Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophages

Abstract As the incessant emergence of drug-resistant bacterial strains, bacterial pneumonia poses a serious threat to the public health worldwide. There is an urgent need to explore unconventional therapeutic strategies. Carbon dots are usually designed to directly kill bacteria, however, carbon do...

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Main Authors: Xuan Jiang, Jun Wang, Lin Gan, Zengshuai Wu, Tong Wu, Fengyang Li, Xiaowei Xu, Liancheng Lei, Na Li
Format: Article
Language:English
Published: BMC 2025-04-01
Series:Journal of Nanobiotechnology
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Online Access:https://doi.org/10.1186/s12951-025-03399-7
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author Xuan Jiang
Jun Wang
Lin Gan
Zengshuai Wu
Tong Wu
Fengyang Li
Xiaowei Xu
Liancheng Lei
Na Li
author_facet Xuan Jiang
Jun Wang
Lin Gan
Zengshuai Wu
Tong Wu
Fengyang Li
Xiaowei Xu
Liancheng Lei
Na Li
author_sort Xuan Jiang
collection DOAJ
description Abstract As the incessant emergence of drug-resistant bacterial strains, bacterial pneumonia poses a serious threat to the public health worldwide. There is an urgent need to explore unconventional therapeutic strategies. Carbon dots are usually designed to directly kill bacteria, however, carbon dots that enhance the anti-infection function of immune cells are rarely reported. In the present study, CDots were synthesized with ascorbic acid and polyethyleneimine, exhibiting outstanding biocompatibility. Functionally, the CDots exhibited a well therapeutic impact on bacterial pneumonia induced by gram-positive multidrug-resistant Staphylococcus aureus (MRSA) or gram-negative Klebsiella pneumoniae (K. pneumoniae) in mice. Utilizing in vitro models of macrophages infected with MRSA and K. pneumoniae, we discovered that CDots augmented the M1 polarization of macrophages, subsequently enhancing their survival and activity of phagocytosis and bactericidal. Further investigations through molecular dynamics simulations and in vitro experiments validated that CDots directly bind to the catalytic subunit (PIK3CD) of phosphoinositide 3-kinase (PI3K), resulting in the inhibition of the PI3K/AKT/mTOR signaling pathway. Moreover, the crucial domain for the binding was located in amino acids 752–787 of PIK3CD. In summary, CDots exerted a protective effect on bacterial pneumonia by targeting the PIK3CD and fostering the PI3K-mediated M1 polarization of macrophages. These findings not only reveal a new role of CDots in the treatment of bacterial pneumonia, but also provide potential targets for future treatment strategies. Graphical Abstract
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spelling doaj-art-1e6c443451e546bebaadcaf868bb481a2025-08-20T02:19:57ZengBMCJournal of Nanobiotechnology1477-31552025-04-0123111610.1186/s12951-025-03399-7Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophagesXuan Jiang0Jun Wang1Lin Gan2Zengshuai Wu3Tong Wu4Fengyang Li5Xiaowei Xu6Liancheng Lei7Na Li8State Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityState Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityState Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityState Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityState Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityState Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityJilin Provincial Key Laboratory of Tooth Development and Bone Remodeling, School and Hospital of Stomatology Jilin UniversityState Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityState Key Laboratory for Diagnosis and Treatment of Severe Zoonotic Infectious Diseases, Key Laboratory for Zoonosis Research of the Ministry of Education Institute of Zoonosis, College of Veterinary Medicine, Jilin UniversityAbstract As the incessant emergence of drug-resistant bacterial strains, bacterial pneumonia poses a serious threat to the public health worldwide. There is an urgent need to explore unconventional therapeutic strategies. Carbon dots are usually designed to directly kill bacteria, however, carbon dots that enhance the anti-infection function of immune cells are rarely reported. In the present study, CDots were synthesized with ascorbic acid and polyethyleneimine, exhibiting outstanding biocompatibility. Functionally, the CDots exhibited a well therapeutic impact on bacterial pneumonia induced by gram-positive multidrug-resistant Staphylococcus aureus (MRSA) or gram-negative Klebsiella pneumoniae (K. pneumoniae) in mice. Utilizing in vitro models of macrophages infected with MRSA and K. pneumoniae, we discovered that CDots augmented the M1 polarization of macrophages, subsequently enhancing their survival and activity of phagocytosis and bactericidal. Further investigations through molecular dynamics simulations and in vitro experiments validated that CDots directly bind to the catalytic subunit (PIK3CD) of phosphoinositide 3-kinase (PI3K), resulting in the inhibition of the PI3K/AKT/mTOR signaling pathway. Moreover, the crucial domain for the binding was located in amino acids 752–787 of PIK3CD. In summary, CDots exerted a protective effect on bacterial pneumonia by targeting the PIK3CD and fostering the PI3K-mediated M1 polarization of macrophages. These findings not only reveal a new role of CDots in the treatment of bacterial pneumonia, but also provide potential targets for future treatment strategies. Graphical Abstracthttps://doi.org/10.1186/s12951-025-03399-7Carbon DotsMultidrug-resistantBacterial pneumoniaPIK3CDMacrophage polarization
spellingShingle Xuan Jiang
Jun Wang
Lin Gan
Zengshuai Wu
Tong Wu
Fengyang Li
Xiaowei Xu
Liancheng Lei
Na Li
Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophages
Journal of Nanobiotechnology
Carbon Dots
Multidrug-resistant
Bacterial pneumonia
PIK3CD
Macrophage polarization
title Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophages
title_full Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophages
title_fullStr Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophages
title_full_unstemmed Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophages
title_short Carbon dot-based treatment for bacterial pneumonia by promoting a PI3K-mediated M1 polarization of macrophages
title_sort carbon dot based treatment for bacterial pneumonia by promoting a pi3k mediated m1 polarization of macrophages
topic Carbon Dots
Multidrug-resistant
Bacterial pneumonia
PIK3CD
Macrophage polarization
url https://doi.org/10.1186/s12951-025-03399-7
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