The immune system of sharks, skates, and rays

Biology of Sharks and Their Relatives

Volumn , Issue , 2004, Pages 369-396

  Luer, Carl A ^a   Walsh, Catherine J ^a   Bodine, Ashby B ^b  

^a CENTER FOR SHARK RESEARCH   (United States)

^b CLEMSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

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EID: 78751534611     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (144)

1. Aguilar, L.K., E. Aguilar-Cordova, J. Cartwright, Jr., and J.W. Belmont. 1994. Thymic nurse cells are sites of thymocyte apoptosis. J. Immunol. 152:2645-2651.
2. Anderson, M., C. Amemiya, C. Luer, R. Litman, J. Rast, Y. Niimura, and G. Litman. 1994. Complete genomic sequence and patterns of transcription of a member of an unusual family of closely related, chromosomally dispersed immunoglobulin gene clusters in Raja. Int. Immunol. 6:1661-1670.
3. Anderson, M., M.J. Shamblott, R.T. Litman, and G.W. Litman. 1995. The generation of immunoglobulin light chain diversity in Raja erinacea is not associated with somatic rearrangement, an exception to a central paradigm of B cell immunity. J. Exp. Med. 181:109-119.
4. Anderson, M., S.J. Strong, R.T. Litman, C.A. Luer, C.T. Amemiya, J.P Rast, and G.W. Litman. 1999. A long form of the skate IgX gene exhibits a striking resemblance to the new shark IgW and IgNARC genes. Immunogenetics 49:56-67.
5. Anderson, M., X. Sun, A.L. Miracle, G.W. Litman, and E.V. Rothenberg. 2001. Evolution of hematopoiesis: Three members of the PU.1 transcription factor family in a cartilaginous fish, Raja eglanteria. Proc. Natl. Acad. Sci. U.S.A.98:553-558.
6. Andrew, W. and C.P Hickman. 1974. Circulatory systems, in Histology of the Vertebrates - A Comparative Text C.6. Mosby, St. Louis, MO, 133-165.
7. Bartl, S. 2001. New major histocompatibility complex class IIB genes from nurse shark. Adv. Exp. Med. Biol 484:1-11.
8. Bartl, S. and I.L. Weissman. 1994. Isolation and characterization of major histocompatibility complex class IIB genes from the nurse shark. Proc. Natl. Acad. Sci. U.S.A 91:262-266.
9. Bartl, S., M.A. Baish, M.F. Flajnik, and Y. Ohta. 1997. Identification of class I genes in cartilaginous fish, the most ancient group of vertebrates displaying an adaptive immune response. J. Immunol. 159:6097-6104.
10. Baur, H., S. Kasperek, and E. Pfaff. 1975. Criteria of viability of isolated liver cells. Hoppe-Seylers Z. Physiol. Chem. 356:827-838.
11. Bernstein, R.M., S.F. Schluter, S. Shen, and J.J. Marchalonis. 1996a. A new high molecular weight immunoglobulin class from the carcharhine shark: implications for the properties of the primordial immunoglobulin. Proc. Natl. Acad. Sci. U.S.A. 93:3289-3293.
12. Bernstein, R.M., S.F. Schluter, H. Bernstein, and J.J. Marchalonis. 1996b. Primordial emergence of the recombination activating gene 1 (RAG 1): sequence of the complete shark gene indicates homology to microbial integrases. Proc. Natl. Acad. Sci. U.S.A. 93:9454-9459.
13. Bird, S., T. Wang, J. Zou, C. Cunningham, and C.J. Secombes. 2002a. The first cytokine sequence within cartilaginous fish: IL-1 beta in the small spotted catshark (Scyliorhinus canicula). J. Immunol. 168:3329-3340.
14. Bird, S., J. Zou, T.B. Wang, B. Munday, C. Cunningham, and C.J. Secombes. 2002b. Evolution of interleukin- 1 beta. Cytokine Growth Factor Rev. 13:483-502.
