Skip to main content
SpringerLink
Log in

Fugu immunoglobulin D: a highly unusual gene with unprecedented duplications in its constant region

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

We have isolated and characterized the cDNA that encodes IgD of fugu (Takifugu rubripes). Though the splicing of μ1 with the δ1 domain was similar to those reported for teleost IgDs, highly unusual and unprecedented domain duplications were found in the constant region of the fugu IgD. The structure of the fugu IgD is like VDJ-μ1-(δ1-δ2-δ3-δ4-δ5-δ6)2-δ7-δm1-δm2. Genomic sequence analysis of the fugu IgD gene supported the results of cDNA sequencing that the first six δ domains in the constant region are duplicated. Such a novel duplication pattern has not been reported in any other vertebrates. However, IgD secretory domains could not be identified in this study. The deduced amino acid sequence of the fugu IgD constant region showed high identity (35–55%) to the sequences of previously reported teleost IgDs. Gene expression analyses based on RT-PCR demonstrated that the IgD gene is preferentially expressed in presumptive lymphoid tissues; moreover, in situ hybridization showed that IgD-positive cells are distributed throughout the spleen and head kidney. The expression pattern is similar to that of IgM, corroborating the hypothesis that IgD plays an important role in the humoral immune system of this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

PBL:

Peripheral blood leucocytes

PBS-T:

Phosphate buffered saline containing 1% Tween-20

PFA:

Paraformaldehyde

RT-PCR:

Reverse transcript polymerase chain reaction

References

  • Aparicio S, Chapman J, Stupka E, Putnam N, Chia J-M, Dehal P, Christoffels A, Rash S, Hoon S, Smith A, Gelpke MDS, Roach J, Oh T, Ho IS, Wong M, Detter C, Verhoef F, Predki P, Tay A, Lucas S, Richardson P, Smith SF, Clark MS, Edwards YJK, Doggett N, Zharkikh A, Tavtigian SV, Pruss D, Barnstead M, Evans T, Baden H, Powell J, Glusman G, Rowen L, Hood L, Tan YH, Elgar G, Trevor H, Venkatesh B, Rokshar D, Brenner S (2002) Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1301–1310

    Article  CAS  PubMed  Google Scholar 

  • Bengten E, Quiniou SMA, Stuge TB, Katagiri T, Miller NW, Clem LW, Warr GW, Wilson MW (2002) The IgH locus of the channel catfish, Ictalurus punctatus, contains multiple constant region gene sequences: different genes encode heavy chains of membrane and secreted IgD. J Immunol 169:2488–2497

    CAS  PubMed  Google Scholar 

  • Breuil B, Vassiloglou B, Pepin JF, Romestand B (1997) Ontogeny of IgM-bearing cells and changes in the immunoglobulin M-like protein level (IgM) during larval stages in sea bass (Dicentrachus labrax). Fish Shellfish Immunol 7:29–43

    Article  Google Scholar 

  • Grøntvedt RN, Espelid S (2003) Immunoglobulin producing cells in the spotted wolffish (Anarhichas minor Olfasen): localization in adults and during juvenile development. Dev Comp Immunol 27:1–10

    Article  PubMed  Google Scholar 

  • Hirono I, Nam BH, Enomoto J, Uchino K, Aoki T (2003) Cloning and characterization of a cDNA encoding Japanese flounder Paralichthys olivaceus IgD. Fish Shellfish Immunol 15:63–70

    Article  CAS  PubMed  Google Scholar 

  • Hordvik I (2002) Identification of a novel immunoglobulin δ transcript and comparative analysis of the genes encoding IgD in Atlantic salmon and Atlantic halibut. Mol Immunol 39:85–91

    Article  CAS  PubMed  Google Scholar 

  • Hordvik I, Thevarajan J, Samdal I, Bastani N, Krossoy B (1999) Molecular cloning and phylogenetic analysis of the Atlantic salmon Immunoglobulin D gene. Scand J Immunol 50:202–210

    Article  CAS  PubMed  Google Scholar 

  • Keer WG, Hendershot LM, Burrows PD (1991) Regulation of IgM and IgD expression in human B-linage cells. J Immunol 146:3314–3321

    PubMed  Google Scholar 

  • Koumans-van Diepen JCE, Taverne-Thiele JJ, van Rens BTTM, Rombout JHMW (1994) Immunocytochemical and flow cytometric analysis of B cells and plasma cells in carp (Cyprinus carpio L.): an ontogenic study. Fish Shellfish Immunol 4:19–28

