Molecular crosstalk between a chemical and a biological stressor and consequences on disease manifestation in rainbow trout

Aquatic Toxicology

Volumn 127, Issue , 2013, Pages 2-8

  Burki, Richard ^a   Krasnov, Aleksei ^b   Bettge, Kathrin ^a   Rexroad, Caird E ^c   Afanasyev, Sergey ^d   Antikainen, Miia ^e   Burkhardt Holm, Patricia ^f   Wahli, Thomas ^a   Segner, Helmut ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b NOFIMA   (Norway)

^c NATIONAL CENTER FOR COOL AND COLD WATER AQUACULTURE   (United States)

^d SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^e UNIVERSITY OF EASTERN FINLAND   (Finland)

^f UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Endocrine disruption; Estrogen; Multiple stressors; Pathogen; Proliferative kidney disease; Rainbow trout

Indexed keywords

ESTRADIOL; ESTROGEN; RNA;

ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; PARASITE; PATHOGEN; POLLUTION EXPOSURE; POPULATION DECLINE; SALMONID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AQUATIC ENVIRONMENT; ARTICLE; CONTROLLED STUDY; ENDOPARASITE; ENVIRONMENTAL STRESS; EXPOSURE; GENE EXPRESSION; KIDNEY; LIVER; MICROARRAY ANALYSIS; MOLECULAR INTERACTION; MORTALITY; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; RAINBOW TROUT; REAL TIME POLYMERASE CHAIN REACTION; TETRACAPSULOIDES BRYOSALMONAE;

ANIMALS; ESTRADIOL; FISH DISEASES; GENE EXPRESSION REGULATION; MYXOZOA; ONCORHYNCHUS MYKISS; PARASITIC DISEASES, ANIMAL; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; WATER POLLUTANTS, CHEMICAL;

MYXOZOA; ONCORHYNCHUS MYKISS; SALMO TRUTTA; SALMONIDAE; TETRACAPSULOIDES BRYOSALMONAE;

EID: 84872194034     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.02.026     Document Type: Article

References (58)

