Complete nucleotide sequence of an immunoglobulin VH gene homologue from Caiman, a phylogenetically ancient reptile

Litman, G. W.; Berger, Leszek; Murphy, Kevin; Litman, Ronda T.; Hinds, K.; Jahn, Carolyn L.; Erickson, Bruce W.

doi:10.1038/303349a0

Cited by 46 publications

(16 citation statements)

References 25 publications

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“…Doubleheaded arrows correspond to (same direction) extension of a given sequence (typically achieved by alternative cloning strategy) overlapping the primary sequence by at least 50 bp or (opposite direction) a single clone sequenced in both directions. Dideoxynucleotide sequencing confirmed the restriction map as well as the sequence reported earlier for C3 (24) and identified several additional HinfI and Dde sites located within 25 bp (below the detection limits) of the map positions previously assigned for these enzymes.…”

supporting

confidence: 52%

“…The construction, amplification, and screening of a caiman-X47.1 library with S107V, a murine VH probe (3), have been described (24). Standard phage purification and subcloning approaches were used.…”

Section: Materials and Met1iodsmentioning

confidence: 99%

“…In earlier reports, we described crosshybridization between restriction enzyme-digested caiman genomic DNA and murine VH probes (23) and demonstrated sequence similarities between caiman and prototypic mammalian VH genes (24). In this report, we compare the coding as well as the 5' and 3' flanking segments of three different caiman (Caiman crocodylus crocodylus) VH genes and identify unique recombination signal sequences associated with one of these genes.…”

mentioning

confidence: 99%

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Complete nucleotide sequences of three VH genes in Caiman, a phylogenetically ancient reptile: evolutionary diversification in coding segments and variation in the structure and organization of recombination elements.

Litman¹,

Murphy²,

Berger³

et al. 1985

Proc. Natl. Acad. Sci. U.S.A.

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Complete nucleotide sequences are described for three caiman (Caiman crocodylus crocodylus) immunoglobulin VH genes (C3, El, and G4) that hybridize with a murine VH probe. The El and G4 genes are physically linked (intergenic distance, --6.5 kilobases) in the same transcriptional orientation but are not directly contiguous with the C3 gene. When the coding segments, including both framework and complementarity-determining regions, of these genes and the murine probe sequences are compared by metric analysis, it is apparent that the caiman genes are only slightly more related to each other than to the mammalian sequence, consistent with significant preservation of nucleotide sequence over an extended period of phylogenetic time. Based on the presence of transcriptionally critical 5' sequences and the absence of terminator codons, frameshift mutations, or other recognizable alterations, the genes do not appear to be pseudogenes. The El gene, however, is distinguished from other VH genes because (i) the spacer region within the 3' recombination signal sequence is 12 base pairs, typical of V,. genes but not of VH genes, which possess 22-to 23-base-pair spacers and (H) a near-perfect VH recombination signal sequence is present within the intervening sequence that splits the segment encoding the leader. These studies establish VH gene multiplicity in a species that arose prior to mammalian radiation and provide a description of differences in the configuration and location of recombination elements associated with an otherwise potentially functional gene.Based on studies in mammals, it is apparent that multiple germ line VH genes contribute to the overall diversity of the humoral immune response that is amplified further by somatic events such as mutation and segmental joining (1-10). This latter process is mediated by relatively short DNA segments located 3' to the coding segments of immunglobulin VH (2, 3, 6, 7, 9) and VL genes (9,11,12) and by complementary segments flanking the D, JH, and JL segments (2, 3, 9-12) located 5' of the constant region genes. Understanding the evolution of the V-region gene families and their associated recombination mechanisms is essential for understanding the developmental control of antibody expression and other genetic processes involving somatic changes in DNA.Since it is likely that significant numbers of V-region genes are not subject to direct selection during the lifetime of an individual, the processes that govern the phylogenetic development, diversification, and stabilization of this multigenic family are important and may be unique.To date, evolutionary studies of VH genes largely have been restricted to comparisons between the members of structurally related families, identified in inbred mouse strains (6,7,(13)(14)(15)(16)(17)(18), as well as between murille and human sequences (19)(20)(21)(22). In earlier reports, we described crosshybridization between restriction enzyme-digested caiman genomic DNA and murine VH probes (23) and demonstrated sequence similariti...

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supporting

confidence: 52%

Section: Materials and Met1iodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Complete nucleotide sequences of three VH genes in Caiman, a phylogenetically ancient reptile: evolutionary diversification in coding segments and variation in the structure and organization of recombination elements.

Litman¹,

Murphy²,

Berger³

et al. 1985

Proc. Natl. Acad. Sci. U.S.A.

