Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration

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 i...

Full description

Saved in:
Bibliographic Details
Published iniScience Vol. 26; no. 9; p. 107455
Main Authors Xu, Hao-Kun, Liu, Jie-Xi, Zheng, Chen-Xi, Liu, Lu, Ma, Chao, Tian, Jiong-Yi, Yuan, Yuan, Cao, Yuan, Xing, Shu-Juan, Liu, Si-Ying, Li, Qiang, Zhao, Ya-Juan, Kong, Liang, Chen, Yong-Jin, Sui, Bing-Dong
Format Journal Article
LanguageEnglish
Published Elsevier Inc 15.09.2023
Elsevier
Subjects
Molecular neuroscience
Orthopedics
Vascular anatomy
Vascular anatomy
Molecular neuroscience
Orthopedics
Online AccessGet full text
ISSN2589-0042
2589-0042
DOI10.1016/j.isci.2023.107455

Cover

Abstract 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. [Display omitted] •Sympathetic nerves spatially and functionally correlate with type H vessels in bone•Sympathoexcitation regulates type H vessel formation and bone mass maintenance•Sympathetic cues regulate angiogenic signaling via an MSC-EC paracrine mode•Pharmacological ADRB inhibition protects type H vessels and bone mass in OVX Vascular anatomy; Orthopedics; Molecular neuroscience
AbstractList 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.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.
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.
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. • Sympathetic nerves spatially and functionally correlate with type H vessels in bone • Sympathoexcitation regulates type H vessel formation and bone mass maintenance • Sympathetic cues regulate angiogenic signaling via an MSC-EC paracrine mode • Pharmacological ADRB inhibition protects type H vessels and bone mass in OVX Vascular anatomy; Orthopedics; Molecular neuroscience
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. [Display omitted] •Sympathetic nerves spatially and functionally correlate with type H vessels in bone•Sympathoexcitation regulates type H vessel formation and bone mass maintenance•Sympathetic cues regulate angiogenic signaling via an MSC-EC paracrine mode•Pharmacological ADRB inhibition protects type H vessels and bone mass in OVX Vascular anatomy; Orthopedics; Molecular neuroscience
ArticleNumber 107455
Author Liu, Jie-Xi
Kong, Liang
Xing, Shu-Juan
Liu, Si-Ying
Li, Qiang
Chen, Yong-Jin
Xu, Hao-Kun
Zheng, Chen-Xi
Ma, Chao
Yuan, Yuan
Tian, Jiong-Yi
Sui, Bing-Dong
Liu, Lu
Cao, Yuan
Zhao, Ya-Juan
Author_xml – sequence: 1
  givenname: Hao-Kun
  surname: Xu
  fullname: Xu, Hao-Kun
  organization: State 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
– sequence: 2
  givenname: Jie-Xi
  surname: Liu
  fullname: Liu, Jie-Xi
  organization: State 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
– sequence: 3
  givenname: Chen-Xi
  surname: Zheng
  fullname: Zheng, Chen-Xi
  organization: State 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
– sequence: 4
  givenname: Lu
  surname: Liu
  fullname: Liu, Lu
  organization: State 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
– sequence: 5
  givenname: Chao
  surname: Ma
  fullname: Ma, Chao
  organization: State 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
– sequence: 6
  givenname: Jiong-Yi
  surname: Tian
  fullname: Tian, Jiong-Yi
  organization: State 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
– sequence: 7
  givenname: Yuan
  surname: Yuan
  fullname: Yuan, Yuan
  organization: State 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
– sequence: 8
  givenname: Yuan
  surname: Cao
  fullname: Cao, Yuan
  organization: State 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
– sequence: 9
  givenname: Shu-Juan
  surname: Xing
  fullname: Xing, Shu-Juan
  organization: State 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
– sequence: 10
  givenname: Si-Ying
  surname: Liu
  fullname: Liu, Si-Ying
  organization: Department of Orthodontics, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China
– sequence: 11
  givenname: Qiang
  surname: Li
  fullname: Li, Qiang
  organization: Department of General Dentistry & Emergency, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China
– sequence: 12
  givenname: Ya-Juan
  surname: Zhao
  fullname: Zhao, Ya-Juan
  organization: Department of General Dentistry & Emergency, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China
– sequence: 13
  givenname: Liang
  surname: Kong
  fullname: Kong, Liang
  email: liangkong2014@163.com
  organization: Department of Oral and Maxillofacial Surgery, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China
– sequence: 14
  givenname: Yong-Jin
  surname: Chen
  fullname: Chen, Yong-Jin
  email: 13991979822@139.com
  organization: Department of General Dentistry & Emergency, School of Stomatology, The Fourth Military Medical University, Xi’an, Shaanxi 710032, China
– sequence: 15
  givenname: Bing-Dong
  surname: Sui
  fullname: Sui, Bing-Dong
  email: bingdong@fmmu.edu.cn
  organization: State 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
BookMark eNp9kV1rHCEUhqUk0DTJH-jVXPZmtuq4jkKhlNCPQKBQkmtx9Mysy4xu1VlIfn2dnRSaXgRE5ZzzPh7P-w6d-eABofcEbwgm_ON-45JxG4ppUwIt227foAu6FbLGmNGzf-5v0XVKe4wxLYtJfoH8Lxhc8HU6gHG9M1V6nA4670KtbQQPcSixCMM86lzqqtBXp1I9uiew1VEns6TmCJXzVVcaq3ZhgpCyTi5V2ttFvYBO-it03usxwfXzeYkevn29v_lR3_38fnvz5a42TMpcc9kaYvuGld3arjeyb1ujiTBtB0RwayV0hHHggjcN47ZrLGE9lRQz0wnWXKLblWuD3qtDdJOOjypop06BEAelY3ZmBLUlRDApqG5kywRjmnYNpoQKUQK9IYX1eWUd5m4Ca8DnqMcX0JcZ73ZqCEdFMBOESl4IH54JMfyeIWU1FcdgHLWHMCdFyy-oZLJZHhNrqYkhpQi9Mi6fRlfQbixMtXiu9mrxXC2eq9XzIqX_Sf-2-Kro0yqC4sbRQVSlArwB6yKYXMblXpP_AaX5yjM
