Skip to main content

Advertisement

Log in

Evolutionary study of multigenic families mapping close to the human MHC class I region

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

During a search for novel coding sequences within the human MHC class I region (chromosome 6p21.3), we found an exon (named B30-2) coding for a 166-amino-acid peptide which is very similar to the C-terminal domain of several coding sequences: human 52-kD Sjögren's syndrome nuclear antigen A/Ro (SS-A/Ro) and ret finger protein (RFP), Xenopus nuclear factor 7 (XNF7), and bovine butyrophilin. The first three of these proteins share similarities over the whole length of the molecule whereas butyrophilin is similar in the C-terminal domain. The N-terminal domain of butyrophilin is similar to rat myelin/oligodendrocyte glycoprotein (MOG) and chicken B blood group system (B-G) protein. These domains are components of a new subfamily of the immunoglobulin superfamily (IgSF). Butyrophilin is thus a mosaic protein composed of the MOG/B-G Ig-like domain and the C-terminal domain of 52-kD SS-A/Ro, RFP, and XNF7 (1330-2-like domain). Moreover, in situ hybridization shows that RFP, butyrophilin, and MOG map to the human chromosome 6p2l.3-6p22 region and are thus close to the MHC class I genes. It is therefore possible that the butyrophilin gene is the product of an exon shuffling event which occurred between ancestors of the RFP and MOG genes. To our knowledge, this is the first example of the colocalization of a chimeric gene and its putative progenitors. Finally, regulatory protein T-lymphocyte 1 (Rpt-1) shares similarities with the N-terminal halves of RFP, 52-kD SS-A/Ro, and XNF7, but not with the B30-2-like domain. We show that the ancestral Rpt-l gene evolved by overprinting.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bahram S, Arnold D, Breshanan M, Strominger JL, Spies T (1991) Two putative subunits of a peptide pump encoded in the human major histocompatibility complex class II region. Proc Natl Acad Sci USA 88:10094–10098

    Google Scholar 

  • Bellini M, Lacroix J-C, Gall JG (1993) A putative zinc-binding protein on lampbrush chromosome loops. EMBO J 12:107–114

    Google Scholar 

  • Buze P, Peck E, Stubbs JD, Gendler S, Parry G (1991) MFG-E8: an apical phospholipid binding protein of mammary epithelia is associated with membrane secretion. J Cell Biol 115:196a

    Google Scholar 

  • Brodsky FM, Guagliardi LE (1991) The cell biology of antigen processing and presentation. Annu Rev Immunol 9:707–744

    Google Scholar 

  • Campbell RD, Caroll MC, Porter RR (1985) The molecular genetics of components of complement. Adv Immunol 38:203–244

    Google Scholar 

  • Carroll MC, Katzman P, Alicot EM, Koller BH, Geraghty DE, Orr HT, Strominger JL, Spies T (1987) Linkage map of the human major histocompatibility complex including the tumor necrosis factor genes. Proc Natl Acad Sci USA 84:8535–8539

    Google Scholar 

  • Chan EKL, Hamel JC, Buyon J-P, Tan EM (1991) Molecular definition of and sequence motifs of the 52-kD component of human SS-A/Ro autoantigen. J Clin Invest 87:68–76

    Google Scholar 

  • 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

    Google Scholar 

  • Dessen P, Fondrat C, Valencien C, Mugnier C (1990) Bisance: a French service for access to biomolecular sequence databases. Comput Appl Biosci 6:355–356

    CAS  PubMed  Google Scholar 

  • Dorit RL, Shoenbach L, Gilbert W (1990) How big is the universe of exons? Science 250:1377–1382

    Google Scholar 

  • Dorit RL, Gilbert W (1991) The limited universe of exons. Curr Opin Genet Dev 1:464–469

    Google Scholar 

  • Frank MB, Itoh K, Fusiyaku A, Pontarotti P, Mattei M-G, Neas BR (1993) The mapping of the human 52-kD Ro/SSA auto-antigen gene to human chromosome 11, and its polymorphisms. Am J Hum Genet 82:183–191

