Abstract
Transcriptionally active, MHC class I (MHCI) loci are located in two separate polymorphic genomic regions in the chicken called B and Y. The YMHCI gene sequences encode molecules with uncommon substitutions in the antigen-binding region indicating that YMHCI molecules are likely unique and may bind a specialized form of antigen distinct from that of other antigen-binding MHCI molecules. To learn whether YMHCI gene expression results in the production of alloantigens at the cell surface, we immunized 15I5 × 7 2 chickens using syngeneic RP9 cells expressing transduced YF1w*7.1, a potentially alloimmunogenic YMHCI allele from the Y7 haplotype present in line C. The resulting antisera show that YF1w*7.1 MHCI molecules are immunogenic and expressed on the surfaces of cells in blood and spleen of line C chickens. Virtually all CD3+, CD4+, and CD8+ cells circulating in line C blood are positive, as are BU1+ cells. The YF1w*7.1 MHCI allele is dynamically expressed at levels comparable to but transcriptionally independent of classical BMHCI on erythrocytes, lymphocytes, granulocytes, monocytes, and thrombocytes within the spleen pre- and post-hatching. The antisera react with cells from two among four haplotypes segregating in closed populations of lines N and P. YMHCI shares features associated with both classical and non-classical MHCI. It is becoming increasingly likely that YMHCI has a fundamental role in avian immunity and thereby needs to be included in the growing spectrum of functionally active, diverse MHCI molecules no longer adequately described by the classical/non-classical dichotomy.
Similar content being viewed by others
Abbreviations
- MHC:
-
Major histocompatibility complex
- Y :
-
formerly Rfp-Y
- MCF:
-
mean channels of fluorescence
- ADOL:
-
Avian Disease and Oncology Laboratory
- RFP:
-
Restriction fragment pattern
- YMHCI:
-
Y MHC class I
- BMHCI:
-
B MHC class I
References
Afanassieff M, Goto RM, Ha J, Zoorob R, Auffray C, Coudert F, Briles WE, Miller MM (2000) Are chicken Rfp-Y class I genes classical or non-classical? In: Kasahara M (ed) The major histocompatibility complex: evolution, structure, and function, 6th international workshop on MHC evolution, Hayama, Kanagawa, Japan. Springer, Berlin Heidelberg New York
Afanassieff M, Goto RM, Ha J, Sherman M, Zhong L, Auffray C, Coudert F, Zoorob R, Miller MM (2001) At least one class I gene in restriction fragment pattern-Y (Rfp-Y), the second MHC gene cluster in the chicken, is transcribed, polymorphic and shows divergent specialization in antigen binding region. J Immunol 166:3324–3333
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
Briles WE, Goto RM, Auffray C, Miller MM (1993) A polymorphic system related to but genetically independent of the chicken major histocompatibility complex. Immunogenetics 37:408–414
Bumstead N (1998) Genetic resistance to avian viruses. Rev Sci Tech 17:249–255
Dunon D, Salomonsen J, Skjodt K, Kaufman J, Imhof BA (1990) Ontogenic appearance of MHC class I (B-F) antigens during chicken embryogenesis. Dev Immunol 1:127–135
Eerola E, Veromaa T, Toivanen P (1987) Special features in the structural organization of the avian lymphoid system. In: Toivanen A, Toivanen P (eds) Avian immunology: basis and practice. CRC, Boca Raton, pp 9–21
Einhauer A, Jungbauer A (2001) The FLAG peptide, a versatile fusion tag for the purification of recombinant proteins. J Biochem Biophys Methods 49:455–465
