Skip to main content

Advertisement

Log in

Major Histocompatibility Complex Class IIB Allele Polymorphism and Its Association with Resistance/Susceptibility to Vibrio anguillarum in Japanese Flounder (Paralichthys olivaceus)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The full length of major histocompatibility complex (MHC) class IIB cDNA was cloned from a Chinese population of Paralichthys olivaceus by homology cloning and rapid amplification of cDNA ends-polymerase chain reaction (RACE-PCR). The MHC IIB genomic sequence is 1,864 bp long and consists of 34-bp 5′UTR, 741-bp open reading frame, 407-bp 3′UTR, 96-bp intron1, 392-bp intron2, 85-bp intron3, and 109-bp intron4. Phylogenetic analysis showed that the putative MHC class IIB amino acid of the Chinese P. olivaceus shared 28.3% to 85.4% identity with that of the reported MHC class IIB in other species. A significant association between MHC IIB polymorphism and disease resistance/susceptibility was found in Chinese P. olivaceus. Thirteen different MHC IIB alleles were identified among 411 clones from 84 individuals. Among the 280 (268) nucleotides, 32 (11.4%) nucleotide positions were variable. Most alleles such as alleles a, b, c, d, e, f, j, k, i, m were commonly found in both resistant and susceptible stock. Via χ2 test, allele d was significantly more prevalent in individuals from susceptible stock than from resistant stock, and their percentages were 23.80% and 7.14%, respectively. In addition, allele g occurred in 9 and allele h in 4 of 42 resistant individuals that were not present in the susceptible stock; their percentages were 21.4% and 9.52%, respectively. Although allele l was found only in 8 individuals from the susceptible stock, its percentage is 19.05%.

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.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  • H Acha-Orbea L Scarpellino (1991) ArticleTitleNonobese diabetic and nonobese nondiabetic mice have unique MHC class II haplotypes Immunogenetics 34 57–59 Occurrence Handle10.1007/BF00212313

    Article  Google Scholar 

  • V Apanius D Penn PR Slev LR Ruff WK Potts (1997) ArticleTitleThe nature of selection on the major histocompatibility complex Rev Immunol 17 179–224

    Google Scholar 

  • S Bartl IL Weissman (1994) ArticleTitleIsolation and characterization of major histocompatibility complex class II B genes from the nurse shark Proc Natl Acad Sci USA 91 262–266 Occurrence Handle10.1073/pnas.91.1.262

    Article  Google Scholar 

  • T Binz C Largiader R Müller C Wedekind (2001) ArticleTitleSequence diversity of Mhc genes in lake whitefish J Fish Biol 58 359–373 Occurrence Handle10.1111/j.1095-8649.2001.tb02258.x

    Article  Google Scholar 

  • WE Briles RW Briles RE Taffs HA Stone (1983) ArticleTitleResistance to a malignant lymphoma in chickens is mapped to subregion of major histocompatibility (B) complex Science 219 977–979 Occurrence Handle10.1126/science.6823560

    Article  Google Scholar 

  • SL Chen MY Xu SN Hu L Li (2004a) ArticleTitleAnalysis of immune–relevant genes expressed in red sea bream (Chrysophrys major) spleen Aquaculture 240 115–130 Occurrence Handle10.1016/j.aquaculture.2004.07.008

    Article  Google Scholar 

  • SL Chen MY Xu XS Ji GC Yu (2004b) ArticleTitleCloning and characterization of natural resistance associated macrophage protein (Nramp) cDNA from red sea bream (Pagrus major) Fish Shellfish Immunol 17 305–313 Occurrence Handle10.1016/j.fsi.2004.04.003

    Article  Google Scholar 

  • SL Chen YX Zhang MY Xu XS Ji GC Yu CF Dong (2006) ArticleTitleMolecular polymorphism and expression analysis of MHC II B gene from red sea bream (Chrysophrys major) Dev Comp Immunol 30 407–418 Occurrence Handle10.1016/j.dci.2005.06.001

    Article  Google Scholar 

  • B Dixon LAJ Nagelkerke E Sibbing RJM Stet (1996) ArticleTitleEvolution of MHC class II β chain-encoding genes in the Lake Tana barbell species flock (Barbus intermedius complex) Immunogenetics 44 IssueID6 419–431 Occurrence Handle10.1007/s002510050148

