Abstract
An RNA polymerase chain reaction strategy was used to amplify and clone a cDNA segment encoding for the complete constant part of the axolotl IgY heavy (Cυ) chain. Cυ is 433 amino acids long and organized into four domains (Cυ1–Cυ4); each has the typical internal disulfide bond and invariant tryptophane residues. Axolotl Cυ is most closely related to Xenopus Cυ (40% identical amino acid residues) and Cυ1 shares 46.4% amino acid residues among these species. The presence of additional cysteines in Cυ1 and Cυ2 domains is consistent with an additional intra-domain S-S bond similar to that suggested for Xenopus Cυ and Cχ, and for the avian Cυ and the human Cε. Cυ4 ends with the Gly-Lys dipeptide characteristic of secreted mammalian Cγ3, human Cε4, and avian and anuran Cυ4, and contains the consensus [G/GT(AA)] nucleotide splice signal sequence for joining Cυ4 to the transmembrane region. These results are consistent with the hypothesis of an ancestral structural relationship between amphibian, avian υ chains, and mammalian ε chains. However, these molecules have different biological properties: axolotl IgY is secretory Ig, anuran and avian IgY behave like mammalian IgG, and mammalian IgE is implicated in anaphylactic reactions.
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Amemiya, C. T., Haire, R. N., and Litman, G. W. Nucleotide sequence of a cDNA encoding a third distinct Xenopus immunoglobulin heavy chain isotype. Nucleic Acids Res 17: 5388, 1989
Bernstein, K. E., Alexander, C. B., Reddy, E. P., and Mage, R. G. Complete sequence of a cloned cDNA encoding rabbit secreted μ-chain of VHa2 allotype: comparison with VHa1 and membrane μ sequences. J Immunol 132: 490–495, 1984
Dahan, A., Reynaud, C.-A., and Weill, J.-C. Nucleotide sequence of the constant region of a chicken μ heavy chain immunoglobulin mRNA. Nucleic Acids Res 11: 5381–5389, 1983
Fellah, J. S. and Charlemagne, J. Characterization of an IgY-like low molecular weight immunoglobulin class in the Mexican axolotl. Molec Immunol 25: 1377–1386, 1988
Fellah, J. S., Iscaki, S., Vaerman, P., and Charlemagne, J. Transient developmental expression of IgY and secretory component-like protein in the gut of the axolotl (Ambystoma mexicanum). Dev Immunol 2: 181–190, 1992a
Fellah, J. S., Vaulot, D., Tournefier, A., and Charlemagne, J. Ontogeny of immunoglobulin expression in the Mexican axolotl. Development 107: 253–263, 1989
Fellah, J. S., Wiles, M. V., Charlemagne, J., and Schwager, J. Evolution of vertebrate IgM: complete amino acid sequence of the constant region of Ambystoma mexicanum μ chain deduced from cDNA sequence. Eur J Immunol 22: 2592–2601, 1992b
Feng, D.-F. and Doolittle, R. F. Progressive sequence alignment as a prerequisite to correct phylogenic trees. J Mol Evol 25: 351–360, 1987
Flanagan, J. G. and Rabbits, T. H. The sequence of a human immunoglobulin epsilon heavy chain constant region gene, and evidence for three non-allelic genes. EMBO J 1: 655–661, 1982
Flanagan, J. G., Lefranc, M. P., and Rabbits, T. H. Mechanisms of divergence and convergence of the human immunoglobulin α-1 and α-2 constant region gene sequences. Cell 36: 681–688, 1984
Frohman, M. A., Dush, M. K., and Martin, G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85: 8998–9002, 1988
Gauthier, J. A., Kluge, A. G., and Rowe, T. The early evolution of the Amniota. In: M. J. Benton (ed): The Phylogeny and Classification of the Tetrapods, vol. 1., Amphibia, Reptiles, Birds, pp. 103–155, Clarendon Press, Oxford, 1988
Grey, H. M. Duck immunoglobulins II. Biological and immunochemical structure. J Immunol 98: 820–827, 1967
Hadji-Azimi, I. Anuran immunoglobulins. A review. Dev Comp Immunol 3: 223–243, 1979
Haire, R. N., Shamblott, M. J., Amemiya, C. T., and Litman, G. W. A second Xenopus immunoglobulin heavy constant region isotype gene. Nucleic Acids Res 17: 117, 1989
Harding, F. A., Amemiya, C. T., Litman, R. T., Cohen, N., and Litman, G. W. Two distinct immunoglobulin heavy chain isotypes in a primitive, cartilagineous fish, Raja erinacea. Nucleic Acids Res 18: 6369–6376, 1990
Hayzer, D. J., Duvoisin, R. M., and Jaton, J.-C. cDNA clones encoding rabbit immunoglobulin λ chains. Evidence for length variation of the third hypervariable region and for a novel constant region. Biochem J 245: 691–697, 1987
Hellman, L., Peterson, U., and Bennich, H. Characterization and molecular cloning of the mRNA for the heavy (ε) chain of rat immunoglobulin E. Proc Natl Acad Sci USA 79: 1264–1266, 1982
Hsu, E., Flajnik, M. F., and du Pasquier, L. A third immunoglobulin class in amphibians. J Immunol 135: 1998–2004, 1985
Kabat, E. A., Wu, T. T., Reid-Miller, M., Perry, H. M., and Gottesman, K. S. Sequences of Proteins of Immunological Interest, 4th edn., HHS National Institute of Health, Bethesda, 1987
