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The Chicken .82-Microglobulin Gene Is Located on a Non-Major

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The Chicken .82-Microglobulin Gene Is Located on a Non-Major Proc. Natl. Acad. Sci. USA Vol. 93, pp. 1243-1248, February 1996 Genetics The chicken .82-microglobulin gene is located on a non-major histocompatibility complex microchromosome: A small, G+C-rich gene with X and Y boxes in the promoter PATRICIA RIEGERT*, ROLF ANDERSENtt, NAT BUMSTEAD§, CHRISTIAN D6HRING*, MARINA DOMINGUEZ-STEGLICH$, JAN ENGBERGt, JAN SALOMONSENII, MICHAEL SCHMID1, JOSEPH SCHWAGER**, KARSTEN SKJ0DTtt, AND JIM KAUFMAN*#t *Basel Institute for Immunology, Basel, Switzerland; tBiochemical Institute B, Panum, University of Copenhagen, Copenhagen, Denmark; §Institute for Animal Health, Compton Laboratories, Compton, United Kingdom; lInstitute for Human Genetics, University of Wiirzburg, Wurzburg, Germany; lllnstitute of Life Sciences and Chemistry, University of Roskilde, Roskilde, Denmark; **Centre de Recherche sur la Nutrition Animale, Societe Roche S. A. Village-Neuf, France; and ttInstitute of Medical Microbiology, University of Odense, Odense, Denmark Communicated by D. Bernard Amos, Duke University Medical Center, Durham, NC, October 26, 1995 ABSTRACT f32-Microglobulin is an essential subunit of birds, that some chromosomes were affected to the point of major histocompatibility complex (Mhc) class I molecules, becoming microchromosomes, and that this process effectively which present antigenic peptides to T lymphocytes. We se- ended in the genomes of the few survivors that actually gave quenced a number of cDNAs and two genomic clones corre- rise to the birds (12-14). sponding to chicken .j2-microglobulin. The chicken 132- Mhc class I molecules are composed of an Mhc-encoded microglobulin gene has a similar genomic organization but polymorphic class I a chain noncovalently associated with a smaller introns and higher G+C content than mammalian small nonpolymorphic protein called P32-microglobulin (322m). f82-microglobulin genes. The promotor region is particularly In mammals, the f32m gene is a relatively large gene with G+C-rich and contains, in addition to interferon regulatory moderate G+C content and is encoded on a non-Mhc chro- elements, potential S/W, X, and Y boxes that were originally mosome (15-18). We have reported the isolation of a chicken described for mammalian class II but not class I a or f32m cDNA clone; as in chicken Mhc genes, the sequence was f82-microglobulin genes. There is a single chicken 132- highly G+C-rich (11). Here we examine the chicken f32m gene microglobulin gene that has little polymorphism in the coding in order to determine which features are similar to and region. Restriction fragment length polymorphisms from Mhc different from mammalian 12m genes, in particular to deter- homozygous lIjpes, Mhc congenic lines, and backcross families, mine whether the high G+C content found in f32m cDNA as well as in situ hybridization, show that the P2-microglobulin gene is located on a microchromosome different from the one correlates with short introns and microchromosomal loca- that contains the chicken Mhc. We propose that the structural tion.§§ similarities between the j32-microglobulin and Mhc genes in the chicken are due to their presence on microchromosomes MATERIALS AND METHODS and suggest that these features and the microchromosomes appeared by deletion of DNA in the lineage leading to the cDNA and Genomic Clones. A partial cDNA clone for birds. chicken f32m (pRA5 from H.B19 spleen; ref. 11) was used to isolate longer cDNA clones (JBlb, JB6a, and JB15b from The avian genome is small and G+C-rich relative to typical H.B19 intestine AZAP library and p34a from CB bursa AZAP- mammalian and amphibian genomes. In addition, most birds II library; chickens from the Basel Institute farm, Gipf- have very similar karyotypes compared with mammals and Oberfrick, Switzerland) and genomic clones [RG5 and RG6 amphibians, with a few chromosomes near mammalian size from H.B15 library using blood cell DNA partially digested (so-called macrochromosomes) and around 30 smaller micro- with Sau3A, size fractionated by sucrose-density gradient chromosomes. By cytological staining, many birds have similar centrifugation, and ligated in BamHI-digested EMBL3 vector banding patterns on the macrochromosomes, indicating a by standard techniques (19); chickens from Copenhagen]. conserved pattern of G+C-rich and A+T-rich isochores, with Genomic Southern Blots. Genomic erythrocyte DNA was most microchromosomes staining G+C-rich. Variations in isolated as described (20) from chickens at the Basel Institute karyotype among birds have been ascribed to chromosomal farm and from H.B21 and H.B15 backcrossed onto CB chick- fusions during evolution, as though all birds derived from an ens at the Danish State Serum Institute (kind gift of Claus ancestor with many microchromosomes (1-6). Koch). Restriction enzyme digestion, agarose gel electro- The major histocompatibility complex (Mhc) of chickens (or phoresis, transfer in 0.4 M