    Article  Google Scholar 

  • S Edwards PW Hedrick (1998) ArticleTitleEvolution and ecology of MHC molecules: from genomics to sexual selection Trends Ecol Evol 13 305–311 Occurrence Handle10.1016/S0169-5347(98)01416-5

    Article  Google Scholar 

  • F Figueroa WE Mayer H Sultmann C O'hUigin H Tichy Y Satta N Takezaki N Takahata J Klein (2000) ArticleTitleMHC class II B gene evolution in East African cichlid fishes Immunogenetics 51 556–575 Occurrence Handle10.1007/s002510000181

    Article  Google Scholar 

  • MF Flajnik C Canel J Kramer M Kasahara (1991) ArticleTitleEvolution of the major histocompatibility complex: molecular cloning of major histocompatibility complex class I from the amphibian Xenopus Proc Natl Acad Sci USA 88 537–541 Occurrence Handle10.1073/pnas.88.2.537

    Article  Google Scholar 

  • T Gjedrem R Salte HM Gjoen (1991) ArticleTitleGenetic variation in susceptibility of Atlantic salmon to furunculosis Aquaculture 97 1–6 Occurrence Handle10.1016/0044-8486(91)90274-B

    Article  Google Scholar 

  • J Glamann (1995) ArticleTitleComplete coding sequence of rainbow trout Mhc II beta chain Scand J Immunol 41 365–372 Occurrence Handle10.1111/j.1365-3083.1995.tb03580.x

    Article  Google Scholar 

  • UB Godwin A Antao MR Wilson VG Chinchar NW Miller et al. (1997) ArticleTitleMHC class II β genes in the channel catfish (Icatalurus punctatus) Dev Comp Immunol 21 13–23 Occurrence Handle10.1016/S0145-305X(97)00003-7

    Article  Google Scholar 

  • U Grimholt I Olsaker CV Lindstrom O Lie (1994) ArticleTitleA study of variability in the MHC class II β1 and class I α2 domain exons of Atlantic salmon (Salmo salar) Anim Genet 25 147–153 Occurrence Handle10.1111/j.1365-2052.1994.tb00103.x

    Article  Google Scholar 

  • U Grimholt S Larsen R Nordmo P Midtlyng S Kjoeglum A Storset S Saebo RJ Stet (2003) ArticleTitleMHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci Immunogenetics 55 210–219 Occurrence Handle10.1007/s00251-003-0567-8

    Article  Google Scholar 

  • D Grossberger P Parham (1992) ArticleTitleReptilian class I major histocompatibility complex genes reveal conserved elements in class I structure Immunogenetics 36 166–174 Occurrence Handle10.1007/BF00661093

    Article  Google Scholar 

  • PW Hedrick TJ Kim (1999) Genetics of complex polymorphisms: parasites and maintenance of MHC variation RS Singh CK Krimbas (Eds) Evolutionary Genetics from Molecules to Morphology Cambridge University Press New York

    Google Scholar 

  • AVS Hill CEM Allsopp D Kwiatkowski et al. (1991) ArticleTitleCommon West African HLA antigens associated with protection from severe malaria Nature 352 595–600 Occurrence Handle10.1038/352595a0

    Article  Google Scholar 

  • AR Hoelzel JC Stephens SJ O'Brien (1999) ArticleTitleMolecular genetic diversity and evolution at the MHC DQB locus in four species of pinnipeds Mol Biol Evol 16 611–618

    Google Scholar 

  • I Hordvik U Grimholt VM Fosse Ø Lie C Endresen (1994) ArticleTitleCloning and sequence analysis of cDNA encoding the MHC class II β chain in Atlantic salmon (Salmo salar) Immunogenetics 37 437–441

    Google Scholar 

  • AL Hughes (2000) ArticleTitleEvolution of introns and exons of class II major histocompatibility complex genes of vertebrates Immunogenetics 51 473–486 Occurrence Handle10.1007/s002510050646

    Article  Google Scholar 

  • D Klein H Ono C O'hUigin V Vincek T Goldschmidt J Klein (1993) ArticleTitleExtensive MHC variability in cichlid fishes of Lake Malawi Nature 364 330–334 Occurrence Handle10.1038/364330a0

    Article  Google Scholar 

  • J Klein (1986) Natural History of the Major Histocompatibility Complex John Wiley & Sons New York

