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Short KIR haplotypes in pygmy chimpanzee (Bonobo) resemble the conserved framework of diverse human KIR haplotypes.

Rajalingam R, Hong M, Adams EJ, Shum BP, Guethlein LA, Parham P - J. Exp. Med. (2001)

Bottom Line: Five of these genes have orthologs in the common chimpanzee, and three of them (KIRCI, KIR2DL4, and KIR2DL5) also have human orthologs.The remaining two genes are KIR3D paralogous to the human and common chimpanzee major histocompatibility complex A- and/or -B-specific KIRs.Simple patterns on Southern blot were due to inheritance of "short" KIR haplotypes containing only three KIR genes, KIRCI, KIR2DL4, and KIR3D, each of which represents one of the three major KIR lineages.

View Article: PubMed Central - PubMed

Affiliation: Department of Structural Biology, Stanford University, Stanford, California 94305, USA.

ABSTRACT
Some pygmy chimpanzees (also called Bonobos) give much simpler patterns of hybridization on Southern blotting with killer cell immunoglobulin-like receptor (KIR) cDNA probes than do either humans or common chimpanzees. Characterization of KIRs from pygmy chimpanzees having simple and complex banding patterns identified nine different KIRs, representing seven genes. Five of these genes have orthologs in the common chimpanzee, and three of them (KIRCI, KIR2DL4, and KIR2DL5) also have human orthologs. The remaining two genes are KIR3D paralogous to the human and common chimpanzee major histocompatibility complex A- and/or -B-specific KIRs. Within a pygmy chimpanzee family, KIR haplotypes were defined. Simple patterns on Southern blot were due to inheritance of "short" KIR haplotypes containing only three KIR genes, KIRCI, KIR2DL4, and KIR3D, each of which represents one of the three major KIR lineages. These three genes in pygmy chimpanzees or their corresponding genes in humans and common chimpanzees form the conserved "framework" common to all KIR haplotypes in these species and upon which haplotypic diversity is built. The fecundity and health of individual pygmy chimpanzees who are homozygotes for short KIR haplotypes attest to the viability of short KIR haplotypes, indicating that they can provide minimal, essential KIRs for the natural killer and T cells of the hominoid immune system.

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Pygmy chimpanzee KIR3D share sequence elements with common chimpanzee and human KIR3D. (A) The scheme in A depicts relationships between the primary structure of KIR3D in the three species. The individual Ig domains (D0, D1, and D2), stem region (S), transmembrane region (T), and cytoplasmic tail (C) are marked. Regions with >96% nucleotide sequence similarity are denoted by common patterns of shading. Relationships in the nucleotide sequences encoding the extracellular domains (panel B) and the transmembrane region plus cytoplasmic domain (panel C) are compared in unrooted phylogenetic trees obtained by maximum parsimony analysis. The names of the pygmy chimpanzee KIRs are boxed. Bootstrap values determined by 1,000 replications are given for pairs of branch points. Trees with similar topology were obtained by the neighbor-joining method and also when constructed from the amino acid sequences (not shown).
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Figure 5: Pygmy chimpanzee KIR3D share sequence elements with common chimpanzee and human KIR3D. (A) The scheme in A depicts relationships between the primary structure of KIR3D in the three species. The individual Ig domains (D0, D1, and D2), stem region (S), transmembrane region (T), and cytoplasmic tail (C) are marked. Regions with >96% nucleotide sequence similarity are denoted by common patterns of shading. Relationships in the nucleotide sequences encoding the extracellular domains (panel B) and the transmembrane region plus cytoplasmic domain (panel C) are compared in unrooted phylogenetic trees obtained by maximum parsimony analysis. The names of the pygmy chimpanzee KIRs are boxed. Bootstrap values determined by 1,000 replications are given for pairs of branch points. Trees with similar topology were obtained by the neighbor-joining method and also when constructed from the amino acid sequences (not shown).

Mentions: To considerable extent the pygmy chimpanzee KIR3D consists of sequence elements present in human and common chimpanzee KIR, but in novel combination (Fig. 5 A). In the region encoding the extracellular part of the molecule (Ig domains and stem), the four Pp-KIR3D form a clade with the common chimpanzee Pt-KIR3DL3 (Fig. 5 B). Comparison of the sequences encoding individual Ig-like domains revealed the D0 domains of Pp-KIR3DLa and Pp-KIR3DSa to be identical and to share sequence segments with both human KIR3DL1 and KIR3DL2. The D0 domains of Pp-KIR3DLb and Pp-KIR3DLc are also identical and have 97.2% sequence similarity with the corresponding domain of human KIR3DL2. In the D1 domain, Pp-KIR3DSa groups with Pp-KIR3DLb and Pp-KIR3DLc, and these closely related sequences have 96% sequence similarity with the D1 domain of KIR3DL2. In the D1 domain, Pp-KIR3DLa diverges from the other Pp-KIR3D but has 98% sequence similarity with the D1 domain of common chimpanzee Pt-KIR3DL3. In the D2 domain, the four Pp-KIR3D are very similar to each other and to Pt-KIR3DL3 (98.5% sequence similarity). Unique to the carboxyl terminal half of the D2 domain of these five KIRs is an insertion of two amino acids followed by a motif of five amino acid substitutions (Fig. 4).


