Abstract
We have isolated two major histocompatibility complex (MHC) class II B genes from the inbred fish strain Xiphophorus maculatus Jp 163 A. We mapped one of these genes, designated here as DXB, to linkage group III, linked to a malic enzyme locus, also syntenic with human and mouse MHC. Comparison of genomic and cDNA clones shows the gene consists of six exons and five introns. The encoded beta1 domain has three amino acids deleted and a cytoplasmic tail nine amino acids longer than in other teleost class II beta chains, more similar to HLA-DRB, clawed frog Xela-F3, and nurse shark Gici-B. Key residues for disulfide bonds, glycosylation, and interaction with alpha chains are conserved. These same features are also present in a swordtail (Xiphophorus helleri) genomic DXB PCR clone. A second type of class II B clone was amplified by PCR from X. maculatus and found to be orthologous to class II genes identified in other fishes. This DAB-like gene is 63% identical to the X. maculatus DXB sequence in the conserved beta2-encoding exon and was mapped to new unassigned linkage group LG U24. The DXB gene, then, represents an unlinked duplicated locus not previously identified in teleosts.
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- Adam D., Dimitrijevic N., Schartl M. Tumor suppression in Xiphophorus by an accidentally acquired promoter. Science. 1993 Feb 5;259(5096):816–819. doi: 10.1126/science.8430335. [DOI] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Bartl S., Weissman I. L. Isolation and characterization of major histocompatibility complex class IIB genes from the nurse shark. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):262–266. doi: 10.1073/pnas.91.1.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benoist C., Mathis D. Regulation of major histocompatibility complex class-II genes: X, Y and other letters of the alphabet. Annu Rev Immunol. 1990;8:681–715. doi: 10.1146/annurev.iy.08.040190.003341. [DOI] [PubMed] [Google Scholar]
- Bingulac-Popovic J., Figueroa F., Sato A., Talbot W. S., Johnson S. L., Gates M., Postlethwait J. H., Klein J. Mapping of mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio. Immunogenetics. 1997;46(2):129–134. doi: 10.1007/s002510050251. [DOI] [PubMed] [Google Scholar]
- Borriello F., Krauter K. S. Reactive site polymorphism in the murine protease inhibitor gene family is delineated using a modification of the PCR reaction (PCR + 1). Nucleic Acids Res. 1990 Sep 25;18(18):5481–5487. doi: 10.1093/nar/18.18.5481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- CLARK E. A method for artificial insemination in viviparous fishes. Science. 1950 Dec 15;112(2920):722–723. doi: 10.1126/science.112.2920.722. [DOI] [PubMed] [Google Scholar]
- Cho S. G., Attaya M., Monaco J. J. New class II-like genes in the murine MHC. Nature. 1991 Oct 10;353(6344):573–576. doi: 10.1038/353573a0. [DOI] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dixon B., Nagelkerke L. A., Sibbing F. A., Egberts E., Stet R. J. Evolution of MHC class II beta chain-encoding genes in the Lake Tana barbel species flock (Barbus intermedius complex). Immunogenetics. 1996;44(6):419–431. [PubMed] [Google Scholar]
- Figueroa F., Ono H., Tichy H., O'Huigin C., Klein J. Evidence for insertion of a new intron into an Mhc gene of perch-like fish. Proc Biol Sci. 1995 Mar 22;259(1356):325–330. doi: 10.1098/rspb.1995.0048. [DOI] [PubMed] [Google Scholar]
- Gelfand M. S., Mironov A. A., Pevzner P. A. Gene recognition via spliced sequence alignment. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9061–9066. doi: 10.1073/pnas.93.17.9061. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Germain R. N. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell. 1994 Jan 28;76(2):287–299. doi: 10.1016/0092-8674(94)90336-0. [DOI] [PubMed] [Google Scholar]
