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Expression profiles of interferon gamma genes in response to immunostimulants and alloantigen in ginbuna crucian carp Carassius auratus langsdorfii

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Abstract

Interferon gamma (IFNγ), a Th1-derived cytokine is one of the key molecules inducing cell-mediated immune responses in mammals. The expression of 2 distinct IFNγ (ifng1 and ifng2) and IFNγrel (ifngrel) genes was examined in kidney leukocytes from clonal ginbuna crucian carp Carassius auratus langsdorfii. The expression of IFNγ and IFNγrel genes was induced in kidney leukocytes by stimulation with lipopolysaccharide or phytohemagglutinin in a dose-dependent manner. The expression levels of IFNγ and IFNγrel genes in kidney leukocytes from allo-sensitized fish cocultured with allogeneic cells were higher than those from fish cocultured with isogeneic cells. The highest expression of ifng1 was observed at day 1, whereas that of ifng2 and ifngrel was detected at day 2 after cocultivation with allogeneic cells. However, the expression pattern of ifng2 and ifngrel in kidney leukocytes from allo-sensitized fish by scale-grafting was similar to those from non-sensitized fish. These results indicate that ifng1 is a major isoform of IFNγ related to antigen-specific cell-mediated immunity (CMI), and will be a useful marker to evaluate induction of CMI in ginbuna crucian carp. In addition, IFNγ would be a crucial type-II interferon compared to IFNγrel, relevant to cell-mediated immunity in fish as in mammals.

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References

  1. Mosmann TR, Sad S (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today 17:138–146

    Article  PubMed  CAS  Google Scholar 

  2. Romagnani S (1999) Th1/Th2 cells. Inflamm Bowel Dis 5:285–294

    Article  PubMed  CAS  Google Scholar 

  3. Stockinger B, Veldhoen M (2007) Differentiation and function of Th17 T cells. Curr Opin Immunol 19:281–286

    Article  PubMed  CAS  Google Scholar 

  4. Bending D, Newland S, Krejci A, Phillips JM, Bray S, Cooke A (2011) Epigenetic change at Il12rb2 and Tbx21 in relation to plasticity behavior of Th17 cells. J Immunol 186:3373–3382

    Article  PubMed  CAS  Google Scholar 

  5. Annunziato F, Cosmi L, Santariasci V, Maggi L, Liotta F, Mazzinghi B, Patrnte E, Filì L, Frosali F, Giudici F, Romagnani P, Parronchi P, Tonelli F, Maggi E, Romagnani S (2007) Phenotypic and functional features of human Th17 cells. J Exp Med 204:1849–1861

    Article  PubMed  CAS  Google Scholar 

  6. Cosmi L, Maggi L, Santarlasci V, Capone M, Cardilicchia E, Frosali F, Querci V, Angeli R, Matucci A, Fambrini M, Liotta F, Parronchi P, Maggi E, Romagnani S, Annunziato F (2010) Identification of a novel subset of human circulating memory CD4(+) T cells that produce both IL-17A and IL-4. J Allergy Clin Immunol 125:222–230

    Article  PubMed  CAS  Google Scholar 

  7. McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, Mcclanahan T, Cua DJ (2007) TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 8:1390–1397

    Article  PubMed  CAS  Google Scholar 

  8. Beriou G, Bradshaw EM, Lozano E, Costantino CM, Hastings WD, Orban T, Elyaman W, Khoury SJ, Kuchroo VK, Baecher-Allan C, Hafler DA (2010) TGF-beta induces IL-9 production from human Th17 cells. J Immunol 185:46–54

    Article  PubMed  CAS  Google Scholar 

  9. Boniface K, Blom B, Liu YJ, De WaalMalefyt R (2008) From interleukin-23 to T-helper 17 cells: human T-helper cell differentiation revisited. Immunol Rev 226:132–146

    Article  PubMed  CAS  Google Scholar 

  10. Bluestone JA, Abbas K (2003) Natural versus adapted regulatory T cells. Nat Rev Immunol 3:253–257

    Article  PubMed  CAS  Google Scholar 

  11. Fontenot JD, Rudensky AY (2005) A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor FoxP3. Nat Immunol 6:331–337

    Article  PubMed  CAS  Google Scholar 

  12. Sakaguchi S (2000) Regulatory T cells: key controllers of immunologic selftolerance. Cell 101:455–458

    Article  PubMed  CAS  Google Scholar 

  13. Shevach EM (2000) Regulatory T cells in autoimmunity. Annu Rev Immunol 18:423–449

    Article  PubMed  CAS  Google Scholar 

  14. Frucht DM, Fukao T, Bogdan C, Schindler H, O’Shea JJ, Koyasu S (2001) IFN-gamma production by antigen presenting cells: mechanisms emerge. Trends Immunol 22:556–560

    Article  PubMed  CAS  Google Scholar 

  15. Boehm U, Klamp T, Groot M, Howard JC (1997) Cellular responses to interferon-gamma. Annu Rev Immunol 15:749–795

    Article  PubMed  CAS  Google Scholar 

  16. Schroder K, Hertzog PJ, Ravasi T, Hume DA (2004) Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75:163–189

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  18. Nakanishi T, Toda H, Shibasaki Y, Somamoto T (2011) Cytotoxic T cells in teleost fish. Dev Comp Immunol 35:1317–1323