    Article  Google Scholar 

  • Lutz C, Ledermann B, Kosco-Vilbosis MH, Ochsenbein A, Zinkernagel RM, Kohler G, Brombacher F (1998) IgD can largely substitute for loss of IgM function in B cells. Nature 393:797–801

    Article  CAS  PubMed  Google Scholar 

  • Magor BG, Ross DA, Pilstrom L, Warr GW (1999) Transcriptional enhancers and the evolution of the IgH locus. Immunol Today 20:13–17

    Article  CAS  PubMed  Google Scholar 

  • Nitscheke L, Kosco MH, Kohler G, Lambers MC (1993) Immunoglobulin D-deficient mice can mount normal immune responses to thymus-independent and -dependent antigens. Proc Natl Acad Sci USA 90:1887–1891

    PubMed  Google Scholar 

  • Roes J, Rajewsky K (1993) Immunoglobulin-D (IgD)- deficient mice reveal an auxiliary receptor function for IgD in antigen-mediated recruitment of B cells. J Exp Med 177:45–55

    Article  CAS  PubMed  Google Scholar 

  • Romano N, Taverne-Thiele JJ, van Maanen JC, Rombout JHMW (1997) Leucocyte subpopulations in developing carp (Cyprinus carpio L.): immunocytochemical studies. Fish Shellfish Immunol 7:439–453

    Article  Google Scholar 

  • Saha NR, Suetake H, Suzuki Y (2004) Characterization and expression of the immunoglobulin light chain in the fugu: evidence of a solitaire type. Immunogenetics 56:47–55

    Google Scholar 

  • Schorder MB, Flano E, Pilstrom L, Jørgensen TØ (1998) Localization of Ig heavy chain mRNA positive cells in Atlantic cod (Gadus morhua L.) tissues; identified by in situ hybridization. Fish Shellfish Immunol 8:565–576

    Article  Google Scholar 

  • Stenvik J, Jørgensen TØ (2000) Immunoglobulin D (IgD) of Atlantic cod has a unique structure. Immunogenetics 51:452–461

    Article  CAS  PubMed  Google Scholar 

  • Stenvik J, Schorder MB, Olsen K, Zapata A, Jørgensen TØ (2001) Expression of immunoglobulin heavy chain transcripts (VH-families, IgM, and IgD) in head kidney and spleen of the Atlantic cod (Gadus morhua L.). Dev Comp Immunol 25:291–302

    Article  CAS  PubMed  Google Scholar 

  • Tucker PW, Liu CP, Mushinski JF, Blattner FR (1980) Mouse immunoglobulin D: messenger RNA and genomic DNA sequences. Science 19:1353–1360

    Google Scholar 

  • White MB, Shen AL, Word CJ, Tucker PW, Blattner FR (1985) Human immunoglobulin D: genomic sequences of the delta heavy chain. Science 228:733–737

    CAS  PubMed  Google Scholar 

  • Wilson M, Bengten E, Miller NW, Clem LW, De Pasquier L, Warr GW (1997) A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proc Natl Acad Sci USA 94:4593–4597

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Kacskovics I, Pan Q, Liberles DA, Geli J, Davis SK, Rabbani H, Hammarstrom L (2002) Artiodactyl IgD: the missing link. J Immunol 169:4408–4416

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular Genetics Department, Benaroya Research Institute at Virginia Mason, 1201 Ninth Avenue, Seattle, WA, 98101, USA

    Nil Ratan Saha

  2. Fisheries Laboratory, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Maisaka, 2971-4, Shizuoka, 431-0211, Japan

    Hiroaki Suetake, Kiyoshi Kikuchi & Yuzuru Suzuki

Authors
  1. Nil Ratan Saha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroaki Suetake
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kiyoshi Kikuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuzuru Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroaki Suetake.

Additional information

The nucleotide sequence data reported in this paper will appear in the DDBJ/EMBL/GenBank nucleotide sequence databases with the accession numbers AB159481 and AB159482.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saha, N.R., Suetake, H., Kikuchi, K. et al. Fugu immunoglobulin D: a highly unusual gene with unprecedented duplications in its constant region. Immunogenetics 56, 438–447 (2004). https://doi.org/10.1007/s00251-004-0693-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-004-0693-y

Keywords

Search

Navigation