Effects of neurotoxic insecticides on heat-shock proteins and cytokine transcription in Chinook salmon (Oncorhynchus tshawytscha)

Ecotoxicology and Environmental Safety

Volumn 72, Issue 1, 2009, Pages 182-190

  Eder, Kai J ^a,c   Leutenegger, Christian M ^b   Köhler, Heinz R ^c   Werner, Ingeborg ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Chlorpyrifos; Esfenvalerate; Hsp60; Hsp70; Hsp90; IGF 1; IL 1 ; Mx protein; Sublethal effects; TGF

Indexed keywords

CHLORPYRIFOS; CYTOKINE; FENVALERATE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INSECTICIDE; INTERLEUKIN 1BETA; MAX PROTEIN; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA;

GENE EXPRESSION; IMMUNE SYSTEM; INSECTICIDE; JUVENILE; POLLUTION EFFECT; POLLUTION EXPOSURE; POLYMERASE CHAIN REACTION; PROTEIN; REAL TIME; SALMONID; TOXIC SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FISH; IMMUNE SYSTEM; IMMUNOTOXICITY; KIDNEY; LIVER; NEUROTOXICITY; NONHUMAN; ONCORHYNCHUS TSHAWYTSCHA; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN; WESTERN BLOTTING;

ANIMALS; CALIFORNIA; CYTOKINES; DNA PRIMERS; DNA, COMPLEMENTARY; GILLS; HEAT-SHOCK PROTEINS; INSECTICIDES; LIVER; MUSCLE, SKELETAL; NEUROTOXINS; POLYMERASE CHAIN REACTION; SALMON; TRANSCRIPTION, GENETIC;

ONCORHYNCHUS TSHAWYTSCHA;

EID: 54049129224     PISSN: 01476513     EISSN: 10902414     Source Type: Journal    
DOI: 10.1016/j.ecoenv.2008.04.020     Document Type: Article

References (86)

