Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarction

NETosis plays a pivotal role in the innate immune response after diabetic myocardial infarction (MI), exerting a profound influence on the overall pathological process and potential recovery outcomes. The metabolism of diabetic cardiomyocyte actively creates a specialized micro environment for the i...

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Main Authors: Song Yang, Longxin Yan, Lang Chen, Gaijuan Su, Long Yang, Lili Gong, Lihong Liu
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Pharmacological Research
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Online Access:http://www.sciencedirect.com/science/article/pii/S1043661825001562
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author Song Yang
Longxin Yan
Lang Chen
Gaijuan Su
Long Yang
Lili Gong
Lihong Liu
author_facet Song Yang
Longxin Yan
Lang Chen
Gaijuan Su
Long Yang
Lili Gong
Lihong Liu
author_sort Song Yang
collection DOAJ
description NETosis plays a pivotal role in the innate immune response after diabetic myocardial infarction (MI), exerting a profound influence on the overall pathological process and potential recovery outcomes. The metabolism of diabetic cardiomyocyte actively creates a specialized micro environment for the innate immune response after MI. However, the mechanism by which cardiac metabolism drives NETosis remains unclear. Utilizing public databases of human MI sc-RNA datasets, we discovered that cardiomyocyte PDK4 expression mediates the intensification of glycolysis, which is strongly correlated with NETosis. Through mass spectrometry imaging and phenotype assessment, we ascertained that specific knockout of PDK4 in cardiomyocytes (PDK4fl/flMyh6Cre, male, 6 weeks) led to a reduction in NETosis by restraining micro environmental lactate (LA) production. In addition, the role of LA in promoting NETosis has been further corroborated by in vivo/in vitro experiments involving LA supplementation and its absence. Moreover, LA redirects neutrophil metabolic flux from glycolysis to the pentose-phosphate pathway (PPP). Mechanistically, LA triggers metabolic remodeling through the PRMT9-mediated methylation of PFKL at the R301 residue, resulting in PFKL inactivation and the consequent restriction of glycolysis. Our findings reveal the crucial role of cardiomyocyte metabolism in NETosis, shedding light on the role of LA as a vital signaling molecule in the crosstalk between cardiomyocytes and neutrophils. Importantly, we screened pitavastatin, a potential inhibitor of PDK4 among the FDA-approved drugs, and verified that it can alleviate NETosis in diabetic MI, which provides a rationale for drug selection in diabetic MI patients.
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spelling doaj-art-8fe5f69a8d984a87b160c74b34e331ee2025-08-20T02:18:55ZengElsevierPharmacological Research1096-11862025-05-0121510773110.1016/j.phrs.2025.107731Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarctionSong Yang0Longxin Yan1Lang Chen2Gaijuan Su3Long Yang4Lili Gong5Lihong Liu6China-Japan Friendship Hospital, Beijing 100029, ChinaChina-Japan Friendship Hospital, Beijing 100029, ChinaChina-Japan Friendship Hospital, Beijing 100029, ChinaDongzhimen Hospital, Beijing University of Chinese Medicine, Beijing 100007, ChinaBeijing Chao-Yang Hospital, Capital Medical University, Beijing 100020, ChinaChina-Japan Friendship Hospital, Beijing 100029, China; Correspondence to: China-Japan Friendship Hospital, 2 Yinghuayuan East Street, Chaoyang District, Beijing 100029, China.China-Japan Friendship Hospital, Beijing 100029, China; Correspondence to: China-Japan Friendship Hospital, 2 Yinghuayuan East Street, Chaoyang District, Beijing 100029, China.NETosis plays a pivotal role in the innate immune response after diabetic myocardial infarction (MI), exerting a profound influence on the overall pathological process and potential recovery outcomes. The metabolism of diabetic cardiomyocyte actively creates a specialized micro environment for the innate immune response after MI. However, the mechanism by which cardiac metabolism drives NETosis remains unclear. Utilizing public databases of human MI sc-RNA datasets, we discovered that cardiomyocyte PDK4 expression mediates the intensification of glycolysis, which is strongly correlated with NETosis. Through mass spectrometry imaging and phenotype assessment, we ascertained that specific knockout of PDK4 in cardiomyocytes (PDK4fl/flMyh6Cre, male, 6 weeks) led to a reduction in NETosis by restraining micro environmental lactate (LA) production. In addition, the role of LA in promoting NETosis has been further corroborated by in vivo/in vitro experiments involving LA supplementation and its absence. Moreover, LA redirects neutrophil metabolic flux from glycolysis to the pentose-phosphate pathway (PPP). Mechanistically, LA triggers metabolic remodeling through the PRMT9-mediated methylation of PFKL at the R301 residue, resulting in PFKL inactivation and the consequent restriction of glycolysis. Our findings reveal the crucial role of cardiomyocyte metabolism in NETosis, shedding light on the role of LA as a vital signaling molecule in the crosstalk between cardiomyocytes and neutrophils. Importantly, we screened pitavastatin, a potential inhibitor of PDK4 among the FDA-approved drugs, and verified that it can alleviate NETosis in diabetic MI, which provides a rationale for drug selection in diabetic MI patients.http://www.sciencedirect.com/science/article/pii/S1043661825001562Diabetic myocardial infarctionPDK4NETosisLactatePFKL methylation
spellingShingle Song Yang
Longxin Yan
Lang Chen
Gaijuan Su
Long Yang
Lili Gong
Lihong Liu
Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarction
Pharmacological Research
Diabetic myocardial infarction
PDK4
NETosis
Lactate
PFKL methylation
title Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarction
title_full Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarction
title_fullStr Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarction
title_full_unstemmed Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarction
title_short Cardiac PDK4 promotes neutrophilic PFKL methylation and drives the innate immune response in diabetic myocardial infarction
title_sort cardiac pdk4 promotes neutrophilic pfkl methylation and drives the innate immune response in diabetic myocardial infarction
topic Diabetic myocardial infarction
PDK4
NETosis
Lactate
PFKL methylation
url http://www.sciencedirect.com/science/article/pii/S1043661825001562
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