Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Jan 15;88(2):537–541. doi: 10.1073/pnas.88.2.537

Evolution of the major histocompatibility complex: molecular cloning of major histocompatibility complex class I from the amphibian Xenopus.

M F Flajnik 1, C Canel 1, J Kramer 1, M Kasahara 1
PMCID: PMC50846  PMID: 1703301

Abstract

Class I major histocompatibility complex (MHC) cDNA clones have been isolated from an expression library derived from mRNA of an MHC homozygous Xenopus laevis. The nucleotide and predicted amino acid sequences show definite similarity to MHC class I molecules of higher vertebrates. The immunoglobulin-like alpha-3 domain is more similar to the immunoglobulin-like domains of mammalian class II beta chains than to those of mammalian class I molecules, and a tree based on nucleotide sequences of representative MHC genes is presented.

Full text

PDF
537

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. 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]
  2. Bilofsky H. S., Burks C. The GenBank genetic sequence data bank. Nucleic Acids Res. 1988 Mar 11;16(5):1861–1863. doi: 10.1093/nar/16.5.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Boss J. M., Strominger J. L. Cloning and sequence analysis of the human major histocompatibility complex gene DC-3 beta. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5199–5203. doi: 10.1073/pnas.81.16.5199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bourlet Y., Béhar G., Guillemot F., Fréchin N., Billault A., Chaussé A. M., Zoorob R., Auffray C. Isolation of chicken major histocompatibility complex class II (B-L) beta chain sequences: comparison with mammalian beta chains and expression in lymphoid organs. EMBO J. 1988 Apr;7(4):1031–1039. doi: 10.1002/j.1460-2075.1988.tb02910.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Brutlag D. L., Dautricourt J. P., Maulik S., Relph J. Improved sensitivity of biological sequence database searches. Comput Appl Biosci. 1990 Jul;6(3):237–245. doi: 10.1093/bioinformatics/6.3.237. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Cameron G. N. The EMBL data library. Nucleic Acids Res. 1988 Mar 11;16(5):1865–1867. doi: 10.1093/nar/16.5.1865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Flajnik M. F., Du Pasquier L. The major histocompatibility complex of frogs. Immunol Rev. 1990 Feb;113:47–63. doi: 10.1111/j.1600-065x.1990.tb00036.x. [DOI] [PubMed] [Google Scholar]
  11. Flajnik M. F., Kaufman J. F., Du Pasquier L. Studies on the Xenopus major histocompatibility complex. Dev Comp Immunol. 1985 Fall;9(4):777–781. doi: 10.1016/0145-305x(85)90043-6. [DOI] [PubMed] [Google Scholar]
  12. Flajnik M. F., Kaufman J. F., Hsu E., Manes M., Parisot R., Du Pasquier L. Major histocompatibility complex-encoded class I molecules are absent in immunologically competent Xenopus before metamorphosis. J Immunol. 1986 Dec 15;137(12):3891–3899. [PubMed] [Google Scholar]
  13. Flajnik M. F., Kaufman J. F., Riegert P., Du Pasquier L. Identification of class I major histocompatibility complex encoded molecules in the amphibian Xenopus. Immunogenetics. 1984;20(4):433–442. doi: 10.1007/BF00345617. [DOI] [PubMed] [Google Scholar]
  14. Flajnik M. F., Kaufman J. F., Riegert P., Du Pasquier L. Identification of class I major histocompatibility complex encoded molecules in the amphibian Xenopus. Immunogenetics. 1984;20(4):433–442. doi: 10.1007/BF00345617. [DOI] [PubMed] [Google Scholar]
  15. Flynn G. C., Chappell T. G., Rothman J. E. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science. 1989 Jul 28;245(4916):385–390. doi: 10.1126/science.2756425. [DOI] [PubMed] [Google Scholar]
  16. George D. G., Barker W. C., Hunt L. T. The protein identification resource (PIR). Nucleic Acids Res. 1986 Jan 10;14(1):11–15. doi: 10.1093/nar/14.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Germain R. N. Antigen processing and CD4+ T cell depletion in AIDS. Cell. 1988 Aug 12;54(4):441–444. doi: 10.1016/0092-8674(88)90062-1. [DOI] [PubMed] [Google Scholar]
  18. Goto R., Miyada C. G., Young S., Wallace R. B., Abplanalp H., Bloom S. E., Briles W. E., Miller M. M. Isolation of a cDNA clone from the B-G subregion of the chicken histocompatibility (B) complex. Immunogenetics. 1988;27(2):102–109. doi: 10.1007/BF00351083. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Güssow D., Rein R., Ginjaar I., Hochstenbach F., Seemann G., Kottman A., Ploegh H. L. The human beta 2-microglobulin gene. Primary structure and definition of the transcriptional unit. J Immunol. 1987 Nov 1;139(9):3132–3138. [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. Kaufman J., Salomonsen J., Skjødt K. B-G cDNA clones have multiple small repeats and hybridize to both chicken MHC regions. Immunogenetics. 1989;30(6):440–451. doi: 10.1007/BF02421176. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Klein J., Figueroa F. Evolution of the major histocompatibility complex. Crit Rev Immunol. 1986;6(4):295–386. [PubMed] [Google Scholar]
