Immunoglobulin in fish - Genes, expression and structure

Fish and Shellfish Immunology

Volumn 6, Issue 4, 1996, Pages 243-262

  Pilström, Lars ^a   Bengtén, Eva ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Fish; Genes; Immunoglobulin

Indexed keywords

EID: 0030140654     PISSN: 10504648     EISSN: None     Source Type: Journal    
DOI: 10.1006/fsim.1996.0026     Document Type: Article

References (113)

1. Abbas, A. K., Lichtman, A. H. & Pbober, J. S. (1994). Cellular and Molecular Immunology. Philadelphia: W. B. Saunders.
2. Acton, R. T., Weinheimer, P. F., Dupree, H. K., Russell, T. R., Wolcott, M., Evans, E. E., Schrohenloher, R. E. & Bennett, J. C. (1971a). Isolation and characterization of the immune macroglobulin from the padddlefish, Polydon spathula. Journal of Biological Chemistry 246, 6760-6769.
3. Acton, R. T., Weinheimer, P. F., Hall, S. J., Niedermeier, W., Shelton, E. & Bennett, J. C. (1971b). Tetrameric Immune Macroglobulins in Three Orders of Bony Fish. Proceedings of the National Academy of Sciences, USA 68, 107-111.
4. Amemiya, C. T. & Litman, G. W. (1990). Complete nucleotide sequence of an immunoglobulin heavy-chain gene and analysis of immunoglobulin gene organization in a primitive teleost species. Proceedings of the National Academy of Sciences, USA 87, 811-815.
5. Amemiya, C. T., Ohta, Y., Litman, R. T., Rast, J. P., Haire, R. N. & Litman, G. W. (1993). Gene organization in a relict species, the coelacanth Latimeria chalumnae: evolutionary implications. Proceedings of the National Academy of Sciences, USA 90, 6661-6665.
6. Anderson, M., Amemiya, C., Luer, C., Litman, R., Rast, J., Niimura, Y. & Litman, G. (1994). Complete genomic sequence and patterns of transcription of a member of an unusual family of closely related, chromosomally dispersed Ig gene clusters in Raja. International Immunology 6, 1661-1670.
7. Andersson, E. & Matsunaga, T. (1995). Evolution of immunoglobulin heavy chain variable region genes: a VH family can last for 150-200 million years or longer. Immunogenetics 41, 18-28.
8. Andersson, E., Törmänen, V. & Matsunaga, T. (1991). Evolution of a VH gene family in low vertebrates. International Immunology 3, 527-533.
9. Bengtén, E. (1994). The immunoglobulin genes in Atlantic cod (Gadus morhua) and rainbow trout (Oncorhynchus mykiss). Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, vol. 19. Sweden: Uppsala University.
10. Bengtén, E., Leanderson, T. & Pilström, L. (1991). Immunoglobulin heavy chain cDNA from the teleost Atlantic cod (Gadus morhua L.): nucleotide sequences of secretory and membrane form show an unusual splicing pattern. European Journal of Immunology 21, 3027-3033.
11. Bengtén, E., Strömberg, S. & Pilström, L. (1994). Immunoglobulin VH regions in Atlantic cod (Gadus morhua L.): their diversity and relationship to VH families from other species. Developmental and Comparative Immunology 18, 109-122.
12. Blomberg, B. B., Rudin, C. M. & Storb, U. (1991). Identification and localization of an enhancer for the human λ L chain Ig gene complex. Journal of Immunology 147, 2354-2358.
13. Bradshaw, C. M., Clem, L. W. & Sigel, M. M. (1971). Immunologic and immunochemical studies of the gar, Lepisosteus platyrhincus. II. Purification and characterization of immunoglobulin. Journal of Immunology 106, 1480-1487.
14. Carlsson, L., Övermo, C. & Holmberg, D. (1992). Developmentally controlled selection of antibody genes: characterisation of individual VH7183 genes and evidence for stage-specific somatic diversification. European Journal of Immunology 22, 71-78.
