Abstract
A gene coding for a putative GTP-binding protein, MMR1, has been localized on band C of the murine Chr 17 within or close to the MHC (Denizot et al. 1992). Its human homolog, HSR1, localized to the human MHC class I region, is described in this paper. Its sequence, compared with MMR1, shows that the conceptual proteins encoded by these genes are highly homologous and have thus been subjected to high constraints during evolution. Furthermore, a detailed databank search with HSR1 leads to the characterization of a new subfamily of GTP-binding proteins, of which HSR1 and MMR1 are the only eukaryotic members. The precise localization of HSR1 within the human MHC class I region is also presented.
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Abderrahim, H., Sambucy, J.L., Iris, F. Ougen, P., Billault, A., Chumakov, I.M., Dausset, J., Cohen, D., Le Paslier, D. (1993). Cloning the human major histocompatibility complex in YACs. Genomics in press.
Ahnn, J., March, P.E., Takiff, H.E., Inouye M. (1986) A GTP-binding protein of Escherichia coli has homology to yeast RAS proteins. Proc. Natl. Acad. Sci. USA 83, 8849–8853.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403–410.
Bahram, S., Arnold, D., Bresnahan, M., Strominger, J.L., Spies, T. (1991). Two putative subunits of a peptide pump encoded in the human major histocompatibility complex class II region. Proc. Natl. Acad. USA 88, 10094–10098.
Bird, A.P. (1986). CpG-rich islands and the function of DNA methylation. Nature 321, 209–213.
Boucraut, J., Guillaudeux, T., Alizadeh, M., Boretto, J., Chimini, G., Malecaze, F., Semana, G., Fauchet, R., Pontarotti, P., Le Bouteiller, P. (1993). HLA-E is the only class I gene that escapes CpG methylation and is transcriptionally active in the trophoblast-derived human cell line JAR. Immunogenetics 38, 117–130.
Bourne, H.R., Sandres, D.A., McCormick, F. (1991). The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117–127.
Campbell, R.D., Trowsdale, J. (1993). Map of the human MHC. Immunol. Today 14, 349–352.
Chimini, G., Boretto, J., Marguet D., Lanau, F., Lauquin G., Pontarotti P. (1990). Molecular analysis of the human MHC class I region using yeast artificial chromosome clones. Immunogenetics 32, 419–426.
Crouau-Roy, B., Amadou, C., Bouissou, C., Clayton, J., Vernet, C., Ribouchon, M.-T. Pontarotti, P. (1993). Localization of the OTF3 gene within the human MHC class I gene region by physical and meiotic mapping. Submitted.
Denizot, F., Mattéi, M.-G., Vernet, C., Pontarotti, P., Chimini, G. (1992). YAC-assisted cloning of a putative G-protein mapping to the MHC class I region. Genomics 14, 857–862.
Doolittle, R.F., (1990). Counting and discounting the universe of exons. Science 253, 677–679.
Dorit, R.L., Schoenbach, L., Gilbert, W. (1990). How, big is the universe of exons? Science 250, 1377–1382.
Eisenberg, D., Weiss, R.M., Terwilliger, T.C. (1984). The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. Natl. Acad. Sci. USA 81, 140–144.
El Kahloun, A., Vernet, C., Jouanolle, A.M., Boretto, J., Mauvieux V., Le Gall, J-Y., David, V., Pontarotti, P. (1992). A continuous restriction map from HLA-A haplotypes. Immunogenetics 35, 183–189.
Feinberg, A.P., Vogelstein, B. (1983). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13.
Fitzgerald, M., Shenk, T. (1981). The sequence 5′-AAUAAA-3′ forms port of the recognition site for polyadenylation of the late SV40 mRNAs. Cell 24, 251–260.
Garnier, J., Osguthorpe, D.J., Robson, B. (1978) Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol. Biol. 120, 97–120.
Geraghty, D.E., Koller, B.H., Hansen, J.A., Orr, H.T. (1992a). The HLA class I gene family includes at least six genes and twelve pseudogenes and genes fragments. J. Immunol. 149, 1934–1946.
Geraghty, D.E., Koller, B.H., Pei, J., Hansen, J.A. (1992b). Examination of four HLA class I pseudogenes. J. Immunol. 149, 1947–1956.
Geraghty, D.E., Pei, J., Lipsky, B., Hansen, J.A., Taillon-Miller, P., Bronson, S.K., Chaplin, D.D. (1992c). Cloning and physical mapping of the HLA class I region, spanning the HLA-E-to-HLA-F interval by using yeast artificial chromosomes. Proc. Natl. Acad. Sci. USA 89, 2669–2673.
Glynne, R., Powis, S.H., Beck, S., Kelly, A., Kerr, L. A., Trowsdale, J. (1991) A proteasome-related gene between the two ABC transporter loci in the class II region of the human MHC. Nature 353, 357–360.
Guillaudeux, T., Mattéi, M.-G., De Petris, D., Le Bouteiller, P., Pontarotti P. (1993). In situ hybridization localizes the human OTF-3 and OTF-3L genes to human chromosomes 6p21.3 and 12p13. Cytogenet. Cell Genet. 63, 212–214.
Hughes, A.L., Nei, M. (1988). Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170.
Kelly, A., Powis, S.H., Glynne, R., Radley, E., Beck, S., Trowsdale, J. (1991). Second proteasome-related gene in the human MHC class II region. Nature 353, 667–668.
Kirisits, M.J., Kunz, H.W., Hassett, A.L., Gill, T.J. III (1992). Genomic DNA sequence and organization of the TL-like gene in the grc-G/C region of the rat. Immunogenetics 35, 365–377.