Fillon V, Zoorob R, Yerle M, Auffray C, Vignal A (1996) Mapping of the genetically independent chicken major histocompatibility complexes B and RFP-Y to the same microchromosome by two-color fluorescent in situ hybridization. Cytogenet Cell Genet 75:7–9
Foster TL, Goto RM, Yokoyama WM, Miller MM (2005) Reporter cell assays reveal interaction between a putative NK cell receptor encoded within chicken MHC B and a nonclassical class I allele encoded within chicken MHC Y. Vol Program Abstract #250.10, Experimental Biology 2005, San Diego, California
Fulton JE, Thacker EL, Bacon LD, Hunt HD (1995) Functional analysis of avian class I (BFIV) glycoproteins by epitope tagging and mutagenesis in vitro. Eur J Immunol 25:2069–2076
Fulton JE, Young EE, Bacon LD (1996) Chicken Mhc alloantiserum cross-reactivity analysis by hemagglutination and flow cytometry. Immunogenetics 43:277–288
Fulton JE, Hunt HD, Bacon LD (2001) Chicken major histocompatibility complex class I definition using antisera induced by cloned class I sequences. Poult Sci 80:1554–1561
Gobel TW, Chen CH, Cooper MD (1996) Avian natural killer cells. Curr Top Microbiol Immunol 212:107–117
Guillemot F, Billault A, Pourquie O, Behar G, Chausse AM, Zoorob R, Kreibich G, Auffray C (1988) A molecular map of the chicken major histocompatibility complex: the class II beta genes are closely linked to the class I genes and the nucleolar organizer. EMBO J 7:2775–2785
Hay FC, Westwood OMR (2002) Practical immunology. Blackwell, Oxford
Hess CM, Edwards SV (2002) The evolution of the major histocompatibility complex in birds. Bioscience 52:423–431
Hughes SH, Greenhouse JJ, Petropoulos CJ, Sutrave P (1987) Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J Virol 61:3004–3012
John JL (1994) The avian spleen: a neglected organ. Q Rev Biol 69:327–351
Kaufman J, Jacob J, Shaw I, Walker B, Milne S, Beck S, Salomonsen J (1999) Gene organisation determines evolution of function in the chicken MHC. Immunol Rev 167:101–117
Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695
Lakshmanan N, Lamont SJ (1998) Rfp-Y region polymorphism and Marek’s disease resistance in multitrait immunocompetence-selected chicken lines. Poult Sci 77:538–541
LePage KT, Miller MM, Briles WE, Taylor RL Jr (2000) Rfp-Y genotype affects the fate of Rous sarcomas in B2B5 chickens. Immunogenetics 51:751–754
Lucas AM, Jamroz C (1961) Atlas of avian hematology. United States Department of Agriculture, Washington
Miller MM, Bacon LD, Hala K, Hunt HD, Ewald SJ, Kaufman J, Zoorob R, Briles WE (2004) Nomenclature for the chicken major histocompatibility (B and Y) complex. Immunogenetics 56:261–279
Miller MM, Goto R, Zoorob R, Auffray C, Briles WE (1994) Regions of homology shared by Rfp-Y and major histocompatibility B complex genes. Immunogenetics 39:71–73
Miller MM, Goto RM, Taylor RL Jr, Zoorob R, Auffray C, Briles RW, Briles WE, Bloom S E (1996) Assignment of Rfp-Y to the chicken major histocompatibility complex/NOR microchromosome and evidence for high-frequency recombination associated with the nucleolar organizer region. Proc Natl Acad Sci U S A 93:3958–3962
Miller MM, Wang C, Parisini E, Coletta R, Goto RM, Lee SY, Barral DC, Townes M, Roura-Mir C, Ford HL, Brenner MB, Dascher CC (2005) Characterization of two avian MHC-like genes reveals an ancient origin of the CD1 family. Proc Natl Acad Sci U S A 102:8674–8679
Okazaki W, Witter RL, Romero C, Nazerian K, Sharma JM, Fadly A, Ewert D (1980) Induction of lymphoid leukosis transplantable tumours and the establishment of lymphoblastoid cell lines. Avian Pathol 9:311–329
Pharr GT, Gwynn AV, Bacon LD (1996) Histocompatibility antigen(s) linked to Rfp-Y (Mhc-like) genes in the chicken. Immunogenetics 45:52–58