1. Altenburger R., Greco W.R. Extrapolation concepts for dealing with multiple contamination in environmental risk assessment. Integr. Environ. Assessm. Manage. 2009, 5:62-68.
2. Arkoosh M.R., Casillas E., Huffman P., Clemons E., Evered J., Stein J.E., Varanasi U. Increased susceptibility of juvenile Chinook salmon from a contaminated estuary to Vibrio anguillarum. Trans. Am. Fish. Soc. 1998, 127:360-374.
3. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., Harries M.A., Hill D.P., Issel-Tarver L., Kasarkis A., Lewis S., Matese J.C., Richardson J.E., Ringwald M., Rubin G.M., Sherlock G. Gene ontology: tool for the unification of biology: the gene Ontology Consortium. Nat. Genet. 2005, 25:25-29.
4. Bettge K., Wahli T., Segner H., Schmidt-Posthaus H. Proliferative kidney disease in rainbow trout: time- and temperature-related renal pathology and parasite distribution. Dis. Aquat. Organ. 2009, 83:67-76.
5. Bettge K., Segner H., Burki R., Schmidt-Posthaus H., Wahlim T. Proliferative kidney disease (PKD) of rainbow trout: temperature- and time-related changes of Tetracapasuloides bryosalmonae DNA in the kidney. Parasitology 2009, 136:615-625.
6. Braunbeck T., Segner H. Preexposure temperature acclimation and diet as modifying factors for the tolerance of golden ide (Leuciscus idus melanotus) to short-term exposure to 4-chloroaniline. Ecotoxicol. Environ. Saf. 1992, 24:72-94.
7. Burkhardt-Holm P., Giger W., Güttinger H., Ochsenbein U., Peter A., Scheurer K., Segner H., Staub E., Suter M.J.F. Where have all the fish gone ?. Environ. l Sci. Technol. 2005, 39:441A-447A.
8. Burki R., Vermeirssen E.L.M., Körner O., Joris C., Burkhardt-Holm P., Segner H. Assessment of estrogenic exposure in brown trout (Salmo trutta) in a Swiss midland river Integrated analysis of passive samplers, wild and caged fish, and vitellogenin mRNA and protein. Environ. Toxicol. Chem. 2006, 25:2077-2086.
9. Cabas I., Liarte S., Garcia-Alcazar A., Meseguer J., Mulero V., Garcia-Ayala A. 17α-Ethynylestradiol alters the immune response of the teleost gilthead seabream (Sparus aurata L.) both in vivo and in vitro. Dev. Comp. Immunol. 2011, 36:547-556.
10. Callahan M.A., Sexton K. If cumulative risk assessment is the answer, what is the question?. Environ. Health Perspect. 2007, 115:799-806.
11. Casanova-Nakayama A., Wenger M., Burki R., Eppler E., Krasnov A., Segner H. Endocrine disrupting compounds: can they target the immune system of fish?. Mar. Pollut. Bull. 2011, 63:412-416.
12. Couillard M., Courtenay S.C., Macdonald R.W., Palace V.P. Chemical-environment interactions affecting the risk of impacts on aquatic organisms: a review with a Canadian perspective - interactions affecting exposure. Can. J. Fish. Aquat. Sci. 2008, 16:1-7.
13. Couillard M., Courtenay S.C., Macdonald R.W. Chemical-environment interactions affecting the risk of impacts on aquatic organisms: a review with a Canadian perspective - interactions affecting vulnerability. Can. J. Fish. Aquat. Sci. 2008, 16:19-44.
14. Coors A., De Meester L. Synergistic, antagonistic and additive effects of multiple stressors: predation threat, parasitism, and pesticide exposure in Daphnia magna. J. Appl. Ecol. 2008, 45:1820-1828.
15. Crain C.M., Kroeker K., Halpern B.S. Interactive and cumulative effects of multiple stressors in marine systems. Ecol. Lett. 2008, 11:1304-1315.
16. D'Silva J., Mulcahy M.F., Kinkelin P. Experimental transmission of proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. J. Fish Dis. 1984, 7:235-239.
17. Felty Q. Estrogen-induced DNA synthesis in vascular endothelial cells is mediated by ROS signaling. BMC Cardiovasc. Disord. 2006, 6:16.
18. Folt C.L., Chen C.Y., Moore M.V., Burnaford J. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 1999, 44:864-877.
19. French S.S., Moore M.C., Demas G.E. Ecological immunology: the organism in context. Integr. Comp. Biol. 2009, 49:246-253.
20. Goetz C.W., Stamm C., Fenner K., Singer H., Schärer M., Hollender J. Targeting aquatic microcontaminants fro monitoring: exposure categorization and application tot he Swiss situation. Environ. Sci. Poll. Res. 2010, 17:341-354.
21. Guerrero R.D. Use of androgens for the production of all-male Tilapia aurea (Steindachner). Trans. Am. Fish. Soc. 1975, 104:342-348.
22. Hedrick R.P., MacConnel E., Kinkelin P. Proliferative kidney disease of salmonid fish. Annual Rev. of Fish Diseases 1993, vol. III. Pergamon Press, New York, pp. 277-290.
23. Heugens E.H.W., Hendriks A.J., Dekker T., Van Straalen N.M., Admiraal W. A review of the effects of multiple stressors on aquatic organism and analysis of uncertainty factors for use in risk assessment. Crit. Rev. Toxicol. 2001, 31:247-284.
24. Hoffmann J.L., Torontali S.P., Thomason R.G., Lee D.M., Brill J.L., Price B.B., Carr G.J., Versteeg D.J. Hepatic gene expression profiling using genechips in zebrafish exposed to 17α-ethynylestradiol. Aquat. Toxicol. 2006, 79:233-246.
