Skip to main content
SpringerLink
Log in

ExpressedPeromyscus maniculatus (Pema) MHC class I genes: evolutionary implications and the identification of a gene encoding a Qa1-like antigen

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

To gain insight into the evolution of rodent major histocompatibility complex (MHC) class I genes and identify important (conserved) nonclassical class I (class Ib) gene products and residues in these proteins, sixPeromyscus maniculatus MHC (Pema) class I cDNA clones were isolated and sequenced. FivePema class I cDNAs appeared most similar to mouse and rat classical class I (class Ia) genes. One exhibited highest similarity to anH2 class Ib gene,H2-T23 (encoding the Qa1 antigen). Phylogenetic trees constructed withPema, RT1, andH2 class I sequences suggested that the lineages of some rodent class Ib genes (e.g.,T23 andT24) originated prior toMus andPeromyscus speciation [>50 million years (My) ago]. Sequences of four Qa1-like proteins from three species permitted the identification of ten Qa1-specific amino acids. On the basis of molecular modeling, three residues showed the potential to interact with T-cell receptors and three residues (all corresponding to polymorphic positions among H2 class Ia proteins) were predicted to influence antigen binding. The recognition of mouse Qa1 proteins by a subset of T-cells in influenced by a locus,Qdm, which encodes the H2-D leader peptide. One of thePema class I cDNA clones classified asH2-K, D/L-like (class Ia) is predicted to encode an identical peptide, implying that an antigen binding protein (Qa1) and the antigen to which it binds (the product ofQdm) has been conserved for over 50 My.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aldrich, C. J., DeCloux, A., Woods, A. S., Cotter, R. J., Soloski, M. J., and Forman, J. Identification of a Tap-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen.Cell 79: 649–658, 1994

    Article  PubMed  CAS  Google Scholar 

  • Aldrich, C. J., Waltrip, R., Hermel, E., Attaya, M., Fischer Lindahl, K., Monaco, J., and Forman, J. T cell recognition of Qa-1b antigens on cells lacking a functional Tap-2 transporter.J Immunol 149: 3082—3773—3777, 1992

    Google Scholar 

  • Aldrich, C., Rodgers, J., and Rich, R. Regulation of Qa-1 expression and determinant modification by an H-2D-linked gene,Qdm. Immunogenetics 28: 334–344, 1988

    Article  CAS  Google Scholar 

  • Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L., and Wiley, D. C. Structure of the human class I histocompatibility antigen, HLA-A2.Nature 329: 506–512, 1987a

    Article  PubMed  CAS  Google Scholar 

  • Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L., and Wiley, D. C. The foreign antigen binding site and T cell recognition regions of class I histocompability antigens.Nature 329: 512–518, 1987b

    Article  PubMed  CAS  Google Scholar 

  • Brorson, K. A., Hunt, S. W., Hunkapiller, T., Sun, Y. H., Cheroutre, H., Nickerson, D. A., and Hood, L. Comparison of exon 5 sequences from 35 class I genes of the BALB/c mouse.J Exp Med 170: 1837–1858, 1989

    Article  PubMed  CAS  Google Scholar 

  • Brownell, E. DNA/DNA hybridization studies of muriod rodents: symmetry and rates of molecular evolution.Evolution 37: 1034–1051, 1983

    Article  CAS  Google Scholar 

  • Connolly, D. J., Cotteril, L. A., Hederer, R. A., Thorpe, C. J., Travers, P. J., McVey, J. H., Dyson, J., and Robinson, P. J. A cDNA clone encoding the mouse Qa-Ia histocompatibility antigen and proposed structure of the putative peptide binding site.J Immunol 151: 6089–6098, 1993

    PubMed  CAS  Google Scholar 

  • Crew, M. D. and Filipowsky, M. E. Sequence of the tumor necrosis factor/cachectin (TNF) gene fromPeromyscus leucopus (family Cricetidae).Immunogenetics 35: 351–353, 1991

