Malachite green toxicity assessed on Asian catfish primary cultures of peripheral blood mononuclear cells by a proteomic analysis

Aquatic Toxicology

Volumn 114-115, Issue , 2012, Pages 142-152

  Pierrard, Marie Aline ^a   Kestemont, Patrick ^a   Delaive, Edouard ^b   Dieu, Marc ^b   Raes, Martine ^b   Silvestre, Frédéric ^a  

^a UNIVERSITY OF NAMUR   (Belgium)

^b University of Namur   (Belgium)

Author keywords

Cytotoxic; Farmed fish; Malachite green (MG); Pangasianodon hypophthalmus; PBMC; Proteomic

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ADENOSINE TRIPHOSPHATASE; ADENOSYLHOMOCYSTEINASE; BETA INTEGRIN; BETA TUBULIN; DNA; F ACTIN; GLUCOSE REGULATED PROTEIN 94; HEAT SHOCK PROTEIN; LIPOCORTIN 4; LUNG RESISTANCE PROTEIN; MALACHITE GREEN; METHYLMALONATE SEMIALDEHYDE DEHYDROGENASE (ACYLATING); PROPIONYL COENZYME A CARBOXYLASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; VALOSIN CONTAINING PROTEIN;

BLOOD; CARCINOGEN; CONCENTRATION (COMPOSITION); FISH CULTURE; GENOTOXICITY; MALACHITE; MITOCHONDRION; PROTEIN; PROTEOMICS; SAMPLING; TOXICITY; TOXICOLOGY;

ANIMAL CELL; ARTICLE; CATFISH; CELL CULTURE; CELL DIVISION; COMPUTER PROGRAM; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; DNA REPAIR; LIQUID CHROMATOGRAPHY; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BLOTTING, WESTERN; CATFISHES; CELLS, CULTURED; GENE EXPRESSION REGULATION; LEUKOCYTES, MONONUCLEAR; ROSANILINE DYES; TANDEM MASS SPECTROMETRY; WATER POLLUTANTS, CHEMICAL;

PANGASIANODON HYPOPHTHALMUS;

EID: 84858740370     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.02.020     Document Type: Article

References (74)

