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The MHC class I linkage group is a major determinant in the in vivo rejection of allogeneic erythrocytes in rainbow trout (Oncorhynchus mykiss)

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An Erratum to this article was published on 26 November 2003

Abstract

Despite accumulating sequence data, information on the function of major histocompatibility complex (MHC) genes in fish is scarce. In contrast to the genome organization in higher vertebrates, the polymorphic MHC class I and II genes are not linked in the teleost genome. A previous study found an MHC class II linkage group to be a major determinant in the rejection of allogeneic scales by a teleost species (Cardwell et al. 2001). The present study investigated whether the teleost MHC class I linkage group can be involved in allograft rejection. Erythrocytes were chosen as grafts since they express MHC class I, but do not express class II. Rainbow trout erythrocytes expressing different MHC class I alleles were differentially stained, mixed and injected into recipients that were of the same sibling group as the donors. The MHC class I linkage group was the major determinant for in vivo graft rejection.

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References

  • Abelli L, Baldassini MR, Mastrolia L, Scapigliati G (1999) Immunodetection of lymphocyte subpopulations involved in allograft rejection in a teleost, Dicentrarchus labrax (L.). Cell Immunol 191:152–160

    Article  CAS  PubMed  Google Scholar 

  • Alcorn SA, Murray AL, Pascho RJ (2002) Effects of rearing temperature on immune functions in sockeye salmon (Oncorhynchus nerka). Fish Shellfish Immunol 12:303–334

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Auchincloss H, Sykes M, Sachs DH (1999) Transplantation immunology. In: Paul WE (ed) Fundamental immunology. Lippincott-Raven, Philadelphia, pp 1175–1236

  • Bach FH, Sachs DH (1987) Current concepts: immunology. Transplantation immunology. N Engl J Med 317:489–492

    CAS  PubMed  Google Scholar 

  • Blajchman MA, Singal DP (1989) The role of red blood cell antigens, histocompatibility antigens, and blood transfusions on renal allograft survival. Transfus Med Rev 3:171–179

    CAS  PubMed  Google Scholar 

  • Cardwell TN, Sheffer RJ, Hedrick PW (2001) MHC variation and tissue transplantation in fish. J Hered 92:305–308

    Article  CAS  PubMed  Google Scholar 

  • Crone M, Simonsen M (1976) Allo-aggression in chickens. II. Cellular expression of the AA gene products. Acta Pathol Microbiol Scand [C] 84:319–324

    Google Scholar 

  • Dijkstra JM, Köllner B, Aoyagi K, Sawamoto Y, Kuroda A, Ototake M, Nakanishi T, Fischer U (2003) The rainbow trout classical MHC class I molecule Onmy-UBA*501 is expressed in similar cell types as mammalian classical MHC class I molecules. Fish Shellfish Immunol 14:1–23

    Article  CAS  PubMed  Google Scholar 

  • Fischer U, Ototake M, Nakanishi T (1998a) In vitro cell-mediated cytotoxicity against allogeneic erythrocytes in ginbuna crucian carp and goldfish using a non-radioactive assay. Dev Comp Immunol 22:195–206

    Article  CAS  PubMed  Google Scholar 

  • Fischer U, Ototake M, Nakanishi T (1998b) Life span of circulating blood cells in ginbuna crucian carp (Carassius auratus langsdorfii). Fish Shellfish Immunol 8:339–349

    Article  Google Scholar 

  • Fischer U, Utke K, Ototake M, Dijkstra JM, Köllner B (2003) Adaptive cell-mediated cytotoxicity against allogeneic targets by CD8-positive lymphocytes of rainbow trout (Oncorhynchus mykiss) Dev Comp Immunol 27:323–337

    Google Scholar 

  • Flajnik MF, Kaufman JF, Riegert P, Du Pasquier L (1984) Identification of class I major histocompatibility complex encoded molecules in the amphibian Xenopus. Immunogenetics 20:433–442

    CAS  PubMed  Google Scholar 

  • Fujiwara A, Kiryu I, Dijkstra JM, Yoshiura Y, Nishida-Umehara C, Ototake M (2003) Chromosome mapping of MHC class I in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 14:171–175

