Abstract
Along with the T-cell receptor and immunoglobulin, the major histocompatibility complex (MHC) plays a key role in mounting immune responses to foreign antigen. To gain insights into the evolution of the MHC, class II A cDNA clones were isolated from nurse sharks, a member of the class of cartilaginous fish. Two closely related cDNA clones, which might encode allelic products, were identified; of the three amino acid substitutions found in the alpha 1 domain, two were located at positions postulated to interact with processed peptides. The deduced nurse shark MHC class II alpha chains showed conspicuous structural similarity to their mammalian counterparts. Isolation of cDNA clones encoding typical MHC class II alpha chains was unexpected since no direct evidence for T-cell-mediated immune responses has been obtained in the cartilaginous fish. The cartilaginous fish is phylogenetically the most primitive class of vertebrates from which any MHC gene has been isolated.
Full text
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Selected References
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- Benoist C. O., Mathis D. J., Kanter M. R., Williams V. E., 2nd, McDevitt H. O. Regions of allelic hypervariability in the murine A alpha immune response gene. Cell. 1983 Aug;34(1):169–177. doi: 10.1016/0092-8674(83)90147-2. [DOI] [PubMed] [Google Scholar]
- Bjorkman P. J., Parham P. Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem. 1990;59:253–288. doi: 10.1146/annurev.bi.59.070190.001345. [DOI] [PubMed] [Google Scholar]
- Bjorkman P. J., Saper M. A., Samraoui B., Bennett W. S., Strominger J. L., Wiley D. C. Structure of the human class I histocompatibility antigen, HLA-A2. Nature. 1987 Oct 8;329(6139):506–512. doi: 10.1038/329506a0. [DOI] [PubMed] [Google Scholar]
- Bjorkman P. J., Saper M. A., Samraoui B., Bennett W. S., Strominger J. L., Wiley D. C. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature. 1987 Oct 8;329(6139):512–518. doi: 10.1038/329512a0. [DOI] [PubMed] [Google Scholar]
- Brown J. H., Jardetzky T., Saper M. A., Samraoui B., Bjorkman P. J., Wiley D. C. A hypothetical model of the foreign antigen binding site of class II histocompatibility molecules. Nature. 1988 Apr 28;332(6167):845–850. doi: 10.1038/332845a0. [DOI] [PubMed] [Google Scholar]
- Calabi F., Milstein C. A novel family of human major histocompatibility complex-related genes not mapping to chromosome 6. Nature. 1986 Oct 9;323(6088):540–543. doi: 10.1038/323540a0. [DOI] [PubMed] [Google Scholar]
- Flajnik M. F., Canel C., Kramer J., Kasahara M. Evolution of the major histocompatibility complex: molecular cloning of major histocompatibility complex class I from the amphibian Xenopus. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):537–541. doi: 10.1073/pnas.88.2.537. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flajnik M. F., Canel C., Kramer J., Kasahara M. Which came first, MHC class I or class II? Immunogenetics. 1991;33(5-6):295–300. doi: 10.1007/BF00216688. [DOI] [PubMed] [Google Scholar]
- Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guillemot F., Billault A., Pourquié O., Béhar G., Chaussé A. M., Zoorob R., Kreibich G., Auffray C. A molecular map of the chicken major histocompatibility complex: the class II beta genes are closely linked to the class I genes and the nucleolar organizer. EMBO J. 1988 Sep;7(9):2775–2785. doi: 10.1002/j.1460-2075.1988.tb03132.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gustafsson K., Widmark E., Jonsson A. K., Servenius B., Sachs D. H., Larhammar D., Rask L., Peterson P. A. Class II genes of the human major histocompatibility complex. Evolution of the DP region as deduced from nucleotide sequences of the four genes. J Biol Chem. 1987 Jun 25;262(18):8778–8786. [PubMed] [Google Scholar]
- Gustafsson K., Wiman K., Emmoth E., Larhammar D., Böhme J., Hyldig-Nielsen J. J., Ronne H., Peterson P. A., Rask L. Mutations and selection in the generation of class II histocompatibility antigen polymorphism. EMBO J. 1984 Jul;3(7):1655–1661. doi: 10.1002/j.1460-2075.1984.tb02026.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HILDEMANN W. H. Tissue transplantation immunity in goldfish. Immunology. 1958 Jan;1(1):46–54. [PMC free article] [PubMed] [Google Scholar]
- Hashimoto K., Nakanishi T., Kurosawa Y. Identification of a shark sequence resembling the major histocompatibility complex class I alpha 3 domain. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2209–2212. doi: 10.1073/pnas.89.6.2209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hashimoto K., Nakanishi T., Kurosawa Y. Isolation of carp genes encoding major histocompatibility complex antigens. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6863–6867. doi: 10.1073/pnas.87.17.6863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill A. V., Allsopp C. E., Kwiatkowski D., Anstey N. M., Twumasi P., Rowe P. A., Bennett S., Brewster D., McMichael A. J., Greenwood B. M. Common west African HLA antigens are associated with protection from severe malaria. Nature. 1991 Aug 15;352(6336):595–600. doi: 10.1038/352595a0. [DOI] [PubMed] [Google Scholar]