CitedBy_id crossref_primary_10_1186_s40779_025_00596_1
crossref_primary_10_1016_j_mtbio_2024_101417
crossref_primary_10_1038_s41413_024_00371_3
crossref_primary_10_17116_profmed20242709160
crossref_primary_10_3390_cancers16162891
crossref_primary_10_1016_j_surfin_2024_104380
crossref_primary_10_1038_s41368_024_00336_6
crossref_primary_10_3390_ijms242015474
crossref_primary_10_1002_med_22031
Cites_doi 10.1007/s10456-021-09778-6
10.1177/0022034519862258
10.1016/j.arr.2011.01.002
10.1016/j.xpro.2022.101674
10.1210/en.2008-0843
10.1161/01.CIR.98.2.132
10.1038/nature03398
10.7150/ijbs.31605
10.1186/s13287-020-1562-9
10.1126/sciimmunol.aav0492
10.1038/s41569-018-0030-z
10.1161/01.CIR.90.2.970
10.7150/thno.18181
10.3389/fendo.2019.00668
10.1111/j.1476-5381.2011.01791.x
10.1073/pnas.1109036109
10.1016/j.cell.2005.06.028
10.7150/thno.34126
10.1126/scitranslmed.3002191
10.1038/s41422-019-0217-9
10.1152/physrev.00007.2020
10.1038/207764a0
10.1111/j.1469-7793.1999.0781u.x
10.1038/s12276-018-0192-0
10.1038/nature13145
10.1038/s41368-022-00193-1
10.1016/S0092-8674(02)01049-8
10.1136/ard.2011.150607
10.7150/thno.45422
10.1016/j.cmet.2005.03.006
10.1161/CIRCRESAHA.111.300152
10.1038/s12276-022-00899-6
10.3791/64135
10.1172/JCI131554
10.1016/j.stemcr.2020.06.007
10.1038/6553
10.1177/0022034518797275
10.7150/thno.50907
10.1038/171433a0
10.1038/277032a0
10.1359/jbmr.081241
10.1126/science.2827305
10.1016/S0092-8674(00)81558-5
10.1038/260582a0
10.1172/JCI122151
10.1038/nature13383
10.1093/humrep/dem265
10.1002/smtd.202100763
10.1002/jbmr.1594
10.1161/CIRCRESAHA.120.317114
10.1161/01.CIR.0000145608.80855.BC
10.1152/physrev.00014.2017
10.1038/s41593-021-00904-7
10.1161/CIRCRESAHA.119.316053
10.1016/j.cell.2020.01.015
10.1002/jbmr.141
10.1038/305627a0
10.1038/nrm2183
10.7150/thno.22144
10.7326/0003-4819-81-3-364
10.1038/s41591-018-0030-x
10.1016/j.devcel.2013.02.003
10.1155/2018/7453161
ContentType Journal Article
Copyright 2023 The Authors
2023 The Authors.
2023 The Authors 2023
Copyright_xml – notice: 2023 The Authors
– notice: 2023 The Authors.
– notice: 2023 The Authors 2023
DBID 6I.
AAFTH
AAYXX
CITATION
7X8
5PM
DOA
DOI 10.1016/j.isci.2023.107455
DatabaseName ScienceDirect Open Access Titles
Elsevier:ScienceDirect:Open Access
CrossRef
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
DeliveryMethod fulltext_linktorsrc
EISSN 2589-0042
ExternalDocumentID oai_doaj_org_article_51184982a3974844a2b3021288397fc1
PMC10481296
10_1016_j_isci_2023_107455
S2589004223015328
GroupedDBID 0R~
53G
6I.
AACTN
AAEDW
AAFTH
AALRI
AAMRU
AAXUO
ABMAC
ADBBV
ADVLN
AEXQZ
AFTJW
AITUG
ALMA_UNASSIGNED_HOLDINGS
AMRAJ
AOIJS
BCNDV
EBS
FDB
GROUPED_DOAJ
HYE
M41
NCXOZ
OK1
ROL
RPM
SSZ
AAYWO
AAYXX
ACVFH
ADCNI
AEUPX
AFPUW
AIGII
AKBMS
AKYEP
APXCP
CITATION
EJD
7X8
5PM
ID FETCH-LOGICAL-c499t-697c1df34c1dddbfc9f77ca18c7be186dd9eb146e6863346db3d14f29204cb843
IEDL.DBID DOA
ISSN 2589-0042
IngestDate Wed Aug 27 01:29:51 EDT 2025
Thu Aug 21 18:36:35 EDT 2025
Fri Jul 11 09:31:08 EDT 2025
Tue Jul 01 02:07:21 EDT 2025
Thu Apr 24 23:07:09 EDT 2025
Sat Feb 15 15:52:40 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 9
Keywords Vascular anatomy
Molecular neuroscience
Orthopedics
Language English
License This is an open access article under the CC BY-NC-ND license.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c499t-697c1df34c1dddbfc9f77ca18c7be186dd9eb146e6863346db3d14f29204cb843
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
These authors contributed equally
Lead contact
OpenAccessLink https://doaj.org/article/51184982a3974844a2b3021288397fc1
PQID 2863294931
PQPubID 23479
ParticipantIDs doaj_primary_oai_doaj_org_article_51184982a3974844a2b3021288397fc1
pubmedcentral_primary_oai_pubmedcentral_nih_gov_10481296
proquest_miscellaneous_2863294931
crossref_citationtrail_10_1016_j_isci_2023_107455
crossref_primary_10_1016_j_isci_2023_107455
elsevier_sciencedirect_doi_10_1016_j_isci_2023_107455
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2023-09-15
PublicationDateYYYYMMDD 2023-09-15
PublicationDate_xml – month: 09
  year: 2023
  text: 2023-09-15
  day: 15
PublicationDecade 2020
PublicationTitle iScience
PublicationYear 2023
Publisher Elsevier Inc
Elsevier
Publisher_xml – name: Elsevier Inc
– name: Elsevier
References Peng, Wu, Li, Crane (bib35) 2020; 10
Scheid, Honeyman, Fay (bib10) 1979; 277
Massion, Dessy, Desjardins, Pelat, Havaux, Belge, Moulin, Guiot, Feron, Janssens, Balligand (bib17) 2004; 110
Ferraro, Lymperi, Méndez-Ferrer, Saez, Spencer, Yeap, Masselli, Graiani, Prezioso, Rizzini (bib31) 2011; 3
Wee, Lorenz, Bekirov, Jacquin, Scheller (bib37) 2019; 10
Pérez Piñero, Bruzzone, Sarappa, Castillo, Lüthy (bib56) 2012; 166
Maryanovich, Zahalka, Pierce, Pinho, Nakahara, Asada, Wei, Wang, Ciero, Xu (bib30) 2018; 24
Jia, Jia, Mo, Yuan, Zheng, He, Chen, Guo, Zheng, Yuan (bib46) 2019; 98
Makita (bib2) 2013; 24
Sui, Hu, Zheng, Shuai, He, Gao, Zhao, Li, Zhang, He (bib63) 2017; 7
Hanyu, Wehbi, Hayata, Moriya, Feinstein, Ezura, Nagao, Saita, Hemmi, Notomi (bib60) 2012; 109
Kovach, Takacs (bib3) 1953; 171
Yianni, Sharpe (bib41) 2019; 98
Qin, Lee, Patel, Walden, Gomez-Salazar, Levi, James (bib21) 2022; 54
Kalucka, de Rooij, Goveia, Rohlenova, Dumas, Meta, Conchinha, Taverna, Teuwen, Veys (bib34) 2020; 180
Hu, Xiang, Wang, Ma, Zhang, Yan, Zhao, Wu, Feng, Lei (bib50) 2021; 11
Zheng, Sui, Zhang, Hu, Chen, Liu, Wu, Ye, Xiang, Qiu (bib58) 2021; 10
Schwab, Gargett (bib40) 2007; 22
Bouxsein, Devlin, Glatt, Dhillon, Pierroz, Ferrari (bib28) 2009; 150
Armstrong, Blackwell, Flower, McGiff, Mullane, Vane (bib7) 1976; 260
Adams, Alitalo (bib52) 2007; 8
Guiducci, Manetti, Romano, Mazzanti, Ceccarelli, Dal Pozzo, Milia, Bellando-Randone, Fiori, Conforti (bib53) 2011; 70
Cocks, Angus (bib11) 1983; 305
Distler, Liebau, Wolff (bib1) 1965; 207
Khosla, Drake, Volkman, Thicke, Achenbach, Atkinson, Joyner, Rosen, Monroe, Farr (bib29) 2018; 128
Ducy, Amling, Takeda, Priemel, Schilling, Beil, Shen, Vinson, Rueger, Karsenty (bib25) 2000; 100
Tuvia, Moses, Gulayev, Levin, Korenstein (bib57) 1999; 516
Vandecasteele, Eschenhagen, Scholz, Stein, Verde, Fischmeister (bib12) 1999; 5
Zaidi (bib47) 2005; 1
