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Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization

Endothelial cell (EC)-derived signals contribute to organ regeneration, but angiocrine metabolic communication is not described. We found that EC-specific loss of the glycolytic regulator pfkfb3 reduced ischemic hindlimb revascularization and impaired muscle regeneration. This was caused by the redu...

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Autores principales: Zhang, Jing, Muri, Jonathan, Fitzgerald, Gillian, Gorski, Tatiane, Gianni-Barrera, Roberto, Masschelein, Evi, D’Hulst, Gommaar, Gilardoni, Paola, Turiel, Guillermo, Fan, Zheng, Wang, TongTong, Planque, Mélanie, Carmeliet, Peter, Pellerin, Luc, Wolfrum, Christian, Fendt, Sarah-Maria, Banfi, Andrea, Stockmann, Christian, Soro-Arnáiz, Inés, Kopf, Manfred, De Bock, Katrien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7267778/
https://www.ncbi.nlm.nih.gov/pubmed/32492393
http://dx.doi.org/10.1016/j.cmet.2020.05.004
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author Zhang, Jing
Muri, Jonathan
Fitzgerald, Gillian
Gorski, Tatiane
Gianni-Barrera, Roberto
Masschelein, Evi
D’Hulst, Gommaar
Gilardoni, Paola
Turiel, Guillermo
Fan, Zheng
Wang, TongTong
Planque, Mélanie
Carmeliet, Peter
Pellerin, Luc
Wolfrum, Christian
Fendt, Sarah-Maria
Banfi, Andrea
Stockmann, Christian
Soro-Arnáiz, Inés
Kopf, Manfred
De Bock, Katrien
author_facet Zhang, Jing
Muri, Jonathan
Fitzgerald, Gillian
Gorski, Tatiane
Gianni-Barrera, Roberto
Masschelein, Evi
D’Hulst, Gommaar
Gilardoni, Paola
Turiel, Guillermo
Fan, Zheng
Wang, TongTong
Planque, Mélanie
Carmeliet, Peter
Pellerin, Luc
Wolfrum, Christian
Fendt, Sarah-Maria
Banfi, Andrea
Stockmann, Christian
Soro-Arnáiz, Inés
Kopf, Manfred
De Bock, Katrien
author_sort Zhang, Jing
collection PubMed
description Endothelial cell (EC)-derived signals contribute to organ regeneration, but angiocrine metabolic communication is not described. We found that EC-specific loss of the glycolytic regulator pfkfb3 reduced ischemic hindlimb revascularization and impaired muscle regeneration. This was caused by the reduced ability of macrophages to adopt a proangiogenic and proregenerative M2-like phenotype. Mechanistically, loss of pfkfb3 reduced lactate secretion by ECs and lowered lactate levels in the ischemic muscle. Addition of lactate to pfkfb3-deficient ECs restored M2-like polarization in an MCT1-dependent fashion. Lactate shuttling by ECs enabled macrophages to promote proliferation and fusion of muscle progenitors. Moreover, VEGF production by lactate-polarized macrophages was increased, resulting in a positive feedback loop that further stimulated angiogenesis. Finally, increasing lactate levels during ischemia rescued macrophage polarization and improved muscle reperfusion and regeneration, whereas macrophage-specific mct1 deletion prevented M2-like polarization. In summary, ECs exploit glycolysis for angiocrine lactate shuttling to steer muscle regeneration from ischemia.
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spelling pubmed-72677782020-06-08 Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization Zhang, Jing Muri, Jonathan Fitzgerald, Gillian Gorski, Tatiane Gianni-Barrera, Roberto Masschelein, Evi D’Hulst, Gommaar Gilardoni, Paola Turiel, Guillermo Fan, Zheng Wang, TongTong Planque, Mélanie Carmeliet, Peter Pellerin, Luc Wolfrum, Christian Fendt, Sarah-Maria Banfi, Andrea Stockmann, Christian Soro-Arnáiz, Inés Kopf, Manfred De Bock, Katrien Cell Metab Article Endothelial cell (EC)-derived signals contribute to organ regeneration, but angiocrine metabolic communication is not described. We found that EC-specific loss of the glycolytic regulator pfkfb3 reduced ischemic hindlimb revascularization and impaired muscle regeneration. This was caused by the reduced ability of macrophages to adopt a proangiogenic and proregenerative M2-like phenotype. Mechanistically, loss of pfkfb3 reduced lactate secretion by ECs and lowered lactate levels in the ischemic muscle. Addition of lactate to pfkfb3-deficient ECs restored M2-like polarization in an MCT1-dependent fashion. Lactate shuttling by ECs enabled macrophages to promote proliferation and fusion of muscle progenitors. Moreover, VEGF production by lactate-polarized macrophages was increased, resulting in a positive feedback loop that further stimulated angiogenesis. Finally, increasing lactate levels during ischemia rescued macrophage polarization and improved muscle reperfusion and regeneration, whereas macrophage-specific mct1 deletion prevented M2-like polarization. In summary, ECs exploit glycolysis for angiocrine lactate shuttling to steer muscle regeneration from ischemia. Cell Press 2020-06-02 /pmc/articles/PMC7267778/ /pubmed/32492393 http://dx.doi.org/10.1016/j.cmet.2020.05.004 Text en © 2020 The Author(s) http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Zhang, Jing
Muri, Jonathan
Fitzgerald, Gillian
Gorski, Tatiane
Gianni-Barrera, Roberto
Masschelein, Evi
D’Hulst, Gommaar
Gilardoni, Paola
Turiel, Guillermo
Fan, Zheng
Wang, TongTong
Planque, Mélanie
Carmeliet, Peter
Pellerin, Luc
Wolfrum, Christian
Fendt, Sarah-Maria
Banfi, Andrea
Stockmann, Christian
Soro-Arnáiz, Inés
Kopf, Manfred
De Bock, Katrien
Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization
title Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization
title_full Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization
title_fullStr Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization
title_full_unstemmed Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization
title_short Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization
title_sort endothelial lactate controls muscle regeneration from ischemia by inducing m2-like macrophage polarization
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7267778/
https://www.ncbi.nlm.nih.gov/pubmed/32492393
http://dx.doi.org/10.1016/j.cmet.2020.05.004
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