Marine Biotechnology

, Volume 11, Issue 1, pp 24–44 | Cite as

Analysis of Genes Isolated from Plated Hemocytes of the Pacific Oyster, Crassostreas gigas

  • Steven Roberts
  • Giles Goetz
  • Samuel White
  • Frederick GoetzEmail author
Original Article


A complementary deoxyribonucleic acid library was constructed from hemocytes of Crassostrea gigas that had been plated on poly-lysine plates for 24 h. From this library, 2,198 expressed sequence tags (ESTs) of greater than or equal to 100 bp were generated and analyzed. A large number of genes that potentially could be involved in the physiology of the oyster hemocyte were uncovered. They included proteins involved in cytoskeleton rearrangement, proteases and antiproteases, regulators of transcription and translation, cell death regulators, receptors and their associated protein factors, lectins, signal transduction proteins, and enzymes involved in eicosanoid and steroid synthesis and xenobiotic metabolism. Based on their relationship with innate immunity, the expression of selected genes was analyzed by quantitative polymerase chain reaction in gills from bacterial-challenged oysters. Several genes observed in the library were significantly upregulated by bacterial challenge including interleukin 17, astacin, cystatin B, the EP4 receptor for prostaglandin E, the ectodysplasin receptor, c-jun, and the p100 subunit of nuclear factor-kB. Using a similar approach, we have been analyzing the genes expressed in trout macrophages. While there are significant differences between the types of genes present in vertebrate macrophages compared with oyster hemocytes, there are some striking similarities including proteins involved in cytoskeletal rearrangement, proteases and antiproteases, and genes involved in certain signal transduction pathways underlying immune processes such as phagocytosis. Finally, C. virginica homologs of some of the C. gigas genes uncovered in the ESTs were obtained by aligning the ESTs reported here, against the assembled C. virginica ESTs at the National Center for Biotechnology Information.


Hemocytes ESTs Pacific oyster C. gigas Innate immunity Bacterial challenge 



This research was supported in part by the Cooperative State Research Education and Extension Service, US Department of Agriculture, under Agreement no. 2003-38500-13505 (SR).

Supplementary material

10126_2008_9117_MOESM1_ESM.rtf (73 kb)
Online Appendix Crassostrea virginica-assembled homologs of selected C. gigas ESTs. Note that the translated products of some of the C. virginica contigs may have stop codons that do not necessarily reflect the true end of the ORF but may be a result of sequencing errors (RTF 73.1 KB)


  1. Acton RT, Bennett JC, Evans EE, Schrohenloher RE (1969) Physical and chemical characterization of an oyster hemagglutinin. J Biol Chem 244:4128–4135PubMedGoogle Scholar
  2. Adema CM, Van Deutekom-Mulder EC, Van Der Knaap WPW, Meuleman EA, Sminia T (1991) Generation of oxygen radicals in hemocytes of the snail Lymnaea stagnalis in relation to the rate of phagocytosis. Dev Comp Immunol 15:17–26PubMedGoogle Scholar
  3. Aitken A, Jones D, Soneji Y, Howell S (1995) 14-3-3 proteins: biological function and domain structure. Biochem Soc Trans 23:605–611PubMedGoogle Scholar
  4. Anderson RS (1999) Perkinsus marinus secretory products modulate superoxide anion production by oyster (Crassostrea virginica) haemocytes. Fish Shellfish Immunol 9:51–60Google Scholar
