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3D-imaging reveals conserved cerebrospinal fluid drainage via meningeal lymphatic vasculature in mice and humans

View ORCID ProfileLaurent Jacob, Jose de Brito Neto, Stephanie Lenck, Celine Corcy, Farhat Benbelkacem, View ORCID ProfileLuiz Henrique Geraldo, Yunling Xu, Jean-Mickael Thomas, Marie-Renee El Kamouh, View ORCID ProfileMarie-Claude Potier, Stephane Haik, Stephane Lehericy, Anne Eichmann, Jean-Leon Thomas
doi: https://doi.org/10.1101/2022.01.13.476230
Laurent Jacob
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
2Université de Paris, PARCC, INSERM, F-75006 Paris, France
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  • ORCID record for Laurent Jacob
Jose de Brito Neto
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
3Biomedical Sciences Institute, Federal University of Rio de Janeiro, 21941-590, Brazil
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Stephanie Lenck
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
4Department of Neuroradiology, Pitie-Salpêtrière Hospital, Sorbonne University, Paris
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Celine Corcy
4Department of Neuroradiology, Pitie-Salpêtrière Hospital, Sorbonne University, Paris
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Farhat Benbelkacem
5Siemens Healthcare SAS, 40 Avenue des Fruitiers, 93527 Saint-Denis Cedex France
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Luiz Henrique Geraldo
2Université de Paris, PARCC, INSERM, F-75006 Paris, France
6Cardiovascular Research Center, Department of Internal Medicine, Yale University School of Medicine, New Haven CT 06511, USA
7Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06511, USA
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Yunling Xu
2Université de Paris, PARCC, INSERM, F-75006 Paris, France
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Jean-Mickael Thomas
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
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Marie-Renee El Kamouh
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
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Marie-Claude Potier
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
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Stephane Haik
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
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Stephane Lehericy
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
4Department of Neuroradiology, Pitie-Salpêtrière Hospital, Sorbonne University, Paris
8CENIR – Centre for NeuroImaging Research, ICM - Institut du Cerveau et de la Moelle épinière, 47 bd de l’Hôpital, 75013 Paris, France
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Anne Eichmann
2Université de Paris, PARCC, INSERM, F-75006 Paris, France
6Cardiovascular Research Center, Department of Internal Medicine, Yale University School of Medicine, New Haven CT 06511, USA
7Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06511, USA
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  • For correspondence: jeanleon.thomas@icm-institute.org anne.eichmann@inserm.fr
Jean-Leon Thomas
1Sorbonne Université, Inserm, CNRS, Institut du Cerveau, Pitié-Salpêtrière Hospital, 75013 Paris, France
9Department of Neurology, Yale University School of Medicine, New Haven, CT 06511, USA
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  • For correspondence: jeanleon.thomas@icm-institute.org anne.eichmann@inserm.fr
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Abstract

Meningeal lymphatic vessels (MLVs) contribute to waste product elimination and immune surveillance in brain tissues. MLVs were identified in the dorsal and caudo-basal regions of the dura mater, where they ensure the clearance of cerebrospinal fluid (CSF). Whether MLVs exist in the complex anterior part of the murine and human skull, and how they connect with the glymphatic system and extracranial lymphatic vasculature remained unclear. Here, we generated three-dimensional (3D) maps of MLV drainage by light-sheet fluorescence microscopy (LSFM) imaging of mouse whole-head preparations following fluorescent OVA-A555 tracer injections into the CSF. In humans, we performed real-time magnetic resonance vessel wall imaging (MR-VWI) after systemic gadobutrol injections. We observed a conserved 3D-anatomy of MLVs in mice and humans, and we discovered an extended anterior network around the dural cavernous sinus including multiple capillary beds and exit routes through the foramina of emissary veins. MR-VWI may provide a diagnostic tool for patients with CSF drainage defects and neurological diseases.

Short abstract We established the 3D-anatomy of meningeal lymphatic vasculature and associated CSF drainage by postmortem light-sheet imaging in mice and by real-time magnetic resonance imaging in humans, demonstrating conserved lymphatic circuitries in contact with dural venous sinuses.

Competing Interest Statement

The authors have declared no competing interest.

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Posted January 17, 2022.
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3D-imaging reveals conserved cerebrospinal fluid drainage via meningeal lymphatic vasculature in mice and humans
Laurent Jacob, Jose de Brito Neto, Stephanie Lenck, Celine Corcy, Farhat Benbelkacem, Luiz Henrique Geraldo, Yunling Xu, Jean-Mickael Thomas, Marie-Renee El Kamouh, Marie-Claude Potier, Stephane Haik, Stephane Lehericy, Anne Eichmann, Jean-Leon Thomas
bioRxiv 2022.01.13.476230; doi: https://doi.org/10.1101/2022.01.13.476230
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3D-imaging reveals conserved cerebrospinal fluid drainage via meningeal lymphatic vasculature in mice and humans
Laurent Jacob, Jose de Brito Neto, Stephanie Lenck, Celine Corcy, Farhat Benbelkacem, Luiz Henrique Geraldo, Yunling Xu, Jean-Mickael Thomas, Marie-Renee El Kamouh, Marie-Claude Potier, Stephane Haik, Stephane Lehericy, Anne Eichmann, Jean-Leon Thomas
bioRxiv 2022.01.13.476230; doi: https://doi.org/10.1101/2022.01.13.476230

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