    Article  CAS  PubMed  Google Scholar 

  • Germain RN (1999) Antigen processing and presentation. In: Paul WE (ed) Fundamental immunology. Lippincott-Raven, Philadelphia, pp 287–340

  • Hansen DJ, Strassburger P, Du Pasquier L (1996) Conservation of α2 domain within the teleostean world, MHC class I from the rainbow trout Oncorhynchus mykiss. Dev Comp Immunol 20:417–425

    CAS  PubMed  Google Scholar 

  • Hansen DJ, Strassburger P, Thorgaard GH, Young WP, Du Pasquier L (1999) Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss. J Immunol 163:774–786

    PubMed  Google Scholar 

  • Heslop BF, Heslop HE (1979) Allogeneic red blood cells fail to induce haemagglutinating antibodies or cellular alloimmunity in rats and are immunosuppressive. Transplantation 28:144–148

    CAS  PubMed  Google Scholar 

  • Hogan RJ, Stuge TB, Clem LW, Miller NW, Chinchar VG (1996) Anti-viral cytotoxic cells in the channel catfish (Ictalurus punctatus). Dev Comp Immunol 20:115–127

    Article  CAS  PubMed  Google Scholar 

  • Kaastrup P, Stet RJ, Tigchelaar AJ, Egberts E, van Muiswinkel WB (1989) A major histocompatibility locus in fish: serological identification and segregation of transplantation antigens in the common carp (Cyprinus carpio L.). Immunogenetics 30:284–290

    CAS  PubMed  Google Scholar 

  • Klempau AE, Cooper EL (1984) T-lymphocyte and B-lymphocyte dichotomy in anuran amphibians: III. Assessment and identification of inducible killer T-lymphocytes (IKTL) and spontaneous killer T-lymphocytes (SKTL). Dev Comp Immunol 8:649–661

    Article  CAS  PubMed  Google Scholar 

  • Koppang EO, Hordvik I, Bjerkås I, Torvund J, Aune L, Thevarajan J, Endresen C (2003) Production of rabbit antisera against recombinant MHC class IIβ chain and identification of immunoreactive cells in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 14:115–132

    Article  CAS  PubMed  Google Scholar 

  • Lechler R, Batchelor R, Lombardi G (1991) The relationship between MHC restricted and allospecific T-cell recognition. Immunol Lett 29:41–50

    Article  CAS  PubMed  Google Scholar 

  • Madden DR (1995) The three-dimensional structure of peptide-MHC complexes. Ann Rev Immunol 13:587–622

    CAS  Google Scholar 

  • Manilay JO, Sykes M (1998) Natural killer cells and their role in graft rejection. Curr Opin Immunol 10:532–538

    Article  CAS  PubMed  Google Scholar 

  • Manning JM, Nakanishi T (1996) The specific immune system: cellular defenses. In: Iwama G, Nakanishi T (eds) The fish immune system. Academic Press, San Diego, pp 159–205

  • Matsumura M, Fremont DH, Peterson PA, Wilson IA (1992) Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 257:927–934

    CAS  PubMed  Google Scholar 

  • Moyes CD, Sharma ML, Lyons C, Leary SC, Leon M, Petrie A, Lund SG, Tufts BL (2002) Origins and consequences of mitochondrial decline in nucleated erythrocytes. Biochim Biophys Acta 1591:11–20

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi T, Fischer U, Dijkstra JM, Hasegawa S, Somamoto T, Okamoto N, Ototake M (2002) Cytotoxic T-cell function in fish. Dev Comp Immunol 26:131–139

    Article  CAS  PubMed  Google Scholar 

  • Ohta Y, Okamura K, McKinney EC, Bartl S, Hashimoto K, Flajnik MF (2000) Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc Natl Acad Sci USA 97:4712–4717

    CAS  PubMed  Google Scholar 

  • Reid ME, Yazdanbakhsh K (1998) Molecular insights into blood groups and implications for blood transfusion. Curr Opin Hematol 5:93–102

