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Viruses. 2018 May 18;10(5). pii: E270. doi: 10.3390/v10050270.

Avian Influenza Virus Subtype H9N2 Affects Intestinal Microbiota, Barrier Structure Injury, and Inflammatory Intestinal Disease in the Chicken Ileum.

Li H1,2,3,4, Liu X5,6,7,8, Chen F9,10,11,12, Zuo K13, Wu C14,15,16,17,18, Yan Y19,20,21,22, Chen W23,24,25,26,27, Lin W28,29,30,31,32, Xie Q33,34,35,36,37.

Author information

1
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. dongkeoffice@scau.edu.cn.
2
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. dongkeoffice@scau.edu.cn.
3
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. dongkeoffice@scau.edu.cn.
4
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. dongkeoffice@scau.edu.cn.
5
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. fky19842004@163.com.
6
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. fky19842004@163.com.
7
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. fky19842004@163.com.
8
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. fky19842004@163.com.
9
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. cfy329@scau.edu.cn.
10
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. cfy329@scau.edu.cn.
11
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. cfy329@scau.edu.cn.
12
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. cfy329@scau.edu.cn.
13
Veterinary Laboratory, Guangzhou Zoo, Guangzhou 510642, China. hnlhxin@126.com.
14
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. che.w@foxmail.com.
15
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. che.w@foxmail.com.
16
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. che.w@foxmail.com.
17
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. che.w@foxmail.com.
18
South China Collaborative Innovation Center for Poultry Disease Control and Product Safety, Guangzhou 510642, China. che.w@foxmail.com.
19
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. liaozhihong@163.com.
20
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. liaozhihong@163.com.
21
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. liaozhihong@163.com.
22
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. liaozhihong@163.com.
23
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. wgchen81@scau.edu.cn.
24
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. wgchen81@scau.edu.cn.
25
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. wgchen81@scau.edu.cn.
26
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. wgchen81@scau.edu.cn.
27
South China Collaborative Innovation Center for Poultry Disease Control and Product Safety, Guangzhou 510642, China. wgchen81@scau.edu.cn.
28
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. wenchenglin@scau.edu.cn.
29
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. wenchenglin@scau.edu.cn.
30
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. wenchenglin@scau.edu.cn.
31
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. wenchenglin@scau.edu.cn.
32
South China Collaborative Innovation Center for Poultry Disease Control and Product Safety, Guangzhou 510642, China. wenchenglin@scau.edu.cn.
33
College of Animal Science, South China Agricultural University, Guangzhou 510642, China. qmx@scau.edu.cn.
34
Key Laboratory of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, Guangzhou 510642, China. qmx@scau.edu.cn.
35
Key Laboratory of Animal Health Aquaculture and Environmental Control, Guangdong, Guangzhou 510642, China. qmx@scau.edu.cn.
36
Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangzhou 510642, China. qmx@scau.edu.cn.
37
South China Collaborative Innovation Center for Poultry Disease Control and Product Safety, Guangzhou 510642, China. qmx@scau.edu.cn.

Abstract

Avian influenza virus subtype H9N2 (H9N2 AIV) has caused significant losses to the poultry industry due to the high mortality associated with secondary infections attributable to E. coli. This study tries to address the underlying secondary mechanisms after H9N2 AIV infection. Initially, nine day-old specific pathogen-free chickens were assigned to control (uninfected) and H9N2-infected groups, respectively. Using Illumina sequencing, histological examination, and quantitative real-time PCR, it was found that H9N2 AIV caused intestinal microbiota disorder, injury, and inflammatory damage to the intestinal mucosa. Notably, the genera Escherichia, especially E. coli, significantly increased (p < 0.01) at five days post-infection (dpi), while Lactobacillus, Enterococcus, and other probiotic organisms were significantly reduced (p < 0.01). Simultaneously, the mRNA expression of tight junction proteins (ZO-1, claudin 3, and occludin), TFF2, and Muc2 were significantly reduced (p < 0.01), indicating the destruction of the intestinal epithelial cell tight junctions and the damage of mucin layer construction. Moreover, the mRNA expression of proinflammatory cytokines IFN-γ, IL-22, IFN-α, and IL-17A in intestinal epithelial cells were significantly upregulated, resulting in the inflammatory response and intestinal injury. Our findings may provide a theoretical basis for observed gastroenteritis-like symptoms such as diarrhea and secondary E. coli infection following H9N2 AIV infection.

KEYWORDS:

E. coli; H9N2 AIV; barrier injury; inflammatory intestinal disease; intestinal microbiota

PMID:
29783653
PMCID:
PMC5977263
DOI:
10.3390/v10050270
[Indexed for MEDLINE]
Free PMC Article

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