Molecular cloning, differential expression and 3D structural analysis of the MHC class-II β chain from sea bass (Dicentrarchus labrax L.)

Fish and Shellfish Immunology

Volumn 23, Issue 4, 2007, Pages 853-866

  Buonocore, Francesco ^a   Randelli, Elisa ^a   Casani, Daniela ^a   Costantini, Susan ^c   Facchiano, Angelo ^c   Scapigliati, Giuseppe ^a   Stet, Renè J M ^b  

^a UNIVERSITY OF TUSCIA   (Italy)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c CNR   (Italy)

Author keywords

3D structure; chain; Cloning; Dicentrarchus labrax; Expression analysis; Major histocompatibility complex class (MHC) II ; Polymorphism; Quantitative PCR; Sea bass

Indexed keywords

BACTERIA (MICROORGANISMS); DICENTRARCHUS LABRAX; MAMMALIA; SERRANIDAE; TELEOSTEI; VERTEBRATA;

EID: 34547592518     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2007.03.013     Document Type: Article

References (74)

1. Auffray C., and Strominger J.L. Molecular genetics of the human major histocompatibility complex. Adv Hum Genet 15 (1986) 197-247
2. Lanzavecchia A. Receptor mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. Annu Rev Immunol 8 (1990) 773-793
3. Konig R., Huang L.-Y., and Germain R.N. MHC class II interaction with CD4 mediated by a region analogous to the MHC class binding site. Nature 356 (1992) 796-798
4. Brodsky F.M., and Guagliardi L.E. The cell biology of antigen processing and presentation. Ann Rev Immunol 9 (1991) 707-744
5. k in complex with a dominant epitope of lysozyme. Immunity 8 (1998) 305-317
6. d-peptide complexes reveal that high affinity can be achieved without large anchor residues. Immunity 8 (1998) 319-329
7. McFarland B.J., Katz J.F., Sant A.J., and Beeson C. Energetics and cooperativity of the hydrogen bonding and anchor interactions that bind peptides to MHC class II protein. J Mol Biol 350 (2005) 170-183
8. Stet R.J.M., Kruiswijk C.P., and Dixon B. Major histocompatibility lineages and immune gene function in teleost fishes: the road not taken. Crit Rev Immunol 23 (2003) 441-471
9. Sato A., Figueroa F., Murray B.W., Malaga-Trillo E., Zaleska-Rutczynska Z., Sultmann H., et al. Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51 (2000) 108-116
10. Walker R.B., McConnell T.J., and Walker R.A. Variability in a MHC Mosa class II beta chain-encoding gene in striped bass (Morone saxatilis). Dev Comp Immunol 18 (1994) 325-342
11. Chen S.-L., Zhang Y.-X., Xu M.-Y., Ji X.-S., Yu G.-C., and Dong C.-F. Molecular polymorphism and expression analysis of MHC class II B gene from red sea bream (Chrysophrys major). Dev Comp Immunol 30 (2006) 407-418
12. Figueroa F., Mayer W.E., Sultmann H., O'hUigin C., Tichy H., Satta Y., et al. MHC class II B gene evolution in East African cichlid fishes. Immunogenetics 51 (2000) 556-575
13. Miller K.M., and Withler R.E. Sequence analysis of a polymorphic MHC class II gene in Pacific salmon. Immunogenetics 43 (1996) 337-351
14. Ristow S.S., Grabowski L.D., Thompson S.M., Warr G.W., Kaattari S.L., de Avila J.M., et al. Coding sequences of the MHC II β chain of homozygous rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 23 (1999) 51-60
15. Stet R.J.M., de Vries B., Mudde K., Hermsen T., van Heerwaarden J., Shump B.P., et al. 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 (2002) 320-331
16. Sultmann H., Mayer W.E., Figueroa F., O'hUigin C., and Klein J. Zebrafish MHC class II α chain-encoding genes: polymorphism, expression, and function. Immunogenetics 38 (1993) 408-420
17. Dixon B., Nagelkerke L.A.J., Sibbing F.A., Egberts E., and Stet R.J.M. Evolution of MHC class II β chain-encoding genes in the Lake Tana barbell species flock (Barbus intermedius complex). Immunogenetics 44 (1996) 419-431
18. Graser R., O'hUigin C., Vincek V., Meyer A., and Klein J. Trans-species polymorphism of class II MHC loci in danio fishes. Immunogenetics 44 (1996) 36-48
19. van Erp S.H.M., Egberts E., and Stet R.J.M. Characterization of major histocompatibility complex class II A and B genes in a gynogenetic carp clone. Immunogenetics 44 (1996) 192-202
20. Stet R.J.M., Kruiswijk C.P., Saeij J.P.J., and Wiegertjes G.F. Major histocompatibility genes in cyprinid fishes: theory and practice. Immunol Rev 166 (1998) 301-316
21. Grimholt U., Larsen S., Nordmo R., Midtlyng P., Kjoeglum S., Storset A., et al. MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55 (2003) 210-219
22. Kurtz J., Kalbe M., Aeschlimann P.B., Haberli M.A., Wegner K.M., Reusch T.B., et al. Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc Biol Sci 271 (2004) 197-204