Sims, Singer, Walsh (bib9) 1988; 239
Schaeffer, Iadecola (bib4) 2021; 24
Zhang, Jiao, Ren, Zhang, Li, Wu, Wang, Liu, Zhou, Chen (bib54) 2020; 11
Baek, Bloomfield (bib59) 2009; 24
Zheng, Chen, Tian, Huang, Jin, Sui (bib65) 2022; 3
Takeda, Elefteriou, Levasseur, Liu, Zhao, Parker, Armstrong, Ducy, Karsenty (bib26) 2002; 111
Zhu, Bennett, Kuek, Xiang, Xu, Rosen, Xu (bib33) 2020; 10
Sui, Chen, Zhang, He, Zhao, Zheng, Li, Hu, Jin (bib62) 2018; 50
Aalkjær, Nilsson, De Mey (bib6) 2021; 101
Swenson (bib14) 2020; 127
Galasso, De Rosa, Ciccarelli, Sorriento, Del Giudice, Strisciuglio, De Biase, Luciano, Piccolo, Pierri (bib19) 2013; 112
He, Jiang, Dai (bib61) 2011; 10
Lee, Kim, Yun, Choi, Jung, Kang, Park, Kim, Ha, Ji (bib20) 2018; 2018
Wang, Dong, Zhong, Yang, Li, Su, Gu, Qian (bib43) 2019; 15
Liu, Zheng, Zhao, Zhu, Hu, Zhang, Chen, Zhang, Zhang, Liu (bib44) 2023
Huang, Yin, Rao, Xie, Cao, Rao, Liu, Wang, Cao, Hu (bib51) 2018; 8
Elefteriou (bib22) 2018; 98
Wang, Liu, Yang, Wang, Yang (bib38) 2019; 29
Elefteriou, Ahn, Takeda, Starbuck, Yang, Liu, Kondo, Richards, Bannon, Noda (bib23) 2005; 434
Ungvari, Tarantini, Kiss, Wren, Giles, Griffin, Murfee, Pacher, Csiszar (bib15) 2018; 15
Fukuchi, Hussain, Giaid (bib18) 1998; 98
Pierroz, Bonnet, Bianchi, Bouxsein, Baldock, Rizzoli, Ferrari (bib27) 2012; 27
Tymko, Lawley, Ainslie, Hansen, Hofstaetter, Rainer, Amin, Moralez, Gasho, Vizcardo-Galindo (bib13) 2020; 127
Hu, Lv, Chen, Xue, Gao, Wang, Zhen, Crane, Pan, Liu (bib55) 2020; 130
Deng, He, Cai, Jiang, Yang, Dan, Luo, Du, Chen, He (bib45) 2021; 12
Kusumbe, Ramasamy, Adams (bib36) 2014; 507
Hu, Sui, Liu, Dang, Chen, Zheng, Shi, Zhao, Dang, He (bib39) 2022; 6
Mastorakos, McGavern (bib5) 2019; 4
Tarazi (bib8) 1974; 81
Xing, Zhang, Tang, Liu, Cao, Zheng, Sui, Jin (bib66) 2022
Sui, Liu, Zheng, Dang, Chen, Cao, Zhang, Liu, Dang, Zhang (bib48) 2022; 14
Arranz, Sánchez-Aguilera, Martín-Pérez, Isern, Langa, Tzankov, Lundberg, Muntión, Tzeng, Lai (bib32) 2014; 512
Radmanesh, Sadeghi Abandansari, Ghanian, Pahlavan, Varzideh, Yakhkeshi, Alikhani, Moradi, Braun, Baharvand (bib42) 2021; 24
Chen, Li, Chen (bib16) 1994; 90
Fu, Patel, Bradley, Wagner, Karsenty (bib24) 2005; 122
Chen, Li, Liu, Zheng, Bao, Chen, Xu, Guan, Bai, Zhou (bib49) 2020; 15
Bouxsein, Boyd, Christiansen, Guldberg, Jepsen, Müller (bib64) 2010; 25
Kalucka (10.1016/j.isci.2023.107455_bib34) 2020; 180
Cocks (10.1016/j.isci.2023.107455_bib11) 1983; 305
Chen (10.1016/j.isci.2023.107455_bib16) 1994; 90
Radmanesh (10.1016/j.isci.2023.107455_bib42) 2021; 24
Takeda (10.1016/j.isci.2023.107455_bib26) 2002; 111
Pérez Piñero (10.1016/j.isci.2023.107455_bib56) 2012; 166
Wang (10.1016/j.isci.2023.107455_bib38) 2019; 29
Vandecasteele (10.1016/j.isci.2023.107455_bib12) 1999; 5
Pierroz (10.1016/j.isci.2023.107455_bib27) 2012; 27
Ungvari (10.1016/j.isci.2023.107455_bib15) 2018; 15
Arranz (10.1016/j.isci.2023.107455_bib32) 2014; 512
Guiducci (10.1016/j.isci.2023.107455_bib53) 2011; 70
Schaeffer (10.1016/j.isci.2023.107455_bib4) 2021; 24
Zheng (10.1016/j.isci.2023.107455_bib58) 2021; 10
Baek (10.1016/j.isci.2023.107455_bib59) 2009; 24
Schwab (10.1016/j.isci.2023.107455_bib40) 2007; 22
Mastorakos (10.1016/j.isci.2023.107455_bib5) 2019; 4
Tarazi (10.1016/j.isci.2023.107455_bib8) 1974; 81
Xing (10.1016/j.isci.2023.107455_bib66) 2022
Swenson (10.1016/j.isci.2023.107455_bib14) 2020; 127
Wang (10.1016/j.isci.2023.107455_bib43) 2019; 15
Makita (10.1016/j.isci.2023.107455_bib2) 2013; 24
Distler (10.1016/j.isci.2023.107455_bib1) 1965; 207
Wee (10.1016/j.isci.2023.107455_bib37) 2019; 10
Hu (10.1016/j.isci.2023.107455_bib39) 2022; 6
Sui (10.1016/j.isci.2023.107455_bib63) 2017; 7
Zhang (10.1016/j.isci.2023.107455_bib54) 2020; 11
Elefteriou (10.1016/j.isci.2023.107455_bib23) 2005; 434
Hu (10.1016/j.isci.2023.107455_bib55) 2020; 130
Hanyu (10.1016/j.isci.2023.107455_bib60) 2012; 109
Ferraro (10.1016/j.isci.2023.107455_bib31) 2011; 3
Deng (10.1016/j.isci.2023.107455_bib45) 2021; 12
Fu (10.1016/j.isci.2023.107455_bib24) 2005; 122
Aalkjær (10.1016/j.isci.2023.107455_bib6) 2021; 101
Tuvia (10.1016/j.isci.2023.107455_bib57) 1999; 516
Zheng (10.1016/j.isci.2023.107455_bib65) 2022; 3
Sui (10.1016/j.isci.2023.107455_bib62) 2018; 50
Sui (10.1016/j.isci.2023.107455_bib48) 2022; 14
Scheid (10.1016/j.isci.2023.107455_bib10) 1979; 277
Bouxsein (10.1016/j.isci.2023.107455_bib28) 2009; 150
Lee (10.1016/j.isci.2023.107455_bib20) 2018; 2018
Ducy (10.1016/j.isci.2023.107455_bib25) 2000; 100
Hu (10.1016/j.isci.2023.107455_bib50) 2021; 11
Bouxsein (10.1016/j.isci.2023.107455_bib64) 2010; 25
Qin (10.1016/j.isci.2023.107455_bib21) 2022; 54
Huang (10.1016/j.isci.2023.107455_bib51) 2018; 8
Adams (10.1016/j.isci.2023.107455_bib52) 2007; 8
Elefteriou (10.1016/j.isci.2023.107455_bib22) 2018; 98
Sims (10.1016/j.isci.2023.107455_bib9) 1988; 239
Tymko (10.1016/j.isci.2023.107455_bib13) 2020; 127
Yianni (10.1016/j.isci.2023.107455_bib41) 2019; 98
He (10.1016/j.isci.2023.107455_bib61) 2011; 10
Galasso (10.1016/j.isci.2023.107455_bib19) 2013; 112
Peng (10.1016/j.isci.2023.107455_bib35) 2020; 10
Massion (10.1016/j.isci.2023.107455_bib17) 2004; 110
Zaidi (10.1016/j.isci.2023.107455_bib47) 2005; 1
Chen (10.1016/j.isci.2023.107455_bib49) 2020; 15
Kusumbe (10.1016/j.isci.2023.107455_bib36) 2014; 507
Zhu (10.1016/j.isci.2023.107455_bib33) 2020; 10
Liu (10.1016/j.isci.2023.107455_bib44) 2023
Maryanovich (10.1016/j.isci.2023.107455_bib30) 2018; 24
Fukuchi (10.1016/j.isci.2023.107455_bib18) 1998; 98
Kovach (10.1016/j.isci.2023.107455_bib3) 1953; 171
Khosla (10.1016/j.isci.2023.107455_bib29) 2018; 128
Armstrong (10.1016/j.isci.2023.107455_bib7) 1976; 260
Jia (10.1016/j.isci.2023.107455_bib46) 2019; 98
References_xml – volume: 6
  year: 2022
  ident: bib39
  article-title: Sympathetic Neurostress Drives Osteoblastic Exosomal MiR-21 Transfer to Disrupt Bone Homeostasis and Promote Osteopenia
  publication-title: Small Methods
– volume: 11
  start-page: 38
  year: 2020
  ident: bib54
  article-title: Exosomes from bone marrow mesenchymal stem cells enhance fracture healing through the promotion of osteogenesis and angiogenesis in a rat model of nonunion
  publication-title: Stem Cell Res. Ther.
