Cloning, characterization, and expression pattern of Atlantic halibut (Hippoglossus hippoglossus L.) CD4-2, Lck, and ZAP-70

Fish and Shellfish Immunology

Volumn 29, Issue 6, 2010, Pages 987-997

  Øvergård, Aina Cathrine ^a,b   Nerland, Audun Helge ^a,b   Patel, Sonal ^a  

^a INSTITUTE OF MARINE RESEARCH   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

70 kDa zeta associated protein; Lymphocyte cell specific kinase; T cell; Teleost

Indexed keywords

HIPPOGLOSSUS HIPPOGLOSSUS; MAMMALIA; TELEOSTEI;

EID: 77957754188     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2010.08.011     Document Type: Article

References (79)

1. Øvergård A.C., Hordvik I., Nerland A.H., Eikeland G., Patel S. Cloning and expression analysis of Atlantic halibut (Hippoglossus hippoglossus) CD3 genes. Fish Shellfish Immunol 2009, 27:707-713.
2. Patel S., Øvergård A.C., Nerland A.H. CD8α and CD8β in Atlantic halibut, Hippoglossus hippoglossus: cloning, characterization and gene expression during viral and bacterial infection. Fish Shellfish Immunol 2008, 25:570-580.
3. Patel S., Øvergård A.C., Nerland A.H. A CD4 homologue in Atlantic halibut (Hippoglossus hippoglossus): molecular cloning and characterisation. Fish Shellfish Immunol 2009, 26:377-384.
4. Dijkstra J.M., Somamoto T., Moore L., Hordvik I., Ototake M., Fischer U. Identification and characterization of a second CD4-like gene in teleost fish. Mol Immunol 2006, 43:410-419.
5. Edholm E.S., Stafford J.L., Quiniou S.M., Waldbieser G., Miller N.W., Bengten E., et al. Channel catfish, Ictalurus punctatus, CD4-like molecules. Dev Comp Immunol 2007, 31:172-187.
6. Laing K.J., Zou J.J., Purcell M.K., Phillips R., Secombes C.J., Hansen J.D. Evolution of the CD4 family: teleost fish possess two divergent forms of CD4 in addition to lymphocyte activation gene-3. J Immunol 2006, 177:3939-3951.
7. Moore L.J., Dijkstra J.M., Koppang E.O., Hordvik I. CD4 homologues in Atlantic salmon. Fish Shellfish Immunol 2009, 26:10-18.
8. Suetake H., Araki K., Suzuki Y. Cloning, expression, and characterization of fugu CD4, the first ectothermic animal CD4. Immunogenetics 2004, 56:368-374.
9. Buonocore F., Randelli E., Casani D., Guerra L., Picchietti S., Costantini S., et al. A CD4 homologue in sea bass (Dicentrarchus labrax): molecular characterization and structural analysis. Mol Immunol 2008, 45:3168-3177.
10. Sun X.F., Shang N., Hu W., Wang Y.P., Guo Q.L. Molecular cloning and characterization of carp (Cyprinus carpio L.) CD8β and CD4-like genes. Fish Shellfish Immunol 2007, 23:1242-1255.
11. Triebel F., Jitsukawa S., Baixeras E., Roman-Roman S., Genevee C., Viegas-Pequignot E., et al. LAG-3, a novel lymphocyte activation gene closely related to CD4. J Exp Med 1990, 171:1393-1405.
12. Brenner S., Venkatesh B., Yap W.H., Chou C.F., Tay A., Ponniah S., et al. Conserved regulation of the lymphocyte-specific expression of lck in the Fugu and mammals. Proc Natl Acad Sci 2002, 99:2936-2941.
13. Laing K.J., Dutton S., Hansen J.D. Molecular and biochemical analysis of rainbow trout LCK suggests a conserved mechanism for T-cell signaling in gnathostomes. Mol Immunol 2007, 44:2737-2748.