    Article  PubMed  CAS  Google Scholar 

  19. Zou J, Yoshiura Y, Dijkstra JM, Sakai M, Ototake M, Secombes C (2004) Identification of an interferon gamma homologue in Fugu, Takifugu rubripes. Fish Shellfish Immunol 17:403–409

    Article  PubMed  CAS  Google Scholar 

  20. Igawa D, Sakai M, Savan R (2006) An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and -26 genes have been described for the first time outside mammals. Mol Immunol 43:999–1009

    Article  PubMed  CAS  Google Scholar 

  21. Zou J, Carrington A, Collet B, Dijkstra JM, Yoshiura Y, Bols N, Secombes C (2005) Identification and bioactivities of IFN-gamma in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 175:2484–2494

    PubMed  CAS  Google Scholar 

  22. Milev-Milovanovic I, Long S, Wilson M, Bengten E, Miller NW, Chinchar VG (2006) Identification and expression analysis of interferon gamma genes in channel catfish. Immunogenetics 58:70–80

    Article  PubMed  CAS  Google Scholar 

  23. Stolte EH, Savelkoul HF, Wiegertjes G, Flik G, Verbung-van Lidy, kemenade BM (2008) Differential expression of two interferon-gamma genes in common carp (Cyprinus carpio L.). Dev Comp Immunol 32:1467–1481

    Article  PubMed  CAS  Google Scholar 

  24. Furnes C, Seppola M, Robertsen B (2009) Molecular characterization and expression analysis of interferon gamma in Atlantic cod (Gadus morhua). Fish Shellfish Immunol 26:285–292

    Article  PubMed  CAS  Google Scholar 

  25. Grayfer L, Belosevic M (2009) Molecular characterization, expression and functional analysis of goldfish (Carassius auratus L.) interferon gamma. Dev Comp Immunol 33:235–246

    Article  PubMed  CAS  Google Scholar 

  26. Matsuyama T, Fujiwara A, Sakai T, Nakayasu C (2009) Molecular cloning and expression analysis of interferon gamma gene in Japanese flounder Paralichthys olivaceus. Fish Sci 75:253–255

    Article  CAS  Google Scholar 

  27. Yabu T, Toda H, Shibasaki Y, Araki K, Yamashita M, Anzai H, Mano N, Masuhiro Y, Hanazawa S, Shiba H, Moritomo T, Nakanishi T (2011) Antiviral protection mechanisms mediated by ginbuna crucian carp interferon gamma isoforms 1 and 2 through two distinct interferon gamma-receptors. J Biochem 150:635–648

    Article  PubMed  CAS  Google Scholar 

  28. 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  PubMed  CAS  Google Scholar 

  29. Somamoto T, Yoshiura Y, Sato A, Nakao M, Nakanishi T, Okamoto N, Ototake M (2006) Expression profiles of TCRβ and CD8α mRNA correlate with virus-specific cell-mediated cytotoxic activity in ginbuna crucian carp. Virology 348:370–377

    Article  PubMed  CAS  Google Scholar 

  30. Somamoto T, Yoshiura Y, Nakanishi T, Ototake M (2005) Molecular cloning and characterization of two types of CD8α from ginbuna crucian carp, Carassius auratus langsdorfii. Dev Comp Immunol 29:693–702

    Article  PubMed  CAS  Google Scholar 

  31. Araki K, Hirano K, Takizawa F, Moritomo T, Ototake M, Nakanishi T (2007) Identification and characterization of multiple lck genes in ginbuna crucian carp Carassius auratus langsdorfii. Fish Sci 73:1017–1024

    Article  CAS  Google Scholar 

  32. Nonaka S, Somamoto T, Kato-Unoki Y, Ototake M, Nakanishi T, Nakao M (2008) Molecular cloning of CD4 from ginbuna crucian carp Carassius auratus langsdorfii. Fish Sci 74:341–346

    Article  CAS  Google Scholar 

  33. Takizawa F, Araki K, Kobayashi I, Moritomo T, Ototake M, Nakanishi T (2008) Molecular cloning and expression analysis of T-bet in ginbuna crucian carp (Carassius auratus langsdorfii). Mol Immunol 45:127–136

    Article  PubMed  CAS  Google Scholar 

  34. Takizawa F, Mizunaga Y, Araki K, Moritomo T, Ototake M, Nakanishi T (2008) GATA3 mRNA in ginbuna crucian carp (Carassius auratus langsdorfii): cDNA cloning, splice variants and expression analysis. Dev Comp Immunol 32:898–907

    Article  PubMed  CAS  Google Scholar 

  35. Toda H, Shibasaki Y, Koike T, Ohtani M, Takizawa F, Ototake M, Moritomo T, Nakanishi T (2009) Alloantigen-specific killing is mediated by CD8-positive T cells in fish. Dev Comp Immunol 33:646–652

