May 2, 1995 - Isolation and characterization of cDNA clones for Japanese quail. (Coturn/x joponica) major histocompatibility complex. (MhcCoja) class I ...
Immunogenetics (1995) 42:213-216
© Springer-Verlag 1995
Takashi Shiina • Asako Ando • Tadashi Imanishi Hisako Kawata • Kei Hanzawa • Takashi Gojobori Hidetoshi Inoko • Seiki Watanabe
Isolation and characterization of cDNA clones for Japanese quail (Coturn/x joponica) major histocompatibility complex (MhcCoja) class I molecules
Received: 4 October 1994 / Revised: 2 May 1995 The chicken major histocompatibility complex [(MHC) (B complex)] includes not only the genes encoding the class I and class II antigens (B-F and B-L, respectively), but also the genes coding for the class IV (B-G) antigens, which have so far been described only in this species as well as, mouse and human (Danielle et al. 1993). Three chicken class I B-F cDNA clones from different haplotypes probably representing three different alleles in a single locus have been isolated and characterized: B-F 10 from the B 12 haplotype, B-F 19 from B 19, and B-FL 1-1 from B b~ (blank; Guillemot et al. 1988; Kaufman et al. 1992; Pharr et al. 1994). The relationship between these cDNAs and six B-F genes so far isolated by gene cloning from the chicken MHC region remains unclear (Guillemot et al. 1988)_ Domestic chicken has been until now the only bird species whose MHC had been studied in detail by molecular cloning techniques, although the class II gene has been recently cloned from the ringnecked pheasant (Wittzell et al. 1994)_ The Japanese quail (Coturnixjaponica) is a bird allied to partridge, inhabiting all of the islands of Japan. The resistant trait to Newcastle disease virus in this species is believed to be conferred by certain alleles of the quail MHC gene(s) (Takahashi et al. 1989). In order to elucidate the molecular structure of the Japanese quail MhcCoja which is The nucleotide sequence d~a reported in this paper have been submitted to the DDBJ, EMBL, and GenBank nucleotide sequence databases and have been assigned the accession numbers D29813 and D29814 T. Shiina • K. Hanzawa - S. Watanabe Laboratory of Animal Physiology, Department of Zootechnical Science, Tokyo University of Agriculture, Sakuragaoka, Setagayaku, Tokyo 156, Japan A. Ando - H_ Kawata • H. Inoko (~) Department of Genetic Information, Division of Molecular Life Science, Tokai University School of Medicine, Bohseidai, Isehara, Kanagawa 259-11, Japan T. Imanishi • T. Gojobori DNA Research Center, National Institute of Genetics, Mishima, Shizuoka 411, Japan
predicted to be evolutionally related to the chicken MHC genes and to investigate how MHC class I genes have evolved in non-mammals, we cloned and sequenced two quail MHC class I cDNAs and compared them with cDNAs from other species including chicken. Japanese quail liver mRNA was prepared from a 3week-old male of the High-IgG line_ A cDNA library was constructed from 5 gg mRNA in the XZAPII vector according to the manufacturer's protocol (UniZAPTMXPUGigapack Gold cloning kit; Stratagene La Jolla, CA). Plaque-forming units (1 x 106) from this library were screened with the chicken MHC class I cDNA clone B-F 10 by plaque hybridization (Guillemot et al. 1988). Positive phage clones were individually purified and converted to plasmid DNAs (pBluescript vector) in vivo for nucleotide sequencing, following the protocol provided by the manufacturer (Stratagene). Nucleotide sequences were determined by the Taq cycle sequencing method using fluorescence-labeled dideoxy terminators with an ABI 373A automated sequencer (Applied Biosystems, Foster City, CA). Genomic DNA (500 ng) was amplified by the polymerase chain reaction (PCR) procedure with 2.5 units of Taq DNA polymerase (Takara Inc., Ohtsu, Siga, Japan). The reaction mixture (100 gl), containing dNTPs (200 gM), MgC12 (2.5 raM), and gelatin (0.01%) was subjected to 30 cycles of 1 min at 96 °C, 1 min at 55 °C, and 1 min at 72 °C by automated PCR thermal sequencer (Astec Co, Ltd., Simen, Fukuoka, Japan). Three different oligonucleotide primers were used for amplification: the QF41-specific sense primer (5'-ACGACAGCACCACAAGA-3'), the QF63-specific sense primer (5'-ACAACAGCACCGCGCGG-3'), and the common anti-sense primer (5'TGTCCTCCCCAGCTCT-3'). The QF41- and QF63-specific sense primers were designed based on the unique sequences in the ~xl domain region of the QF4! and QF63 loci, respectively, for specific amplification of each locus along with the common anti-sense primer corresponding to the 3' conserved end of the c~2 domain region. A quail liver cDNA library was screened by plaque hybridization with the chicken class I B-F cDNA probe B-F
214
T. Shiina et al.: MHC class I cDNA clones for Japanese quail
