MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954

Klebsiella variicola is a member of Klebsiella pneumoniae complex and an emerging zoonotic pathogen. As part of the lymphatic system, the spleen plays a pivotal role in destroying invading pathogens. Various microRNAs (miRNAs) are involved in host resistance to pathogens. However, specific miRNAs th...

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Main Authors: Lei Yin, Xuehuai Shen, Dongdong Yin, Hongyan Hou, Jieru Wang, Ruihong Zhao, Kezong Qi, Yin Dai, Xiaocheng Pan
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Cellular and Infection Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2025.1544506/full
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author Lei Yin
Lei Yin
Xuehuai Shen
Xuehuai Shen
Dongdong Yin
Dongdong Yin
Hongyan Hou
Hongyan Hou
Jieru Wang
Jieru Wang
Ruihong Zhao
Ruihong Zhao
Kezong Qi
Yin Dai
Yin Dai
Xiaocheng Pan
Xiaocheng Pan
author_facet Lei Yin
Lei Yin
Xuehuai Shen
Xuehuai Shen
Dongdong Yin
Dongdong Yin
Hongyan Hou
Hongyan Hou
Jieru Wang
Jieru Wang
Ruihong Zhao
Ruihong Zhao
Kezong Qi
Yin Dai
Yin Dai
Xiaocheng Pan
Xiaocheng Pan
author_sort Lei Yin
collection DOAJ
description Klebsiella variicola is a member of Klebsiella pneumoniae complex and an emerging zoonotic pathogen. As part of the lymphatic system, the spleen plays a pivotal role in destroying invading pathogens. Various microRNAs (miRNAs) are involved in host resistance to pathogens. However, specific miRNAs that act against K. variicola remain unknown. Therefore, RNA sequencing (RNA-Seq) of the miRNA profile of the chicken spleen was conducted to further clarify the host immune response to K. variicola infection. Challenge of 7-day-old chicks with K. variicola strain AHKV-S01 caused severe damage and enlargement of the spleen. In total, 22 differentially expressed (DE) miRNAs (fold change>2, q< 0.05) were identified. Functional annotation analysis of the target genes of DE miRNAs found that signaling pathways related to innate immunity, inflammation, and metabolism were significantly enriched. Notably, expression of gga-miR-2954 was significantly upregulated in the infection group as compared to the control group. In vitro, gga-miR-2954 directly repressed luciferase reporter gene activity by binding to the 3′ untranslated regions of STAB1. Overexpression of gga-miR-2954 in HD11 macrophages significantly inhibited expression of STAB1, which is involved in activation of several proinflammatory cytokines. K. variicola induced damage to the spleen by over activation of inflammatory and innate immune responses. The observed changes to the miRNA expression profile of the chicken spleen elucidate host immune responses to K. variicola infection, providing critical insights for developing novel therapeutic strategies to enhance chicken resistance against this pathogen.
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spelling doaj-art-77d41efdb71645708f562b64cb89d8ce2025-08-20T02:57:17ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882025-05-011510.3389/fcimb.2025.15445061544506MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954Lei Yin0Lei Yin1Xuehuai Shen2Xuehuai Shen3Dongdong Yin4Dongdong Yin5Hongyan Hou6Hongyan Hou7Jieru Wang8Jieru Wang9Ruihong Zhao10Ruihong Zhao11Kezong Qi12Yin Dai13Yin Dai14Xiaocheng Pan15Xiaocheng Pan16Livestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaLivestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaLivestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaLivestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaLivestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaLivestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, College of Animal Science and Technology, Anhui Agricultural University, Hefei, ChinaLivestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaLivestock and Poultry Epidemic Diseases Research Center of Anhui Province, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaAnhui Province Key Laboratory of Livestock and Poultry Product Safety, Institute of Animal Husbandry and Veterinary Science, Anhui Academy of Agricultural Sciences, Hefei, Anhui, ChinaKlebsiella variicola is a member of Klebsiella pneumoniae complex and an emerging zoonotic pathogen. As part of the lymphatic system, the spleen plays a pivotal role in destroying invading pathogens. Various microRNAs (miRNAs) are involved in host resistance to pathogens. However, specific miRNAs that act against K. variicola remain unknown. Therefore, RNA sequencing (RNA-Seq) of the miRNA profile of the chicken spleen was conducted to further clarify the host immune response to K. variicola infection. Challenge of 7-day-old chicks with K. variicola strain AHKV-S01 caused severe damage and enlargement of the spleen. In total, 22 differentially expressed (DE) miRNAs (fold change>2, q< 0.05) were identified. Functional annotation analysis of the target genes of DE miRNAs found that signaling pathways related to innate immunity, inflammation, and metabolism were significantly enriched. Notably, expression of gga-miR-2954 was significantly upregulated in the infection group as compared to the control group. In vitro, gga-miR-2954 directly repressed luciferase reporter gene activity by binding to the 3′ untranslated regions of STAB1. Overexpression of gga-miR-2954 in HD11 macrophages significantly inhibited expression of STAB1, which is involved in activation of several proinflammatory cytokines. K. variicola induced damage to the spleen by over activation of inflammatory and innate immune responses. The observed changes to the miRNA expression profile of the chicken spleen elucidate host immune responses to K. variicola infection, providing critical insights for developing novel therapeutic strategies to enhance chicken resistance against this pathogen.https://www.frontiersin.org/articles/10.3389/fcimb.2025.1544506/fullKlebsiella variicolaspleenmiRNAsimmune responseinflammation
spellingShingle Lei Yin
Lei Yin
Xuehuai Shen
Xuehuai Shen
Dongdong Yin
Dongdong Yin
Hongyan Hou
Hongyan Hou
Jieru Wang
Jieru Wang
Ruihong Zhao
Ruihong Zhao
Kezong Qi
Yin Dai
Yin Dai
Xiaocheng Pan
Xiaocheng Pan
MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954
Frontiers in Cellular and Infection Microbiology
Klebsiella variicola
spleen
miRNAs
immune response
inflammation
title MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954
title_full MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954
title_fullStr MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954
title_full_unstemmed MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954
title_short MicroRNA warfare: how chickens combat Klebsiella variicola with gga-miR-2954
title_sort microrna warfare how chickens combat klebsiella variicola with gga mir 2954
topic Klebsiella variicola
spleen
miRNAs
immune response
inflammation
url https://www.frontiersin.org/articles/10.3389/fcimb.2025.1544506/full
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