1. Amweg E.L., Weston D.P., and Ureda N.M. Use and toxicity of pyrethroid pesticides in the Central Valley, California, USA. Environ. Toxicol. Chem. 24 4 (2005) 966-972
2. Amweg E.L., Weston D.P., and Ureda N.M. Erratum. Environ. Toxicol. Chem. 24 5 (2005) 1300-1301
3. Amweg E.L., Weston D.P., You J., and Lydy M.J. Pyrethroid insecticides and sediment toxicity in urban creeks from California and Tennessee. Environ. Sci. Technol. 40 (2006) 1700-1706
4. Anderson B.S., Phillips B.M., Hunt J.W., Connor V., Richard N., and Tjeerdema R.S. Identifying primary stressors impacting macroinvertebrates in the Salinas River (California, USA): relative effects of pesticides and suspended particles. Environ. Pollut. 141 3 (2006) 402-408
5. Bacey J., Spurlock F., Starner K., Feng J., Hsu J., White J., and Tran D.M. Residues and toxicity of esfenvalerate and permethrin in water and sediments, in tributaries of the Sacramento and San Joaquin Rivers, California, USA. Bull. Environ. Contam. Toxicol. 74 (2005) 864-871
6. Basu N., Todgham A.E., Ackerman P.A., Bibeau M.R., Nakano K., Schulte P.M., and Iwama G.K. Heat shock protein genes and their functional significance in fish. Gene 295 (2002) 173-183
7. Beaman J.R., Finch R., Gardner H., Hoffmann F., Rosencrance A., and Zelikoff J.T. Mammalian immunoassays for predicting the toxicity of malathion in a laboratory fish model. J. Toxicol. Environ. Health 56 (1999) 523-542
8. Blattler D.P., Garner F., Van Slyke K., and Bradley A. Quantitative electrophoresis in polyacrylamide gels of 2-40%. J. Chromatogr. 64 (1972) 147-155
9. Bradbury S.P., McKim J.M., and Coats J.R. Physiological responses of rainbow trout (Salmo gairdneri) to acute fenvalerate intoxication. Pestic. Biochem. Phys. 27 (1987) 275-288
10. Brewer S.K., Little E.E., DeLonay A.J., Beauvais S.L., Jones S.B., and Ellersieck M.R. Behavioral dysfunctions correlate to altered physiology in rainbow trout (Oncorynchus mykiss) exposed to cholinesterase-inhibiting chemicals. Arch. Environ. Contam. Toxicol. 40 (2001) 70-76
11. Central Valley Regional Water Quality Control Board, 2008. Irrigated Lands Regulatory Program, URL: 〈www.waterboards.ca.gov/centralvalley/water_issues/irrigated_lands〉.
12. Clifford M.A., Eder K.J., Werner I., and Hedrick R.P. Synergistic effects of esfenvalerate and infectious hematopoietic necrosis virus on juvenile Chinook salmon mortality. Environ. Toxicol. Chem. 24 7 (2005) 1766-1772
13. Crepeau, K.L., Baker, L.M., Kuivila, K.M., 2000. Method of analysis and quality-assurance practices for determination of pesticides in water by solid-phase extraction and capillary-column gas chromatography/mass spectrometry at the US Geological Survey California District Organic Chemistry Laboratory, 1996-99. Open-File Report 00-229. US Geological Survey, Sacramento, CA, USA.
14. Daughaday W.H., and Rotwein P. Insulin-like growth factors I and II peptide messenger ribonucleic acid and gene structures serum and tissue concentrations. Endocr. Rev. 10 (1989) 68-91
15. De Vlaming V., Connor V., DiGiorgio C., Bailey H.C., Deanovic L.A., and Hinton D.E. Application of whole effluent toxicity test procedures to ambient water quality assessment. Environ. Toxicol. Chem. 19 (2000) 42-62
16. Dinarello C.A. Interleukin-1. Cytokine Growth Factor Rev. 8 (1997) 253-265
17. Domagalski, J.L., Knifong, D.L., Dileanis, P.D., Brown, L.R., May, J.T., Connor, V., Alpers, C.N., 2000. Water quality in the Sacramento River Basin, California, 1994-98. US Geological Survey Circular 1215, US Geological Survey, Sacramento, CA, USA.
18. Donaldson, D., Kiely, T., Grube, A., 2002. Pesticides industry sales and usage. 1998 and 1999 market estimates. EPA-733-R-02-001. Office of Prevention, Pesticides and Toxic Substances, US Environmental Protection Agency, Washington, DC, USA.
19. Dubrovsky, N., Kratzer, C., Brown, L., Gronberg, J., Burow, K., 1998. Water quality in the San Joaquin-Tulare Basins, California, 1992-95. US Geological Survey Circular 1159, US Geological Survey, Sacramento, CA, USA.
20. Duguay S.J., Park L.K., Samadpour M., and Dickhoff W.W. Nucleotide sequence and tissue distribution of three insulin-like growth factor i prohormones in salmon. Mol. Endocrinol. 6 (1992) 1202-1210
21. Dutta H.M., Richmonds C.R., and Zeno T. Effects of diazinon on the gills of bluegill sunfish Lepomis macrochirus. J. Environ. Pathol. Toxicol. 12 (1993) 219-227