14. Langenau D.M., Ferrando A.A., Traver D., Kutok J.L., Hezel J.P., Kanki J.P., et al. In vivo tracking of T cell development, ablation, and engraftment in transgenic zebrafish. Proc Natl Acad Sci 2004, 101:7369-7374.
15. Christie T.L., Carter A., Rollins E.L., Childs S.J. Syk and Zap-70 function redundantly to promote angioblast migration. Dev Biol 2010, 340:22-29.
16. Patel S., Malde K., Lanzen A., Olsen R.H., Nerland A.H. Identification of immune related genes in Atlantic halibut (Hippoglossus hippoglossus L.) following in vivo antigenic and in vitro mitogenic stimulation. Fish Shellfish Immunol 2009, 27:729-738.
17. Radonic A., Thulke S., Mackay I.M., Landt O., Siegert W., Nitsche A. Guideline to reference gene selection for quantitative real-time PCR. Biochem Biophys Res Commun 2004, 313:856-862.
18. Øvergård A.C., Nerland A.H., Patel S. Evaluation of potential reference genes for real time RT-PCR studies in Atlantic halibut (Hippoglossus Hippoglossus L.); during development, in tissues of healthy and NNV-injected fish, and in anterior kidney leucocytes. BMC Mol Biol 2010, 11:36.
19. -DDCT Method. Methods 2001, 25:402-408.
20. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
21. Kim P.W., Sun Z.Y., Blacklow S.C., Wagner G., Eck M.J. A zinc clasp structure tethers Lck to T cell coreceptors CD4 and CD8. Science 2003, 301:1725-1728.
22. lck to CD4 and CD8alpha. J Biol Chem 1998, 273:32878-32882.
23. Yurchak L.K., Sefton B.M. Palmitoylation of either Cys-3 or Cys-5 is required for the biological activity of the Lck tyrosine protein kinase. Mol Cell Biol 1995, 15:6914-6922.
24. Yasuda K., Kosugi A., Hayashi F., Saitoh S., Nagafuku M., Mori Y., et al. Serine 6 of Lck tyrosine kinase: a critical site for Lck myristoylation, membrane localization, and function in T lymphocytes. J Immunol 2000, 165:3226-3231.
25. Kabouridis P.S., Magee A.I., Ley S.C. S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. Embo J 1997, 16:4983-4998.
26. Chan A.C., Dalton M., Johnson R., Kong G.H., Wang T., Thoma R., et al. Activation of ZAP-70 kinase activity by phosphorylation of tyrosine 493 is required for lymphocyte antigen receptor function. EMBO J 1995, 14:2499-2508.
27. Wange R.L., Guitian R., Isakov N., Watts J.D., Aebersold R., Samelson L.E. Activating and inhibitory mutations in adjacent tyrosines in the kinase domain of ZAP-70. J Biol Chem 1995, 270:18730-18733.
28. Kong G., Dalton M., Bubeck Wardenburg J., Straus D., Kurosaki T., Chan A.C. Distinct tyrosine phosphorylation sites in ZAP-70 mediate activation and negative regulation of antigen receptor function. Mol Cell Biol 1996, 16:5026-5035.
29. Zeitlmann L., Knorr T., Knoll M., Romeo C., Sirim P., Kolanus W. T cell activation induced by novel gain-of-function mutants of Syk and ZAP-70. J Biol Chem 1998, 273:15445-15452.
30. Di Bartolo V., Mege D., Germain V., Pelosi M., Dufour E., Michel F., et al. Tyrosine 319, a newly identified phosphorylation site of ZAP-70, plays a critical role in T cell antigen receptor signaling. J Biol Chem 1999, 274:6285-6294.
31. Di Bartolo V., Malissen M., Dufour E., Sechet E., Malissen B., Acuto O. Tyrosine 315 determines optimal recruitment of ZAP-70 to the T cell antigen receptor. Eur J Immunol 2002, 32:568-575.
