Transcription of signal-3 cytokines, IL-12 and IFNαβ, coincides with the timing of CD8αβ up-regulation during viral infection of common carp (Cyprinus carpio L.)

Molecular Immunology

Volumn 45, Issue 6, 2008, Pages 1531-1547

  Forlenza, Maria ^a   Dias, João D A de Carvalho ^a   Veselý, Tomas ^b   Pokorová, Dagmar ^b   Savelkoul, Huub F J ^a   Wiegertjes, Geert F ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b VETERINARY RESEARCH INSTITUTE   (Czech Republic)

Author keywords

CD8; Cytotoxic T cells; Fish; IL 12; Type I interferon; Virus

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; CD8ALPHA ANTIGEN; CD8BETA ANTIGEN; INTERLEUKIN 12; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; CARP; CLONING; CYTOTOXIC T LYMPHOCYTE; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; TRANSCRIPTION INITIATION; VIRUS INFECTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD28; ANTIGENS, CD8; CARPS; CD8-POSITIVE T-LYMPHOCYTES; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; GENE DOSAGE; INTERFERON-ALPHA; INTERFERON-BETA; INTERLEUKIN-12; MOLECULAR SEQUENCE DATA; PROTOZOAN INFECTIONS, ANIMAL; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RHABDOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRYPANOSOMA; UP-REGULATION; VESICULOVIRUS;

CYPRINUS CARPIO; MAMMALIA;

EID: 38949086898     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2007.10.010     Document Type: Article

References (66)