  28. Lalanne J. L., Delarbre C., Gachelin G., Kourilsky P. A cDNA clone containing the entire coding sequence of a mouse H-2Kd histocompatibility antigen. Nucleic Acids Res. 1983 Mar 11;11(5):1567–1577. doi: 10.1093/nar/11.5.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Landau N. R., St John T. P., Weissman I. L., Wolf S. C., Silverstone A. E., Baltimore D. Cloning of terminal transferase cDNA by antibody screening. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5836–5840. doi: 10.1073/pnas.81.18.5836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Lawlor D. A., Warren E., Ward F. E., Parham P. Comparison of class I MHC alleles in humans and apes. Immunol Rev. 1990 Feb;113:147–185. doi: 10.1111/j.1600-065x.1990.tb00040.x. [DOI] [PubMed] [Google Scholar]
  32. Martin L. H., Calabi F., Milstein C. Isolation of CD1 genes: a family of major histocompatibility complex-related differentiation antigens. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9154–9158. doi: 10.1073/pnas.83.23.9154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Moriuchi J., Moriuchi T., Silver J. Nucleotide sequence of an HLA-DQ alpha chain derived from a DRw9 cell line: genetic and evolutionary implications. Proc Natl Acad Sci U S A. 1985 May;82(10):3420–3424. doi: 10.1073/pnas.82.10.3420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Nagy Z. A., Lehmann P. V., Falcioni F., Muller S., Adorini L. Why peptides? Their possible role in the evolution of MHC-restricted T-cell recognition. Immunol Today. 1989 Apr;10(4):132–138. doi: 10.1016/0167-5699(89)90247-8. [DOI] [PubMed] [Google Scholar]
  36. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  37. Radojcic A., Stranick K. S., Locker J., Kunz H. W., Gill T. J., 3rd Nucleotide sequence of a rat class I cDNA clone. Immunogenetics. 1989;29(2):134–137. doi: 10.1007/BF00395865. [DOI] [PubMed] [Google Scholar]
  38. Reyes A. A., Johnson M. J., Schöld M., Ito H., Ike Y., Morin C., Itakura K., Wallace R. B. Identification of an H-2Kb-related molecule by molecular cloning. Immunogenetics. 1981;14(5):383–392. doi: 10.1007/BF00373318. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Salter R. D., Benjamin R. J., Wesley P. K., Buxton S. E., Garrett T. P., Clayberger C., Krensky A. M., Norment A. M., Littman D. R., Parham P. A binding site for the T-cell co-receptor CD8 on the alpha 3 domain of HLA-A2. Nature. 1990 May 3;345(6270):41–46. doi: 10.1038/345041a0. [DOI] [PubMed] [Google Scholar]
  41. Schneider C., Newman R. A., Sutherland D. R., Asser U., Greaves M. F. A one-step purification of membrane proteins using a high efficiency immunomatrix. J Biol Chem. 1982 Sep 25;257(18):10766–10769. [PubMed] [Google Scholar]
  42. Strachan T., Sodoyer R., Damotte M., Jordan B. R. Complete nucleotide sequence of a functional class I HLA gene, HLA-A3: implications for the evolution of HLA genes. EMBO J. 1984 Apr;3(4):887–894. doi: 10.1002/j.1460-2075.1984.tb01901.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Trowsdale J., Kelly A. The human HLA class II alpha chain gene DZ alpha is distinct from genes in the DP, DQ and DR subregions. EMBO J. 1985 Sep;4(9):2231–2237. doi: 10.1002/j.1460-2075.1985.tb03919.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Waneck G. L., Sherman D. H., Calvin S., Allen H., Flavell R. A. Tissue-specific expression of cell-surface Qa-2 antigen from a transfected Q7b gene of C57BL/10 mice. J Exp Med. 1987 May 1;165(5):1358–1370. doi: 10.1084/jem.165.5.1358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Williams A. F., Barclay A. N. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. doi: 10.1146/annurev.iy.06.040188.002121. [DOI] [PubMed] [Google Scholar]
  47. Zinkernagel R. M., Doherty P. C. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature. 1974 Apr 19;248(5450):701–702. doi: 10.1038/248701a0. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. van Hoof M., de Geus J. P., Roos M., Brown C., Jacobs H., Ploegh H. The primary structure of a feline class I gene: striking similarity to HLA-A. Immunogenetics. 1989;30(5):330–334. doi: 10.1007/BF02425272. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES