The sea urchin immune system

Invertebrate Survival Journal

Volumn 3, Issue 1, 2006, Pages 25-39

  Smith, L Courtney ^a   Rast, J P ^b   Brockton, V ^a   Terwilliger, D P ^a   Nair, S V ^c   Buckley, K M ^a   Majeske, A J ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

185 333 genes; Coelomocyte; Complement; Deuterostome; Diversification; Echinoderm; Evolution; Innate immunity

Indexed keywords

EID: 33751545412     PISSN: None     EISSN: 1824307X     Source Type: Journal    
DOI: None     Document Type: Review

References (95)

1. Al-Sharif WZ, Sunyer JO, Lambris JD, Smith LC. Sea urchin coelomocytes specifically express a homologue of the complement component C3. J. Immunol. 160: 2983- 2997, 1998.
2. Azumi K, De Santis R, De Tomaso A, Rigoutsos I, Yoshizaki F, Pinto MR et al. Genomic analysis of immunity in a urochordate and the emergence of the vertebrate immune system: "Waiting for Godot". Immunogenetics 55: 570-581, 2003.
3. Bertheussen K, Seljelid R. Echinoid phagocytes in vitro. Exp. Cell Res. 111: 401-412, 1978.
4. Bertheussen K. Endocytosis by echinoid phagocytes in vitro. II. Mechanisms of endocytosis. Dev. Comp. Immunol. 5: 557-564, 1981.
5. Bertheussen K. Receptors for complement on echinoid phagocytes. II. Purified human complement mediates echinoid phagocytosis. Dev. Comp. Immunol. 6: 635-642, 1982.
6. Bertheussen K. Complement-like activity in sea urchin coelomic fluid. Dev. Comp. Immunol. 7: 21-31, 1983.
7. Blandin S, Levashina EA. Thioester-containing proteins and insect immunity. Mol. Immunol. 40: 903-908, 2004.
8. Blumbach B, Pancer Z, Diehl-Seifert B, Steffen R, Munkner J, Muller I et al. The putative sponge aggregation receptor. Isolation and characterization of a molecule composed of scavenger receptor cysteine-rich domains and short consensus repeats. J. Cell Sci. 111: 2635-2644, 1998.
9. Boolootian RA, Geise CA. Coelomic corpuscles of echinoderms. Biol. Bull. 15: 53-56, 1958.
10. Burke RD, Murray G, Rise M, Wang D. Integrins on eggs: the beta C subunit is essential for formation of the cortical actin cytoskeleton in sea urchin eggs. Dev. Biol. 265: 53- 60, 2004.
11. Castellani C, Rast JP, Davidson EH. Isolation of pigment cell specific genes in the sea urchin embryo by differential macroarray screening. Development 130: 4587-4596, 2003.
12. Clow LA, Gross PS, Shih CS, Smith LC. Expression of SpC3, the sea urchin complement component, in response to lipopolysaccharide. Immunogenetics 51: 1021-1033, 2000.
13. Clow LA, Raftos DA, Gross PS, Smith LC. The sea urchin complement homologue, SpC3, functions as an opsonin. J. Exp. Biol. 207: 2147-2155, 2004.
14. Coffaro KA. Memory and specificity in the sea urchin Lytechinus pictus. Doctoral Dissertation, University of California, 1979.
15. Coffaro KA. Memory and specificity in the sea urchin Lytechinus pictus. Elsevier/North Holland Biomedical Press, New York, USA, 1980.
16. Coffaro KA, Hinegardner RT. Immune response in the sea urchin Lytechinus pictus. Science 197: 1389-1390, 1977.
17. Dangott LJ, Jordan JE, Bellet RA, Garbers DL. Cloning of the mRNA for the protein that crosslinks to the egg peptide speract. Proc. Natl. Acad. Sci. USA 86: 2128-2132, 1989.
18. Dishaw LJ, Smith SL, Bigger CH. Characterization of a C3-like cDNA in a coral: Phylogenetic implications. Immunogenetics 57: 535-548, 2005.
19. Dodds AW, Law SK. The phylogeny and evolution of the thioester bond-containing proteins C3, C4 and alpha 2- macroglobulin. Immunol. Rev. 166: 15-26, 1998.
20. Edds KT. Dynamic aspects of filopodial formation by reorganization of microfilaments. J. Cell. Biol. 73: 479-491, 1977.
21. Edds KT. Isolation and characterization of two forms of a cytoskeleton. J. Cell. Biol. 83: 109-15, 1979
22. Edds KT. Coelomocyte cytoskeletons. Interaction with cytochalasin B. Exp. Cell. Res. 130: 371-6, 1980.
23. Edds KT. Cell biology of echinoid coelomocytes. I. Diversity and characterization of cell types. J. Invert. Biol. 61: 173-178, 1993.
