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Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration

BACKGROUND: Deer antlers are the only known mammalian structure that undergoes full regeneration. In addition, it is peculiar because when growing, it contains vascularized cartilage. The differentiation of antler stem cells (ASCs) into chondrocytes while inducing endochondral extension of blood ves...

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Autores principales: Li, Xunsheng, Shi, Wanwan, Wei, Guanning, Lv, Jinpeng, Wang, Datao, Xing, Baorui, Zhou, Jue, Zhao, Jianwei, Sun, Hongmei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184426/
https://www.ncbi.nlm.nih.gov/pubmed/37189051
http://dx.doi.org/10.1186/s11658-023-00456-7
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author Li, Xunsheng
Shi, Wanwan
Wei, Guanning
Lv, Jinpeng
Wang, Datao
Xing, Baorui
Zhou, Jue
Zhao, Jianwei
Sun, Hongmei
author_facet Li, Xunsheng
Shi, Wanwan
Wei, Guanning
Lv, Jinpeng
Wang, Datao
Xing, Baorui
Zhou, Jue
Zhao, Jianwei
Sun, Hongmei
author_sort Li, Xunsheng
collection PubMed
description BACKGROUND: Deer antlers are the only known mammalian structure that undergoes full regeneration. In addition, it is peculiar because when growing, it contains vascularized cartilage. The differentiation of antler stem cells (ASCs) into chondrocytes while inducing endochondral extension of blood vessels is necessary to form antler vascularized cartilage. Therefore, antlers provide an unparalleled opportunity to investigate chondrogenesis, angiogenesis, and regenerative medicine. A study found that Galectin-1 (GAL-1), which can be used as a marker in some tumors, is highly expressed in ASCs. This intrigued us to investigate what role GAL-1 could play in antler regeneration. METHODS: We measured the expression level of GAL-1 in antler tissues and cells by immunohistochemistry, WB and QPCR. We constructed antlerogenic periosteal cells (APCs, one cell type of ASCs) with the GAL-1 gene knocked out (APC(GAL-1−/−)) using CRISPR-CAS9 gene editing system. The effect of GAL-1 on angiogenesis was determined by stimulating human umbilical vein endothelial cells (HUVECs) using APC(GAL-1−/−) conditioned medium or adding exogenous deer GAL-1 protein. The effect of APC(GAL-1−/−) on chondrogenic differentiation was evaluated compared with the APCs under micro-mass culture. The gene expression pattern of APC(GAL-1−/−) was analyzed by transcriptome sequencing. RESULTS: Immunohistochemistry revealed that GAL-1 was widely expressed in the antlerogenic periosteum (AP), pedicle periosteum (PP) and antler growth center. Western blot and qRT-PCR analysis using deer cell lines further supports this result. The proliferation, migration, and tube formation assays of human umbilical vein endothelial cells (HUVECs) showed that the proangiogenic activity of APC(GAL-1−/−) medium was significantly decreased (P < 0.05) compared with the APCs medium. The proangiogenic activity of deer GAL-1 protein was further confirmed by adding exogenous deer GAL-1 protein (P < 0.05). The chondrogenic differentiation ability of APC(GAL-1−/−) was impeded under micro-mass culture. The terms of GO and KEGG enrichment of the differentially expressed genes (DEGs) of APC(GAL-1−/−) showed that down-regulated expression of pathways associated with deer antler angiogenesis, osteogenesis and stem cell pluripotency, such as the PI3K-AKT signaling pathway, signaling pathways regulating pluripotency of stem cells and TGF-β signaling pathway. CONCLUSIONS: Deer GAL-1, has strong angiogenic activity, is widely and highly expressed in deer antler. The APCs can induce angiogenesis by secreting GAL-1. The knockout of GAL-1 gene of APCs damaged its ability to induce angiogenesis and differentiate into chondrocytes. This ability is crucial to the formation of deer antler vascularized cartilage. Moreover, Deer antlers offer a unique model to explore explore how angiogenesis at high levels of GAL-1 expression can be elegantly regulated without becoming cancerous. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s11658-023-00456-7.