  5. Anestis A, Lazou A, Portner HO, Michaelidis B (2007) Behavioral, metabolic, and molecular stress responses of marine bivalve Mytilus galloprovincialis during long-term acclimation at increasing ambient temperature. Am J Physiol Regul Integr Comp Physiol 293:R911–R921PubMedGoogle Scholar
  6. Badariotti F, Lelong C, Dubos MP, Favrel P (2007) Characterization of chitinase-like proteins (Cg-Clp1 and Cg-Clp2) involved in immune defence of the mollusc Crassostrea gigas. FEBS J 274:3646–3654PubMedGoogle Scholar
  7. Begley M, Gahan CG, Hill C (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29:625–651PubMedGoogle Scholar
  8. Black BL, Olson EN (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Ann Rev Cell Dev Biol 14:167–196Google Scholar
  9. Brash AR (1999) Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem 274:23679–23682PubMedGoogle Scholar
  10. Brocchieri L, Conway De Macario E, Macario AJ (2008) hsp70 genes in the human genome: conservation and differentiation patterns predict a wide array of overlapping and specialized functions. BMC Evol Biol 8:19PubMedGoogle Scholar
  11. Canesi L, Scarpato A, Betti M, Ciacci C, Pruzzo C, Gallo G (2002) Bacterial killing by Mytilus hemocyte monolayers as a model for investigating the signaling pathways involved in mussel immune defence. Mar Environ Res 54:547–551PubMedGoogle Scholar
  12. Chaty S, Rodius F, Vasseur P (2004) A comparative study of the expression of CYP1A and CYP4 genes in aquatic invertebrate (freshwater mussel, Unio tumidus) and vertebrate (rainbow trout, Oncorhynchus mykiss). Aquat Toxicol 69:81–94PubMedGoogle Scholar
  13. Cheng TC (1975) Functional morphology and biochemistry of molluscan phagocytes. Ann NY Acad Sci 266:343–379PubMedGoogle Scholar
  14. Cheng TC (1996) Hemocytes: forms and functions. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster, Crassostrea virginica. Maryland Sea Grant College, College Park, MDGoogle Scholar
  15. Cheng TC, Rodrick GE (1975) Lysosomal and other enzymes in the hemolymph of Crassostrea virginica and Mercenaria mercenaria. Comp Biochem Physiol B 52:443–447PubMedGoogle Scholar
  16. Chomcynski P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and protein from cell and tissue samples. Biotechniques 15:532–537Google Scholar
  17. Chomcynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol extraction. Anal Biochem 162:156–159Google Scholar
  18. Cristofoletti PT, Ribeiro AF, Terra WR (2005) The cathepsin L-like proteinases from the midgut of Tenebrio molitor larvae: sequence, properties, immunocytochemical localization and function. Insect Biochem Mol Biol 35:883–901PubMedGoogle Scholar
  19. Delaporte M, Soudant P, Moal J, Giudicelli E, Lamber C, Seguineau C, Samain JF (2006) Impact of 20:4n-6 supplementation on the fatty acid composition and hemocyte parameters of the Pacific oyster Crassostreas gigas. Lipids 41:567–576PubMedGoogle Scholar
  20. Dempsey PW, Doyle SE, He JQ, Cheng G (2003) The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev 14:193–209PubMedGoogle Scholar
  21. Desmazes C, Galineau L, Gauthier F, Bromme D, Lalmanach G (2003) Kininogen-derived peptides for investigating the putative vasoactive properties of human cathepsins K and L. Eur J Biochem 270:171–178PubMedGoogle Scholar
  22. Devries ME, Kelvin AA, Xu L, Ran L, Robinson J, Kelvin DJ (2006) Defining the origins and evolution of the chemokine/chemokine receptor system. J Immunol 176:401–415PubMedGoogle Scholar