1. Alderman D.J. Malachite green: a review. J. Fish Dis. 1985, 8:289-298.
2. Arroyo D., Ortiz M.C., Sarabia L.A., Palacios F. Determination and identification, according to European Union Decision 2002/657/EC, of malachite green and its metabolite in fish by liquid chromatography-tandem mass spectrometry using an optimized extraction procedure and three-way calibration. J. Chromatogr. A 2009, 1216(29):5472-5482.
3. Bauer A., Chauvet S., Huber O., Usseglio F., Rothbächer U., Aragnol D., Kemler R., Pradel J. Pontin52 and reptin52 function as antagonistic regulators of beta-catenin signalling activity. EMBO J. 2000, 19(22):6121-6130.
4. Bauer K., Dangschat H., Knöppler H.O. Aufnahme und ausscheidung von malachitgrün bei regenbogenforellen. Arch. Lebensmittelhyg. 1988, 39:97-102. in Schuetze, A., Heberer, T., Juergensen, S., 2008. Occurrence of residues of the veterinary drug malachite green in eels caught downstream from municipal sewage treatment plants. Chemosphere 72, 1664-1670.
5. BfR, 2007. Collection and pre-selection of available data to be used for the risk assessment of malachite green residues by the Joint FAO/WHO Expert Committee on Food Additives (JECFA). Federal Institute for Risk Assessment. BfR Expert Opinion No. 036/2007.
6. Bols N.C., Lee L.E.J. Technology and uses of cell cultures from the tissues and organs of bony fish. Cytotechnology 1991, 6:163-187.
7. Bose B., Motiwale L., Rao K.V.K. DNA damage and G2/M arrest in Syrian hamster embryo cells during malachite green exposure are associated with elevated phosphorylation of ERK1 and JNK1. Cancer Lett. 2005, 230:260-270.
8. Bras M., Queenan B., Susin S.A. Programmed cell death via mitochondria: different modes of dying. Biochemistry (Mosc.) 2005, 70(2):231-239.
9. Bullough D.A., Ceccarelli E.A., Roise D., Allison W.S. Inhibition of the bovine-heart mitochondrial F1-ATPase by cationic dyes and amphipathic peptides. Acta Biochim. Biophys. 1989, 975(3):377-383.
10. Candé C., Cecconi F., Dessen P., Kroemer G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death?. J. Cell Sci. 2002, 115(Pt 24):4727-4734.
11. Castaño A., Bols N., Braunbeck T., Dierickx P., Halder M., Isomaa B., Kawahara K., Lee L.E.J., Mothersill C., Pärt P., Repetto G., Sintes J.R., Rufli H., Smith R., Wood C., Segner H. The use of fish cells in ecotoxicology. The report and recommendations of ECVAM Workshop 47. Altern. Lab. Anim. 2003, 31(3):317-351.
12. Chiang P.K. Biological effects of inhibitors of S-adenosylhomocysteine hydrolase. Pharmacol. Ther. 1998, 77(2):115-134.
13. Ciocca D.R., Fuqua S.A.W., Lock-Lim S., Toft D.O., Welch W.J., McGuire W.L. Response of human breast cancer cells to heat shock and chemotherapeutic drugs. Cancer Res. 1992, 52:3648-3654.
14. Clark E.A., Brugge J.S. Integrins and signal transduction pathways: the road taken. Science 1995, 268(5208):233-239.
15. Ctrnáctá V., Fritzler J.M., Surinová M., Hrdý I., Zhu G., Stejskal F. Efficacy of S-adenosylhomocysteine hydrolase inhibitors, d-eritadenine and (S)-DHPA, against the growth of Cryptosporidium parvum in vitro. Exp. Parasitol. 2010, 126(2):113-116.
16. Culp S.J., Beland F.A. Malachite green: a toxicological review. J. Am. Coll. Toxicol. 1996, 15:219-238.
17. Davoren M., Ni{dotless}óShúilleabháin S., Hartl M.G., Sheehan D., O'Brien N.M., O'Halloran J., Van Pelt F.N., Mothersill C. Assessing the potential of fish cell lines as tools for the cytotoxicity testing of estuarine sediment aqueous elutriates. Toxicol. In Vitro 2005, 19:421-431.
18. De Wit M., Keil D., Remmerie N., Van der Ven K., Van den Brandhof E.J., Knapen D., Witters E., De Coen W. Molecular targets of TBBPA in zebrafish analysed through integration of genomic and proteomic approaches. Chemosphere 2008, 74(1):96-105.