1. Ahne W., Bjorklund H.V., Essbauer S., Fijan N., Kurath G., and Winton J.R. Spring viremia of carp (SVC). Dis. Aquat. Org. 52 (2002) 261-272
2. Bernard D., Riteau B., Hansen J.D., Phillips R.B., Michel F., Boudinot P., and Benmansour A. Costimulatory receptors in a teleost fish: typical CD28, elusive CTLA4. J. Immunol. 176 (2006) 4191-4200
3. Bernard D., Six A., Rigottier-Gois L., Messiaen S., Chilmonczyk S., Quillet E., Boudinot P., and Benmansour A. Phenotypic and functional similarity of gut intraepithelial and systemic T cells in a teleost fish. J. Immunol. 176 (2006) 3942-3949
4. Boudinot P., Boubekeur S., and Benmansour A. Rhabdovirus infection induces public and private T cell responses in teleost fish. J. Immunol. 167 (2001) 6202-6209
5. Buonocore F., Randelli E., Bird S., Secombes C.J., Costantini S., Facchiano A., Mazzini M., and Scapigliati G. The CD8alpha from sea bass (Dicentrarchus labrax L.): cloning, expression and 3D modelling. Fish Shellfish Immunol. 20 (2006) 637-646
6. Casabo L.G., Mamalaki C., Kioussis D., and Zamoyska R. T cell activation results in physical modification of the mouse CD8 beta chain. J. Immunol. 152 (1994) 397-404
7. Cole D.K., and Gao G.F. CD8: adhesion molecule, co-receptor and immuno-modulator. Cell. Mol. Immunol. 1 (2004) 81-88
8. Curtsinger J.M., Johnson C.M., and Mescher M.F. CD8 T cell clonal expansion and development of effector function require prolonged exposure to antigen, costimulation, and signal 3 cytokine. J. Immunol. 171 (2003) 5165-5171
9. Curtsinger J.M., Lins D.C., and Mescher M.F. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J. Exp. Med. 197 (2003) 1141-1151
10. Curtsinger J.M., Schmidt C.S., Mondino A., Lins D.C., Kedl R.M., Jenkins M.K., and Mescher M.F. Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J. Immunol. 162 (1999) 3256-3262
11. Curtsinger J.M., Valenzuela J.O., Agarwal P., Lins D., and Mescher M.F. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174 (2005) 4465-4469
12. Daniels M.A., Devine L., Miller J.D., Moser J.M., Lukacher A.E., Altman J.D., Kavathas P., Hogquist K.A., and Jameson S.C. CD8 binding to MHC class I molecules is influenced by T cell maturation and glycosylation. Immunity 15 (2001) 1051-1061
13. Devine L., Kieffer L.J., Aitken V., and Kavathas P.B. Human CD8 beta, but not mouse CD8 beta, can be expressed in the absence of CD8 alpha as a beta beta homodimer. J. Immunol. 164 (2000) 833-838
14. DiSanto J.P., Smith D., de Bruin D., Lacy E., and Flomenberg N. Transcriptional diversity at the duplicated human CD8 beta loci. Eur. J. Immunol. 23 (1993) 320-326
15. Fijan N., Sulimanovic D., Bearzotti M., Muzinic D., Zwillenberg L.O., Chilmonczyk S., Vautherot J.F., and de kinkelin P. Some properties of the Epithelioma papulosum cyprini (EPC) cell line from carp Cyprinus carpio. Ann. Virol. (Institue Pasteur) 134 (1983) 207-220
16. Filatenkov A.A., Jacovetty E.L., Fischer U.B., Curtsinger J.M., Mescher M.F., and Ingulli E. CD4 T cell-dependent conditioning of dendritic cells to produce IL-12 results in CD8-mediated graft rejection and avoidance of tolerance. J. Immunol. 174 (2005) 6909-6917
17. Fischer U., Ototake M., and Nakanishi T. In vitro cell-mediated cytotoxicity against allogeneic erythrocytes in ginbuna crucian carp and goldfish using a non-radioactive assay. Dev. Comp. Immunol. 22 (1998) 195-206
18. Fischer U., Utke K., Ototake M., Dijkstra J.M., and Kollner B. Adaptive cell-mediated cytotoxicity against allogeneic targets by CD8-positive lymphocytes of rainbow trout (Oncorhynchus mykiss). Dev. Comp. Immunol. 27 (2003) 323-337
19. Fischer U., Utke K., Somamoto T., Kollner B., Ototake M., and Nakanishi T. Cytotoxic activities of fish leucocytes. Fish Shellfish Immunol. 20 (2006) 209-226
20. Gonzalez S.F., Chatziandreou N., Nielsen M.E., Li W., Rogers J., Taylor R., Santos Y., and Cossins A. Cutaneous immune responses in the common carp detected using transcript analysis. Mol. Immunol. 44 (2007) 1664-1679
21. Groves T., Smiley P., Cooke M.P., Forbush K., Perlmutter R.M., and Guidos C.J. Fyn can partially substitute for Lck in T lymphocyte development. Immunity 5 (1996) 417-428
22. Gubler U., Chua A.O., Schoenhaut D.S., Dwyer C.M., McComas W., Motyka R., Nabavi N., Wolitzky A.G., Quinn P.M., Familletti P.C., et al. Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 4143-4147