32. Pacini S., Ulivieri C., Di Somma M.M., Isacchi A., Lanfrancone L., Pelicci P.G., et al. Tyrosine 474 of ZAP-70 is required for association with the Shc adaptor and for T-cell antigen receptor-dependent gene activation. J Biol Chem 1998, 273:20487-20493.
33. Pancer Z., Mayer W.E., Klein J., Cooper M.D. Prototypic T cell receptor and CD4-like coreceptor are expressed by lymphocytes in the agnathan sea lamprey. Proc Natl Acad Sci 2004, 101:13273-13278.
34. Wang J.H., Meijers R., Xiong Y., Liu J.H., Sakihama T., Zhang R., et al. Crystal structure of the human CD4 N-terminal two-domain fragment complexed to a class II MHC molecule. Proc Natl Acad Sci 2001, 98:10799-10804.
35. Ioerger T.R., Du C., Linthicum D.S. Conservation of cys-cys-trp structural triads and their geometry in the protein domains of immunoglobulin superfamily members. Mol Immunol 1999, 36:373-386.
36. Maddon P.J., Molineaux S.M., Maddon D.E., Zimmerman K.A., Godfrey M., Alt F.W., et al. Structure and expression of the human and mouse T4 genes. Proc Natl Acad Sci 1987, 84:9155-9159.
37. Maekawa A., Schmidt B., Fazekas de St Groth B., Sanejouand Y.H., Hogg P.J. Evidence for a domain-swapped CD4 dimer as the coreceptor for binding to class II MHC. J Immunol 2006, 176:6873-6878.
38. Moldovan M.C., Yachou A., Levesque K., Wu H., Hendrickson W.A., Cohen E.A., et al. CD4 dimers constitute the functional component required for T cell activation. J Immunol 2002, 169:6261-6268.
39. Moldovan M.C., Sabbagh L., Breton G., Sekaly R.P., Krummel M.F. Triggering of T cell activation via CD4 dimers. J Immunol 2006, 176:5438-5445.
40. Crise B., Rose J.K. Identification of palmitoylation sites on Cd4, the human-immunodeficiency-virus receptor. J Biol Chem 1992, 267:13593-13597.
41. Fragoso R., Ren D.J., Zhang X.P., Su M.W.C., Burakoff S.J., Jin Y.J. Lipid raft distribution of CD4 depends on its palmitoylation and association with Lck, and evidence for CD4-induced lipid raft aggregation as an additional mechanism to enhance CD3 signaling. J Immunol 2003, 170:913-921.
42. Pitcher C., Honing S., Fingerhut A., Bowers K., Marsh M. Cluster of differentiation antigen 4 (CD4) endocytosis and adaptor complex binding require activation of the CD4 endocytosis signal by serine phosphorylation. Mol Biol Cell 1999, 10:677-691.
43. Koskinen R., Lamminmaki U., Tregaskes C.A., Salomonsen J., Young J.R., Vainio O. Cloning and modeling of the first nonmammalian CD4. J Immunol 1999, 162:4115-4121.
44. Moore L.J., Somamoto T., Lie K.K., Dijkstra J.M., Hordvik I. Characterisation of salmon and trout CD8α and CD8β Mol Immunol 2005, 42:1225-1234.
45. Bergman M., Mustelin T., Oetken C., Partanen J., Flint N.A., Amrein K.E., et al. The human p50csk tyrosine kinase phosphorylates p56lck at Tyr-505 and down regulates its catalytic activity. EMBO J 1992, 11:2919-2924.
46. Mustelin T., Coggeshall K.M., Altman A. Rapid activation of the T-cell tyrosine protein kinase pp56lck by the CD45 phosphotyrosine phosphatase. Proc Natl Acad Sci 1989, 86:6302-6306.
