Differential protein expression in two bivalve species; Mytilus galloprovincialis and Corbicula fluminea; exposed to Cylindrospermopsis raciborskii cells

Aquatic Toxicology

Volumn 101, Issue 1, 2011, Pages 109-116

  Puerto, Maria ^a   Campos, Alexandre ^b   Prieto, Ana ^a   Cameán, Ana ^a   Almeida, André Martinho de ^c,d,g   Coelho, Ana Varela ^d,e   Vasconcelos, Vitor ^a,f  

^a UNIVERSITY OF SEVILLE   (Spain)

^b UNIVERSITY OF PORTO   (Portugal)

^c INSTITUTO DE INVESTIGAÇÃO CIENTÍFICA TROPICAL   (Portugal)

^d INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^e UNIVERSITY OF ÉVORA   (Portugal)

^f UNIVERSITY OF PORTO   (Portugal)

^g FACULDADE DE MEDICINA VETERINÁRIA   (Portugal)

Author keywords

Corbicula fluminea; Cylindrospermopsin; Cylindrospermopsis raciborskii; Mytilus galloprovincialis; Proteomics

Indexed keywords

ACTIN; CYLINDROSPERMOPSIN; EXTRAPALLIAL FLUID PROTEIN; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 60; PROTEIN PRECURSOR; TRIOSEPHOSPHATE ISOMERASE; TUBULIN; UNCLASSIFIED DRUG;

BIVALVE; CYANOBACTERIUM; DEFENSE MECHANISM; GREEN ALGA; POLLUTION EXPOSURE; PROTEIN; PROTEOMICS; TOXICITY; TOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AQUATIC ENVIRONMENT; ARTICLE; BACTERIAL CELL; CHLORELLA VULGARIS; CONTROLLED STUDY; CORBICULA; CORBICULA FLUMINEA; CYLINDROSPERMOPSIS; CYLINDROSPERMOPSIS RACIBORSKII; DIGESTIVE SYSTEM; DOWN REGULATION; ECOTOXICOLOGY; ENZYME ACTIVITY; GILL; MYTILUS GALLOPROVINCIALIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE INJURY;

ALKALOIDS; ANIMALS; BACTERIAL TOXINS; CHAPERONIN 60; CORBICULA; CYLINDROSPERMOPSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION; MYTILUS; PORTUGAL; TRIOSE-PHOSPHATE ISOMERASE; URACIL;

ANIMALIA; BIVALVIA; CHLORELLA VULGARIS; CHLOROPHYTA; CORBICULA FLUMINEA; CYANOBACTERIA; CYLINDROSPERMOPSIS RACIBORSKII; MYTILUS GALLOPROVINCIALIS;

EID: 78649908934     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.09.009     Document Type: Article

References (56)

