Skip to main content
Log in

Major histocompatibility complex class II A gene polymorphism in the striped bass

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

Abstract

Adaptions of the polymerase chain reaction were used to isolate cDNA sequences encoding the Major histocompatibility complex(Mhc) class II A gene(s) of the striped bass (Morone saxatilis). Four complete Mhc class II A genes were cloned and sequenced from a specimen originating in the Roanoke River, North Carolina, and another three A genes from a specimen originating from the Santee-Cooper Reservoir, South Carolina, identifying a total of seven unique sequences. The sequence suggests the presence of at least two Mhc class II A loci. The extensive sequence variability observed between the seven different Mhc class II clones was concentrated in the α1 encoding domain. The encoded α2, transmembrane, and cytoplasmic regions of all seven striped genes correlated well with those of known vertebrate Mhc class II proteins. Overall, the striped bass sequences showed greatest similarity to the Mhc class II A genes of the zebrafish. Southern blot analysis demonstrated extensive polymorphism in the Mhc class II A genes in members of a Roanoke river-caught population of striped bass versus a lesser degree of polymorphism in an aquacultured Santee-Cooper population of striped bass.

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

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. Basic local alignment search tool. J Mol Biol 215: 403–410, 1990

    Article  CAS  PubMed  Google Scholar 

  • Bartl, S. and Weissman, I. L. Isolation and characterization of major histocompatibility complex class IIB genes from the nurse shark. Proc Natl Acad Sci USA 91: 262–266, 1994

    Google Scholar 

  • Bjorkman, P. J. and Parham, P. Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem 59: 253–288, 1990

    Google Scholar 

  • Borriello, F. and Krauter, K. S. Reactive site polymorphism in the murine protease inhibitor gene family is delineated using a modification of the PCR reaction (PCR+1). Nucleic Acids Res 18: 5481–5487, 1990

    CAS  PubMed  Google Scholar 

  • Bourlet, Y., Béhar, G., Guillemot, F., Chaussé, A. M., Zoorob, R., and Auffray, C. Isolation of chicken major histocompatibility complex class II (B-L) beta chain sequences: comparison with mammalian beta chains and expression in lumphoid organs. EMBO J 7: 1031–1039, 1988

    CAS  PubMed  Google Scholar 

  • Brown, J. H., Jardetzky, T., Saper, M. A., Samraoui, b., Bjorkman, P. J., and Wiley, D. C. A hypothetical model of the foreign antigen binding site of class II histocompatibility molecules. Nature 332: 845–850, 1988

    Google Scholar 

  • Brown, J. H., Jardezky, T. S., Gorga, J. C., Stern, L. J., Urban, R. G., Strominger, J. L., and Wiley, D. C. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364: 33–39, 1993

    Article  CAS  PubMed  Google Scholar 

  • Cosson, P. and Bonifacino, J. S. Role of transmembrane domain interactions in the assembly of class II MHC molecules. Science 258: 659–662, 1992

    Google Scholar 

  • Devereux, J., Haebeli, P., and Smithies, O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387–395, 1984

    CAS  PubMed  Google Scholar 

  • Flajnik, M. F., Canel, C., Kramer, J., and Kasahara, M. Evolution of the major histocompatibility complex: molecular doning of major histocompatibility complex class I from the amphibian Xenopus. Proc Natl Acad Sci USA 88: 537–541, 1991

    Google Scholar 

  • Frohman, M. A. Rapid amplification of cDNA ends (RACE): user friendly cDNA cloning. Amplifications 5: 11–15, 1990

    Google Scholar 

  • Gorsky, J. and Mach, B. Polymorphism of human Ia antigens: gene conversion between two DR β loci result in a new HLA-D/DR specificity. Nature 322: 67–70, 1986

    Google Scholar 

  • Guillemot, F., Billault, A., Pourquié, O., Béhar, G., Chaussé, A.-M., Zoorob, R., Kreibich, G., and Auffray, C. A molecular map of the chicken major histocompatibility complex: the class II β genes are closely linked to the class I genes and the nucleolar organizer. EMBO J 7: 2775–2785, 1988

    CAS  PubMed  Google Scholar 

  • Gyllensten, U. B., Sundvall, M., and Erlich, H. A. A generation of allelic polymorphism at the DRB1 locus of primates by exchange of polymorphic domains: a plausible hypothesis? In J. Klein and D. Klein (eds.): Molecular Evolution of the Major Histocompatibility Complex, pp. 103–109, Springer, Berlin Heidelberg, 1991

