Characterization of the major plasma protein of the eastern oyster, Crassostrea virginica, and a proposed role in host defense

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 158, Issue 1, 2011, Pages 9-22

  Itoh, Naoki ^a   Xue, Qing Gang ^a   Schey, Kevin L ^b   Li, Yanli ^a   Cooper, Richard K ^a   La Peyre, Jerome F ^a  

^a LOUISIANA STATE UNIVERSITY AGRICULTURAL CENTER   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cavortin; Dominin; Extrapallial fluid; Invertebrate immunity; Iron binding; Mussels; Oysters; Plasma; Superoxide dismutase

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; DOMININ; MESSENGER RNA; PLASMA PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; HOST RESISTANCE; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OYSTER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CRASSOSTREA GIGAS; CRASSOSTREA VIRGINICA; INVERTEBRATA; OSTREIDAE; PERNA CANALICULUS; SACCOSTREA GLOMERATA;

EID: 78649634592     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.06.006     Document Type: Article

References (67)

1. Abebe A.T., Devoid S.J., Sugumaran M., Etter R., Robinson W.E. Identification and quantification of histidine-rich glycoprotein (HRG) in the blood plasma of six marine bivalves. J. Comp. Biochem. Physiol. B 2007, 147:74-81.
2. Acton R.T., Bennet J.C., Evans E.E., Schrohenloher R.E. Physical and chemical characterization of an oyster hemagglutinin. J. Biol. Chem. 1969, 244:4128-4135.
3. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
4. Banci L., Bertini I., Calderone V., Cramaro F., Conte R.D., Fantoni A., Mangani S., Quattrone A., Viezzoli M.S. A prokaryotic superoxide dismutase paralog lacking two Cu ligands: from largely unstructured in solution to ordered in the crystal. Proc. Natl Acad. Sci. USA 2005, 102:7541-7546.
5. Bao Y., Li L., Wu Q., Zhang G. Cloning, characterization, and expression analysis of extracellular copper/zinc superoxide dismutase gene from bay scallop Argopecten irradians. Fish Shellfish Immunol. 2009, 27:17-25.
6. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
7. Blom N., Gammeltoft S., Brunak S. Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 1999, 294:1351-1362.
8. Bordo D., Djinović K., Bolognesi M. Conserved patterns in the Cu, Zn superoxide dismutase family. J. Mol. Biol. 1994, 238:366-386.
9. Bourne Y., Redford S.M., Steinman H.M., Lepock J.R., Tainer J.A., Getzoff E.D. Novel dimeric interface and electrostatic recognition in bacterial Cu. Zn superoxide dismutase. Proc. Natl Acad. Sci. USA 1996, 93:12774-12779.
10. Brown R.S., 1975. Evidence of metal-protein complexes precipitating around blood cells as the mechanism of extracellular blood clotting in the American oyster Crassostrea virginica (Gmelin). Ph.D. dissertation, Baltimore, MD: John Hopkins University, 106 pp.
11. Candiano G., Petretto A., Bruschi M., Santucci L., Dimuccio V., Prunotto M., Gusmano R., Urbani A., Chiggeri G.M. J. Proteomics 2009, 73:188-195.
12. Cellura C., Toubiana M., Parrinello N., Roch P. HSP70 gene expression in Mytilus galloprovincialis hemocytes is triggered by moderate heat shock and Vibrio anguillarum, but not V. splendidus or Micrococcus lysodeikticus. Dev. Comp. Immunol. 2006, 30:984-997.
13. Chang W.-C., Lee T.-Y., Shien D.-M., Hsu J.B.-K., Horng J.-T., Hsu P.-C., Wang T.-Y., Huang H.-D., Pan R.-L. Incorporating support vector machine for identifying protein tyrosine sulfation sites. J. Comput. Chem. 2009, 30:2526-2537.
