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Transcription Factor T-Bet in Atlantic Salmon: Characterization and Gene Expression in Mucosal Tissues during Aeromonas Salmonicida Infection.

Kumari J, Zhang Z, Swain T, Chi H, Niu C, Bøgwald J, Dalmo RA - Front Immunol (2015)

Bottom Line: Phylogenetic study and gene synteny revealed it is as a homolog to mammalian T-bet.Quantitative PCR analysis of different tissues in healthy fish showed that salmon T-bet gene was highly expressed in spleen, followed by head kidney, and was expressed in intestine, skin, and liver at lower levels.Moreover, the time-dependent expression profile of T-bet, interferon gamma (IFNγ), interleukin-22 (IL-22), and natural killer enhancement factor in mucosal tissues during water-borne infection with live Aeromonas salmonicida, indicated the involvement of T-bet in mucosal immune response in Atlantic salmon.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Biosciences, Fisheries and Economics, Norwegian College of Fishery Science, University of Tromsø , Tromsø , Norway ; Nofima , Tromsø , Norway.

ABSTRACT
The T-box transcription factor T-bet is expressed in a number of hematopoietic cell types in mammals and plays an essential role in the lineage determination of Th1 T-helper cells and is considered as an essential feature for both innate and adaptive immune responses in higher vertebrates. In the present study, we have identified and characterized the full-length Atlantic salmon T-bet cDNA (3502 bp). The putative primary structure of the polypeptide deduced from the cDNA sequence contained 612 aa, which possessed a T-box DNA binding domain. Phylogenetic study and gene synteny revealed it is as a homolog to mammalian T-bet. Quantitative PCR analysis of different tissues in healthy fish showed that salmon T-bet gene was highly expressed in spleen, followed by head kidney, and was expressed in intestine, skin, and liver at lower levels. Moreover, the time-dependent expression profile of T-bet, interferon gamma (IFNγ), interleukin-22 (IL-22), and natural killer enhancement factor in mucosal tissues during water-borne infection with live Aeromonas salmonicida, indicated the involvement of T-bet in mucosal immune response in Atlantic salmon.

No MeSH data available.


Related in: MedlinePlus

Phylogenetic tree showing the relationship of salmon T-bet gene with other known vertebrate members of the Tbr1 subfamily. The phylogram was constructed on ClustalX2 and MEGA 4.1. The neighbor-joining (N-J) method with bootstrap values of 1000 replications was adopted. Accession numbers or ENSEMBL gene IDs are as follows: Human (Homo sapiens) Eomes, NP_005433; Mouse (Mus musculus) Eomes, NP_034266; Cattle (Bos taurus) Eomes, NP_001178117; Frog (Xenopus laevis) Eomes, NP_001081810; Chicken (Gallus gallus), Eomes, XP_426003; Zebrafish (Danio rerio) Eomes a, NP_571754; Zebrafish Eomes b, NP_001077044; Salmon (Salmo salar) Eomes, EU418014; Amphioxus (Branchiostoma floridae) Eomes/Tbr1/Tbx21, AF262568; Human Tbr1, NP_006584; Mouse Tbr1, NP_033348.2; Cattle Tbr1, NP_001178978; Zebrafish Tbr1, NP_001108562; Human T-bet, NP_037483; Mouse T-bet, NP_062380; Cattle T-bet, NP_001179069; Pig (Sus scrofa) T-bet, ENSSSCP00000018565; Frog T-bet, NP_001088247; Lizard (Anolis carolinensis) T-bet, ENSACAP00000006911; Medaka (Oryzias latipes) T-bet, ENSORLP00000015259; Fugu (Takifugu rubripes) T-bet, ENSTRUP00000032964; Stickleback (Gasterosteus aculeatus) T-bet, ENSGACP00000005023; Tetraodon (Tetraodon nigroviridis) T-bet, ENSTNIP00000013001; Zebrafish T-bet, NP_001164070; Crucian carp (Carassius auratus langsdorfii) T-bet, BAF73805.1; Trout (Oncorhynchus mykiss) T-bet, NM_001182722.
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Figure 3: Phylogenetic tree showing the relationship of salmon T-bet gene with other known vertebrate members of the Tbr1 subfamily. The phylogram was constructed on ClustalX2 and MEGA 4.1. The neighbor-joining (N-J) method with bootstrap values of 1000 replications was adopted. Accession numbers or ENSEMBL gene IDs are as follows: Human (Homo sapiens) Eomes, NP_005433; Mouse (Mus musculus) Eomes, NP_034266; Cattle (Bos taurus) Eomes, NP_001178117; Frog (Xenopus laevis) Eomes, NP_001081810; Chicken (Gallus gallus), Eomes, XP_426003; Zebrafish (Danio rerio) Eomes a, NP_571754; Zebrafish Eomes b, NP_001077044; Salmon (Salmo salar) Eomes, EU418014; Amphioxus (Branchiostoma floridae) Eomes/Tbr1/Tbx21, AF262568; Human Tbr1, NP_006584; Mouse Tbr1, NP_033348.2; Cattle Tbr1, NP_001178978; Zebrafish Tbr1, NP_001108562; Human T-bet, NP_037483; Mouse T-bet, NP_062380; Cattle T-bet, NP_001179069; Pig (Sus scrofa) T-bet, ENSSSCP00000018565; Frog T-bet, NP_001088247; Lizard (Anolis carolinensis) T-bet, ENSACAP00000006911; Medaka (Oryzias latipes) T-bet, ENSORLP00000015259; Fugu (Takifugu rubripes) T-bet, ENSTRUP00000032964; Stickleback (Gasterosteus aculeatus) T-bet, ENSGACP00000005023; Tetraodon (Tetraodon nigroviridis) T-bet, ENSTNIP00000013001; Zebrafish T-bet, NP_001164070; Crucian carp (Carassius auratus langsdorfii) T-bet, BAF73805.1; Trout (Oncorhynchus mykiss) T-bet, NM_001182722.