24. Freeman M, Ashkenas J, Rees DJ, Kingsley DM, Copeland NG, Jenkins NA, Krieger M. An ancient, highly conserved family of cysteine-rich protein domains revealed by cloning type I and type II murine macrophage scavenger receptors. Proc. Natl. Acad. Sci. USA 87: 8810-8814, 1990.
25. Gerardi P, Lassegues M, Canicatti C. Cellular-distribution of seaurchin antibacterial activity. Biol. Cell 70: 153-157, 1990.
26. Gibson AW, Burke RD. The origin of pigment cells in embryos of the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 107: 414-419, 1985.
27. Gibson AW, Burke RD. Migratory and invasive behaviour of pigment cells in normal and animalized sea urchin embryos. Exp. Cell Res. 173: 546-557, 1987.
28. Giga Y, Ikai A, Takahashi K. The complete amino acid sequence of echinoidin, a lectin from the coelomic fluid of the sea urchin Anthocidaris crassispina. Homologies with mammalian and insect lectins. J. Biol. Chem. 262: 6197- 6203, 1987.
29. Gross PS, Al-Sharif WZ, Clow LA, Smith LC. Echinoderm immunity and the evolution of the complement system. Dev. Comp. Immunol. 23: 429-442, 1999.
30. Gross PS, Clow LA, Smith LC. SpC3, the complement homologue from the purple sea urchin, Strongylocentrotus purpuratus, is expressed in two subpopulations of the phagocytic coelomocytes. Immunogenetics 51: 1034-1044, 2000.
31. Haug T, Kjuul AK, Styrvold OB, Sandsdalen E, Olsen OM, Stensvag K. Antibacterial activity in Strongylocentrotus droebachiensis (Echinoidea), Cucumaria frondosa (Holothuroidea), and Asterias rubens (Asteroidea). J. Invert. Path. 81: 94-102, 2002.
32. Henson JH, Nesbitt D, Wright BD, Sholey JS. Immunolocalization of kinesin in sea urchin coelomocytes: association of kinesin with intracellular organelles. J. Cell. Sci. 103: 309-320, 1992.
33. Henson JH, Svitkina TM, Burns AR, Hughes HE, MacPartland KJ, Nazarian R, Borisy GG. Two components of actinbased retrograde flow in sea urchin coelomocytes. Mol. Biol. Cell 10: 4075-4090, 1999.
34. Hildemann WH, Dix TG. Transplantation reactions of tropical australian echinoderms. Transplantation 14: 624-633, 1972.
35. Hillier BJ, Vacquier VD. Amassin, an olfactomedin protein, mediates the massive intercellular adhesion of sea urchin coelomocytes. J. Cell Biol. 160: 597-604, 2003.
36. Holmskov U, Mollenhauer J, Madsen J, Vitved L, Gronlund J, Tornoe I, Kliem A, Reid KB, Poustka A, Skjodt K. Cloning of gp-340, a putative opsonin receptor for lung surfactant protein D. Proc. Natl. Acad. Sci. USA 96: 10794-10799, 1999.
37. Ishiguro H, Kobayashi K, Suzuki M, Titani K, Tomonaga S, Kurosawa Y. Isolation of a hagfish gene that encodes a complement component. EMBO J. 11: 829-837, 1992.
38. Johnson PT. The coelomic elements of the sea urchins (Strongulocentratus) III. In vitro reaction to bacteria. J. Invert. Pathol. 13: 42-62, 1969.
39. Johnson PT. Infection with diatoms and other microorganisms in the sea urchin spines (Strongylocentrotus fanciscanus). J. Invert. Pathol. 16: 268-276, 1970.
40. Kaplan G, Bertheussen K. The morphology of echinoid phagocytes and mouse peritoneal macrophages during phagocytosis in vitro. Scand. J. Immunol. 6: 1289-1296, 1977.
41. Karp RD, Coffaro KA. Cellular defense systems of the echinodermata. In: Manning ED (ed), Phylogeny of immunological memory, Elsevier/North Holland, Amsterdam, The Netherlands, pp 257-282, 1980.
42. Karp RD, Hildemann WH. Specific allograft reactivity in the sea star Dermasterias imbricata. Transplantation 22: 434- 439, 1976.
43. Lagueux M, Perrodou E, Levashina EA, Capovilla M, Hoffmann JA. Constitutive expression of a complement-like protein in TOLL and JAK gain-of-function mutants of Drosophila. Proc. Natl. Acad. Sci. USA 97: 11427-11432, 2000.
44. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709- 718, 2001.
45. Marino R, Kimura Y, De Santis R, Lambris JD, Pinto MR. Complement in urochordates: Cloning and characterization of two C3-like genes in the ascidian Ciona intestinalis. Immunogenetics 53: 1055-1064, 2002.
