,

Holtzman, Michael J.,

Dani, Neil,

Gao, Fan,

Zhang, Yong

2023

Overview

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 Ttr mNeonGreen 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. The choroid plexus (ChP) modulates cerebrospinal fluid (CSF) composition and the blood-CSF barrier. Here the authors show that the ChP is a critical circadian component with time-of-day variations in translation, barrier, and metabolism to alter CSF composition.

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Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio

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13/51

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/ 147/143

/ 38

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/ 45

/ 45/88