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A preliminary analysis of the immunoglobulin genes in the African elephant (Loxodonta africana).

Guo Y, Bao Y, Wang H, Hu X, Zhao Z, Li N, Zhao Y - PLoS ONE (2011)

Bottom Line: The Igκ locus, found on three scaffolds (202, 50 and 86), contains a total of 153 V(κ) gene segments, three J(κ) segments, and a single C(κ) gene.These data suggest that the elephant immunoglobulin gene repertoire is highly diverse and complex.Our results provide insights into the immunoglobulin genes in a placental mammal that is evolutionarily distant from humans, mice, and domestic animals.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of AgroBiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People's Republic of China.

ABSTRACT
The genomic organization of the IgH (Immunoglobulin heavy chain), Igκ (Immunoglobulin kappa chain), and Igλ (Immunoglobulin lambda chain) loci in the African elephant (Loxodonta africana) was annotated using available genome data. The elephant IgH locus on scaffold 57 spans over 2,974 kb, and consists of at least 112 V(H) gene segments, 87 D(H) gene segments (the largest number in mammals examined so far), six J(H) gene segments, a single μ, a δ remnant, and eight γ genes (α and ε genes are missing, most likely due to sequence gaps). The Igκ locus, found on three scaffolds (202, 50 and 86), contains a total of 153 V(κ) gene segments, three J(κ) segments, and a single C(κ) gene. Two different transcriptional orientations were determined for these V(κ) gene segments. In contrast, the Igλ locus on scaffold 68 includes 15 V(λ) gene segments, all with the same transcriptional polarity as the downstream J(λ)-C(λ) cluster. These data suggest that the elephant immunoglobulin gene repertoire is highly diverse and complex. Our results provide insights into the immunoglobulin genes in a placental mammal that is evolutionarily distant from humans, mice, and domestic animals.

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Alignment of the amino acid sequences of the nine elephant γ genes.The deduced amino acid sequences of three γ chain-coding exons and two membrane exons of nine elephant γ genes are aligned. The first exons (CH1) of γ1 and γ2 are both missing due to gaps. A premature stop codon is marked with a star and a frameshift mutation is marked by shadowing in the CH3 exon of γ3. In each panel, the amino acid residues that are identical to the top sequences are represented by dots. The dashes were used to adjust the alignment. The hinge exons are not included in the figure.
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pone-0016889-g002: Alignment of the amino acid sequences of the nine elephant γ genes.The deduced amino acid sequences of three γ chain-coding exons and two membrane exons of nine elephant γ genes are aligned. The first exons (CH1) of γ1 and γ2 are both missing due to gaps. A premature stop codon is marked with a star and a frameshift mutation is marked by shadowing in the CH3 exon of γ3. In each panel, the amino acid residues that are identical to the top sequences are represented by dots. The dashes were used to adjust the alignment. The hinge exons are not included in the figure.

Mentions: In addition to the eight γ genes (γ1 to γ8) in scaffold 57 (Fig. 1), an additional γ gene (tentatively named as γ9) was identified in scaffold 495 (data not shown), which spans 77 kb. Scaffold 495 is not assembled together with scaffold 57; therefore, γ9 could potentially be either an additional subclass encoding gene or an allelic variant. The identification of multiple IgG subclass-encoding genes is in accordance with a previous report, which indicated that there were at least five subclasses of IgG in African elephant sera [20]. Sequence analysis showed no additional Ig genes in genomic scaffold 495, except for the γ9 gene. The greatest variation among mammalian IgG subclasses is usually concentrated in their hinge regions [52]–[54]. However, no elephant IgG cDNA sequences have been sequenced, it is very difficult to accurately assess the hinge regions of the elephant IgG heavy chains. The hinge region is usually encoded on a separate exon that could not be identified in the elephant due to the low level of conservation and the absence of cDNA sequences. An amino acid alignment of the nine elephant IgG subclasses is presented in Fig. 2. The first exons (CH1) of γ1 and γ2 are both missing because of gaps. The CH3 exon of γ3 is pseudogenized because of a premature stop codon (marked with a star in Fig. 2), and a frame-shift mutation (marked with shadowing in Fig. 2) caused by nucleotide (adenine) insertions at positions 148 and 158, respectively. To clarify the relationship among γ chains from mammalian species, a phylogenetic tree of IgG CH2 and CH3 exons was constructed and is shown in Figure S3. The elephant γ genes form a distinct cluster. This is consistent with previous analysis, which showed that the divergence of IgG subclasses occurred after speciation [52].


A preliminary analysis of the immunoglobulin genes in the African elephant (Loxodonta africana).

