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Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation

Obesity-induced metabolic syndrome is a rapidly growing conundrum, reaching epidemic proportions globally. Chronic inflammation in obese adipose tissue plays a key role in metabolic syndrome with a series of local and systemic effects such as inflammatory cell infiltration and inflammatory cytokine...

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Autores principales: Lin, Zhuomiao, Lin, Xiaochun, Lai, Ying, Han, Congcong, Fan, Xinran, Tang, Jie, Mo, Shiqi, Su, Jiahui, Liang, Sijia, Shang, Jinyan, Lv, Xiaofei, Guo, Siwan, Pang, Ruiping, Zhou, Jiaguo, Zhang, Tingting, Zhang, Feiran
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9705588/
https://www.ncbi.nlm.nih.gov/pubmed/36457708
http://dx.doi.org/10.3389/fphar.2022.1040999
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author Lin, Zhuomiao
Lin, Xiaochun
Lai, Ying
Han, Congcong
Fan, Xinran
Tang, Jie
Mo, Shiqi
Su, Jiahui
Liang, Sijia
Shang, Jinyan
Lv, Xiaofei
Guo, Siwan
Pang, Ruiping
Zhou, Jiaguo
Zhang, Tingting
Zhang, Feiran
author_facet Lin, Zhuomiao
Lin, Xiaochun
Lai, Ying
Han, Congcong
Fan, Xinran
Tang, Jie
Mo, Shiqi
Su, Jiahui
Liang, Sijia
Shang, Jinyan
Lv, Xiaofei
Guo, Siwan
Pang, Ruiping
Zhou, Jiaguo
Zhang, Tingting
Zhang, Feiran
author_sort Lin, Zhuomiao
collection PubMed
description Obesity-induced metabolic syndrome is a rapidly growing conundrum, reaching epidemic proportions globally. Chronic inflammation in obese adipose tissue plays a key role in metabolic syndrome with a series of local and systemic effects such as inflammatory cell infiltration and inflammatory cytokine secretion. Adipose tissue macrophages (ATM), as one of the main regulators in this process, are particularly crucial for pharmacological studies on obesity-related metabolic syndrome. Ponatinib, a multi-targeted tyrosine kinase inhibitor originally used to treat leukemia, has recently been found to improve dyslipidemia and atherosclerosis, suggesting that it may have profound effect on metabolic syndrome, although the mechanisms underlying have not yet been revealed. Here we discovered that ponatinib significantly improved insulin sensitivity in leptin deficient obese mice. In addition to that, ponatinib treatment remarkably ameliorated high fat diet-induced hyperlipidemia and inhibited ectopic lipid deposition in the liver. Interestingly, although ponatinib did not reduce but increase the weight of white adipose tissue (WAT), it remarkably suppressed the inflammatory response in WAT and preserved its function. Mechanistically, we showed that ponatinib had no direct effect on hepatocyte or adipocyte but attenuated free fatty acid (FFA) induced macrophage transformation from pro-inflammatory to anti-inflammatory phenotype. Moreover, adipocytes co-cultured with FFA-treated macrophages exhibited insulin resistance, while pre-treat these macrophages with ponatinib can ameliorate this process. These results suggested that the beneficial effects of ponatinib on metabolic disorders are achieved by inhibiting the inflammatory phenotypic transformation of ATMs, thereby maintaining the physiological function of adipose tissue under excessive obesity. The data here not only revealed the novel therapeutic function of ponatinib, but also provided a theoretical basis for the application of multi-target tyrosine kinase inhibitors in metabolic diseases.
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spelling pubmed-97055882022-11-30 Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation Lin, Zhuomiao Lin, Xiaochun Lai, Ying Han, Congcong Fan, Xinran Tang, Jie Mo, Shiqi Su, Jiahui Liang, Sijia Shang, Jinyan Lv, Xiaofei Guo, Siwan Pang, Ruiping Zhou, Jiaguo Zhang, Tingting Zhang, Feiran Front Pharmacol Pharmacology Obesity-induced metabolic syndrome is a rapidly growing conundrum, reaching epidemic proportions globally. Chronic inflammation in obese adipose tissue plays a key role in metabolic syndrome with a series of local and systemic effects such as inflammatory cell infiltration and inflammatory cytokine secretion. Adipose tissue macrophages (ATM), as one of the main regulators in this process, are particularly crucial for pharmacological studies on obesity-related metabolic syndrome. Ponatinib, a multi-targeted tyrosine kinase inhibitor originally used to treat leukemia, has recently been found to improve dyslipidemia and atherosclerosis, suggesting that it may have profound effect on metabolic syndrome, although the mechanisms underlying have not yet been revealed. Here we discovered that ponatinib significantly improved insulin sensitivity in leptin deficient obese mice. In addition to that, ponatinib treatment remarkably ameliorated high fat diet-induced hyperlipidemia and inhibited ectopic lipid deposition in the liver. Interestingly, although ponatinib did not reduce but increase the weight of white adipose tissue (WAT), it remarkably suppressed the inflammatory response in WAT and preserved its function. Mechanistically, we showed that ponatinib had no direct effect on hepatocyte or adipocyte but attenuated free fatty acid (FFA) induced macrophage transformation from pro-inflammatory to anti-inflammatory phenotype. Moreover, adipocytes co-cultured with FFA-treated macrophages exhibited insulin resistance, while pre-treat these macrophages with ponatinib can ameliorate this process. These results suggested that the beneficial effects of ponatinib on metabolic disorders are achieved by inhibiting the inflammatory phenotypic transformation of ATMs, thereby maintaining the physiological function of adipose tissue under excessive obesity. The data here not only revealed the novel therapeutic function of ponatinib, but also provided a theoretical basis for the application of multi-target tyrosine kinase inhibitors in metabolic diseases. Frontiers Media S.A. 2022-11-15 /pmc/articles/PMC9705588/ /pubmed/36457708 http://dx.doi.org/10.3389/fphar.2022.1040999 Text en Copyright © 2022 Lin, Lin, Lai, Han, Fan, Tang, Mo, Su, Liang, Shang, Lv, Guo, Pang, Zhou, Zhang and Zhang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Pharmacology
Lin, Zhuomiao
Lin, Xiaochun
Lai, Ying
Han, Congcong
Fan, Xinran
Tang, Jie
Mo, Shiqi
Su, Jiahui
Liang, Sijia
Shang, Jinyan
Lv, Xiaofei
Guo, Siwan
Pang, Ruiping
Zhou, Jiaguo
Zhang, Tingting
Zhang, Feiran
Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation
title Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation
title_full Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation
title_fullStr Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation
title_full_unstemmed Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation
title_short Ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation
title_sort ponatinib modulates the metabolic profile of obese mice by inhibiting adipose tissue macrophage inflammation
topic Pharmacology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9705588/
https://www.ncbi.nlm.nih.gov/pubmed/36457708
http://dx.doi.org/10.3389/fphar.2022.1040999
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