Innate immune complexity in the purple sea urchin: Diversity of the Sp185/333 system

Frontiers in Immunology

Volumn 3, Issue APR, 2012, Pages

  Courtney Smith, L ^a  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

Coelomocyte; Echinoid; Evolution; Gene; Innate immunity; Invertebrate; Microsatellites; RNA editing

Indexed keywords

EID: 84874154834     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00070     Document Type: Review

References (99)

1. Al-Sharif, W. Z., Sunyer, J. O., Lam- bris, J. D., and Smith, L. C. (1998). Sea urchin coelomocytes specifically express a homologue of the com- plement component C3. J. Immunol. 160, 2983-2997.
2. Arizza, V., Giaramita, F. T., Parrinello, D., Cammarata, M., and Parrinello, N. (2007). Cell cooperation in coelo- mocyte cytotoxic activity of Paracen- trotus lividus coelomocytes. Comp. Biochem. Physiol. A Mol. Integr. Phys- iol. 147, 389-394.
3. Bagshaw, A. T., Pitt, J. P., and Gem- mell, N. J. (2008). High fre- quency of microsatellites in S. cerevisiae meiotic recombination hotspots. BMC Genomics 9, 49. doi:10.1186/1471-2164-9-49
4. Bertheussen, K., and Seijelid, R. (1978). Echinoid phagocytes in vitro. Exp. Cell Res. 111, 401-412.
5. Biermann, C. H. (1998). The mole- cular evolution of sperm binding in six species of sea urchins (Echi- noidea: Strongylocentrotidae). Mol. Biol. Evol. 15, 1761-1771.
6. Boolootian, R. A., and Geise, C. A. (1958). Coelomic corpuscles of echinoderms. Biol. Bull. 15, 53-56.
7. Brack, C., Hirama, M., Lenhard- Schuuler, R., and Tonegawa, S. (1978). A complete immunoglobu- lin gene is created by somatic recom- bination. Cell 15, 1-14.
8. Brites, D., Mctaggart, S., Morris, K., Anderson, J., Thomas, K., Colson, I., Fabbro, T., Little, T. J., Ebert, D., and Du Pasquier, L. (2008). The Dscam homologue of the crustacean Daph- nia is diversified by alternative splic- ing like in insects. Mol. Biol. Evol. 25, 1429-1439.
9. Brockton, V., Henson, J. H., Raftos, D. A., Majeske, A. J., Kim, Y. O., and Smith, L. C. (2008). Localiza- tion and diversity of 185/333 pro- teins from the purple sea urchin - unexpected protein-size range and protein expression in a new coelo- mocyte type. J. Cell. Sci. 121, 339-348.
10. Buckley, K. M., Florea, L. D., and Smith, L. C. (2009). A method of identify- ing alternative or cryptic splice sites within gene and mRNA sequences. Comparisons among sequences from vertebrates, echinoderms and other groups. BMC Genomics 10, 318. doi:10.1186/1471-2164-10-318
11. Buckley, K. M., Munshaw, S., Kepler, T. B., and Smith, L. C. (2008a). The 185/333 gene family is a rapidly diversifying host-defense gene clus- ter in the purple sea urchin, Strongy- locentrotus purpuratus. J. Mol. Biol. 379, 912-928.
12. Buckley, K. M., Terwilliger, D., and Smith, L. C. (2008b). Sequence vari- ations in 185/333 messages from the purple sea urchin suggest posttran- scriptional modifications to increase immune diversity. J. Immunol. 181, 8585-8594.
13. Buckley, K. M., and Smith, L. C. (2007). Extraordinary diversity among members of the large gene family, 185/333, from the purple sea urchin, Strongylocentrotus purpuratus. BMC Mol. Biol. 8, 68. doi:10.1186/1471-2199-8-68
14. Calestani, C., Rast, J. P., and David- son, E. H. (2003). Isolation of pigment cell specific genes in the sea urchin embryo by differential macroarray screening. Development 130, 4587-4596.
15. Cannon, J. P., Haire, R. N., Schnitker, N., Mueller, M. G., and Litman, G. W. (2004). Individual protochordates have unique immune-type receptor repertoires. Curr. Biol. 14, R465- R466.