    Google Scholar 

  • Hashimoto, K., Nakanishi, T., and Kurosawa, Y. Isolation of carp genes encoding major histocompatibility complex antigens. Proc Natl Acad Sci USA 87: 6863–6867, 1990

    Google Scholar 

  • Hassler, T. J. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific south-west)-striped bass. U. S. Fish Wildlife Serv Biol Rep 82(11.82): 1–29, 1988

    Google Scholar 

  • Hordvik, I., Grimholt, U., Fosse, V. M., Lie, Ø.,and Endresen, C. Cloning and sequence analysis of cDNAs encoding the MHC class II β chain in Atlantic salmon (Salmo salar). Immunogenetics 37: 437–441, 1993

    Google Scholar 

  • Hughes, A. L. and Nei, M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170, 1988

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L. and Nei, M. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86: 958–962, 1989

    CAS  PubMed  Google Scholar 

  • jeffreys, A. J., Wilson, V., and Thein, S. L. Hypervariable “minisatellite” regions in human DNA. Nature 314: 67–73, 1985

    Google Scholar 

  • Juul-Madsen, H. R., Glamann, J., Madsen, H. O., and Simonsen, M. MHC class II beta-chain expression in the rainbow trout. Scand J Immunol 35: 687–694, 1992

    Google Scholar 

  • Kasahara, M., Vazquez, M., Sato, K., McKinney, E. C., and Flajnik, M. F. Evolution of the major histocompatibility complex: isolation of class II A cDNA clones from the cartilaginous fish. Proc Natl Acad Sci USA 89: 6688–6692, 1992

    Google Scholar 

  • Kasahara, M., McKinney, E. C., Flajnik, M. F., and Ishibashi, T. The evolutionary origin of the major histocompatibility complex: polymorphism of class II α chain genes in the cartilaginous fish. Eur J Immunol 23: 2160–2165, 1993

    Google Scholar 

  • Kaufman, J. F., Skjoedt, K., and Salomonsen, J. The MHC molecules of nonmammalian vertebrates. Immunol Rev 113: 83–117, 1990

    Google Scholar 

  • Kelly, A. P., Monaco, J. J., Cho, S., and Trowsdale, J. A new human HLA class II-related locus, DM. Nature 353: 571–573, 1991

    Google Scholar 

  • Kimura, M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111–120, 1980

    CAS  PubMed  Google Scholar 

  • Klein, D., Ono, H., O'hUigin, C., Vincek, V., Goldshmidt, T., and Klein, J. Extensive MHC variability in cichlid fishes of Lake Malawi. Nature 364: 330–334, 1993

    Google Scholar 

  • Klein, Jan. Natural History of the Majhor Histocompatibility Complex. John Wiley, New York, 1986

    Google Scholar 

  • Klein, J., Bontrop, R. E., Dawkins, R. L., Erlich, H. A., Gyllensten, U. B., Heise, E. R., Jones, P. P., Parham, P., Wakeland, E. K., and Watkins, D. I. Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics 31: 217–219, 1990

    CAS  PubMed  Google Scholar 

  • Klein, J., Satta, Y., and O'hUigin, C. The molecular descent of the major histocompatibility complex. Annu Rev Immunol 11: 269–295, 1993

    Article  CAS  PubMed  Google Scholar 

  • Koetsier, P. A., Schorr, J., and Doerfler, W. A rapid opimized protocol for downward alkaline southern blotting of DNA. Biotechniques 15: 260–262, 1993

    Google Scholar 

  • Kozak, M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res 12: 857–872, 1984

    Google Scholar 

  • Kumar, S., Tamura, K., and Nei, M. MEGA: Molecular Evolutionary Genetics Analysis,version 1.02, The Pennsylvania State University, University Park, PA, 1993

    Google Scholar 

  • L'Abbe, D., Belmaaza, A., Decary, F., and Chartrand, P. Elimination of heteroduplex artifacts when sequencing HLA genes amplified by polymerase chain reaction (PCR). Immunogenetics 35: 395–397, 1992

    CAS  PubMed  Google Scholar 

  • Lanzavecchia, A. Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. Annu Rev Immunol 8: 773–793, 1990

    Google Scholar 

  • Miller, N. W., Sizemore, R. C., and Clem, L. W. Phylogeny of lymphocyte heterogeneity: the cellular requirements for in vitro antibody responses of channel catfish leucocytes. J Immunol 134: 2884–2888, 1985

    Google Scholar 

  • Miller, N. W., Rycyzn, M. A., Wilson, M. R., Warr, G. W., Naftel, J. P., and Clem, L. W. Development and characterization of channel catfish long term B cell lines. J Immunol 152: 2180–2189, 1994