– volume: 127
  start-page: 247
  year: 2020
  end-page: 248
  ident: bib14
  article-title: Sympathetic Nervous System Activation and Vascular Endothelial Function With Chronic Hypoxia
  publication-title: Circ. Res.
– volume: 111
  start-page: 305
  year: 2002
  end-page: 317
  ident: bib26
  article-title: Leptin regulates bone formation via the sympathetic nervous system
  publication-title: Cell
– volume: 12
  year: 2021
  ident: bib45
  article-title: Analysis and Validation of Hub Genes in Blood Monocytes of Postmenopausal Osteoporosis Patients
  publication-title: Front. Endocrinol.
– volume: 260
  start-page: 582
  year: 1976
  end-page: 586
  ident: bib7
  article-title: Genetic hypertension in rats is accompanied by a defect in renal prostaglandin catabolism
  publication-title: Nature
– volume: 24
  start-page: 792
  year: 2009
  end-page: 799
  ident: bib59
  article-title: Beta-adrenergic blockade and leptin replacement effectively mitigate disuse bone loss
  publication-title: J. Bone Miner. Res.
– volume: 29
  start-page: 870
  year: 2019
  end-page: 872
  ident: bib38
  article-title: BoneClear: whole-tissue immunolabeling of the intact mouse bones for 3D imaging of neural anatomy and pathology
  publication-title: Cell Res.
– volume: 15
  start-page: 2110
  year: 2019
  end-page: 2118
  ident: bib43
  article-title: Extracellular Vesicles (EVs) from Lung Adenocarcinoma Cells Promote Human Umbilical Vein Endothelial Cell (HUVEC) Angiogenesis through Yes Kinase-associated Protein (YAP) Transport
  publication-title: Int. J. Biol. Sci.
– volume: 3
  year: 2022
  ident: bib65
  article-title: Optimized immunofluorescence staining protocol for identifying resident mesenchymal stem cells in bone using LacZ transgenic mice
  publication-title: STAR Protoc.
– volume: 98
  start-page: 132
  year: 1998
  end-page: 139
  ident: bib18
  article-title: Heterogeneous expression and activity of endothelial and inducible nitric oxide synthases in end-stage human heart failure: their relation to lesion site and beta-adrenergic receptor therapy
  publication-title: Circulation
– volume: 10
  start-page: 5957
  year: 2020
  end-page: 5965
  ident: bib33
  article-title: Endothelial cells produce angiocrine factors to regulate bone and cartilage via versatile mechanisms
  publication-title: Theranostics
– volume: 110
  start-page: 2666
  year: 2004
  end-page: 2672
  ident: bib17
  article-title: Cardiomyocyte-restricted overexpression of endothelial nitric oxide synthase (NOS3) attenuates beta-adrenergic stimulation and reinforces vagal inhibition of cardiac contraction
  publication-title: Circulation
– volume: 10
  start-page: 253
  year: 2011
  end-page: 263
  ident: bib61
  article-title: The roles of the sympathetic nervous system in osteoporotic diseases: A review of experimental and clinical studies
  publication-title: Ageing Res. Rev.
– volume: 305
  start-page: 627
  year: 1983
  end-page: 630
  ident: bib11
  article-title: Endothelium-dependent relaxation of coronary arteries by noradrenaline and serotonin
  publication-title: Nature
– volume: 24
  start-page: 340
  year: 2013
  end-page: 341
  ident: bib2
  article-title: Nerve control of blood vessel patterning
  publication-title: Dev. Cell
– year: 2023
  ident: bib44
  article-title: Mesenchymal Stem Cell Aggregation-Released Extracellular Vesicles Induce CD31(+) EMCN(+) Vessels in Skin Regeneration and Improve Diabetic Wound Healing
  publication-title: Adv. Healthc. Mater.
– volume: 3
  start-page: 104ra101
  year: 2011
  ident: bib31
  article-title: Diabetes impairs hematopoietic stem cell mobilization by altering niche function
  publication-title: Sci. Transl. Med.
– volume: 98
  start-page: 107
  year: 2019
  end-page: 116
  ident: bib46
  article-title: Berberine Ameliorates Periodontal Bone Loss by Regulating Gut Microbiota
  publication-title: J. Dent. Res.
– volume: 4
  year: 2019
  ident: bib5
  article-title: The anatomy and immunology of vasculature in the central nervous system
  publication-title: Sci. Immunol.
– volume: 8
  start-page: 2435
  year: 2018
  end-page: 2446
  ident: bib51
  article-title: Harmine enhances type H vessel formation and prevents bone loss in ovariectomized mice
  publication-title: Theranostics
– volume: 101
  start-page: 495
  year: 2021
  end-page: 544
  ident: bib6
  article-title: Sympathetic and Sensory-Motor Nerves in Peripheral Small Arteries
  publication-title: Physiol. Rev.
– volume: 54
  start-page: 1844
  year: 2022
  end-page: 1849
  ident: bib21
  article-title: Neurovascular coupling in bone regeneration
  publication-title: Exp. Mol. Med.
– volume: 14
  start-page: 39
  year: 2022
  ident: bib48
  article-title: Targeted inhibition of osteoclastogenesis reveals the pathogenesis and therapeutics of bone loss under sympathetic neurostress
  publication-title: Int. J. Oral Sci.
– volume: 507
  start-page: 323
  year: 2014
  end-page: 328
  ident: bib36
  article-title: Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone
  publication-title: Nature
– volume: 5
  start-page: 331
  year: 1999
  end-page: 334
  ident: bib12
  article-title: Muscarinic and beta-adrenergic regulation of heart rate, force of contraction and calcium current is preserved in mice lacking endothelial nitric oxide synthase
  publication-title: Nat. Med.
– volume: 11
  start-page: 3796
  year: 2021
  end-page: 3812
  ident: bib50
  article-title: Impairment of type H vessels by NOX2-mediated endothelial oxidative stress: critical mechanisms and therapeutic targets for bone fragility in streptozotocin-induced type 1 diabetic mice
  publication-title: Theranostics
– volume: 50
  start-page: 1
  year: 2018
  end-page: 14
  ident: bib62
  article-title: Gender-independent efficacy of mesenchymal stem cell therapy in sex hormone-deficient bone loss via immunosuppression and resident stem cell recovery
  publication-title: Exp. Mol. Med.