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10 (Guillemot et al. 1988). Through the screening o f 1 x 106 plaques, 23 c D N A clones were found to hybridize with the chicken class I c D N A probe under low-stringency conditions. A m o n g them, two clones (QF41 and QF63) gave positive signals even under high-stringency conditions and these were chosen for further analyses. The nucleotide sequences of both strands of QF41 and QF63 were determined by the Taq cycle sequencing method after subcloning into the pBluescript vector. As expected, the sequences were found to be quite similar to that o f the chicken class I B-F o~ chain (B-F 10)_ The c D N A insert of QF41 consists of 1253 base pairs (bp) and begins within the 5' untranslated (UT) region, thus representing almost the full-length transcript. The c D N A insert of QF63 is 1200 bp in length and lacks the 5 ' U T region. QF41 has a 6 bp
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Fig. 1 Amino acid sequence comparison of the Japanese quail cDNA clones (QF41 and QF63), and representative MHC class I o~chains of other species• Numbering of residues is based on the QF41 sequence• Dashes indicate identity to the top sequence; '-' indicates gap introduced to maximize sequence similarity; P represents the putative phosphorylated site. The potencial N-linked glycosylation site is indicated by CHO. -S-S- indicates the disulfide bond. Sequence references are as follows: chicken B-F 10 (Guillemot et al. 1988); chicken B-F 19 (Kaufman et al. 1992); chicken B-FLI-I (Pharr et al. 1994); human HLA-A2 (Koller et al. 1985); lizard LC1 (Grossberger and Parham 1992); Xenopus CL13 (Flajnik et al. 1991); salmon p30 (Grimholt et al. 1993)
215
T. Shiina et al.: MHC class I eDNA clones for Japanese quail
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Fig. 2 Phylogenetic tree showing relationships of the Japanese quail class I genes to representative MHC class I genes of other species. The dendrogram was constructed by the neighbor-joining method of Saitou and Nei (1987) using the nucleotide sequences of the extracellular (cd, ~2, and a3) domains of MHC class I molecules. A value in a circle indicates bootstrap value
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insertion (CCTGGA) at nucleotide positions from 250 to 255 in the c~l domain a s compared with QF63 and chicken B-F 10, which has never been observed in any other MHC class I molecules. QF41 and QF63 contain an additional 33 bp segment in the cytoplasmic domain, which is absent in the chicken class I cDNA clone, B-F 10 from the B 12 haplotype, although other chicken class I cDNAs from the B 19 and Bb! haplotypes (B-F 19 and B-FL I-1, respectively) have the cytoplasmic domain with the same size as the quail class I cDNAs (Guillemot et al. 1988; Kaufman et al_ 1992; Pharr et al. 1994). This probably reflects the use of exon 7 encoding a part of the cytoplasmic domain in the Japanese quail MHC class I system (Kroemer et al. 1990). The chicken cG domain regions of B-F 10 and B-F 19 have a remarkably high G+C content, 96% and 97%, respectively, in the third codon position (Kaufman et al. 1992). Similarly, QF41 and QF63 also have a high G+C content, 90% and 88%, respectively, in the third codon position as compared with the mammalian class I genes with 75% ~ 80% G+C content (Aota and Ikemura 1986). A polypeptide of 355 amino acids was predicted from the nucleotide sequence of QF41 (Fig. 1). QF41 is characterized by a two amino acid addition (Pro-53, Gly-54) due to a 6 bp insertion at amino acid position 53 and 54 within the ~1 domain, as described above. The Japanese quail class I amino acid sequences have a deletion of two amino acids (Asp-Ser at positions 40 and in human) in the middle of the c~l domain as observed in chicken, lizard, Xenopus, and salmon (Fig. 1). QF41 and QF63 share only 79% amino acid identity, diverging from each other to a significant extent throughout the entire domains including the ~3 (93%) and TM+CY (73%) regions, which are generally well conserved in MHC class I molecules with the same isotype, implying the presence of at least two distinct class I loci in the Japanese quail. Amino acid sequence comparison with representative MHC class I proteins from other species revealed a conspicuous structural similarity between the mammalian and non-mammalian counterparts (Fig. 1). The most similar class I ~ chain among them is chicken B-F (74%~78%), followed by lizard LC 1 (42%~43%), and human HLA-A2
0.4 0.2_
