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Divergent T-cell receptor delta chains from marsupials

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Abstract

Complementary DNAs (cDNAs) encoding T-cell receptor delta (TRD) chains from the northern brown bandicoot, Isoodon macrourus, were identified while sequencing expressed sequence tags (ESTs) from a thymus cDNA library. Surprisingly, the I. macrourus TRD sequences were not orthologous to previously published TRD sequences from another Australian marsupial, the tammar wallaby, Macropus eugenii. Identification of TRD genes in the recently completed whole genome sequence of the South American opossum, Monodelphis domestica, revealed the presence of two highly divergent TRD loci. To determine whether the presence of multiple TRD loci accounts for the lack of orthology between the I. macrourus and M. eugenii cDNAs, additional TRD sequences were obtained from both species of marsupials. The results of this analysis revealed that, unlike eutherian mammals, all three species of marsupials have multiple, highly divergent TRD loci. One group of marsupial TRD sequences was closely related to TR sequences from eutherian mammals. A second group of TRD sequences formed a unique marsupial-specific clade, separate from TR sequences from eutherians. An interesting expression pattern of TRD variable (TRDV) and constant (TRDC) segments was evident in cDNAs from I. macrourus and M. eugenii. TRDV and TRDC sequences that were closely related to TRD genes from eutherian mammals were only found in association with each other in cDNAs from both marsupial species. A similar pattern was seen between TRDV and TRDC sequences that were most closely related to other marsupial TRD genes.

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References

  • Altschul SF, Gish W, Miller W, Myers EM, Lipman DJ (1990) Basic local alignment search tool. J Mol Evol 215:403–410

    CAS  Google Scholar 

  • Baker ML, Rosenberg GH, Zuccolotto P, Harrison GA, Deane EM, Miller RD (2001) Further characterization of T cell receptor chains of marsupials. Dev Comp Immunol 25:F495–F507

    Article  Google Scholar 

  • Baker ML, Wares JP, Harrison GA, Miller RD (2004) The relationship of the marsupial families and the mammalian subclasses based on recombination activating gene-1. J Mamm Evol 11:1–16

    Article  Google Scholar 

  • Belov K, Harrison GA, Miller RD, Cooper DW (2002) Molecular cloning of four lambda light chain cDNAs from the Australian brushtail possum (Trichosurus vulpecula). Eur J Immunogenet 29:95–99

    Article  PubMed  CAS  Google Scholar 

  • Belov K, Miller RD, Ilijeski A, Hellman L, Harrison GA (2004) Isolation of monotreme T cell receptor α and β chains. Immunogenetics 56:164–169

    Article  PubMed  CAS  Google Scholar 

  • Campbell KS, Backstrom BT, Tiefenthaler G, Palmer E (1994) CART: a conserved antigen receptor transmembrane motif. Semin Immunol 6:393–410

    Article  PubMed  CAS  Google Scholar 

  • Carding SR, Egan PJ (2002) γδ T cells: functional plasticity and heterogeneity. Nat Rev Immunol 2:336–345

    Article  PubMed  CAS  Google Scholar 

  • Chien Y, Jores R, Crowley MP (1996) Recognition by γ/δ T cells. Annu Rev Immunol 14:511–532

    Article  PubMed  CAS  Google Scholar 

  • Flajnik MF (1998) Churchill and the immune system of ectothermic vertebrates. Immunol Rev 166:5–14

    Article  PubMed  CAS  Google Scholar 

  • Fox DH, Rowlands DT, Wilson DM (1976) Proliferative reactivity of opossum peripheral blood leukocytes to allogeneic cells, mitogens and specific antigens. Transplantation 21:164–168

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harrison GA, Taylor CL, Miller RD, Deane EM (2003) Primary structure and variation of the T cell receptor δ-chain from a marsupial, Macropus eugenii. Immunol Lett 88:117–125

    Article  PubMed  CAS  Google Scholar 

  • Hayday AC (2000) γδ T cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18:975–1026

    Article  PubMed  CAS  Google Scholar 

  • Hein WR (1994) Structural and functional evolution of the extracellular regions of T cell receptors. Semin Immunol 6:361–372

    Article  PubMed  CAS  Google Scholar 

  • Infante AJ, Samples NK, Croix DA, Redding TS, Vandeberg JL, Stone WH (1991) Cellular immune response of a marsupial, Monodelphis domestica. Dev Comp Immunol 15:189–199

    Article  PubMed  CAS  Google Scholar 

  • Janke A, Xu X, Arnason U (1997) The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata Marsupialia, and Eutheria. Proc Natl Acad Sci U S A 94:1276

    Article  PubMed  CAS  Google Scholar 

  • Kirsch JAW, Lapointe F, Springer MS (1997) DNA-hybridisation studies of marsupials and their implications for metatherian classification. Aust J Zoology 45:211–280

    Article  CAS  Google Scholar 

  • Kubota T, Wang J, Gobel TWF, Hockett RD, Cooper MD, Chen CH (1999) Characterization of an avian (Gallus gallus domessticus) TR αδ gene locus. J Immunol 163:3858–3866

    PubMed  CAS  Google Scholar 

  • Livak F, Schatz DG (1998) Alternative splicing of rearranged T cell receptor δ sequences to the constant region of the α locus. Proc Natl Acad Sci U S A 95:5694–5699

    Article  PubMed  CAS  Google Scholar 

  • Marchalonis JJ, Schluter SF (1990) Origins of immunoglobulins and immune recognition molecules. Bioscience 40:758–768