– volume: 434
  start-page: 514
  year: 2005
  end-page: 520
  ident: bib23
  article-title: Leptin regulation of bone resorption by the sympathetic nervous system and CART
  publication-title: Nature
– volume: 516
  start-page: 781
  year: 1999
  end-page: 792
  ident: bib57
  article-title: Beta-adrenergic agonists regulate cell membrane fluctuations of human erythrocytes
  publication-title: J. Physiol.
– volume: 10
  year: 2021
  ident: bib58
  article-title: Apoptotic vesicles restore liver macrophage homeostasis to counteract type 2 diabetes
  publication-title: J. Extracell. Vesicles
– volume: 24
  start-page: 1198
  year: 2021
  end-page: 1209
  ident: bib4
  article-title: Revisiting the neurovascular unit
  publication-title: Nat. Neurosci.
– volume: 98
  start-page: 1066
  year: 2019
  end-page: 1072
  ident: bib41
  article-title: Perivascular-Derived Mesenchymal Stem Cells
  publication-title: J. Dent. Res.
– volume: 130
  start-page: 3483
  year: 2020
  end-page: 3498
  ident: bib55
  article-title: Sensory nerves regulate mesenchymal stromal cell lineage commitment by tuning sympathetic tones
  publication-title: J. Clin. Invest.
– volume: 128
  start-page: 4832
  year: 2018
  end-page: 4842
  ident: bib29
  article-title: Sympathetic beta1-adrenergic signaling contributes to regulation of human bone metabolism
  publication-title: J. Clin. Invest.
– volume: 109
  start-page: 7433
  year: 2012
  end-page: 7438
  ident: bib60
  article-title: Anabolic action of parathyroid hormone regulated by the beta2-adrenergic receptor
  publication-title: Proc. Natl. Acad. Sci. USA
– volume: 8
  start-page: 464
  year: 2007
  end-page: 478
  ident: bib52
  article-title: Molecular regulation of angiogenesis and lymphangiogenesis
  publication-title: Nat. Rev. Mol. Cell Biol.
– volume: 24
  start-page: 657
  year: 2021
  end-page: 676
  ident: bib42
  article-title: Hydrogel-mediated delivery of microRNA-92a inhibitor polyplex nanoparticles induces localized angiogenesis
  publication-title: Angiogenesis
– volume: 150
  start-page: 144
  year: 2009
  end-page: 152
  ident: bib28
  article-title: Mice lacking beta-adrenergic receptors have increased bone mass but are not protected from deleterious skeletal effects of ovariectomy
  publication-title: Endocrinology
– volume: 15
  start-page: 110
  year: 2020
  end-page: 124
  ident: bib49
  article-title: Gli1(+) Cells Couple with Type H Vessels and Are Required for Type H Vessel Formation
  publication-title: Stem Cell Rep.
– volume: 112
  start-page: 1026
  year: 2013
  end-page: 1034
  ident: bib19
  article-title: beta2-Adrenergic receptor stimulation improves endothelial progenitor cell-mediated ischemic neoangiogenesis
  publication-title: Circ. Res.
– volume: 2018
  year: 2018
  ident: bib20
  article-title: Angiotensin II Attenuates the Bioactivities of Human Endothelial Progenitor Cells via Downregulation of beta2-Adrenergic Receptor
  publication-title: Stem Cells Int.
– volume: 122
  start-page: 803
  year: 2005
  end-page: 815
  ident: bib24
  article-title: The molecular clock mediates leptin-regulated bone formation
  publication-title: Cell
– volume: 22
  start-page: 2903
  year: 2007
  end-page: 2911
  ident: bib40
  article-title: Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium
  publication-title: Hum. Reprod.
– volume: 70
  start-page: 2011
  year: 2011
  end-page: 2021
  ident: bib53
  article-title: Bone marrow-derived mesenchymal stem cells from early diffuse systemic sclerosis exhibit a paracrine machinery and stimulate angiogenesis in vitro
  publication-title: Ann. Rheum. Dis.
– volume: 27
  start-page: 1252
  year: 2012
  end-page: 1262
  ident: bib27
  article-title: Deletion of beta-adrenergic receptor 1, 2, or both leads to different bone phenotypes and response to mechanical stimulation
  publication-title: J. Bone Miner. Res.
– year: 2022
  ident: bib66
  article-title: Isolation, Characterization, and Therapeutic Application of Extracellular Vesicles from Cultured Human Mesenchymal Stem Cells
  publication-title: J. Vis. Exp.
– volume: 239
  start-page: 190
  year: 1988
  end-page: 193
  ident: bib9
  article-title: Antagonistic adrenergic-muscarinic regulation of M current in smooth muscle cells
  publication-title: Science
– volume: 171
  start-page: 433
  year: 1953
  end-page: 434
  ident: bib3
  article-title: Response of the vascular system to sympathetic stimuli during shock
  publication-title: Nature
– volume: 166
  start-page: 721
  year: 2012
  end-page: 736
  ident: bib56
  article-title: Involvement of alpha2- and beta2-adrenoceptors on breast cancer cell proliferation and tumour growth regulation
  publication-title: Br. J. Pharmacol.
– volume: 10
  start-page: 426
  year: 2020
  end-page: 436
  ident: bib35
  article-title: Type H blood vessels in bone modeling and remodeling
  publication-title: Theranostics
– volume: 15
  start-page: 555
  year: 2018
  end-page: 565
  ident: bib15
  article-title: Endothelial dysfunction and angiogenesis impairment in the ageing vasculature
  publication-title: Nat. Rev. Cardiol.
– volume: 10
  start-page: 668
  year: 2019
  ident: bib37
  article-title: Shared Autonomic Pathways Connect Bone Marrow and Peripheral Adipose Tissues Across the Central Neuraxis
  publication-title: Front. Endocrinol.
– volume: 1
  start-page: 219
  year: 2005
  end-page: 221
  ident: bib47
  article-title: Neural surveillance of skeletal homeostasis
  publication-title: Cell Metab.
– volume: 25
  start-page: 1468
  year: 2010
  end-page: 1486
  ident: bib64
  article-title: Guidelines for assessment of bone microstructure in rodents using micro-computed tomography
  publication-title: J. Bone Miner. Res.
– volume: 512
  start-page: 78
  year: 2014
  end-page: 81
  ident: bib32
  article-title: Neuropathy of haematopoietic stem cell niche is essential for myeloproliferative neoplasms
  publication-title: Nature
– volume: 90
  start-page: 970
  year: 1994
  end-page: 975
  ident: bib16
  article-title: Physical conditioning decreases norepinephrine-induced vasoconstriction in rabbits. Possible roles of norepinephrine-evoked endothelium-derived relaxing factor
  publication-title: Circulation
– volume: 81
  start-page: 364
  year: 1974
  end-page: 371
  ident: bib8
  article-title: Sympathomimetic agents in the treatment of shock
  publication-title: Ann. Intern. Med.
– volume: 207
  start-page: 764
  year: 1965
  end-page: 765
  ident: bib1
  article-title: Action of angiotensin on sympathetic nerve endings in isolated blood vessels
  publication-title: Nature
– volume: 180
  start-page: 764
  year: 2020
  end-page: 779.e20
  ident: bib34
  article-title: Single-Cell Transcriptome Atlas of Murine Endothelial Cells
  publication-title: Cell
– volume: 7
  start-page: 1225
  year: 2017
  end-page: 1244
  ident: bib63
  article-title: Recipient Glycemic Micro-environments Govern Therapeutic Effects of Mesenchymal Stem Cell Infusion on Osteopenia
  publication-title: Theranostics
– volume: 98
  start-page: 1083
  year: 2018
  end-page: 1112
  ident: bib22
  article-title: Impact of the Autonomic Nervous System on the Skeleton
  publication-title: Physiol. Rev.