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“…For comparison we include sequences of two rabbit C regions (14,15), one rabbit V segment (16), two rat C regions (17,18), one rat V segment (17), one caiman V segment (19) and one chicken C region (20). The number of sequences is distributed as follows:…”

Section: The Samplementioning

confidence: 99%

Coding strategy differences between constant and variable segments of immunoglobulin genes

Perrin¹

1984

Nucl Acids Res

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Vertebrate immunoglobulin (Ig) mRNAs reveal intraspecies variation in codon usage distinct from that seen with yeast or bacterial genes.Comparison of all available Ig gene sequences shows that %(G+C) in codon position III is consistently lower in variable (V) segments than in constant (C) segments. I find an even lower %(G+C) in the hypervariable domains of V segments. This analysis suggests that base substitution in Ig genes correlates positively with local A+T content.

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“…However, when cloned mouse VH genes were used as probes to isolate their human counterparts, mouse group III VH genes identified their human homologues more easily than did mouse group I and II VH genes (4,5). Mouse group III probes could also identify VH genes in several other mammalian species (9,10), the reptile Caiman (9,11), the amphibian Xenopus (7), and the elasmobranch Heterodontus (12). Moreover, VH genes in the rabbit and chicken, which may have only one VH gene family, belong to group III (13,14).…”

mentioning

confidence: 99%

Conservation of an immunoglobulin variable-region gene family indicates a specific, noncoding function.

Tutter¹,

Riblet²

1989

Proc. Natl. Acad. Sci. U.S.A.

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Blot-hybridization and DNA sequence analyses reveal the particular evolutionary conservation of a group of immunoglobulin heavy-chain variable-region (VH) genes in all mammalian species examined. These particular genes are group m genes-the VH7183 family in the mouse and the homologous VH HI family in human. This conservation is localized to sequences encoding framework regions 1 and 3 of the antibody variable region and is exerted at the nucleotide level. Because selection acting at the amino acid level alone cannot explain the conservation of these sequences, these sequences must have a noncoding function. The preferential rearrangement of VH7183 and VH HI genes, together with the similarity of the conserved sequences to elements implicated in recombination in other systems, suggest that these sequences function to target the series of rearrangements that assemble complete immunoglobulin genes.There are three major groups ofimmunoglobulin heavy-chain variable-region (VH) genes (I, II, and III) in both mouse and human (1). In both species, these groups have been further divided into families on the basis of cross-hybridization and sequence similarity (2)(3)(4)(5)(6). Homology between several human and mouse VH families in each group has been inferred from sequence similarity (Table 1). Thus, the divergence of the three major groups of VH families (and certain VH families therein) preceded the mammalian radiation 60-80 million years (Myr) ago, when contemporary orders of placental mammals last shared a common ancestor. The recent isolation of VH genes homologous to groups I and III from Xenopus (7,8) indicates that the divergence of the three major groups is considerably more ancient, over 300 Myr ago.If the three groups of VH genes were subjected to similar evolutionary pressures, then they would be expected to be similarly conserved. However, when cloned mouse VH genes were used as probes to isolate their human counterparts, mouse group III VH genes identified their human homologues more easily than did mouse group I and II VH genes (4, 5). Mouse group III probes could also identify VH genes in several other mammalian species (9, 10), the reptile Caiman (9, 11), the amphibian Xenopus (7), and the elasmobranch Heterodontus (12). Moreover, VH genes in the rabbit and chicken, which may have only one VH gene family, belong to group III (13,14). Collectively, these observations suggest that while other VH groups may evolve more freely (and in some cases even be lost), group III VH genes, in particular, are a conserved and obligatory component of heavy-chain loci in widely divergent mammalian and nonmammalian lineages.Here, we use Southern blot hybridization to show that discrete segments ofgroup III VH genes have been conserved throughout mammalian evolution. Examination of published sequences identifies specific candidate sequences in mouse VH7183 and human VH III gene families; these sequences have been conserved at the level of nucleotide sequence rather than coded protein sequence. Our results indicate ...

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Complete nucleotide sequence of an immunoglobulin VH gene homologue from Caiman, a phylogenetically ancient reptile

Cited by 46 publications

References 25 publications

Complete nucleotide sequences of three VH genes in Caiman, a phylogenetically ancient reptile: evolutionary diversification in coding segments and variation in the structure and organization of recombination elements.

Complete nucleotide sequences of three VH genes in Caiman, a phylogenetically ancient reptile: evolutionary diversification in coding segments and variation in the structure and organization of recombination elements.

Coding strategy differences between constant and variable segments of immunoglobulin genes

Conservation of an immunoglobulin variable-region gene family indicates a specific, noncoding function.

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