- Hughes A. L., Nei M. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci U S A. 1989 Feb;86(3):958–962. doi: 10.1073/pnas.86.3.958. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hughes A. L., Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. doi: 10.1038/335167a0. [DOI] [PubMed] [Google Scholar]
- Jonsson A. K., Andersson L., Rask L. Complete sequences of DQA1 and DQB1 cDNA clones corresponding to the DQw4 specificity. Immunogenetics. 1989;30(3):232–234. doi: 10.1007/BF02421214. [DOI] [PubMed] [Google Scholar]
- Jonsson A. K., Rask L. Human class II DNA and DOB genes display low sequence variability. Immunogenetics. 1989;29(6):411–413. doi: 10.1007/BF00375872. [DOI] [PubMed] [Google Scholar]
- Kappes D. J., Arnot D., Okada K., Strominger J. L. Structure and polymorphism of the HLA class II SB light chain genes. EMBO J. 1984 Dec 1;3(12):2985–2993. doi: 10.1002/j.1460-2075.1984.tb02245.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaufman J., Skjoedt K., Salomonsen J. The MHC molecules of nonmammalian vertebrates. Immunol Rev. 1990 Feb;113:83–117. doi: 10.1111/j.1600-065x.1990.tb00038.x. [DOI] [PubMed] [Google Scholar]
- Kelly A. P., Monaco J. J., Cho S. G., Trowsdale J. A new human HLA class II-related locus, DM. Nature. 1991 Oct 10;353(6344):571–573. doi: 10.1038/353571a0. [DOI] [PubMed] [Google Scholar]
- Koller B. H., Orr H. T. Cloning and complete sequence of an HLA-A2 gene: analysis of two HLA-A alleles at the nucleotide level. J Immunol. 1985 Apr;134(4):2727–2733. [PubMed] [Google Scholar]
- Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Larhammar D., Hammerling U., Denaro M., Lund T., Flavell R. A., Rask L., Peterson P. A. Structure of the murine immune response I-A beta locus: sequence of the I-A beta gene and an adjacent beta-chain second domain exon. Cell. 1983 Aug;34(1):179–188. doi: 10.1016/0092-8674(83)90148-4. [DOI] [PubMed] [Google Scholar]
- Lee J. S., Trowsdale J., Travers P. J., Carey J., Grosveld F., Jenkins J., Bodmer W. F. Sequence of an HLA-DR alpha-chain cDNA clone and intron-exon organization of the corresponding gene. Nature. 1982 Oct 21;299(5885):750–752. doi: 10.1038/299750a0. [DOI] [PubMed] [Google Scholar]
- Mathis D. J., Benoist C. O., Williams V. E., 2nd, Kanter M. R., McDevitt H. O. The murine E alpha immune response gene. Cell. 1983 Mar;32(3):745–754. doi: 10.1016/0092-8674(83)90060-0. [DOI] [PubMed] [Google Scholar]
- McKinney E. C., Haynes L., Droese A. L. Macrophage-like effector of spontaneous cytotoxicity from the shark. Dev Comp Immunol. 1986 Fall;10(4):497–508. doi: 10.1016/0145-305x(86)90171-0. [DOI] [PubMed] [Google Scholar]
- Miller N. W., Deuter A., Clem L. W. Phylogeny of lymphocyte heterogeneity: the cellular requirements for the mixed leucocyte reaction with channel catfish. Immunology. 1986 Sep;59(1):123–128. [PMC free article] [PubMed] [Google Scholar]
- Miller N. W., Sizemore R. C., Clem L. W. Phylogeny of lymphocyte heterogeneity: the cellular requirements for in vitro antibody responses of channel catfish leukocytes. J Immunol. 1985 May;134(5):2884–2888. [PubMed] [Google Scholar]
- Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
- Saito H., Maki R. A., Clayton L. K., Tonegawa S. Complete primary structures of the E beta chain and gene of the mouse major histocompatibility complex. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5520–5524. doi: 10.1073/pnas.80.18.5520. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tonnelle C., DeMars R., Long E. O. DO beta: a new beta chain gene in HLA-D with a distinct regulation of expression. EMBO J. 1985 Nov;4(11):2839–2847. doi: 10.1002/j.1460-2075.1985.tb04012.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Townsend A., Bodmer H. Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol. 1989;7:601–624. doi: 10.1146/annurev.iy.07.040189.003125. [DOI] [PubMed] [Google Scholar]
- Wang C. R., Loveland B. E., Lindahl K. F. H-2M3 encodes the MHC class I molecule presenting the maternally transmitted antigen of the mouse. Cell. 1991 Jul 26;66(2):335–345. doi: 10.1016/0092-8674(91)90623-7. [DOI] [PubMed] [Google Scholar]
- Watts S., Vogel J. M., Harriman W. D., Itoh T., Stauss H. J., Goodenow R. S. DNA sequence analysis of the C3H H-2Kk and H-2Dk loci. Evolutionary relationships to H-2 genes from four other mouse strains. J Immunol. 1987 Dec 1;139(11):3878–3885. [PubMed] [Google Scholar]
- Zoorob R., Béhar G., Kroemer G., Auffray C. Organization of a functional chicken class II B gene. Immunogenetics. 1990;31(3):179–187. doi: 10.1007/BF00211553. [DOI] [PubMed] [Google Scholar]