19. Ding F., Liu W., Liu F., Li Z.Y., Sun Y. A study of the interaction between malachite green and lysozyme by steady-state fluorescence. J. Fluoresc. 2009, 19:783-791.
20. Dorts J., Kestemont P., Dieu M., Raes M., Silvestre F. Proteomic response to sublethal cadmium exposure in a sentinel fish species, Cottus gobio. J. Proteome Res. 2011, 10(2):470-478.
21. FAO, 2009. The state of world fisheries and aquaculture: 2008. Fisheries Department, Food and Agriculture Organization of the United Nations, Rome, Italy.
22. Feng Y., Lee N., Fearon E.R. TIP49 regulates b-catenin-mediated neoplastic transformation and T-cell factor target gene induction via effects on chromatin remodeling. Cancer Res. 2003, 63:8726-8734.
23. Fessard V., Godard T., Huet S., Mourot A., Poul J.M. Mutagenicity of malachite green and leucomalachite green in in vitro tests. J. Appl. Toxicol. 1999, 19(6):421-430.
24. Forné I., Abián J., Cerdà J. Fish proteome analysis: model organisms and non-sequenced species. Proteomics 2010, 10:858-872.
25. Gartner W., Rossbacher J., Zierhut B., Daneva T., Base W., Weissel M., Waldhäusl W., Pasternack M.S., Wagner L. The ATP-dependent helicase RUVBL1/TIP49a associates with tubulin during mitosis. Cell Motil. Cytoskeleton 2003, 56(2):79-93.
26. Gibson K.D., Wilson J.D., Udenfriend S. The enzymatic conversion of phospholipid ethanolamine to phospholipid choline in rat liver. J. Biol. Chem. 1961, 236:673-679.
27. Gillardin V., Silvestre F., Dieu M., Delaive E., Raes M., Thomé J.P., Kestemont P. Protein expression profiling in the African clawed frog Xenopus laevis tadpoles exposed to the polychlorinated biphenyl mixture aroclor 1254. Mol. Cell. Proteomics 2009, 8(4):596-611.
28. Goodwin G.W., Rougraff P.M., Davis E.J., Harris R.A. Purification and characterization of methylmalonate-semialdehyde dehydrogenase from rat liver. Identity to malonate-semialdehyde dehydrogenase. J. Biol. Chem. 1989, 264(25):14965-14971.
29. Gorynia S., Matias P.M., Gonçalves S., Coelho R., Lopes G., Thomaz M., Huber M., Haendler B., Donner P., Carrondo M.A. Expression, purification, crystallization and preliminary X-ray analysis of the human RuvB-like protein RuvBL1. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2006, 62(Pt 1):61-66.
30. Gupta S., Sundarrajan M., Rao K.V.K. Tumor promotion by metanil yellow and malachite green during rat hepatocarcinogenesis is associated with dysregulated expression of cell cycle regulatory proteins. Teratog. Carcinog. Mutagen. 2003, 1:301-312.
31. Hill W.G., Kaetzel M.A., Kishore B.K., Dedman J.R., Zeidel M.L. Annexin A4 reduces water and proton permeability of model membranes but does not alter aquaporin 2-mediated water transport in isolated endosomes. J. Gen. Physiol. 2003, 121(5):413-425.
32. Imamura S., Ojima N., Yamashita M. Cold-inducible expression of the cell division cycle gene CDC48 and its promotion of cell proliferation during cold acclimation in zebrafish cells. FEBS Lett. 2003, 549(1-3):14-20.
33. Jiang Y., Xie P., Liang G. Distribution and depuration of the potentially carcinogenic malachite green in tissues of three freshwater farmed Chinese fish with different food habits. Aquaculture 2009, 288:1-6.
34. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74(20):5383-5392.
35. Kickhoefer V.A., Rajavel K.S., Scheffer G.L., Dalton W.S., Scheper R.J., Rome L.H. Vaults are up-regulated in multidrug-resistant cancer cell lines. J. Biol. Chem. 1998, 273(15):8971-8974.
36. Kinoshita M. Assembly of mammalian septins. J. Biochem. 2003, 134(4):491-496.
37. Kinoshita M., Kumar S., Mizoguchi A., Ide C., Kinoshita A., Haraguchi T., Hiraoka Y., Noda M. Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes Dev. 1997, 11:1535-1547.
38. 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(6):1163-1175.