  23. Donald KM, Day AJ, Smerdon GR, Cross LJ, Hawkins AJS (2003) Quantification of gene transcription and enzyme activity for functionally important proteolytic enzymes during early development in the Pacific oyster Crassostrea gigas. Comp Biochem Physiol Part B Biochem Mol Biol 136:383–392Google Scholar
  24. Droin NM, Pinkoski MJ, Dejardin E, Green DR (2003) Egr family members regulate nonlymphoid expression of Fas ligand, TRAIL, and tumor necrosis factor during immune responses. Mol Cell Biol 23:7638–7647PubMedGoogle Scholar
  25. Dumitriu IE, Baruah P, Manfredi AA, Bianchi ME, Rovere-Querini P (2005) HMGB1: guiding immunity from within. Trends Immunol 26:381–387PubMedGoogle Scholar
  26. Durr E, Yu J, Krasinska KM, Carver LA, Yates III JR, Testa JE, Oh P, Schnitzer JE (2004) Direct proteomic mapping of the lung microvascular endothelial cell surface in vivo and in cell culture. Nat Biotechnol 22:985–992PubMedGoogle Scholar
  27. Ensor CM, Tai HH (1995) 15-Hydroxyprostaglandin dehydrogenase. J Lipid Mediators Cell Signal 12:313–319Google Scholar
  28. Fisher WS (1986) Structure and functions of oyster hemocytes. In: Brehelin M (ed) Immunity in invertebrates. Springer, BerlinGoogle Scholar
  29. Ford SE, Tripp MR (1996) Disease and defense mechanisms. In: Kennedy VS, Newell RIE, Eble AF (eds) The eastern oyster, Crassostrea virginica. Maryland Sea Grant College, College Park, MDGoogle Scholar
  30. Fu H, Subramanian RR, Masters SC (2000) 14-3-3 proteins: structure, function, and regulation. Annu Rev Pharmacol Toxicol 40:617–647PubMedGoogle Scholar
  31. Gadelhak GG, Pedibhotla VK, Stanley-Samuelson DW (1995) Eicosanoid biosynthesis by hemocytes from the tobacco hornworm, Manduca sexta. Insect Biochem and Mol Biol 25:743–749Google Scholar
  32. Ge G, Fernandez CA, Moses MA, Greenspan DS (2007) Bone morphogenetic protein 1 processes prolactin to a 17-kDa antiangiogenic factor. Proc Natl Acad Sci U S A 104:10010–10015PubMedGoogle Scholar
  33. Gestal C, Costa M, Figueras A, Novoa B (2007) Analysis of differentially expressed genes in response to bacterial stimulation in hemocytes of the carpet-shell clam Ruditapes decussatus: identification of new antimicrobial peptides. Gene 406:134–143PubMedGoogle Scholar
  34. Gilmore TD (1999) The Rel/NF-kappaB signal transduction pathway: introduction. Oncogene 18:6842–6844PubMedGoogle Scholar
  35. Goetz FW, Iliev DB, Mccauley LA, Liarte CQ, Tort LB, Planas JV, Mackenzie S (2004a) Analysis of genes isolated from lipopolysaccharide-stimulated rainbow trout (Oncorhynchus mykiss) macrophages. Mol Immunol 41:1199–1210PubMedGoogle Scholar
  36. Goetz FW, Planas JV, Mackenzie S (2004b) Tumor necrosis factors. Dev Comp Immunol 28:487–497PubMedGoogle Scholar
  37. Gonzalez M, Romestand B, Fievet J, Huvet A, Lebart MC, Gueguen Y, Bachère E (2005) Evidence in oyster of a plasma extracellular superoxide dismutase which binds LPS. Biochem Biophys Res Commun 338:1089–1097PubMedGoogle Scholar
  38. Gueguen Y, Cadoret J-P, Flament D, Barreau-Roumiguiere C, Girardot A-L, Garnier J, Hoareau A, Bachere E, Escoubas J-M (2003) Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 303:139–145PubMedGoogle Scholar
  39. Han J, Jiang Y, Li Z, Kravchenko VV, Ulevitch RJ (1997) Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 386:296–299PubMedGoogle Scholar
  40. Hashim S, Mukherjee K, Raje M, Basu SK, Mukhopadhyay A (2000) Live salmonella modulate expression of rab proteins to persist in a specialized compartment and escape transport to lysosomes. J Biol Chem 275:16281–16288PubMedGoogle Scholar