15. Blaxhall, PC. and K.W. Daisley. 1973. Routine hematological methods for use with fish blood. J. Fish Biol. 5:771-782.
16. Borysenko, M. and W.H. Hildemann. 1970. Reactions to skin allografts in the horn shark, Heterodontus francisci. Transplantation 10:545-551.
17. 6-(1-iminoethyl)lysine. Biochemistry 37:4844-4852.
18. Campos-Perez, J.J., M. Ward, PS. Grabowski, A.E. Ellis, and C.J. Secombes. 2000. The gills are an important site of iNOS expression in rainbow trout Oncorhynchus mykiss after challenge with the gram-positive pathogen Renibacterium salmoninarum. Immunology 99:153-161.
19. Chiba, A., M. Torroba, Y. Honma, and A.G. Zapata. 1988. Occurrence of lymphohaemopoietic tissue in the meninges of the stingray Dasyatis akajei (Elasmobranchii, chondrichthyes). Am. J. Anat 183:268-276.
20. Clem, L.W. and PA. Small, Jr. 1967. Phylogeny of immunoglobulin structure and function. I. Immunoglobulins of the lemon shark. J. Exp. Med. 125:893-920.
21. Clem, L.W., F. DeBoutaud, and M.M. Sigel. 1967. Phylogeny of immunoglobulin structure and function. II. Immunoglobulins of the nurse shark. J. Immunol. 99:1226-1235.
22. Cohen, J.J., R.C. Duke, V.A. Fadok, and K.S. Sellins. 1992. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10:267-293.
23. Compton, M.M., PS. Gibbs, and L.R. Swicegood. 1990. Glucocorticoid-mediated activation of DNA degradation in avian lymphocytes. Gen. Comp. Endocrinol. 80:68-79.
24. Culbreath, L., S.L. Smith, and S.D. Obenauf. 1991. Alternative complement pathway activity in nurse shark serum. Am. Zool 31:131A.
25. Czop, J.K. and J. Kay. 1991. Isolation and characterization of ß-glucan receptors on human mononuclear phagocytes. J. Exp. Med. 173:1511-1520.
26. De Koning, J. and S.L. Kaattari. 1992. Use of homologous salmonid plasma for the improved responsiveness of salmonid leukocyte cultures, in Techniques in Fish Immunology; 2. J. S. Stolen et al., Eds., SOS Publications, Fair Haven, NJ, 61-65.
27. De Waal Malefijt, R., W. Leene, PJ.M. Roholl, J. Wormmeester, and K.A. Hoeben. 1986. T cell differentiation within thymic nurse cells. Lab. Invest. 55:25-34.
28. Dijkman, H.B.PM., S. Mentzel, A.S. DeJohng, and K.J.M. Assmann. 1995. RNA in situ hybridization using digoxigenin-labeled cRNA probes. Biochemica 2:23-27.
29. Dodds, A.W., S.L. Smith, R.P Levine, and A.C. Willis. 1998. Isolation and initial characterization of complement components C3 and C4 of the nurse shark and the channel catfish. Dev. Comp. Immunol 22:207-216.
30. Ducoroy, P, M. Lesourd, M.R. Padros, and A. Tournefier. 1999. Natural and induced apoptosis during lymphocyte development in the axolotl. Dev. Comp. Immunol 23:241-252.
31. Egami, N., H. Mitani, Y. Shimada, J. Suzuki, Y. Akimoto, N. Onizuka, A. Kanamori, A. Shimada, S. Amemeya, and T. Satao. 1984. A note of the acute radiation death of sharks. J. Fac. Sci. Univ. Tokyo 15:363-365.
32. Ellis, A.E. 1977. The leucocytes of fish: a review. J. Fish Biol. 11:453-491.
33. Ellis, A.E. and R.M.E. Parkhouse. 1975. Surface immunoglobulins on the lymphocytes of the skate Raja naevus. Eur. J. Immunol. 5:726-728.