Pharr GT, Vallejo RL, Bacon LD (1997) Identification of Rfp-Y (Mhc-like) haplotypes in chickens of Cornell lines N and P. J Hered 88:504–512
Pinard-van der Laan MH, Soubieux D, Merat L, Bouret D, Luneau G, Dambrine G, Thoraval P (2004) Genetic analysis of a divergent selection for resistance to Rous sarcomas in chickens. Genet Sel Evol 36:65–81
Praharaj N, Beaumont C, Dambrine G, Soubieux D, Merat L, Bouret D, Luneau G, Alletru JM, Pinard-van der Laan MH, Thoraval P, Mignon-Grasteau S (2004) Genetic analysis of the growth curve of Rous sarcoma virus-induced tumors in chickens. Poult Sci 83:1479–1488
Rodgers JR, Cook RG (2005) MHC class Ib molecules bridge innate and acquired immunity. Nat Rev Immunol 5:459–471
Salomonsen J, Sorensen MR, Marston DA, Rogers SL, Collen T, van Hateren A, Smith AL, Beal RK, Skjodt K, Kaufman J (2005) Two CD1 genes map to the chicken MHC, indicating that CD1 genes are ancient and likely to have been present in the primordial MHC. Proc Natl Acad Sci U S A 102:8668–8673
Schaefer-Klein J, Givol I, Barsov EV, Whitcomb JM, VanBrocklin M, Foster DN, Federspiel MJ, Hughes SH (1998) The EV-O-derived cell line DF-1 supports the efficient replication of avian leukosis-sarcoma viruses and vectors. Virology 248:305–311
Schaefer-Klein J, Givol I, Barsov EV, Whitcomb JM, VanBrocklin M, Foster DN, Federspiel MJ, Hughes SH (1998) The EV-O-derived cell line DF-1 supports the efficient replication of avian leukosis-sarcoma viruses and vectors. Virology 248:305–311
Shen PF, Smith EJ, Bacon LD (1984) The ontogeny of blood cells, complement, and immunoglobulins in 3- to 12-week-old 15I5-B congenic white Leghorn chickens. Poult Sci 63:1083–1093
Shiina T, Shimizu S, Hosomichi K, Kohara S, Watanabe S, Hanzawa K, Beck S, Kulski JK, Inoko H (2004) Comparative genomic analysis of two avian (quail and chicken) MHC regions. J Immunol 172:6751–6763
Thoraval P, Afanassieff M, Bouret D, Luneau G, Esnault E, Goto RM, Chausse AM, Zoorob R Soubieux D, Miller MM, Dambrine G (2003) Role of nonclassical class I genes of the chicken major histocompatibility complex Rfp-Y locus in transplantation immunity. Immunogenetics 55:647–651
Vallejo RL, Pharr GT, Liu HC, Cheng HH, Witter RL, Bacon LD (1997) Non-association between Rfp-Y major histocompatibility complex-like genes and susceptibility to Marek’s disease virus-induced tumours in 6(3) × 7(2) F2 intercross chickens. Anim Genet 28:31–37
Wakenell PS, Miller MM, Goto RM, Gauderman WJ, Briles WE (1996) Association between the Rfp-Y haplotype and the incidence of Marek’s disease in chickens. Immunogenetics 44:242–245
Acknowledgements
We thank Evelyn Young and Dr. Terry Lemme for excellent assistance in producing the antisera and for assistance in flow cytometry evaluation. This material is based upon the work supported in part by the U.S. Department of Agriculture/National Research Initiative Competitive Grants Program (92-37204-8244 and 2002-35205-11628), the U.S. Department of Agriculture/Foreign Agricultural Service/International Collaborative Research/Research and Scientific Exchange Division (58-3148-5-023), and by the National Science Foundation under Grants 9118199 and 9604589.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hunt, H.D., Goto, R.M., Foster, D.N. et al. At least one YMHCI molecule in the chicken is alloimmunogenic and dynamically expressed on spleen cells during development. Immunogenetics 58, 297–307 (2006). https://doi.org/10.1007/s00251-005-0074-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00251-005-0074-1