Mentions: In Figure 2, a multiple alignment of amino acid sequence in salmon and other vertebrates is depicted. Salmon T-bet shared 96.6, 72.5, and 42.2% amino acid identity with rainbow trout, zebrafish, and human T-bet, respectively (Table S1 in Supplementary Material). Compared to teleost, there were gaps in both in the 5′ and 3′ end of the amino acid sequence in mammals, monkey, and mouse – especially at the 3′ end side, resulting in shorter and divergent sequences compared to those in teleost. The phylogenetic study (Figure 3) showed that teleost T-bet formed an independent clade, but grouped with mammalian T-bet with a high bootstrap value (96%) that was higher than the other members of Tbr1 subfamily. This finding supported the notion that the salmon T-bet is a real T-bet ortholog. Furthermore, gene synteny analysis (Figure 4) revealed it is a homolog to mammalian T-bet having the same loci order and orientation: OSBPL7, MRPL10, PNPO, PRR15L (except in tetraodon), CD5KPRAP3, NFE2L1, and CBX. In addition, TBKBP1 in fugu, tetraodon, medaka, zebrafish, human, and mouse was observed to, with the same orientation, locate in the same position as T-bet gene in the corresponding genome.


Transcription Factor T-Bet in Atlantic Salmon: Characterization and Gene Expression in Mucosal Tissues during Aeromonas Salmonicida Infection.

Kumari J, Zhang Z, Swain T, Chi H, Niu C, Bøgwald J, Dalmo RA - Front Immunol (2015)

Phylogenetic tree showing the relationship of salmon T-bet gene with other known vertebrate members of the Tbr1 subfamily. The phylogram was constructed on ClustalX2 and MEGA 4.1. The neighbor-joining (N-J) method with bootstrap values of 1000 replications was adopted. Accession numbers or ENSEMBL gene IDs are as follows: Human (Homo sapiens) Eomes, NP_005433; Mouse (Mus musculus) Eomes, NP_034266; Cattle (Bos taurus) Eomes, NP_001178117; Frog (Xenopus laevis) Eomes, NP_001081810; Chicken (Gallus gallus), Eomes, XP_426003; Zebrafish (Danio rerio) Eomes a, NP_571754; Zebrafish Eomes b, NP_001077044; Salmon (Salmo salar) Eomes, EU418014; Amphioxus (Branchiostoma floridae) Eomes/Tbr1/Tbx21, AF262568; Human Tbr1, NP_006584; Mouse Tbr1, NP_033348.2; Cattle Tbr1, NP_001178978; Zebrafish Tbr1, NP_001108562; Human T-bet, NP_037483; Mouse T-bet, NP_062380; Cattle T-bet, NP_001179069; Pig (Sus scrofa) T-bet, ENSSSCP00000018565; Frog T-bet, NP_001088247; Lizard (Anolis carolinensis) T-bet, ENSACAP00000006911; Medaka (Oryzias latipes) T-bet, ENSORLP00000015259; Fugu (Takifugu rubripes) T-bet, ENSTRUP00000032964; Stickleback (Gasterosteus aculeatus) T-bet, ENSGACP00000005023; Tetraodon (Tetraodon nigroviridis) T-bet, ENSTNIP00000013001; Zebrafish T-bet, NP_001164070; Crucian carp (Carassius auratus langsdorfii) T-bet, BAF73805.1; Trout (Oncorhynchus mykiss) T-bet, NM_001182722.
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Related In: Results  -  Collection

