Comparative proteomic analysis of a sea urchin (Heliocidaris erythrogramma) antibacterial response revealed the involvement of apextrin and calreticulin

Journal of Invertebrate Pathology

Volumn 106, Issue 2, 2011, Pages 223-229

  Dheilly, Nolwenn M ^a   Haynes, Paul A ^a   Bove, Ulysse ^a   Nair, Sham V ^a   Raftos, David A ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Apextrin; Calreticulin; Comparative proteomics; Echinoderms; Invertebrate immunity; Liquid chromatography tandem mass spectrometry

Indexed keywords

BACTERIUM ANTIBODY; CALRETICULIN; HEET 1 PROTEIN, HELIOCIDARIS ERYTHROGRAMMA; HEET-1 PROTEIN, HELIOCIDARIS ERYTHROGRAMMA; PROTEIN;

ANIMAL; ARTICLE; COMPARATIVE STUDY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEOMICS; SEA URCHIN; VIBRIO; VIBRIOSIS;

ANIMALS; ANTIBODIES, BACTERIAL; CALRETICULIN; PROTEINS; PROTEOMICS; SEA URCHINS; VIBRIO; VIBRIO INFECTIONS;

BACTERIA (MICROORGANISMS); DEUTEROSTOMIA; ECHINODERMATA; ECHINOIDEA; HELIOCIDARIS ERYTHROGRAMMA; INVERTEBRATA; STRONGYLOCENTROTUS; STRONGYLOCENTROTUS PURPURATUS;

EID: 78751581603     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2010.09.008     Document Type: Article

References (36)

