Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniae

ABSTRACTMultidrug-resistant Klebsiella pneumoniae strains, especially carbapenem-resistant K. pneumoniae, have become a rapidly emerging crisis worldwide, greatly limiting current therapeutic options and posing new challenges to infection management. Therefore, it is imperative to develop novel and...

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Main Authors: Wenting Wang, Yaozhen Chen, Yutong Chen, Erxiong Liu, Jing Li, Ning An, Jinmei Xu, Shunli Gu, Xuan Dang, Jing Yi, Qunxing An, Xingbin Hu, Wen Yin
Format: Article
Language:English
Published: American Society for Microbiology 2024-03-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.01279-23
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author Wenting Wang
Yaozhen Chen
Yutong Chen
Erxiong Liu
Jing Li
Ning An
Jinmei Xu
Shunli Gu
Xuan Dang
Jing Yi
Qunxing An
Xingbin Hu
Wen Yin
author_facet Wenting Wang
Yaozhen Chen
Yutong Chen
Erxiong Liu
Jing Li
Ning An
Jinmei Xu
Shunli Gu
Xuan Dang
Jing Yi
Qunxing An
Xingbin Hu
Wen Yin
author_sort Wenting Wang
collection DOAJ
description ABSTRACTMultidrug-resistant Klebsiella pneumoniae strains, especially carbapenem-resistant K. pneumoniae, have become a rapidly emerging crisis worldwide, greatly limiting current therapeutic options and posing new challenges to infection management. Therefore, it is imperative to develop novel and effective biological agents for the treatment of multidrug-resistant K. pneumoniae infections. Platelets play an important role in the development of inflammation and immune responses. The main component responsible for platelet antibacterial activity lies in the supernatant stimulated by gram-positive bacteria. However, little research has been conducted on the interaction of gram-negative bacteria with platelets. Therefore, we aimed to explore the bacteriostatic effect of the supernatant derived from platelet-K. pneumoniae coculture and the mechanism underlying this effect to further assess the potential of platelet-bacterial coculture supernatant. We conducted this study on the gram-negative bacteria K. pneumoniae and CRKP and detected turbidity changes in K. pneumoniae and CRKP cultures when grown with platelet-K. pneumoniae coculture supernatant added to the culture medium. We found that platelet-K. pneumoniae coculture supernatant significantly inhibited the growth of K. pneumoniae and CRKP in vitro. Furthermore, transfusion of platelet-K. pneumoniae coculture supernatant alleviated the symptoms of K. pneumoniae and CRKP infection in a murine model. Additionally, we observed apoptosis-like changes, such as phosphatidylserine exposure, chromosome condensation, DNA fragmentation, and overproduction of reactive oxygen species in K. pneumoniae following treatment with the supernatant. Our study demonstrates that the platelet-K. pneumoniae coculture supernatant can inhibit K. pneumoniae growth by inducing an apoptosis-like death, which is important for the antibacterial strategies development in the future.IMPORTANCEWith the widespread use of antibiotics, bacterial resistance is increasing, and a variety of multi-drug resistant Gram-negative bacteria have emerged, which brings great challenges to the treatment of infections caused by Gram-negative bacteria. Therefore, finding new strategies to inhibit Gram-negative bacteria and even multi-drug- resistant Gram-negative bacteria is crucial for treating infections caused by Gram-negative bacteria, improving the abuse of antibiotics, and maintaining the balance between bacteria and antibiotics. K. pneumoniae is a common clinical pathogen, and drug-resistant CRKP is increasingly difficult to cure, which brings great clinical challenges. In this study, we found that the platelet-K. pneumoniae coculture supernatant can inhibit K. pneumoniae growth by inducing an apoptosis-like death. This finding has inspired the development of future antimicrobial strategies, which are expected to improve the clinical treatment of Gram-negative bacteria and control the development of multidrug-resistant strains.
