Skip to main content
Log in

Organization, complexity and allelic diversity of the porcine (Sus scrofa domestica) immunoglobulin lambda locus

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

Abstract

We have characterized the organization, complexity, and expression of the porcine (Sus scrofa domestica) immunoglobulin lambda (IGL) light chain locus, which accounts for about half of antibody light chain usage in swine, yet is nearly totally unknown. Twenty-two IGL variable (IGLV) genes were identified that belong to seven subgroups. Nine genes appear to be functional. Eight possess stop codons, frameshifts, or both, and one is missing the V-EXON. Two additional genes are missing an essential cysteine residue and are classified as ORF (open reading frame). The IGLV genes are organized in two distinct clusters, a constant (C)-proximal cluster dominated by genes similar to the human IGLV3 subgroup, and a C-distal cluster dominated by genes most similar to the human IGLV8 and IGLV5 subgroups. Phylogenetic analysis reveals that the porcine IGLV8 subgroup genes have recently expanded, suggesting a particularly effective role in immunity to porcine-specific pathogens. Moreover, expression of IGLV genes is nearly exclusively restricted to the IGLV3 and IGLV8 genes. The constant locus comprises three tandem cassettes comprised of a joining (IGLJ) gene and a constant (IGLC) gene, whereas a fourth downstream IGLJ gene has no corresponding associated IGLC gene. Comparison of individual BACs generated from the same individual revealed polymorphisms in IGLC2 and several IGLV genes, indicating that allelic variation in IGLV further expands the porcine antibody light chain repertoire.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    PubMed  CAS  Google Scholar 

  • Archibald AL, Bolund L, Churcher C, Fredholm M, Groenen MAM, Harlizius B, Lee KT, Milan D, Rogers J, Rothschild MF, Uenishi H, Wang J, Schook LB, the Swine Genome Sequencing Consortium (2010) Pig genome sequence – analysis and publication strategy. BMC Genom 11:438

    Article  Google Scholar 

  • Bergman LW, Kuehl WM (1979) Formation of an intrachain disulfide bond on nascent immunoglobulin light chains. J Biol Chem 254:8869–8876

    PubMed  CAS  Google Scholar 

  • Berman JE, Nickerson KG, Pollock RR, Barth JE, Schuurman RK, Knowles DM, Chess L, Alt FW (1991) VH usage in humans: biased usage of the VH6 gene in immature B lymphoid cells. Eur J Immunol 21:1311–1314

    Article  PubMed  CAS  Google Scholar 

  • Butler JE, Wertz N, Sun J, Wang H, Lemke C, Chardon P, Piumi F, Wells K (2005) The pre-immune variable kappa repertoire of swine is selectively generated from certain subfamilies of Vκ2 and one Jκ gene. Vet Immunol Immunop 108:127–137

    Article  CAS  Google Scholar 

  • Butler JE, Sun J, Wertz N, Sinkora M (2006) Antibody repertoire development in swine. Dev Comp Immunol 30:199–221

    Article  PubMed  CAS  Google Scholar 

  • Eguchi-Ogawa T, Wertz N, Sun XZ, Puimi F, Uenishi H, Wells K, Chardon P, Tobin GJ, Butler JE (2010) Antibody repertoire development in fetal and neonatal piglets: XI. The relationship of variable heavy chain gene usage and the genomic organization of the variable heavy chain locus. J Immunol 184:3734–3742

    Article  PubMed  CAS  Google Scholar 

  • Frippiat JP, Williams SC, Tomlinson IM, Cook GP, Cherif D, Le Paslier D, Collins JE, Dunham I, Winter G, Lefranc M-P (1995) Organization of the human immunoglobulin lambda light-chain locus on chromosome 22q11.2. Hum Mol Genet 4:983–991

    Article  PubMed  CAS  Google Scholar 

  • Giudicelli V, Chaume D, Lefranc M-P (2005) IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res 33:D256–D261