14. Creighton T.E. Disulfide bond formation in proteins. Meth. Enzymol. 1984, 107:305-329.
15. Denz C.R., Dube D.K. The benefits of 28S rRNA for standardization of reverse transcription-polymerase chain reaction for studying gene expression. Anal. Biochem. 2005, 341:382-394.
16. Devoid S.J., Etter R., Sugumaran M., Wallace G.T., Robinson W.E. Histidine-rich glycoprotein from the hemolymph of the marine mussel Mytilus edulis L. binds class A, class B, and borderline metals. Environ. Toxicol. Chem. 2007, 26:872-877.
17. Fernandez-Robledo J.-A.F., Courville P., Cellier M.F.M., Vasta G.R. Gene organization and expression of the divalent cation transporter Nramp in the protistan parasite Perkinsus marinus. J. Parasitol. 2004, 90:1004-1014.
18. Fisher W.S. Antimicrobial activity of copper and zinc accumulated in eastern oyster amebocytes. J. Shellfish Res. 2004, 23:321-351.
19. Gauthier J.D., Vasta G.R. Inhibition of in vitro replication of the oyster parasite Perkinsus marinus by the natural iron chelators transferrin, lactoferrin and desferrrioxamine. Dev. Comp. Immunol. 1994, 18:277-286.
20. Georges S.G., Pirie B.J.S. Metabolism of zinc in the mussel Mytilus edulis (L.): a combined ultrastructural and biochemical study. J. Mar. Biol. Assoc. UK 1980, 60:575-590.
21. Georges S.G., Pirie B.J.S., Frazier J.M. Efects of cadmium exposure on metal-containing granules of the oyster Ostrea edulis. Mar. Biol. 1983, 76:63-66.
22. Giribet G., Wheeler W. On bivalve phylogeny: a high-level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data. Invertebr. Biol. 2002, 12:271-324.
23. Gonzalez M., Romestand B., Fievet J., Huvet A., Lebart M., Gueguen Y., Bachère E. Evidence in oyster of a plasma extracellular superoxide dismutase which binds LPS. Biochem. Biophys. Res. Commun. 2005, 338:1089-1097.
24. Gonzalez M., Gueguen Y., Desserre G., de Lorgeril J., Romestand B., Bachère E. Molecular characterization of two isoforms of defensin from hemocytes of the oyster Crassostrea gigas. Dev. Comp. Immunol. 2007, 31:332-339.
25. Green T.J., Dixon T.J., Devic E., Adlard R.D., Barnes A.C. Differential expression of genes encoding anti-oxidant enzymes in Sydney rock oysters, Saccostrea glomerata (Gould) selected for disease resistance. Fish Shellfish Immunol. 2009, 26:799-810.
26. Halliwell B. Albumin-an important extracellular antioxidant?. Biochem. Pharmacol. 1988, 37:569-571.
27. Hamilton M.G., Fernandez J., 2005. Is the 1.9 megadalton protein found in the hemolymph of oysters 'cavortin'? FEBS meeting abstracts http://www.febs-iubmb-2005.com/abs_abs.php?aid=1381.
28. Hattan S.J., Laue T.M., Chasteen N.D. Purification and characterization of a novel-calcium binding protein from the extrapallial fluid of the mollusk Mytilus edulis. J. Biol. Chem. 2001, 276:4461-4468.
29. Howard D.W., Smith C.S. Histological techniques for marine bivalves mollusks. NOAA technical memorandum NMFS-F/NEC-25. Woods Hole 1983, US Department of Commerce, Massachusetts.
30. Huvet A., Herpin A., Degremont L., Labreuche Y., Samain J., Cunningham C. The identification of genes from the oyster Crassostrea gigas that are differentially expressed in progeny exhibiting opposed susceptibility to summer mortality. Gene 2004, 343:211-220.
31. Itoh N., Xue Q.-G., Li Y., Cooper R., La Peyre J.F. cDNA cloning and tissue expression of plasma lysozyme in the eastern oyster, Crassostrea virginica. Fish Shellfish Immunol. 2007, 23:957-968.
