Transcriptomic and proteomic effects of a neonicotinoid insecticide mixture in the marine mussel (Mytilus galloprovincialis, Lam.)

Science of the Total Environment

Volumn 408, Issue 18, 2010, Pages 3775-3786

  Dondero, Francesco ^a   Negri, Alessandro ^a   Boatti, Lara ^a   Marsano, Francesco ^a   Mignone, Flavio ^b   Viarengo, Aldo ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Functional genomics; Imidacloprid; Metallothioneins; Microarrays; Mixture toxicity; Mode of action; Proteomics; Thiacloprid

Indexed keywords

FUNCTIONAL GENOMICS; IMIDACLOPRIDS; METALLOTHIONEINS; MIXTURE TOXICITY; MODE OF ACTION; PROTEOMICS;

AQUACULTURE; BINARY MIXTURES; CHEMICALS; ELECTROPHORESIS; GENE EXPRESSION; INSECTICIDES; MICROARRAYS; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; ONTOLOGY; PROTEINS; RISK ANALYSIS; RISK MANAGEMENT; TOXICITY;

RISK ASSESSMENT;

ACETYLCHOLINESTERASE; BIOLOGICAL MARKER; CELL PROTEIN; IMIDACLOPRID; INSECTICIDE; THIACLOPRID; UNCLASSIFIED DRUG;

BIOMARKER; DNA; ECOTOXICOLOGY; ELECTROKINESIS; GENE EXPRESSION; GENOMICS; INSECTICIDE; MOLLUSC; POLYMERASE CHAIN REACTION; PROTEIN; TOXICITY;

ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; ECOTOXICOLOGY; ENZYME ACTIVITY; EXOCRINE GLAND; FUNCTIONAL GENOMICS; GENE EXPRESSION PROFILING; LETHALITY; LYSOSOME MEMBRANE; MOLECULAR DYNAMICS; MUSSEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; TOXICITY TESTING; TRANSCRIPTOMICS; UNINDEXED SEQUENCE;

ANIMALS; BIOLOGICAL MARKERS; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMIDAZOLES; INSECTICIDES; MYTILUS; NITRO COMPOUNDS; PROTEOME; PYRIDINES; THIAZINES; WATER POLLUTANTS, CHEMICAL;

HEXAPODA; MYTILIDAE; MYTILUS GALLOPROVINCIALIS;

EID: 77955054540     PISSN: 00489697     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2010.03.040     Document Type: Article

References (58)