Koller, B., Geraghty, D.E., DeMars, R., Orr., H.T. (1988) HLA-E. A novel HLA class I gene expressed in resting T-lymphocytes. J. Immunol. 141, 897–904.
Kozak, M., (1991). An analysis of vertebrate mRNA sequences: intimations of translational control. J. Cell Biol. 115, 887–903.
Kyte, J., Doolittle, R.F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105–132.
Lawlor, D.A., Ward, F.E., Ennis, P.D., Jackson, P.A., Parham, P. (1988). HLA-A and-B polymorphisms predate the divergence of humans and chimpanzees. Nature 335, 268–271.
Lindsay, S., Bird, A. (1987). Use of restriction enzymes to detect potential gene sequences in mammalian DNA. Nature 327, 336–338.
Mayer, W.E., Lonker, M., Klein, D., Ivanyi, P., Van Seventer, G., Klein, J. (1988). Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO J. 7, 2765–2774.
Mizuno, S., Trapani., J.A., Koller, B.H., Dupont, B., Yang, S.Y. (1988). Isolation and nucleotide sequence of a cDNA clone encoding a novel class I gene. J. Immunol. 140, 4024–4030.
Nagata, S., Tsunetsugu-Yokota, Y., Naito, A., Kaziro Y. (1983). Molecular cloning and sequence determination of the nuclear gene coding for mitochondrial elongation factor Tu of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 80, 6192–6196.
Ogasawara, N., Yoshikawa, H. (1992). Genes and their organization in the replication origin region of the bacterial chromosome. Mol. Microbiol 6, 629–634.
Pardo, L., Ballesteros, J.A., Osman, R., Weinstein, H. (1992). On the use of the transmembrane domain of bacteriorhodopsin as a template for modeling the three-dimensional structure of guanine nucleotide-binding regulatory protein-coupled receptors. Proc. Natl. Acad. Sci. USA 89, 4009–4012.
Pearson, W.R., Lipman D.J. (1988). Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85, 2444–2448.
Pontarotti, P., Chimini, G., NGuyen C., Boretto, J., Jordan, B.R. (1989). Organization of the HLA class I region. In Immunobiology, of HLA, Vol. II, B. Dupont, ed. (New York: Springer Verlag), pp. 79–82.
Sanger, F., Nicklen, S., Coulson, A.R. (1977). DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–5467.
Shimmin, L.C., Dennis, P.P. (1989). Characterization of the L11, 11, L10 and L12 equivalent ribosomal protein gene cluster of the halophilic archaebacterium Halobacterium cutirubrum. EMBO J. 8, 1225–1235.
Spies, T., Bresnahan, M., Strominger, J.L. (1989). Human major histocompatibility complex contains a minimum of 19 genes between the complement cluster and HLA-B. Proc. Natl. Acad. Sci. USA 86, 8955–8958.
Spies, T., Bresnahan, M., Bahram, S., Arnold, D., Blank, G., Mellins, E., Pious, D., DeMars, R. (1990). A gene in the human major histocompatibility complex class II region controlling the class I antigen presentation pathway. Nature 348, 744–747.
Trach, K., Hoch, J.A. (1989). The Bacillus subtilis spoOB stage O sporulation operon encodes an essential GTP-binding protein. J. Bacteriol. 171, 1362–1371.
Trowsdale, J., Hanson, I., Mockridge, J., Beck, S., Townsend, A., Kelly, A. (1990). Sequences encoded in the class II region of the MHC related to the “ABC” superfamily of transporters. Nature 348, 741–744.
Uehara, H. (1991). Mouse Oct-3 maps between the tcl12 embryonic lethal gene and the Qa gene in the H-2 complex. Immunogenetics 34, 266–269.
Vernet, C., Ribouchon, M.-T., Chimini, G., Jouanolle, A.-M., Sidibé, I., Pontarotti, P. (1993). A novel coding sequence belonging to a new multicopy gene family mapping within the MHC class I region. Immunogenetics 38, 47–53.
Vernet, C., Boretto, J., Mattéi, M.-G., Takahashi, M., Jack, L.J.W., Mather, I.H., Rouquier, S., Pontarotti, P. (1993). Evolutionary study of multigenic families mapping close to the human MHC class I region. J. Mol. Evol., in press.
Volz, A., Weiss, E., Trowsdale, J., Uchanska-Ziegler, B., Ziegler, A. (1993). The gene for the β-chain of tubulin (TUBB) maps to the HLA class I region. Cytogenet. Cell Genet. 62, 80.
Von Heijne, G. (1986). A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14, 4683–4690.
Wang, C.-R., Loveland, B.E., Fischer Lindahl, K. (1991). H-2M3 encodes the MHC class I molecule presenting the maternally transmitted antigen of the mouse. Cell 66, 335–345.
Watkins, D.I., Chen, Z.W., Hughes, A.L., Evans, M.G., Tedder, T.F., Letvin, N.L. (1990). Evolution of the MHC class I genes of a New World primate from ancestral homologues of human non-classical genes. Nature 346, 60–63.
Wei, X.H., Orr, H.T., (1990). Differential expression of HLA-E, HLA-F and HLA-G transcripts in human tissue. Hum. Immunol. 29, 131–142.
Yeom, Y.I., Ha, H.S., Balling, R., Scholer, H.R., Artzt, K. (1991). Structure, experession and chromosomal location of the Oct-4 gene. Mech. Dev. 35, 171–179.
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Vernet, C., Ribouchon, M.T., Chimini, G. et al. Structure and evolution of a member of a new subfamily of GTP-binding proteins mapping to the human MHC class I region. Mammalian Genome 5, 100–105 (1994). https://doi.org/10.1007/BF00292335
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DOI: https://doi.org/10.1007/BF00292335