47. Ostergaard H.L., Shackelford D.A., Hurley T.R., Johnson P., Hyman R., Sefton B.M., et al. Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc Natl Acad Sci 1989, 86:8959-8963.
48. Mustelin T., Altman A. Dephosphorylation and activation of the T cell tyrosine kinase pp56lck by the leukocyte common antigen (CD45). Oncogene 1990, 5:809-813.
49. Xu W., Harrison S.C., Eck M.J. Three-dimensional structure of the tyrosine kinase c-Src. Nature 1997, 385:595-602.
50. Veillette A., Fournel M. The CD4 associated tyrosine protein kinase p56lck is positively regulated through its site of autophosphorylation. Oncogene 1990, 5:1455-1462.
51. Watts J.D., Sanghera J.S., Pelech S.L., Aebersold R. Phosphorylation of serine 59 of p56lck in activated T cells. J Biol Chem 1993, 268:23275-23282.
52. Winkler D.G., Park I., Kim T., Payne N.S., Walsh C.T., Strominger J.L., et al. Phosphorylation of Ser-42 and Ser-59 in the N-terminal region of the tyrosine kinase p56lck. Proc Natl Acad Sci 1993, 90:5176-5180.
53. lck in human peripheral blood T lymphocytes is dependent on co- stimulation through accessory receptors: involvement of phospholipase C, protein kinase C and MAP-kinases in vivo. Eur J Immunol 2000, 30:635-643.
54. Park I., Chung J., Walsh C.T., Yun Y., Strominger J.L., Shin J. Phosphotyrosine-independent binding of a 62-kDa protein to the src homology 2 (SH2) domain of p56lck and its regulation by phosphorylation of Ser-59 in the lck unique N-terminal region. Proc Natl Acad Sci 1995, 92:12338-12342.
55. Chan A.C., Iwashima M., Turck C.W., Weiss A. ZAP-70: a 70 kd protein-tyrosine kinase that associates with the TCR zeta chain. Cell 1992, 71:649-662.
56. Iwashima M., Irving B.A., van Oers N.S., Chan A.C., Weiss A. Sequential interactions of the TCR with two distinct cytoplasmic tyrosine kinases. Science 1994, 263:1136-1139.
57. Alabyev B.Y., Guselnikov S.V., Najakshin A.M., Mechetina L.V., Taranin A.V. CD3ε homologues in the chondrostean fish Acipenser ruthenus. Immunogenetics 2000, 51:1012-1020.
58. Araki K., Suetake H., Kikuchi K., Suzuki Y. Characterization and expression analysis of CD3ε and CD3γ/δ in fugu, Takifugu rubripes. Immunogenetics 2005, 57:158-163.
59. Liu Y., Moore L., Olaf Koppang E., Hordvik I. Characterization of the CD3ζ, CD3γδ and CD3ε subunits of the T cell receptor complex in Atlantic salmon. Dev Comp Immunol 2008, 32:26-35.
60. Park C.I., Hirono I., Aoki T. Molecular characterization of the Japanese flounder, Paralichthys olivaceus, CD3epsilon and evolution of the CD3 cluster. Dev Comp Immunol 2005, 29:123-133.
61. Park C.I., Hirono I., Enomoto J., Nam B.H., Aoki T. Cloning of Japanese flounder Paralichthys olivaceus CD3 cDNA and gene, and analysis of its expression. Immunogenetics 2001, 53:130-135.
62. Shang N., Sun X.F., Hu W., Wang Y.P., Guo Q.L. Molecular cloning and characterization of common carp (Cyprinus carpio L.) TCRγ and CD3γ/δ chains. Fish Shellfish Immunol 2008, 24:412-425.
63. Guselnikov S.V., Najakshin A.M., Taranin A.V. Fugu rubripes possesses genes for the entire set of the ITAM-bearing transmembrane signal subunits. Immunogenetics 2003, 55:472-479.