34. Ellsaesser, C.F., N.W. Miller, and M.A. Cuchens. 1985. Analysis of channel catfish peripheral blood leukocytes by bright-field microscopy and flow cytometry. Trans. Am. Fish. Soc 114:279-285.
35. Fänge, R. 1987. Lymphomyeloid system and blood cell morphology in elasmobranchs. Arch. Biol. 98:187-208.
36. Fänge, R. and A. Mattisson. 1981. The lymphomyeloid (hemopoietic) system of the Atlantic nurse shark, Ginglymostoma cirratum. Biol. Bull. 160:240-249.
37. Fänge, R. and A. Pulsford. 1983. Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L. Cell Tissue Res. 230:337-351.
38. Fesus, L. 1992. Apoptosis. Immunol. Today 13:A16-A17.
39. Flajnik, M.F. and L.L. Rumfelt. 2000. The immune system of cartilaginous fish. Curr. Top. Microbiol. Immunol. 248:249-270.
40. Fowlkes, B.J. and D.M. Pardoll. 1989. Molecular and cellular events of T cell development. Adv. Immunol. 44:207-264.
41. Greenberg, A.S., D. Avila, M. Hughes, A. Hughes, E.C. McKinney, and M.F. Flajnik. 1995. A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 374:168-173.
42. Greenberg, A.S., A.L. Hughes, J. Guo, D. Avila, E.C. McKinney, and M.F. Flajnik. 1996. A novel “chimeric” antibody class in cartilaginous fish: IgM may not be the primordial immunoglobulin. Eur. J. Immunol. 26:1123-1129.
43. Greenhalgh, P and L.A. Steiner. 1995. Recombination activating gene 1 (Rag1) in zebrafish and shark. Immunogenetics 41:54-55.
44. Haire, R.N., A.L. Miracle, J.P Rast, and G.W. Litman. 2000. Members of the Ikaros gene family are present in early representative vertebrates. J. Immunol.165:306-312.
45. Harding, F.A., N. Cohen, and G.W. Litman. 1990a. Immunoglobulin heavy chain gene organization and complexity in the skate, Raja erinacea, Nucleic Acids Res 18:1015-1020.
46. Harding, F.A., C.T. Amemiya, R.T. Litman, N. Cohen, and G.W. Litman. 1990b. Two distinct immunoglobulin heavy chain isotypes in a primitive, cartilaginous fish, Raja erinacea, Nucleic Acids Res 18:6369-6376.
47. Hart, S., A.B. Wrathmell, J.E. Harris, and T.H. Grayson. 1988. Gut immunology in fish: a review. Dev. Comp. Immunol 12:453-480.
48. Hashimoto, K., T. Nakanishi, and Y. Kurosawa. 1992. Identification of a shark sequence resembling the major histocompatibility complex class I a3 domain. Proc. Natl. Acad. Sci. U.S.A. 89:2209-2212.
49. Hawke, N.A., J.P Rast, and G.W. Litman. 1996. Extensive diversity of transcribed TCR-ß in a phylogenetically primitive vertebrate. J. Immunol. 156:2458-2464.
50. Haynes, L. and E.C. McKinney. 1991. Shark spontaneous cytotoxicity: characterization of the regulatory cell. Dev. Comp. Immunol 15:123-134.
51. Haynes, L., L. Fuller, and E.C. McKinney. 1988. Fc receptor for shark immunoglobulin. Dev. Comp. Immunol 12:561-571.
52. Hiemstra, PS. 1993. Role of neutrophils and mononuclear phagocytes in host defense and inflammation. J. Int. Fed. Clin. Chem. 5:94-99.
53. H segmental elements during vertebrate evolution. Nature 320:546-549.
54. Hinds-Frey, K.R., H. Nishikata, R.T. Litman, and G.W. Litman. 1993. Somatic variation precedes extensive diversification of germline sequences and combinatorial joining in the evolution of immunoglobulin heavy chain diversity. J. Exp. Med. 178:825-834.