Guo Y, Bao Y, Wang H, Hu X, Zhao Z, Li N, Zhao Y - PLoS ONE (2011)

Alignment of the amino acid sequences of the nine elephant γ genes.The deduced amino acid sequences of three γ chain-coding exons and two membrane exons of nine elephant γ genes are aligned. The first exons (CH1) of γ1 and γ2 are both missing due to gaps. A premature stop codon is marked with a star and a frameshift mutation is marked by shadowing in the CH3 exon of γ3. In each panel, the amino acid residues that are identical to the top sequences are represented by dots. The dashes were used to adjust the alignment. The hinge exons are not included in the figure.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3045440&req=5

pone-0016889-g002: Alignment of the amino acid sequences of the nine elephant γ genes.The deduced amino acid sequences of three γ chain-coding exons and two membrane exons of nine elephant γ genes are aligned. The first exons (CH1) of γ1 and γ2 are both missing due to gaps. A premature stop codon is marked with a star and a frameshift mutation is marked by shadowing in the CH3 exon of γ3. In each panel, the amino acid residues that are identical to the top sequences are represented by dots. The dashes were used to adjust the alignment. The hinge exons are not included in the figure.
Mentions: In addition to the eight γ genes (γ1 to γ8) in scaffold 57 (Fig. 1), an additional γ gene (tentatively named as γ9) was identified in scaffold 495 (data not shown), which spans 77 kb. Scaffold 495 is not assembled together with scaffold 57; therefore, γ9 could potentially be either an additional subclass encoding gene or an allelic variant. The identification of multiple IgG subclass-encoding genes is in accordance with a previous report, which indicated that there were at least five subclasses of IgG in African elephant sera [20]. Sequence analysis showed no additional Ig genes in genomic scaffold 495, except for the γ9 gene. The greatest variation among mammalian IgG subclasses is usually concentrated in their hinge regions [52]–[54]. However, no elephant IgG cDNA sequences have been sequenced, it is very difficult to accurately assess the hinge regions of the elephant IgG heavy chains. The hinge region is usually encoded on a separate exon that could not be identified in the elephant due to the low level of conservation and the absence of cDNA sequences. An amino acid alignment of the nine elephant IgG subclasses is presented in Fig. 2. The first exons (CH1) of γ1 and γ2 are both missing because of gaps. The CH3 exon of γ3 is pseudogenized because of a premature stop codon (marked with a star in Fig. 2), and a frame-shift mutation (marked with shadowing in Fig. 2) caused by nucleotide (adenine) insertions at positions 148 and 158, respectively. To clarify the relationship among γ chains from mammalian species, a phylogenetic tree of IgG CH2 and CH3 exons was constructed and is shown in Figure S3. The elephant γ genes form a distinct cluster. This is consistent with previous analysis, which showed that the divergence of IgG subclasses occurred after speciation [52].

Bottom Line: The Igκ locus, found on three scaffolds (202, 50 and 86), contains a total of 153 V(κ) gene segments, three J(κ) segments, and a single C(κ) gene.These data suggest that the elephant immunoglobulin gene repertoire is highly diverse and complex.Our results provide insights into the immunoglobulin genes in a placental mammal that is evolutionarily distant from humans, mice, and domestic animals.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of AgroBiotechnology, College of Biological Sciences, China Agricultural University, Beijing, People's Republic of China.

ABSTRACT
The genomic organization of the IgH (Immunoglobulin heavy chain), Igκ (Immunoglobulin kappa chain), and Igλ (Immunoglobulin lambda chain) loci in the African elephant (Loxodonta africana) was annotated using available genome data. The elephant IgH locus on scaffold 57 spans over 2,974 kb, and consists of at least 112 V(H) gene segments, 87 D(H) gene segments (the largest number in mammals examined so far), six J(H) gene segments, a single μ, a δ remnant, and eight γ genes (α and ε genes are missing, most likely due to sequence gaps). The Igκ locus, found on three scaffolds (202, 50 and 86), contains a total of 153 V(κ) gene segments, three J(κ) segments, and a single C(κ) gene. Two different transcriptional orientations were determined for these V(κ) gene segments. In contrast, the Igλ locus on scaffold 68 includes 15 V(λ) gene segments, all with the same transcriptional polarity as the downstream J(λ)-C(λ) cluster. These data suggest that the elephant immunoglobulin gene repertoire is highly diverse and complex. Our results provide insights into the immunoglobulin genes in a placental mammal that is evolutionarily distant from humans, mice, and domestic animals.

Show MeSH