Skip to main content

Advertisement

SpringerLink
Log in

MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci

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

Abstract

Few studies have yet addressed the functional aspects of MHC molecules in fish. To lay the foundation for this, we evaluated the association between disease resistance and MHC class I and class II polymorphism in Atlantic salmon. Standardized disease challenge trials were performed on a semi-wild Atlantic salmon population with subsequent MHC typing and statistical analysis. The pathogens employed were infectious salmon anaemia virus (ISAV) causing infectious salmon anaemia and the Aeromonas salmonicida bacteria causing furunculosis. The material consisted of 1,182 Atlantic salmon from 33 families challenged with A. salmonicida and 1,031 Atlantic salmon from 25 families challenged with ISAV. We found highly significant associations between resistance towards infectious diseases caused by both pathogens and MH class I and class II polymorphism in Atlantic salmon. The observed associations were detected due to independently segregating MH class I and class II single loci, and inclusion of a large number of fish allowing an extensive statistical analysis.

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

Fig. 1.
Fig. 2.

Similar content being viewed by others

References

  • Agresti (1990) Categorical Data Analysis. Wiley, New York

  • Aoyagi K, Dijkstra JM, Xia C, Denda I, Ototake M, Hashimoto K, Nakanishi T (2002) Classical MHC class I genes composed of highly divergent sequence lineages share a single locus in rainbow trout (Oncorhynchus mykiss). J Immunol 168:260–273

    CAS  PubMed  Google Scholar 

  • Bacon LD (1987) Influence of the major histocompatibility complex on disease resistance and productivity. Poult Sci 66:802–811

    CAS  PubMed  Google Scholar 

  • Bacon LD, Hunt HD, Cheng HH (2000) A review of the development of chicken lines to resolve genes determining resistance to diseases. Poult Sci 79:1082–1093

    CAS  PubMed  Google Scholar 

  • Bot A, Casares S, Bot S, von Boehmer H, Bona C (1998) Cellular mechanisms involved in protection against influenza virus infection in transgenic mice expressing a TCR receptor specific for class II hemagglutinin peptide in CD4+ and CD8+ T cells. J Immunol 160:4500–4507

    CAS  PubMed  Google Scholar 

  • Carrington M, O'Brien SJ (2003) The influence of HLA genotype on AIDS. Annu Rev Med 54:535–551

    Article  CAS  PubMed  Google Scholar 

  • Cheng HH, Levin I, Vallejo RL, Khatib H, Dodgson JB, Crittenden LB, Hillel J (1995) Development of a genetic map of the chicken with markers of high utility. Poult Sci 74:1855–1874

    CAS  PubMed  Google Scholar 

  • Clouthier SC, Rector T, Brown NE, Anderson ED (2002) Genomic organization of infectious salmon anaemia virus. J Gen Virol 83:421–8

    CAS  PubMed  Google Scholar 

  • Douglas GA (1991) Practical statistics for medical research. Chapman and Hall, London

  • Egidius E (1987) Import of furunculosis to Norway with Atlantic salmon smolts from Scotland. International Council for the Exploration of the sea (ICES). Mariculture Committee C.M.1987/F:8. Report

  • Emmerich R, Weibel E (1894) Ueber eine durch bakterien erzengte seuche unter den forellen. Arch Hyg Bacteriol 21:1–21

    Google Scholar 

  • Falk K, Namork E, Rimstad E, Mjaaland S, Dannevig BH (1997) Characterization of infectious salmon anemia virus, an orthomyxo-like virus isolated from Atlantic salmon (Salmo salar L.). J Virol 71:9016–9023

    CAS  PubMed  Google Scholar 

  • Feder JN, Gnirke A, Thomas W, Tsuchihashi Z, Ruddy DA, Basava A, Dormishian F, Domingo R Jr, Ellis MC, Fullan A, Hinton LM, Jones NL, Kimmel BE, Kronmal GS, Lauer P, Lee VK, Loeb DB, Mapa FA, McClelland E, Meyer NC, Mintier GA, Moeller N, Moore T, Morikang E, Wolff RK, et al. (1996) A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat Genet 13:399–408

    PubMed  Google Scholar 

  • Garduno RA, Moore AR, Olivier G, Lizama AL, Garduno E, Kay WW (2000) Host cell invasion and intracellular residence by Aeromonas salmonicida: role of the S-layer. Can J Microbiol 46:660–668

    Article  CAS  PubMed  Google Scholar 

  • Gjedrem T (2000) Genetic improvement of cold-water fish species. Aquaculture 31:25–33

    Article  Google Scholar 

  • Gjedrem T, Gjoen HM, Gjerde B (1991) Genetic origin of Norwegian farmed Atlantic salmon. Aquaculture 98:41–50

    Google Scholar 

  • Graser R, O'hUigin C, Vincek V, Meyer A, Klein J (1996) Trans-species polymorphism of class II Mhc loci in danio fishes. Immunogenetics 44:36–48