39. Komarov P.G., Shtil A.A., Holian O., Tee L., Buckingham L., Mechetner E.B., Roninson I.B., Coon J.S. Activation of the LRP (lung resistance-related protein) gene by short-term exposure of human leukemia cells to phorbol ester and cytarabine. Oncol. Res. 1998, 10(4):185-192.
40. Kowaltowski A.J., Turin J., Indig G.L., Vercesi A.E. Mitochondrial effects of triarylmethane dyes. J. Bioenerg. Biomembr. 1999, 31(6):581-590.
41. Leal J.F., Ferrer I., Blanco-Aparicio C., Hernández-Losa J., Ramón Y., Cajal S., Carnero A., Lleonart M.E. S-Adenosylhomocysteine hydrolase downregulation contributes to tumorigenesis. Carcinogenesis 2008, 29(11):2089-2095.
42. Lilienblum W., Dekant W., Foth H., Gebel T., Hengstler J.G., Kahl R., Kramer P.J., Schweinfurth H., Wollin K.M. Alternative methods to safety studies in experimental animals: role in the risk assessment of chemicals under the new European Chemicals Legislation (REACH). Arch. Toxicol. 2008, 82(4):211-236.
43. Love D.C., Rodman S., Neff R.A., Nachman K.E. Veterinary drug residues in seafood inspected by the European Union, United States, Canada, and Japan from 2000 to 2009. Environ. Sci. Technol. 2011, 45(17):7232-7240.
44. Mai M.S., Allison W.S. Inhibition of an oligomycin-sensitive ATPase by cationic dyes, some of which are atypical uncouplers of intact mitochondria. Arch. Biochem. Biophys. 1983, 221(2):467-476.
45. Mazerski J., Martelli S., Borowski E. The geometry of intercalation complex of antitumor mitoxantrone and ametantrone with DNA: molecular dynamics simulations. Acta Biochim. Pol. 1998, 45(1):1-11.
46. Miller N.W., Chinchar V.G., Clem L.W. Development of leukocyte cell lines from the channel catfish (Ictalurus punctatus). J. Tissue Cult. Methods 1994, 16:117-123.
47. Moreno S.N., Gadelha F.R., Docampo R. Crystal violet as an uncoupler of oxidative phosphorylation in rat liver mitochondria. J. Biol. Chem. 1988, 263(25):12493-12499.
48. Nesvizhskii A.I., Keller A., Kolker E., Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 2003, 75:4646-4658.
49. Niewiarowski A., Bradley A.S., Gor J., McKay A.R., Perkins S.J., Tsaneva I.R. Oligomeric assembly and interactions within the human RuvB-like RuvBL1 and RuvBL2 complexes. Biochem. J. 2010, 429(1):113-125.
50. Pierrard, M-A., Roland, K., Kestemont, P., Dieu, M., Raes, M., Silvestre, F., Fish peripheral blood mononuclear cell preparation for future monitoring applications. Submitted for publication in Analytical Biochemistry: Methods in the Biological Sciences.
51. Piljić A., Schultz C. Annexin A4 Self-Association Modulates General Membrane Protein Mobility in Living Cells. Mol. Biol. Cell 2006, 17(7):3318-3328.
52. Qiu X.B., Lin Y.L., Thome K.C., Pian P., Schlegel B.P., Weremowicz S., Parvin J.D., Dutta A. An eukaryotic RuvB-like protein (RUVBL1) essential for growth. J. Biol. Chem. 1998, 273(43):27786-27793.
53. Rahman M.M., Islam M.S., Halder G.C., Tanaka M. Cage culture of sutchi catfish, Pangasius sutchi (Fowler 1937): effects of stocking density on growth, survival, yield and farm profitability. Aquacult. Res. 2006, 37(1):33-39.
54. Rao K.V., Fernandes C.L. Progressive effects of malachite green at varying concentrations on the development of N-nitrosodiethylamine induced hepatic preneoplastic lesions in rats. Tumori 1996, 82(3):280-286.
55. Rao K.V., Mahudawala D.M., Redkar A.A. Abrogation of cell cycle checkpoint controls during malignant transformation of syrian hamster embryo cells is associated with decreased sensitivity to apoptosis. J. Environ. Pathol. Toxicol. Oncol. 2001, 20(3):177-188.
56. Rao K.V.K. Comparative cytotoxic effects of the nonpermitted food colouring agents metanil yellow, orange II, rhodamine B and malachite green on hamster dermal and C3H/10 T1/2 fibroblasts. Bombay Hosp. J. 1990, 32:61-65.