55. Hine, PM. and J.M. Wain. 1987. The enzyme cytochemistry and composition of elasmobranch granulocytes. J. Fish Biol. 30:465-476.
56. Hohman, V.S., S.F. Schluter, and J.J. Marchalonis. 1992. Complete sequence of a cDNA clone specifying sandbar shark immunoglobulin light chain: gene organization and implications for the evolution of light chains. Proc. Natl. Acad. Sci. U.S.A. 89:276-280.
57. Hohman, V. S., D.B. Schuchman, S.F. Schluter, and J.J. Marchalonis. 1993. Genomic clone for the sandbar shark lambda light chain: generation of diversity in the absence of gene rearrangement. Proc. Natl. Acad. Sci. U.S.A.90:9882-9886.
58. Honma, Y., K. Okabe, and A. Chiba. 1984. Comparative histology of the Leydig and epigonal organs in some elasmobranchs. Jpn. J. Ichthyol. 31:47-54.
59. Hyder, S.L., M.L. Cayer, and C.L. Pettey. 1983. Cell types in peripheral blood of the nurse shark: an approach to structure and function. Tissue Cell 15:437-455.
60. Janeway, C.A., P. Travers, and M. Walport. 1999. The complement system in humoral immunity, in Immunobiology: The Immune System in Health and Disease Garland, New York, 339-359.
61. Jensen, J.A., E. Festa, D.S. Smith, and M. Cayer. 1981. The complement system of the nurse shark: hemolytic and comparative aspects. Science 214:566-569.
62. Kasahara, M., M. Vazquez, K. Sato, E.C. McKinney, and M.F. Flajnik. 1992. Evolution of the major histocompatibility complex: Isolation of class II a cDNA clones from the cartilaginous fish. Proc. Natl. Acad. Sci. U.S.A.89:6688-6692.
63. Kasahara, M., E.C. McKinney, M.F. Flajnik, and T. Ishibashi. 1993. The evolutionary origin of the major histocompatibility complex: polymorphism of class II a chain genes in the cartilaginous fish. Eur. J. Immunol 23:2160-2165.
64. Kobayashi, K. and S. Tomonaga. 1988. The second immunoglobulin class is commonly present in cartilaginous fish belonging to the order Rajiformes. Mol. Immunol. 25:115-120.
65. Kobayashi, K., S. Tomonaga, and T. Kajii. 1984. A second class of immunoglobulin other than IgM present in the serum of a cartilaginous fish, the skate, Raja kenojei: isolation and characterization. Mol. Immunol. 21:397-404.
66. Kobayashi, K., S. Tomonaga, K. Teshima, and T. Kajii. 1985. Ontogenic studies on the appearance of two classes of immunoglobulin-forming cells in the spleen of the Aleutian skate, Bathyraja aleutica, a cartilaginous fish. Eur. J. Immunol. 15:952-956.
67. Kobayashi, K., S. Tomonaga, and S. Tanaka. 1992. Identification of a second immunoglobulin in the most primitive shark, the frill shark, Chlamydoselachus anguineus. Dev. Comp. Immunol 16:295-299.
68. Kokubu, F., K. Hinds, R. Litman, M.J. Shamblott, and G.W. Litman. 1987. Extensive families of constant region genes in a phylogenetically primitive vertebrate indicate an additional level of immunoglobulin complexity. Proc. Natl. Acad. Sci. U.S.A. 84:5868-5872.
69. Kokubu, F., K. Hinds, R. Litman, M.J. Shamblott, and G.W. Litman, G.W. 1988a. Complete structure and organization of immunoglobulin heavy chain constant region genes in a phylogenetically primitive vertebrate. EMBO J. 7:1979-1988.
