Proteomic characterization of the hemolymph of Octopus vulgaris infected by the protozoan parasite Aggregata octopiana

Journal of Proteomics

Volumn 105, Issue , 2014, Pages 151-163

  Castellanos Martínez, Sheila ^a   Diz, Angel P ^b   Álvarez Chaver, Paula ^b   Gestal, Camino ^a  

^a INSTITUTO DE INVESTIGACIONES MARINAS   (Spain)

^b UNIVERSITY OF VIGO   (Spain)

Author keywords

Aggregata octopiana; Hemolymph; Immune response; Mass spectrometry; Octopus vulgaris; Proteome

Indexed keywords

BIOLOGICAL MARKER; FASCIN; FILAMIN; PEROXIREDOXIN; RNA; PROTEOME;

AGGREGATA OCTOPIANA; AQUACULTURE; ARTICLE; BLOOD CELL; CEPHALOPOD; CONTROLLED STUDY; DATA BASE; GASTROINTESTINAL DISEASE; GENOMICS; HEMOLYMPHATIC SYSTEM; HOST PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL TOLERANCE; INFECTION; MALABSORPTION; MASS SPECTROMETRY; NONHUMAN; NUTRITIONAL STATUS; OCTOPUS VULGARIS; PARASITE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; PROTOZOON; TWO DIMENSIONAL ELECTROPHORESIS; ANIMAL; COCCIDIA; COCCIDIOSIS; HEMOLYMPH; METABOLISM; OCTOPUS; PARASITOLOGY; PROCEDURES; VETERINARY;

AGGREGATA OCTOPIANA; CEPHALOPODA; COCCIDIA; MOLLUSCA; OCTOPUS; OCTOPUS VULGARIS; PROTOZOA;

ANIMALS; COCCIDIA; COCCIDIOSIS; HEMOLYMPH; OCTOPODIFORMES; PROTEOME; PROTEOMICS;

EID: 84901820987     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.12.008     Document Type: Article

References (67)

