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Reduction of neuronal activity mediated by blood-vessel regression in the brain

Xiaofei Gao, Jun-Liszt Li, Xingjun Chen, Bo Ci, Fei Chen, Nannan Lu, Bo Shen, Lijun Zheng, Jie-Min Jia, Yating Yi, Shiwen Zhang, Ying-Chao Shi, Kaibin Shi, Nicholas E Propson, Yubin Huang, Katherine Poinsatte, Zhaohuan Zhang, Yuanlei Yue, Dale B Bosco, Ying-mei Lu, Shi-bing Yang, Ralf H. Adams, Volkhard Lindner, Fen Huang, Long-Jun Wu, Hui Zheng, Feng Han, Simon Hippenmeyer, Ann M. Stowe, Bo Peng, Marta Margeta, Xiaoqun Wang, Qiang Liu, Jakob Körbelin, Martin Trepel, Hui Lu, Bo O. Zhou, Hu Zhao, Wenzhi Su, Robert M. Bachoo, View ORCID ProfileWoo-ping Ge
doi: https://doi.org/10.1101/2020.09.15.262782
Xiaofei Gao
1Children’s Research Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
2Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA
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Jun-Liszt Li
3Chinese Institute for Brain Research, Beijing, Beijing 102206, China
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Xingjun Chen
3Chinese Institute for Brain Research, Beijing, Beijing 102206, China
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Bo Ci
1Children’s Research Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
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Fei Chen
1Children’s Research Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
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Nannan Lu
1Children’s Research Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
4Institute of Pharmacology and Toxicology, College of Pharmaceutical Sciences, Zhejiang University, Hangzhou 310058, China
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Bo Shen
1Children’s Research Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
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Lijun Zheng
3Chinese Institute for Brain Research, Beijing, Beijing 102206, China
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Jie-Min Jia
1Children’s Research Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
5School of Life Sciences, Westlake University, Hangzhou 310024, China
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Yating Yi
6Department of Restorative Sciences, School of Dentistry, Texas A&M University, Dallas, TX, 75246, USA
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Shiwen Zhang
6Department of Restorative Sciences, School of Dentistry, Texas A&M University, Dallas, TX, 75246, USA
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Ying-Chao Shi
7State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Beijing MRI Centre for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing Institute for Brain Disorders, Beijing 100101, China
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Kaibin Shi
8Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, AZ 85013, USA
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Nicholas E Propson
9Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA
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Yubin Huang
10Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
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Katherine Poinsatte
11Department of Neurology and Neurotherapeutics, UT Southwestern Medical Center, Dallas, TX75390, USA
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Zhaohuan Zhang
1Children’s Research Institute, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
12Department of Neurology, Changzheng Hospital, Second Military Medical University, Shanghai 200003, China
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Yuanlei Yue
13GW Institute for Neuroscience, the George Washington University, Washington, DC 20037, USA
14Department of Pharmacology and Physiology, School of Medicine and Health Sciences, The George Washington University, Washington, DC 20037, USA
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Dale B Bosco
15Department of Neurology, Mayo Clinic, Rochester, MN 55905, USA
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Ying-mei Lu
16Department of Physiology, School of Basic Medical Sciences, Nanjing Medical University, Nanjing, China
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Shi-bing Yang
17Departments of Physiology, Biochemistry and Biophysics, University of California at San Francisco, CA94158, USA
18Institute of Biomedical Sciences, Academia Sinica, Taipei 115, Taiwan
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Ralf H. Adams
19Department of Tissue Morphogenesis, Max-Planck-Institute for Molecular Biomedicine, and Faculty of Medicine, University of Münster, D-48149 Münster, Germany
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Volkhard Lindner
20Center for Molecular Medicine, Maine Medical Center Research Institute, Scarborough, ME04074, United States
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Fen Huang
17Departments of Physiology, Biochemistry and Biophysics, University of California at San Francisco, CA94158, USA
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Long-Jun Wu
15Department of Neurology, Mayo Clinic, Rochester, MN 55905, USA
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Hui Zheng
9Huffington Center on Aging, Baylor College of Medicine, Houston, TX 77030, USA
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Feng Han
21Key Laboratory of Cardiovascular & Cerebrovascular Medicine, School of Pharmacy, Nanjing Medical University, Nanjing 211166, China
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Simon Hippenmeyer
22Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
23Department of Biology, Stanford University, Stanford, CA94305, USA
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Ann M. Stowe
11Department of Neurology and Neurotherapeutics, UT Southwestern Medical Center, Dallas, TX75390, USA
24Neurology, University of Kentucky, Lexington, KY 40536, USA
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Bo Peng
10Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
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Marta Margeta
25Department of Pathology, University of California at San Francisco, CA 94143, USA
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Xiaoqun Wang
7State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Beijing MRI Centre for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing Institute for Brain Disorders, Beijing 100101, China
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Qiang Liu
8Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, AZ 85013, USA
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Jakob Körbelin
26Department of Oncology, Hematology and Bone Marrow Transplantation, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
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Martin Trepel
27Department of Hematology and Clinical Oncology, University Medical Center Augsburg, Augsburg 86156, Germany
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Hui Lu
13GW Institute for Neuroscience, the George Washington University, Washington, DC 20037, USA
14Department of Pharmacology and Physiology, School of Medicine and Health Sciences, The George Washington University, Washington, DC 20037, USA
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Bo O. Zhou
28State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences; University of Chinese Academy of Sciences, Shanghai 200031, China
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Hu Zhao
6Department of Restorative Sciences, School of Dentistry, Texas A&M University, Dallas, TX, 75246, USA
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Wenzhi Su
3Chinese Institute for Brain Research, Beijing, Beijing 102206, China
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Robert M. Bachoo
2Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA
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Woo-ping Ge
3Chinese Institute for Brain Research, Beijing, Beijing 102206, China
29Children’s Research Institute, Department of Pediatrics and Neuroscience, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA
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  • ORCID record for Woo-ping Ge
  • For correspondence: woopingge@cibr.ac.cn
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Summary