70. H gene loci in a primitive vertebrate. EMBO J. 7:3413-3422.
71. Laing, K.J., L.J. Hardie, W. Aartsen, P.S. Grabowski, and C.J. Secombes. 1999. Expression of an inducible nitric oxide synthase gene in rainbow trout, Oncorhynchus mykiss. Dev. Comp. Immunol 23:71-85.
72. Litman, G.W., B.W. Erickson, L. Lederman, and O. Mäkelä. 1982. Antibody response in Heterodontus. Mol. Cell Biochem. 45:49-57.
73. Litman, G.W., M.K. Anderson, and J.P Rast. 1999. Evolution of antigen binding receptors. Annu. Rev. Immunol. 17:109-147.
74. Lopez, D.M., M.M. Sigel, and J.C. Lee. 1974. Phylogenetic studies on T cells. I. Lymphocytes of the shark with differential response to phytohemagglutinin and concanavalin A. Cell. Immunol. 10:287-293.
75. Luer, C.A. 1989. Elasmobranchs (sharks, skates, and rays) as animal models for biomedical research, in Nonmammalian Models for Biomedical Research A. Woodhead, Ed., CRC Press, Boca Raton, FL, 121-147.
76. Luer, C.A. and PW. Gilbert. 1985. Mating behavior, egg deposition, incubation period, and hatching in the clearnose skate, Raja eglanteria. Environ. Biol. Fish. 13:161-171.
77. Luer, C.A., C.J. Walsh, A.B. Bodine, J.T. Wyffels, and T.R. Scott. 1995. The elasmobranch thymus: anatomical, histological, and preliminary functional characterization. J. Exp. Zool. 273:342-354.
78. Machaca, K. and M.M. Compton. 1993. Analysis of thymic lymphocyte apoptosis using in vitro techniques. Dev. Comp. Immunol. 17:263-276.
79. Mäkelä, O. and G.W. Litman. 1980. Lack of heterogeneity in anti-hapten antibodies of a phylogenetically primitive shark. Nature 287:639-640.
80. Manning, M.J. and T. Nakanishi. 1996. The specific immune system: cellular defenses, in The Fish Immune System G. Iwama and T. Nakanishi, Eds., Academic Press, San Diego, 160-205.
81. Marchalonis, J.J. and G.M. Edelman, G.M. 1965. Phylogenetic origins of antibody structure. I. Multichain structure of immunoglobulins in the smooth dogfish (Mustelus canis). J. Exp. Med. 122:601-618.
82. Marchalonis, J.J. and G.M. Edelman. 1966. Polypeptide chains of immunoglobulins of the smooth dogfish (Mustelus canis). Science 154:1567-1568.
83. Mattison, A. and R. Fänge. 1982. The cellular structure of the Leydig organ in the shark, Etmopterus spinax (L.). Biol. Bull. 162:182-194.
84. McCarthy, J.E., PH. Redmond, S.M. Duggan, R.W.G. Watson, C.M. Condron, J.R. O’Donnell, and D.J. Bouchier-Hayes. 1995. Characterization of the defects in murine peritoneal macrophage function in the early postsplenectomy period. J. Immunol.155:387-396.
85. McKinney, E.C. 1990. Shark cytotoxic macrophages interact with target membrane amino groups. Cell. Immunol. 127:506-513.
86. McKinney, E.C. 1992a. Shark lymphocytes: primitive antigen reactive cells. Annu. Rev. Fish Dis 2:43-51.
87. McKinney, E.C. 1992b. Proliferation of shark leukocytes. In Vitro Cell. Dev. Biol 28A:303-305.
88. McKinney, E.C. and M.F. Flajnik. 1997. IgM-mediated opsonization and cytotoxicity in the shark. J. Leukocyte Biol. 61:141-146.
89. McKinney, E.C., L. Haynes, and A.L. Droese. 1986. Macrophage-like effector of spontaneous cytotoxicity from the shark. Dev. Comp. Immunol 10:497-508.