64. Neumeister E.N., Zhu Y., Richard S., Terhorst C., Chan A.C., Shaw A.S. Binding of ZAP-70 to phosphorylated T-cell receptor zeta and eta enhances its autophosphorylation and generates specific binding sites for SH2 domain-containing proteins. Mol Cell Biol 1995, 15:3171-3178.
65. Bubeck Wardenburg J., Fu C., Jackman J.K., Flotow H., Wilkinson S.E., Williams D.H., et al. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J Biol Chem 1996, 271:19641-19644.
66. Zhang W., Sloan-Lancaster J., Kitchen J., Trible R.P., Samelson L.E. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 1998, 92:83-92.
67. Caron L., Abraham N., Pawson T., Veillette A. Structural requirements for enhancement of T-cell responsiveness by the lymphocyte-specific tyrosine protein kinase p56lck. Mol Cell Biol 1992, 12:2720-2729.
68. Duplay P., Thome M., Herve F., Acuto O. p56lck interacts via its src homology 2 domain with the ZAP-70 kinase. J Exp Med 1994, 179:1163-1172.
69. Pelosi M., Di Bartolo V., Mounier V., Mege D., Pascussi J.M., Dufour E., et al. Tyrosine 319 in the interdomain B of ZAP-70 is a binding site for the Src homology 2 domain of Lck. J Biol Chem 1999, 274:14229-14237.
70. Williams B.L., Irvin B.J., Sutor S.L., Chini C.C., Yacyshyn E., Bubeck Wardenburg J., et al. Phosphorylation of Tyr319 in ZAP-70 is required for T-cell antigen receptor-dependent phospholipase C-gamma1 and Ras activation. EMBO J 1832-44, 1999:18.
71. Wu J., Zhao Q., Kurosaki T., Weiss A. The Vav binding site (Y315) in ZAP-70 is critical for antigen receptor-mediated signal transduction. J Exp Med 1997, 185:1877-1882.
72. 319 phosphorylation: a potential role for tyrosine phosphatases. J Immunol 2002, 168:4420-4429.
73. Lupher M.L., Songyang Z., Shoelson S.E., Cantley L.C., Band H. The Cbl phosphotyrosine-binding domain selects a D(N/D)XpY motif and binds to the Tyr292 negative regulatory phosphorylation site of ZAP-70. J Biol Chem 1997, 272:33140-33144.
74. Watts J.D., Affolter M., Krebs D.L., Wange R.L., Samelson L.E., Aebersold R. Identification by electrospray ionization mass spectrometry of the sites of tyrosine phosphorylation induced in activated Jurkat T cells on the protein tyrosine kinase ZAP-70. J Biol Chem 1994, 269:29520-29529.
75. Hansen J.D., Zapata A.G. Lymphocyte development in fish and amphibians. Immunol Rev 1998, 166:199-220.
76. van Oers N.S., Weiss A. The Syk/ZAP-70 protein tyrosine kinase connection to antigen receptor signalling processes. Semin Immunol 1995, 7:227-236.
77. Chan A.C., van Oers N.S., Tran A., Turka L., Law C.L., Ryan J.C., et al. Differential expression of ZAP-70 and Syk protein tyrosine kinases, and the role of this family of protein tyrosine kinases in TCR signaling. J Immunol 1994, 152:4758-4766.
78. Law C.L., Sidorenko S.P., Chandran K.A., Draves K.E., Chan A.C., Weiss A., et al. Molecular cloning of human Syk. A B cell protein-tyrosine kinase associated with the surface immunoglobulin M-B cell receptor complex. J Biol Chem 1994, 269:12310-12319.
79. Patel S., Sørhus E., Fiksdal I.U., Espedal P.G., Bergh Ø, Rødseth O.M., et al. Ontogeny of lymphoid organs and development of IgM-bearing cells in Atlantic halibut (Hippoglossus hippoglossus L.). Fish Shellfish Immunol 2009, 26:385-395.