Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of Macrophages

<i>P. multocida</i> is notorious for inducing excessive inflammation with high lethality in multiple animals, such as cattle, pigs, and chickens. Our previous study revealed that L-serine was decreased in the lungs of mice infected with <i>P. multocida</i> capsular type A str...

Full description

Saved in:
Bibliographic Details
Main Authors: Fang He, Zhengchun Lang, Yanlan Huang, Yangyang Qiu, Pan Xiong, Nengzhang Li, Guangfu Zhao, Yuanyi Peng
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Veterinary Sciences
Subjects:
Online Access:https://www.mdpi.com/2306-7381/12/3/254
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850277467752759296
author Fang He
Zhengchun Lang
Yanlan Huang
Yangyang Qiu
Pan Xiong
Nengzhang Li
Guangfu Zhao
Yuanyi Peng
author_facet Fang He
Zhengchun Lang
Yanlan Huang
Yangyang Qiu
Pan Xiong
Nengzhang Li
Guangfu Zhao
Yuanyi Peng
author_sort Fang He
collection DOAJ
description <i>P. multocida</i> is notorious for inducing excessive inflammation with high lethality in multiple animals, such as cattle, pigs, and chickens. Our previous study revealed that L-serine was decreased in the lungs of mice infected with <i>P. multocida</i> capsular type A strain CQ2 (PmCQ2), and 2 mg/kg of L-serine could alleviate PmCQ2-induced lung inflammation in vivo, which may largely depend on macrophages. However, the underlying intrinsic alterations remain unknown. Here, we demonstrated that 10 mM of L-serine significantly inhibited the release of inflammatory cytokines (e.g., IL-1β and TNF-α) by blocking inflammasome activation (including NALP1, NLRP3, NLRC4, AIM2, and Caspase-1) in PmCQ2-infected macrophages. Furthermore, the results of RNA-seq and metabonomics revealed that exogenous L-serine supplementation substantially reprogrammed macrophage transcription and metabolism. Mechanically, L-serine reduced inflammatory responses via the inhibition of glycolysis in macrophages based on a seahorse assay. Together, these findings characterize the intrinsic molecular alterations in activated macrophages and provide new targets for modulating <i>P. multocida</i> infection-induced macrophage inflammation.
format Article
id doaj-art-deec2f5553d44ec2b45384452d040757
institution OA Journals
issn 2306-7381
language English
publishDate 2025-03-01
publisher MDPI AG
record_format Article
series Veterinary Sciences
spelling doaj-art-deec2f5553d44ec2b45384452d0407572025-08-20T01:49:53ZengMDPI AGVeterinary Sciences2306-73812025-03-0112325410.3390/vetsci12030254Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of MacrophagesFang He0Zhengchun Lang1Yanlan Huang2Yangyang Qiu3Pan Xiong4Nengzhang Li5Guangfu Zhao6Yuanyi Peng7College of Veterinary Medicine, Southwest University, Chongqing 400715, ChinaCollege of Veterinary Medicine, Southwest University, Chongqing 400715, ChinaCollege of Veterinary Medicine, Southwest University, Chongqing 400715, ChinaCollege of Veterinary Medicine, Southwest University, Chongqing 400715, ChinaCollege of Veterinary Medicine, Southwest University, Chongqing 400715, ChinaCollege of Veterinary Medicine, Southwest University, Chongqing 400715, ChinaCollege of Veterinary Medicine, Southwest University, Chongqing 400715, ChinaCollege of Veterinary Medicine, Southwest University, Chongqing 400715, China<i>P. multocida</i> is notorious for inducing excessive inflammation with high lethality in multiple animals, such as cattle, pigs, and chickens. Our previous study revealed that L-serine was decreased in the lungs of mice infected with <i>P. multocida</i> capsular type A strain CQ2 (PmCQ2), and 2 mg/kg of L-serine could alleviate PmCQ2-induced lung inflammation in vivo, which may largely depend on macrophages. However, the underlying intrinsic alterations remain unknown. Here, we demonstrated that 10 mM of L-serine significantly inhibited the release of inflammatory cytokines (e.g., IL-1β and TNF-α) by blocking inflammasome activation (including NALP1, NLRP3, NLRC4, AIM2, and Caspase-1) in PmCQ2-infected macrophages. Furthermore, the results of RNA-seq and metabonomics revealed that exogenous L-serine supplementation substantially reprogrammed macrophage transcription and metabolism. Mechanically, L-serine reduced inflammatory responses via the inhibition of glycolysis in macrophages based on a seahorse assay. Together, these findings characterize the intrinsic molecular alterations in activated macrophages and provide new targets for modulating <i>P. multocida</i> infection-induced macrophage inflammation.https://www.mdpi.com/2306-7381/12/3/254L-serine<i>Pasteurella multocida</i>macrophageinflammasomemetabolic reprogramming
spellingShingle Fang He
Zhengchun Lang
Yanlan Huang
Yangyang Qiu
Pan Xiong
Nengzhang Li
Guangfu Zhao
Yuanyi Peng
Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of Macrophages
Veterinary Sciences
L-serine
<i>Pasteurella multocida</i>
macrophage
inflammasome
metabolic reprogramming
title Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of Macrophages
title_full Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of Macrophages
title_fullStr Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of Macrophages
title_full_unstemmed Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of Macrophages
title_short Exogenous L-Serine Alleviates <i>Pasteurella multocida</i>-Induced Inflammation by Reprogramming the Transcription and Metabolism of Macrophages
title_sort exogenous l serine alleviates i pasteurella multocida i induced inflammation by reprogramming the transcription and metabolism of macrophages
topic L-serine
<i>Pasteurella multocida</i>
macrophage
inflammasome
metabolic reprogramming
url https://www.mdpi.com/2306-7381/12/3/254
work_keys_str_mv AT fanghe exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages
AT zhengchunlang exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages
AT yanlanhuang exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages
AT yangyangqiu exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages
AT panxiong exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages
AT nengzhangli exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages
AT guangfuzhao exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages
AT yuanyipeng exogenouslserinealleviatesipasteurellamultocidaiinducedinflammationbyreprogrammingthetranscriptionandmetabolismofmacrophages