    Article  PubMed  CAS  Google Scholar 

  • Giudicelli V, Duroux P, Ginestoux C, Folch G, Jabado-Michaloud J, Chaume D, Lefranc M-P (2006) IMGT/LIGM-DB, the IMGT® comprehensive database of immunoglobulin and T cell receptor nucleotide sequences. Nucleic Acids Res 34:D781–D784

    Article  PubMed  CAS  Google Scholar 

  • Gorodkin J, Cirera S, Hedegaard J, Gilchrist MJ, Panitz F, Jørgensen C, Scheibye-Knudsen K, Arvin T, Lumholdt S, Sawera M, Green T, Nielsen BJ, Havgaard JH, Rosenkilde C, Wang J, Li H, Li R, Liu B, Hu S, Dong W, Li W, Yu J, Wang J, Stærfeldt H, Wernersson R, Madsen LB, Thomsen B, Hornshøj H, Bujie Z, Wang X, Wang X, Bolund L, Brunak S, Yang H, Bendixen C, Fredholm M (2007) Porcine transcriptome analysis based on 97 non-normalized cDNA libraries and assembly of 1,021,891 expressed sequence tags. Genome Biol 8:R45

    Article  PubMed  Google Scholar 

  • Hubbard T, Barker D, Birney E, Cameron G, Chen Y, Clark L, Cox T, Cuff J, Curwen V, Down T, Durbin R, Eyras E, Gilbert J, Hammond M, Huminiecki L, Kasprzyk A, Lehvaslaiho H, Lijnzaad P, Melsopp C, Mongin E, Pettett R, Pocock M, Potter S, Rust A, Schmidt E, Searle S, Slater G, Smith J, Spooner W, Stabenau A, Stalker J, Stupka E, Ureta-Vidal A, Vastrik I, Clamp M (2002) The Ensembl genome database project. Nucleic Acids Res 30:38–41

    Article  PubMed  CAS  Google Scholar 

  • Humphray SJ, Scott CE, Clark R, Marron B, Bender C, Camm N, Davis J, Jenks A, Noon A, Patel M, Sehra H, Yang F, Rogatcheva MB, Milan D, Chardon P, Rohrer G, Nonneman D, de Jong P, Meyers SN, Archibald A, Beever JE, Schook LB, Rogers J (2007) A high utility map of the pig genome. Genome Biol 8:R139

    Article  PubMed  Google Scholar 

  • Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinform 8:460

    Article  Google Scholar 

  • Jung D, Giallourakis C, Mostoslavsky R, Alt FW (2006) Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus. Annu Rev Immunol 24:541–570

    Article  PubMed  CAS  Google Scholar 

  • Kim DR, Oettinger MA (2000) V(D)J recombination: site-specific cleavage and repair. Mol Cells 10:367–374

    PubMed  CAS  Google Scholar 

  • Knight KL, Becker RS (1990) Molecular basis of the allelic inheritance of rabbit immunoglobulin VH allotypes: implications for the generation of antibody diversity. Cell 60:963–970

    Article  PubMed  CAS  Google Scholar 

  • Lammers BM, Beaman KD, Kim YB (1991) Sequence analysis of porcine immunoglobulin light chain cDNAs. Mol Immunol 28:877–880

    Article  PubMed  CAS  Google Scholar 

  • Lefranc M-P (2007) WHO-IUIS Nomenclature Subcommittee for Immunoglobulins and T cell receptors report. Immunogenetics 59:899–902

    Article  PubMed  Google Scholar 

  • Lefranc M-P (2008) WHO-IUIS Nomenclature Subcommittee for Immunoglobulins and T cell receptors report. Immunoglobulins and T cell receptors report August 2007, 13th International Congress of Immunology, Rio de Janeiro, Brazil. Dev Comp Immunol 32:461–463

    Article  PubMed  Google Scholar 

  • Lefranc M-P, Lefranc G (2001) The immunoglobulin factsbook. Academic Press, London, pp 1–458

