Characterization of IL-22 Bioactivity and IL-22-Positive Cells in Grass Carp Ctenopharyngodon idella

Yang, Yibing; Wang, Junya; Xu, Jiawen; Liu, Qin; Wang, Zixuan; Zhu, Xiao-Zhen; Ai, Xiaohui; Gao, Qian; Chen, Xinhua; Zou, Jun

doi:10.3389/fimmu.2020.586889

Cited by 25 publications

(5 citation statements)

References 50 publications

(107 reference statements)

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“…IL-22 is conserved in zebrafish (Igawa et al, 2006;Siupka et al, 2014) and also found in other fish species (Corripio-Miyar et al, 2009;Monte et al, 2011;Costa et al, 2013;Yang et al, 2020). In zebrafish, expression of IL-22 was seen in the intestine and gill at baseline and increased after a challenge with TLR agonists (LPS/Poly I:C) (Siupka et al, 2014).…”

Section: Function Of Interleukin 22 In Gut Microbial Compositionmentioning

confidence: 78%

Colonizing Microbes, IL-10 and IL-22: Keeping the Peace at the Mucosal Surface

2021

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Our world is filled with microbes. Each multicellular organism has developed ways to interact with this microbial environment. Microbes do not always pose a threat; they can contribute to many processes that benefit the host. Upon colonization both host and microbes adapt resulting in dynamic ecosystems in different host niches. Regulatory processes develop within the host to prevent overt inflammation to beneficial microbes, yet keeping the possibility to respond when pathogens attempt to adhere and invade tissues. This review will focus on microbial colonization and the early (innate) host immune response, with special emphasis on the microbiota-modifying roles of IL-10 and IL-22 in the intestine. IL-10 knock out mice show an altered microbial composition, and spontaneously develop enterocolitis over time. IL-22 knock out mice, although not developing enterocolitis spontaneously, also have an altered microbial composition and increase of epithelial-adherent bacteria, mainly caused by a decrease in mucin and anti-microbial peptide production. Recently interesting links have been found between the IL-10 and IL-22 pathways. While IL-22 can function as a regulatory cytokine at the mucosal surface, it also has inflammatory roles depending on the context. For example, lack of IL-22 in the IL-10–/– mice model prevents spontaneous colitis development. Additionally, the reduced microbial diversity observed in IL-10–/– mice was also reversed in IL-10/IL-22 double mutant mice (Gunasekera et al., 2020). Since in early life, host immunity develops in parallel and in interaction with colonizing microbes, there is a need for future studies that focus on the effect of the timing of colonization in relation to the developmental phase of the host. To illustrate this, examples from zebrafish research will be compared with studies performed in mammals. Since zebrafish develop from eggs and are directly exposed to the outside microbial world, timing of the development of host immunity and subsequent control of microbial composition, is different from mammals that develop in utero and only get exposed after birth. Likewise, colonization studies using adult germfree mice might yield different results from those using neonatal germfree mice. Lastly, special emphasis will be given to the need for host genotype and environmental (co-housing) control of experiments.

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Section: Function Of Interleukin 22 In Gut Microbial Compositionmentioning

confidence: 78%

Colonizing Microbes, IL-10 and IL-22: Keeping the Peace at the Mucosal Surface

2021

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“…In previous studies on IL-22RA1 KO mice, the induction of Bcl2115 , Nupr1 , and Chac1 transcripts was suggested to be associated with the IL-22/IL-22RA1 axis via STAT3 activation ( 52 ). Furthermore, a recombinant protein-based functional study on teleost IL-22 revealed that recombinant IL-22 can induce defb and hamp expression in rainbow trout ( 29 ), il1b expression in grass carp ( 56 ), and il22bp and hamp expression in mandarin fish ( 33 ). Thus, the phenotypic characteristics of IL-22-KO medaka showed several similarities with those reported in previous studies on the IL-22 induction abilities in mammals and teleosts.…”