    Google Scholar 

  • CP Kruiswijk TT Hermsen AH Westphal HFJ Savelkoul RJM Stet (2002) ArticleTitleA novel functional class I lineage in zebrafish (Danio rerio), carp (Cyprinus carpio), and large barbus (Barbus ingtermedius) showing an unusual conservation of the peptide binding domains J Immunol 169 1936–1947

    Google Scholar 

  • S Kumar K Tamura I Jakobsen M Nei (2001) ArticleTitleMEGA2.0: Molecular evolutionary genetics analysis software Bioinformatics 17 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244

    Article  Google Scholar 

  • A Langefors J Lohm T Schantz ParticleVon (2001) ArticleTitleAllelic polymorphism in MHC class II β in four populations of Atlantic salmon (Salmo salar) Immunogenetics 53 329–336 Occurrence Handle10.1007/s002510100329

    Article  Google Scholar 

  • Å Langefors J Lohm M Grahn O Andersen T Schantz Particlevon (2001) ArticleTitleAssociation between Mhc class II B alleles and resistance to Aeromonas salmonicida in Atlantic salmon Proc R Soc Lond B 268 479–485 Occurrence Handle10.1098/rspb.2000.1378

    Article  Google Scholar 

  • Y Liu M Kasahara LL Rumfelt MF Flajnik (2002) ArticleTitleXenopus class II a genes: studies if genetics, polymorphism, and expression Dev Comp. Immunol 26 735–750 Occurrence Handle10.1016/S0145-305X(02)00034-4

    Article  Google Scholar 

  • YG Liu SL Chen BF Li (2005) ArticleTitleAssessing the genetic structure of three Japanese flounder (Paralichthys olivaceus) stocks by microsatellite markers Aquaculture 243 103–111 Occurrence Handle10.1016/j.aquaculture.2004.10.024

    Article  Google Scholar 

  • J Lohm M Grahn A Langefors O Andersen A Storset T Schantz Particlevon (2002) ArticleTitleExperimental evidence for major histocompatibility complex-allele-specific resistance to a bacterial infection Proc Biol Sci 269 2029–2033 Occurrence Handle10.1098/rspb.2002.2114

    Article  Google Scholar 

  • E Medina RJ North (1998) ArticleTitleResistance ranking of some common inbred mouse strains to Mycobacterium tuberculosis and relationship to major histocompatibility complex haplotype and Nramp1 genotype Immunology 93 270–274 Occurrence Handle10.1046/j.1365-2567.1998.00419.x

    Article  Google Scholar 

  • MM Miller R Goto A Bernot R Zoorob C Auffray N Bumstead WE Briles (1994) ArticleTitleTwo Mhc class I and two Mhc class II genes map to the chicken Rfp-y system outside the B complex Proc Natl Acad Sci USA 91 4397–4401 Occurrence Handle10.1073/pnas.91.10.4397

    Article  Google Scholar 

  • YK Ohta EC Okamura S McKinney BK Hashimoto MF Flajnik (2000) ArticleTitlePrimitive synteny of vertebrate major histocompatibility complex class I and class II genes Proc Natl Acad Sci USA 97 IssueID9 4712–4717 Occurrence Handle10.1073/pnas.97.9.4712

    Article  Google Scholar 

  • H Ono D Klein V Vincek F Figueroa C O'hUigin H Tichy J Klein (1992) ArticleTitleMajor histocompatibility complex class II genes of zebrafish Proc Natl Acad Sci USA 89 11886–11890 Occurrence Handle10.1073/pnas.89.24.11886

    Article  Google Scholar 

  • RA Padgett PJ Grabowski MM Konarska S Seiler PA Sharp (1986) ArticleTitleSplicing of messenger RNA precursors Annu Rev Biochem 55 1119–1150 Occurrence Handle10.1146/annurev.bi.55.070186.005351

    Article  Google Scholar 

  • Y Palti MN Krista KI Waller JE Parsons GH Thorgaard (2001) ArticleTitleAssociation between DNA polymorphisms tightly linked to MHC class II genes and IHV virus resistance in backcrosses of rainbow and cutthroat trout Aquaculture 194 283–289 Occurrence Handle10.1016/S0044-8486(00)00526-3

    Article  Google Scholar 

  • P Parham T Ohta (1996) ArticleTitlePopulation biology of antigen presentation by MHC class I molecules Science 272 67–74 Occurrence Handle10.1126/science.272.5258.67