90. Migliorati, G., I. Nicoletti, G. Nocentini, M.C. Pagliaccia, and C. Roccordi. 1994. Dexamethasone and interleukins modulate apoptosis of murine thymocytes and peripheral T-lymphocytes. Pharmacol. Res. 30:43-52.
91. Miracle, A.L., M.K. Anderson, R.T. Litman, C.J. Walsh, C.A. Luer, E.V. Rothenberg, and G.W. Litman. 2001. Complex expression patterns of lymphocyte-specific genes during the development of cartilaginous fish implicate unique lymphoid tissues in generating an immune repertoire. Int. Immunol. 13:567-580.
92. Mulero, V. and J. Meseguer. 1998. Functional characterization of a macrophage-activating factor produced by leucocytes of gilthead seabram (Sparus aurata L.). Fish Shellfish Immunol. 8:143-156.
93. Nakanishi, T., K. Aoyagi, C. Xia, J.M. Dijkstra, and M. Ototake. 1999. Specific cell-mediated immunity in fish. Vet. Immunol. Immunopathol.72:101-109.
94. Nathan, C. 1992. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:3051-3064.
95. Nathan, C. and J.B. Hibbs, Jr. 1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol 3:65-70.
96. Neumann, N.F., D. Faga, and M. Belosevic. 1995. Macrophage activating factor(s) secreted by mitogen stimulated goldfish kidney leukocytes synergize with bacterial lipopolysaccharide to induce nitric oxide production in teleost macrophages. Dev. Comp. Immunol. 19:473-482.
97. Nonaka, M. and S.L. Smith. 2000. Complement system of bony and cartilaginous fish. Fish Shellfish Immunol. 10:215-228.
98. Nussler, A. and T. Billiar. 1993. Inflammation, immunoregulation, and inducible nitric oxide synthase. J. Leukocyte Biol 54:171-178.
99. Obenauf, S.D. and S. Hyder Smith. 1985. Chemotaxis of nurse shark leukocytes. Dev. Comp. Immunol 9:221-230.
100. Ohta, Y., K. Okamura, E.C. McKinney, S. Bartl, K. Hashimoto, and M.F. Flajnik. 2000. Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc. Natl. Acad. Sci. U.S.A. 97:4712-4717.
101. Okamura, K., M. Ototake, T. Nakanishi, Y. Kurosawa, and K. Hashimoto. 1997. The most primitive vertebrates possess highly polymorphic class I genes comparable to those of humans. Immunity 7:777-790.
102. Owen, J.J., M.D. Cooper, and M.C. Raff. 1974. In vitro generation of B lymphocytes in mouse foetal liver, a mammalian “bursa equivalent.” Nature 249:361-363.
103. Panoskaltis-Mortori, A. and R.P Bucy. 1995. In situ hybridization with digoxigenin-labeled RNA probes: facts and artifacts. BioTechniques 18:300-307.
104. Parish, N., A. Wrathmell, S. Hart, and J.E. Harris. 1986a. Phagocytic cells in the dogfish, Scyliorhinus canicula L. I. In vitro studies. Acta Zool. (Stockholm) 67:215-224.
105. Parish, N., A. Wrathmell, S. Hart, and J.E. Harris. 1986b. Phagocytic cells in the peripheral blood of the dogfish, Scyliorhinus canicula L. II. In vivo studies. Acta Zool. (Stockholm) 67:225-234.
106. Perey, D.Y.E., J. Finstad, B. Pollara, and R.A. Good. 1968. Evolution of the immune response. VI. First and second set skin homograft rejections in primitive fishes. Lab. Invest. 19:591-597.
107. Pettey, C.L. and E.C. McKinney. 1981. Mitogen-induced cytotoxicity in the nurse shark. Dev. Comp. Immunol 5:53-64.
108. Pettey, C.L. and E.C. McKinney. 1983. Temperature and cellular regulation in the shark. Eur. J. Immunol. 13:133-138.
