Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing

Abstract Background Vascular insufficiency is associated with the pathogenesis and therapeutic outcomes of diabetic foot ulcers (DFU). While mesenchymal stem cells (MSCs) hold potential for DFU treatment, further enhancement in promoting angiogenesis in the challenging DFU wounds is imperative. Meth...

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Main Authors: Qiong Deng, Fangzhou Du, Shenzhen Pan, Yuchen Xia, Yuxin Zhu, Jingzhong Zhang, Chenglong Li, Shuang Yu
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Stem Cell Research & Therapy
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Online Access:https://doi.org/10.1186/s13287-025-04207-7
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author Qiong Deng
Fangzhou Du
Shenzhen Pan
Yuchen Xia
Yuxin Zhu
Jingzhong Zhang
Chenglong Li
Shuang Yu
author_facet Qiong Deng
Fangzhou Du
Shenzhen Pan
Yuchen Xia
Yuxin Zhu
Jingzhong Zhang
Chenglong Li
Shuang Yu
author_sort Qiong Deng
collection DOAJ
description Abstract Background Vascular insufficiency is associated with the pathogenesis and therapeutic outcomes of diabetic foot ulcers (DFU). While mesenchymal stem cells (MSCs) hold potential for DFU treatment, further enhancement in promoting angiogenesis in the challenging DFU wounds is imperative. Methods The differential expression of pro- and anti-angiogenic factors during both normal and diabetic wound healing was compared using quantitative PCR. MSCs derived from the umbilical cord was prepared, and the engineered MSC (MSCANG1) overexpressing both the candidate pro-angiogenic gene, angiopoietin-1 (ANG1), and green fluorescent protein (GFP) was constructed using a lentiviral system. The pro-vascular stabilizing effects of MSCANG1 were assessed in primary endothelial cell cultures. Subsequently, MSCANG1 was transplanted into streptozotocin (STZ)-induced diabetic wound models to evaluate therapeutic effects on angiogenesis and wound healing. The underlying mechanisms were further examined both in vitro and in vivo. Results The comprehensive analysis of the temporal expression of pro- and anti-angiogenic factors revealed a consistent impairment in ANG1 expression throughout diabetic wound healing. MSCANG1 exhibited robust EGFP expression in 80% of cells, with overexpression and secretion of the ANG1 protein. MSCANG1 notably enhanced the survival and tubulogenesis of endothelial cells and promoted the expression of junction proteins, facilitating the establishment of functional vasculature with improved vascular leakage. Although MSCANG1 did not enhance the survival of engrafted MSCs in diabetic wounds, it significantly promoted angiogenesis in diabetic wound healing, fostering the establishment of stable vasculature during the healing process. Activation of the protein kinase B (Akt) pathway and suppression of proto-oncogene tyrosine kinase Src (Src) activity in MSCANG1-treated diabetic wounds confirmed efficient angiogenesis process. Consequently, epidermal and dermal reconstruction, as well as skin appendage regeneration were markedly accelerated in MSCANG1-treated diabetic wounds compared to MSC-treated wounds. Conclusion Treatment with MSCs alone promotes angiogenesis and DFU healing, while the engineering of MSCs with ANG1 provides substantial additional benefits to this therapeutic process. The engineering of MSCs with ANG1 presents a promising avenue for developing innovative strategies in managing DFU.
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spelling doaj-art-626dc675b4b84c3daebaaa83ddbb11112025-08-20T02:15:15ZengBMCStem Cell Research & Therapy1757-65122025-02-0116111610.1186/s13287-025-04207-7Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healingQiong Deng0Fangzhou Du1Shenzhen Pan2Yuchen Xia3Yuxin Zhu4Jingzhong Zhang5Chenglong Li6Shuang Yu7Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of SciencesSuzhou Institute of Biomedical Engineering and Technology, Chinese Academy of SciencesSuzhou Institute of Biomedical Engineering and Technology, Chinese Academy of SciencesSuzhou Institute of Biomedical Engineering and Technology, Chinese Academy of SciencesSuzhou Institute of Biomedical Engineering and Technology, Chinese Academy of SciencesSuzhou Institute of Biomedical Engineering and Technology, Chinese Academy of SciencesDepartment of Vascular Surgery, The Second Affiliated Hospital of Soochow UniversitySuzhou Institute of Biomedical Engineering and Technology, Chinese Academy of SciencesAbstract Background Vascular insufficiency is associated with the pathogenesis and therapeutic outcomes of diabetic foot ulcers (DFU). While mesenchymal stem cells (MSCs) hold potential for DFU treatment, further enhancement in promoting angiogenesis in the challenging DFU wounds is imperative. Methods The differential expression of pro- and anti-angiogenic factors during both normal and diabetic wound healing was compared using quantitative PCR. MSCs derived from the umbilical cord was prepared, and the engineered MSC (MSCANG1) overexpressing both the candidate pro-angiogenic gene, angiopoietin-1 (ANG1), and green fluorescent protein (GFP) was constructed using a lentiviral system. The pro-vascular stabilizing effects of MSCANG1 were assessed in primary endothelial cell cultures. Subsequently, MSCANG1 was transplanted into streptozotocin (STZ)-induced diabetic wound models to evaluate therapeutic effects on angiogenesis and wound healing. The underlying mechanisms were further examined both in vitro and in vivo. Results The comprehensive analysis of the temporal expression of pro- and anti-angiogenic factors revealed a consistent impairment in ANG1 expression throughout diabetic wound healing. MSCANG1 exhibited robust EGFP expression in 80% of cells, with overexpression and secretion of the ANG1 protein. MSCANG1 notably enhanced the survival and tubulogenesis of endothelial cells and promoted the expression of junction proteins, facilitating the establishment of functional vasculature with improved vascular leakage. Although MSCANG1 did not enhance the survival of engrafted MSCs in diabetic wounds, it significantly promoted angiogenesis in diabetic wound healing, fostering the establishment of stable vasculature during the healing process. Activation of the protein kinase B (Akt) pathway and suppression of proto-oncogene tyrosine kinase Src (Src) activity in MSCANG1-treated diabetic wounds confirmed efficient angiogenesis process. Consequently, epidermal and dermal reconstruction, as well as skin appendage regeneration were markedly accelerated in MSCANG1-treated diabetic wounds compared to MSC-treated wounds. Conclusion Treatment with MSCs alone promotes angiogenesis and DFU healing, while the engineering of MSCs with ANG1 provides substantial additional benefits to this therapeutic process. The engineering of MSCs with ANG1 presents a promising avenue for developing innovative strategies in managing DFU.https://doi.org/10.1186/s13287-025-04207-7Mesenchymal stem cellsAngiopoietin-1Diabetic Wound HealingAngiogenesisVascular leakage
spellingShingle Qiong Deng
Fangzhou Du
Shenzhen Pan
Yuchen Xia
Yuxin Zhu
Jingzhong Zhang
Chenglong Li
Shuang Yu
Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing
Stem Cell Research & Therapy
Mesenchymal stem cells
Angiopoietin-1
Diabetic Wound Healing
Angiogenesis
Vascular leakage
title Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing
title_full Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing
title_fullStr Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing
title_full_unstemmed Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing
title_short Activation of angiopoietin-1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing
title_sort activation of angiopoietin 1 signaling with engineering mesenchymal stem cells promoted efficient angiogenesis in diabetic wound healing
topic Mesenchymal stem cells
Angiopoietin-1
Diabetic Wound Healing
Angiogenesis
Vascular leakage
url https://doi.org/10.1186/s13287-025-04207-7
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