Short KIR haplotypes in pygmy chimpanzee (Bonobo) resemble the conserved framework of diverse human KIR haplotypes.

Rajalingam R, Hong M, Adams EJ, Shum BP, Guethlein LA, Parham P - J. Exp. Med. (2001)

Pygmy chimpanzee KIR3D share sequence elements with common chimpanzee and human KIR3D. (A) The scheme in A depicts relationships between the primary structure of KIR3D in the three species. The individual Ig domains (D0, D1, and D2), stem region (S), transmembrane region (T), and cytoplasmic tail (C) are marked. Regions with >96% nucleotide sequence similarity are denoted by common patterns of shading. Relationships in the nucleotide sequences encoding the extracellular domains (panel B) and the transmembrane region plus cytoplasmic domain (panel C) are compared in unrooted phylogenetic trees obtained by maximum parsimony analysis. The names of the pygmy chimpanzee KIRs are boxed. Bootstrap values determined by 1,000 replications are given for pairs of branch points. Trees with similar topology were obtained by the neighbor-joining method and also when constructed from the amino acid sequences (not shown).
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Related In: Results  -  Collection

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Figure 5: Pygmy chimpanzee KIR3D share sequence elements with common chimpanzee and human KIR3D. (A) The scheme in A depicts relationships between the primary structure of KIR3D in the three species. The individual Ig domains (D0, D1, and D2), stem region (S), transmembrane region (T), and cytoplasmic tail (C) are marked. Regions with >96% nucleotide sequence similarity are denoted by common patterns of shading. Relationships in the nucleotide sequences encoding the extracellular domains (panel B) and the transmembrane region plus cytoplasmic domain (panel C) are compared in unrooted phylogenetic trees obtained by maximum parsimony analysis. The names of the pygmy chimpanzee KIRs are boxed. Bootstrap values determined by 1,000 replications are given for pairs of branch points. Trees with similar topology were obtained by the neighbor-joining method and also when constructed from the amino acid sequences (not shown).
Mentions: To considerable extent the pygmy chimpanzee KIR3D consists of sequence elements present in human and common chimpanzee KIR, but in novel combination (Fig. 5 A). In the region encoding the extracellular part of the molecule (Ig domains and stem), the four Pp-KIR3D form a clade with the common chimpanzee Pt-KIR3DL3 (Fig. 5 B). Comparison of the sequences encoding individual Ig-like domains revealed the D0 domains of Pp-KIR3DLa and Pp-KIR3DSa to be identical and to share sequence segments with both human KIR3DL1 and KIR3DL2. The D0 domains of Pp-KIR3DLb and Pp-KIR3DLc are also identical and have 97.2% sequence similarity with the corresponding domain of human KIR3DL2. In the D1 domain, Pp-KIR3DSa groups with Pp-KIR3DLb and Pp-KIR3DLc, and these closely related sequences have 96% sequence similarity with the D1 domain of KIR3DL2. In the D1 domain, Pp-KIR3DLa diverges from the other Pp-KIR3D but has 98% sequence similarity with the D1 domain of common chimpanzee Pt-KIR3DL3. In the D2 domain, the four Pp-KIR3D are very similar to each other and to Pt-KIR3DL3 (98.5% sequence similarity). Unique to the carboxyl terminal half of the D2 domain of these five KIRs is an insertion of two amino acids followed by a motif of five amino acid substitutions (Fig. 4).

Bottom Line: Five of these genes have orthologs in the common chimpanzee, and three of them (KIRCI, KIR2DL4, and KIR2DL5) also have human orthologs.The remaining two genes are KIR3D paralogous to the human and common chimpanzee major histocompatibility complex A- and/or -B-specific KIRs.Simple patterns on Southern blot were due to inheritance of "short" KIR haplotypes containing only three KIR genes, KIRCI, KIR2DL4, and KIR3D, each of which represents one of the three major KIR lineages.

View Article: PubMed Central - PubMed

Affiliation: Department of Structural Biology, Stanford University, Stanford, California 94305, USA.

ABSTRACT
Some pygmy chimpanzees (also called Bonobos) give much simpler patterns of hybridization on Southern blotting with killer cell immunoglobulin-like receptor (KIR) cDNA probes than do either humans or common chimpanzees. Characterization of KIRs from pygmy chimpanzees having simple and complex banding patterns identified nine different KIRs, representing seven genes. Five of these genes have orthologs in the common chimpanzee, and three of them (KIRCI, KIR2DL4, and KIR2DL5) also have human orthologs. The remaining two genes are KIR3D paralogous to the human and common chimpanzee major histocompatibility complex A- and/or -B-specific KIRs. Within a pygmy chimpanzee family, KIR haplotypes were defined. Simple patterns on Southern blot were due to inheritance of "short" KIR haplotypes containing only three KIR genes, KIRCI, KIR2DL4, and KIR3D, each of which represents one of the three major KIR lineages. These three genes in pygmy chimpanzees or their corresponding genes in humans and common chimpanzees form the conserved "framework" common to all KIR haplotypes in these species and upon which haplotypic diversity is built. The fecundity and health of individual pygmy chimpanzees who are homozygotes for short KIR haplotypes attest to the viability of short KIR haplotypes, indicating that they can provide minimal, essential KIRs for the natural killer and T cells of the hominoid immune system.

Show MeSH
Related in: MedlinePlus