109. Pettey, C.L. and E.C. McKinney. 1988. Induction of cell-mediated cytotoxicity by shark 19S IgM. Cell. Immunol. 111:28-38.
110. Pica, A., L. Cristino, F. Sasso, and P. Guerriero. 2000. Haemopoietic regeneration after autohaemotransplant in sub-lethal X-irradiated marbled electric rays. Comp. Haematol. Int. 10:43-49.
111. Rast, J.P. and G.W. Litman. 1994. T cell receptor gene homologs are present in the most primitive jawed vertebrates. Proc. Natl. Acad. Sci. U.S.A. 91:9248-9252.
112. Rast, J.P, M.K. Anderson, S.J. Strong, C. Luer, R.T. Litman, and G.W. Litman. 1997. a, ß, γ, and δ T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity 6:1-11.
113. Reynaud, C.-A., V. Anquez, H. Grimal, and J.-C. Weill. 1987. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell 48:379-388.
114. Rosenshein, I.L., S.F. Schluter, and J.J. Marchalonis. 1986. Conservation among the immunoglobulins of carcharhine sharks and phylogenetic conservation of variable region determinants. Vet. Immunol. Im- munopathol. 12:13-20.
115. Ross, G. and J. Jensen. 1973. The first component (C1n) of the complement system of the nurse shark (Ginglymostoma cirratum). J. Immunol. 110:175-182.
116. Rowley, T.C., T.C. Hunt, M. Page, and G. Mainwaring. 1988. Fish, in Vertebrate Blood Cells. Cambridge University Press, Cambridge, U.K., 19-127.
117. Ruben, L.N., D.R. Buchholz, P. Ahmadi, R.O. Johnson, R.H. Clothier, and S. Shiigi. 1994. Apoptosis in thymus of adult Xenopus laevis. Dev. Comp. Immunol 18:231-238.
118. Saeij, J.P, R.J. Stet, A. Groeneveld, L. Verburg van Kemenade, W. Muiswinkel, and G.F. Wiegertjes. 2000. Molecular and functional characterization of a fish inducible-type nitric oxide synthase. Immunogenetics 51:339-346.
119. Schluter, S.F., R.M. Bernstein, and J.J. Marchalonis. 1997. Molecular origins and evolution of immunoglobulin heavy-chain genes of jawed vertebrates. Immunol. Today 81:543-548.
120. Secombes, C. J. 1996. The nonspecific immune system: cellular defenses, in The Fish Immune System. G. Iwama and T. Nakanishi, Eds., Academic Press, San Diego, 63-103.
121. Secombes, C.J., T. Wang, S. Hong, S. Peddie, M. Crampe, K.J. Laing, C. Cunningham, and J. Zou. 2001. Cytokines and innate immunity of fish. Dev. Comp. Immunol 25:713-723.
122. Shamblott, M.J. and G.W. Litman. 1989. Complete nucleotide sequence of primitive vertebrate immunoglobulin light chain genes. Proc. Natl. Acad. Sci. U.S.A. 86:4684-4688.
123. Shortman, K. and R. Scollay. 1994. Death in the thymus. Nature 372:44-45.
124. Sigel, M.M., J.C. Lee, E.C. McKinney, and D.M. Lopez. 1978. Cellular immunity in fish as measured by lymphocyte stimulation. Mar. Fish Rev. 40:6-11.
125. Silverstein, S.C., R.M. Steinman, and Z.A. Cohn. 1977. Endocytosis. Annu. Rev. Biochem.46:669-722.
126. Smith, S. 1998. Shark complement: an assessment. Immunol. Rev. 166:67-78.
127. Smith, S., M. Riesgo, S. Obenauf, and C. Woody. 1997. Anaphylactic and chemotactic response of mammalian cells to zymosan- activated shark serum. Fish Shellfish Immunol. 7:503-514.