23. Hangartner L., Zinkernagel R.M., and Hengartner H. Antiviral antibody responses: the two extremes of a wide spectrum. Nat. Rev. Immunol. 6 (2006) 231-243
24. Hansen J.D., and Strassburger P. Description of an ectothermic TCR coreceptor, CD8 alpha, in rainbow trout. J. Immunol. 164 (2000) 3132-3139
25. Hasegawa S., Nakayasu C., Yoshitomi T., Nakanishi T., and Okamoto N. Specific cell-mediated cytotoxicity against an allogeneic target cell line in isogeneic ginbuna crucian carp. Fish Shellfish Immunol. 8 (1998) 303-313
26. Hernandez J., Aung S., Marquardt K., and Sherman L.A. Uncoupling of proliferative potential and gain of effector function by CD8(+) T cells responding to self-antigens. J. Exp. Med. 196 (2002) 323-333
27. Huising M.O., van Schijndel J.E., Kruiswijk C.P., Nabuurs S.B., Savelkoul H.F.J., Flik G., and Verburg-van Kemenade B.M.L. 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 (2006) 1519-1533
28. Imai E., Ishikawa J., Moritomo T., and Tomana M. Characterisation of T cell antigen receptor alpha chain isotypes in the common carp. Fish Shellfish Immunol. 19 (2005) 205-216
29. Irnazarow I. Genetic variability of Polish and Hungarian carp lines. Aquacult. Res. 129 (1995) 215-219
30. Kanellos T., Sylvester I.D., D'Mello F., Howard C.R., Mackie A., Dixon P.F., Chang K.C., Ramstad A., Midtlyng P.J., and Russell P.H. DNA vaccination can protect Cyprinus Carpio against spring viraemia of carp virus. Vaccine 24 (2006) 4927-4933
31. Kohlmann K., Gross R., Murakaeva A., and Kersten P. Genetic variability and structure of common carp (Cyprinus carpio) populations throughout the distribution range inferred from allozyme, microsatellite and mitochondrial DNA markers. Aquat. Living Res. 16 (2003) 421-431
32. Kolumam G.A., Thomas S., Thompson L.J., Sprent J., and Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202 (2005) 637-650
33. Koumans-van Diepen J.E., Egberts E., Peixoto B.R., Taverne N., and Rombout J.H.W.M. B cell and immunoglobulin heterogeneity in carp (Cyprinus carpio L.); An immuno(cyto)chemical study. Dev. Comp. Immunol. 19 (1995) 97-108
34. Koutna M., Vesely T., Psikal I., and Hulova J. Identification of spring viraemia of carp virus (SVCV) by combined RT-PCR and nested PCR. Dis. Aquat. Org. 55 (2003) 229-235
35. Mescher M.F., Curtsinger J.M., Agarwal P., Casey K.A., Gerner M., Hammerbeck C.D., Popescu F., and Xiao Z. Signals required for programming effector and memory development by CD8+ T cells. Immunol. Rev. 211 (2006) 81-92
36. Moody A.M., Chui D., Reche P.A., Priatel J.J., Marth J.D., and Reinherz E.L. Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell 107 (2001) 501-512
37. Moore L.J., Somamoto T., Lie K.K., Dijkstra J.M., and Hordvik I. Characterisation of salmon and trout CD8alpha and CD8beta. Mol. Immunol. 42 (2005) 1225-1234
38. Morales H.D., and Robert J. Characterization of primary and memory CD8 T-cell responses against ranavirus (FV3) in Xenopus laevis. J. Virol. 81 (2007) 2240-2248
39. Nakauchi H., Shinkai Y., and Okumura K. Molecular cloning of Lyt-3, a membrane glycoprotein marking a subset of mouse T lymphocytes: molecular homology to immunoglobulin and T-cell receptor variable and joining regions. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 4210-4214
40. Nascimento D.S., Vale A.d., Tomas A.M., Zou J., Secombes C.J., and dos Santos N.M.S. Cloning, promoter analysis and expression in response to bacterial exposure of sea bass (Dicentrarchus labrax L.) interleukin-12 p40 and p35 subunits. Mol. Immunol. 44 (2007) 2277-2291
41. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
42. Priatel J.J., Chui D., Hiraoka N., Simmons C.J., Richardson K.B., Page D.M., Fukuda M., Varki N.M., and Marth J.D. The ST3Gal-I sialyltransferase controls CD8+ T lymphocyte homeostasis by modulating O-glycan biosynthesis. Immunity 12 (2000) 273-283
43. Reed R.J., and Muench H. A simple method of estimating 50% endpoints. Am. J. Hyg. 27 (1938) 493-497
44. Renard V., Romero P., Vivier E., Malissen B., and Luescher I.F. CD8 beta increases CD8 coreceptor function and participation in TCR-ligand binding. J. Exp. Med. 184 (1996) 2439-2444