1. Almeida A.M., Campos A., Francisco R., Harten S.V., Cardoso L.A., Coelho A.V. Proteomic investigation of the effects of weight loss in the gastrocnemius muscle of wild and NZW rabbits via 2D-electrophoresis and MALDI-TOF MS. Anim. Genet. 2010, 41:260-272.
2. Alvarez C., Sztul E.S. Brefeldin A (BFA) disrupts the organization of the microtubule and the actin cytoskeletons. Eur. J. Cell Biol. 1999, 78:1-14.
3. Amorim Á., Vasconcelos V. Dynamics of microcystins in the mussel Mytilus galloprovincialis. Toxicon 1999, 37:1041-1052.
4. Bain P., Shaw G., Patel B. Induction of p53-regulated gene expression in human cell lines exposed to the cyanobacterial toxin cylindrospermopsin. J. Toxicol. Environ. Health A 2007, 70:1687-1693.
5. Bareyre F.M., Raghupathi R., Saatman K.E., McIntosh T.K. DNaseI disinhibition is predominantly associated with actin hyperpolymerization after traumatic brain injury. J. Neurochem. 2001, 77:173-181.
6. Bazin E., Mourot A., Humpage A.R., Fessard V. Genotoxicity of a freshwater cyanotoxin, cylindrospermopsin, in two human cell lines: Caco-2 and HepaRG. Environ. Mol. Mutagen. 2010, 51:251-259.
7. Berry J.P., Gibbs P.D.L., Schmale M.C., Saker M.L. Toxicity of cylindrospermopsin, and other apparent metabolites from Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum, to the zebrafish (Danio rerio) embryo. Toxicon 2009, 53:289-299.
8. Beyer D., Suranyi G., Vasas G., Roszik J., Erdodi F., M-Hamvas H., Bacsi I., Batori R., Serfozo Z., Szigeti Z.M., Vereb G., Demeter Z., Gonda S., Mathe C. Cylindrospermopsin induces alterations of root histology and microtubule organization in common reed (Phragmites australis) plantlets cultured in vitro. Toxicon 2009, 54:440-449.
9. Bláha L., Babica P., Hilscherová K., Upham B.L. Inhibition of gap-junctional intercellular communication and activation of mitogen-activated protein kinases by cyanobacterial extracts-indications of novel tumor-promoting cyanotoxins?. Toxicon 2010, 55:126-134.
10. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
11. Brown S.B., Bailey K., Savill J. Actin is cleaved during constitutive apoptosis. Biochem. J. 1997, 323:233-237.
12. Bursch W., Ellinger A., Gerner C., Frohwein U., Schulte-Hermann R. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others?. Ann. N.Y. Acad. Sci. 2000, 926:1-12.
13. Campos A., da Costa G., Coelho A., Fevereiro P. Identification of bacterial protein markers and enolase as a plant response protein in the infection of Olea europaea subsp. europaea by Pseudomonas savastanoi pv. savastanoi. Eur. J. Plant Pathol. 2009, 125:603-616.
14. Campos A., Vasconcelos V. Molecular mechanisms of microcystin toxicity in animal cells. Int. J. Mol. Sci. 2010, 11:268-287.
15. Fastner J., Rücker J., Stüken A., Preussel K., Nixdorf B., Chorus I., Köhler A., Wiedner C. Occurrence of the cyanobacterial toxin cylindrospermopsin in northeast Germany. Environ. Toxicol. 2007, 22:26-32.
16. Froscio S.M., Humpage A.R., Burcham P.C., Falconer I.R. Cell-free protein synthesis inhibition assay for the cyanobacterial toxin cylindrospermopsin. Environ. Toxicol. 2001, 16:408-412.
17. Froscio S.M., Humpage A.R., Wickramasinghe W., Shaw G., Falconer I.R. Interaction of the cyanobacterial toxin cylindrospermopsin with the eukaryotic protein synthesis system. Toxicon 2008, 51:191-198.
18. Gácsi M., Antal O., Vasas G., Máthé C., Borbély G., Saker M.L., Gyori J., Farkas A., Vehovszky A., Bánfalvi G. Comparative study of cyanotoxins affecting cytoskeletal and chromatin structures in CHO-K1 cells. Toxicol. In Vitro 2009, 23:710-718.