128. Stokes, E.E. and B.G. Firkin. 1971. Studies of the peripheral blood of the Port Jackson shark (Heterodontus portusjacksoni) with particular reference to the thrombocytes. Br. J. Haematol. 20:427-435.
129. Surh, C.D. and J. Sprent. 1994. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:101-103.
130. Tafalla, C. and B. Novoa. 2000. Requirements for nitric oxide production by turbot (Scophthalmus maximus) head kidney macrophages. Dev. Comp. Immunol 24:623-631.
131. Takemoto, T., S. Smith, T. Terado, H. Kimura, and M. Nonaka. 2000. Molecular cloning of complement B/C2 and C3/C4 of a Japanese shark Triakis scyllia. Dev. Comp. Immunol 24:S25.
132. Tomonaga, S., K. Kobayashi, K. Hagiwara, K. Yamaguchi, and K. Awaya. 1986. Gut-associated lymphoid tissue in the elasmobranchs. Zool. Sci. 3:453-458.
133. Tomonaga, S., H. Zhang, K. Kobayashi, R. Fujii, and K. Teshima. 1992. Plasma cells in the spleen of the Aleutian skate, Bathyraja aleutica. Arch. Histol. Cytol. 55:287-284.
134. Velardi, A. and M.D. Cooper. 1984. An immunofluorescence analysis of the ontogeny of myeloid, T, and B lineage cells in mouse hemopoietic tissues. J. Immunol. 133:672-677.
135. Walsh, C.J. and C.A. Luer. 1998. Comparative phagocytic and pinocytic activities of leucocytes from peripheral blood and lymphomyeloid tissues of the nurse shark (Ginglymostoma cirratum Bonaterre) and the clearnose skate (Raja eglanteria Bosc). Fish Shellfish Immunol. 8:197-215.
136. Walsh, C.J. and C.A. Luer. In press. Elasmobranch hematology: identification of cell types and practical applications, in Elasmobranch Husbandry Manual. M. Smith, D. Warmolts, D. Thoney, and R. Hueter, Eds., Special Publication of the Ohio Biological Survey 16, Columbus, OH.
137. Walsh, C.J., J.T. Wyffels, A.B. Bodine, and C.A. Luer. 2002. Dexamethasone-induced apoptosis in immune cells from peripheral circulation and lymphomyeloid tissues of juvenile clearnose skates, Raja eglanteria. Dev. Comp. Immunol 26:623-633.
138. Warr, G.W. 1995. The immunoglobulin genes of fish. Dev. Comp. Immunol 19:1-12.
139. Weissman, G., M.C. Finkelstein, J. Csernanasky, J.P. Quigley, R.S. Quinn, L. Techner, W. Troll, and PB. Dunham. 1978. Attack of sea urchin eggs by dogfish phagocytes: model of phagocyte-mediated cellular toxicity. Proc. Natl. Acad. Sci. U.S.A. 75:1825-1829.
140. Weyts, F.A.A., B.M.L. Verburg-van Kemenade, G. Flik, J.G.D. Lambert, and S.E Wendelaar Bonga. 1997. Conservation of apoptosis as an immune regulatory mechanism: effects of cortisol and cortisone on carp lymphocytes. Brain Behav. Immunol. 11:95-105.
141. Wyffels, J.T. 2001. Acute Radiation Exposure in the Clearnose Skate, Raja eglanteria: A Histological Study of the Immune System. Ph.D. dissertation, Clemson University, Clemson, SC.
142. Wyllie, A.H. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556.
143. Yin, Z., T.J. Lam, and Y.M. Sin. 1997. Cytokine-mediated antimicrobial immune response of catfish, Clarias gariepinus, as a defense against Aeromonas hydrophila. Fish Shellfish Immunol. 7:93-104.
144. Zapata, A.G., M. Torroba, R. Sacedon, A. Varas, and A. Vicente. 1996. Structure of the lymphoid organs of elasmobranchs. J. Exp. Zool. 275:125-143.