15. Clem, L. W. (1971). Phylogeny of immunoglobulin structure and function. IV. Immunoglobulins of the giant grouper, Epinephelus itaira. Journal of Biological Chemistry 246, 9-15.
16. Clem, L. W. & McLean, W. E. (1975). Phylogeny of immunoglobulin structure and function. VII. Monomeric and tetrameric immunoglobulins of the margate, a marine teleost. Immunology 29, 791-799.
17. Clerx, J. P. M., Castel, A., Bol, J. F. & Gerwig, G. J. (1980). Isolation and characterization of the immunoglobulin of pike (Esox lucius L.). Veterinary Immunology and Immunopathology 1, 125-144.
18. Daggfeldt, A., Bengtén, E. & Pilström, L. (1993). A cluster type organization of the loci of the immunoglobulin light chain in Atlantic cod (Gadus morhua L.) and rainbow trout (Oncorhynchus mykiss Walbaum) indicated by nucleotide sequences of cDNA and hybridization analysis. Immunogenetics 38, 199-209.
19. Du Pasquier, L. (1982). Antibody diversity in lower vertebrates - why is it so restricted? (Review article). Nature 296, 311-313.
20. Du Pasquier, L., Schwager, J. & Flajnik, M. F. (1989). The immune system of Xenopus. Annual Review of Immunology 7, 251-275.
21. Elcombe, B. M., Chang, R. J., Taves, C. J. & Winkelhake, J. L. (1985). Evolution of antibody structure and effector functions: Comparative hemolytic activities of monomeric and tetrameric IgM from rainbow trout, Salmo gairdneri. Comparative Biochemistry and Physiology 80B, 697-706.
22. Estévez, J., Leiro, J., Sanmartin, M. L. & Umbeira, F. M. (1993). Isolation and partial characterization of turbot (Scophthalmus maximus) immunoglobulins. Comparative Biochemistry and Physiology 105A, 275-281.
23. Estévez, J., Leiro, J., Santamarina, M. T., Dominguez, J. & Ubeira, F. M. (1994). Monoclonal antibodies to turbot (Scophthalmus maximus) immunoglobulins: characterization and applicability in immunoassays. Veterinary Immunology and Immunopathology 41, 353-366.
24. Falkner, F. G. & Zachau, H. G. (1984). Correct transcription of an immunoglobulin κ gene requires an upstream fragment containing conserved sequence elements. Nature 310, 71-74.
25. Fletcher, T. C. & Grant, P. T. (1969). Immunoglobulins in serum and mucus of the plaice (Pleuronectes platessa). Biochemical Journal 115, 65 pp.
26. Ghaffari, S. H. & Lobb, C. J. (1991). Heavy chain variable region gene families evolved early in phylogeny. Ig complexity in fish. Journal of Immunology 146, 1037-1046.
27. Ghaffari, S. H. & Lobb, C. J. (1992). Organization of immunoglobulin heavy chain constant and joining region genes in the channel catfish. Molecular Immunology 29, 151-159.
28. Ghaffari, S. H. & Lobb, C. J. (1993). Structure and genomic organization of immunoglobulin light chain in the channel catfish. An unusual genomic organizational pattern of segmental genes. Journal of Immunology 151, 6900-6912.
29. Grandien, A., Coutinho, A., Andersson, J. & Freitas, A. A. (1991). Endogenous VH gene family expression in immunoglobulin-transgenic mice: evidence for selection of antibody repertoires. International Immunology 3, 67-73.
30. Greenberg, A. S., Steiner, L., Kasahara, M. & Flajnik, M. F. (1993). Isolation of a shark immunoglobulin light chain cDNA clone encoding a protein resembling mammalian κ light chains: Implications for the evolution of light chains. Proceedings of the National Academy of Sciences, USA 90, 10603-10607.
31. Greenberg, A. S., Avila, D., Hughes, M., Hughes, A., McKinney, E. C. & Flajnik, M. F. (1995). A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 374, 168-173.