19. Gobom J., Nordhoff E., Mirgorodskaya E., Ekman R., Roepstorff P. Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J. Mass Spectrom. 1999, 34:105-116.
20. Griffiths D.J., Saker M.L. The Palm Island mystery disease 20 years on: a review of research on the cyanotoxin cylindrospermopsin. Environ. Toxicol. 2003, 18:78-93.
21. Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974, 249:7130-7139.
22. Hattan S.J., Laue T.M., Chasteen N.D. Purification and characterization of a novel calcium-binding protein from the extrapallial fluid of the mollusc Mytilus edulis. J. Biol. Chem. 2001, 276:4461-4468.
23. Hawkins P.R., Runnegar M.T., Jackson A.R., Falconer I.R. Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir. Appl. Environ. Microbiol. 1985, 50:1292-1295.
24. Humpage A.R., Fontaine F., Froscio S., Burcham P., Falconer I.R. Cylindrospermopsin genotoxicity and cytotoxicity: role of cytochrome P-450 and oxidative stress. J. Toxicol. Environ. Health A 2005, 68:739-753.
25. Ibarz A., Martín-Pérez M., Blasco J., Bellido D., Oliveira E.d., Fernández-Borràs J. Gilthead sea bream liver proteome altered at low temperatures by oxidative stress. Proteomics 2010, 10:963-975.
26. Kanlaya R., Pattanakitsakul S.-n., Sinchaikul S., Chen S.-T., Thongboonkerd V. Alterations in actin cytoskeletal assembly and junctional protein complexes in human endothelial cells induced by dengue virus infection and mimicry of leukocyte transendothelial migration. J. Proteome Res. 2009, 8:2551-2562.
27. Kinnear S.H.W., Fabbro L.D., Duivenvoorden L.J., Hibberd E.M.A. Multiple-organ toxicity resulting from cylindrospermopsin exposure in tadpoles of the cane toad (Bufo marinus). Environ. Toxicol. 2007, 22:550-558.
28. Koll H., Guiard B., Rassow J., Ostermann J., Horwich A.L., Neupert W., Hartl F.U. Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell 1992, 68:1163-1175.
29. Lawrence R.A., Burk R.F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 1976, 71:952-958.
30. Leyva J.A., Bianchet M.A., Amzel L.M. Understanding ATP synthesis: structure and mechanism of the F1-ATPase. Mol. Membr. Biol. 2003, 20:27-33. Review.
31. Martins J.C., Leão P.N., Vasconcelos V. Differential protein expression in Corbicula fluminea upon exposure to a Microcystis aeruginosa toxic strain. Toxicon 2009, 53:409-416.
32. Metcalf J.S., Barakate A., Codd G.A. Inhibition of plant protein synthesis by the cyanobacterial hepatotoxin, cylindrospermopsin. FEMS Microbiol. Lett. 2004, 235:125-129.
33. Mihali T.K., Kellmann R., Muenchhoff J., Barrow K.D., Neilan B.A. Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis. Appl. Environ. Microbiol. 2008, 74:716-722.
34. Neuhoff V., Arold N., Taube D., Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 1988, 9:255-262.
35. Nogueira I.C.G., Saker M.L., Pflugmacher S., Wiegand C., Vasconcelos V.M. Toxicity of the cyanobacterium Cylindrospermopsis raciborskii to Daphnia magna. Environ. Toxicol. 2004, 19:453-459.
36. Ohtani I., Moore R.E., Runnegar M.T.C. Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. J. Am. Chem. Soc. 1992, 114:7941-7942.
37. Ou K., Yu K., Kesuma D., Hooi M., Huang N., Chen W., Lee S.Y., Goh X.P., Tan L.k., Liu J., Soon S.Y., Bin Abdul Rashid S., Putti T.C., Jikuya H., Ichikawa T., Nishimura O., Salto-Tellez M., Tan P. Novel breast cancer biomarkers identified by integrative proteomic and gene expression mapping. J. Proteome Res. 2008, 7:1518-1528.
38. Pandey A., Mann M. Proteomics to study genes and genomes. Nature 2000, 405:837-846.
39. Riedmaier I., Tichopad A., Reiter M., Pfaffl M.W., Meyer H.H.D. Identification of potential gene expression biomarkers for the surveillance of anabolic agents in bovine blood cells. Anal. Chim. Acta 2009, 638:106-113.