46. Matranga V, Pinsino A, Celi M, Di Bella G, Natoli A. Impacts of UV-B radiation on short-term cultures of sea urchin coelomocytes. Mar. Biol. 149: 25-34, 2006.
47. Metchnikoff E. Lectures on the comparative pathology of inflamation: Delivered at the pasteur institute in 1891. Kegan Paul, Trench, Trubner & Co. Ltd., 1893.
48. Miyazaki T, Hirokami Y, Matsuhashi N, Takatsuka H, Naito M. Increased susceptibility of thymocytes to apoptosis in mice lacking aim, a novel murine macrophage-derived soluble factor belonging to the scavenger receptor cysteine-rich domain superfamily. J. Exp. Med. 189: 413- 422, 1999.
49. Multerer KA, Smith LC. Two cDNAs from the purple sea urchin, Strongylocentrotus purpuratus, encoding mosaic proteins with domains found in factor H, factor I, and complement components C6 and C7. Immunogenetics 56: 89-106, 2004.
50. Murray G, Reed C, Marsden M, Rise M, Wang D, Burke RD. The alphaBbetaC integrin is expressed on the surface of the sea urchin egg and removed at fertilization. Dev. Biol. 227: 633-647, 2000.
51. Nair SV, Del Valle H, Gross PS, Terwilliger DP, Smith LC. Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol. Genomics 22: 33-47, 2005.
52. Nakao M, Fushitani Y, Fujiki K, Nonaka M, Yano T. Two diverged complement factor B/C2-like cDNA sequences from a teleost, the common carp (Cyprinus carpio). J. Immunol. 161: 4811-4818, 1998.
53. Nonaka M, Azumi K. Opsonic complement system of the solitary ascidian, Halocynthia roretzi. Dev. Comp. Immunol. 23: 421-427, 1999.
54. Nonaka M, Yoshizaki F. Primitive complement system of invertebrates. Immunol. Rev. 198: 203-215, 2004.
55. Okazaki K. Normal development to metamorphosis. Springer Verlag, New York, 1975.
56. Paavilainen VO, Bertling E, Falck S, Lappalainen P. Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trend. Cell Biol. 14: 386-394, 2004.
57. Pancer Z, Rast JP, Davidson EH. Origins of immunity: Transcription factors and homologues of effector genes of the vertebrate immune system expressed in sea urchin coelomocytes. Immunogenetics 49: 773-786, 1999.
58. Pancer Z. Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proc. Natl. Acad. Sci. USA 97: 13156-13161, 2000.
59. Pancer Z, Cooper MD. The evolution of adaptive immunity. Annu. Rev. Immunol. 24: 497-518, 2006.
60. Pasare C, Medzhitov R. Toll-like receptors: Linking innate and adaptive immunity. Adv. Exp. Med. Biol. 560: 11-18, 2005.
61. Perez-Villar JJ, Whitney GS, Bowen MA, Hewgill DH, Aruffo AA, Kanner SB. CD5 negatively regulates the t-cell antigen receptor signal transduction pathway: Involvement of SH2- containing phosphotyrosine phosphatase SHP-1. Mol. Cell. Biol. 19: 2903-2912, 1999.
62. Plytycz B, Seljelid R. Bacterial clearance by the sea urchin, Strongylocentrotus droebachiensis. Dev. Comp. Immunol. 17: 283-289, 1993.
63. Raftos DA, Nair SV, Robbins J, Newton RA, Peters R. A complement component C3-like protein from the tunicate, Styela plicata. Dev. Comp. Immunol. 26: 307-312, 2002.
64. Rast JP, Pancer Z, Davidson EH. New approaches towards an understanding of deuterostome immunity. Curr. Top. Microbiol. Immunol. 248: 3-16, 2000.
65. Reinisch CL, Bang FB. Cell recognition: Reactions of the sea star (Asterias vulgaris) to the injection of amebocytes of sea urchin (Arbacia punctulata). Cell. Immunol. 2: 496-503, 1971.
66. Robertson AJ, Dickey CE, McCarthy JJ, Coffman JA. The expression of SpRunt during sea urchin embryogenesis. Mech. Dev. 117: 327-330, 2002.
67. Sarrias MR, Gronlund J, Padilla O, Madsen J, Holmskov U, Lozano F. The scavenger receptor cysteine-rich (SRCR) domain: An ancient and highly conserved protein module of the innate immune system. Crit. Rev. Immunol. 24: 1-37, 2004.
68. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL. Drosophila DSCAM is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101: 671-684, 2000.
69. Service M, Wardlaw AC. Echinochrome-a as a bactericidal substance in the coelomic fluid of Echinus esculentus (l). Comp. Biochem. Physiol. 79B: 161-165, 1984.