1. Abou-Donia M.B., Goldstein L.B., Bullman S., Tu T., Khan W.A., Dechkovskaia A.M., et al. Imidacloprid induces neurobehavioral deficits and increases expression of glial fibrillary acidic protein in the motor cortex and hippocampus in offspring rats following in utero exposure. J Toxicol Environ Health A 2008, 71:119-130.
2. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 1995, 57:289-300.
3. Berger A.B., Decourty L., Badis G., Nehrbass U., Jacquier A., Gadal O. Hmo1 is required for TOR-dependent regulation of ribosomal protein gene transcription. Mol Cell Biol 2007, 27:8015-8026.
4. Birkbeck T.H., Mchenery J.G. Chitinase in the mussel, Mytilus edulis (Lam.). Comp Biochem Physiol 1984, 77B:861-865.
5. Bona E., Marsano F., Cavaletto M., Berta G. Proteomic characterization of copper stress response in Cannabis sativa roots. Proteomics 2007, 7:1121-1130.
6. Bonazzi MC. Italy keeps ban on neonicotinoid seed coating to save bees. May 26th 2009. http://www.youris.com/Environment/Bees/Italy_keeps_ban_on_neonicotinoid_seed_coating_to_save_bees.kl.
7. Booth E.O., Van Driessche N., Zhuchenko O., Kuspa A., Shaulsky G. Microarray phenotyping in Dictyostelium reveals a regulon of chemotaxis genes. Bioinformatics 2005, 21:4371-4377.
8. Capowiez Y., Rault M., Mazzia C., Belzunces L. Earthworm behaviour as a biomarker-a case study using imidacloprid. Pedobiologia 2003, 47:542-547.
9. Carrabino D, Castrignanò T, Dondero F, Negri A, Oliveri C, Pesole G, Viarengo A, Mignone F. TDHand: a high throughput Transcriptomic Data Handling system. Network Tools and Applications in Biology (NETTAB) Symposium, May 19-21 2008, Varenna, The Como Lake, Italy.
10. Cassee F.R., Groten J.P., van Bladeren P.J., Feron V.J. Toxicological evaluation and risk assessment of chemical mixtures. Crit Rev Toxicol 1998, 28:73-101.
11. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159.
12. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
13. Conti B.J., Davis B.K., Zhang J., O'connor W., Williams K.L., Ting J.P. CATERPILLER 16.2 (CLR16.2), a novel NBD/LRR family member that negatively regulates T cell function. J Biol Chem 2005, 280:18375-18385.
14. Corbel V., Stankiewicz M., Bonnet J., Grolleau F., Hougard J.M., Lapied B. Synergism between insecticides permethrin and propoxur occurs through activation of presynaptic muscarinic negative feedback of acetylcholine release in the insect central nervous system. Neurotoxicology 2006, 27:508-519.
15. D'haeseleer P. How does gene expression clustering work?. Nat Biotech 2005, 23:1499-1501.
16. De Camilli P., Emr S.D., Mcpherson P.S., Novick P. Phosphoinositides as regulators in membrane traffic. Science 1996, 271:1533-1539.
17. Dell'arciprete M.L., Santos-Juanes L., Sanz A.A., Vicente R., Amat A.M., Furlong J.P., et al. Reactivity of hydroxyl radicals with neonicotinoid insecticides: mechanism and changes in toxicity. Photochem Photobiol Sci 2009, 8:1016-1023.
18. Dondero F., Piacentini L., Banni M., Rebelo M., Burlando B., Viarengo A. Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 2005, 345:259-270.
19. Dondero F., Marsano F., Venier P., Vergani L., Franzellitti S., Fabbri E., et al. Gene transcription profiling in pollutant exposed mussels (Mytilus spp.) using a new low-density oligonucleotide microarray. Gene 2006, 376:24-36.
20. El Hassani A.K., Dacher M., Gary V., Lambin M., Gauthier M., Armengaud C. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Arch Environ Contam Toxicol 2008, 54:653-661.
21. Elbert A., Haas M., Springer B., Thielert W., Nauen R. Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 2008, 64:1099-1105.
22. Ellman G.L., Courtney D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 1961, 7:88-95.
23. Gomez-Eyles J.L., Svendsen C., Lister L., Martin H., Hodson M.E., Spurgeon D.J. Measuring and modelling mixture toxicity of imidacloprid and thiacloprid on Caenorhabditis elegans and Eisenia fetida. Ecotoxicol Environ Saf 2009, 72:71-79.
24. Gorg A., Weiss W., Dunn M.J. Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4:3665-3685.
25. Gygi S.P., Rochon Y., Franza B.R., Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999, 19:1720-1730.
26. Ideker T., Thorsson V., Ranish J.A., Christmas R., Buhler J., Eng J.K., et al. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 2001, 292:929-934.
27. Jansen R.C., Nap J.P., Mlynárová L. Errors in genomics and proteomics. Nat Biotechnol 2002, 20:19.
28. Jemec A., Tišler T., Drobne D., Sepcić K., Fournier D., Trebse P. Comparative toxicity of imidacloprid, of its commercial liquid formulation and of diazinon to a non-target arthropod, the microcrustacean Daphnia magna. Chemosphere 2007, 68:1408-1418.
29. Ji Y., Schroeder D., Byrne D., Zipser B., Jellies J., Johansen K.M., et al. Molecular identification and sequence analysis of Hillarin, a novel protein localized at the axon hillock. Biochim Biophys Acta 2001, 1519:246-249.
30. Laetz C.A., Baldwin D.H., Collier T.K., Hebert V., Stark J.D., Scholz N.L. The synergistic toxicity of pesticide mixtures: implications for risk assessment and the conservation of endangered Pacific salmon. Environ Health Perspect 2009, 17:348-353.