32. Grey, H. M., Abel, C. A., Yount, W. J. & Kunkel, H. G. (1968). A subclass of human gamma-A-globulins (gamma A-2) which lacks the disulfide bonds linking heavy and light chains. Journal of Experimental Medicine 128, 1223-1236.
33. Hadji-Azimi, I. & Michea-Hamzehpor, M. (1976). Xenopus laevis 19S immunoglobulin. Ultrastructure and J chain isolation. Immunology 30, 587-591.
34. Harding, F. A., Amemiya, C. T., Litman, R. T., Cohen, N. & Litman, G. W. (1990a). Two distinct immunoglobulin heavy chain isotypes in a primitive, cartilaginous fish, Raja erinacea. Nucleic Acids Research 18, 6369-6376.
35. Harding, F. A., Cohen, N. & Litman, G. W. (1990b). Immunoglobulin heavy chain gene organization and complexity in the skate, Raja erinacea. Nucleic Acids Research 18, 1015-1020.
36. Hayman, J. R., Ghaffari, S. H. & Lobb, C. J. (1993). Heavy chain joining region segments of the channel catfish. Journal of Immunology 151, 3587-3596.
37. Hinds, K. R. & Litman, G. W. (1986). Major reorganization of immunoglobulin VH-segmental elements during vertebrate evolution. Nature 320, 546-549.
38. Hinds-Frey, K. R., Nishikata, H., Litman, R. T. & Litman, G. W. (1993). Somatic variation precedes extensive diversification of germline sequences and combinatorial joining in the evolution of immunoglobulin heavy chain diversity. Journal of Experimental Medicine 178, 815-824.
39. Hohman, V. S., Schluter, S. F. & Marchalonis, J. J. (1992). Complete sequence of a cDNA clone specifying sandbar shark immunoglobulin light chain: gene organization and implications for the evolution of light chains. Proceedings of the National Academy of Sciences, USA 89, 276-280.
40. Hohman, V. S., Schuchman, D. B., Schluter, S. F. & Marchalonis, J. J. (1993). Genomic clone for sandbar shark λ light chain: Generation of diversity in the absence of gene rearrangement. Proceedings of the National Academy of Sciences, USA 90, 9882-9886.
41. Hole, N. J. K., Harindranath, N., Young-Cooper, G. O., Garcia, R. & Mage, R. G. (1991). Identification of enhancer sequences 3′ of the rabbit Ig κL chain loci. Journal of Immunology 146, 4377-4384.
42. Hordvik, I., Voie, A. M., Glette, J., Male, R. & Endresen, C. (1992). Cloning and sequence analysis of two isotypic IgM heavy chain genes from Atlantic salmon, Salmo salar, L. European Journal of Immunology 22, 2957-2962.
43. Hsu, E. & Steiner, L. A. (1992). Primary structure of immunoglobulins through evolution. Current Opinion in Structural Biology 2, 422-431.
44. Håverstein, L. S., Aasjord, P. M., Ness, S. & Endresen, C. (1988). Purification and partial characterization of an IgM-like serum immunoglobulin from Atlantic salmon (Salmo salar). Developmental and Comparative Immunology 12, 773-785.
45. Höchtl, J., Müller, C. R. & Zachau, H. G. (1982). Recombined flanks of the variable and joining segments of immunoglobulin genes. Proceedings of the National Academy of Sciences, USA 79, 1383-1387.
46. Kabat, E. A., Wu, T. T., Perry, H. M., Gottesman, K. S. & Foeller, C. (1991). Sequences of proteins of immunological interest. U.S. Department of Health and Human Services, Public Health Service, National Institute of Health.
47. Knight, K. L. (1992). Restricted VH usage and generation of antibody diversity in rabbit. Annual Review of Immunology 10, 593-616.
48. Kobayashi, K. & Tomonaga, S. (1988). The second immunoglobulin class is commonly present in cartilaginous fish belonging to the order Rajiformes. Molecular Immunology 25, 115-120.