22. Dutta H.M., Roy P.K., Singh N.K., Adhikari S., and Munshi J.D. Effect of sublethal levels of malathion on the gills of Heteropneustes fossilis: scanning electron microscopic study. J. Environ. Pathol. Toxicol. 17 (1998) 51-63
23. Eder, K.J., 2006. Effects of sublethal pesticide concentrations on juvenile Chinook salmon (Oncorhynchus tshawytscha): subcellular changes and alterations of immune-regulatory gene expression. Ph.D. Thesis, University of Tübingen, Tübingen, Germany.
24. Eder K.J., Köhler H.-R., and Werner I. Pesticide and pathogen: heat shock protein expression and acetylcholinesterase inhibition in juvenile Chinook salmon in response to multiple stressors. Environ. Toxicol. Chem. 26 (2007) 1233-1242
25. Epstein L., Bassein S., Zalom F.G., and Wilhoit L.R. Changes in pest management practice in almond orchards during the rainy season in California, USA. Agric. Ecosyst. Environ. 83 (2001) 111-120
26. Eshleman A.J., and Murray T.F. Pyrethroid insecticides indirectly inhibit gaba-dependent chloride-36 influx in synaptoneurosomes from the trout brain. Neuropharmacology 30 (1991) 1333-1342
27. Espevik T., Figari I.S., Shalaby R.M., Lackides G.A., Lewis G.D., Shepard M.H., and Palladino M.A.J. Inhibition of cytokine production by cyclosporin A and transforming growth factor β. J. Exp. Med. 166 (1987) 571-576
28. Feder, M.E., Hofmann, G.E., 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. In: Hoffman, J.F. (Author), Annual Review of Physiology, 61. Annual Reviews Inc., Palo Alto, CA, USA, pp. 243-282.
29. Fisher F.W. Past and present status of Central Valley Chinook salmon. Conserv. Biol. 8 (1994) 870-873
30. Floyd, E.Y., Geist, J.P., Werner, I., in press. Short-term exposure of the fathead minnow (Pimephales promelas) to a pyrethroid insecticide: Implications for growth, behavior, and predation risk. Environ. Toxicol. Chem.
31. Fulton M.H., and Key P.B. Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ. Toxicol. Chem. 20 (2001) 37-45
32. Geist J., Werner I., Eder K.J., and Leutenegger C.M. Comparisons of tissue-specific transcription of stress response genes with whole animal endpoints of adverse effect in striped bass (Morone saxatilis) following treatment with copper and esfenvalerate. Aquat. Toxicol. 85 (2007) 28-39
33. Hardie L.J., Laing K.L., Daniels G.D., Grabowski P.S., Cunningham C., and Secombes C.J. Isolation of the first piscine transforming growth factor beta gene: analysis reveals tissue specific expression and a potential regulatory sequence in rainbow trout (Oncorhynchus mykiss). Cytokine 10 (1998) 555-563
34. Hassanein H.M.A., Banhawy M.A., Soliman F.M., Abdel-Rehim S.A., Mueller W.E.G., and Schroeder H.C. Induction of hsp70 by the herbicide oxyfluorfen (Goal) in the Egyptian Nile Fish, Oreochromis niloticus. Arch. Environ. Contam. Toxicol. 37 (1999) 78-84
35. Heemskerk V.H., Daemen M.A.R.C., and Buurman W.A. Insulin-like growth factor-1 (IGF-1) and growth hormone (GH) in immunity and inflammation. Cytokine Growth Factor Rev. 10 (1999) 5-14
36. Holcombe G.W., Phipps G.L., and Tanner D.K. The acute toxicity of kelthane, dursban, disulfoton pydrin and permethrin to fathead minnows (Pimephales-promelas) and rainbow trout (Salmo-gairdneri). Environ. Pollut. A 29 (1982) 167-178
37. Hunt J.W., Anderson B.S., Phillips B.M., Nicely P.N., Tjeerdema R.S., Puckett H.M., Stephenson M., Worcester K., and De Vlaming V. Ambient toxicity due to chlorpyrifos and diazinon in a central California coastal watershed. Environ. Monit. Assess. 82 (2003) 83-112
38. Iwama G.K., Thomas P.T., Forsyth R.B., and Vijayan M.M. Heat shock protein expression in fish. Rev. Fish Biol. Fisher 8 (1998) 35-56
39. Jang S.I., Hardie L.J., and Secombes C.J. Effects of transforming growth factor beta-1 on rainbow trout Oncorhynchus mykiss macrophage respiratory burst activity. Dev. Comp. Immunol. 18 (1994) 315-323
40. Jensen V., and Robertsen B. Cloning of an Mx cDNA from Atlantic halibut (Hippoglossus hippoglossus) and characterization of Mx mRNA expression in response to double-stranded RNA or infectious pancreatic necrosis virus. J. Interferon Cytokine Res. 20 (2000) 701-710
41. Jensen I., Albuquerque A., Sommer A.-I., and Robertsen B. Effect of poly I:C on the expression of Mx proteins and resistance against infection by infectious salmon anaemia virus in Atlantic salmon. Fish Shellfish Immun. 13 (2002) 311-326