40. Rogers E.H., Zehr R.D., Gage M.I., Humpage A.R., Falconer I.R., Marr M., Chernoff N. The cyanobacterial toxin, cylindrospermopsin, induces fetal toxicity in the mouse after exposure late in gestation. Toxicon 2007, 49:855-864.
41. Saker M.L., Eaglesham G.K. The accumulation of cylindrospermopsin from the cyanobacterium Cylindrospermopsis raciborskii in tissues of the Redclaw crayfish Cherax quadricarinatus. Toxicon 1999, 37:1065-1077.
42. Saker M.L., Metcalf J.S., Codd G.A., Vasconcelos V.M. Accumulation and depuration of the cyanobacterial toxin cylindrospermopsin in the freshwater mussel Anodonta cygnea. Toxicon 2004, 43:185-194.
43. Saker M.L., Nogueira I.C.G., Vasconcelos V.M., Neilan B.A., Eaglesham G.K., Pereira P. First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters. Ecotoxicol. Environ. Saf. 2003, 55:243-250.
44. Saker M.L., Thomas A.D., Norton J.H. Cattle mortality attributed to the toxic cyanobacterium Cylindrospermopsis raciborskii in an outback region of North Queensland. Environ. Toxicol. 1999, 14:179-182.
45. Santoro M.G. Heat shock factors and the control of the stress response. Biochem. Pharmacol. 2000, 59:55-63.
46. Santos R., da Costa G., Franco C., Gomes-Alves P., Flammang P., Coelho A.V. First insights into the biochemistry of tube foot adhesive from the sea urchin Paracentrotus lividus (Echinoidea Echinodermata). Mar. Biotechnol. 2009, 11:686-698.
47. Schembri M.A., Neilan B.A., Saint C.P. Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environ. Toxicol. 2001, 16:413-421.
48. Shalev-Alon G., Sukenik A., Livnah O., Schwarz R., Kaplan A. A novel gene encoding amidinotransferase in the cylindrospermopsin producing cyanobacterium Aphanizomenon ovalisporum. FEMS Microbiol. Lett. 2002, 209:87-91.
49. Terao K., Ohmori S., Igarashi K., Ohtani I., Watanabe M.F., Harada K.I., Ito E., Watanabe M. Electron microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from blue-green alga Umezakia natans. Toxicon 1994, 32:833-843.
50. Valério E., Pereira P., Saker M.L., Franca S., Tenreiro R. Molecular characterization of Cylindrospermopsis raciborskii strains isolated from Portuguese freshwaters. Harmful Algae 2005, 4:1044-1052.
51. Vasas G., Gáspár A., Surányi G., Batta G., Gyémánt G., M-Hamvas M., Máthé C., Grigorszky I., Molnár E., Borbély G. Capillary electrophoretic assay and purification of cylindrospermopsin, a cyanobacterial toxin from aphanizomenon ovalisporum, by plant test (blue-green sinapis test). Anal. Biochem. 2002, 302:95-103.
52. Welker M., Bickel H., Fastner J. HPLC-PDA detection of cylindrospermopsin-opportunities and limits. Water Res. 2002, 36:4659-4663.
53. White S.H., Duivenvoorden L.J., Fabbro L.D., Eaglesham G.K. Mortality and toxin bioaccumulation in Bufo marinus following exposure to Cylindrospermopsis raciborskii cell extracts and live cultures. Environ. Pollut. 2007, 147:158-167.
54. White S.H., Duivenvoorden L.J., Fabbro L.D., Eaglesham G.K. Influence of intracellular toxin concentrations on cylindrospermopsin bioaccumulation in a freshwater gastropod (Melanoides tuberculata). Toxicon 2006, 47:497-509.
55. Yin Y., Huang J., Paine M.L., Reinhold V.N., Chasteen N.D. Structural characterization of the major extrapallial fluid protein of the mollusc mytilus edulis: implications for function. Biochemistry 2005, 44:10720-10731.
56. Zhang X., Zhou J., Wu Y., Zheng X., Ma G., Wang Z., Jin Y., He J., Yan Y. Differential Proteome Analysis of Host Cells Infected with Porcine Circovirus Type 2. J. Proteome Res. 2009, 8:5111-5119.