    Google Scholar 

  • Ono, H., Klein, D., Vincek, V., Figueroa, F., O'hUigin, C., Tichy, H., and Klein, J. Major histocompatibility complex class II genes of zebrafish. Proc Natl Acad Sci USA 89: 11886–11890, 1992

    Google Scholar 

  • Ono, H., O'hUigin, C., Tichy, H., and Klein, J. Major histocompatibility complex variation in two species of cichlid fishes from Lake Malawi. Mol Biol Evol 10(sa5): 1060–1072, 1993a

    Google Scholar 

  • Ono, H., O'hUigin, C., Vincek, V., Stet, R. J. M., figueroa, F., and Klein, J. New β chain-encoding Mhc class II genes in the carp. Immunogenetics 38: 146–149, 1993b

    Google Scholar 

  • Ono, H., O'hUigin, C., Vincek, V., and Klein, J., Exon-intron organization of fish major histocompatibility complex class II B genes. Immunogenetics 38: 223–234, 1993c

    Google Scholar 

  • Rothbard, J. B. and Gefter, M. L. Interactions between immunogenic peptides and Mhc proteins. Annu Rev Immunol 9: 527–565, 1991

    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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sato, K., Flajnik, M. F., Pasquier, L. D., Katagiri, M., and Kasahara, M. Evolution of the MHC: isolation of class II beta-chain cDNA clones from the Amphibian Xenopus laevis. J Immunol 150: 2831–2843, 1992

    Google Scholar 

  • Schamboeck, A., Korman, A. J., Kamb, A., and Strominger, J. L. Organization of the transcriptional unit of a human class II histocompatibility antigen: HLA-DR heavy chain. Nucleic Acids Res 11: 8663–8675, 1983

    Google Scholar 

  • She, J.-X. and Wakeland, E. K. Molecular and genetic mechanisms involved in the generation of Mhc diversity. In J. Klein and D. Klein (eds.): Molecular Evolution of the Major Histocompatibility Complex, pp. 139–154, Springer, Berlin Heidelberg, 1991

    Google Scholar 

  • Smith, G. R. Mechanism and control of homologous recombination in Escherichia coli. Annu Rev Genetics 21: 179–201, 1987

    Google Scholar 

  • Stern, L. J., Brown, J. H., Jardetzky, T. S., Gorga, J. C., Urban, R. G., Strominger, J. L., and Wiley, D. C. Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza peptide. Nature 368: 215–221, 1994

    Google Scholar 

  • Stet, R. J. M. and Egberts, E. The histocompatibility system in teleost fishes: from multiple histocompatibility loci to a major histocompatibility complex. Fish and Shellfish Immunology 1: 1–16, 1991

    Google Scholar 

  • Stet, R. J. M., van Erp, S. H. M., Hermsen, T., Sültmann, H. A., and Egberts, E. Polymorphism and estimation of the number of MhcCyca class I and class II genes in laboratory strains of the common carp (Cyprinus carpio L.). Dev Comp Immunol 17: 141–156, 1993

    Google Scholar 

  • Sültmann, H., Werner, W. E., Figueroa, F., O'hUigin, C., and Klein, J. Zebrafish Mhc class II α chain-encoding genes: polymorphism, expression, and function. Immunogenetics 38: 408–420, 1993

    Google Scholar 

  • Sültmann, H., Mayer, W. E., Figueroa, F., O'hUigin, C., and Klein, J. Organization of the Mhc class II B genes in the zebrafish (Brachydanio rerio). Genomics 23: 1–14, 1994

    Article  PubMed  Google Scholar 

  • Vallejo, A. N., Miller, N. W., and Clem, L. W. Antigen processing and presentation in teleost immune responses. Annu Rev Fish Diseases 2: 73–89, 1992

    Google Scholar 

  • Walker, R. B. and McConnell, T. J. Variability in an MhcMosa class II β chain-encoding gene in the striped bass (Morone saxatilis). Dev Comp Immunol 18: 325–342, 1994

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

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 (Mosa-A-S5) L35062, (Mosa-A-S8) L35066, (Mosa-A-R7) L35067, and (Mosa-A-S7) L35072 L35066, (Mossa-A-R7) L35067, and (Mosa-A-S7) L35072

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hardee, J.J., Godwin, U., Benedetto, R. et al. Major histocompatibility complex class II A gene polymorphism in the striped bass. Immunogenetics 41, 229–238 (1995). https://doi.org/10.1007/BF00172064

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00172064

Keywords

Navigation