    Google Scholar 

  • Lefranc M-P, Pommié 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

    Article  PubMed  CAS  Google Scholar 

  • Lefranc M-P, Pommié C, Kaas Q, Duprat E, Bosc N, Guiraudou D, Jean C, Ruiz M, Da Piédade I, Rouard M, Foulquier E, Thouvenin V, Lefranc G (2005) IMGT unique numbering for immunoglobulin and T cell receptor constant domains and Ig superfamily C-like domains. Dev Comp Immunol 29:185–203

    Article  PubMed  CAS  Google Scholar 

  • Lefranc M-P, Giudicelli V, Ginestoux C, Jabado-Michaloud J, Folch G, Bellahcene F, Wu Y, Gemrot E, Brochet X, Lane J, Regnier L, Ehrenmann F, Lefranc G, Duroux P (2009) IMGT®, the international ImMunoGeneTics information system®. Nucleic Acids Res 37:D1006–D1012

    Article  PubMed  CAS  Google Scholar 

  • Malynn BA, Yancopoulos GD, Barth JE, Bona CA, Alt FW (1990) Biased expression of JH-proximal VH genes occurs in the newly generated repertoire of neonatal and adult mice. J Exp Med 171:843–859

    Article  PubMed  CAS  Google Scholar 

  • McBlane JF, Van Gent DC, Ramsden DA, Romeo C, Cuomo CA, Gellert M, Oettinger MA (1995) Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell 83:387–395

    Article  PubMed  CAS  Google Scholar 

  • Parslow TG, Blair DL, Murphy WJ, Granner DK (1984) Structure of the 5′ ends of immunoglobulin genes: a novel conserved sequence. Proc Natl Acad Sci U S A 81:2650–2654

    Article  PubMed  CAS  Google Scholar 

  • Pasman Y, Saini SS, Smith E, Kaushik AK (2010) Organization and genomic complexity of bovine λ-light chain gene locus. Vet Immunol Immunop 135:306–313

    Article  CAS  Google Scholar 

  • Ramsden DA, Baetz KA, Wu GE (1994) Conservation of sequence in recombination signal sequence spacers. Nucleic Acids Res 22:1785–1796

    Article  PubMed  CAS  Google Scholar 

  • Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945

    Article  PubMed  CAS  Google Scholar 

  • Sanchez P, Nadel B, Cazenave PA (1991) V lambda–J lambda rearrangements are restricted within a V–J–C recombination unit in the mouse. Eur J Immunol 21:907–911

    Article  PubMed  CAS  Google Scholar 

  • Schook LB, Beever JE, Rogers J, Humphray S, Archibald A, Chardon P, Milan D, Rohrer G, Eversole K (2005) Swine Genome Sequencing Consortium (SGSC): a strategic roadmap for sequencing the pig genome. Comp Funct Genom 6:251–255

    Article  CAS  Google Scholar 

  • Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123

    Article  PubMed  CAS  Google Scholar 

  • Wu TT, Kabat EA (1970) An analysis of the sequences of the variable regions of Bence Jones proteins and their myeloma light chains and their implications for antibody complementarity. J Exp Med 132:211–250

    Article  PubMed  CAS  Google Scholar 

  • Yancopolous GD, Desiderio SV, Paskind M, Kearney JF, Baltimore D, Alt FW (1984) Preferential utilization of the most JH-proximal VH gene segments in pre-B-cell lines. Nature 311:727–733

    Article  Google Scholar 

  • Yerle M, Lahbib-Mansais Y, Pinton P, Robic A, Goureau A, Milan D, Gellin J (1997) The cytogenetic map of the domestic pig (Sus scrofa domestica). Mamm Genom 8:592–607

    Article  CAS  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de bruijn graphs. Genome Res 18:821–829

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Erin Babineau for excellent technical assistance, and Dr. Jane Loveland for generous review of the manuscript. This work was supported by a grant from the U.S. National Pork Board (10-139).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John C. Schwartz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schwartz, J.C., Lefranc, MP. & Murtaugh, M.P. Organization, complexity and allelic diversity of the porcine (Sus scrofa domestica) immunoglobulin lambda locus. Immunogenetics 64, 399–407 (2012). https://doi.org/10.1007/s00251-011-0594-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-011-0594-9

Keywords

Navigation