– volume: 24
  start-page: 782
  year: 2018
  end-page: 791
  ident: bib30
  article-title: Adrenergic nerve degeneration in bone marrow drives aging of the hematopoietic stem cell niche
  publication-title: Nat. Med.
– volume: 127
  start-page: e1
  year: 2020
  end-page: e13
  ident: bib13
  article-title: Global Reach 2018 Heightened alpha-Adrenergic Signaling Impairs Endothelial Function During Chronic Exposure to Hypobaric Hypoxia
  publication-title: Circ. Res.
– volume: 100
  start-page: 197
  year: 2000
  end-page: 207
  ident: bib25
  article-title: Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass
  publication-title: Cell
– volume: 277
  start-page: 32
  year: 1979
  end-page: 36
  ident: bib10
  article-title: Mechanism of beta-adrenergic relaxation of smooth muscle
  publication-title: Nature
– volume: 24
  start-page: 657
  year: 2021
  ident: 10.1016/j.isci.2023.107455_bib42
  article-title: Hydrogel-mediated delivery of microRNA-92a inhibitor polyplex nanoparticles induces localized angiogenesis
  publication-title: Angiogenesis
  doi: 10.1007/s10456-021-09778-6
– volume: 98
  start-page: 1066
  year: 2019
  ident: 10.1016/j.isci.2023.107455_bib41
  article-title: Perivascular-Derived Mesenchymal Stem Cells
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034519862258
– volume: 10
  start-page: 253
  year: 2011
  ident: 10.1016/j.isci.2023.107455_bib61
  article-title: The roles of the sympathetic nervous system in osteoporotic diseases: A review of experimental and clinical studies
  publication-title: Ageing Res. Rev.
  doi: 10.1016/j.arr.2011.01.002
– volume: 3
  year: 2022
  ident: 10.1016/j.isci.2023.107455_bib65
  article-title: Optimized immunofluorescence staining protocol for identifying resident mesenchymal stem cells in bone using LacZ transgenic mice
  publication-title: STAR Protoc.
  doi: 10.1016/j.xpro.2022.101674
– volume: 150
  start-page: 144
  year: 2009
  ident: 10.1016/j.isci.2023.107455_bib28
  article-title: Mice lacking beta-adrenergic receptors have increased bone mass but are not protected from deleterious skeletal effects of ovariectomy
  publication-title: Endocrinology
  doi: 10.1210/en.2008-0843
– volume: 98
  start-page: 132
  year: 1998
  ident: 10.1016/j.isci.2023.107455_bib18
  article-title: Heterogeneous expression and activity of endothelial and inducible nitric oxide synthases in end-stage human heart failure: their relation to lesion site and beta-adrenergic receptor therapy
  publication-title: Circulation
  doi: 10.1161/01.CIR.98.2.132
– volume: 434
  start-page: 514
  year: 2005
  ident: 10.1016/j.isci.2023.107455_bib23
  article-title: Leptin regulation of bone resorption by the sympathetic nervous system and CART
  publication-title: Nature
  doi: 10.1038/nature03398
– volume: 15
  start-page: 2110
  year: 2019
  ident: 10.1016/j.isci.2023.107455_bib43
  article-title: Extracellular Vesicles (EVs) from Lung Adenocarcinoma Cells Promote Human Umbilical Vein Endothelial Cell (HUVEC) Angiogenesis through Yes Kinase-associated Protein (YAP) Transport
  publication-title: Int. J. Biol. Sci.
  doi: 10.7150/ijbs.31605
– volume: 11
  start-page: 38
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib54
  article-title: Exosomes from bone marrow mesenchymal stem cells enhance fracture healing through the promotion of osteogenesis and angiogenesis in a rat model of nonunion
  publication-title: Stem Cell Res. Ther.
  doi: 10.1186/s13287-020-1562-9
– volume: 4
  year: 2019
  ident: 10.1016/j.isci.2023.107455_bib5
  article-title: The anatomy and immunology of vasculature in the central nervous system
  publication-title: Sci. Immunol.
  doi: 10.1126/sciimmunol.aav0492
– volume: 15
  start-page: 555
  year: 2018
  ident: 10.1016/j.isci.2023.107455_bib15
  article-title: Endothelial dysfunction and angiogenesis impairment in the ageing vasculature
  publication-title: Nat. Rev. Cardiol.
  doi: 10.1038/s41569-018-0030-z
– volume: 90
  start-page: 970
  year: 1994
  ident: 10.1016/j.isci.2023.107455_bib16
  article-title: Physical conditioning decreases norepinephrine-induced vasoconstriction in rabbits. Possible roles of norepinephrine-evoked endothelium-derived relaxing factor
  publication-title: Circulation
  doi: 10.1161/01.CIR.90.2.970
– volume: 7
  start-page: 1225
  year: 2017
  ident: 10.1016/j.isci.2023.107455_bib63
  article-title: Recipient Glycemic Micro-environments Govern Therapeutic Effects of Mesenchymal Stem Cell Infusion on Osteopenia
  publication-title: Theranostics
  doi: 10.7150/thno.18181
– volume: 10
  start-page: 668
  year: 2019
  ident: 10.1016/j.isci.2023.107455_bib37
  article-title: Shared Autonomic Pathways Connect Bone Marrow and Peripheral Adipose Tissues Across the Central Neuraxis
  publication-title: Front. Endocrinol.
  doi: 10.3389/fendo.2019.00668
– volume: 166
  start-page: 721
  year: 2012
  ident: 10.1016/j.isci.2023.107455_bib56
  article-title: Involvement of alpha2- and beta2-adrenoceptors on breast cancer cell proliferation and tumour growth regulation
  publication-title: Br. J. Pharmacol.
  doi: 10.1111/j.1476-5381.2011.01791.x
– volume: 109
  start-page: 7433
  year: 2012
  ident: 10.1016/j.isci.2023.107455_bib60
  article-title: Anabolic action of parathyroid hormone regulated by the beta2-adrenergic receptor
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1109036109
– volume: 122
  start-page: 803
  year: 2005
  ident: 10.1016/j.isci.2023.107455_bib24
  article-title: The molecular clock mediates leptin-regulated bone formation
  publication-title: Cell
  doi: 10.1016/j.cell.2005.06.028
– volume: 10
  start-page: 426
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib35
  article-title: Type H blood vessels in bone modeling and remodeling
  publication-title: Theranostics
  doi: 10.7150/thno.34126
– volume: 3
  start-page: 104ra101
  year: 2011
  ident: 10.1016/j.isci.2023.107455_bib31
  article-title: Diabetes impairs hematopoietic stem cell mobilization by altering niche function
  publication-title: Sci. Transl. Med.
  doi: 10.1126/scitranslmed.3002191
– volume: 29
  start-page: 870
  year: 2019
  ident: 10.1016/j.isci.2023.107455_bib38
  article-title: BoneClear: whole-tissue immunolabeling of the intact mouse bones for 3D imaging of neural anatomy and pathology
  publication-title: Cell Res.
  doi: 10.1038/s41422-019-0217-9
– volume: 101
  start-page: 495
  year: 2021
  ident: 10.1016/j.isci.2023.107455_bib6
  article-title: Sympathetic and Sensory-Motor Nerves in Peripheral Small Arteries
  publication-title: Physiol. Rev.
  doi: 10.1152/physrev.00007.2020
– volume: 207
  start-page: 764
  year: 1965
  ident: 10.1016/j.isci.2023.107455_bib1
  article-title: Action of angiotensin on sympathetic nerve endings in isolated blood vessels
  publication-title: Nature
  doi: 10.1038/207764a0
– volume: 516
  start-page: 781
  year: 1999
  ident: 10.1016/j.isci.2023.107455_bib57
  article-title: Beta-adrenergic agonists regulate cell membrane fluctuations of human erythrocytes
  publication-title: J. Physiol.
