Home LiteratureArticle Details
PMID: 15753291 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Origin and evolution of the chicken leukocyte receptor complex.

Nikolaidis N, Makalowska I, Chalkia D, Makalowski W, Klein J, Nei M

Abstract

In mammals, the cell surface receptors encoded by the leukocyte receptor complex (LRC) regulate the activity of T lymphocytes and B lymphocytes, as well as that of natural killer cells, and thus provide protection against pathogens and parasites. The chicken genome encodes many Ig-like receptors that are homologous to the LRC receptors. The chicken Ig-like receptor (CHIR) genes are members of a large monophyletic gene family and are organized into genomic clusters, which are in conserved synteny with the mammalian LRC. One-third of CHIR genes encode polypeptide molecules that contain both activating and inhibitory motifs. These genes are present in different phylogenetic groups, suggesting that the primordial CHIR gene could have encoded both types of motifs in a single molecule. In contrast to the mammalian LRC genes, the CHIR genes with similar function (inhibition or activation) are evolutionarily closely related. We propose that, in addition to recombination, single nucleotide substitutions played an important role in the generation of receptors with different functions. Structural models and amino acid analyses of the CHIR proteins reveal the presence of different types of Ig-like domains in the same phylogenetic groups, as well as sharing of conserved residues and conserved changes of residues between different CHIR groups and between CHIRs and LRCs. Our data support the notion that the CHIR gene clusters are regions homologous to the mammalian LRC gene cluster and favor a model of evolution by repeated processes of birth and death (expansion-contraction) of the Ig-like receptor genes.

MeSH Terms
Animals Chickens/genetics Evolution, Molecular Leukocytes/metabolism Protein Structure, Tertiary Receptors, Cell Surface/genetics,metabolism Sequence Analysis, DNA
Chemicals
Receptors, Cell Surface
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Nikolaidis Nikolas
Institute of Molecular Evolutionary Genetics, Department of Biology, Pennsylvania State University, University Park, PA 16802, USA. [email protected]
Makalowska Izabela
Chalkia Dimitra
Makalowski Wojciech
Klein Jan
Nei Masatoshi
References (28)
28 references, click to expand
  1. Enhanced genome annotation using structural profiles in the program 3D-PSSM.
    J Mol Biol. 2000 Jun 2;299(2):499-520 PMID: 10860755
  2. Origin and evolution of the Ig-like domains present in mammalian leukocyte receptors: insights from chicken, frog, and fish homologues.
    Immunogenetics. 2005 Apr;57(1-2):151-7 PMID: 15702330
  3. Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2).
    Immunity. 2000 Nov;13(5):727-36 PMID: 11114384
  4. Computational inference of homologous gene structures in the human genome.
    Genome Res. 2001 May;11(5):803-16 PMID: 11337476
  5. The genomic context of natural killer receptor extended gene families.
    Immunol Rev. 2001 Jun;181:20-38 PMID: 11513141
  6. Genesis of the ILT/LIR/MIR clusters within the human leukocyte receptor complex.
    Immunol Rev. 2001 Jun;181:39-51 PMID: 11513150
  7. Structure of killer cell immunoglobulin-like receptors and their recognition of the class I MHC molecules.
    Immunol Rev. 2001 Jun;181:66-78 PMID: 11513153
  8. MEGA2: molecular evolutionary genetics analysis software.
    Bioinformatics. 2001 Dec;17(12):1244-5 PMID: 11751241
  9. Identification of six novel genes by experimental validation of GeneMachine predicted genes.
    Gene. 2002 Feb 6;284(1-2):203-13 PMID: 11891061
  10. Leukocyte Ig-like receptor complex (LRC) in mice and men.
    Trends Immunol. 2002 Feb;23(2):81-8 PMID: 11929131
  11. KIR2DL4 (CD158d), an NK cell-activating receptor with inhibitory potential.
    J Immunol. 2002 Jun 15;168(12):6208-14 PMID: 12055234
  12. Evolution of the human killer cell inhibitory receptor family.
    Mol Phylogenet Evol. 2002 Nov;25(2):330-40 PMID: 12414314
  13. Natural killer cell receptor signaling.
    Curr Opin Immunol. 2003 Jun;15(3):308-14 PMID: 12787756
  14. SWISS-MODEL: An automated protein homology-modeling server.
    Nucleic Acids Res. 2003 Jul 1;31(13):3381-5 PMID: 12824332
  15. Killer-cell immunoglobulin-like receptor (KIR) nomenclature report, 2002.
    Tissue Antigens. 2003 Jul;62(1):79-86 PMID: 12859599
  16. The Pfam protein families database.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D138-41 PMID: 14681378
  17. SMART 4.0: towards genomic data integration.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D142-4 PMID: 14681379
  18. Comparative genomic analysis of two avian (quail and chicken) MHC regions.
    J Immunol. 2004 Jun 1;172(11):6751-63 PMID: 15153492
  19. WebLogo: a sequence logo generator.
    Genome Res. 2004 Jun;14(6):1188-90 PMID: 15173120
  20. Genomic organization and evolutionary analysis of Ly49 genes encoding the rodent natural killer cell receptors: rapid evolution by repeated gene duplication.
    Immunogenetics. 2004 Aug;56(5):343-54 PMID: 15316687
  21. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  22. Evolution of immunoglobulin VH pseudogenes in chickens.
    Mol Biol Evol. 1995 Jan;12(1):94-102 PMID: 7877500
  23. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  24. Coevolution of immunoglobulin heavy- and light-chain variable-region gene families.
    Mol Biol Evol. 1998 Jun;15(6):617-25 PMID: 9615443
  25. Chicken Ig-like receptor B2, a member of a multigene family, is mainly expressed on B lymphocytes, recruits both Src homology 2 domain containing protein tyrosine phosphatase (SHP)-1 and SHP-2, and inhibits proliferation.
    J Immunol. 2004 Dec 15;173(12):7385-93 PMID: 15585863
  26. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution.
    Nature. 2004 Dec 9;432(7018):695-716 PMID: 15592404
  27. Single haplotype analysis demonstrates rapid evolution of the killer immunoglobulin-like receptor (KIR) loci in primates.
    Genome Res. 2005 Jan;15(1):25-35 PMID: 15632087
  28. Paired Ig-like receptor homologs in birds and mammals share a common ancestor with mammalian Fc receptors.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13245-50 PMID: 11078516
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-03-15
Epub
2005-00-07
Pages
4057-62
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC554838
Subset
IM
Grants
NIGMS NIH HHS · R01 GM020293 · United States
NIGMS NIH HHS · GM20293 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]