23. Koppang E.O., Lundin M., McL P., Ronningen K., and Lie O. Differing levels of Mhc class II β chain expression in a range of tissues from vaccinated and non-vaccinated Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 8 (1998) 183-196
24. Park K.C., Osborne J.A., Tsoi S.C., Brown L.L., and Johnson S.C. Expressed sequence tags analysis of Atlantic halibut (Hippoglossus hippoglossus) liver, kidney and spleen tissues following vaccination against Vibrio anguillarum and Aeromonas salmonicida. Fish Shellfish Immunol 18 (2005) 393-415
25. Tafalla C., Coll J., and Secombes C.J. Expression of genes related to the early immune response in rainbow trout (Oncorhynchus mykiss) after viral haemorrhagic septicemia virus (VHSV) infection. Dev Comp Immunol 29 (2005) 615-626
26. (+) cells in the gills of Atlantic salmon (Salmo salar L.) affected by amoebic gill disease. Vet Immunol Immunopathol 109 (2006) 297-303
27. Wegner K.M., Kalbe M., Rauch G., Kurtz J., Schaschl H., and Reusch T.B. Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15 (2006) 1153-1164
28. Hill A.V., Allsopp C.E.M., Kwiatkowski D., Anstey N.M., Twumasi P., Rowe P.A., et al. Common West African HLA antigens are associated with protection from severe malaria. Nature 352 (1991) 595-600
29. Hofmann A., Plachy J., Hunt L., Kaufman J., and Hala K. v-src oncogene-specific carboxy-terminal peptide is immunoprotective against Rous sarcoma growth in chickens with MHC class I allele B-F12. Vaccine 21 (2003) 4694-4699
30. Venkatesh B., Ning Y., and Brenner S. Late changes in spliceosomal introns define clades in vertebrate evolution. Proc Natl Acad Sci USA 96 (1999) 10267-10271
31. Scapigliati G., Buonocore F., Bird S., Zou J., Pelegrin P., Falasca C., et al. Phylogeny of cytokines: molecular cloning and expression analysis of sea bass Dicentrarchus labrax interleukin-1 beta. Fish Shellfish Immunol 11 (2001) 711-726
32. Pearson W.R., and Lipman D.J. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85 (1988) 2444-2448
33. Altschul S.F., Gish W., Miller W., Myers E., and Lipman D.J. Best local alignment search tool. J Mol Biol 215 (1990) 403-410
34. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5 (2004) 150-163
35. Nielsen H., Engelbrecht J., Brunak S., and von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10 (1997) 1-6
36. Julenius K., Molgaard A., Gupta R., and Brunak S. Prediction, conservation analysis and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15 (2005) 153-164
37. Brudno M., Chapman M., Gottgens B., Batzoglou S., and Morgenstern B. Fast and sensitive multiple alignment of large genomic sequences. BMC Bioinformatics 4 (2003) 66-77
38. Buonocore F., Mazzini M., Forlenza M., Randelli E., Secombes C.J., Zou J., et al. Expression in Escherichia coli and purification of sea bass (Dicentrarchus labrax) interleukin-1β, a possible immuno-adjuvant in aquaculture. Marine Biotech 6 (2004) 53-59
39. Buonocore F., Forlenza M., Randelli E., Benedetti S., Bossù P., Meloni S., et al. Biological activity of sea bass (Dicentrarchus labrax) recombinant interleukin-1β. Marine Biotech 7 (2005) 609-617
40. Facchiano A.M., Stiuso P., Chiusano M.L., Caraglia M., Giuberti G., Marra M., et al. Homology modelling of the human eukaryotic initiation factor 5A (eIF-5A). Protein Eng 14 (2001) 881-890
41. Marabotti A., D'Auria S., Rossi M., and Facchiano A.M. Theoretical model of the three-dimensional structure of a sugar binding protein from Pyrococcus horikoshii: structural analysis and sugar binding simulations. Biochem J 280 (2004) 677-684
42. Scapigliati G., Costantini S., Colonna G., Facchiano A., Buonocore F., Bossù P., et al. Modelling of fish interleukin 1 and its receptor. Dev Comp Immunol 28 (2004) 429-441
43. Costantini S., Colonna G., Rossi M., and Facchiano A.M. Modelling of HLA-DQ2 and simulations of its interaction with gluten peptides to explain molecular recognition in celiac disease. J Mol Graph Model 23 (2005) 419-431
44. Buonocore F., Randelli E., Bird S., Secombes C.J., Costantini S., Facchiano A., et al. The CD8alpha from sea bass (Dicentrarchus labrax L.): cloning, expression and 3D modelling. Fish Shellfish Immunol 20 (2006) 637-646
45. Wallner B., and Elofsson A. All are not equal: a benchmark of different homology modelling programs. Protein Sci 14 (2005) 1315-1327
46. Reinherz E.L., Tan K., Tang L., Kern P., Liu J., Xiong Y., et al. The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science 286 (1999) 1913-1921