49. Kobayashi, K., Tomonaga, S. & Kajii, T. (1984). A second class of immunoglobulin other than IgM present in the serum of a cartilaginous fish, the skate Raja kenojei: isolation and characterization. Molecular Immunology 21, 397-404.
50. Kobayashi, K., Tomonaga, S. & Tanaka, S. (1992). Identification of a second immunoglobulin in the most primitive shark, the frill shark, Chlamydoselachus anguineus. Developmental and Comparative Immunology 16, 295-299.
51. Kokubu, F., Hinds, K., Litman, R., Shamblott, M. J. & Litman, G. W. (1988a). Complete structure and organization of immunoglobulin heavy chain constant region genes in a phylogenetically primitive vertebrate. The EMBO Journal 7, 1979-1988.
52. Kokubu, F., Litman, R., Shamblott, M. J., Hinds, K. & Litman, G. W. (1988b). Diverse organisation of immunoglobulin VH gene loci in a primitive vertebrate. The EMBO Journal 7, 3413-3422.
53. Lafaille, J. J., DeCloux, A., Bonneville, M., Takagaki, Y. & Tonegawa, S. (1989). Junctional sequences of T cell receptor γδ genes: Implications for γδ T cell linages and for novel intermediate of V-(D)-J joining. Cell 59, 859-870.
54. Landau, N. R., Schatz, D. G., Rosa, M. & Baltimore, D. (1987). Increased frequency of N-region insertion in a murine pre-B-cell line infected with terminal deoxynucleotidyl transferase retroviral expression vector. Molecular and Cellular Biology 7, 3237-3243.
55. Ledford, B. E., Magor, B. G., Middleton, D. L., Miller, R. L., Wilson, M. R., Miller, N. W., Clem, L. W. & Warr, G. W. (1993). Expression of a mouse-channel catfish chimeric IgM molecule in a mouse myeloma cell. Molecular Immunology 30, 1405-1417.
56. Lee, M. A., Bengtén, E., Daggfeldt, A., Rytting, A.-s. & Pilström, L. (1993). Characterization of rainbow trout cDNAs encoding a secreted and membrane-bound Ig heavy chain and the genomic intron upstream of the first constant exon. Molecular Immunology 30, 641-648.
57. Litman, G. W., Frommel, D., Finstad, J. & Good, R. A. (1971). The evolution of the immune response: IX. Immunoglobulins of the bowfin: purification and characterization. Journal of Immunology 106, 747-754.
58. Litman, G. W., Haire, R. N., Hinds, K. R., Amemiya, C. T., Rast, J. P. & Hulst, M. (1992). Evolutonary Development of the B-Cell Repertoire. Annals New York Academy of Science 351, 360-368.
59. Litman, G. W., Rast, J. P., Hulst, M. A., Litman, R. T., Shamblott, M. J., Haire, R. N., Hinds-Frey, K. R., Buell, R. D., Margittai, M., Ohta, Y., Zilch, A. C., Good, R. A. & Amemiya, C. T. (1992). Evolutionary origins of immunoglobulin gene diversity. Progress in Immunology VIII, 107-114.
60. Litman, G. W., Rast, J. P., Shamblott, M. J., Haire, R. N., Hulst, M., Roess, W., Litman, R., Hinds-Frey, K. R., Zilch, A. & Amemiya, C. T. (1993). Phylogenetic diversification of immunoglobulin genes and antibody repertoire. Molecular Biology Evolution 10, 60-72.
61. Lobb, C. J. & Clem, L. W. (1981). Phylogeny of immunoglobulin structure and function - X. Humoral immunoglobulins of the sheephead, Archosargus probatocephalus. Developmental and Comparative Immunology 5, 271-282.
62. Lobb, C. J. & Clem, L. W. (1983). Distinctive subpopulations of catfish serum antibody and immunoglobulin. Molecular Immunology 20, 811-818.
63. Lobb, C. J., Olson, M. O. & Clem, L. W. (1984). Immunoglobulin light chain classes in a teleost fish. Journal of Immunology 132, 1917-1923.