32. Johnstone M.B., Ellis S., Mount A.S. Visualization of shell matrix proteins in hemocytes and tissues of eastern oyster, Crassostrea virginica. J. Exp. Zool. (Mol. Dev. Evol.) 2008, 310B:227-239.
33. Kozak M. Initiation of translation in prokaryotes and eukaryotes. Gene 1999, 234:187-208.
34. La Peyre J.F., Chu F.-L.C., Meyers J.M. Haemocytic and humoral activities of eastern and Pacific oysters following challenge by the protozoan Perkinsus marinus. Fish Shellfish Immunol. 1995, 5:179-190.
35. La Peyre J.F., Xue Q.-G., Itoh N., Li Y., Cooper R.K. Serine protease inhibitor cvSI-1 potential role in the eastern oyster host defense against the protozoan parasite Perkinsus marinus. Dev. Comp. Immunol. 2010, 34:84-92.
36. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
37. Landis G.N., Tower J. Superoxide dismutase evolution and life span regulation. Mech. Age Dev. 2005, 126:365-379.
38. Larade K., Storey K.B. Living without oxygen: anoxia-responsive gene expression and regulation. Curr. Genomics 2009, 10:76-85.
39. Liu W., Saint D.A. A new quantitative method of real time reverse transcription polymerase chain reaction assays based on simulation of polymerase chain reaction kinetics. Anal. Biochem. 2002, 302:52-59.
40. Marchler-Bauer A., Anderson J.B., Cherukuri P.F., DeWeese-Scott C., Geer L.Y., Gwadz M., He S., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Liebert C.A., Liu C., Lu F., Marchler G.H., Mullokandov M., Shoemaker B.A., Simonyan V., Song J.S., Thiessen P.A., Yamashita R.A., Yin J.J., Zhang D., Bryant S.H. CDD: A Conserved Domain Database for protein classification. Nucleic Acids Res. 2005, 33:192-196.
41. Martin A.W., Harrison F.M., Huston M.I., Stewart D.M. The blood volumes of some representative mollusks. J. Exp. Biol. 1958, 35:260-279.
42. Myers J.M., Johnstone M.B., Mount A.S., Silverman H., Wheeler A.P. TEM immunocytochemistry of a 48kDa MW organic matrix phosphoprotein produced in the mantle epithelial cells of Eastern oyster (Crassostrea virginica). Tissue Cell 2007, 39:247-256.
43. Nair P.S., Robinson W.E. Purification and characterization of a histidine-rich glycoprotein that binds cadmium from the blood plasma of the bivalve Mytilus edulis. Arch. Biochem. Biophys. 1999, 366:8-14.
44. Nielsen S.A., Frieden E. Some chemical and kinetic properties of oyster carbonic anhydrase. Comp. Biochem. Physiol. B 1972, 41:875-889.
45. Oury T.D., Crapo J.D., Valnickova Z., Enghild J.J. Human extracellular superoxide dismutase is a tetramer composed of two disulphide-linked dimers: a simplified, high-yield purification of extracellular superoxide dismutase. Biochem. J. 1996, 17:51-57.
46. Petersen S.V., Oury T.D., Valnickova Z., Thogersen I.B., Hojrup P., Crapo J.D., Enghild J.J. The dual nature of human extracellular superoxide dismutase: one sequence and two structures. Proc. Natl Acad. Sci. USA 2003, 100:13875-13880.
47. Renwrantz L., Werner I. Origin of a metal-binding protein in serum of Mytilus edulis. J. Mol. Stud. 2008, 74:11-17.
48. Renwrantz L., Schmalmach W., Steenbuck M. Molecular size of native proteins of Mytilus serum which contains a dominant fraction with heavy metal-binding properties. Comp. Biochem. Physiol. A 1998, 121:175-180.
49. Robinson W.E., Ryan D.K. Transport of cadmium and other metals in the blood of the bivalve mollusk Mercenaria mercenaria. Mar. Biol. 1988, 97:101-109.
50. Rusenko K.W., Donachy J.E., Wheeler A.P. Purification and characterization of a shell matrix phosphoprotein from the American oyster. Surface Reactive Peptides and Polymers 1991, 107-124. ACS Books, Washington DC. C.S. Sikes, A.P. Wheeler (Eds.).