45. Ririe K.M., Rasmussen R.P., and Wittwer C.T. Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal. Biochem. 245 (1997) 154-160
46. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol. 20 (2006) 172-191
47. Sakano H., Huppi K., Heinrich G., and Tonegawa S. Sequences at the somatic recombination sites of immunoglobulin light-chain genes. Nature 280 (1979) 288-294
48. Schmidt C.S., and Mescher M.F. Peptide antigen priming of naive, but not memory, CD8 T cells requires a third signal that can be provided by IL-12. J. Immunol. 168 (2002) 5521-5529
49. Shaw A.S., Chalupny J., Whitney J.A., Hammond C., Amrein K.E., Kavathas P., Sefton B.M., and Rose J.K. Short related sequences in the cytoplasmic domains of CD4 and CD8 mediate binding to the amino-terminal domain of the p56lck tyrosine protein kinase. Mol. Cell. Biol. 10 (1990) 1853-1862
50. Somamoto T., Yoshiura Y., Nakanishi T., and Ototake M. Molecular cloning and characterization of two types of CD8alpha from ginbuna crucian carp, Carassius auratus langsdorfii. Dev. Comp. Immunol. 29 (2005) 693-702
51. Somamoto T., Yoshiura Y., Sato A., Nakao M., Nakanishi T., Okamoto N., and Ototake M. Expression profiles of TCRbeta and CD8alpha mRNA correlate with virus-specific cell-mediated cytotoxic activity in Ginbuna crucian carp. Virology 348 (2006) 370-377
52. Steinhagen D., Kruse P., and Körting W. The parasitemia of cloned Trypanoplasma borreli Laveran and Mesnil, 1901 in laboratory-infected common carp (Cyprinus carpio L.). J. Parasitol. 75 (1989) 685-689
53. Suetake H., Araki K., Akatsu K., Somamoto T., Dijkstra J.M., Yoshiura Y., Kikuchi K., and Suzuki Y. Gene organization and expression of CD8α and CD8β genes in fugu Takifugu rubripes. Fish Shellfish Immunol. 23 (2007) 1107-1118
54. Thai B.T., Burridge C.P., Pham T.A., and Austin C.M. Using mitochondrial nucleotide sequences to investigate diversity and genealogical relationships within common carp (Cyprinus carpio L.). Anim. Gen. 36 (2004) 23-28
55. Tichopad A., Dilger M., Schwarz G., and Pfaffl M.W. Standardized determination of real-time PCR efficiency from a single reaction set-up. Nucleic Acids Res. 31 (2003) e122
56. Utke K., Bergmann S., Lorenzen N., Kollner B., Ototake M., and Fischer U. Cell-mediated cytotoxicity in rainbow trout, Oncorhynchus mykiss, infected with viral haemorrhagic septicaemia virus. Fish Shellfish Immunol. 22 (2007) 182-196
57. van Den Broek M., Bachmann M.F., Kohler G., Barner M., Escher R., Zinkernagel R., and Kopf M. IL-4 and IL-10 antagonize IL-12-mediated protection against acute vaccinia virus infection with a limited role of IFN-gamma and nitric oxide synthetase 2. J. Immunol. 164 (2000) 371-378
58. van Erp S.H., Dixon B., Figueroa F., Egberts E., and Stet R.J.M. Identification and characterization of a new major histocompatibility complex class I gene in carp (Cyprinus carpio L.). Immunogenetics 44 (1996) 49-61
59. van Stipdonk M.J., Lemmens E.E., and Schoenberger S.P. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2 (2001) 423-429
60. Wiegertjes G.F., Forlenza M., Joerink M., and Scharsack J.P. Parasite infections revisited. Dev. Comp. Immunol. 29 (2005) 749-758
61. Witte T., Spoerl R., and Chang H.C. The CD8beta ectodomain contributes to the augmented coreceptor function of CD8alphabeta heterodimers relative to CD8alphaalpha homodimers. Cell Immunol. 191 (1999) 90-96
62. Wong J.S., Wang X., Witte T., Nie L., Carvou N., Kern P., and Chang H.C. Stalk region of beta-chain enhances the coreceptor function of CD8. J. Immunol. 171 (2003) 867-874
63. Yoshiura Y., Kiryu I., Fujiwara A., Suetake H., Suzuki Y., Nakanishi T., and Ototake M. Identification and characterization of Fugu orthologues of mammalian interleukin-12 subunits. Immunogenetics 55 (2003) 296-306
64. Zamoyska R. The CD8 coreceptor revisited: one chain good, two chains better. Immunity 1 (1994) 243-246
65. Zamoyska R., Basson A., Filby A., Legname G., Lovatt M., and Seddon B. The influence of the src-family kinases, Lck and Fyn, on T cell differentiation, survival and activation. Immunol. Rev. 191 (2003) 107-118
66. Zhou J.F., Wu Q.J., Ye Y.Z., and Tong J.G. Genetic devergence between Cyprinus carpio carpio and Cyprinus carpio haematopterus as assessed by mitochondrial DNA analysis, with enphasis on origin of European domestic carp. Genetica 119 (2003) 93-97