  41. Hibino T, Loza-Coll M, Messier C, Majeske AJ, Cohen AH, Terwilliger DP, Buckley KM, Brockton V, Nair SV, Berney K, Fugmann SD, Anderson MK, Pancer Z, Cameron RA, Smith LC, Rast JP (2006) The immune gene repertoire encoded in the purple sea urchin genome. Dev Biol 300:349–365PubMedGoogle Scholar
  42. Hu G, Tang J, Zhang B, Lin Y, Hanai J-I, Galloway J, Bedell V, Bahary N, Han Z, Ramchandran R, Thisse B, Thisse C, Zon LI, Sukhatme VP (2006) A novel endothelial-specific heat shock protein HspA12B is required in both zebrafish development and endothelial functions in vitro. J Cell Sci 119:4117–4126PubMedGoogle Scholar
  43. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877PubMedGoogle Scholar
  44. Huang X, Tsuji N, Miyoshi T, Nakamura-Tsuruta S, Hirabayashi J, Fujisaki K (2007) Molecular characterization and oligosaccharide-binding properties of a galectin from the argasid tick Ornithodoros moubata. Glycobiology 17:313–323PubMedGoogle Scholar
  45. Huising MO, Kruiswijk CP, Flik G (2006) Phylogeny and evolution of class-I helical cytokines. J Endocrinol 189:1–25PubMedGoogle Scholar
  46. Huovila AP, Turner AJ, Pelto-Huikko M, Karkkainen I, Ortiz RM (2005) Shedding light on ADAM metalloproteinases. Trends Biochem Sci 30:413–422PubMedGoogle Scholar
  47. Huvet A, Herpin A, Dégremont L, Labreuche Y, Samain JF, Cunningham C (2004) The identification of genes from the oyster Crassostrea gigas that are differentially expressed in progeny exhibiting opposed susceptibility to summer mortality. Gene 343:211–220PubMedGoogle Scholar
  48. Ikegami R, Sugimoto Y, Segi E, Katsuyama M, Karahashi H, Amano F, Maruyama T, Yamane H, Tsuchiya S, Ichikawa A (2001) The expression of prostaglandin E receptors EP2 and EP4 and their different regulation by lipopolysaccharide in C3H/HeN peritoneal macrophages. J Immunol 166:4689–4696PubMedGoogle Scholar
  49. Iliev DB, Liarte CQ, MacKenzie S, Goetz FW (2005) Activation of rainbow trout (Oncorhynchus mykiss) mononuclear phagocytes by different pathogen associated molecular pattern (PAMP) bearing agents. Mol Immunol 42:1215–1223PubMedGoogle Scholar
  50. Iliev DB, Goetz GW, MacKenzie S, Planas JV, Goetz FW (2006) Pathogen-associated gene expression profiles in rainbow trout macrophages. Comp Biochem Physiol D-Genomics & Proteomics 1:416-422Google Scholar
  51. Jenny MJ, Ringwood AH, Lacy ER, Lewitus AJ, Kempton JW, Gross PS, Warr GW, Chapman RW (2002) Potential indicators of stress response identified by expressed sequence tag analysis of hemocytes and embryos from the American oyster, Crassostrea virginica. Mar Biotechnol 4:81–93PubMedGoogle Scholar
  52. Jiang N, Tan NS, Ho B, Ding JL (2007) Respiratory protein-generated reactive oxygen species as an antimicrobial strategy. Nat Immunol 8(10):1114–1122PubMedGoogle Scholar
  53. Jones GE (2000) Cellular signaling in macrophage migration and chemotaxis. J Leukoc Biol 68:593–602PubMedGoogle Scholar
  54. Kang YS, Kim YM, Park KI, Kim Cho S, Choi KS, Cho M (2006) Analysis of EST and lectin expressions in hemocytes of Manila clams (Ruditapes philippinarum) (Bivalvia: Mollusca) infected with Perkinsus olseni. Dev Comp Immunol 30:1119–1131PubMedGoogle Scholar
  55. Karlstrom RO, Wilder LP, Bastiani MJ (1993) Lachesin: an immunoglobulin superfamily protein whose expression correlates with neurogenesis in grasshopper embryos. Development 118:509–522PubMedGoogle Scholar