    Google Scholar 

  • Crew, M. D., Filipowsky, M. E., Zeller, E. C., Smith, G. S., and Walford, R. L. Major histocompatibility complex class I genes ofPeromyscus leucopus.Immunogenetics 32: 371–379, 1990

    Article  PubMed  CAS  Google Scholar 

  • Crew, M. D., Douglass, C. A., and Brorson, K. H-2T24 and PemaT24: orthologous expressed MHC class Ib genes from mouse andPeromyscus maniculatus.Immunogenetics 39: 412–417, 1994

    Article  PubMed  CAS  Google Scholar 

  • Duran, L. W. and Pease, L. R. Tracing the evolution of H-2 D region gene using sequences associated with a repetitive element.J Immunol 141: 295–301, 1988

    PubMed  CAS  Google Scholar 

  • Fremont, D. H., Matsumura, M., Stura, E. A., Peterson, P. A., and Wilson, I. A. Crystal structures of two viral peptides in complex with murine MHC class I H-2Kb.Science 257: 919–927, 1992

    Article  PubMed  CAS  Google Scholar 

  • Germain, R. N. and Margulies, D. H. The biochemistry and cell biology of antigen processing and presentation.Annu Rev Immunol 11: 403–450, 1993

    Article  PubMed  CAS  Google Scholar 

  • Genetics Computer Group, Inc. Program Manual for the Wisconsin Package Version 8. Genetics Computer Group, Inc. Madison, WI, USA, 1994

    Google Scholar 

  • Hughes, A. L. and Nei, M. Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals.Mol Biol Evol 6: 559–579, 1989

    PubMed  CAS  Google Scholar 

  • Hughes, A. L. Independent gene duplications, not concerted evolution, explain relationships among class I MHC genes of murine rodents.Immunogenetics 33: 367–373, 1991.

    Article  PubMed  CAS  Google Scholar 

  • Imani, F. and Soloski, M. Heat shock proteins can regulate expression of the T1a region-encoded class Ib molecule Qa-1.Proc Natl Acad Sci USA 88: 10475–10479, 1991

    Article  PubMed  CAS  Google Scholar 

  • Insight II User Guide, version 2.1.0: Biosym Technologies. San Diego, CA, 1992

  • Ito, K., Van Kaer, L., Bonneville, M., Hsu, S., Murphy, D. B., and Tonegawa, S. Recognition of the product of a novel MHC TL region gene (27b) by a mouse γδ T cell receptor.Cell 62: 549–561. 1990.

    Article  PubMed  CAS  Google Scholar 

  • Jiang H., Ware, R., Stall, A., Flaherty, L., Chess, L., and Pernis, B. Murine CD8+ T cells that specifically delete autologous CD4+ T cells expressing V beta 8 TCR: a role of the Qa-1 molecule.Immunity 2: 185–194, 1995

    Article  PubMed  CAS  Google Scholar 

  • Kirisitis, M. J., Kunz, H. W., Cortese Hassett, A. L., and Gill, T. J., III. Genomic DNA sequence and organization of aTl-like gene in thegrc-G/C region.Immunogenetics 35: 365–377, 1992

    Article  Google Scholar 

  • Kirisitis, M. J., Sawai, H., Kunz, H. W., and Gill, T. J., III. MultipleTL-like loci in thegrc-G/C region of the rat.Immunogenetics 39: 301–315, 1994

    Google Scholar 

  • Kumar, S., Tamura, K., and Nei, M.MEGA: Molecular Evolutionary Genetics Analysis, version 1.01. The Pennsylvania State University, University Park, PA, 1993

    Google Scholar 

  • Kurlander, R. J., Shawar, S. M., Brown, M. L., and Rich, R. R. Specialized role for a murine class I-b MHC molecule in prokaryotic host defense.Science 257: 678–679, 1992

    Article  PubMed  CAS  Google Scholar 

  • Lowen, L. C., Aldrich, C. J. and Forman, J. Analysis of T cell receptors specific for recognition of class IB antigens.J Immunol 151: 6155–6165, 1993