    CAS  PubMed  Google Scholar 

  • Grimholt U, Hordvik I, Fosse VM, Olsaker I, Endresen C, Lie O (1993) Molecular cloning of major histocompatibility complex class I cDNAs from Atlantic salmon (Salmo salar). Immunogenetics 37:469–473

    CAS  PubMed  Google Scholar 

  • Grimholt U, Getahun A, Hermsen T, Stet RJ (2000) The major histocompatibility class II alpha chain in salmonid fishes. Dev Comp Immunol 24:751–63

    CAS  PubMed  Google Scholar 

  • Grimholt U, Drabløs F, Jørgensen SM, Høyheim B, Stet RJM (2002) The major histocompatibility class I locus in Atlantic salmon (Salmo salar L.): polymorphism, linkage analysis and protein modelling. Immunogenetics 54:570–581

    Article  CAS  PubMed  Google Scholar 

  • Hansen JD, Strassburger P, Thorgaard GH, Young WP, Du PL (1999) Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss. J Immunol 163:774–86

    PubMed  Google Scholar 

  • Harris EK, Albert A (1991) Survivorship analysis for clinical studies. Dekker, New York

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

    CAS  PubMed  Google Scholar 

  • Hill AV (1998) The immunogenetics of human infectious diseases. Annu Rev Immunol 16:593–617

    Article  CAS  PubMed  Google Scholar 

  • Hill AV, Yates SN, Allsopp CE, Gupta S, Gilbert SC, Lalvani A, Aidoo M, Davenport M, Plebanski M (1994) Human leukocyte antigens and natural selection by malaria. Philos Trans R Soc Lond B Biol Sci 346:379–385

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jacob JP, Milne S, Beck S, Kaufman J (2000) The major and a minor class II beta-chain (B-LB) gene flank the Tapasin gene in the B-F/B-L region of the chicken major histocompatibility complex. Immunogenetics 51:138–147

    CAS  PubMed  Google Scholar 

  • Kaufman J, Milne S, Gobel TW, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925

    Article  PubMed  Google Scholar 

  • Krossoy B, Nilsen F, Falk K, Endresen C, Nylund A (2001) Phylogenetic analysis of infectious salmon anaemia virus isolates from Norway, Canada and Scotland. Dis Aquat Organ 44:1–6

    CAS  PubMed  Google Scholar 

  • Lamont SJ (1998) The chicken major histocompatibility complex and disease. Rev Sci Tech 17:128–142

    CAS  PubMed  Google Scholar 

  • Langefors A, Lohm J, Grahn M, Andersen O, von Schantz T (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond B Biol Sci 268:479–485

    Article  CAS  PubMed  Google Scholar 

  • Lehmann EL (1975) Non-parametrics: statistical methods based on ranks. Holden-Day, San Fransisco

  • Marsh SGE, Parham P, Barber LD (2000) The HLA factsbook. San Diego

  • Martinez-Borra J, Gonzalez S, Lopez-Vazquez A, Gelaz MA, Armas JB, Kanga U, Mehra NK, Lopez-Larrea C (2000) HLA-B27 alone rather than B27-related class I haplotypes contributes to ankylosing spondylitis susceptibility. Hum Immunol 61:131–139

    Article  CAS  PubMed  Google Scholar 

  • Mjaaland S, Rimstad E, Falk K, Dannevig BH (1997) Genomic characterization of the virus causing infectious salmon anemia in Atlantic salmon (Salmo salar L.): an orthomyxo-like virus in a teleost. J Virol 71:7681–7686

    CAS  PubMed  Google Scholar 

  • Mullins JE, Groman D, Wadowska D (1998) Infectious salmon anaemia in salt water Atlantic salmon (Salmo salar L.) in New Brunswick, Canada. Bull Eur Assoc Fish Pathol 18:110–114

    Google Scholar 

  • Nakanishi T, Aoyagi K, Xia C, Dijkstra JM, Ototake M (1999) Specific cell-mediated immunity in fish. Vet Immunol Immunopathol 72:101–109

    Article  CAS  PubMed  Google Scholar 

  • Nordmo R (1997) Strengths and weaknesses of different challenge methods. In: Gudding R, Lillehaug A, Midtlyng P, Brown F (eds): Fish Vaccinology. Karger, Basel, pp 303–309

  • Nordmo R, Ramstad A, Riseth JMH (1998) Induction of experimental furunculosis in heterogeneous test populations of Atlantic salmon (Salmo salar L.) by use of a cohabitation method. Aquaculture 162:11–21

    Article  Google Scholar 

  • Ozaki A, Sakamoto T, Khoo S, Nakamura K, Coimbra MR, Akutsu T, Okamoto N (2001) Quantitative trait loci (QTLs) associated with resistance/susceptibility to infectious pancreatic necrosis virus (IPNV) in rainbow trout (Oncorhynchus mykiss). Mol Genet Genomics 265:23–31

    Article  CAS  PubMed  Google Scholar 

  • Parham P, Ohta T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272:67–74

    PubMed  Google Scholar 

  • Pocock SJ (1983) Clinical trials: a practical approach. Wiley, New York

    Google Scholar 

  • Puel A, Mevel JC, Bouthillier Y, Feingold N, Fridman WH, Mouton D (1996) Toward genetic dissection of high and low antibody responsiveness in Biozzi mice. Proc Natl Acad Sci USA 93:14742–14746

