Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickens
ABSTRACT: Avian pathogenic Escherichia coli (APEC) is a serious systemic infectious disease in poultry infections, causing severe economic losses to the poultry industry. Previous studies have shown that secretion of virulence proteins was required for the pathogenicity of APEC through the secretion...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2023-02-01
|
Series: | Poultry Science |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S0032579122006587 |
_version_ | 1811175501842087936 |
---|---|
author | Zhe Li Lulu Niu Lizhen Wang Ting Mei Wenbin Shang Xi Cheng Yuqing Li Feng Xi Xiangjun Song Ying Shao Yuping Xu Jian Tu |
author_facet | Zhe Li Lulu Niu Lizhen Wang Ting Mei Wenbin Shang Xi Cheng Yuqing Li Feng Xi Xiangjun Song Ying Shao Yuping Xu Jian Tu |
author_sort | Zhe Li |
collection | DOAJ |
description | ABSTRACT: Avian pathogenic Escherichia coli (APEC) is a serious systemic infectious disease in poultry infections, causing severe economic losses to the poultry industry. Previous studies have shown that secretion of virulence proteins was required for the pathogenicity of APEC through the secretion system. Outer membrane vesicles (OMVs) are a generalized secretion system of Gram-negative bacteria that play a key role in the long-distance delivery of virulence factors, but whether they are associated with the pathogenic mechanism of APEC has not been determined. In this study, OMVs were purified and characterized from AE17 (O2 serotype) by ultracentrifugation and density gradient centrifugation and their protein cargo was identified using liquid chromatography-tandem mass spectrometry (LC-MS/MS). In addition, 89Zr was labeled after chelating AE17 OMVs by DFO and positron emission tomography PET imaging was used to track 89Zr-DFO-OMVs in chickens and to pathologically analyze the distribution sites. This study showed that AE17 OMVs were membrane vesicles ranging in size from 20 to 200 nm and proteomic analysis revealed the presence of virulence proteins, including adhesion proteins OmpA, OmpC, OmpF, OmpX, FimH, FimC and FigE, and serum resistance proteins OmpT and MliC and immune response regulator proteins (FliC). In addition, in vivo PET imaging to track the biodistribution of AE17 OMVs showed that AE17 OMVs were taken up by the lung region and the gastrointestinal and renal regions but were not detected in other areas. Pathological analysis of the tissue sites where AE17 OMVs were ingested showed inflammatory responses and damage. These findings suggested that AE17 OMVs not only contained a group of virulence proteins associated with AE17 infection but can also deliver these virulence proteins over long distances and caused tissue inflammatory damage. Our study revealed a previously unidentified causative microbial signal in the pathogenesis of APEC that could aid in the development of vaccines and antibiotics effective against APEC. |
first_indexed | 2024-04-10T19:38:06Z |
format | Article |
id | doaj.art-d07b3097db6e4efc9a395aa8c61b4f8f |
institution | Directory Open Access Journal |
issn | 0032-5791 |
language | English |
last_indexed | 2024-04-10T19:38:06Z |
publishDate | 2023-02-01 |
publisher | Elsevier |
record_format | Article |
series | Poultry Science |
spelling | doaj.art-d07b3097db6e4efc9a395aa8c61b4f8f2023-01-30T04:11:26ZengElsevierPoultry Science0032-57912023-02-011022102364Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickensZhe Li0Lulu Niu1Lizhen Wang2Ting Mei3Wenbin Shang4Xi Cheng5Yuqing Li6Feng Xi7Xiangjun Song8Ying Shao9Yuping Xu10Jian Tu11Anhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, China; NHC Key Laboratory of Nuclear Medicine, Jiangsu Key Laboratory of Molecular Nuclear Medicine, Jiangsu Institute of Nuclear Medicine. Wuxi, Jiangsu 214063, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, ChinaNHC Key Laboratory of Nuclear Medicine, Jiangsu Key Laboratory of Molecular Nuclear Medicine, Jiangsu Institute of Nuclear Medicine. Wuxi, Jiangsu 214063, ChinaAnhui Province Engineering Laboratory for Animal Food Quality and Bio-safety, College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China; Anhui Province Key Laboratory of Veterinary Pathobiology and Disease Control, Anhui Agricultural University, Hefei 230036, China; Corresponding authors:ABSTRACT: Avian pathogenic Escherichia coli (APEC) is a serious systemic infectious disease in poultry infections, causing severe economic losses to the poultry industry. Previous studies have shown that secretion of virulence proteins was required for the pathogenicity of APEC through the secretion system. Outer membrane vesicles (OMVs) are a generalized secretion system of Gram-negative bacteria that play a key role in the long-distance delivery of virulence factors, but whether they are associated with the pathogenic mechanism of APEC has not been determined. In this study, OMVs were purified and characterized from AE17 (O2 serotype) by ultracentrifugation and density gradient centrifugation and their protein cargo was identified using liquid chromatography-tandem mass spectrometry (LC-MS/MS). In addition, 89Zr was labeled after chelating AE17 OMVs by DFO and positron emission tomography PET imaging was used to track 89Zr-DFO-OMVs in chickens and to pathologically analyze the distribution sites. This study showed that AE17 OMVs were membrane vesicles ranging in size from 20 to 200 nm and proteomic analysis revealed the presence of virulence proteins, including adhesion proteins OmpA, OmpC, OmpF, OmpX, FimH, FimC and FigE, and serum resistance proteins OmpT and MliC and immune response regulator proteins (FliC). In addition, in vivo PET imaging to track the biodistribution of AE17 OMVs showed that AE17 OMVs were taken up by the lung region and the gastrointestinal and renal regions but were not detected in other areas. Pathological analysis of the tissue sites where AE17 OMVs were ingested showed inflammatory responses and damage. These findings suggested that AE17 OMVs not only contained a group of virulence proteins associated with AE17 infection but can also deliver these virulence proteins over long distances and caused tissue inflammatory damage. Our study revealed a previously unidentified causative microbial signal in the pathogenesis of APEC that could aid in the development of vaccines and antibiotics effective against APEC.http://www.sciencedirect.com/science/article/pii/S0032579122006587avian pathogenic Escherichia coliouter membrane vesiclesproteomicsbiodistributionPETpathogenicity |
spellingShingle | Zhe Li Lulu Niu Lizhen Wang Ting Mei Wenbin Shang Xi Cheng Yuqing Li Feng Xi Xiangjun Song Ying Shao Yuping Xu Jian Tu Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickens Poultry Science avian pathogenic Escherichia coli outer membrane vesicles proteomics biodistribution PET pathogenicity |
title | Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickens |
title_full | Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickens |
title_fullStr | Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickens |
title_full_unstemmed | Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickens |
title_short | Biodistribution of 89Zr-DFO-labeled avian pathogenic Escherichia coli outer membrane vesicles by PET imaging in chickens |
title_sort | biodistribution of 89zr dfo labeled avian pathogenic escherichia coli outer membrane vesicles by pet imaging in chickens |
topic | avian pathogenic Escherichia coli outer membrane vesicles proteomics biodistribution PET pathogenicity |
url | http://www.sciencedirect.com/science/article/pii/S0032579122006587 |
work_keys_str_mv | AT zheli biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT luluniu biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT lizhenwang biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT tingmei biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT wenbinshang biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT xicheng biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT yuqingli biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT fengxi biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT xiangjunsong biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT yingshao biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT yupingxu biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens AT jiantu biodistributionof89zrdfolabeledavianpathogenicescherichiacolioutermembranevesiclesbypetimaginginchickens |