    Google Scholar 

  • Franke WW, Heid HW, Grund C, Winter S. Freudenstein C, Schmid E, Jarasch E-D, Keenam TW (1981) Antibodies to the major insoluble milk fat globule membrane-associated protein: specific location in apical regions of lactating epithelial cells. J Cell Biol 89:485

    Google Scholar 

  • Freemont PS, Hanson IM, Trowsdale J (1991) A novel cysteinerich sequence motif. Cell 64:483–484

    Google Scholar 

  • Gilbert WA (1985) Genes-in-pieces revisited. Science 228:823

    Google Scholar 

  • Gardinier MW, Amiguet P, Linington C, Matthieu J-M (1992) Myelin/oligodendrocyte glycoprotein is a unique member of the immunoglobulin superfamily. J Neurosci Res 33:177–187

    Google Scholar 

  • Glynne R, Powis SH, Beck S, Kelly A, Kerr LA, 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

    Google Scholar 

  • Grassé PP (1977) Evolution of living organisms. Academic Press, New York, p 297

    Google Scholar 

  • Heid HW, Winter S, Bruder G, Keenan TW, Jarasch E-D (1983) Butyrophilin, an apical plasma membrane-associated glycoprotein characteristic of lactating mammary glands of diverse species. Biochim Biophys Acta 728:228–238

    Google Scholar 

  • Hunkapiller T, Hood L (1989) Diversity of the immunoglobulin gene superfamily. Adv Immunol 44:1–63

    Google Scholar 

  • Isomura T, Koizumi-Tamiya K, Suzuki M, Yoshida S, Taniguchi M, Matsuyama M, Ishigaki T, Sakuma S, Takahashi M (1992) RFP is a DNA binding protein associated with the nuclear matrix. Nucleic Acids Res 20:5305–5310

    Google Scholar 

  • Itoh K, Itoh Y, Frank MB (1991) Protein heterogeneity in the human Ro/SSA ribonucleoproteins. The 52- and 60-kD Ro/SSA autoantigens are encoded by separate genes. Clin Invest 87:177–186

    Google Scholar 

  • Jack LJW, Mather IH (1990) Cloning and analysis of cDNA encoding bovine butyrophilin, an apical glycoprotein expressed in mammary tissue and secreted in association with the milk-fat globule membrane during lactation. J Biol Chem 265: 14481–14486

    Google Scholar 

  • Keese PK, Gibbs A (1992) Origins of genes: “big bang” or continuous creation? Proc Natl Acad Sci USA 89:9489–9493

    Google Scholar 

  • Kelly A, Powis SH, Glynne R, Radley E, Beck S, Trowsdale J (1991) Second proteasome-related gene in the human MHC class II region. Nature 353:667–668

    Google Scholar 

  • Kelly A, Powis SH, Kerr LA, Mockridge I, Elliot T, Bastin J, Uchanska-Ziegler B, Ziegler A, Trowsdale J, Townsend A (1992) Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature 355:641–644

    Google Scholar 

  • Kleijmeer MJ, Kelly A, Geuze H.J., Slot JW, Townsend A, Trowsdale J (1992) Location of MHC-encoded transporters in the endoplasmic reticulum and cis-Golgi. Nature 357:342–344

    Google Scholar 

  • Leung-Hagesteijn C, Spence M, Stern BD, Y Zhou Y, Su MW, Hedgecock EM, Culotti G (1992) UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71:289–299

    Google Scholar 

  • Mattei M-G, Philip N, Passage E, Moisan J-P, Mandel J, Mattei JF (1985) DNA probe localization at 18p113 band by in situ hybridization of a small supernumerary chromosome. Human Genetic 69:268–271

    Google Scholar 

  • Miller M, Reddy AB, Kloc M, Li XX, Dreyer C, Etkin LD (1991a) The nuclear-cytoplasmic distribution of the Xenopus nuclear factor, xnf7, coincides with its state of phosphorylation during early development. Development 113:569–575