57. Rovida C., Hartung T. Re-evaluation of animal numbers and costs for in vivo tests to accomplish REACH legislation requirements for chemicals - a report by the transatlantic think tank for toxicology (t(4)). Altex 2009, 26(3):187-208.
58. Scherpenisse P., Bergwerff A.A. Determination of residues of malachite green in finfish by liquid chromatography tandem mass spectrometry. Acta Anal. Chim. 2005, 529(1-2):173-177.
59. Schirmer K. Proposal to improve vertebrate cell cultures to establish them as substitutes for the regulatory testing of chemicals and effluents using fish. Toxicology 2006, 224:163-183.
60. Schuetze A., Heberer T., Juergensen S. Occurrence of residues of the veterinary drug malachite green in eels caught downstream from municipal sewage treatment plants. Chemosphere 2008, 72:1664-1670.
61. Silvestre F., Dierick J.F., Dumont V., Dieu M., Raes M., Devos P. Differential protein expression profiles in anterior gills of Eriocheir sinensis during acclimation to cadmium. Aquat. Toxicol. 2006, 76(1):46-58.
62. Silvestre F., Linares-Casenave J., Doroshov S.I., Kültz D. A proteomic analysis of green and white sturgeon larvae exposed to heat stress and selenium. Sci. Total Environ. 2010, 408(16):3176-3188.
63. Silvestre F., Tu H.T., Bernard A., Dorts J., Dieu M., Raes M., Phuong N.T., Kestemont P. A differential proteomic approach to assess the effects of chemotherapeutics and production management strategy on giant tiger shrimp Penaeus monodon. Comp. Biochem. Physiol. 2010, 5(3):227-233.
64. Sokatch J.R., Sanders L.E., Marshall V.P. Oxidation of methylmalonate semialdehyde to propionyl coenzyme A in Pseudomonas aeruginosa grown on valine. J. Biol. Chem. 1968, 243(10):2500-2506.
65. Srivastava S., Sinha R., Roy D. Toxicological effects of malachite green. Aquat. Toxicol. 2004, 66(3):319-329.
66. Stammati A., Nebbia C., Angelis I.D., Albo A.G., Carletti M., Rebecchi C., Zampaglioni F., Dacasto M. Effects of malachite green (MG) and its major metabolite, leucomalachite green (LMG), in two human cell lines. Toxicol. In Vitro 2005, 19(7):853-858.
67. Steiner E., Holzmann K., Pirker C., Elbling L., Micksche M., Sutterlüty H., Berger W. The major vault protein is responsive to and interferes with interferon-gamma-mediated STAT1 signals. J. Cell Sci. 2006, 119(Pt 3):459-469.
68. Sudova E., Machova J., Svobodova Z., Vesely T. Negative effects of malachite green and possibilities of its replacement in the treatment of fish eggs and fish: a review. Med. Vet. 2007, 52(12):527-539.
69. Sundarrajan M., Fernandis A.Z., Subrahmanyam G., Prabhudesai S., Krishnamurthy S.C., Rao K.V. Overexpression of G1/S cyclins and PCNA and their relationship to tyrosine phosphorylation and dephosphorylation during tumor promotion by metanil yellow and malachite green. Toxicol. Lett. 2000, 116(1-2):119-130.
70. Vij N. AAA ATPase p97/VCP: cellular functions, disease and therapeutic potential. J. Cell. Mol. Med. 2008, 12(6A):2511-2518.
71. Wang Q., Song C., Li C.C. Molecular perspectives on p97-VCP: progress in understanding its structure and diverse biological functions. J. Struct. Biol. 2004, 146(1-2):44-57.
72. Wixler V., Geerts D., Laplantine E., Westhoff D., Smyth N., Aumailley M., Sonnenberg A., Paulsson M. The LIM-only protein DRAL/FHL2 binds to the cytoplasmic domain of several alpha and beta integrin chains and is recruited to adhesion complexes. J. Biol. Chem. 2000, 275(43):33669-33678.
73. Yonar M.E., Yonar S.M. Changes in selected immunological parameters and antioxidant status of rainbow trout exposed to malachite green (Oncorhynchus mykiss, Walbaum, 1792). Pest. Biochem. Physiol. 2010, 97:19-23.
74. Zahn T., Braunbeck T. Cytotoxic effects of sublethal concentrations of malachite green in isolated hepatocytes from rainbow trout (Oncorhynchus mykiss). Toxicol. In Vitro 1995, 9(5):729-741.