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spelling doaj.art-f74dcd2badbf4c50805540271d128fed2024-03-05T14:04:36ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-03-0112310.1128/spectrum.01279-23Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniaeWenting Wang0Yaozhen Chen1Yutong Chen2Erxiong Liu3Jing Li4Ning An5Jinmei Xu6Shunli Gu7Xuan Dang8Jing Yi9Qunxing An10Xingbin Hu11Wen Yin12Department of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaFaculty of Life Science College, Southwest Forestry University, Kunming, Yunnan, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaDepartment of Transfusion Medicine, Xijing Hospital, Fourth Military Medical University, Xi’an, Shaanxi, ChinaABSTRACTMultidrug-resistant Klebsiella pneumoniae strains, especially carbapenem-resistant K. pneumoniae, have become a rapidly emerging crisis worldwide, greatly limiting current therapeutic options and posing new challenges to infection management. Therefore, it is imperative to develop novel and effective biological agents for the treatment of multidrug-resistant K. pneumoniae infections. Platelets play an important role in the development of inflammation and immune responses. The main component responsible for platelet antibacterial activity lies in the supernatant stimulated by gram-positive bacteria. However, little research has been conducted on the interaction of gram-negative bacteria with platelets. Therefore, we aimed to explore the bacteriostatic effect of the supernatant derived from platelet-K. pneumoniae coculture and the mechanism underlying this effect to further assess the potential of platelet-bacterial coculture supernatant. We conducted this study on the gram-negative bacteria K. pneumoniae and CRKP and detected turbidity changes in K. pneumoniae and CRKP cultures when grown with platelet-K. pneumoniae coculture supernatant added to the culture medium. We found that platelet-K. pneumoniae coculture supernatant significantly inhibited the growth of K. pneumoniae and CRKP in vitro. Furthermore, transfusion of platelet-K. pneumoniae coculture supernatant alleviated the symptoms of K. pneumoniae and CRKP infection in a murine model. Additionally, we observed apoptosis-like changes, such as phosphatidylserine exposure, chromosome condensation, DNA fragmentation, and overproduction of reactive oxygen species in K. pneumoniae following treatment with the supernatant. Our study demonstrates that the platelet-K. pneumoniae coculture supernatant can inhibit K. pneumoniae growth by inducing an apoptosis-like death, which is important for the antibacterial strategies development in the future.IMPORTANCEWith the widespread use of antibiotics, bacterial resistance is increasing, and a variety of multi-drug resistant Gram-negative bacteria have emerged, which brings great challenges to the treatment of infections caused by Gram-negative bacteria. Therefore, finding new strategies to inhibit Gram-negative bacteria and even multi-drug- resistant Gram-negative bacteria is crucial for treating infections caused by Gram-negative bacteria, improving the abuse of antibiotics, and maintaining the balance between bacteria and antibiotics. K. pneumoniae is a common clinical pathogen, and drug-resistant CRKP is increasingly difficult to cure, which brings great clinical challenges. In this study, we found that the platelet-K. pneumoniae coculture supernatant can inhibit K. pneumoniae growth by inducing an apoptosis-like death. This finding has inspired the development of future antimicrobial strategies, which are expected to improve the clinical treatment of Gram-negative bacteria and control the development of multidrug-resistant strains.https://journals.asm.org/doi/10.1128/spectrum.01279-23plateletKlebsiella pneumoniaecarbapenem-resistant K. pneumoniaeinfectionreactive oxygen speciesapoptosis-like death
spellingShingle Wenting Wang
Yaozhen Chen
Yutong Chen
Erxiong Liu
Jing Li
Ning An
Jinmei Xu
Shunli Gu
Xuan Dang
Jing Yi
Qunxing An
Xingbin Hu
Wen Yin
Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniae
Microbiology Spectrum
platelet
Klebsiella pneumoniae
carbapenem-resistant K. pneumoniae
infection
reactive oxygen species
apoptosis-like death
title Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniae
title_full Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniae
title_fullStr Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniae
title_full_unstemmed Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniae
title_short Supernatant of platelet-Klebsiella pneumoniae coculture induces apoptosis-like death in Klebsiella pneumoniae
title_sort supernatant of platelet klebsiella pneumoniae coculture induces apoptosis like death in klebsiella pneumoniae
topic platelet
Klebsiella pneumoniae
carbapenem-resistant K. pneumoniae
infection
reactive oxygen species
apoptosis-like death
url https://journals.asm.org/doi/10.1128/spectrum.01279-23
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