1. García-García J., Rodríguez-Gonzalez L.M., García-García B. Cost analysis of octopus ongrowing installation in Galicia. Span J Agric Res 2004, 2:531-537.
2. Berthe F.C.J. Diseases in mollusc hatcheries and their paradox in health management. Dis Asian Aquac V: Fish Health Sect 2005, 239-248. Asian Fisheries Society, Manila. P. Walker, R. Lester, M.G. Bondad-Reantaso (Eds.).
3. Hochberg F.G. Diseases of Mollusca: Cephalopoda. Dis mar anim vol 3: Cephalopoda Urochordata 1990, 47-227. Biologisches Anstalt Helgoland, Hamburg. O. Kinne (Ed.).
4. Pascual S., Gestal C., Estévez J.M., Rodríguez H., Soto M., Abollo E., et al. Parasites in commercially-exploited cephalopods (Mollusca, Cephalopoda) in Spain: an updated perspective. Aquaculture 1996, 142:1-10.
5. Gestal C., Abollo E., Pascual S. Observations on associated histopathology with Aggregata octopiana infection (Protista: Apicomplexa) in Octopus vulgaris. Dis Aquat Org 2002, 50:45-49.
6. Gestal C., Páez de la Cadena M., Pascual S. Malabsorption syndrome observed in the common octopus Octopus vulgaris infected with Aggregata octopiana (Protista: Apicomplexa). Dis Aquat Org 2002, 1:61-65.
7. Gestal C., Guerra A., Pascual S. Aggregata octopiana (Protista: Apicomplexa): a dangerous pathogen during commercial Octopus vulgaris ongrowing. ICES J Mar Sci 2007, 64:1743-1748.
8. Roch P. Defense mechanisms and disease prevention in farmed marine invertebrates. Aquaculture 1999, 72:125-145.
9. Malham S.K., Runham N.W. A brief review of the immunobiology of Eledone cirrhosa. S Afr J Mar Sci 1998, 20:385-391.
10. Ford L.A. Host defense mechanisms of cephalopods. Annu Rev Fish Dis 1992, 25-41.
11. Novoa B., Tafalla C., Guerra A., Figueras A. Cellular immunological parameters of the octopus, Octopus vulgaris. J Shellfish Res 2002, 21:243-248.
12. Rodríguez-Domínguez H., Soto-Búa M., Iglesias-Blanco R., Crespo-González C., Arias-Fernández C., García-Estévez J. Preliminary study on the phagocytic ability of Octopus vulgaris Cuvier, 1797 (Mollusca: Cephalopoda) haemocytes in vitro. Aquaculture 2006, 254:563-570.
13. Cheng T.C. Functional morphology and biochemistry of molluscan phagocytes. Ann N Y Acad Sci 1975, 226:343-379.
14. Rögener W., Renwrantz L., Unlenbruck G. Isolation and characterization of a lectin from the hemolymph of the cephalopod Octopus vulgaris (Lam.) inhibited by α-d-lactose and n-acetyl-lactosamine. Dev Comp Immunol 1985, 9:605-616.
15. Alpuche J., Pereyra A., Mendoza-Hernández G., Agundis C., Rosas C., Zenteno E. Purification and partial characterization of an agglutinin from Octopus maya serum. Comp Biochem Physiol B 2010, 156:1-5.
16. Gardy J.L., Lynn D.J., Brinkman F.S.L., Hancock R.E.W. Enabling a systems biology approach to immunology: focus on innate immunity. Trends Immunol 2009, 30:249-262.
17. Wang L., Song L., Zhao J., Qiu L., Zhang H., Xu W., et al. Expressed sequence tags from the zhikong scallop (Chlamys farreri): discovery and annotation of host-defense genes. Fish Shellfish Immunol 2009, 26:744-750.
18. Gueguen Y., Cadore J.P., Flament D., Barreau-Roumiguière C., Girardot A.L., Garnier J., et al. Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 2003, 303:139-145.
19. Perrigault M., Tanguy A., Allam B. Identification and expression of differentially expressed genes in the hard clam, Mercenaria mercenaria, in response to quahog parasite unknown (QPX). BMC Genomics 2009, 10:377. 10.1186/1471-2164-10-377.
20. Prado-Alvarez M., Gestal C., Novoa B., Figueras A. Differentially expressed genes of the carpet Shell clam Ruditapes decussatus against Perkinsus olseni. Fish Shellfish Immunol 2009, 26:72-83.
21. Travers M.A., Meistertzheim A.L., Cardinaud M., Friedman C., Huachette S., Moraga D., et al. Gene expression patterns of abalone, Haliotis tuberculata, during successive infections by the pathogen Vibrio harveyi. J Invertebr Pathol 2010, 105:289-297.
22. López J.L. Two-dimensional electrophoresis in proteome expression analysis. J Chromatogr B 2007, 849:190-202.
23. Diz A.P., Martínez-Fernandez M., Rolán-Alvarez E. Proteomics in evolutionary ecology: linking the genotype with the phenotype. Mol Ecol 2012, 21(5):1060-1080.
24. Albertin C.B., Bonnaud L., Brown C.T., Crookes-Goodson W.J., da Fonseca R.R., Di Cristo C., et al. Cephalopod genomics: a plan of strategies and organization. Stand Genomic Sci 2012, 7:175-188.
25. Schleicher R.R., Nyholm S. V. Characterizing the host and symbiont proteomes in the association between the bobtail squid, Euprymna scolopes, and the bacterium, Vibrio fischeri. PLoS ONE 2011, 6(10):e25649.
26. Collins A.J., Schleicher T.R., Rader B.A., Nyholm S.V. Understanding the role of host hemocyte in a squid/Vibrio symbiosis using transcriptomics and proteomics. Front Immunol 2012, 3:1-14.
27. Messenger J.B., Nixon M., Ryan K.P. Magnesium chloride as an anaesthetic for cephalopods. Comp Biochem Physiol 1985, 82C:203-205.
28. Moltschaniwskyj N.A., Hall K., Lipinski M.R., Marian J.E.A.R., Nishiguchi M., Saki M., et al. Ethical and welfare considerations when using cephalopods as experimental animals. Rev Fish Biol Fish 2007, 17:455-476.
29. Culling C.F.A., Allison R.T., Barr W.T. Cellular pathology techniques 1985, Butterworth &Co, London.
30. Ramagli L.S., Rodríguez L.V. Quantitation of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 1985, 6:559-563.
31. Pernemalm M., Lewensohn R., Lehtiö J. Affinity prefractionation for MS-based plasma proteomics. Proteomics 2009, 9:1420-1427.
32. Diz A.P., Skibinski D.O.F. Evolution of 2-DE protein patterns in a mussel hybrid zone. Proteomics 2007, 7:2111-2120.
33. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal Chem 1996, 68:850-858.
34. Diz A.P., Carvajal-Rodríguez A., Skibinski D.O.F. Multiple hypotheses testing in proteomics: a strategy for experimental work. Mol Cell Proteomics 2011, 10. [M110.004374].
35. Carvajal-Rodríguez A., Uña-Alvarez J. Assessing significance in high-throughput experiments by Sequential Goodness of Fit and q-value estimation. PLoS ONE 2011, 6(9):e24700.
36. Carvajal-Rodríguez A., Uña-Alvarez J., Rolán-Alvarez E. A new multitest correction (SGoF) that increases its statistical power when increasing the number of tests. BMC Bioinforma 2009, 10:209.
37. Andersen C.L., Jensen J.L., Orntoft T.F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer datasets. Cancer Res 2004, 64:5245-5250.
38. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3(7). [research0034].
39. Pfaffl M.W., Tichopad A., Prgomet C., Neuvians T.P. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 2004, 26:509-515.
40. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:2002-2007.
41. Molloy M.P., Brzezinski E.E., Hang J., McDowell M.T., VanBogelen R.A. Overcoming technical variation and biological variation in quantitative proteomics. Proteomics 2003, 3:1912-1919.
42. Vaz-Pires P., Seixas P., Barbosa A. Aquaculture potential of the common octopus (Octopus vulgaris Cuvier, 1797): a review. Aquaculture 2004, 238:221-238.
43. Gestal C., Roch P., Renault T., Pallavicini A., Paillar Ch., Novoa B., et al. Study of diseases and the immune system of bivalves using molecular biology and genomics. Rev Fish Sci 2008, 16(S1):131-154.
44. Bouchut A., Sautiere P.E., Coustau C., Mitta G. Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of proteins from hemocytes revealed by a proteomic approach. Acta Trop 2006, 98:234-246.
45. Cao A., Fuentes J., Comesaña P., Casas S.M., Villalba A. A proteomic approach envisaged to analyse the bases of oyster tolerance/resistance to bonamiosis. Aquaculture 2009, 295:149-156.
46. Cha I.S., Castillo C.S., Nho S.W., Hikima J., Aoki T., Jung T.S. Innate immune response in the hemolymph of an ascidian, Halocynthia roretzi, showing soft tunic syndrome, using label-free quantitative proteomics. Dev Comp Immunol 2011, 35:809-816.
47. Riva C., Binelli A., Rusconi F., Colombo G., Pedriali A., Zippel R., et al. A proteomic study using zebra mussels (D. polymorpha) exposed to benzo (α) pyrene: the role of gender and exposure concentrations. Aquat Toxicol 2011, 104:14-22.
48. Doino L.J., McFall-Ngai M.J. Alterations in the proteome of the Euprymna scolopes light organ in response to symbiotic Vibrio fischeri. Appl Environ Microbiol 2000, 66(9):4091-4097.
49. Otero J., González F.A., Sieiro P.M., Guerra A. Reproductive cycle and energy allocation of Octopus vulgaris in Galician waters. Northeast Atlantic Fish Res 2007, 85(1-2):122-129.
50. Martínez-Fernández M., Rodríguez-Piñeiro A.M., Oliveira E., Páez de la Cadena M., Rolán-Alvarez E. Proteomic comparison between two marine snail ecotypes reveals details about the biochemistry of adaptation. J Proteome Res 2008, 7:4926-4934.
51. Goodson H.V., Hawse W.F. Molecular evolution of the actin family. J Cell Sci 2002, 115:2619-2622.
52. Morga B., Renault T., Faury N., Chollet B., Arzul I. Cellular and molecular responses of haemocytes from Ostrea edulis during in vitro infection by the parasite Bonamia ostreae. Int J Parasitol 2011, 41:755-764.
53. Vasselon T., Detmers A.P. Toll receptors: a central element in innate immune responses. Infec Immun 2002, 70:1033-1041.
54. Feng Y., Walsh C.A. The many faces of filamin: a versatile molecular scaffold for cell motility and signaling. Nat Cell Biol 2004, 6:1034-1038.
55. Yamashiro S., Yamakita Y., Ono S., Matsumura F. Fascin, and actin-bundling protein, induces membrane protrusion and increases cell motility of epithelial cells. Mol Biol Cell 1998, 9:993-1006.
56. Castellanos-Martínez S., Gestal C. Immune response of Octopus vulgaris against the infection by the gastrointestinal parasite Aggregata octopiana. J Shellfish Res 2011, 30:997-998.
57. Buttgereit F., Burmester G.R., Brand M.D. Bioenergetics of immune functions: fundamental and therapeutic aspects. Immunol Today 2000, 21:192-199.
58. Huang Q.Y., Fang C.W., Huang H.Q. Alteration of heart tissue protein profiles in acute cadmium-treated scallops Patinopecten yessoensis. Arch Environ Contam Toxicol 2011, 60:90-98.
59. Coyne V.E. The importance of ATP in the immune system of molluscs. Invertebr Surviv J 2011, 8:48-55.
60. Immenschuh S., Baumgart-Vogt E. Peroxiredoxins, oxidative stress, and cell proliferation. Antioxid Redox Signal 2005, 7:768-777.
61. Ahn H.M., Lee K.S., Lee D.S., Yu K. JNK/FOXO mediated peroxiredoxinV expression regulates redox homeostasis during Drosophila melanogaster gut infection. Dev Comp Immunol 2012, 38:466-473.
62. Castellanos-Martínez S., Gestal C. Pathogen and immune response of cephalopods. J Exp Mar Biol Ecol 2013, 447:14-22.
63. Volety A.K., Chu F.L.E. Suppression of chemiluminescence of eastern oyster (Crassostrea virginica) hemocytes by the protozoan parasite Perkinsus marinus. Dev Comp Immunol 1995, 19:135-142.
64. Novo E., Parola M. Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis Tissue Repair 2008, 1:5.
65. Barrett J., Jeffreries J.R., Brophy P.M. Parasite proteomics. Parasitol Today 2000, 16(9):400-403.
66. Rögener W., Renwrantz L., Uhlenbruck G. Analysis of Octopus vulgaris hemolymph containing a glycoprotein with blood group A-like properties. Comp Biochem Physiol 1987, 86B(2):347-351.
67. Van Holde K.E., Miller K.I. Hemocyanins. Adv Protein Chem 1995, 47:1-81.