  doi: 10.1111/j.1469-7793.1999.0781u.x
– volume: 50
  start-page: 1
  year: 2018
  ident: 10.1016/j.isci.2023.107455_bib62
  article-title: Gender-independent efficacy of mesenchymal stem cell therapy in sex hormone-deficient bone loss via immunosuppression and resident stem cell recovery
  publication-title: Exp. Mol. Med.
  doi: 10.1038/s12276-018-0192-0
– volume: 507
  start-page: 323
  year: 2014
  ident: 10.1016/j.isci.2023.107455_bib36
  article-title: Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone
  publication-title: Nature
  doi: 10.1038/nature13145
– volume: 14
  start-page: 39
  year: 2022
  ident: 10.1016/j.isci.2023.107455_bib48
  article-title: Targeted inhibition of osteoclastogenesis reveals the pathogenesis and therapeutics of bone loss under sympathetic neurostress
  publication-title: Int. J. Oral Sci.
  doi: 10.1038/s41368-022-00193-1
– volume: 111
  start-page: 305
  year: 2002
  ident: 10.1016/j.isci.2023.107455_bib26
  article-title: Leptin regulates bone formation via the sympathetic nervous system
  publication-title: Cell
  doi: 10.1016/S0092-8674(02)01049-8
– volume: 70
  start-page: 2011
  year: 2011
  ident: 10.1016/j.isci.2023.107455_bib53
  article-title: Bone marrow-derived mesenchymal stem cells from early diffuse systemic sclerosis exhibit a paracrine machinery and stimulate angiogenesis in vitro
  publication-title: Ann. Rheum. Dis.
  doi: 10.1136/ard.2011.150607
– volume: 10
  start-page: 5957
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib33
  article-title: Endothelial cells produce angiocrine factors to regulate bone and cartilage via versatile mechanisms
  publication-title: Theranostics
  doi: 10.7150/thno.45422
– volume: 1
  start-page: 219
  year: 2005
  ident: 10.1016/j.isci.2023.107455_bib47
  article-title: Neural surveillance of skeletal homeostasis
  publication-title: Cell Metab.
  doi: 10.1016/j.cmet.2005.03.006
– volume: 112
  start-page: 1026
  year: 2013
  ident: 10.1016/j.isci.2023.107455_bib19
  article-title: beta2-Adrenergic receptor stimulation improves endothelial progenitor cell-mediated ischemic neoangiogenesis
  publication-title: Circ. Res.
  doi: 10.1161/CIRCRESAHA.111.300152
– volume: 54
  start-page: 1844
  year: 2022
  ident: 10.1016/j.isci.2023.107455_bib21
  article-title: Neurovascular coupling in bone regeneration
  publication-title: Exp. Mol. Med.
  doi: 10.1038/s12276-022-00899-6
– year: 2022
  ident: 10.1016/j.isci.2023.107455_bib66
  article-title: Isolation, Characterization, and Therapeutic Application of Extracellular Vesicles from Cultured Human Mesenchymal Stem Cells
  publication-title: J. Vis. Exp.
  doi: 10.3791/64135
– volume: 130
  start-page: 3483
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib55
  article-title: Sensory nerves regulate mesenchymal stromal cell lineage commitment by tuning sympathetic tones
  publication-title: J. Clin. Invest.
  doi: 10.1172/JCI131554
– volume: 15
  start-page: 110
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib49
  article-title: Gli1(+) Cells Couple with Type H Vessels and Are Required for Type H Vessel Formation
  publication-title: Stem Cell Rep.
  doi: 10.1016/j.stemcr.2020.06.007
– volume: 12
  year: 2021
  ident: 10.1016/j.isci.2023.107455_bib45
  article-title: Analysis and Validation of Hub Genes in Blood Monocytes of Postmenopausal Osteoporosis Patients
  publication-title: Front. Endocrinol.
– volume: 5
  start-page: 331
  year: 1999
  ident: 10.1016/j.isci.2023.107455_bib12
  article-title: Muscarinic and beta-adrenergic regulation of heart rate, force of contraction and calcium current is preserved in mice lacking endothelial nitric oxide synthase
  publication-title: Nat. Med.
  doi: 10.1038/6553
– volume: 98
  start-page: 107
  year: 2019
  ident: 10.1016/j.isci.2023.107455_bib46
  article-title: Berberine Ameliorates Periodontal Bone Loss by Regulating Gut Microbiota
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034518797275
– volume: 11
  start-page: 3796
  year: 2021
  ident: 10.1016/j.isci.2023.107455_bib50
  article-title: Impairment of type H vessels by NOX2-mediated endothelial oxidative stress: critical mechanisms and therapeutic targets for bone fragility in streptozotocin-induced type 1 diabetic mice
  publication-title: Theranostics
  doi: 10.7150/thno.50907
– year: 2023
  ident: 10.1016/j.isci.2023.107455_bib44
  article-title: Mesenchymal Stem Cell Aggregation-Released Extracellular Vesicles Induce CD31(+) EMCN(+) Vessels in Skin Regeneration and Improve Diabetic Wound Healing
  publication-title: Adv. Healthc. Mater.
– volume: 171
  start-page: 433
  year: 1953
  ident: 10.1016/j.isci.2023.107455_bib3
  article-title: Response of the vascular system to sympathetic stimuli during shock
  publication-title: Nature
  doi: 10.1038/171433a0
– volume: 277
  start-page: 32
  year: 1979
  ident: 10.1016/j.isci.2023.107455_bib10
  article-title: Mechanism of beta-adrenergic relaxation of smooth muscle
  publication-title: Nature
  doi: 10.1038/277032a0
– volume: 24
  start-page: 792
  year: 2009
  ident: 10.1016/j.isci.2023.107455_bib59
  article-title: Beta-adrenergic blockade and leptin replacement effectively mitigate disuse bone loss
  publication-title: J. Bone Miner. Res.
  doi: 10.1359/jbmr.081241
– volume: 239
  start-page: 190
  year: 1988
  ident: 10.1016/j.isci.2023.107455_bib9
  article-title: Antagonistic adrenergic-muscarinic regulation of M current in smooth muscle cells
  publication-title: Science
  doi: 10.1126/science.2827305
– volume: 100
  start-page: 197
  year: 2000
  ident: 10.1016/j.isci.2023.107455_bib25
  article-title: Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass
  publication-title: Cell
  doi: 10.1016/S0092-8674(00)81558-5
– volume: 10
  year: 2021
  ident: 10.1016/j.isci.2023.107455_bib58
  article-title: Apoptotic vesicles restore liver macrophage homeostasis to counteract type 2 diabetes
  publication-title: J. Extracell. Vesicles
– volume: 260
  start-page: 582
  year: 1976
  ident: 10.1016/j.isci.2023.107455_bib7
  article-title: Genetic hypertension in rats is accompanied by a defect in renal prostaglandin catabolism
  publication-title: Nature
  doi: 10.1038/260582a0
– volume: 128
  start-page: 4832
  year: 2018
  ident: 10.1016/j.isci.2023.107455_bib29
  article-title: Sympathetic beta1-adrenergic signaling contributes to regulation of human bone metabolism
  publication-title: J. Clin. Invest.
  doi: 10.1172/JCI122151
– volume: 512
  start-page: 78
  year: 2014
  ident: 10.1016/j.isci.2023.107455_bib32
  article-title: Neuropathy of haematopoietic stem cell niche is essential for myeloproliferative neoplasms
  publication-title: Nature
  doi: 10.1038/nature13383
– volume: 22
  start-page: 2903
  year: 2007
  ident: 10.1016/j.isci.2023.107455_bib40
  article-title: Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium
  publication-title: Hum. Reprod.