16. Chan, L., Chang, B. H.-J., Makamuta, M., Li, W.-H., and Smith, L. C. (1997). Apobec-1 and apolipopro- tein B mRNA editing. Biochim. Bio- phys. Acta 1345, 11-26.
17. Coffaro, K. A. (1979). Memory and Specificity in the Sea Urchin Lytech- inus pictus. Doctoral Dissertation, University of California, Santa Cruz.
18. Coffaro, K. A. (1980). Memory and Specificity in the Sea Urchin Lytechinus pictus.NewYork,NY: Elsevier/North Holland Biomedical Press.
19. Coffaro, K. A., and Hinegardner, R. T. (1977). Immune response in the sea urchin Lytechinus pictus. Science 197, 1389-1390.
20. De Tomaso, A. W., Nyholm, S. V., Palmeri, K. J., Ishizuka, K. J., Ludington, W. B., Mitchel, K., and Weissman, I. L. (2005). Isolation and characterization of a proto- chordate histocompatibility locus. Nature 438, 454-945.
21. Despons, L., Uzunov, Z., and Louis, V. L. (2011). Tandem gene arrays, plas- tic chromosomal organizations. C. R. Biol. 334, 639-646.
22. Dheilly, N., Nair, S. V., Birch, D., and Raftos, D. A. (2011). Ultra- structural localization of the highly variable immune response protein (He185/333) within coelomocytes and the gut tissues of the sea urchin, Heliocidaris erythrogramma. Immunol. Cell Biol. 89, 861-869.
23. Dheilly, N. M., Nair, S. V., Smith, L. C., and Raftos, D. A. (2009). Highly variable immune-response proteins (185/333) from the sea urchin Strongylocentrotus purpura- tus: proteomic analysis identifies diversity within and between indi- viduals. J. Immunol. 182, 2203-2212
24. Dishaw, L., Ota, T., Mueller, M., Can- non, J., Haire, R., Gwatney, N., Lit- man, R., and Litman, G. (2010). The basis for haplotype complexity in VCBPs, an immune-type receptor in amphioxus. Immunogenetics 62, 623-631.
25. Dishaw, L. J., Mueller, M. G., Gwat- ney, N., Cannon, J. P., Haire, R. N., Litman, R. T., Amemiya, C. T., Ota, T., Rowen, L., Glusman, G., and Litman, G. W. (2008). Genomic complexity of the variable region- containing chitin-binding proteins in amphioxus. BMC Genet. 9, 78. doi:10.1186/1471-2156-9-78
26. Dong, D., He, G., Zhang, S., and Zhang, Z. (2009). Evolution of olfactory receptor genes in primates domi- nated by birth-and-death process. Genome Biol. Evol. 1, 258-264.
27. Dong, Y., and Dimopoulos, G. (2009). Anopheles fibrinogen-related pro- teins provide expanded pattern recognition capacity against bacteria and malaria parasites. J. Biol. Chem. 284, 9835-9844.
28. Dong, Y., Taylor, H. E., and Dimopou- los, G. (2006). AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol. 4, e229. doi:10.1371/journal.pbio.0040229
29. Edds, K. T. (1977). Dynamic aspects of filopodial formation by reorganiza- tion of microfilaments. J. Cell Biol. 73, 479-491.
30. Edds, K. T. (1979). Isolation and characterization of two forms of a cytoskeleton. J. Cell Biol. 83, 109-115.
31. Edds, K. T. (1993). Cell biology of echi- noid coelomocytes. J. Invertebr. Biol. 61, 173-178.
32. Furukawa, R., Takahashi, Y., Kanajima, Y., Dan-Sohkawa, M., and Kaneko, H. (2009). Defense system by mes- enchyme cells in bipinnaria larvae of the starfish, Asterina pectinifera. Dev. Comp. Immunol. 33, 205-215.
33. Gendrel, C.-G., Boulet, A., and Dutreix, M. (2000). (CA/GT)n microsatel- lites affect homologous recombina- tion during yeast meiosis. Genes Dev. 14, 1261-1268.
34. Ghosh, J., Lun, C. M., Majeske,A. J., Sac- chi, S., Schrankel, C. S., and Smith, L. C. (2011). Invertebrate immune diversity. Dev. Comp. Immunol. 35, 959-974.