64. Magor, B. G., Wilson, M. R., Miller, N. W., Clem, L. W., Middleton, D. L. & Warr, G. W. (1994a). An Ig heavy chain enhancer of the channel catfish Ictalurus punctatus: evolutionary conservation of function but not structure. Journal of Immunology 153, 5556-5563.
65. Magor, K. E., Higgins, D. A., Middleton, D. L. & Warr, G. W. (1994b). One gene encodes the heavy chain for three different forms of IgY in the duck. Journal of Immunology 153, 5549-5555.
66. Marchalonis, J. J. (1969). Isolation and characterization of immunoglobulin-like proteins of the Australian lungfish (Neoceratodus forsteri). Australian Journal of Experimental Biology and Medical Sciences 47, 405-419.
67. Marchalonis, J. J. (1971). Isolation and partial characterization of immunoglobulins of goldfish (Carassius auratus) and carp (Cyprinus carpio). Immunology 20, 161-173.
68. Marchalonis, J. J., Hohman, V. S. & Schluter, S. F. (1993). Antibodies of sharks. Novel methods of generation diversity. The Immunologist 1, 115-120.
69. Matsuda, F., Shin, E. K., Nagaoka, H., Matsumura, R., Haino, M., Fukida, Y., Taka-ishi, S., Imai, T., Riley, J. H., Anand, R., Soeda, E. & Honjo, T. (1993). Structure and physical map of 64 variable segments in the 3′ 0·8-megabase region of the human immunoglobulin heavy-chain locus. Nature Genetics 3, 88-94.
70. Matsunaga, T., Chen, T. & Törmänen, V. (1990). Characterization of a complete immunoglobulin heavy-chain variable region germline gene of rainbow trout. Proceedings of the National Academy of Sciences, USA 87, 7767-7771.
71. Max, E. (1993). Immunoglobulins - molecular genetics. In Fundamental Immunology (W. E. Paul, ed.) pp. 315-382. New York: Raven Press.
72. McCormack, W. T., Carlson, L. M., Tjoelker, L. W. & Thompson, C. B. (1989). Evolutionary comparison of the avian IgL locus: combinatorial diversity plays a role in the generation of the antibody repertoire in some avian species. International Immunology 1, 332-341.
73. Michard-Vanhée, C., Chourrout, D., Strömberg, S., Thuvander, A. & Pilström, L. (1994). Lymphocyte expression in transgenic trout by mouse immunoglobulin promoter/enhancer. Immunogenetics 40, 1-8.
74. Mikoryak, C. A. & Steiner, L. A. (1984). Noncovalent association of heavy and light chains in Rana catesbeiana immunoglobulins. Journal of Immunology 133, 376-383.
75. Miller, N. W., Rycyzyn, M. A., Wilson, M. R., Warr, G. W., Naftel, J. P. & Clem, L. W. (1994). Development and characterization of channel catfish long term B cell lines. Journal of Immunology 152, 2180-2189.
76. Navarro, V., Quesada, J. A., Abad, M. E., Taverne, N. & Rombout, J. H. W. M. (1993). Immuno(cyto)chemical characterization of monoclonal antibodies to giltheaded seabream (Spartus aurata) immunoglobulin. Fish & Shellfish Immunology 3, 167-177.
77. Nelson, G. (1989). Phylogeny of major fish groups. In The Hierarchy of Life. Molecules and Morphology in Phylogenetic Analysis (B. Fernholm, K. Bremer & H. Jörnvall, eds), pp. 325-336. Amsterdam: Elsevier Science Publishers B.V.
78. Parslow, T., Blair, D., Murphy, W. & Granner, D. (1984). Structure of the 5′ ends of the immunoglobulin genes: a novel conserved sequence. Proceedings of the National Academy of Sciences, USA 81, 2650-2654.
79. Partula, S. & Charlemagne, J. (1993). Characterization of serum immunoglobulins in a chondrostean fish, Acipenser baeri. Developmental and Comparative Immunology 17, 515-524.