47. 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 USA 98 (2001) 10799-10804
48. Thompson J.D., Higgins D.G., Gibson T.J., and Clustal W. improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 (1994) 4673-4680
49. Sali A., and Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234 (1993) 779-815
50. Laskowski R.A., MacArthur M.W., and Moss D.S. Thornton JM PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26 (1993) 283-291
51. Sippl M.J. Recognition of errors in three-dimensional structures of proteins. Proteins 17 (1993) 355-362
52. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
53. Orengo C.A., Michie A.D., Jones S., Jones D.T., Swindells M.B., and Thornton J.M. CATH - a hierarchic classification of protein domain structures. Structure 5 (1997) 1093-1108
54. Jones S., and Thornton J.M. Principles of protein-protein interactions derived from structural studies. Proc Natl Acad Sci USA 93 (1996) 13-20
55. Hubbard S.J., Campbell S.F., and Thornton J.M. Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. J Mol Biol 220 (1991) 507-530
56. Klein J. Natural history of the major histocompatibility complex (1986), John Wiley, New York
57. Brown J.H., Jardetzky T.S., Gorga J.C., Stern L.J., Urban R.G., Strominger J.L., et al. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364 (1993) 33-39
58. Godwin U.B., Antao A., Wilson M.R., Chinchar G., Miller N.W., Clem W., et al. MHC class II B genes in the channel catfish (Ictalurus punctatus). Dev Comp Immunol 21 (1997) 13-23
59. van Lierop M.-J.C., Knight J., Secombes C.J., Hermsen T.T., Groeneveld A., and Stet J.M. Production and characterisation of an antiserum raised against recombinant rainbow trout (Oncorhynchus mykiss) MHC class II beta-chain (MhcOnmy-DAB). Fish Shellfish Immunol 8 (1998) 231-243
60. Nath S., Kales S., Fujiki K., and Dixon B. Major histocompatibility class II genes in rainbow trout (Oncorhynchus mykiss) exhibit temperature dependent downregulation. Immunogenetics 58 (2006) 443-453
61. Hong S., Zou J., Crampe M., Peddie S., Scapigliati G., Bols N., et al. The production and bioactivity of rainbow trout (Oncorhynchus mykiss) recombinant IL-1β. Vet Immunol Immunopathol 81 (2001) 1-14
62. Sommer S. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2 (2005) 16
63. Cosson P., and Bonifacino J.S. Role of the transmembrane domain interactions in the assembly of class II MHC molecules. Science 258 (1992) 659-662
64. Morris D.J., Adams A., and Richards R.H. In situ hybridisation identifies the gill as a portal of entry for PKK (Phylum Myxozoa), the causative agent of proliferative kidney disease in salmonids. Parasitol Res 86 (2000) 950-956
65. Ramsay E., Falk K., Mikalsen A.B., and Teig A. Xenoma formation during microsporidial gill disease of salmonids caused by Loma salmonae is affected by host species (Oncorhynchus tshawytscha, O. kisutch, O. mykiss) but not by salinity. Dis Aquat Org 48 (2002) 125-131
66. Morrison R.N., Koppang E.O., Hordvik I., and Nowak B.F. MHC class II+ cells in the gills of the Atlantic salmon (Salmo salar L.) affected by amoebic gill disease. Vet Immunol Immunopathol (2006) 297-303
67. Abelli L., Picchietti S., Romano N., Mastrolia L., and Scapigliati G. Immunohistochemistry of gut-associated lymphoid tissue of the sea bass Dicentrarchus labrax (L.). Fish Shellfish Immunol 7 (1997) 235-246
68. Dinarello C.A. The interleukin-1 family: 10 years of discovery. Fed Am Soc Exp Biol 8 (1994) 1314-1325
69. Koppang E.O., Dannevig B.H., Lie O., Ronningen K., and Press C.M. Expression of the MHC class I and II mRNA in a macrophage-like cell line (SHK-1) derived from Atlantic salmon, Salmo salar, head kidney. Fish Shellfish Immunol 9 (1999) 473-489
70. 2 modulation of gene expression in an Atlantic salmon (Salmo salar) macrophage-like cell line (SHK-1). Dev Comp Immunol 29 (2005) 951-963
71. Hansen J.D., and La Patra S. Induction of the rainbow trout MHC class I pathway during acute IHNV infection. Immunogenetics 54 (2002) 654-661
72. 2, or glucocorticoids. Scand J Immunol 32 (1990) 601-609
73. Rohn W., Tang L.P., Dong W., and Benveniste E.T. IL-1β inhibits IFN-γ-induced class II MHC expression by suppressing transcription of the class II transactivator gene. J Immunol 162 (1999) 886-896
74. Coronel A., Boyer A., Franssen J.D., Romet-Lemonne J.L., Fridman W.H., and Teillaud J.L. Cytokine production and T-cell activation by macrophage-dendritic cells generated for therapeutic use. Br J Haematol 114 (2001) 671-680