Section: Discussionmentioning

confidence: 99%

Interleukin-22 Deficiency Contributes to Dextran Sulfate Sodium-Induced Inflammation in Japanese Medaka, Oryzias latipes

et al. 2021

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Mucosal tissue forms the first line of defense against pathogenic microorganisms. Cellular damage in the mucosal epithelium may induce the interleukin (IL)-22-related activation of many immune cells, which are essential for maintaining the mucosal epithelial barrier. A previous study on mucosal immunity elucidated that mammalian IL-22 contributes to mucus and antimicrobial peptides (AMPs) production and anti-apoptotic function. IL-22 has been identified in several teleost species and is also induced in response to bacterial infections. However, the roles of IL-22 in teleost immunity and mucus homeostasis are poorly understood. In this study, Japanese medaka (Oryzias latipes) was used as a model fish. The medaka il22, il22 receptor A1 (il22ra1), and il22 binding protein (il22bp) were cloned and characterized. The expression of medaka il22, il22ra1, and il22bp in various tissues was measured using qPCR. These genes were expressed at high levels in the mucosal tissues of the intestines, gills, and skin. The localization of il22 and il22bp mRNA in the gills and intestines was confirmed by in situ hybridizations. Herein, we established IL-22-knockout (KO) medaka using the CRISPR/Cas9 system. In the IL-22-KO medaka, a 4-bp deletion caused a frameshift in il22. To investigate the genes subject to IL-22-dependent regulation, we compared the transcripts of larval medaka between wild-type (WT) and IL-22-KO medaka using RNA-seq and qPCR analyses. The comparison was performed not only in the naïve state but also in the dextran sulfate sodium (DSS)-exposed state. At the transcriptional level, 368 genes, including immune genes, such as those encoding AMPs and cytokines, were significantly downregulated in IL-22-KO medaka compared that in WT medaka in naïve states. Gene ontology analysis revealed that upon DSS stimulation, genes associated with cell death, acute inflammatory response, cell proliferation, and others were upregulated in WT medaka. Furthermore, in DSS-stimulated IL-22-KO medaka, wound healing was delayed, the number of apoptotic cells increased, and the number of goblet cells in the intestinal epithelium decreased. These results suggested that in medaka, IL-22 is important for maintaining intestinal homeostasis, and the disruption of the IL-22 pathway is associated with the exacerbation of inflammatory pathology, as observed for mammalian IL-22.

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“…Gene syntenic relationships were analyzed using the Ensembl website (https://asia.ensembl. org/index.html) as previous studies on the IL-10 family [15,[33][34][35]. The NCBI genome databases, BioEdit and Ultra-Edit-32 programs, were used to analyze IL-10 family gene organizations in spotted sea bass.…”

Section: 3mentioning

confidence: 99%

Identification and Expression Analysis of IL-10 Family in Spotted Sea Bass (Lateolabrax maculatus)

Chen,

Gao,

et al. 2023

Aquaculture Research

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Interleukin (IL)-10 family members play important roles in regulating the immune responses during host defense. In the present study, four IL-10 family members (IL-10, IL-20L, IL-22, and IL-26) were identified from spotted sea bass (Lateolabrax maculatus) and their expression patterns were investigated following Edwardsiella tarda and lipopolysaccharide (LPS) challenge. The four ILs of spotted sea bass shared conserved features of IL-10 family and were well clustered with the IL-10 family of fish, respectively. The expressions of these four ILs in normal tissues were different, but all were highly expressed in gills, indicating their roles in mucosal immunity. After E. tarda and LPS challenge, the four ILs were upregulated in several immune-related tissues (gills, head kidney, intestine, and spleen). These results indicated that these four ILs involved in the antibacterial immune responses of spotted sea bass, providing basis for understanding the function and networks of IL-10 family members in fish.

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Characterization of IL-22 Bioactivity and IL-22-Positive Cells in Grass Carp Ctenopharyngodon idella

Cited by 25 publications

References 50 publications

Colonizing Microbes, IL-10 and IL-22: Keeping the Peace at the Mucosal Surface

Colonizing Microbes, IL-10 and IL-22: Keeping the Peace at the Mucosal Surface

Interleukin-22 Deficiency Contributes to Dextran Sulfate Sodium-Induced Inflammation in Japanese Medaka, Oryzias latipes

Identification and Expression Analysis of IL-10 Family in Spotted Sea Bass (Lateolabrax maculatus)

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