80. Pilström, L. & Petersson, A. (1991). Isolation and partial characterization of immunoglobulin from cod (Gadus morhua L.). Developmental and Comparative Immunology 15, 143-152.
81. Pollara, B., Suran, A., Finstad, J. & Good, R. A. (1968). N-terminal amino acid sequences of immunoglobulin chains in Polyodon spathula. Proceedings of the National Academy of Sciences, USA 59, 1307-1312.
82. Rast, J. P., Anderson, M. K., Ota, T., Litman, R. T., Margittai, M., Shamblott, M. J. & Litman, G. W. (1994). Immunoglobulin light chain class multiplicity and alternative organizational forms in early vertebrate phylogeny. Immunogenetics 40, 83-99.
83. Reynaud, C.-A., Dahan, A., Anques, V. & Weill, J.-C. (1989). Development of the chicken antibody repertoire. In Immunoglobulin Genes. (T. Honjo, F. W. Alt & T. H. Rabbitts, eds), pp. 151-162. London: Academic Press.
84. Richter, R. & Ambrosius, H. (1972). Beiträge zur Immunbiologie poikilithermer Wirbeltiere. VIII. Ein hochmolekulares Immunglobulin des Flussbarsches (Perca fluviatilis L.). Acta Biologica et Medica, Germanica 26, 309-318.
85. Richter, R., Frenzel, E.-M., Hädge, D., Kopperschläger, G. & Ambrosius, H. (1973). Strukturelle und Immunchemische Untersuchungen am Immunoglobulin des Karpfens (Cyprinus carpio L.). I. Analyse am Gesamtmolkül. Acta Biologica et Medica Germanica 30, 735-749.
86. Roman, T. & Charlemagne, J. (1994). The immunoglobulin repertoire of the rainbow trout (Oncorhynchus mykiss): definition of nine Igh-V families. Immunogenetics 40, 210-216.
87. Roman, T., De Guerra, A. & Charlemagne, J. (1995). Evolution of specific antigen recognition: size reduction and restricted length distribution of the CDRH3 regions in the rainbow trout. European Journal of Immunology 25, 269-273.
88. Roth, M. G., Nakajima, P. B., Menetski, J. P., Bosma, M. J. & Gellert, M. (1992). V(D)J recombination in mouse thymocytes: double-strand breaks near T cell delta rearrangement signals. Cell 69, 41-53.
89. Russell, W. J., Voss, E. W. & Sigel, M. M. (1970). Some characteristics of anti-dinitrophenyl antibody of the gray snapper. Journal of Immunology 105, 262-264.
90. Shamblott, M. J. & Litman, G. W. (1989a). Complete nucleotide sequence of primitive vertebrate immunoglobulin light chain genes. Proceedings of the National Academy of Sciences, USA 86, 4684-4688.
91. Shamblott, M. J. & Litman, G. W. (1989b). Genomic organization and sequences of immunoglobulin light chain genes in a primitive vertebrate suggest coevolution of immunoglobulin gene organization. The EMBO Journal 8, 3733-3739.
92. Shelton, E. & Smith, M. (1970). The ultrastructure of carp (Cyprinus carpio) immunoglobulin: a tetrameric macroglobulin. Journal of Molecular Biology 54, 615-617.
93. Staudt, L. M. & Lenardo, M. J. (1991). Immunoglobulin gene transcription. Annual Review of Immunology 9, 373-398.
94. Trump, G. N. (1970). Goldfish immunoglobulins and antibodies to bovine serum albumin. Journal of Immunology 104, 1267-1275.
95. Turner, M. & Owen, M. (1993). Antigen receptor molecules. In Immunology (I. M. Roitt, J. Brostoff & D. K. Male, eds), pp. 4.1-4.20. London: Mosby-Year Book Europe Ltd.
96. Tutter, A. Brodeur, P., Shlomchik, M. & Riblet, R. (1991). Structure, map position, and evolution of two newly diverged mouse Ig VH gene families. Journal of Immunology 147, 3215-3223.