Kobayashi, K., Tomogana, S., and Tanaka, S. Identification of a second immunoglobulin in the most primitive shark, the trill shark, Chlamydoselachus anguineus. Dev Comp Immunol 16: 295–299, 1992
Kokubu, F., Hinds, K., Litman, R., Shamblott, M. J., and Litman, G. W. Complete structure and organization of immunoglobulin heavy chain constant region genes in a phylogenetically primitive vertebrate. EMBO J 7: 1979–1988, 1988
Leslie, G. A. and Clem, L. W. Phylogeny of immunoglobulin structure and function. II. 17S, 7.5S and 5.7S anti-DNP of the turtle, Pseudamys scripta. J Immunol 108: 1656–1664, 1972
Litman, G. W., Wang, A. C., Funderberg, H. H., and Good, R. A. N-terminal amino-acid sequence of African lungfish immunoglobulin light chains. Proc Natl Acad Sci USA 68: 2321–2324, 1971
Liu, F.-T., Albrandt, K., Sutcliffe, J. G., and Katz, D. H. Cloning and nucleotide sequence of mouse immunoglobulin ε chain cDNA. Proc Natl Acad Sci USA 79: 7852–7856, 1982
Lobb, C. J. and Clem, W. Phylogeny of immunoglobulin structure and function-X. Humoral immunoglobulins of the sheep-head, Archosargus probatocephalus. Dev Comp Immunol 5: 271–282, 1981
Magor, K. E., Warr, G. W., Middleton, D., Wilson, M. R., and Higgins, D. A. Structural relationships between the two IgY of the duck, Anas platyrhynchus: molecular genetic evidence. J Immunol 149: 2627–2633, 1992
Mansikka, A. Chicken IgA H chains. Implication concerning the evolution of H chain genes. J Immunol 149: 855–861, 1992
Marchalonis, J. J. Isolation and characterization of immunoglobulin-like proteins of Australian lungfish (Neoceratodus fosteri). Aust J Exp Biol Med Sci 47: 405–419, 1969
Martens, C. L., Currier, S. J., and Knight, K. L. Molecular genetic analysis of genes encoding the heavy chains of rabbit IgG. J Immunol 133: 1022–1027, 1984
Meyer, A. and Wilson, A. C. Origin of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 31: 359–364, 1990
Milner, A. R. The relationships and origin of living amphibians. In M. J. Benton (ed.): The Phylogeny and Classification of Tetrapods, vol, 1., Amphibians, Reptiles, Birds, pp. 59–102, Clarendon Press, Oxford, 1988
Parvari, R., Avivi, A., Lentner, F., Ziv, E., Tel-Oz, S., Burnstein, Y., and Schechter, I. Chicken immunoglobulin γ-heavy chains: limited VH gene repertoire, combinatorial diversification by D gene segments and evolution of the heavy chain locus. EMBO J 7: 739–744, 1988
Pearson, W. R. and Lipman, D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444–2448, 1988
Reynaud, C.-A., Dahan, A., and Weill, J.-C. Complete sequence of a chicken λ chain immunoglobulin derived from the nucleotide sequence of its mRNA. Proc Natl Acad Sci USA 80: 4099–4103, 1983
Saitou, N. and Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425, 1987
Sanger, F., Nicklen, S., and Coulson, A. R. DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467, 1977
Schluter, S. F., Hohman, V. S., Edmundson, A. B., and Marchalonis, J. Evolution of immunoglobulin light chains: cDNA clones specifying Sandbar shark constant regions. Proc Natl Acad Sci USA 86: 9961–9965, 1989
Schwager, J., Bürckert, N., Courtet, M., and du Pasquier, L. The ontogeny of diversification at the immunoglobulin heavy chain locus in Xenopus. EMBO J 10: 2461–2470, 1991
Schwager, J., Mikoryak, C. A., and Steiner, L. Amino acid sequence of heavy chain from Xenopus laevis IgM deduced from cDNA sequence: implications for evolution of immunoglobulin domains. Proc Natl Acad Sci USA 85: 2245–2249, 1988
Seno, M., Kurokawa, T., Ono, Y., Onda, H., Sasada, R., Igarashi, K., Kikuchi, M., Sugeno, Y., Nishida, Y., and Honjo, T. Molecular cloning and nucleotide sequencing of human immunoglobulin ε chain cDNA. Nucleic Acids Res 11: 719–723, 1983
Shamblott, M. J. and Litman, G. W. Complete nucleotide sequence of primitive vertebrate immunoglobulin light chain genes. Proc Natl Acad Sci USA 86: 4684–4688, 1989
Symons, D. B. A., Clarkson, C. A., and Baele, D. Structure of bovine immunoglobulin constant region heavy chain gamma 1 and gamma 2 genes. Mol Immunol 26: 841–850, 1989
Word, C. J., White, M. B., Kuziel, w. A., Shen, A. L., Blattner, F. R., and Tucker, P. W. The human immunoglobulin Cμ-C locus. Complete nucleotide sequence and structural analysis. Int Immunol 1: 296–309
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The nucleotide sequence data reported in this paper have been submitted to the EMBL/GenBank nucleotide sequence database and have been assigned the accession number X69492.
Correspondence to: J. S. Fellah.
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Fellah, J.S., Kerfourn, F., Wiles, M.V. et al. Phylogeny of immunoglobulin heavy chain isotypes: structure of the constant region of Ambystoma mexicanum υ chain deduced from cDNA sequence. Immunogenetics 38, 311–317 (1993). https://doi.org/10.1007/BF00210471
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DOI: https://doi.org/10.1007/BF00210471