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Show All Figures
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Figure 3: Phylogenetic tree showing the relationship of salmon T-bet gene with other known vertebrate members of the Tbr1 subfamily. The phylogram was constructed on ClustalX2 and MEGA 4.1. The neighbor-joining (N-J) method with bootstrap values of 1000 replications was adopted. Accession numbers or ENSEMBL gene IDs are as follows: Human (Homo sapiens) Eomes, NP_005433; Mouse (Mus musculus) Eomes, NP_034266; Cattle (Bos taurus) Eomes, NP_001178117; Frog (Xenopus laevis) Eomes, NP_001081810; Chicken (Gallus gallus), Eomes, XP_426003; Zebrafish (Danio rerio) Eomes a, NP_571754; Zebrafish Eomes b, NP_001077044; Salmon (Salmo salar) Eomes, EU418014; Amphioxus (Branchiostoma floridae) Eomes/Tbr1/Tbx21, AF262568; Human Tbr1, NP_006584; Mouse Tbr1, NP_033348.2; Cattle Tbr1, NP_001178978; Zebrafish Tbr1, NP_001108562; Human T-bet, NP_037483; Mouse T-bet, NP_062380; Cattle T-bet, NP_001179069; Pig (Sus scrofa) T-bet, ENSSSCP00000018565; Frog T-bet, NP_001088247; Lizard (Anolis carolinensis) T-bet, ENSACAP00000006911; Medaka (Oryzias latipes) T-bet, ENSORLP00000015259; Fugu (Takifugu rubripes) T-bet, ENSTRUP00000032964; Stickleback (Gasterosteus aculeatus) T-bet, ENSGACP00000005023; Tetraodon (Tetraodon nigroviridis) T-bet, ENSTNIP00000013001; Zebrafish T-bet, NP_001164070; Crucian carp (Carassius auratus langsdorfii) T-bet, BAF73805.1; Trout (Oncorhynchus mykiss) T-bet, NM_001182722.
Mentions: In Figure 2, a multiple alignment of amino acid sequence in salmon and other vertebrates is depicted. Salmon T-bet shared 96.6, 72.5, and 42.2% amino acid identity with rainbow trout, zebrafish, and human T-bet, respectively (Table S1 in Supplementary Material). Compared to teleost, there were gaps in both in the 5′ and 3′ end of the amino acid sequence in mammals, monkey, and mouse – especially at the 3′ end side, resulting in shorter and divergent sequences compared to those in teleost. The phylogenetic study (Figure 3) showed that teleost T-bet formed an independent clade, but grouped with mammalian T-bet with a high bootstrap value (96%) that was higher than the other members of Tbr1 subfamily. This finding supported the notion that the salmon T-bet is a real T-bet ortholog. Furthermore, gene synteny analysis (Figure 4) revealed it is a homolog to mammalian T-bet having the same loci order and orientation: OSBPL7, MRPL10, PNPO, PRR15L (except in tetraodon), CD5KPRAP3, NFE2L1, and CBX. In addition, TBKBP1 in fugu, tetraodon, medaka, zebrafish, human, and mouse was observed to, with the same orientation, locate in the same position as T-bet gene in the corresponding genome.

Bottom Line: Phylogenetic study and gene synteny revealed it is as a homolog to mammalian T-bet.Quantitative PCR analysis of different tissues in healthy fish showed that salmon T-bet gene was highly expressed in spleen, followed by head kidney, and was expressed in intestine, skin, and liver at lower levels.Moreover, the time-dependent expression profile of T-bet, interferon gamma (IFNγ), interleukin-22 (IL-22), and natural killer enhancement factor in mucosal tissues during water-borne infection with live Aeromonas salmonicida, indicated the involvement of T-bet in mucosal immune response in Atlantic salmon.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Biosciences, Fisheries and Economics, Norwegian College of Fishery Science, University of Tromsø , Tromsø , Norway ; Nofima , Tromsø , Norway.

ABSTRACT
The T-box transcription factor T-bet is expressed in a number of hematopoietic cell types in mammals and plays an essential role in the lineage determination of Th1 T-helper cells and is considered as an essential feature for both innate and adaptive immune responses in higher vertebrates. In the present study, we have identified and characterized the full-length Atlantic salmon T-bet cDNA (3502 bp). The putative primary structure of the polypeptide deduced from the cDNA sequence contained 612 aa, which possessed a T-box DNA binding domain. Phylogenetic study and gene synteny revealed it is as a homolog to mammalian T-bet. Quantitative PCR analysis of different tissues in healthy fish showed that salmon T-bet gene was highly expressed in spleen, followed by head kidney, and was expressed in intestine, skin, and liver at lower levels. Moreover, the time-dependent expression profile of T-bet, interferon gamma (IFNγ), interleukin-22 (IL-22), and natural killer enhancement factor in mucosal tissues during water-borne infection with live Aeromonas salmonicida, indicated the involvement of T-bet in mucosal immune response in Atlantic salmon.

No MeSH data available.


Related in: MedlinePlus