  56. Kenjo A, Takahashi M, Matsushita M, Endo Y, Nakata M, Mizuochi T, Fujita T (2001) Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 276:19959–19965PubMedGoogle Scholar
  57. Kuhn H, O’Donnell VB (2006) Inflammation and immune regulation by 12/15-lipoxygenases. Prog Lipid Res 45:334–356PubMedGoogle Scholar
  58. Lamprou I, Mamali I, Dallas K, Fertakis V, Lampropoulou M, Marmaras VJ (2007) Distinct signalling pathways promote phagocytosis of bacteria, latex beads and lipopolysaccharide in medfly haemocytes. Immunology 121:314–327PubMedGoogle Scholar
  59. Legarda-Addison D, Ting AT (2007) Negative regulation of TCR signaling by NF-{kappa}B2/p100. J Immunol 178:7767–7778PubMedGoogle Scholar
  60. Lelong C, Badariotti F, Le Quere H, Rodet F, Dubos MP, Favrel P (2007) Cg-TGF-beta, a TGF-beta/activin homologue in the Pacific Oyster Crassostrea gigas, is involved in immunity against Gram-negative microbial infection. Dev Comp Immunol 31:30–38PubMedGoogle Scholar
  61. Liu L, Warner AH (2006) Further characterization of the cathepsin L-associated protein and its gene in two species of the brine shrimp, Artemia. Comp Biochem Physiol Part A Mol Integr Physiol 145:458–467Google Scholar
  62. Mackenzie S, Planas JV, Goetz FW (2003) LPS-stimulated expression of a tumor necrosis factor-alpha mRNA in primary trout monocytes and in vitro differentiated macrophages. Dev Comp Immunol 27:393–400PubMedGoogle Scholar
  63. Mah SA, Moy GW, Swanson WJ, Vacquier VD (2004) A perforin-like protein from a marine mollusk. Biochem Biophys Res Commun 316:468–475Google Scholar
  64. Manaka J, Kuraishi T, Shiratsuchi A, Nakai Y, Higashida H, Henson P, Nakanishi Y (2004) Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J Biol Chem 279:48466–48476PubMedGoogle Scholar
  65. Matsumoto T, Nakamura AM, Mori K, Kayano T (2003) Molecular characterization of a cDNA encoding putative vitellogenin from the Pacific oyster Crassostrea gigas. Zoolog Sci 20:37–42PubMedGoogle Scholar
  66. Matsumoto T, Nakamura AM, Mori K, Akiyama I, Hirose H, Takahashi Y (2007) Oyster estrogen receptor: cDNA cloning and immunolocalization. Gen Comp Endocrinol 151(2):195–201PubMedGoogle Scholar
  67. Matsushita M, Endo Y, Taira S, Sato Y, Fujita T, Ichikawa N, Nakata M, Mizuochi T (1996) A novel human serum lectin with collagen- and fibrinogen-like domains that functions as an opsonin. J Biol Chem 271:2448–2454PubMedGoogle Scholar
  68. Matsuzawa S, Takayama S, Froesch BA, Zapata JM, Reed JC (1998) p53-inducible human homologue of Drosophila seven in absentia (Siah) inhibits cell growth: suppression by BAG-1. EMBO J 17:2736–2747PubMedGoogle Scholar
  69. Mcclain JS, Oris JT, Burton GAJ, Lattier D (2003) Laboratory and field validation of multiple molecular biomarkers of contaminant exposure in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 22:361–370PubMedGoogle Scholar
  70. Minami M, Shimizu K, Okamoto Y, Folco E, Ilasaca ML, Feinberg MW, Aikawa M, Libby P (2008) Prostaglandin E Receptor Type 4-associated protein interacts directly with NF-[kappa]B1 and attenuates macrophage activation. J Biol Chem 283:9692–9703PubMedGoogle Scholar
  71. Mistry AC, Honda S, Hirose S (2001) Structure, properties and enhanced expression of galactose-binding C-type lectins in mucous cells of gills from freshwater Japanese eels (Anguilla japonica). Biochem J 360:107–115PubMedGoogle Scholar
  72. Mizuta T, Kubokawa K (2007) Presence of sex steroids and cytochrome P450 genes in Amphioxus. Endocrinology 148:3554–3565PubMedGoogle Scholar
