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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Jul 15;90(14):6811–6814. doi: 10.1073/pnas.90.14.6811

Conserved structure of amphibian T-cell antigen receptor beta chain.

J S Fellah 1, F Kerfourn 1, F Guillet 1, J Charlemagne 1
PMCID: PMC47022  PMID: 8341702

Abstract

All jawed vertebrates possess well-differentiated thymuses and elicit T-cell-like cell-mediated responses; however, no surface T-cell receptor (TCR) molecules or TCR genes have been identified in ectothermic vertebrate species. Here we describe cDNA clones from an amphibian species, Ambystoma mexicanum (the Mexican axolotl), that have sequences highly homologous to the avian and mammalian TCR beta chains. The cloned amphibian beta chain variable region (V beta) shares most of the structural characteristics with the more evolved vertebrate V beta and presents approximately 56% amino acid identities with the murine V beta 14 and human V beta 18 families. The two different cloned axolotl beta chain joining regions (J beta) were found to have conserved all the invariant mammalian J beta residues, and in addition, the presence of a conserved glycine at the V beta-J beta junction suggests the existence of diversity elements. The extracellular domains of the two axolotl beta chain constant region isotypes C beta 1 and C beta 2 show an impressively high degree of identity, thus suggesting that a very efficient mechanism of gene correction has been in operation to preserve this structure at least from the early tetrapod evolution. The transmembrane axolotl C beta domains have been less well conserved when compared to the mammalian C beta but they do maintain the lysine residue that is thought to be involved in the charged interaction between the TCR alpha beta heterodimer and the CD3 complex.

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Selected References

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  1. Alcover A., Mariuzza R. A., Ermonval M., Acuto O. Lysine 271 in the transmembrane domain of the T-cell antigen receptor beta chain is necessary for its assembly with the CD3 complex but not for alpha/beta dimerization. J Biol Chem. 1990 Mar 5;265(7):4131–4135. [PubMed] [Google Scholar]
  2. Allison J. P., Lanier L. L. Structure, function, and serology of the T-cell antigen receptor complex. Annu Rev Immunol. 1987;5:503–540. doi: 10.1146/annurev.iy.05.040187.002443. [DOI] [PubMed] [Google Scholar]
  3. Brenner M. B., Strominger J. L., Krangel M. S. The gamma delta T cell receptor. Adv Immunol. 1988;43:133–192. [PubMed] [Google Scholar]
  4. Britten R. J., Davidson E. H. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol. 1971 Jun;46(2):111–138. doi: 10.1086/406830. [DOI] [PubMed] [Google Scholar]
  5. Davis M. M. T cell receptor gene diversity and selection. Annu Rev Biochem. 1990;59:475–496. doi: 10.1146/annurev.bi.59.070190.002355. [DOI] [PubMed] [Google Scholar]
  6. Fellah J. S., Wiles M. V., Charlemagne J., Schwager J. Evolution of vertebrate IgM: complete amino acid sequence of the constant region of Ambystoma mexicanum mu chain deduced from cDNA sequence. Eur J Immunol. 1992 Oct;22(10):2595–2601. doi: 10.1002/eji.1830221019. [DOI] [PubMed] [Google Scholar]
  7. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gascoigne N. R., Chien Y., Becker D. M., Kavaler J., Davis M. M. Genomic organization and sequence of T-cell receptor beta-chain constant- and joining-region genes. Nature. 1984 Aug 2;310(5976):387–391. doi: 10.1038/310387a0. [DOI] [PubMed] [Google Scholar]
  9. Johnson N. A., Carland F., Allen P. M., Glimcher L. H. T cell receptor gene segment usage in a panel of hen-egg white lysozyme specific, I-Ak-restricted T helper hybridomas. J Immunol. 1989 May 1;142(9):3298–3304. [PubMed] [Google Scholar]
  10. Jouvin-Marche E., Heller M., Rudikoff S. Gene correction in the evolution of the T cell receptor beta chain. J Exp Med. 1986 Dec 1;164(6):2083–2088. doi: 10.1084/jem.164.6.2083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Novotný J., Tonegawa S., Saito H., Kranz D. M., Eisen H. N. Secondary, tertiary, and quaternary structure of T-cell-specific immunoglobulin-like polypeptide chains. Proc Natl Acad Sci U S A. 1986 Feb;83(3):742–746. doi: 10.1073/pnas.83.3.742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Rudikoff S., Fitch W. M., Heller M. Exon-specific gene correction (conversion) during short evolutionary periods: homogenization in a two-gene family encoding the beta-chain constant region of the T-lymphocyte antigen receptor. Mol Biol Evol. 1992 Jan;9(1):14–26. doi: 10.1093/oxfordjournals.molbev.a040701. [DOI] [PubMed] [Google Scholar]
  14. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Schiffer M., Wu T. T., Kabat E. A. Subgroups of variable region genes of beta chains of T-cell receptors for antigen. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4461–4463. doi: 10.1073/pnas.83.12.4461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Shamblott M. J., Litman G. W. Complete nucleotide sequence of primitive vertebrate immunoglobulin light chain genes. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4684–4688. doi: 10.1073/pnas.86.12.4684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Tanaka A., Ishiguro N., Shinagawa M. Sequence and diversity of bovine T-cell receptor beta-chain genes. Immunogenetics. 1990;32(4):263–271. doi: 10.1007/BF00187097. [DOI] [PubMed] [Google Scholar]
  18. Tjoelker L. W., Carlson L. M., Lee K., Lahti J., McCormack W. T., Leiden J. M., Chen C. L., Cooper M. D., Thompson C. B. Evolutionary conservation of antigen recognition: the chicken T-cell receptor beta chain. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7856–7860. doi: 10.1073/pnas.87.20.7856. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Tunnacliffe A., Kefford R., Milstein C., Forster A., Rabbitts T. H. Sequence and evolution of the human T-cell antigen receptor beta-chain genes. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5068–5072. doi: 10.1073/pnas.82.15.5068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Williams A. F., Barclay A. N. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. doi: 10.1146/annurev.iy.06.040188.002121. [DOI] [PubMed] [Google Scholar]
  21. Williams C. B., Gutman G. A. T cell receptor beta-chain genes in the rat. Availability and pattern of utilization of V gene segments differs from that in the mouse. J Immunol. 1989 Feb 1;142(3):1027–1035. [PubMed] [Google Scholar]
  22. Wilson R. K., Lai E., Concannon P., Barth R. K., Hood L. E. Structure, organization and polymorphism of murine and human T-cell receptor alpha and beta chain gene families. Immunol Rev. 1988 Jan;101:149–172. doi: 10.1111/j.1600-065x.1988.tb00736.x. [DOI] [PubMed] [Google Scholar]

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