    Article  PubMed  CAS  Google Scholar 

  36. Toda H, Saito Y, Koike T, Takizawa F, Araki K, Yabu T, Somamoto T, Suetake H, Suzuki Y, Ototake M, Moritomo T, Nakanishi T (2011) Conservation of characteristics and functions of CD4 positive lymphocytes in a teleost fish. Dev Comp Immunol 35:650–660

    Article  PubMed  CAS  Google Scholar 

  37. Hasegawa S, Nakayasu C, Okamoto N, Nakanishi T, Ikeda Y (1997) Fin cell line from isogeneic ginbuna crucian carp. In Vitro Cell Biol Anim 33:232–233

    Article  CAS  Google Scholar 

  38. Nakanishi T, Ototake M (1999) The graft-versus-host reaction (GVHR) in the ginbuna crucian carp, Carassius auratus langsdorfii. Dev Comp Immunol 23:15–26

    Article  PubMed  CAS  Google Scholar 

  39. Sizemore RC, Miller NW, Cuchens MA, Lobb CJ, Clem LW (1984) Phylogeny of lymphocyte heterogeneity: the cellular requirements for in vitro mitogenic responses of channel catfish leukocytes. J Immunol 133:2920–2924

    PubMed  CAS  Google Scholar 

  40. Wang C, Noga EJ, Avtalion R, Levy MG (1997) Whole blood assay for examining lymphocyte blastogenesis of percichthyid bass (Morone). Vet Immunol Immunopathol 58:355–362

    Article  PubMed  CAS  Google Scholar 

  41. Kehrer SR, Hannan CM, Raison RL (1998) Identification of a subpopulation of leucocytes from the rainbow trout (Oncorhynchus mykiss) responsive to pokeweed mitogen. Fish Shellfish Immunol 8:477–487

    Article  Google Scholar 

  42. Morrison RN, Lyons AB, Nowak BF, Hayball JD (2004) Snapper (Pagrus auratus) leukocyte proliferation is synergistically enhanced by simultaneous stimulation with LPS and PHA. Fish Shellfish Immunol 16:307–319

    Article  PubMed  CAS  Google Scholar 

  43. Blohm U, Siegl E, Köllner B (2003) Rainbow trout (Oncorhynchus mykiss) sIgM-leukocytes secrete an interleukin-2 like growth factor after mitogenic stimulation in vitro. Fish Shellfish Immunol 14:449–466

    Article  PubMed  CAS  Google Scholar 

  44. Araki K, Akatsu K, Suetake H, Kikuchi K, Suzuki Y (2008) Characterization of CD8+ leukocytes in fugu (Takifugu rubripes) with antiserum against fugu CD8α. Dev Comp Immunol 32:850–858

    Article  PubMed  CAS  Google Scholar 

  45. Negishi M, Izumi Y, Aleemuzzaman S, Inaba N, Hayakawa S (2011) Lipopolysaccharide (LPS)-induced interferon (IFN)-gamma production by decidual mononuclear cells (DMNC) in interleukin (IL)-2 and IL-12 dependent. Am J Reprod Immunol 65:20–27

    Article  PubMed  CAS  Google Scholar 

  46. Takizawa F, Dijkstra JM, Kotterba P, Korytář T, Kock H, Köllner B, Jaureguiberry B, Nakanishi T, Fischer U (2011) The expression of CD8α discriminates distinct T cell subsets in teleost fish. Dev Comp Immunol 35:752–763

    Article  PubMed  CAS  Google Scholar 

  47. Castro R, Martin SA, Zou J, Secombes CJ (2010) Establishment of an IFN-γ specific reporter cell line in fish. Fish Shellfish Immunol 28:312–319

    Article  PubMed  CAS  Google Scholar 

  48. Saeji JP, Stet RJ, de Vries BJ, van Muiswinkel WB, Wiegertjes GF (2003) Molecular and functional characterization of carp TNF: a link between TNF polymorphism and trypanotolerance? Dev Comp Immunol 27:29–41

    Article  Google Scholar 

  49. Engelsma MY, Stet RJ, Saeij JP, Verburg-van Kemenade BM (2003) Differential expression and haplotypic variation of two interleukin-1beta genes in the common carp (Cyprinus carpio L.). Cytokine 22:21–32

    Article  PubMed  CAS  Google Scholar 

  50. Huising MO, van Schijindel JE, Kruiswijk CP, Nabuurs SB, Savelkoul HF, Flik G, Verburg-van Kemenade BM (2006) The presence of multiple and differentially regulated interleukin-12p40 genes in bony fishes signifies an expansion of the vertebrate heterodimeric cytokine family. Mol Immunol 43:1519–1533

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Ministry of Education, Science, Sports and Culture, Grant-in-Aid for Young Scientists (B) from Japan Society for the Promotion of Science (JSPS).

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Correspondence to Teruyuki Nakanishi.

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Araki, K., Takizawa, F., Yamasaki, M. et al. Expression profiles of interferon gamma genes in response to immunostimulants and alloantigen in ginbuna crucian carp Carassius auratus langsdorfii . Fish Sci 79, 213–220 (2013). https://doi.org/10.1007/s12562-012-0590-5

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