    Google Scholar 

  • Miller MM, Goto R, Young S, Chirivella J, Hawke D, Miyada GC (1991b) Immunoglobulin variable-region-like domains of diverse sequences within the major histocompatibility complex of the chicken. Proc Natl Acad Sci USA 88:4377–4381

    CAS  PubMed  Google Scholar 

  • Nadeau JH, Davison MT, Dootlittle DP, Grant P, Hillyard AL, Kosowsky MR, Roderick TH (1992) Comparative map for mice and humans. Mammalian Genome 3:480–536

    Google Scholar 

  • Ohno S (1984) Birth of a unique enzyme from an alternative reading frame of the preexisted, internally repetitious coding sequence. Proc Natl Acad Sci USA 82:2421–2425

    Google Scholar 

  • Patarca R, Freeman GJ, Schwartz J, Singh RP, Kong QT, Murphy E, Anderson Y, Wei Sheng FY, Singh P, Johnson KA, Guarnagia SM, Durfee T, Blattner F, Cantor H (1988) rpt-1, an intracellular protein from helper/inducer T cells that regulates gene expression of interleukin 2 receptor and human immunodeficiency virus type 1. Proc Natl Acad Sci USA 85:2733–2737

    Google Scholar 

  • Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448

    CAS  PubMed  Google Scholar 

  • Reddy B, Kloc M, Etkin L (1991) The cloning and characterization of a maternally expressed novel zinc finger nuclear phosphoprotein (xnf7) in Xenopus laevis. Dev Biol 148:107–116

    Google Scholar 

  • Reddy BA, Etkin LD (1992) A unique bipartite cysteine-histidine motif defines a subfamily of potential zinc-finger proteins. Nucleic Acids Res 22:6330

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467

    CAS  PubMed  Google Scholar 

  • Spies T, Bresnahan M, Bahrain S, Arnold D, Blanck G, Mellins E, Pious D, De Mars R (1990) A gene in the human major histocompatibility complex class II region controlling the class I antigen pathway. Nature 348:744–747

    Google Scholar 

  • Stubbs JD, Lekutis C, Singer KL, Bui A, Yukuzi D, Srinivasan U, Parry G (1990) cDNA cloning of a mouse mammary epithelial cell surface protein reveals the existence of epidermal growth factor-like domains linked to factor VIII-like sequences. Proc Natl Acad Sci USA 87:8417–8421

    Google Scholar 

  • Takahashi M, Ritz J, Cooper MGM (1985) Activation of a novel human transforming gene, ret, by DNA rearrangement. Cell 42:581–588

    Google Scholar 

  • Takahashi M, Cooper GM (1987) ret transforming gene encodes a fusion protein homologous to tyrosine kinases. Mol Cell Biol 7:1378–1385

    Google Scholar 

  • Takahashi M, Inaguma Y, Hiai H, Hirose F (1988) Developmentally regulated expression of a human “finger”-containing gene encoded by the 5' half of the ret transforming gene. Mol Cell Biol 8:1853–1856

    Google Scholar 

  • Trowsdale J, Hanson I, Mockridge I, 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

    Google Scholar 

  • Trowsdale J, Campbell RD (1992) Complexity in the major histocompatibility complex. Europ J Immunogenet 19:45–55

    Google Scholar 

  • Vernet C, Ribouchon M-T, Chimini G, Jouanolle AM, Sidibe I, Pontarotti P (1993) A novel coding sequence belonging to a new multicopy gene family mapping within the human MHC class I region. Immunogenetics 38:47–53

    Google Scholar 

  • Ziegler A, Field LL, Sakaguchi AY (1991) Report of the committee on the genetic constitution of chromosome 6. Cytogenet Cell Genet 58:1–43

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Correspondence to: P. Pontarotti

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vernet, C., Boretto, J., Mattéi, MG. et al. Evolutionary study of multigenic families mapping close to the human MHC class I region. J Mol Evol 37, 600–612 (1993). https://doi.org/10.1007/BF00182746

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00182746

Key words

Navigation