- Glamann J. Complete coding sequence of rainbow trout Mhc II beta chain. Scand J Immunol. 1995 Apr;41(4):365–372. doi: 10.1111/j.1365-3083.1995.tb03580.x. [DOI] [PubMed] [Google Scholar]
- Godwin U. B., Antao A., Wilson M. R., Chinchar V. G., Miller N. W., Clem L. W., McConnell T. J. MHC class II B genes in the channel catfish (Ictalurus punctatus). Dev Comp Immunol. 1997 Jan-Feb;21(1):13–23. doi: 10.1016/s0145-305x(97)00003-7. [DOI] [PubMed] [Google Scholar]
- Gordon M. The Genetics of a Viviparous Top-Minnow Platypoecilus; the Inheritance of Two Kinds of Melanophores. Genetics. 1927 May;12(3):253–283. doi: 10.1093/genetics/12.3.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hardee J. J., Godwin U., Benedetto R., McConnell T. J. Major histocompatibility complex class II A gene polymorphism in the striped bass. Immunogenetics. 1995;41(4):229–238. doi: 10.1007/BF00172064. [DOI] [PubMed] [Google Scholar]
- Harless J., Svensson R., Kallman K. D., Morizot D. C., Nairn R. S. Assignment of an erbB-like DNA sequence to linkage group VI in fishes of the genus Xiphophorus (Poeciliidae). Cancer Genet Cytogenet. 1990 Nov 1;50(1):45–51. doi: 10.1016/0165-4608(90)90236-4. [DOI] [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]
- Hordvik I., Grimholt U., Fosse V. M., Lie O., Endresen C. Cloning and sequence analysis of cDNAs encoding the MHC class II beta chain in Atlantic salmon (Salmo salar). Immunogenetics. 1993;37(6):437–441. doi: 10.1007/BF00222467. [DOI] [PubMed] [Google Scholar]
- Hughes A. L., Hughes M. K. Natural selection on the peptide-binding regions of major histocompatibility complex molecules. Immunogenetics. 1995;42(4):233–243. doi: 10.1007/BF00176440. [DOI] [PubMed] [Google Scholar]
- KALLMAN K. D. AN ESTIMATE OF THE NUMBER OF HISTOCOMPATIBILITY LOCI IN THE TELEOST XIPHOPHORUS MACULATUS. Genetics. 1964 Oct;50:583–595. doi: 10.1093/genetics/50.4.583. [DOI] [PMC free article] [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]
- Kazianis S., Morizot D. C., McEntire B. B., Nairn R. S., Borowsky R. L. Genetic mapping in Xiphophorus hybrid fish: assignment of 43 AP-PCR/RAPD and isozyme markers to multipoint linkage groups. Genome Res. 1996 Apr;6(4):280–289. doi: 10.1101/gr.6.4.280. [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]
- Klein J., Bontrop R. E., Dawkins R. L., Erlich H. A., Gyllensten U. B., Heise E. R., Jones P. P., Parham P., Wakeland E. K., Watkins D. I. Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics. 1990;31(4):217–219. doi: 10.1007/BF00204890. [DOI] [PubMed] [Google Scholar]
- Kobari F., Sato K., Shum B. P., Tochinai S., Katagiri M., Ishibashi T., Du Pasquier L., Flajnik M. F., Kasahara M. Exon-intron organization of Xenopus MHC class II beta chain genes. Immunogenetics. 1995;42(5):376–385. doi: 10.1007/BF00179399. [DOI] [PubMed] [Google Scholar]
- Kuroda N., Wada H., Naruse K., Simada A., Shima A., Sasaki M., Nonaka M. Molecular cloning and linkage analysis of the Japanese medaka fish complement Bf/C2 gene. Immunogenetics. 1996;44(6):459–467. doi: 10.1007/BF02602808. [DOI] [PubMed] [Google Scholar]
- Mach B., Steimle V., Martinez-Soria E., Reith W. Regulation of MHC class II genes: lessons from a disease. Annu Rev Immunol. 1996;14:301–331. doi: 10.1146/annurev.immunol.14.1.301. [DOI] [PubMed] [Google Scholar]
- Morizot D. C., Slaugenhaupt S. A., Kallman K. D., Chakravarti A. Genetic linkage map of fishes of the genus Xiphophorus (Teleostei: Poeciliidae). Genetics. 1991 Feb;127(2):399–410. doi: 10.1093/genetics/127.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morizot D. C. Use of fish gene maps to predict ancestral vertebrate genome organization. Prog Clin Biol Res. 1990;344:207–234. [PubMed] [Google Scholar]