    Article  CAS  PubMed  Google Scholar 

  • Raynard RS, Murray AG, Gregory A (2001) Infectious salmon anaemia virus in wild fish from Scotland. Dis Aquat Organ 46:93–100

    CAS  PubMed  Google Scholar 

  • Rodger HD, Turnbull T, Muir F, Millar S, Richards RH (1998) Infectious salmon anaemia (ISA) in the United Kingdom. Bull Eur Assoc Fish Pathol 18:115–116

    Google Scholar 

  • Sakamoto T, Danzmann RG, Gharbi K, Howard P, Ozaki A, Khoo SK, Woram RA, Okamoto N, Ferguson MM, Holm LE, Guyomard R, Hoyheim B (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345

    CAS  PubMed  Google Scholar 

  • Sato A, Figueroa F, Murray BW, Malaga-Trillo E, Zaleska-Rutczynska Z, Sultmann H, Toyosawa S, Wedekind C, Steck N, Klein J (2000) Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51:108–116

    PubMed  Google Scholar 

  • Satta Y, O'hUigin C, Takahata N, Klein J (1994) Intensity of natural selection at the major histocompatibility complex loci. Proc Natl Acad Sci USA 91:7184–7188

    CAS  PubMed  Google Scholar 

  • Shum BP, Guethlein L, Flodin LR, Adkison MA, Hedrick RP, Nehring RB, Stet RJ, Secombes C, Parham P (2001) Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J Immunol 166:3297–3308

    CAS  PubMed  Google Scholar 

  • Stet RJM, de Vries B, Mudde K, Hermsen TT, van Heerwaarden J, Shum BP, Grimholt U (2002) Unique haplotypes of co-segregating major histocompatibility class II A and class II B alleles in Atlantic salmon (Salmo salar) give rise to diverse class II genotypes. Immunogenetics 54:320–331

    Article  CAS  PubMed  Google Scholar 

  • Takami K, Zaleska-Rutczynska Z, Figueroa F, Klein J (1997) Linkage of LMP, TAP, and RING3 with Mhc class I rather than class II genes in the zebrafish. J Immunol 159:6052–6060

    PubMed  Google Scholar 

  • The MHC Sequencing Consortium (1999) Complete sequence and gene map of a human major histocompatiblity complex. Nature 401:921–923

    PubMed  Google Scholar 

  • Thorud K, Djupvik HO (1988) Infectious anaemia in Atlantic salmon (Salmo salar L.). Bull Eur Ass Fish Pathol 8:111

    Google Scholar 

  • Vallejo RL, Bacon LD, Liu HC, Witter RL, Groenen MA, Hillel J, Cheng HH (1998) Genetic mapping of quantitative trait loci affecting susceptibility to Marek's disease virus induced tumors in F2 intercross chickens. Genetics 148:349–360

    CAS  PubMed  Google Scholar 

  • Yonash N, Bacon LD, Witter RL, Cheng HH (1999) High resolution mapping and identification of new quantitative trait loci (QTL) affecting susceptibility to Marek's disease. Anim Genet 30:126–135

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by a grant from the European Commission (Fair CT97-3643). All animal experiments performed in this study comply with the current laws of Norway. We would like to thank Beja de Vries, Karin Mudde, Trudi Hermsen, Elin Urdahl, Siv Malme, Eirik Balgaard, Sven Martin Jørgensen and Christian Gløckner for their excellent technical support. The nucleotide sequences in this study are available upon request for research purposes.

Author information

Author notes

  1. Rolf Nordmo

    Present address: Biotec AS, Oslo, Norway

Authors and Affiliations

  1. Department of Morphology, Genetics and Aquatic Biology, Section of Genetics, Norwegian School of Veterinary Science, Ullevaalsveien 72, P.O. Box 8146 Dep., 0033, Oslo, Norway

    Unni Grimholt, Stig Larsen & Sissel Kjoeglum

  2. VESO Vikan AkvaVet, 7810 , Alhusstrand, Norway

    Rolf Nordmo & Paul Midtlyng

  3. Aqua Gen AS, 7200, Kyrksaeterøra, Norway

    Sissel Kjoeglum & Arne Storset

  4. Department of Mathematical Sciences, Agricultural University of Norway, 1432, Ås, Norway

    Solve Saebø

  5. Wageningen Institute of Animal Sciences, Cell Biology and Immunology Group, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands

    René J. M. Stet

Authors
  1. Unni Grimholt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stig Larsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rolf Nordmo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul Midtlyng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sissel Kjoeglum
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arne Storset
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Solve Saebø
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. René J. M. Stet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Unni Grimholt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grimholt, U., Larsen, S., Nordmo, R. et al. MHC 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 (2003). https://doi.org/10.1007/s00251-003-0567-8

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-003-0567-8

Keywords

Search

Navigation