  doi: 10.1093/humrep/dem265
– volume: 6
  year: 2022
  ident: 10.1016/j.isci.2023.107455_bib39
  article-title: Sympathetic Neurostress Drives Osteoblastic Exosomal MiR-21 Transfer to Disrupt Bone Homeostasis and Promote Osteopenia
  publication-title: Small Methods
  doi: 10.1002/smtd.202100763
– volume: 27
  start-page: 1252
  year: 2012
  ident: 10.1016/j.isci.2023.107455_bib27
  article-title: Deletion of beta-adrenergic receptor 1, 2, or both leads to different bone phenotypes and response to mechanical stimulation
  publication-title: J. Bone Miner. Res.
  doi: 10.1002/jbmr.1594
– volume: 127
  start-page: 247
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib14
  article-title: Sympathetic Nervous System Activation and Vascular Endothelial Function With Chronic Hypoxia
  publication-title: Circ. Res.
  doi: 10.1161/CIRCRESAHA.120.317114
– volume: 110
  start-page: 2666
  year: 2004
  ident: 10.1016/j.isci.2023.107455_bib17
  article-title: Cardiomyocyte-restricted overexpression of endothelial nitric oxide synthase (NOS3) attenuates beta-adrenergic stimulation and reinforces vagal inhibition of cardiac contraction
  publication-title: Circulation
  doi: 10.1161/01.CIR.0000145608.80855.BC
– volume: 98
  start-page: 1083
  year: 2018
  ident: 10.1016/j.isci.2023.107455_bib22
  article-title: Impact of the Autonomic Nervous System on the Skeleton
  publication-title: Physiol. Rev.
  doi: 10.1152/physrev.00014.2017
– volume: 24
  start-page: 1198
  year: 2021
  ident: 10.1016/j.isci.2023.107455_bib4
  article-title: Revisiting the neurovascular unit
  publication-title: Nat. Neurosci.
  doi: 10.1038/s41593-021-00904-7
– volume: 127
  start-page: e1
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib13
  article-title: Global Reach 2018 Heightened alpha-Adrenergic Signaling Impairs Endothelial Function During Chronic Exposure to Hypobaric Hypoxia
  publication-title: Circ. Res.
  doi: 10.1161/CIRCRESAHA.119.316053
– volume: 180
  start-page: 764
  year: 2020
  ident: 10.1016/j.isci.2023.107455_bib34
  article-title: Single-Cell Transcriptome Atlas of Murine Endothelial Cells
  publication-title: Cell
  doi: 10.1016/j.cell.2020.01.015
– volume: 25
  start-page: 1468
  year: 2010
  ident: 10.1016/j.isci.2023.107455_bib64
  article-title: Guidelines for assessment of bone microstructure in rodents using micro-computed tomography
  publication-title: J. Bone Miner. Res.
  doi: 10.1002/jbmr.141
– volume: 305
  start-page: 627
  year: 1983
  ident: 10.1016/j.isci.2023.107455_bib11
  article-title: Endothelium-dependent relaxation of coronary arteries by noradrenaline and serotonin
  publication-title: Nature
  doi: 10.1038/305627a0
– volume: 8
  start-page: 464
  year: 2007
  ident: 10.1016/j.isci.2023.107455_bib52
  article-title: Molecular regulation of angiogenesis and lymphangiogenesis
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/nrm2183
– volume: 8
  start-page: 2435
  year: 2018
  ident: 10.1016/j.isci.2023.107455_bib51
  article-title: Harmine enhances type H vessel formation and prevents bone loss in ovariectomized mice
  publication-title: Theranostics
  doi: 10.7150/thno.22144
– volume: 81
  start-page: 364
  year: 1974
  ident: 10.1016/j.isci.2023.107455_bib8
  article-title: Sympathomimetic agents in the treatment of shock
  publication-title: Ann. Intern. Med.
  doi: 10.7326/0003-4819-81-3-364
– volume: 24
  start-page: 782
  year: 2018
  ident: 10.1016/j.isci.2023.107455_bib30
  article-title: Adrenergic nerve degeneration in bone marrow drives aging of the hematopoietic stem cell niche
  publication-title: Nat. Med.
  doi: 10.1038/s41591-018-0030-x
– volume: 24
  start-page: 340
  year: 2013
  ident: 10.1016/j.isci.2023.107455_bib2
  article-title: Nerve control of blood vessel patterning
  publication-title: Dev. Cell
  doi: 10.1016/j.devcel.2013.02.003
– volume: 2018
  year: 2018
  ident: 10.1016/j.isci.2023.107455_bib20
  article-title: Angiotensin II Attenuates the Bioactivities of Human Endothelial Progenitor Cells via Downregulation of beta2-Adrenergic Receptor
  publication-title: Stem Cells Int.
  doi: 10.1155/2018/7453161
SSID ssj0002002496
Score 2.3026059
Snippet Type H vessels couple angiogenesis with osteogenesis, while sympathetic cues regulate vascular and skeletal function. The crosstalk between sympathetic nerves...
SourceID doaj
pubmedcentral
proquest
crossref
elsevier
SourceType Open Website
Open Access Repository
Aggregation Database
Enrichment Source
Index Database
Publisher
StartPage 107455
SubjectTerms Molecular neuroscience
Orthopedics
Vascular anatomy
Title Region-specific sympatho-adrenergic regulation of specialized vasculature in bone homeostasis and regeneration
URI https://dx.doi.org/10.1016/j.isci.2023.107455
https://www.proquest.com/docview/2863294931
https://pubmed.ncbi.nlm.nih.gov/PMC10481296
https://doaj.org/article/51184982a3974844a2b3021288397fc1
Volume 26
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV29S8UwEA_i5CKKis8vIrhJ1bRpmowqigg6iIJbSPOBFW3l9b1B_3rvmj5pF11cOrRJm-Yuvbvmd78j5AjWFy8cg0jVG5lA_JXCkoKYR6ozU9gza5jFH_p39-Lmid8-58-DUl-ICYv0wHHiTtED5kqmBgwnl5ybtMyQllyCZS-C7QIfsHmDYOq1215DKryuslyOmCBQzT5jJoK7MOP1BCuHnyAgEfP8BlapI-8fGaeB8zmGTg5s0fUaWe2dSHoeB79Olny9QeoHj9jiBHMnEf9D2893rDfcJAaztf0UvnF0GkvPQzvaBNrG4vPVl3e0h6TihgKtalo2tacvzbtvwH1sq5aa2mHvjqUa-2-Sp-urx8ubpK-mkFiIamaJUIVlLmQcjs6VwapQFCALaYvSMymcU_Dd5sILKbKMC1dmjvGA1ay4LSXPtshyDc_eJpRJV4RUlGluGHcsgB6AjbNCycyIIMKEsMVsattTjWPFize9wJS9apSARgnoKIEJOf7p8xGJNn5tfYFC-mmJJNndCVAd3auO_kt1JiRfiFj3_kb0I-BW1a8PP1zog4bFiDsspvbNvNUpTF2quMrg3nKkKKORjq_U1UtH682QuidVYuc_3m2XrOCIEdnC8j2yPJvO_T64T7PyoFsp38wFFnk
linkProvider Directory of Open Access Journals
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Region-specific+sympatho-adrenergic+regulation+of+specialized+vasculature+in+bone+homeostasis+and+regeneration&rft.jtitle=iScience&rft.au=Xu%2C+Hao-Kun&rft.au=Liu%2C+Jie-Xi&rft.au=Zheng%2C+Chen-Xi&rft.au=Liu%2C+Lu&rft.date=2023-09-15&rft.issn=2589-0042&rft.eissn=2589-0042&rft.volume=26&rft.issue=9&rft.spage=107455&rft_id=info:doi/10.1016%2Fj.isci.2023.107455&rft.externalDBID=n%2Fa&rft.externalDocID=10_1016_j_isci_2023_107455
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2589-0042&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2589-0042&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2589-0042&client=summon