35. Ghosh, J. G., Buckley, K. M., Nair, S. V., Raftos, D. A., Miller, C. A., Majeske, A. J., Hibino, T., Rast, J. P., Roth, M., and Smith, L. C. (2010). Sp185/333: a novel family of genes and proteins involved in the purple sea urchin immune response. Dev. Comp. Immunol. 34, 235-245.
36. Gilad,Y., Man, O., Paabo, S., and Lancet, D. (2003). Human specific loss of olfactory receptor genes. Proc. Natl. Acad. Sci. U.S.A. 100, 3324-3327.
37. Graveley, B. R. (2005). Mutually exclu- sive splicing of the insect Dscam pre-mRNA directed by competing intronic RNA secondary structures. Cell 123, 65-73.
38. Gross, P. S., Clow, L. A., and Smith, L. C. (2000). SpC3, the comple- ment homologue from the pur- ple sea urchin, Strongylocentrotus purpuratus, is expressed in two subpopulations of the phagocytic coelomocytes. Immunogenetics 51, 1034-1044.
39. Grula, J. W., Hall, T. J., Hunt, J. A., Guiugni, D. F., Graham, G. J., David- son, E. H., and Britten, R. J. (1982). Sea urchin DNA sequence variation and reduced interspecies differences of the less variable DNA sequences. Evolution 36, 655-676.
40. Hanington, P. C., and Zhang, S.- M. (2010). The primary role of fibrinogen-related proteins in inver- tebrates is defense, not coagulation. J. Innate Immun. 3, 17-27.
41. Henson, J. H., Nesbitt, D., Wright, B. D., and Scholey, J. M. (1992). Immunolocalization of kinesin in sea urchin coelomocytes. Associa- tion of kinesin with intracellular organelles. J. Cell. Sci. 103(Pt 2), 309-320.
42. Henson, J. H., Svitkina, T. M., Burns, A. R., Hughes, H. E., Macpartland, K. J., Nazarian, R., and Borisy, G. G. (1999). Two components of actin- based retrograde flow in sea urchin coelomocytes. Mol. Biol. Cell 10, 4075-4090.
43. Hibino, T., Loza-Coll, M., Messier, C., Majeske, A. J., Cohen, A., Terwilliger, D. P., Buckley, K. M., Brockton, V., Nair, S., Berney, K., Fugmann, S. D., Anderson, M. K., Pancer, Z., Cameron, R. A., Smith, L. C., and Rast, J. P. (2006). The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 300, 349-365.
44. Hildemann, W. H., and Dix, T. G. (1972). Transplantation reactions of tropical Australian echinoderms. Transplantation 14, 624-633.
45. Holm, K., Dupont, S., Skold, H., Ste- nius, A., Thorndyke, M., and Hern- roth, B. (2008). Induced cell pro- liferation in putative haematopoi- etic tissues of the sea star, Aster- ias rubens (L.).J.Exp.Biol.211, 2551-2558.
46. Hozumi, N., and Tonegawa, S. (1976). Evidence for somatic rearrangement of immunoglobulin genes coding for variable and constant regions. Proc. Natl. Acad. Sci. U.S.A. 73, 3628-3632.
47. Huelsenbeck, J. P., and Bull, J. J. (1996). A likelihood ratio test to detect conflicting phylogenetic signal. Syst. Biol. 45, 92-98.
48. Hyman, L. H. (1955). The Invertebrates: Echinodermata, the Coelomate Bila- teria,Vol. 4. NewYork, NY: McGraw- Hill Book Co., Inc.
49. Johnson, P. T. (1969a). The coelomic elements of sea urchins (Strongy- locentrotus). I. The normal coelomocytes; their morphol- ogy and dynamics in hanging drops. J. Invertebr. Pathol. 13, 25-41.
50. Johnson, P. T. (1969b). The coelomic elements of the sea urchins (Strongy- locentrotus) III. In vitro reaction to bacteria. J. Invertebr. Pathol. 13, 42-62.
51. Johnson, P. T., and Chapman, F. A. (1970). Abnormal epithelial growth in sea urchin spines (Strongylo- centrotus franciscanus). J. Invertebr. Pathol. 16, 116-122.
