Abstract
Complementary DNAs encoding immunoglobulin light chains were isolated from two monotreme species, Ornithorhynchus anatinus (duckbill platypus) and Tachyglossus aculeatus (echidna). The sequences of both the variable and constant regions of these clones had greater similarity to IGK than to other light chain classes and phylogenetic analyses place them squarely within the mammalian IGK group, establishing them as monotreme IGK homologues. The constant region sequences of all clones were essentially identical within each species and, along with Southern blot results, the data are consistent with a single IGKC in each species. The expressed IGKV repertoires from both platypus and echidna were randomly sampled and there appear to be at least four platypus and at least nine echidna IGKV subgroups. The IGKV subgroups are highly divergent within species, in some cases sharing as little as 57% nucleotide identity. Two of the IGKV subgroups are present in both species, so there is some degree of overlap in the germline repertoires of these two monotremes. Overall the complexity seen in platypus and echidna IGK light chains is comparable with that of other mammals considered to have high levels of germline diversity and is in contrast to what has been found so far for monotreme IGL.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Atwell JL, Marchalonis JJ (1977) Immunoglobulin gamma chains of a monotreme mammal, the echidna (Tachyglossus aculeatus): amino acid composition and partial amino acid sequence. J Immunogenet 4:73–80
Atwell JL, Marchalonis JJ, Ealey EHM (1973) Major immunoglobulin classes of the echidna (Tachyglossus aculeatus). Immunology 25:835–846
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 Mammal Evol 11:1–16
Belov K, Hellman L, Cooper DW (2002a) Characterization of immunoglobulin gamma 1 from a monotreme, Tachyglossus aculeatus. Immunogenetics 53:1065–1071
Belov K, Hellman L, Cooper DW (2002b) Characterisation of echidna IgM provides insights into the time of divergence of extant mammals. Dev Comp Immunol 26:831–839
Brodeur PH, Riblet R (1984) The immunoglobulin heavy chain variable region (Igh-V) locus in the mouse I. One hundred Igh-V genes comprise seven families of homologous genes. Eur J Immunol 14:922–930
Diener E, Ealey EHM (1965) Immune system in a monotreme: studies on the Australian echidna. Nature 208:950–953
Diener E, Wistar R, Ealey EHM (1967) Phylogenetic studies on the immune response. II. The immune response of the Australian echidna Tachyglossus aculeatus. Immunology 13:329–337
Greenberg AS, Steiner L, Kasahara M, Flajnik MF (1993) Isolation of a shark immunoglobulin light chain cDNA clone encoding a protein resembling mammalian kappa light chains: implications for the evolution of light chains. Proc Natl Acad Sci USA 90:10603–10607
Griffiths M (1978) The biology of the monotremes. Academic, New York
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Huxley TH (1880) On the application of laws of evolution to the arrangement of the Vertebrata, and more particularly of the Mammalia. Proc Zool Soc Lond 43:649–662
Johansson J, Aveskogh M, Munday B, Hellman L (2002) Heavy chain V region diversity in the duck-billed platypus (Ornithorhynchus anatinus): long and highly variable complementarity-determining region 3 compensates for limited germline diversity. J Immunol 168:5155–5162
Jurd RD (1994) Not proper mammals: immunity in monotremes and marsupials. Comp Immunol Microbiol Infect Dis 17:41–52
Kawasaki K, Minoshima S, Nakato E, Shibuya K, Shintani A, Asakawa S, Sasaki T, Klobeck H-G, Combriato G, Zachau HG, Shimizu N (2001) Evolutionary dynamics of the human immunoglobulin κ locus and the germline repertoire of Vκ genes. Eur J Immunol 31:1017–1028
Killian JK, Buckley TR, Stewart N, Munday BL, Jirtle RL (2001) Marsupials and eutherians reunited: genetic evidence for the Theria hypothesis of mammalian evolution. Mamm Genome 12:513–517
Kumar S, Tamura K, Jakobsen IB, Nei N (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245