    PubMed  CAS  Google Scholar 

  • Matsumura, M., Fremont, D. H., Peterson, P. A., and Wilson, I. A. Emerging principles for the recognition of peptide antigens for MHC class I molecules.Science 257: 927–934, 1992

    Article  PubMed  CAS  Google Scholar 

  • Mauxion, F., Sobczak, J., and Kress, M. Characterization of five distinct cDNA clones encoding for class I RT1 antigens.Immunogenetics 29: 397–401, 1989

    Article  PubMed  CAS  Google Scholar 

  • Parker, K. E., Carter, C. A., and Fabre, J. W. A rat class I cDNA with anAlu-like sequence and mapping to two genes inRT1.C/E.Immunogenetics 31: 211–214, 1990

    Article  PubMed  CAS  Google Scholar 

  • Parker, K. E., Carter, C. A., Murphy, G., and Fabre, J. W. The ratRT.BM1 MHC class I cDNA shows a high level of sequence similarity to the mouseH-2T23 d gene.Immunogenetics 34: 211–213, 1991

    Article  PubMed  CAS  Google Scholar 

  • Pease, L. R., Horton, R. M., Pullen, J. K., and Cai, Z. Structure and diversity of class I antigen presenting molecules in the mouse.Crit Rev Immunol 11: 1–32, 1991

    PubMed  CAS  Google Scholar 

  • Pullen, J. K., Horton, R. M., Cai, Z., and Pease, L. R. Structural diversity of the classical H-2 genes:K, D, andL.J Immunol 148: 953–967, 1992

    PubMed  CAS  Google Scholar 

  • Rada, C., Lorenzi, R., Powis, S. J., van den Bogaerde, J., Parham, P., and Howard, J. C. Concerted evolution of class I genes in the major histocompatibility complex of murine rodents.Proc Natl Acad Sci USA 87: 2167–2171, 1990

    Article  PubMed  CAS  Google Scholar 

  • Radojcic, A., Stranick, K. S., Locker, J., Kunz, H. W., and Gill, T. J., III. Nucleotide sequence of a rat class I cDNA clone.Immunogenetics 29: 134–137, 1989

    Article  PubMed  CAS  Google Scholar 

  • Robinson, P. J., Bevec, D., Mellor, A. L., and Weiss, E. H. Sequence of the mouse Q4 class I gene and characterization of the gene product.Immunogenetics 27: 79–86, 1988

    Article  PubMed  CAS  Google Scholar 

  • Rogers, J. H. Mouse histocompatibility-related genes are not conserved in other mammals.EMBO J 4: 749–753, 1985

    PubMed  CAS  Google Scholar 

  • Saitou, N. and Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees.Mol Biol Evol 4: 406–425, 1987

    PubMed  CAS  Google Scholar 

  • Singer, D. S., Hare, J., Golding, H., Flaherty, L., and Rudikoff, S. Characterization of a new subfamily of class I genes in the H-2 complex of the mouse.Immunogenetics 28: 13–21, 1988

    Article  PubMed  CAS  Google Scholar 

  • Shawar, S. M., Vyas, J. M., Rodgers, J. R., and Rich, R. R. Antigen presentation by major histocompatibility complex class I-b molecules.Annu Rev Immunol 12: 839–880, 1994

    Article  PubMed  CAS  Google Scholar 

  • Shawar, S. M., Vyas, J. M., Rodgers, J. R., Cook, R. G., and Rich, R. R. Specialized functions of major histocompatibility complex class I molecules. II. Hmt binds N-formylated peptides of mitochondrial and prokaryotic origin.J Exp Med 174: 941–944, 1991

    Article  PubMed  CAS  Google Scholar 

  • Stroynowski, I. Molecules related to class I major histocompatibility complex antigens.Annu Rev Immunol 8: 501–530, 1990