97. Tutter, A. & Riblet, R. (1989). Conservation of an immunoglobulin variable-region family indicate a specific, noncoding function. Proceedings of the National Academy of Sciences, USA 86, 7460-7464.
98. van der Heijden, M. H. T., Rooijakkers, J. B. M. A., Booms, G. H. R., Rombout, J. H. W. M. & Boon, J. H. (1995). Production, characterization and applicability of monoclonal antibodies to European eel (Anguilla anguilla L., 1758) immunoglobulin. Veterinary Immunology and Immunopathology 45, 151-164.
99. van Dijk, K. W., Motari, F., Kirkham, P. M., Schroeder Jr, H. W. & Milner, E. C. B. (1993). The human immunoglobulin VH7 gene family consists of a small polymorphic group of six to eight gene segments dispersed throughout the VH locus. European Journal of Immunology 23, 832-839.
100. Ventura-Holman, T., Cay Jones, J., Ghaffari, S. H. & Lobb, C. J. (1994). Structure and genomic organisation of VH gene segments in the channel catfish: Members of different VH gene families are interspersed and closely linked. Molecular Immunology 31, 823-832.
101. Vilain, C., Wetzel, M.-C., Du Pasquier, L. & Charlemagne, J. (1984). Structural and functional analysis of spontaneous anti-nitrophenyl antibodies in three cyprinid species: carp (Cyprinus carpio), goldfish (Carassius auratus) and tench (Tinca tinca). Developmental and Comparative Immunology 8, 611-622.
102. Voss, E. W., Groberg, W. J. & Fryer, J. L. (1978). Binding affinity of tetrameric coho salmon Ig anti-hapten antibodies. Immunochemistry 15, 459-464.
103. Warr, G. W. (1983). Immunoglobulin of the toadfish, Spheroides glaber. Comparative Biochemistry and Physiology 76B, 507-514.
104. Warr, G. W. (1995). The immunoglobulin genes of fish. Developmental and Comparative Immunology 19, 1-12.
105. Warr, G. W., Middleton, D. L., Miller, N. W., Clem, L. W. & Wilson, M. R. (1991). An additional family of VH sequences in the channel catfish. European Journal of Immunogenetics 18, 393-397.
106. Whittington, R. J. (1993). Purification and partial characterisation of serum immunoglobulin of the European perch (Perca fluviatilis L.). Fish & Shellfish Immunology 3, 331-343.
107. Wiersma, E. J. & Shulman, M. J. (1995). Assembly of IgM. Role of disulfide bonding and noncovalent interaction. Journal of Immunology 154, 5265-5272.
108. Wilson, M., Hsu,, E., Marcuz, A., Courtet, M., Du Pasquier, L. & Steinberg, C. (1992). What limits affinity maturation of antibodies in Xenopus - the rate of somatic mutation or the ability to select mutants? The EMBO Journal 11, 4337-4347.
109. Wilson, M. R., Marcus, A., vanGinkel, F., Miller, N. W., Clem, L. W., Middleton, D. & Warr, G. W. (1990). The immunoglobulin M heavy chain constant region gene of the channel catfish, Ictalurus punctatus: an unusual mRNA splice pattern produces the membrane form of the molecule. Nucleic Acids Research 18, 5227-5233.
110. Wilson, M. R., Middleton, D. & Warr, G. W. (1991). Immunoglobulin VH genes of the goldfish, Carassius auratus: a reexamination. Molecular Immunology 28, 449-457.
111. Wilson, M. R., Ross, D. A., Miller, N. W., Clem, L. W., Middleton, D. L. & Warr, G. W. (1995). Alternative pre-mRNA processing pathways in the production of membrane IgM heavy chains in holostean fish. Developmental and Comparative Immunology 19, 165-177.
112. Wilson, M. R. & Warr, G. W. (1992). Fish immunoglobulins and the genes that encode them. (A review). Annual Review of Fish Diseases 2, 201-221.
113. Xu B. & Selsing, E. (1994). Analysis of sequence transfers resembling gene conversion in a mouse antibody transgene. Science 265, 1590-1593.