  73. Montagnani C, Le Roux F, Berthe F, Escoubas J-M (2001) Cg-TIMP, an inducible tissue inhibitor of metalloproteinase from the Pacific oyster Crassostrea gigas with a potential role in wound healing and defense mechanisms. FEBS Lett 500:64–70PubMedGoogle Scholar
  74. Moseley TA, Haudenschild DR, Rose L, Reddi AH (2003) Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev 14:155–174PubMedGoogle Scholar
  75. Nakagawa T, Roth W, Wong P, Nelson A, Farr A, Deussing J, Villadangos JA, Ploegh H, Peters C, Rudensky AY (1998) Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280:450–453PubMedGoogle Scholar
  76. Nakazono E, Kamata Y, Yamafuji K (2002) Determination of the mRNA sequence of cathepsin Y, a cysteine endopeptidase from rat spleen, 1 and confirmation of its ubiquitous expression. Biol Chem 383:1971–1975PubMedGoogle Scholar
  77. Owen CA, Campbell EJ (1999) The cell biology of leukocyte-mediated proteolysis. J Leukoc Biol 65:137–150PubMedGoogle Scholar
  78. Pallavicini A, Costa Mdel M, Gestal C, Dreos R, Figueras A, Venier P, Novoa B (2008) High sequence variability of myticin transcripts in hemocytes of immune-stimulated mussels suggests ancient host-pathogen interactions. Dev Comp Immunol 32:213–226PubMedGoogle Scholar
  79. Pulido R, Van Huijsduijnen RH (2008) Protein tyrosine phosphatases: dual-specificity phosphatases in health and disease. FEBS J 275:848–866PubMedGoogle Scholar
  80. Quilang J, Wang S, Li P, Abernathy J, Peatman E, Wang Y, Wang L, Shi Y, Wallace R, Guo X, Liu Z (2007) Generation and analysis of ESTs from the eastern oyster, Crassostrea virginica Gmelin and identification of microsatellite and SNP markers. BMC Genomics 8:157PubMedGoogle Scholar
  81. Raftos D, Nair S (2004) Tunicate cytokine-like molecules and their involvement in host defense responses. Prog Mol Subcell Biol 34:165–182PubMedGoogle Scholar
  82. Roberts S, Gueguen Y, De Lorgeril J, Goetz F (2008) Rapid accumulation of an interleukin 17 homolog transcript in Crassostrea gigas hemocytes following bacterial exposure. Dev Comp Immunol 32:1099–104PubMedGoogle Scholar
  83. Robertson AJ, Croce J, Carbonneau S, Voronina E, Miranda E, Mcclay DR, Coffman JA (2006) The genomic underpinnings of apoptosis in Strongylocentrotus purpuratus. Dev Biol 300:321–334PubMedGoogle Scholar
  84. Saavedra C, Bachere E (2006) Bivalve genomics. Aquaculture 256:1–14Google Scholar
  85. Saha SK, Cheng G (2006) TRAF3: a new regulator of type I interferons. Cell Cycles 5:804–807Google Scholar
  86. Sakamoto E, Sakao Y, Taniguchi Y, Yamafuju K (1999) Cathepsin Y (a novel thiol enzyme) produces kinin potentiating peptide from the component protein of rat plasma. Immunopharmacology 45:207–214PubMedGoogle Scholar
  87. Scotti PD, Dearing SC, Greenwood DR, Newcomb RD (2001) Pernin: a novel, self-aggregating haemolymph protein from the New Zealand green-lipped mussel, Perna canaliculus (Bivalvia: Mytilidae). Comp Biochem Physiol Part B: Biochem and Mol Biol 128:767–779Google Scholar
  88. Serrels B, Serrels A, Brunton VG, Holt M, Mclean GW, Gray CH, Jones GE, Frame MC (2007) Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat Cell Biol 9:1046–1056PubMedGoogle Scholar
  89. Shibayama H, Takai E, Matsumura I, Kouno M, Morii E, Kitamura Y, Takeda J, Kanakura Y (2004) Identification of a cytokine-induced antiapoptotic molecule anamorsin essential for definitive hematopoiesis. J Exp Med 199:581–592PubMedGoogle Scholar
