Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration
Summary: Type H vessels couple angiogenesis with osteogenesis, while sympathetic cues regulate vascular and skeletal function. The crosstalk between sympathetic nerves and type H vessels in bone remains unclear. Here, we first identify close spatial connections between sympathetic nerves and type H...
Main Authors: | , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2023-09-01
|
Series: | iScience |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223015328 |
_version_ | 1797732852734885888 |
---|---|
author | Hao-Kun Xu Jie-Xi Liu Chen-Xi Zheng Lu Liu Chao Ma Jiong-Yi Tian Yuan Yuan Yuan Cao Shu-Juan Xing Si-Ying Liu Qiang Li Ya-Juan Zhao Liang Kong Yong-Jin Chen Bing-Dong Sui |
author_facet | Hao-Kun Xu Jie-Xi Liu Chen-Xi Zheng Lu Liu Chao Ma Jiong-Yi Tian Yuan Yuan Yuan Cao Shu-Juan Xing Si-Ying Liu Qiang Li Ya-Juan Zhao Liang Kong Yong-Jin Chen Bing-Dong Sui |
author_sort | Hao-Kun Xu |
collection | DOAJ |
description | Summary: Type H vessels couple angiogenesis with osteogenesis, while sympathetic cues regulate vascular and skeletal function. The crosstalk between sympathetic nerves and type H vessels in bone remains unclear. Here, we first identify close spatial connections between sympathetic nerves and type H vessels in bone, particularly in metaphysis. Sympathoexcitation, mimicked by isoproterenol (ISO) injection, reduces type H vessels and bone mass. Conversely, beta-2-adrenergic receptor (ADRB2) deficiency maintains type H vessels and bone mass in the physiological condition. In vitro experiments reveal indirect sympathetic modulation of angiogenesis via paracrine effects of mesenchymal stem cells (MSCs), which alter the transcription of multiple angiogenic genes in endothelial cells (ECs). Furthermore, Notch signaling in ECs underlies sympathoexcitation-regulated type H vessel formation, impacting osteogenesis and bone mass. Finally, propranolol (PRO) inhibits beta-adrenergic activity and protects type H vessels and bone mass against estrogen deficiency. These findings unravel the specialized neurovascular coupling in bone homeostasis and regeneration. |
first_indexed | 2024-03-12T12:19:34Z |
format | Article |
id | doaj.art-51184982a3974844a2b3021288397fc1 |
institution | Directory Open Access Journal |
issn | 2589-0042 |
language | English |
last_indexed | 2024-03-12T12:19:34Z |
publishDate | 2023-09-01 |
publisher | Elsevier |
record_format | Article |
series | iScience |
spelling | doaj.art-51184982a3974844a2b3021288397fc12023-08-30T05:54:35ZengElsevieriScience2589-00422023-09-01269107455Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regenerationHao-Kun Xu0Jie-Xi Liu1Chen-Xi Zheng2Lu Liu3Chao Ma4Jiong-Yi Tian5Yuan Yuan6Yuan Cao7Shu-Juan Xing8Si-Ying Liu9Qiang Li10Ya-Juan Zhao11Liang Kong12Yong-Jin Chen13Bing-Dong Sui14State Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China; Department of Oral Anatomy and Physiology, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China; Department of Orthodontics, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China; Exercise Immunology Center, Wuhan Sports University, Wuhan, Hubei 430079, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China; Department of Orthodontics, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaDepartment of Orthodontics, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaDepartment of General Dentistry & Emergency, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaDepartment of General Dentistry & Emergency, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, ChinaDepartment of Oral and Maxillofacial Surgery, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China; Corresponding authorDepartment of General Dentistry & Emergency, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China; Corresponding authorState Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China; Corresponding authorSummary: Type H vessels couple angiogenesis with osteogenesis, while sympathetic cues regulate vascular and skeletal function. The crosstalk between sympathetic nerves and type H vessels in bone remains unclear. Here, we first identify close spatial connections between sympathetic nerves and type H vessels in bone, particularly in metaphysis. Sympathoexcitation, mimicked by isoproterenol (ISO) injection, reduces type H vessels and bone mass. Conversely, beta-2-adrenergic receptor (ADRB2) deficiency maintains type H vessels and bone mass in the physiological condition. In vitro experiments reveal indirect sympathetic modulation of angiogenesis via paracrine effects of mesenchymal stem cells (MSCs), which alter the transcription of multiple angiogenic genes in endothelial cells (ECs). Furthermore, Notch signaling in ECs underlies sympathoexcitation-regulated type H vessel formation, impacting osteogenesis and bone mass. Finally, propranolol (PRO) inhibits beta-adrenergic activity and protects type H vessels and bone mass against estrogen deficiency. These findings unravel the specialized neurovascular coupling in bone homeostasis and regeneration.http://www.sciencedirect.com/science/article/pii/S2589004223015328Vascular anatomyOrthopedicsMolecular neuroscience |
spellingShingle | Hao-Kun Xu Jie-Xi Liu Chen-Xi Zheng Lu Liu Chao Ma Jiong-Yi Tian Yuan Yuan Yuan Cao Shu-Juan Xing Si-Ying Liu Qiang Li Ya-Juan Zhao Liang Kong Yong-Jin Chen Bing-Dong Sui Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration iScience Vascular anatomy Orthopedics Molecular neuroscience |
title | Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration |
title_full | Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration |
title_fullStr | Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration |
title_full_unstemmed | Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration |
title_short | Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration |
title_sort | region specific sympatho adrenergic regulation of specialized vasculature in bone homeostasis and regeneration |
topic | Vascular anatomy Orthopedics Molecular neuroscience |
url | http://www.sciencedirect.com/science/article/pii/S2589004223015328 |
work_keys_str_mv | AT haokunxu regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT jiexiliu regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT chenxizheng regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT luliu regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT chaoma regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT jiongyitian regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT yuanyuan regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT yuancao regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT shujuanxing regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT siyingliu regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT qiangli regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT yajuanzhao regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT liangkong regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT yongjinchen regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration AT bingdongsui regionspecificsympathoadrenergicregulationofspecializedvasculatureinbonehomeostasisandregeneration |