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spelling pubmed-101844262023-05-16 Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration Li, Xunsheng Shi, Wanwan Wei, Guanning Lv, Jinpeng Wang, Datao Xing, Baorui Zhou, Jue Zhao, Jianwei Sun, Hongmei Cell Mol Biol Lett Research Letter BACKGROUND: Deer antlers are the only known mammalian structure that undergoes full regeneration. In addition, it is peculiar because when growing, it contains vascularized cartilage. The differentiation of antler stem cells (ASCs) into chondrocytes while inducing endochondral extension of blood vessels is necessary to form antler vascularized cartilage. Therefore, antlers provide an unparalleled opportunity to investigate chondrogenesis, angiogenesis, and regenerative medicine. A study found that Galectin-1 (GAL-1), which can be used as a marker in some tumors, is highly expressed in ASCs. This intrigued us to investigate what role GAL-1 could play in antler regeneration. METHODS: We measured the expression level of GAL-1 in antler tissues and cells by immunohistochemistry, WB and QPCR. We constructed antlerogenic periosteal cells (APCs, one cell type of ASCs) with the GAL-1 gene knocked out (APC(GAL-1−/−)) using CRISPR-CAS9 gene editing system. The effect of GAL-1 on angiogenesis was determined by stimulating human umbilical vein endothelial cells (HUVECs) using APC(GAL-1−/−) conditioned medium or adding exogenous deer GAL-1 protein. The effect of APC(GAL-1−/−) on chondrogenic differentiation was evaluated compared with the APCs under micro-mass culture. The gene expression pattern of APC(GAL-1−/−) was analyzed by transcriptome sequencing. RESULTS: Immunohistochemistry revealed that GAL-1 was widely expressed in the antlerogenic periosteum (AP), pedicle periosteum (PP) and antler growth center. Western blot and qRT-PCR analysis using deer cell lines further supports this result. The proliferation, migration, and tube formation assays of human umbilical vein endothelial cells (HUVECs) showed that the proangiogenic activity of APC(GAL-1−/−) medium was significantly decreased (P < 0.05) compared with the APCs medium. The proangiogenic activity of deer GAL-1 protein was further confirmed by adding exogenous deer GAL-1 protein (P < 0.05). The chondrogenic differentiation ability of APC(GAL-1−/−) was impeded under micro-mass culture. The terms of GO and KEGG enrichment of the differentially expressed genes (DEGs) of APC(GAL-1−/−) showed that down-regulated expression of pathways associated with deer antler angiogenesis, osteogenesis and stem cell pluripotency, such as the PI3K-AKT signaling pathway, signaling pathways regulating pluripotency of stem cells and TGF-β signaling pathway. CONCLUSIONS: Deer GAL-1, has strong angiogenic activity, is widely and highly expressed in deer antler. The APCs can induce angiogenesis by secreting GAL-1. The knockout of GAL-1 gene of APCs damaged its ability to induce angiogenesis and differentiate into chondrocytes. This ability is crucial to the formation of deer antler vascularized cartilage. Moreover, Deer antlers offer a unique model to explore explore how angiogenesis at high levels of GAL-1 expression can be elegantly regulated without becoming cancerous. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s11658-023-00456-7. BioMed Central 2023-05-15 /pmc/articles/PMC10184426/ /pubmed/37189051 http://dx.doi.org/10.1186/s11658-023-00456-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Letter
Li, Xunsheng
Shi, Wanwan
Wei, Guanning
Lv, Jinpeng
Wang, Datao
Xing, Baorui
Zhou, Jue
Zhao, Jianwei
Sun, Hongmei
Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration
title Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration
title_full Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration
title_fullStr Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration
title_full_unstemmed Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration
title_short Galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration
title_sort galectin-1 promotes angiogenesis and chondrogenesis during antler regeneration
topic Research Letter
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184426/
https://www.ncbi.nlm.nih.gov/pubmed/37189051
http://dx.doi.org/10.1186/s11658-023-00456-7
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