    Article  Google Scholar 

  • Marchalonis JJ, Schluter SF, Edmundson AB (1997) The T cell receptor as immunoglobulin: paradigm regained. Proc Soc Exp Biol Med 216:303–318

    PubMed  CAS  Google Scholar 

  • Nam BH, Hirono I, Aoki T (2003) The four TR genes of teleost fish: the cDNA and genomic DNA analysis of Japanese flounder (Paralichthys olivaceus) TR α-, β-, and δ-chains. J Immunol 170:3081–3090

    PubMed  CAS  Google Scholar 

  • Partula S, de Guerra A, Fellah JS, Charlemagne J (1995) Structure and diversity of the T cell receptor β chain in a teleost fish. J Immunol 155:699–706

    PubMed  CAS  Google Scholar 

  • Rast JP, Litman GW (1994) T cell receptor gene homologues are present in the most primitive jawed vertebrates. Proc Natl Acad Sci U S A 91:9248–9252

    Article  PubMed  CAS  Google Scholar 

  • Rast JP, Anderson MK, Strong SJ, Luer C, Litman RT, Litman GW (1997) α, β, γ, and δ T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity 6:1–11

    Article  PubMed  CAS  Google Scholar 

  • Richards MH, Nelson JL (2000) The evolution of vertebrate antigen receptors: a phylogenetic approach. Mol Biol Evol 17:146–155

    PubMed  CAS  Google Scholar 

  • Rowlands DT, Blakslee DT, Angala E (1974) Acquired immunity in opossum (Didelphis virginiana). J Immunol 112:2148–2153

    PubMed  CAS  Google Scholar 

  • Saito H, Kranz DM, Takagaki Y, Hayday AC, Eisen HN, Tonegawa S (1984) Complete primary structure of a heterodimic T cell receptor deduced from cDNA sequences. Nature 309:757–762

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1997) The neighbor joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406

    Google Scholar 

  • Sottini A, Imberti L, Fiordalisi G, Primi D (1991) Use of variable human Vδ genes to create functional T cell receptor α chain transcripts. Eur J Immunol 21:2455–2459

    Article  PubMed  CAS  Google Scholar 

  • Stone WH, Bruun DA, Scott Manis G, Holste SB, Hoffman ES, Spong KD, Walunas TL (1996) The immunobiology of the marsupial, Monodelphis domestica. In: modulators of immune responses: an evolutionary trail, SOS Publications, pp 149–165

  • Stone WH, Manis GH, Hoffman ES, Saphire DG, Hubbard GB, VandeBerg JL (1997) Fate of allogeneic skin transplantations in a marsupial (Monodelphis domestica) Lab Anim Sci 47:283–287

    PubMed  CAS  Google Scholar 

  • Stone WH, Bruun DA, Foster EB, Manis GS, Hoffman ES, Saphire DG, VandeBerg JL, Infante AJ (1998) Absence of a significant mixed lymphocyte reaction in a marsupial (Monodelphis domestica). Lab Anim Sci 48:184–189

    PubMed  CAS  Google Scholar 

  • Strominger JL (1989) Developmental biology of T cell receptors. Science 244:943–950

    Article  PubMed  CAS  Google Scholar 

  • Su C, Jakobsen I, Gu X, Nei M (1999) Diversity and evolution of T cell receptor variable region genes in mammals and birds. Immunogenetics 50:301–308

    Article  PubMed  CAS  Google Scholar 

  • Swofford D (1998) Phylogenetic analysis using parsimony and other methods (PAUP*4.0b4a), Sinauer Associates

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of the progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4676–4680

    Article  Google Scholar 

  • Tjoelker LW, Carlson LM, Lee K, Lahti J, McCormack WT, Chen CH, Cooper MD, Thompson CB (1990) Evolutionary conservation of antigen recognition: the chicken T cell receptor β chain. Proc Natl Acad Sci U S A 87:7856–7860

    Article  PubMed  CAS  Google Scholar 

  • Watson D, Ando T, Knight JF (2000) Sequence and diversity of the rat delta T cell receptor. Immunogenetics 51:714–722

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson R, Kotlarski I, Barton M, Phillips P (1992) Isolation of koala lymphoid cells and their in vitro responses to mitogens. Vet Immunol Immunopathol 31:21–33

    Article  PubMed  CAS  Google Scholar 

  • Zuccolotto PD, Harrison GA, Deane EM (2000) Cloning of marsupial T cell receptor α and β constant region cDNAs Immunol. Cell Biol 78 103–109

    CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Robert Gemmell for supplying the bandicoot tissue and Dr. Marilyn Renfree and Dr. Andrew Pask for supplying the tammar wallaby tissue used for the construction of the cDNA libraries. The authors also thank Dr. Ellen Goldberg for critically reading the manuscript. This publication was made possible by the National Institutes of Health grant No. IP20RR18754 from the Institutional Development Award (IDeA) program of the National Center for Research Resources to MLB.

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  1. Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA

    Michelle L. Baker, Amy K. Osterman & Sandra Brumburgh

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  1. Michelle L. Baker
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  2. Amy K. Osterman
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  3. Sandra Brumburgh
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Correspondence to Michelle L. Baker.

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Baker, M.L., Osterman, A.K. & Brumburgh, S. Divergent T-cell receptor delta chains from marsupials. Immunogenetics 57, 665–673 (2005). https://doi.org/10.1007/s00251-005-0030-0

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