- Nairn R. S., Kazianis S., McEntire B. B., Della Coletta L., Walter R. B., Morizot D. C. A CDKN2-like polymorphism in Xiphophorus LG V is associated with UV-B-induced melanoma formation in platyfish-swordtail hybrids. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13042–13047. doi: 10.1073/pnas.93.23.13042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ono H., Klein D., Vincek V., Figueroa F., O'hUigin C., Tichy H., Klein J. Major histocompatibility complex class II genes of zebrafish. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11886–11890. doi: 10.1073/pnas.89.24.11886. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ono H., O'hUigin C., Vincek V., Klein J. Exon-intron organization of fish major histocompatibility complex class II B genes. Immunogenetics. 1993;38(3):223–234. doi: 10.1007/BF00211522. [DOI] [PubMed] [Google Scholar]
- Prestridge D. S. SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci. 1991 Apr;7(2):203–206. doi: 10.1093/bioinformatics/7.2.203. [DOI] [PubMed] [Google Scholar]
- Sato A., Figueroa F., O'hUigin C., Reznick D. N., Klein J. Identification of major histocompatibility complex genes in the guppy, Poecilia reticulata. Immunogenetics. 1996;43(1-2):38–49. doi: 10.1007/BF00186602. [DOI] [PubMed] [Google Scholar]
- Sato K., Flajnik M. F., Du Pasquier L., Katagiri M., Kasahara M. Evolution of the MHC: isolation of class II beta-chain cDNA clones from the amphibian Xenopus laevis. J Immunol. 1993 Apr 1;150(7):2831–2843. [PubMed] [Google Scholar]
- Senapathy P., Shapiro M. B., Harris N. L. Splice junctions, branch point sites, and exons: sequence statistics, identification, and applications to genome project. Methods Enzymol. 1990;183:252–278. doi: 10.1016/0076-6879(90)83018-5. [DOI] [PubMed] [Google Scholar]
- Singal D. P., Qiu X. Polymorphism in both X and Y box motifs controls level of expression of HLA-DRB1 genes. Immunogenetics. 1996;43(1-2):50–56. doi: 10.1007/BF00186603. [DOI] [PubMed] [Google Scholar]
- Sültmann H., Mayer W. E., Figueroa F., O'HUigin C., Klein J. Organization of Mhc class II B genes in the zebrafish (Brachydanio rerio). Genomics. 1994 Sep 1;23(1):1–14. doi: 10.1006/geno.1994.1452. [DOI] [PubMed] [Google Scholar]
- Tajima F., Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984 Apr;1(3):269–285. doi: 10.1093/oxfordjournals.molbev.a040317. [DOI] [PubMed] [Google Scholar]
- Tieber V. L., Abruzzini L. F., Didier D. K., Schwartz B. D., Rotwein P. Complete characterization and sequence of an HLA class II DR beta chain cDNA from the DR5 haplotype. J Biol Chem. 1986 Feb 25;261(6):2738–2742. [PubMed] [Google Scholar]
- Walker R. B., McConnell T. J., Walker R. A. Variability in an MHCMosa class II beta chain-encoding gene in striped bass (Morone saxatilis). Dev Comp Immunol. 1994 Jul-Aug;18(4):325–342. doi: 10.1016/s0145-305x(94)90358-1. [DOI] [PubMed] [Google Scholar]
- Walter R. B., Rolig R. L., Kozak K. A., McEntire B., Morizot D. C., Nairn R. S. Cloning and gene map assignment of the Xiphophorus DNA ligase 1 gene. Mol Biol Evol. 1993 Nov;10(6):1227–1238. doi: 10.1093/oxfordjournals.molbev.a040066. [DOI] [PubMed] [Google Scholar]
- Wittbrodt J., Adam D., Malitschek B., Mäueler W., Raulf F., Telling A., Robertson S. M., Schartl M. Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature. 1989 Oct 5;341(6241):415–421. doi: 10.1038/341415a0. [DOI] [PubMed] [Google Scholar]
- Xu Y. X., Pitcovski J., Peterson L., Auffray C., Bourlet Y., Gerndt B. M., Nordskog A. W., Lamont S. J., Warner C. M. Isolation and characterization of three class II MHC genomic clones from the chicken. J Immunol. 1989 Mar 15;142(6):2122–2132. [PubMed] [Google Scholar]
- van Erp S. H., Egberts E., Stet R. J. Characterization of class II A and B genes in a gynogenetic carp clone. Immunogenetics. 1996;44(3):192–202. doi: 10.1007/BF02602585. [DOI] [PubMed] [Google Scholar]