52. Karp, R. D., and Hildemann, W. H. (1976). Specific allograft reactivity in the sea star Dermasterias imbri- cata. Transplantation 22, 434-439.
53. Kishishita, N., Matsuno, T., Takahashi, Y., Takaba, H., Nishizumi, H., and Nagawa, F. (2010). Regulation of antigen-receptor gene assembly in hagfish. EMBO Rep. 11, 126-132.
54. Lee, C., Kim, N., Roy, M., and Grav- eley, B. R. (2010). Massive expan- sions of Dscam splicing diversity via staggered homologous recombi- nation during arthropod evolution. RNA 16, 91-105.
55. Lee, Y. H. (2003). Molecular phyloge- nies and divergence times of sea urchin species of Strongylocentroti- dae, Echinoidea. Mol. Biol. Evol. 20, 1211-1221.
56. Llobet-Brossa, E., Rossello-Mora, R., and Amann, R. (1998). Micro- bial community composition of Wadden sea sediments as revealed by fluorescence in situ hybridiza- tion. Appl. Environ. Microbiol. 64, 2691-2696.
57. Loker, E. S. (2010). "Gastropod immunobiology," in Invertebrate Immunity, ed. K. Soderhall (Austin: Landes Bioscience and Springer Science+Business Media), 17-43.
58. Loker, E. S., Adema, C. M., Zhang, S.- M., and Kepler, T. B. (2004). Inverte- brate immune systems - not homo- geneous, not simple, not well under- stood. Immunol. Rev. 198, 10-24.
59. Maas, S., and Rich, A. (2000). Changing genetic information through RNA editing. Bioessays 22, 790-802.
60. Massana, R., Murray, A. E., Preston, C. M., and Delong, E. F. (1997). Ver- tical distribution and phylogenetic characterization of marine palnk- tonic Archaea in the Santa Barbara chanel. Appl. Environ. Microbiol. 63, 50-56.
61. McKitrick, T. R., and De Tomaso, A. W. (2010). Molecular mechanisms of allorecognition in a basal chordate. Semin. Immunol. 22, 34-38.
62. Messer, L. I., and Wardlaw, A. C. (1980). "Separation of coelomocytes of Ech- inus esculentus by density gradi- ent centrifugation," in Proceedings of the European Colloquium on Echino- derms, ed. M. Jangoux (Rotterdam: A. A. Balkema), 319-323.
63. Metchnikoff, E. (1893). Lectures on the Comparative Pathology of Inflamma- tion: Delivered at the Pasteur Institute in 1891. Kegan Paul,Trench,Trubner & Co. Ltd, London.
64. Michevich, M. F., and Ferris, J. S. (1981). The implications of congruence in Mendida. Syst. Zool. 30, 351-370.
65. Miller, C. A., Buckley, K. M., Easley, R. L., and Smith, L. C. (2010). An Sp185/333 gene cluster from the purple sea urchin and putative microsatellite-mediated gene diver- sification. BMC Genomics 11, 575. doi:10.1186/1471-2164-11-575
66. Multerer, K. A., and Smith, L. C. (2004). Two cDNAs from the purple sea urchin, Strongylocentrotus purpura- tus, encoding mosaic proteins with domains found in factor H, fac- tor I, and complement components C6 and C7. Immunogenetics 56, 89-106.
67. Nagawa, F., Kishishita, N., Shimizu, K., Hirose, S., Miyoshi, M., Nezu, J., Nishimura, T., Nishizumi, H., Taka- hashi, Y., Hashimoto, S., Takeuchi, M., Miyajima, A., Takemori, T., Otsuka, A. J., and Sakano, H. (2007). Antigen-receptor genes of the agnathan lamprey are assembled by a process involving copy choice. Nat. Immunol. 8, 206-213.
68. Nair, S. V., Del Valle, H., Gross, P. S., Terwilliger, D. P., and Smith, L. C. (2005). Macroarray analy- sis of coelomocyte gene expres- sion in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol. Genomics 22, 33-47.
69. Plytycz, B., and Seljelid, R. (1993). Bac- terial clearance by the sea urchin, Strongylocentrotus droebachiensis. Dev. Comp. Immunol. 17, 283-289.