Lefranc M-P (2003) IMGT, the international ImMunoGeneTics information system®. Nucleic Acids Res 31:307–310
Lefranc M-P, Lefranc G (2001) The immunoglobulin FactsBook. Academic, London
Lefranc M-P, Pommie C, Ruiz M, Giudicelli V, Foulquier E, Truong L, Thouvenin-Contet V, Lefranc G (2003) IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev Comp Immunol 27:55–77
Lucero JE, Rosenberg GH, Miller RD (1998) Marsupial light chains: complexity and conservation of λ in the opossum Monodelphis domestica. J Immunol 161:6724–6732
Lundqvist M, Bengten E, Stromberg S, Pilstrom L (1996) Ig light chain gene in the siberian sturgeon (Acipenser baeri). Implications for the evolution of the immune system. J Immunol 157:2031–2038
Marchalonis JJ, Atwell JL, Goding JW (1978) 7S immunoglobulins of a monotreme, the echidna Tachyglossus aculeatus: two distinct isotypes which bind A protein of Staphylococcus aureus. Immunology 34:97–103
Messer M, Weiss AS, Shaw DC, Westerman M (1998) Evolution of the monotremes: phylogenetic relationship to marsupials and eutherians, and estimation of divergence dates based on α-lactalbumin amino acid sequences. J Mammal Evol 5:95–105
Miller RD, Bergemann ER, Rosenberg GH (1999) Marsupial light chains: IGK with four V families in the opossum Monodelphis domestica. Immunogenetics 50:329–335
Musser AM (2003) Review of the monotreme fossil record and comparison of paleontological and molecular data. Comp Biochem Physiol A Mol Integr Physiol 136:927–942
Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA 94:7799–7806
Pilstrom L (2002) The mysterious immunoglobulin light chain. Dev Comp Immunol 26:207–215
Poorafshar M, Aveskogh M, Munday BL, Hellman L (2000) Identification and structural analysis of four serine proteases in a monotreme, the platypus, Ornithorhynchus anatinus. Immunogenetics 52:19–28
Rast JP, Anderson MK, Litman GW (1995) Ig genes in lower vertebrates. In: Honjo T, Alt FW (eds) Immunoglobulin genes. Academic, San Diego, p 315
Retief JD, Winkfein RJ, Dixon GH (1993) Evolution of the monotremes: the sequences of the protamine P1 genes of platypus and echidna. Eur J Biochem 218:457–461
Schwager J, Bürckert N, Schwager M, Wilson M (1991) Evolution of immunoglobulin light chain genes: analysis of Xenopus IgL isotypes and their contribution to antibody diversity. EMBO J 10:505–511
Shapiro MA, Weigert M (1987) How immunoglobulin VK genes rearrange. J Immunol 139:3834–3839
Sitnikova T, Su C (1998) Coevolution of immunoglobulin heavy- and light-chain variable-region gene families. Mol Biol Evol 15:617–625
Strohal RA, Helmberg A, Kroemer G, Kofler R (1989) Mouse Vκ gene classification by nucleic acid sequence similarity. Immunogenetics 30:475–493
Swofford DL (1998) PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4.0 beta. Sinauer, Sunderland
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Vernesson M, Aveskogh M, Munday BL, Hellman L (2002) Evidence for an early appearance of modern posts-witch immunoglobulin isotypes in mammalian evolution (II); cloning of IgE, IgG1 and IgG2 from a monotreme, the duck-billed platypus, Omithorhynchus anatinus. Eur J Immunol 32:2145–2155
Vernesson M, Aveskogh M, Hellman L (2004) Cloning of IgE from the echidna (Tachyglossus aculeatus) and a comparative analysis of ε chains from all three extant mammalian lineages. Dev Comp Immunol 28:61–75
Zezza DJ, Stewart SE, Steiner LA (1992) Genes encoding Xenopus laevis Ig L chains. Implications for the evolution of κ and λ chains. J Immunol 149:3968–3977
Acknowledgements
The work reported was supported by the National Science Foundation (MCB-9981960 to R.D.M.) and the Swedish Natural Sciences Research Council (L.H.).
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Nowak, M.A., Parra, Z.E., Hellman, L. et al. The complexity of expressed kappa light chains in egg-laying mammals. Immunogenetics 56, 555–563 (2004). https://doi.org/10.1007/s00251-004-0720-z
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00251-004-0720-z