A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury

Abstract Background The brain vascular basement membrane (brain-VBM) is an important component of the brain extracellular matrix, and the three-dimensional structure of the cerebrovascular network nested with many cell-adhesive proteins may provide guidance for brain tissue regeneration. However, th...

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Main Authors: Wanqing Ji, Zhiru Wu, Jiaming Wen, Hengxin Tang, Zhuopeng Chen, Bo Xue, Zhenming Tian, Yueyang Ba, Ning Zhang, Xuejun Wen, Bo Hou
Format: Article
Language:English
Published: American Association for the Advancement of Science (AAAS) 2023-01-01
Series:Biomaterials Research
Subjects:
Online Access:https://doi.org/10.1186/s40824-023-00341-6
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author Wanqing Ji
Zhiru Wu
Jiaming Wen
Hengxin Tang
Zhuopeng Chen
Bo Xue
Zhenming Tian
Yueyang Ba
Ning Zhang
Xuejun Wen
Bo Hou
author_facet Wanqing Ji
Zhiru Wu
Jiaming Wen
Hengxin Tang
Zhuopeng Chen
Bo Xue
Zhenming Tian
Yueyang Ba
Ning Zhang
Xuejun Wen
Bo Hou
author_sort Wanqing Ji
collection DOAJ
description Abstract Background The brain vascular basement membrane (brain-VBM) is an important component of the brain extracellular matrix, and the three-dimensional structure of the cerebrovascular network nested with many cell-adhesive proteins may provide guidance for brain tissue regeneration. However, the potential of ability of brain-VBM to promote neural tissue regeneration has not been examined due to the technical difficulty of isolating intact brain-VBM. Methods The present study developed a simple, effective method to isolate structurally and compositionally intact brain-VBM. Structural and component properties of the brain-VBM were characterized to confirm the technique. Seed cells were cocultured with brain-VBM in vitro to analyze biocompatibility and neurite extension. An experimental rat model of focal traumatic brain injury (TBI) induced by controlled cortical impact were conducted to further test the tissue regeneration ability of brain-VBM. Results Brain-VBM isolated using genipin showed significantly improved mechanical properties, was easy to handle, supported high cell viability, exhibited strong cell adhesive properties, and promoted neurite extension and outgrowth. Further testing of the isolated brain-VBM transplanted at lesion sites in an experimental rat model of focal TBI demonstrated considerable promise for reconstructing a complete blood vessel network that filled in the lesion cavity and promoting repopulation of neural progenitor cells and neurons. Conclusion The technique allows isolation of intact brain-VBM as a 3D microvascular scaffold to support brain tissue regeneration following TBI and shows considerable promise for the production of naturally-derived biomaterials for neural tissue engineering. Graphical Abstract
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spelling doaj.art-93909d05eb5942c8848000582881c3832024-03-02T18:38:41ZengAmerican Association for the Advancement of Science (AAAS)Biomaterials Research2055-71242023-01-0127112410.1186/s40824-023-00341-6A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injuryWanqing Ji0Zhiru Wu1Jiaming Wen2Hengxin Tang3Zhuopeng Chen4Bo Xue5Zhenming Tian6Yueyang Ba7Ning Zhang8Xuejun Wen9Bo Hou10Department of Obstetrics, Guangzhou Women and Children’s Medical Center, Guangzhou Medical University, Guangdong Provincial Clinical Research Center for Child HealthDepartment of Nephrology, Dongcheng branch of the First Affiliated Hospital of Anhui Medical UniversityDepartment of Obstetrics, Guangzhou Women and Children’s Medical Center, Guangzhou Medical University, Guangdong Provincial Clinical Research Center for Child HealthGuangzhou First People’s Hospital, South China University of TechnologyDepartment of Neurosurgery, The Third Affiliated Hospital, Sun Yat-sen UniversityShared Research Facilities, West Virginia UniversityDepartment of Neurosurgery, The Third Affiliated Hospital, Sun Yat-sen UniversityDepartment of Neurosurgery, The Third Affiliated Hospital, Sun Yat-sen UniversityDepartment of Biomedical Engineering, Institute For Engineering and Medicine, Virginia Commonwealth UniversityDepartment of Chemical and Life Science Engineering, Virginia Commonwealth UniversityDepartment of Neurosurgery, The Third Affiliated Hospital, Sun Yat-sen UniversityAbstract Background The brain vascular basement membrane (brain-VBM) is an important component of the brain extracellular matrix, and the three-dimensional structure of the cerebrovascular network nested with many cell-adhesive proteins may provide guidance for brain tissue regeneration. However, the potential of ability of brain-VBM to promote neural tissue regeneration has not been examined due to the technical difficulty of isolating intact brain-VBM. Methods The present study developed a simple, effective method to isolate structurally and compositionally intact brain-VBM. Structural and component properties of the brain-VBM were characterized to confirm the technique. Seed cells were cocultured with brain-VBM in vitro to analyze biocompatibility and neurite extension. An experimental rat model of focal traumatic brain injury (TBI) induced by controlled cortical impact were conducted to further test the tissue regeneration ability of brain-VBM. Results Brain-VBM isolated using genipin showed significantly improved mechanical properties, was easy to handle, supported high cell viability, exhibited strong cell adhesive properties, and promoted neurite extension and outgrowth. Further testing of the isolated brain-VBM transplanted at lesion sites in an experimental rat model of focal TBI demonstrated considerable promise for reconstructing a complete blood vessel network that filled in the lesion cavity and promoting repopulation of neural progenitor cells and neurons. Conclusion The technique allows isolation of intact brain-VBM as a 3D microvascular scaffold to support brain tissue regeneration following TBI and shows considerable promise for the production of naturally-derived biomaterials for neural tissue engineering. Graphical Abstracthttps://doi.org/10.1186/s40824-023-00341-6Vascular basement membraneMicrovascular scaffoldBrain extracellular matrixBiomaterialsTraumatic brain injury
spellingShingle Wanqing Ji
Zhiru Wu
Jiaming Wen
Hengxin Tang
Zhuopeng Chen
Bo Xue
Zhenming Tian
Yueyang Ba
Ning Zhang
Xuejun Wen
Bo Hou
A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury
Biomaterials Research
Vascular basement membrane
Microvascular scaffold
Brain extracellular matrix
Biomaterials
Traumatic brain injury
title A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury
title_full A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury
title_fullStr A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury
title_full_unstemmed A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury
title_short A simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury
title_sort simple method to isolate structurally and chemically intact brain vascular basement membrane for neural regeneration following traumatic brain injury
topic Vascular basement membrane
Microvascular scaffold
Brain extracellular matrix
Biomaterials
Traumatic brain injury
url https://doi.org/10.1186/s40824-023-00341-6
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