  90. Shiomi K, Fujiwara Y, Atsumi T, Kajiura Z, Nakagaki M, Tanaka Y, Mizoguchi A, Yaginuma T, Yamashita O (2005) Myocyte enhancer factor 2 (MEF2) is a key modulator of the expression of the prothoracicotropic hormone gene in the silkworm, Bombyx mori. FEBS J 272:3853–3862PubMedGoogle Scholar
  91. Song HY, Dunbar JD, Zhang YX, Guo D, Donner DB (1995) Identification of a protein with homology to hsp90 that binds the type 1 tumor necrosis factor receptor. J Biol Chem 270:3574–3581PubMedGoogle Scholar
  92. Sorrell TC, Rochester CP, Breen FN, Muller M (1989) Eicosanoids produced during interactions between Pseudomonas aeruginosa and alveolar macrophages are specie-dependent. Immunol Cell Biol 67:169–176PubMedGoogle Scholar
  93. Spilsbury K, O’Mara MA, Wu WM, Rowe PB, Symonds G, Takayama Y (1995) Isolation of a novel macrophage-specific gene by differential cDNA analysis. Blood 85:1620–1629PubMedGoogle Scholar
  94. Stanley D (2006) Prostaglandins and other eicosanoids in insects: biological significance. Annu Rev Entomol 51:25–44PubMedGoogle Scholar
  95. Steagall RJ, Rusinol AE, Truong QA, Han Z (2006) HSPA12B Is Predominantly Expressed in Endothelial Cells and Required for Angiogenesis. Arterioscler Thromb Vasc Biol 26:2012–2018PubMedGoogle Scholar
  96. Takayama K, Sukhova GK, Chin MT, Libby P (2006) A novel prostaglandin E receptor 4-associated protein participates in antiinflammatory signaling. Circ Res 98:499–504PubMedGoogle Scholar
  97. Tanguy A, Guo X, Ford SE (2004) Discovery of genes expressed in response to Perkinsus marinus challenge in Eastern (Crassostrea virginica) and Pacific (C. gigas) oysters. Gene 338:121–131PubMedGoogle Scholar
  98. Tanguy A, Bierne N, Saavedra C, Pina B, Bachere E, Kube M, Bazin E, Bonhomme F, Boudry P, Boulo V, Boutet I, Cancela L, Dossat C, Favrel P, Huvet A, Jarque S, Jollivet D, Klages S, Lapegue S, Leite R, Moal J, Moraga D, Reinhardt R, Samain JF, Zouros E, Canario A (2008) Increasing genomic information in bivalves through new EST collections in four species: development of new genetic markers for environmental studies and genome evolution. Gene 408:27–36PubMedGoogle Scholar
  99. Tasumi S, Vasta GR (2007) A galectin of unique domain organization from hemocytes of the Easter oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus. J Immunol 179:3086–3089PubMedGoogle Scholar
  100. Temnykh S, Declerck G, Lukashova A, Lipovich L, Cartinhour S, Mccouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452PubMedGoogle Scholar
  101. Torfs P, Nieto J, Veelaert D, Boon D, Van De Water G, Waelkens E, Derua R, Calderon J, De Loof A, Schoofs L (1999) The kinin peptide family in invertebrates. Ann NY Acad Sci 897:361–373PubMedGoogle Scholar
  102. Turk D, Janjiƒá V, Stern I, Podobnik M, Lamba D, Dahl SW, Lauritzen C, Pedersen J, Turk V, Turk B (2001) Structure of human dipeptidyl peptidase I (cathepsin C): exclusion domain added to an endopeptidase framework creates the machine for activation of granular serine proteases. The EMBO journal 20:6570–6582PubMedGoogle Scholar
  103. Uinuk-Ool T, Mayer WE, Sato A, Dongak R, Cooper MD, Klein J (2002) Lamprey lymphocyte-like cells express homologs of genes involved in immunologically relevant activities of mammalian lymphocytes. Proc Natl Acad Sci USA 99:14356–14361PubMedGoogle Scholar
  104. Venier P, De Pitt C, Pallavicini A, Marsano F, Varotto L, Romualdi C, Dondero F, Viarengo A, Lanfranchi G (2006) Development of mussel mRNA profiling: can gene expression trends reveal coastal water pollution? Mutat Res Fundam Mol Mech Mutagen 602:121–134Google Scholar