70. Shah M, Brown KM, Smith LC. The gene encoding the sea urchin complement protein, SpC3, is expressed in embryos and can be upregulated by bacteria. Dev. Comp. Immunol. 27: 529-538, 2003.
71. Silva JR. The onset of phagocytosis and identity in the embryo of Lytechinus variegatus. Dev. Comp. Immunol. 24: 733-739, 2000.
72. Sim RB, Sim E. Autolytic fragmentation of complement components C3 and C4 under denaturing conditions, a property shared with alpha 2-macroglobulin. Biochem. J. 193: 129-141, 1981.
73. Sim RB, Sim E. Autolytic fragmentation of complement components C3 and C4 and its relationship to covalent binding activity. Ann. NY Acad. Sci. 421: 259-276, 1983.
74. Smith VJ. The echinoiderms. In: Ratcliffe NA, Rowley AF (eds), Invertebrate blood cells, Academic Press, New York, NY, pp 513-562, 1981.
75. Smith LC, Britten RJ, Davidson EH. SpCoel1: A sea urchin profilin gene expressed specifically in coelomocytes in response to injury. Mol. Biol. Cell 3: 403-414, 1992.
76. Smith LC, Davidson EH. The echinoid immune system and the phylogenetic occurrence of immune mechanisms in deuterostomes. Immunol. Today 13: 356-362, 1992.
77. Smith LC, Davidson EH. The echinoderm immune system. Characters shared with vertebrate immune systems and characters arising later in deuterostome phylogeny. Ann. NY Acad. Sci. 712: 213-226, 1994.
78. Smith LC, Britten RJ, Davidson EH. Lipopolysaccharide activates the sea urchin immune system. Dev. Comp. Immunol. 19: 217-224, 1995.
79. Smith LC, Chang L, Britten RJ, Davidson EH. Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags. Complement homologues and other putative immune response genes suggest immune system homology within the deuterostomes. J. Immunol. 156: 593-602, 1996.
80. Smith LC, Shih CS, Dachenhausen SG. Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J. Immunol. 161: 6784-6793, 1998.
81. Smith LC, Azumi K, Nonaka M. Complement systems in invertebrates. The ancient alternative and lectin pathways. Immunopharmacology 42: 107-120, 1999.
82. Smith LC. The complement system in sea urchins. Adv. Exp. Med. Biol. 484: 363-372, 2001.
83. Smith LC, Clow LA, Terwilliger DP. The ancestral complement system in sea urchins. Immunol. Rev. 180: 16-34, 2001.
84. Smith LC. Thioester function is conserved in SpC3, the sea urchin homologue of the complement component C3. Dev. Comp. Immunol. 26: 603-614, 2002.
85. Smith LC. Host responses to bacteria: Innate immunity in invertebrates, Cambridge University Press, 2005.
86. Strathmann RR. Larval feeding in echinoderms. Amer. Zool. 15: 717-730, 1975.
87. Takito J, Hikita C, Al-Awqati Q. Hensin, a new collecting duct protein involved in the in vitro plasticity of intercalated cell polarity. J. Clin. Invest. 98: 2324-2331, 1996.
88. Tamboline CR, Burke RD. Secondary mesenchyme of the sea urchin embryo: ontogeny of blastocoelar cells. J. Exp. Zool. 262: 51-60, 1992.
89. Terwilliger DP, Buckley KM, Mehta D, Moorjani PG, Smith LC. Unexpected diversity displayed in cDNAs expressed by the immune cells of the purple sea urchin, Strongylocentrotus purpuratus. Physiol. Genomics, 2006, in press.
90. Terwilliger DP, Clow LA, Gross PS, Smith LC. Constitutive expression and alternative splicing of the exons encoding SCRS in Sp152, the sea urchin homologue of complement factor B. Implications on the evolution of the Bf/C2 gene family. Immunogenetics 56: 531-543, 2004.
91. Trahey M, Weissman IL. Cyclophilin c-associated protein: A normal secreted glycoprotein that down-modulates endotoxin and proinflammatory responses in vivo. Proc. Natl. Acad. Sci. USA 96: 3006-3011, 1999.
92. Volanakis JE. Overview of the complement system. Immunol. Med. 20: 9-32, 1998.
93. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309: 1874-1878, 2005.
94. Yui M, Bayne C. Echinoderm immunity: Bacterial clearance by the sea urchin Strongylocentrotus purpuratus. Biol. Bull. 165: 473-485, 1983.
95. Zhu Y, Thangamani S, Ho B, Ding JL. The ancient origin of the complement system. EMBO J. 24: 382-394, 2005.