    Article  Google Scholar 

  • S Paterson K Wilson JM Pemberton (1998) ArticleTitleMajor histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population Proc Natl Acad Sci USA 95 3714–3719 Occurrence Handle10.1073/pnas.95.7.3714

    Article  Google Scholar 

  • O Pedro HFV Houria CZ Sophie et al. (2003) ArticleTitleAssociations of MHC ancestral haplotypes with resistance/susceptibility to AIDS disease development J Immunol 170 1925–1929

    Google Scholar 

  • SS Ristow LD Grabowski SM Thompson GW Warr SL Kaattari JM Avila Particlede GH Thorgaard (1999) ArticleTitleCoding sequences of the MHC class II β chain of homozygous rainbow trout (Oncorhynchus mykiss) Dev Comp Immunol 23 51–60 Occurrence Handle10.1016/S0145-305X(98)00039-1

    Article  Google Scholar 

  • JB Rothbard ML Gefter (1991) ArticleTitleInteractions between immunogenetic peptides and Mhc proteins Annu Rev Immunol 9 527–565 Occurrence Handle10.1146/annurev.iy.09.040191.002523

    Article  Google Scholar 

  • P Srisapoome T Ohira I Hirono T Aoki (2004) ArticleTitleCloning, characterization and expression of cDNA containing major histocompatibility complex class II α and II β genes of Japanese flounder Paralichthys olivaceus Fish Sci 70 264 Occurrence Handle10.1111/j.1444-2906.2003.00800.x

    Article  Google Scholar 

  • RJM Stet CP Kruiswijk JP Saeij GF Wiegertjes (1998) ArticleTitleMajor histocompatibility genes in cyprinid fishes: theory and practice Immunol. Rev 166 301–316 Occurrence Handle10.1111/j.1600-065X.1998.tb01271.x

    Article  Google Scholar 

  • H Sültmann W Mayer F Figueroa C O'Huigin J Klein (1994) ArticleTitleOrganization of Mhc class II B genes in the zebrafish (Brachydanio rerio) Genomics 23 1–14 Occurrence Handle10.1006/geno.1994.1452

    Article  Google Scholar 

  • JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleClustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions- specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673–4680 Occurrence Handle10.1093/nar/22.22.4673

    Article  Google Scholar 

  • J Trowsdale (1995) ArticleTitleBoth man and bird and beast: comparative organization of MHC genes Immunogenetics 41 1–17 Occurrence Handle10.1007/BF00188427

    Article  Google Scholar 

  • SHM Erp ParticleVan E Egberts RJ Stet (1996) ArticleTitleCharacterization of class II A and B genes in a gynogenetic carp clone Immunogenetics 44 192–202 Occurrence Handle10.1007/s002510050111

    Article  Google Scholar 

  • RB Walker TJ McConnell RA Walker (1994) ArticleTitleVariability in an MHC Mosa class II beta chain-encoding gene in striped bass (Morone saxatilis) Dev Comp Immunol 18 325–342 Occurrence Handle10.1016/S0145-305X(94)90358-1

    Article  Google Scholar 

  • H Wittzell T Madsen H Westerdahl R Shine T Schantz ParticleVon (1999) ArticleTitleMHC variations in birds and reptiles Genetics 104 301–309

    Google Scholar 

  • Wynne J, Cook MT, Barbara FN, Nicholas GE (2004) Polymorphism within MHC genes associated with resistance and susceptibility to amoebic gill disease (AGD) in Atlantic salmon Salmo salar. Australian aquaculture posters presented by CSIRO scientists.

  • Zhang YX, Chen SL (2006) Molecular identification, polymorphism and expression analysis of major histocompatibility complex class II A and B genes of turbot (Scophthalmus maximus). Marine Biotechnol, DOI: 10.1007/s10126-005-6174-y

Download references

Acknowledgments

This work was supported by grants from National Major Basic Research Program (973) (2004CB117403) and National Nature Science Foundation of China (30413240) and state 863 High-Technology R&D Project of China (2002AA626010).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. L. Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Y.X., Chen, S.L., Liu, Y.G. et al. Major Histocompatibility Complex Class IIB Allele Polymorphism and Its Association with Resistance/Susceptibility to Vibrio anguillarum in Japanese Flounder (Paralichthys olivaceus). Mar Biotechnol 8, 600–610 (2006). https://doi.org/10.1007/s10126-005-6185-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-005-6185-8

Keywords

Navigation