    CAS  PubMed  Google Scholar 

  • Rodrigues PN, Hermsen TT, Rombout JH, Egberts E, Stet RJ (1995) Detection of MHC class II transcripts in lymphoid tissues of the common carp (Cyprinus carpio L.). Dev Comp Immunol 19:483–496

    Article  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 

  • Sgonc R, Hala K, Wick G (1987) Relationship between the expression of class I antigen and reactivity of chicken thymocytes. Immunogenetics 26:150–154

    CAS  PubMed  Google Scholar 

  • Shen L, Stuge TB, Zhou H, Khayat M, Barker KS, Quiniou SM, Wilson M, Bengten E, Chinchar VG, Clem LW, Miller NW (2002) Channel catfish cytotoxic cells: a mini-review. Dev Comp Immunol 26:141–149

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Spack E Jr, Edidin M (1986) The class I MHC antigens of erythrocytes: a serologic and biochemical study. J Immunol 136:2943–2952

    CAS  PubMed  Google Scholar 

  • Stet RJ, van Erp SH, Hermsen T, Sultmann HA, Egberts E (1993) 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

    Article  CAS  PubMed  Google Scholar 

  • Stet RJ, de Vries B, Mudde K, Hermsen T, 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 

  • Williams VM, Wetherall JD, Simms G, Papadimitriou JM (1981) Evolution of the major histocompatibility complex. I. Survival of autologous, allogeneic and xenogeneic red blood cells in the lizard Tiliqua rugosa. Dev Comp Immunol 5:629-638

    CAS  PubMed  Google Scholar 

  • Xia C, Kiryu I, Dijkstra JM, Azuma T, Nakanishi T, Ototake M (2002) Differences in MHC class I genes between strains of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 12:287–301

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto M, Iuchi I (1975) Electron microscopic study of erythrocytes in developing rainbow trouts, Salmo gairdnerii irideus, with particular reference to changes in the cell line. J Exp Zool 191:407–426

    CAS  PubMed  Google Scholar 

  • Yoshinaga K, Okamoto N, Kurata O, Ikeda Y (1994) Individual variations of natural killer activity of rainbow trout leucocytes against IPN virus-infected and uninfected RTG-2 cells. Fish Pathol 29:1–4

    Google Scholar 

Download references

Acknowledgements

This study was supported by a postdoctoral fellowship for Md. Rafiqul Islam Sarder from the Science and Technology Agency of Japan and by “the promotion of basic research activities for innovative biosciences” funded by Bio-oriented Technology Research Advancement Institution (BRAIN), Japan. All the work reported here was performed in compliance with all applicable institutional and federal regulations. We thank Dr. James D. Moore, Bodega Marine Laboratory, USA, for his help editing this manuscript.

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Authors and Affiliations

  1. Inland Station, National Research Institute of Aquaculture, Fisheries Research Agency, Tamaki, 519-0423, Mie, Japan

    Md. Rafiqul Islam Sarder, Johannes Martinus Dijkstra, Ikunari Kiryu, Yasutoshi Yoshiura & Mitsuru Ototake

  2. Institutes for Infectiology and Diagnostic Virology, Friedrich-Loeffler-Institutes, 17498, Insel Riems, Germany

    Uwe Fischer & Bernd Köllner

  3. Nikko Branch, National Research Institute of Aquaculture, Fisheries Research Agency, Chugushi, Nikko, 321-1661, Tochigi, Japan

    Teruo Azuma

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  1. Md. Rafiqul Islam Sarder
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  2. Uwe Fischer
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  3. Johannes Martinus Dijkstra
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Correspondence to Mitsuru Ototake.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00251-003-0632-3

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Sarder, M.R.I., Fischer, U., Dijkstra, J.M. et al. The MHC class I linkage group is a major determinant in the in vivo rejection of allogeneic erythrocytes in rainbow trout (Oncorhynchus mykiss). Immunogenetics 55, 315–324 (2003). https://doi.org/10.1007/s00251-003-0587-4

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  • DOI: https://doi.org/10.1007/s00251-003-0587-4

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