70. Rast, J. P., and Messier-Solek, C. (2008). Marine invertebrate genome sequences and our evolving under- standing of animal immunity. Biol. Bull. 214, 274-283.
71. Rast, J. P., Pancer, Z., and Davidson, E. H. (2000). New approaches towards an understanding of deuterostome immunity. Curr. Top. Microbiol. Immunol. 248, 3-16.
72. Rast, J. P., Smith, L. C., Loza-Coll, M., Hibino, T., and Litman, G. W. (2006). Genomic insights into the immune system of the sea urchin. Science 314, 952-956.
73. Reinisch, C. L., and Bank, F. B. (1971). Cell recognition: reactions of the sea star (Asterias vulgaris) to the injec- tion of amebocytes of sea urchin (Arbacia punctulata). Cell. Immunol. 2, 496-503.
74. Rogozin, I. B., Iyer, L. M., Liang, L., Glazko, G. V., Liston, V. G., Pavlov, Y. I., Aravind, L., and Pancer, Z. (2007). Evolution and diversifica- tion of lamprey antigen receptors: evidence for involvement of an AID- APOBEC family cytosine deami- nase. Nat. Immunol. 8, 647-656.
75. Schmucker, D., and Chen, B. (2009). Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes Dev. 23, 147-156.
76. Schmucker, D., Clemens, J. C., Shu, H., Worby, C. A., Xiao, J., Muda, M., Dixon, J. E., and Zipursky, S. L. (2000). Drosophila Dscam is an axon guidance receptor exhibiting extra- ordinary molecular diversity. Cell 101, 671-684.
77. Service, M., and Wardlaw, A. C. (1984). Echinochrome-A as a bactericidal substance in the coelomic fluid of Echinus esculentus (L). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 79, 161-165.
78. Silva, J. R. (2000). The onset of phago- cytosis and identity in the embryo of Lytechinus variegatus. Dev. Comp. Immunol. 24, 733-739.
79. Siu, G., Clark, S. P., Yoshikai, Y., Malis- sen,M.,Yanagi,Y.,Strauss,E.,Mak,T. W.,and Hood,L. (1984). The human T cell antigen receptor is encoded by variable, diversity, and joining gene segments that rearrange to generate a complete V gene. Cell 37, 393-401. Smith, L. C. (2010). Diversification of innate immune genes: lessons from the purple sea urchin. Dis. Model Mech. 3, 274-279.
80. Smith, L. C., Chang, L., Britten, R. J., and Davidson, E. H. (1996). Sea urchin genes expressed in acti- vated coelomocytes are identified by expressed sequence tags. Comple- ment homologues and other puta- tive immune response genes suggest immune system homology within the deuterostomes. J. Immunol. 156, 593-602.
81. Smith, L. C., and Davidson, E. H. (1992). The echinoid immune sys- tem and the phylogenetic occur- rence of immune mechanisms in deuterostomes. Immunol. Today 13, 356-362.
82. Smith, L. C., Ghosh, J., Buckley, K. M., Clow, L. A., Dheilly, N. M., Haug, T., Henson, J. H., Li, C., Lun, C. M., Majeske, A. J., Matranga, V., Nair, S. V., Rast, J. P., Raftos, D. A., Roth, M., Sacchi, S., Schrankel, C. S., and Stensvag, K. (2010). Echinoderm immunity, in Inver- tebrate Immunity, ed. K. Soder- hall (Austin: Landes Bioscience and Spring Science+Business Media), 260-301.
83. Smith, L. C., Shih, C. S., and Dachen- hausen, S. G. (1998). Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J. Immunol. 161, 6784-6793.
84. Smith, V. J. (1981). The echinoderms, in Invertebrate Blood Cells, eds N. A. Ratcliffe and A. F. Rowley (NewYork, NY: Academic Press), 513-562.