NaOH to nylon filters (Zeta-Probe, B complex) is a genetic region that is located on a microchro- Bio-Rad), hybridization, and detection using x-ray film were by mosome (number 16 in size) (7). Overall, the chicken Mhc standard methods; the pRA5 insert was twice isolated from appears to be smaller and simpler than the Mhc of mammals, low-melting-point agarose and labeled by random priming with the few polymorphic class I a and class 1 genes being (19). closely spaced, compact, and G+C-rich (8-12). We have suggested that the small introns, small intragenic Abbreviations: f32m, P32-microglobulin; RFLP, restriction fragment distances, and high G+C content of chicken Mhc genes are due length polymorphism; UT, untranslated region. to the fact that they are located on a microchromosome. We lPresent address: Carlsberg Laboratory, Gamle Carlsberg Vej 10, have further proposed that during evolution, some unknown Valby, Denmark DK-2500, Denmark. agent deleted DNA at random in the lineage that led to the *tTo whom reprint requests should be sent at present address: Institute for Animal Health, Compton Laboratories, Compton, United King- dom RG20 7NN. The publication costs of this article were defrayed in part by page charge §§The sequences reported in this paper have been deposited in the payment. This article must therefore be hereby marked "advertisement" in GenBank data base [accession nos. Z48922 (genomic clone RG5), accordance with 18 U.S.C. §1734 solely to indicate this fact. Z48931 (genomic clone RG6), and Z48921 (cDNA)]. 1243 Downloaded by guest on September 23, 2021 1244 Genetics: Riegert et al. Proc. Natl. Acad. Sci. USA 93 (1996) I I RG5 I E E I! 5 10 15 H S H H RG6 ..4..L r I - _jj 2 I I m..J. 10 15 H, Hind Ill; K, Kpn l; N, Nco l; Nt, Not l; S, Sac l; Sm, Sma I, distances In kB s NSm* N Sm N H S Nt I -.I-- 0 _ . -&_ . I * 1 2 3 5' I A II B III C lV 3, length (nt) 577 109 101 279 109 35 983 654 739 (845) (104) (-3900) (279)(616) (26) (1244) (583) (48) %G+C 71 77 77 64 74 63 53 44 61 (49) (63) (-41) (42) (41) (59) (39) (34) (33) CpG (pairs) 66 14 9 25 14 3 27 7 33 (27) (7) (>9) (3) (3) (1) (2) (3) (0) FIG. 1. Restriction enzyme maps of the genomic clones RG5 and RG6 and a subclone that represents the sequenced region. Sm* indicates a Sma I site present in RG5 but not RG6. Boxes in the genomic clones indicate hybridizing fragments; boxes in the subclone indicate exons. Indicated below for each region is length in nucleotides, % G+C nucleotides, and the number of CpG dinucleotides, with the values for the corresponding regions in human 132m [ref. 17 and analysis of sequences in GenBank/European Molecular Biology Laboratory (EMBL) data base] in parentheses. Subcloning and Sequencing. Restriction enzyme digestion sequence that matched the cDNA and protein sequences and Southern blot analysis of the genomic clones (Fig. 1) were reported for chicken f32m (11, 24). The exons are roughly the used to select subclones for further sequence analysis. RG5 same length as in mammalian genes (Fig. 1 and data not and RG6 Sac I fragments were subcloned in Bluescript plasmid shown), but only exon II has significant sequence identity (43% (Stratagene) and sequenced as double-stranded DNA by identity in 279 nt for human, 46-48% for different mouse dideoxy chain termination using modified T7 DNA poly- species, 36-38% for different fish species found in EMBL/ merase (Sequenase 2.0 kit, United States Biochemical), GenBank). Exon IV contains a single poly(A) site but is dATP[35S], and specific primers. The 5' Sac I subclones were otherwise not very similar in sequence to mammalian genes further subcloned as Sma I fragments, single-stranded DNA (best match is 55% identity in 124 nt with human exon IV). was produced by coinfection of XL-1 Blue with the helper All three introns of the chicken gene are much shorter than phage VCSM13 (Stratagene), and Taq polymerase, fluores- those in the mammalian /32m genes (Fig. 1 and other compar- cent dye terminators, a thermocycler, and a 373A DNA isons not shown). The chicken 132m introns contain the appro- sequencer (Applied Biosystems) were used for automatic priate signals for splicing (in phase 1 like most Mhc genes) but sequencing. The sequences were analyzed using the GCG are otherwise virtually unrelated in sequence to the mamma- software (Genetics Computer Group, Madison, WI) and the lian j32m introns (best match is 67% identity in 48 nt with Transcription Factor Database (21) on a VAX cluster, and human intron C). SeqEd (Applied Biosystems) on a Macintosh Quadra 900. The j32m Gene of Chickens Has a Much Higher G+C In Situ Hybridization of Chromosomes. The genomic clone Content than Mammals. In contrast to mammalian 12m RG5 was biotin-labeled by nick-translation through incorpo- sequences, the cDNA of chicken /32m contains many more G ration of biotin-11 dUTP and separated from the unincorpo- and C residues, with the 5'UT consisting of GGAGC repeats rated nucleotides using Sephadex G-50 spin columns in the and the wobble bases of the protein coding region being 97% presence of 0.1% SDS.
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