(38%~41%), with the most divergence in the transmembrane and cytoplasmic regions. The salmon MHC class I chain showed the lowest amino acid sequence identity to QF41 and QF63 (28%~30%). Domain-by-domain sequence comparison between the Japanese quail and other MHC class I proteins revealed that the region most conserved across species is the c~3 domain. A phylogenetic tree was constructed using the nucleotide sequences of the three extracellular ctl, ~2, and cG domains of the class I ~ chains of the Japanese quail and other representative MHC class I genes (Fig. 2), Sequences were aligned by the MegAlign software in the ODEN system (Ina 1991) and a phylogenetic tree was built by the neighbor-joining method (Saitou and Nei 1987). The QF41 and QF63 sequences from the Japanese quail are more closely related to each other than to any other MHC class I sequences of other vertebrates including chicken, mammal, amphibian, and fish, suggesting that duplication of the two quail class I loci took place after this species diverged from chickens. In order to confirm the presence of two distinct class I loci in the Japanese quail, PCR amplification of the genomic DNA from the c~l to ~2 domain regions was performed using the QF41- or QF63-specific upstream primer along with the common downstream primer as described above. The PCR-amplified products with the different band sizes were observed, about 400 bp for QF41 and 600 bp for QF63 in all Japanese quail lines so far examined, including the High- and Low-IgG lines (Fig. 3). Nucleotide sequence determination of the PCRamplified products confirmed that they were indeed really amplified from the QF41 and QF63 loci and also indicated that the 18 bp intron is present between the putative a l and cc2 domain exons in the QF63 loci, but absent in the QF41 loci (data not shown). This result revealed the different exon-intron organization of the gene structure between the QF41 and QF63 loci.
216 Serological typing has not been extensively performed in the Japanese quail M H C system; MhcCoja and only three serologically defined haplotypes (Lyl, Ly2, Ly3) have been proposed (Katoh and Wakasugi, 1981: Cheng and Kimura 1990). The relationship of these serologically defined MhcCoja antigens to the genetic loci identified in this paper remains to be determined. Although the M H C systems of some species such as human, mouse, carp, snake, lizard, and so on express multiple distinct class I genes, most other species including chicken and frog (Xenopus) are believed to have only one functional class I molecule, suggesting that multiple loci may not be necessary for a functioning adoptive immune response. In this study, we isolated two distinct class I c D N A clones, QF41 and QF63, from the Japanese quail, evolutionally related to chicken. These two cDNAs reveal characteristic features of functional M H C class I antigen presentation molecules. The fact that QF41 and QF63 exhibit only 79% identity in terms of amino acids, diverging throughout the entire domains including the relatively well-conserved transmembrane and cytoplasmic domains (73% identity), indicates the presence of two transcribed MhcCoja class I loci. This was also supported by Southern hybridization analysis showing different band patterns with unique band intensity detected by the QF41 and QF63 c D N A probes (data not shown), and also by PCR analysis with the QF41 and QF63 specific primers showing the different exon-intron organization around the a l and c~2 domain regions. In fact, we found several allelic sequences in each of the QF41 and QF63 loci by characterizing their nucleotide sequences from many individuals (data not shown). Accordingly, we decided to designate two loci represented by QF41 and QF63 as Coja-A and Coja-B, respectively. The presence of these two loci in the Japanese quail M H C complex will have to be confirmed by isolation of genomic clones, which is now underway in our laboratory. In summary, two cDNAs clones (QF41 and QF63) corresponding to the M H C class I genes of the Japanese quail (Coturnixjaponica) were isolated by screening a liver c D N A library with the chicken class ! c D N A (B-F) as a probe. The overall amino acid sequence identity between the Japanese quail and chicken M H C class I c~ chain is from 74% to 78%, with the most divergence in the transmembrane (TM) and cytoplasmic region (CY). Between the QF41 and QF63 c D N A clones, there was only 79% amino acid identity with the highest homology (93%) in the functionally conserved c~3 domain. PCR analysis using genomic D N A as a template with the QF41- and QF63specific primers revealed the different and unique exonintron organization around the c~l and c~2 domain regions. Taken together, these results suggest that the Japanese quail has at least two distinct expressed M H C class I loci, designated Coja-A and Coja-B.
T. Shiina et al.: MHC class I cDNA clones for Japanese quail
Acknowledgments We thank Dr. John Trowsdale for critical reading of the manuscript.
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