31. Lindström M.S. Emerging functions of ribosomal proteins in gene-specific transcription and translation. Biochem Biophys Res Commun 2009, 379:167-170.
32. Ling K., Bairstow S.F., Carbonara C., Turbin D.A., Huntsman D.G., Anderson R.A. Type-I gamma phosphatidylinositol phosphate kinase modulates adherens junction and E-cadherin trafficking via a direct interaction with mu 1B adaptin. J Cell Biol 2007, 176:343-353.
33. Loewe S., Muischnek M. Effect of combinations: mathematical basis of the problem. Arch Exp Pathol Pharmakol 1926, 114:313-326.
34. Luo S., Zhang B., Dong X.P., Tao Y., Ting A., Zhou Z., et al. HSP90 beta regulates rapsyn turnover and subsequent AChR cluster formation and maintenance. Neuron 2008, 60:97-110.
35. Manoli T., Gretz N., Gröne H.J., Kenzelmann M., Eils R., Brors B. Group testing for pathway analysis improves comparability of different microarray datasets. Bioinformatics 2006, 22:2500-2506.
36. Margulies M., Egholm M., Altman W.E., Attiya S., Bader J.S., Bemben L.A., et al. Genome sequencing in open microfabricated high density picoliter reactors. Nature 2005, 437:376-380.
37. Matsuda K., Buckingham S.D., Kleier D., Rauh J.J., Grauso M., Sattelle D.B. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 2001, 22:573-580.
38. Matsuda K., Shimomura M., Ihara M., Akamatsu M., Sattelle D.B. Neonicotinoids show selective and diverse actions on their nicotinic receptor targets: electrophysiology, molecular biology, and receptor modeling studies. Biosci Biotechnol Biochem 2005, 69:1442-1452.
39. McCaffery A., Nauen R. The Insecticide Resistance Action Committee (IRAC): Public responsibility and enlightened industrial self-interest. Outlooks Pest Manag 2006, 17:11-14.
40. Mileson B.E., Chambers J.E., Chen W.L., Dettbarn W., Ehrich M., Eldefrawi A.T., et al. Common mechanism of toxicity: a case study of organophosphorus pesticides. Toxicol Sci 1998, 41:8-20.
41. Moore M.N. Cytochemical demonstration of latency of lysosomal hydrolases in digestive cells of the common mussel, Mytilus edulis, and changes induced by thermal stress. Cell Tissue Res 1976, 175:279-287.
42. Morakchi S., Maïza A., Farine P., Aribi N., Soltani N. Effects of a neonicotinoid insecticide (acetamiprid) on acetylcholinesterase activity and cuticular hydrocarbons profile in German cockroaches. Commun Agric Appl Biol Sci 2005, 70:843-848.
43. Nørgaard K.B., Cedergreen N. Pesticide cocktails can interact synergistically on aquatic crustaceans. Environ Sci Pollut Res Int 2010, 17:957-967.
44. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
45. Riaz M.A., Poupardin R., Reynaud S., Strode C., Ranson H., David J.P. Impact of glyphosate and benzo[a]pyrene on the tolerance of mosquito larvae to chemical insecticides. Role of detoxification genes in response to xenobiotics. Aquat Toxicol 2009, 93:61-69.
46. Rodriguez-Ortega M.J., Grosvik B.E., Rodriguez-Ariza A., Goksoyr A., Lopez-Barea J. Changes in protein expression profiles in bivalve molluscs (Chamaelea gallina) exposed to four model environmental pollutants. Proteomics 2003, 3:1535-1543.
47. Skandrani D., Gaubin Y., Beau B., Murat J.C., Vincent C., Croute F. Effect of selected insecticides on growth rate and stress protein expression in cultured human A549 and SH-SY5Y cells. Toxicol In Vitro 2006, 20:1378-1386.
48. Smyth G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3. Article 3.
49. Smyth G.K., Michaud J., Scott H. The use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 2005, 21:2067-2075.
50. Strode C., Wondji C.S., David J.P., Hawkes N.J., Lumjuan N., Nelson D.R., et al. Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem Mol Biol 2008, 38:113-123.
51. Suchail S., Guez D., Belzunces L.P. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 2001, 20:2482-2486.
52. Tan J., Galligan J.J., Hollingworth R.M. Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. Neurotoxicology 2007, 28:829-842.
53. Tišler T., Jemec A., Mozetǐ B., Trebše P. Hazard identification of imidacloprid to aquatic environment. Chemosphere 2009, 76:907-914.
54. Tomizawa M., Casida J.E. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 2005, 45:247-268.
55. Tomizawa M., Maltby D., Talley T.T., Durkin K.A., Medzihradszky K.F., Burlingame A.L., et al. Atypical nicotinic agonist bound conformations conferring subtype selectivity. Proc Natl Acad Sci U S A 2008, 105:1728-1732.
56. Venier P., De Pitta C., Pallavicini A., Marsano F., Varotto L., Romualdi C., et al. Development of mussel mRNA profiling: can gene expression trends reveal coastal water pollution?. Mutat Res 2006, 602:121-134.
57. Wilkinson C.F., Christoph G.R., Julien E., Kelley J.M., Kronenberg J., McCarthy J., et al. Assessing the risks of exposures to multiple chemicals with a common mechanism of toxicity: how to cumulate?. Regul Toxicol Pharmacol 2000, 31:30-43.
58. Yang E.C., Chuang Y.C., Chen Y.L., Chang L.H. Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 2008, 101:1743-1748.