85. Sodergren, E., Weinstock, G. M., David- son, E. H., Cameron, R. A., Gibbs, R. A., Angerer, R. C., Angerer, L. M., Arnone, M. I., Burgess, D. R., Burke, R. D.,Coffman,J. A.,Dean,M.,Elph- ick, M. R., Ettensohn, C. A., Foltz, K. R., Hamdoun, A., Hynes, R. O., Klein,W. H.,Marzluff,W.,Mcclay,D. R.,Morris,R. L.,Mushegian,A.,Rast, J. P., Smith, L. C., Thorndyke, M. C., Vacquier, V. D., Wessel, G. M., Wray, G., Zhang, L., Elsik, C. G., Ermo- laeva, O., Hlavina, W., Hofmann, G., Kitts, P., Landrum, M. J., Mackey, A. J., Maglott, D., Panopoulou, G., Poustka, A. J., Pruitt, K., Sapojnikov, V., Song, X., Souvorov, A., Solovyev, V., Wei, Z., Whittaker, C. A., Wor- ley, K., Durbin, K. J., Shen, Y., Fedrigo, O., Garfield, D., Haygood, R.,Primus,A.,Satija,R.,Severson,T., Gonzalez-Garay, M. L., Jackson, A. R., Milosavljevic, A., Tong, M., Kil- lian, C. E., Livingston, B. T., Wilt, F. H., Adams, N., Belle, R., Car- bonneau, S., Cheung, R., Cormier, P., Cosson, B., Croce, J., Fernandez- Guerra, A., Geneviere, A. M., Goel, M., Kelkar, H., Morales, J., Mulner- Lorillon, O., Robertson, A. J., Gold- stone, J. V., Cole, B., Epel, D., Gold, B., Hahn, M. E., Howard-Ashby, M., Scally, M., Stegeman, J. J., Allgood, E. L., Cool, J., Judkins, K. M., Mccaf- ferty, S. S., Musante, A. M., Obar, R. A., Rawson, A. P., Rossetti, B. J., Gib- bons,I. R.,Hoffman,M. P.,Leone,A., Istrail, S., Materna, S. C., Samanta, M. P., Stolc, V., Tongprasit, W., Tu, Q., Bergeron, K. F., Brandhorst, B. P., Whittle, J., Berney, K., Bottjer, D. J., Calestani, C., Peterson, K., Chow, E., Yuan, Q. A., Elhaik, E., Graur, D., Reese, J. T., Bosdet, I., Heesun, S., Marra, M. A., Schein, J., Ander- son, M. K., Brockton, V., Buckley, K. M., Cohen, A. H., Fugmann, S. D., Hibino, T., Loza-Coll, M., Majeske, A. J., Messier, C., Nair, S. V., Pancer, Z., Terwilliger, D. P.,Agca, C., Arboleda, E., Chen, N., Churcher, A. M., Hallböök, F., Humphrey, G. W., Idris, M. M., Kiyama, T., Liang, S., Mellott,D.,Mu,X.,Murray,G.,Olin- ski, R. P., Raible, F., Rowe, M., Taylor, J. S., Tessmar-Raible, K., Wang, D., Wilson, K. H., Yaguchi, S., Gaaster- land, T., Galindo, B. E., Gunaratne, H. J.,Juliano,C.,Kinukawa,M.,Moy, G. W., Neill, A. T., Nomura, M., Raisch, M., Reade, A., Roux, M. M., Song, J. L., Su, Y. H., Townley, I. K., Voronina, E., Wong, J. L., Amore, G., Branno, M., Brown, E. R., Cavalieri, V., Duboc, V., Duloquin, L., Flytza- nis, C., Gache, C., Lapraz, F., Lepage, T.,Locascio,A.,Martinez,P.,Matassi, G., Matranga,V., Range, R., Rizzo, F., Röttinger, E., Beane, W., Bradham, C., Byrum, C., Glenn, T., Hussain, S., Manning, G., Miranda, E., Thoma- son, R., Walton, K., Wikramanayke, A., Wu, S. Y., Xu, R., Brown, C. T., Chen, L., Gray, R. F., Lee, P. Y., Nam, J., Oliveri, P., Smith, J., Muzny, D., Bell, S., Chacko, J., Cree,A., Curry, S., Davis, C., Dinh, H., Dugan-Rocha, S., Fowler, J., Gill, R., Hamilton, C., Hernandez, J., Hines, S., Hume, J., Jackson, L., Jolivet, A., Kovar, C., Lee, S., Lewis, L., Miner, G., Mor- gan, M., Nazareth, L. V., Okwuonu, G., Parker, D., Pu, L. L., Thorn, R., and Wright, R. (2006). The genome of the sea urchin, Strongy- locentrotus purpuratus. Science 314, 941-952.