1. Al-Sharif W.Z., Sunyer J.O., Lambris J.D., Smith L.C. Sea urchin coelomocytes specifically express a homologue of the complement component C3. J. Immunol. 1998, 160:2983-2997.
2. Arosa F.A., de Jesus O., Porto G., Carmo A.M., de Sousa M. Calreticulin is expressed on the cell surface of activated human peripheral blood T lymphocytes in association with major histocompatibility complex class I molecules. J. Biol. Chem. 1999, 274:16917-16922.
3. Ball M.S., Karuso P. Mass spectral compatibility of four proteomics stains. J. Proteome Res. 2007, 6:4313-4320.
4. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell. Biol. 2000, 1:11-21.
5. Breci L., Hattrup E., Keeler M., Letarte J., Johnson R., Haynes P.A. Comprehensive proteomics in yeast using chromatographic fractionation, gas phase fractionation, protein gel electrophoresis, and isoelectric focusing. Proteomics 2005, 5:2018-2028.
6. Chia F.S., Xing J. Echinoderm coelomocytes. Zoological Studies 1996, 35:231-254.
7. Clow L.A., Gross P.S., Shih C.-S., Smith L.C. Expression of SpC3, the sea urchin complement component, in response to lipopolysaccharide. Immunogenetics 2000, 51:1021-1033.
8. Clow L.A., Raftos D.A., Gross P.S., Smith L.C. The sea urchin complement homologue, SpC3, functions as an opsonin. J. Exp. Biol. 2004, 207:2147-2155.
9. Corda D., Di Girolamo M. Mono-ADP-Ribosylation: a tool for modulating immune response and cell signalling. Sci. STKE 2002, 2002:53.
10. Dupuis M., Schaerer E., Krause K., Tschopp J. The calcium-binding protein calreticulin is a major constituent of lytic granules in cytolytic T lymphocytes. J. Exp. Med. 1993, 177:1-7.
11. Ebert T.A., Southon J.R. Red sea urchins (Strongylocentrotus franciscanus) can live over 100 years: confirmation with A-bomb 14 carbon. Fish Bull. (Sacramento, Calif.) 2003, 101:915.
12. 2+-binding chaperone of the endoplasmic reticulum, Int. J. Biochem. Cell Biol. 2005, 37:260-266.
13. Gerardi G., Lassegues M., Canicatti C. Cellular distribution of sea urchin antibacterial activity. Biol. Cell. 1990, 70:153-157.
14. Gross P.S., Al-Sharif W.Z., Clow L.A., Smith L.C. Echinoderm immunity and the evolution of the complement system. Dev. Comp. Immunol. 1999, 23:429-442.
15. Gross P.S., Clow L.A., Smith L.C. SpC3, the complement homologue from the purple sea urchin, Strongylocentrotus purpuratus, is expressed in two subpopulations of the phagocytic coelomocytes. Immunogenetics 2000, 51:1034-1044.
16. Haag E.S., Sly B.J., Andrews M.E., Raff R.A. Apextrin, a novel extracellular protein associated with larval ectoderm evolution in Heliocidaris erythrogramma. Dev. Biol. 1999, 211:77-87.
17. Hamm H.E. The many faces of G protein signalling. J. Biol. Chem. 1998, 273:669-672.
18. Haug T., Kjuul A.K., Styrvold O.B., Sandsdalen E., Olsen O.M., Stensvag K. Antibacterial activity in Strongylocentrotus droebachiensis (Echinoidea), Cucumaria frondosa (Holothuroidea), and Asterias rubens (Asteroidea). J. Invertebr. Pathol. 2002, 81:94-102.
19. Haynes P.A., Miller S., Radabaugh T., Galligan M., Breci L., Rohrbough J., Hickman F., Merchant N. The wildcat toolbox: a set of perl script utilities for use in peptide mass spectral database searching and proteomics experiments. J. Biomol. Technol. 2006, 17:97-102.
20. Hibino T., Loza-Coll M., Messier C., Majeske A., Cohen A.H., Terwilliger D.P., Buckley K.M., Brockton V., Nair S.V., Berney K., Fugmann S.D., Anderson M.K., Pancer Z., Cameron R.A., Smith L.C., Rast J.P. The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 2006, 300:349-365.
21. Huang G., Liu H., Han Y., Fan L., Zhang Q., Liu J., Yu X., Zhang L., Chen S., Dong M., Wang L., Xu A. Profile of acute immune response in Chinese amphioxus upon Staphylococcus aureus and Vibrio parahaemolyticus infection. Dev. Comp. Immunol. 2007, 31:1013-1023.
22. Miller D.J., Hemmrich G., Ball E., Hayward D., Khalturin K., Funoyama N., Agata K., Bosch T.C.G. The innate immune repertoire in cnidaria-ancestral complexity and stochastic gene loss. Genome Biol. 2007, 8:R59.
23. Nair S.V., Del Valle H., Gross P.S., Terwilliger D.P., Smith L.C. Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol. Genomics 2005, 22:33-47.
24. Oh-hora M., Rao A. Calcium signaling in lymphocytes. Curr. Opin. Immunol. 2008, 20:250-258.
25. Rast J.P., Smith L.C., Loza-Coll M., Hibino T., Litman G.W. Genomic insights into the immune system of the sea urchin. Science 2006, 314:952-956.
26. Roberts M.R., de Bruxelles G.L. Plant 14-3-3 protein families: evidence for isoform-specific functions?. Biochem. Soc. Trans. 2002, 30:373-378.
27. Rohrbough J.G., Breci L., Merchant N., Miller S., Haynes P.A. Verification of single-peptide protein identifications by the application of complementary database search algorithms. J. Biomol. Technol. 2006, 17:327-332.
28. Rosado C.J., Kondos S., Bull T.E., Kuiper M.J., Law R.H., Buckle A.M., Voskoboinik I., Bird P.I., Trapani J.A., Whisstock J.C., Dunstone M.A. The MACPF/CDC family of pore-forming toxins. Cell Microbiol. 2008, 10:1765-1774.
29. Service M., Wardlaw A. Echinochrome-A as a bactericidal substance in the coelomic fluid of Echinus esculentus (L.). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1984, 79:161-165.
30. Smith L., Britten R., Davidson E. SpCoel1: a sea urchin profilin gene expressed specifically in coelomocytes in response to injury. Mol. Biol. Cell 1992, 3:403-414.
31. Smith L., Britten R., Davidson E. Lipopolysaccharide activates the sea urchin immune system. Dev. Comp. Immunol. 1995, 19:217-224.
32. Smith L., Chang L., Britten R., Davidson E. 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. 1996, 156:593-602.
33. Smith L.C., Shih C.-S., Dachenhausen S.G. Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J. Immunol. 1998, 161:6784-6793.
34. Stabili L., Pagliara M., Metrangolo M., Canicatti C. Comparative aspects of Echinoidea cytolysins: the cytolytic activity of Spherechinus granularis (Echinoidea) coelomic fluid. Comp. Biochem. Physiol. 1992, 101A:553-556.
35. Terwilliger D., Buckley K., Brockton V., Ritter N., Smith L.C. Distinctive expression patterns of 185/333 genes in the purple sea urchin, Strongylocentrotus purpuratus: an unexpectedly diverse family of transcripts in response to LPS, beta-1, 3-glucan, and dsRNA. BMC Mol. Biol. 2007, 8:16.
36. Wilson G.S., Raftos D.A., Corrigan S.L., Nair S.V. Diversity and antimicrobial activities of surface-attached marine bacteria from Sydney Harbour, Australia. Microbiol. Res. 2010, 165:300-311.