42. Jensen I., Larsen R., and Robertsen B. An antiviral state induced in Chinook salmon embryo cells (CHSE-214) by transfection with the double-stranded RNA poly I:C. Fish Shellfish Immun. 13 (2002) 367-378
43. Jones J.I., and Clemmons D.R. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16 (1995) 3-34
44. Kikuchi M., Miyagaki T., and Wakabayashi M. Evaluation of pesticides used in golf links by acute toxicity test on rainbow trout. Nippon Suisan Gakk. 62 (1996) 414-419
45. Kim C.H., Johnson M.C., Drennan J.D., Simon B.E., Thomann E., and Leong J.-A.C. DNA vaccines encoding viral glycoproteins induce nonspecific immunity and Mx protein synthesis in fish. J. Virol. 74 (2000) 7048-7054
46. Koehler H.-R., Bartussek C., Eckwert H., Farian K., Graenzer S., Knigge T., and Kunz N. The hepatic stress protein (hsp70) response to interacting abiotic parameters in fish exposed to various levels of pollution. J. Aquat. Ecosyst. Stress Recov. 8 (2001) 261-279
47. Kuivila K.M., and Foe C.G. Concentration, transport and biological effects of dormant spray pesticides in the San Francisco Estuary, California. Environ. Toxicol. Chem. 14 (1995) 1141-1150
48. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
49. Laing K.J., Cunningham C., and Secombes C.J. Genes for three different isoforms of transforming growth factor-beta are present in plaice (Pleuronectes platessa) DNA. Fish Shellfish Immun. 10 (2000) 261-271
50. Lee J.-Y., Hirono I., and Aoki T. Cloning and analysis of expression of Mx cDNA in Japanese flounder, Paralichthys olivaceus. Dev. Comp. Immunol. 24 (2000) 407-415
51. Leonard R.A. Movement of pesticides into surface waters. In: Cheng H.H. (Ed). Pesticides in the Soil Environment: Processes, Impacts, and Modeling vol. 2 (1990), Soil Science Society of America Book Series, Madison, WI, USA 303-350
52. Leutenegger C.M., Mislin C.N., Sigrist B., Ehrengruber M.U., Hofmann-Lehmann R., and Lutz H. Quantitative real-time PCR for the measurement of feline cytokine mRNA. Vet. Immunol. Immunopathol. 71 (1999) 291-305
53. Leutenegger C.M., Alluwaimi A.M., Smith W.L., Perani L., and Cullor J.S. Quantitation of bovine cytokine mRNA in milk cells of healthy cattle by real-time TaqMan(R) polymerase chain reaction. Vet. Immunol. Immunopathol. 77 (2000) 275-287
54. Little E.E., Archeski R.D., Flerov B.A., and Kozlovskaya V.I. Behavioral indicators of sublethal toxicity in rainbow trout. Arch. Environ. Contam. Toxicol. 19 (1990) 380-385
55. Moore A., and Waring C.P. Sublethal effects of the pesticide Diazinon on olfactory function in mature male Atlantic salmon parr. J. Fish Biol. 48 (1996) 758-775
56. Moore A., and Waring C.P. The effects of a synthetic pyrethroid pesticide on some aspects of reproduction in Atlantic salmon (Salmo salar L.). Aquat. Toxicol. 52 (2001) 1-12
57. Nygaard R., Husgard S., Sommer A.-I., Leong J.-A.C., and Robertsen B. Induction of Mx protein by interferon and double-stranded RNA in salmonid cells. Fish Shellfish Immun. 10 (2000) 435-450
58. Peddie S., Zou J., Cunningham C., and Secombes C.J. Rainbow trout (Oncorhynchus mykiss) recombinant IL-1beta and derived peptides induce migration of head-kidney leucocytes in vitro. Fish Shellfish Immun. 11 (2001) 697-709
59. Phillips B.M., Anderson B.S., Hunt J.W., Nicely P.A., Kosaka R.A., Tjeerdema R.S., de Vlaming V., and Richard N. In situ water and sediment toxicity in an agricultural watershed. Environ. Toxicol. Chem. 23 (2004) 435-442
60. Phipps G.L., and Holcombe G.W. A method for aquatic multiple species toxicant testing acute toxicity of 10 chemicals to 5 vertebrates and 2 invertebrates. Environ. Pollut. A 38 (1985) 141-158
61. Rand G.M., and Petrocelli S.R. Fundamentals of Aquatic Toxicology. Methods and Applications (1985), Hemisphere Publishing Corporation, New York
62. Rao J.V., Rani C.H.S., Kavitha P., Rao R.N., and Madhavendra S.S. Toxicity of chlorpyrifos to the fish Oreochromis mossambicus. Bull. Environ. Contam. Toxicol. 70 (2003) 985-992
63. Ross L.J., Bennett K.D., Kim K.D., Hefner K., and Hernandez J. Reducing Dormant Spray Runoff from Orchards. EH 97-03 (1997), Environmental Monitoring and Pest Management Branch, California Department of Pesticide Regulation, Sacramento, CA, USA
64. Samuel C.E. Antiviral actions of interferon interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology 183 (1991) 1-11