  105. Wang D, Li Y, Shen B (2002) A novel erythroid differentiation related gene EDRF1 upregulating globin gene expression in HEL cells. Chin Med J (Engl) 115:1701–1705Google Scholar
  106. Wang G-D, Zhang K-F, Zhang Z-P, Zou Z-H, Jia X-W, Wang S-H, Lin P, Wang Y-L (2008) Molecular cloning and responsive expression of macrophage expressed gene from small abalone Haliotis diversicolor supertexta. Fish Shellfish Immunol 24:346–359PubMedGoogle Scholar
  107. Ware CF (2003) The TNF superfamily. Cytokine Growth Factor Rev 14:181–184PubMedGoogle Scholar
  108. Welch MD, Depace AH, Verma S, Iwamatsu A, Mitchison TJ (1997a) The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J Cell Biol 138:375–384PubMedGoogle Scholar
  109. Welch MD, Iwamatsu A, Mitchison TJ (1997b) Actin polymerization is induced by Arp 2/3 protein complex at the surface of Listeria monocytogenes. Nature 385:265–269PubMedGoogle Scholar
  110. Weston CR, Davis RJ (2002) The JNK signal transduction pathway. Curr Opin Genet Dev 12:14–21PubMedGoogle Scholar
  111. Xiong X, Chen L, Li Y, Xie L, Zhang R (2006) Pf-ALMP, a novel astacin-like metalloproteinase with cysteine arrays, is abundant in hemocytes of pearl oyster Pinctada fucata. Biochim Biophys Acta N Gene Struct Expr 1759:526–534Google Scholar
  112. Yoshino TP, Cheng TC (1976) Experimentally induced elevation of aminopeptidase activity in hemolymph cells of the American oyster, Crassostrea virginica. J Invertebr Pathol 27:367–370PubMedGoogle Scholar
  113. Yoshino TP, Dinguirard N, Kunert J, Hokke CH (2008) Molecular and functional characterization of a tandem-repeat galectin from the freshwater snail Biomphalaria glabrata, intermediate host of the human blood fluke Schistosoma mansoni. Gene 411:46–58PubMedGoogle Scholar
  114. Zhai J, Lin H, Nie Z, Wu J, Canete-Soler R, Schlaepfer WW, Schlaepfer DD (2003) Direct interaction of focal adhesion kinase with p190RhoGEF. J Biol Chem 278:24865–24873PubMedGoogle Scholar
  115. Zhang HM, Cheung P, Yanagawa B, Mcmanus BM, Yang DC (2003) BNips: a group of pro-apoptotic proteins in the Bcl-2 family. Apoptosis 8:229–236PubMedGoogle Scholar
  116. Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1045–1062Google Scholar
  117. Zhou Q, Zhao J, Stout JG, Luhm RA, Wiedmer T, Sims PJ (1997) Molecular cloning of human plasma membrane phospholipid scramblase. a protein mediating transbilayer movement of plasma membrane phospholipids. J Biol Chem 272:18240–18244PubMedGoogle Scholar
  118. Zhou Q, Zhao J, Wiedmer T, Sims PJ (2002) Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood 99:4030–4038PubMedGoogle Scholar
  119. Zhou Z, Yang H, Xu X, Wang X, Lai R (2006) The first report of kininogen from invertebrates. Biochem Biophys Res Commun 347:1099–1102PubMedGoogle Scholar
  120. Zhu L, Song L, Chang Y, Xu W, Wu L (2006) Molecular cloning, characterization and expression of a novel serine proteinase inhibitor gene in bay scallops (Argopecten irradians, Lamarck 1819). Fish Shellfish Immunol 20:320–331PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Steven Roberts
    • 1
  • Giles Goetz
    • 2
  • Samuel White
    • 1
  • Frederick Goetz
    • 2
    Email author
  1. 1.School of Aquatic and Fishery SciencesUniversity of Washington—SeattleSeattleUSA
  2. 2.Great Lakes WATER InstituteUniversity of Wisconsin—MilwaukeeMilwaukeeUSA

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