    Article  PubMed  CAS  Google Scholar 

  • Transy, C., Nash, S. B., David-Watine, B., Cochet, M., Hunt, S. W., Hood, L. E., and Kourilsky, P. A low polymorphic mouseH-2 class I gene from theTla complex is expressed in a broad variety of cell types.J Exp Med 166: 341–361, 1987

    Article  PubMed  Google Scholar 

  • Trowsdale, J. “Both man & bird & beast”: comparative organization of MHC genes.Immunogenetics 41: 1–17, 1995

    Article  PubMed  CAS  Google Scholar 

  • Vidovic, D., Roglic, M., McKune, K., Guerder, S., Mackay, C., and Dembic, Z. Qa-1 restricted recognition of foreign antigen by a γδ T-cell hybridoma.Nature 340: 646–650, 1989

    Article  PubMed  CAS  Google Scholar 

  • Wang, C.-R., Loveland, B. E., and Fischer Lindahl, K.H-2M3 encodes the MHC class I molecule presenting the maternally transmitted antigen of the mouse.Cell 66: 335–345, 1991.

    Article  PubMed  CAS  Google Scholar 

  • Wang, C.-R., Castano, A. R., Peterson, P. A., Slaughter, C., Fischer Lindahl, K., and Deisenhofer, J.. Nonclassical binding of formylated peptide in crystal structure of the MHC class Ib molecule H-2M3.Cell 82: 655–663, 1995

    Article  PubMed  CAS  Google Scholar 

  • Watts, S., Davis, A. C., Gaut, B., Wheeler, C., Hill, L., and Goodenow, R. S. Organization and structure of the major histocompatibility complex of the C3H mouse: implications for Qa function and class I evolution.EMBO J 8: 1749–1759, 1989a

    PubMed  CAS  Google Scholar 

  • Watts, S., Wheeler, C., Morse, R., and Goodenow, R. S. Amino acid comparison of the class I antigens of mouse major histocompatibility complex.Immunogenetics 30: 392–390, 1989b

    Article  Google Scholar 

  • Wolf P. R. and Cook, R. G. TheTL region gene37 encodes a Qa-1 antigen.J Exp Med 172: 1795–1804, 1990

    Article  PubMed  CAS  Google Scholar 

  • Wolf, P. R. and Cook, R. G. The class I-b molecule Qa-1 forms heterodimers with H-2Ld and a novel 50-kd glycoprotein encoded centromeric toI-Eβ,J Exp Med 181: 657–668, 1995

    Article  PubMed  CAS  Google Scholar 

  • Zemmour, J. and Parham, P. HLA class I nucleotide sequences, 1991.Hum Immunol 31: 195–206, 1991

    Article  PubMed  CAS  Google Scholar 

  • Zheng, Y.-W., Bey, M., Liu, H., and Felder, M. R. Molecular basis of the alcohol dehygogenase-negative deer mouse.J Biol Chem 268: 24933–24939, 1993

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine, Division of Aging, University of Arkansas for Medical Sciences, 72205, Little Rock, AR, USA

    Mark D. Crew, Linda M. Bates & Carolyn A. Douglass

  2. Geriatric Research Education and Clinical Center (GRECC), John L. McClellan Veterans Administration Hospital, 151 Research, 72205, Little Rock, AR, USA

    Mark D. Crew

  3. Department of Biochemistry & Molecular Biology, University of Arkansas for Medical Sciences, 72205, Little Rock, AR, USA

    Mark D. Crew & J. Lyndal York

Authors
  1. Mark D. Crew
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Linda M. Bates
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolyn A. Douglass
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Lyndal York
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers U12822 (Pm13), U12885 (Pm41), U12886 (Pm52), U12887 (Pm62), U16846 (Pm11), and U16847 (Pm53)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crew, M.D., Bates, L.M., Douglass, C.A. et al. ExpressedPeromyscus maniculatus (Pema) MHC class I genes: evolutionary implications and the identification of a gene encoding a Qa1-like antigen. Immunogenetics 44, 177–185 (1996). https://doi.org/10.1007/BF02602583

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02602583

Keywords

Search

Navigation