86. Stevens, M. E., Dhillon, J., Miller, C. A., Messier-Solek, C., Rast, J. P., Majeske, A. J., Zuelke, D., and Smith, L. C. (2010). SpTie1/2 from the sea urchin Strongylocentrotus pur- puratus, is an orthologue of verte- brate Tie1 and Tie2 and is expressed in coelomocytes, axial organ and embryos. Dev. Comp. Immunol. 34, 884-895.
87. Stout, B. A., Adema, C. M., Zhang, S. M., and Loker, E. S. (2009). "The biology of FREPs: diversi- fied lectins with fibrinogen-related domains from the freshwater snail Biomphalaria glabrata," in Animal Lectins: A Functional View,ed.V. A. Ahmen (New York: CRC Press, Taylor & Francis), 475-491.
88. Terwilliger, D. P., Buckley, K. M., Brock- ton, V., Ritter, N. J., and Smith, L. C. (2007). Distinctive expres- sion patterns of 185/333 genes in the purple sea urchin, Strongylo- centrotus purpuratus: an unexpect- edly diverse family of transcripts in response to LPS, beta-1,3-glucan, and dsRNA. BMC Mol. Biol. 8, 16. doi:10.1186/1471-2199-8-16
89. Terwilliger, D. P., Buckley, K. M., Mehta, D., Moorjani, P. G., and Smith, L. C. (2006). Unexpected diversity dis- played in cDNAs expressed by the immune cells of the purple sea urchin, Strongylocentrotus purpura- tus. Physiol. Genomics 26, 134-144.
90. Tingaud-Sequeira, A., Calusinska, M., Finn, R. M., Chauvigne, F., Lozano, J.,and Cerda,J. (2010). The zebrafish genome encodes the largest verte- brate repertoire of functional aqua- porins with dual paralogy and sub- strate specificities similar to mam- mals. BMC Evol. Biol. 10, 38. doi:10.1186/1471-2148-10-38
91. Trifonov,E. N. (2003)."Tuning function of tandemly repeating sequences: a molecular device for fast adapta- tion," in Evolutionary Theory and Processes: Modern Horizons, Papers in Honor of Eviatar Nevo, ed. S. P. Wassser (Amsterdam: Kluwer Acad- emic Publishers), 1-24.
92. Varadarajan, J., and Karp, R. D. (1983). Histological versus morphological assessment of graft rejection in invertebrates. Transplantation 36, 629-631.
93. Watson, F. L., Puttmann-Holgado, R., Thomas, F., Lamar, D. L., Hughes, M., Kondo, M., Rebel, V. I., and Schmucker, D. (2005). Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309, 1874-1878.
94. Weigert, M., Gatmaitan, L., Loh, E., Schilling, J., and Hood, L. (1978). Rearrangement of genetic information may produce immunoglobulin diversity. Nature 276, 785-790.
95. Whitman, W. B., Coleman, D. C., and Wiebe,W. J. (1998). Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U.S.A. 95, 6578-6583.
96. Whittaker, C. A., Bergeron, K. F., Whit- tle, J., Brandhorst, B. P., Burke, R. D., and Hynes, R. O. (2006). The echin- oderm adhesome. Dev. Biol. 300, 252-266.
97. Wilson, M. J., Torkar, M., Haude, A., Milne, S., Jones, T., Sheer, D., Beck, S., and Trowsdale, J. (2000). Plastic- ity in the organization and sequences of human KIR/ILT gene families. Proc. Natl. Acad. Sci. U.S.A. 97, 4778-4783.
98. Yui, M., and Bayne, C. (1983). Echin- oderm immunity:bacterial clearance by the sea urchin Strongylocentrotus purpuratus. Biol. Bull. 165, 473-485.
99. Zhang, S. M., Adema, C. M., Kepler, T. B., and Loker, E. S. (2004). Diversifi- cation of Ig superfamily genes in an invertebrate. Science 305, 251-254.