51. Scatena M., Liaw L., Giachelli C.M. Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2302-2309.
52. Schneeweiss H., Scmalmack W., Luedeking A., Jarck F., Behlich L.-K., Back F. Heavy Metal Binding Protein HIP 2002, Swiss-Prot Database, Swiss Institute of Bioinformatics, Geneva, Switzerland, Accesssion number P83425.
53. Scotti P.D., Dearing S.C., Greenwood D.R., Newcomb R.D. Pernin: a novel, self-aggregating haemolymph protein from the New Zealand Green-lipped mussel, Perna canaliculus (Bivalvia: Mytilidae). Comp. Biochem. Physiol. B 2001, 128:767-779.
54. Scotti P.D., Dearing S.C., Greenwood D.R. Characterisation of cavortin, the major haemolymph protein of the Pacific oyster (Crassostrea gigas). N.Z. J. Mar. Freshwater Res. 2007, 41:91-101.
55. Simonian M., Nair S.V., Nell J.A., Raftos D.A. Proteomic clues to the identification of QX disease-resistance biomarkers in selectively bred Sydney rock oysters, Saccostrea glomerata. J. Proteomics 2009, 73:209-217.
56. Storey K.B., Storey J.M. Tribute to PI Lutz: Putting life on 'pause'-molecular regulation of hypometabolism. J. Exp. Biol. 2007, 210:1700-1714.
57. Tan N.S., Ng M.L.P., Yau Y.H., Chong P.K.W., Ho B., Ding J.L. Definition of endotoxin binding sites in horseshoe crab factor C recombinant sushi proteins and neutralization of endotoxin by sushi peptides. FASEB J. 2000, 14:1801-1813.
58. Tanguy A., Guo X., Ford S.E. Discovery of genes expressed in response to Perkinsus marinus challenge in Eastern (Crassostrea virginica) and Pacific (C. gigas) oysters. Gene 2004, 338:121-131.
59. Taris N., Lang R.P., Reno P.W., Camara M.D. Transcriptome response of the Pacific oyster (Crassostrea gigas) to infection with Vibrio tubiashii using cDNA AFLP differential display. Anal. Genet. 2009, 40:663-677.
60. Thellin O., Zorzi W., Lakaye B., De Borma B., Coumans B., Hennen G., Grisar T., Igout A., Heinen E. Housekeeping genes as internal standards: use and limits. J. Biotechnol. 1999, 75:291-295.
61. Thompson R.J., Bayne C.J., Moore M.N., Carefoot T.H. Hemolymph volume, changes in biochemical composition of blood, and cytological responses of digestive cells in Mytilus californianus Conrad, induced by nutritional, thermal and exposure stress. J. Comp. Physiol. 1978, 127:287-298.
62. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The clustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 24:4876-4882.
63. Tripp M.R. Hemagglutinin in the blood of the eastern oyster. J. Invertebr. Pathol. 1966, 8:478-484.
64. Xue Q.G., Waldrop G.L., Schey K.L., Itoh N., Ogawa M., Cooper R.K., Losso J.N., La Peyre J.F. A novel slow-tight binding serine protease inhibitor from eastern oyster (Crassostrea virginica) plasma inhibits perkinsin, the major extracellular protease of the oyster protozoan parasite Perkinsus marinus. Comp. Biochem. Physiol. B 2006, 145:16-26.
65. Yin Y., Huang J., Paine M.L., Reinhold P.V., Chasteen N.D. Structural characterization of the major extrapallial fluid protein of the mollusk Mytilus edulis: implications for function. Biochemistry 2005, 44:10720-10731.
66. Zhang C., Zhang R. Matrix proteins in the outer shells of mollusks. Mar. Biotechnol. 2006, 8:572-586.
67. Zhao G., Bou-Abdallah F., Yang X., Arosio P., Chasteen N.D. Is hydrogen peroxide produced during iron (II) oxidation in mammalian apoferritins. Biochemistry 2001, 40:10832-10838.