The brain vasculature supplies neurons with glucose and oxygen, but little is known about how vascular plasticity contributes to brain function. Using longitudinal in vivo imaging, we reported that a substantial proportion of blood vessels in the adult brain sporadically occluded and regressed. Their regression proceeded through sequential stages of blood-flow occlusion, endothelial cell collapse, relocation or loss of pericytes, and retraction of glial endfeet. Regressing vessels were found to be widespread in mouse, monkey and human brains. Both brief occlusions of the middle cerebral artery and lipopolysaccharide-mediated inflammation induced an increase of vessel regression. Blockage of leukocyte adhesion to endothelial cells alleviated LPS-induced vessel regression. We further revealed that blood vessel regression caused a reduction of neuronal activity due to a dysfunction in mitochondrial metabolism and glutamate production. Our results elucidate the mechanism of vessel regression and its role in neuronal function in the adult brain.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Reduction of neuronal activity mediated by blood-vessel regression in the brain
Xiaofei Gao, Jun-Liszt Li, Xingjun Chen, Bo Ci, Fei Chen, Nannan Lu, Bo Shen, Lijun Zheng, Jie-Min Jia, Yating Yi, Shiwen Zhang, Ying-Chao Shi, Kaibin Shi, Nicholas E Propson, Yubin Huang, Katherine Poinsatte, Zhaohuan Zhang, Yuanlei Yue, Dale B Bosco, Ying-mei Lu, Shi-bing Yang, Ralf H. Adams, Volkhard Lindner, Fen Huang, Long-Jun Wu, Hui Zheng, Feng Han, Simon Hippenmeyer, Ann M. Stowe, Bo Peng, Marta Margeta, Xiaoqun Wang, Qiang Liu, Jakob Körbelin, Martin Trepel, Hui Lu, Bo O. Zhou, Hu Zhao, Wenzhi Su, Robert M. Bachoo, Woo-ping Ge
bioRxiv 2020.09.15.262782; doi: https://doi.org/10.1101/2020.09.15.262782
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Reduction of neuronal activity mediated by blood-vessel regression in the brain
Xiaofei Gao, Jun-Liszt Li, Xingjun Chen, Bo Ci, Fei Chen, Nannan Lu, Bo Shen, Lijun Zheng, Jie-Min Jia, Yating Yi, Shiwen Zhang, Ying-Chao Shi, Kaibin Shi, Nicholas E Propson, Yubin Huang, Katherine Poinsatte, Zhaohuan Zhang, Yuanlei Yue, Dale B Bosco, Ying-mei Lu, Shi-bing Yang, Ralf H. Adams, Volkhard Lindner, Fen Huang, Long-Jun Wu, Hui Zheng, Feng Han, Simon Hippenmeyer, Ann M. Stowe, Bo Peng, Marta Margeta, Xiaoqun Wang, Qiang Liu, Jakob Körbelin, Martin Trepel, Hui Lu, Bo O. Zhou, Hu Zhao, Wenzhi Su, Robert M. Bachoo, Woo-ping Ge
bioRxiv 2020.09.15.262782; doi: https://doi.org/10.1101/2020.09.15.262782

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