65. Scholz N.L., Truelove N.K., French B.L., Berejikian B.A., Quinn T.P., Casillas E., and Collier T.K. Diazinon disrupts antipredator and homing behaviors in chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish Aquat. Sci. 57 (2000) 1911-1918
66. Secombes C.J. Cloning and bioactivity of fish cytokines and their relevance to disease resistance. Bull. Eur. Assoc. Fish Pathol. 22 (2002) 110-116
67. Secombes C.J., Hardie L.J., and Daniels G. Cytokines in fish: an update. Fish Shellfish Immun. 6 (1996) 291-304
68. Secombes C.J., Bird S., Cunningham C., and Zou J. Interleukin-1 in fish. Fish Shellfish Immun. 9 (1999) 335-343
69. Secombes C.J., Zou J., Laing K., Daniels G.D., and Cunningham C. Cytokine genes in fish. Aquaculture 172 (1999) 93-102
70. Shamblott M.J., and Chen T.T. Age-related and tissue-specific levels of five forms of insulin-like growth factor mRNA in a teleost. Mol. Mar. Biol. Biotech. 2 (1993) 351-361
71. Siepmann, S., Holm, S., 2000. Hazard assessment of the synthetic pyrethroid insecticides bifenthrin, cypermethrin, esfenvalerate, and permethrin to aquatic organisms in the Sacramento-San Joaquin River system. Administrative Report 00-6, California Department of Fish and Game, Pesticide Investigations Unit, Rancho Cordova, CA, USA.
72. Simon A., Fah J., Haller O., and Staeheli P. Interferon-regulated mx genes are not responsive to interleukin-1 tumor necrosis factor and other cytokines. J. Virol. 65 (1991) 968-971
73. US EPA, 2000. Pesticide ecotoxicity database. 43358311. Office of Pesticide Programs, Environmental Fate and Effects Division, US EPA, Washington, DC, USA.
74. US Geological Survey, 1999. The quality of our nation's waters-nutrients and pesticides. US Geological Survey Circular 1225, US Geological Survey, Reston, VA, USA.
75. van Buul-Offers S.C., and Kooijman R. The role of growth hormone and insulin-like growth factors in the immune system. Cell Mol. Life Sci. 54 (1998) 1083-1094
76. Varo I., Serrano R., Pitarch E., Amat F., Lopez F.J., and Navarro J.C. Bioaccumulation of chlorpyrifos through an experimental food chain: study of protein HSP70 as biomarker of sublethal stress in fish. Arch. Environ. Contam. Toxicol. 42 (2002) 229-235
77. Vijayan M.M., Pereira C., Kruzynski G., and Iwama G.K. Sublethal concentrations of contaminant induce the expression of hepatic heat shock protein 70 in two salmonids. Aquat. Toxicol. 40 (1998) 101-108
78. Weigent D.A., Baxter J.B., and Glalosk J.E. The production of growth hormone and insulin-like growth factor-1 by the same subpopulation of rat mononuclear leukocytes. Brain Behav. Immun. 6 (1992) 365-376
79. Werner I., Deanovic L.A., Connor V., de Vlaming V., Bailey H.C., and Hinton D.E. Insecticide-caused toxicity to Ceriodaphnia dubia (Cladocera) in the Sacramento-San Joaquin River Delta, California, USA. Environ. Toxicol. Chem. 19 (2000) 215-227
80. Werner I., Zalom F.G., Oliver M.N., Deanovic L.A., Kimball T.S., Henderson J.D., Wilson B.W., Krueger W., and Wallender W.W. Toxicity of stormwater runoff after dormant spray application in a French prune orchard, Glenn County, California, USA. Temporal patterns and the effect of ground covers. Environ. Toxicol. Chem. 23 11 (2004) 2719-2726
81. Weston D.P., You J.C., and Lydy M.J. Distribution and toxicity of sediment-associated pesticides in agriculture-dominated water bodies of California's Central Valley. Environ. Sci. Technol. 38 (2004) 2752-2759
82. Weston D.P., Amweg E.L., Mekebri A., Ogle R.S., and Lydy M.J. Aquatic effects of aerial spraying for mosquito control over an urban area. Environ. Sci. Technol. 15 (2006) 5817-5822
83. Wheelock C.E., Eder K.J., Werner I., Huang H., Jones P.D., Brammell B.F., Elskus A.A., and Hammock B.D. Individual variability in esterase activity and CYP1A levels in Chinook salmon (Oncorhynchus tshawytscha) exposed to esfenvalerate and chlorpyrifos. Aquat. Toxicol. 74 (2005) 172-192
84. Yamashita M., Hirayoshi K., and Nagata K. Characterization of multiple members of the HSP70 family in platyfish culture cells: molecular evolution of stress protein HSP70 in vertebrates. Gene 336 (2004) 207-218
85. Zelikoff J.T., Raymond A., Carlson E., Li Y., Beaman J.R., and Anderson M. Biomarkers of immunotoxicity in fish: from the lab to the ocean. Toxicol. Lett. (Amst.) (2000) 325-331
86. Zou J., Holland J., Pleguezuelos O., Cunningham C., and Secombes C.J. Factors influencing the expression of interleukin-1β in cultured rainbow trout (Oncorhynchus mykiss) leucocytes. Dev. Comp. Immunol. 24 (2000) 575-582