25. Jayachandran M., Sanzo A., Owen W.G., Miller V.M. Estrogenic regulation of tissue factor and tissue factor pathway inhibitor in platelets. Am. J. Physiol. Heart Circul. Physiol. 2005, 289:1908-1916.
26. Jokela J., Taskinen J., Mutikainen P., Kopp K. Virulence of parasites in hosts under environmental stress: experiments with anoxia and starvation. Oikos 2005, 108:156-164.
27. Kiesecker J.M. Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature?. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:9900-9904.
28. Kiesecker J.M., Blaustein A.R., Belden L.K. Complex causes of amphibian population declines. Nature 2001, 410:681-684.
29. Kling P.G., Olsson P.-E. Involvement of differential metallothionein expression in free radical sensitivity of RTG-2 and CHSE-214 cells. Free Radic. Biol. Med. 2000, 28:1628-1637.
30. Koskinen H., Pehkonen P., Vehniäinen E., Krasnov A., Rexroad C., Afanasyev S., Mölsä H., Oikari A. Response of rainbow trout transcriptome to model chemical contaminants. Biochem. Biophys. Res. Commun. 2004, 320:745-753.
31. Krasnov A., Koskinen H., Rexroad C., Afanasyev S., Mölsä H., Oikari A. Transcriptome responses to carbon tetrachloride and pyrene in the kidney and liver of juvenile rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 2005, 74:70-81.
32. Krasnov A., Afanasyev S., Oikari A. Hepatic responses of gene expression in juvenile brown trout (Salmo trutta lacustris) exposed to three model contaminants applied singly and in combination. Environ. Toxicol. Chem. 2007, 26:100-109.
33. Landis W.G., Duncan P., Hayes E., Markiewicz A.J., Thomas J.F. A regional retrospective assessment of the potential stressors causing the decline of the Cherry Point Pacific Herring run. Human Ecol. Risk Assess. 2004, 3:287-297.
34. MacKenzie S., Iliev D., Liarte C., Koskinen H., Planas J., Goetz F.W., Mölsä H., Krasnov A., Tort L. Transcriptional analysis of LPS-stimulated activation of trout (O. mykiss) monocyte/macrophage cells in primary culture treated with cortisol. Mol. Immunol. 2006, 43:1340-1348.
35. Martin J.T. Sex dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur. J. Pharmacol. 2000, 405:251-261.
36. Milla S., Depiereux S., Kestemont P. The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review. Ecotoxicology 2011, 20:305-319.
37. Moggs J.G. Molecular responses to xenoestrogens: mechanistic insights form toxicogenomics. Toxicology 2005, 213:177-193.
38. Morley N.J. Interactive effects of infectious diseases and pollution in aquatic mollusks. Aquat. Toxicol. 2010, 96:27-36.
39. Nakamura K., Yonezawa S., Yoshizaki N. Vitellogenesis-related ovary cathepsin D from Xenopus laevis: purification and properties in comparison with liver cathepsin D. Comp. Biochem. Physiol. 1996, 113B:835-840.
40. Rice C.D. Fish immunotoxicology: understanding mechanisms of action. Target Organ Toxicity in Marine and Freshwater Teleosts 2001, vol. 2:96-138. Taylor & Francis, London.
41. Rohr J.R., Schotthoegr A.M., Raffel T.R., Carrick H.J., Halstead N., Hoverman J.T., Johnson V.M., Lieske C., Piwoni M.D., Schoff P.K., Beasley V.R. Agrochemicals increase trematode infections in declining amphibian species. Nature 2008, 455:1235.
42. Segner H. Response of fed and starved roach, Rutilus rutilus, to sublethal copper contamination. J. Fish Biol. 1987, 30:423-438.
43. Segner H. Ecotoxicology - how to assess the impact of toxicants in a multifactorial environment?. Multiple Stressors: A Challenge for the Future. NATO Advanced Workshop. Environmental Security 2007, 39-56. Springer, Heidelberg/New York. C. Mothersill, I. Mosse, C. Seymour (Eds.).
44. Segner H. Moving beyond a descriptive aquatic toxicology: the value of biological process and trait information. Aquat. Toxicol. 2011, 105S:50-55.
45. Segner H. Reproductive and developmental toxicity in fishes. Reproductive and Developmental Toxicology 2011, 1145-1166. Elsevier, Amsterdam. R.C. Gupta (Ed.).
46. Sheras N.T., Ross P.M. Toxic cascades: multiple anthropogenic stressors have complex and unanticipated interactive effects on temperate reefs. Ecol. Lett. 2010, 13:1149-1159.
47. Skugor S., Jørgensen S.M., Gjerde B., Krasnov A. Hepatic gene expression profiling reveals protective responses in Atlantic salmon vaccinated against furunculosis. BMC Genomics 2009, 10:503.
48. Song J.Y., Nakayama K., Murakami Y., Kitamura S.I. Heavy oil exposure induces high mortalities in virus carrier Japanes flounder (Paralichthys oliveaceus). Mar. Pollut. Bull. 2011, 63:362-365.
49. Springman K.R., Kurath G., Anderson J.J., Emlen J.M. Contaminants as viral cofactors: assessing indirect population effects. Aquat. Toxicol. 2005, 71:13-23.
50. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
51. Sutherland R.L., Prall O.W.J., Watts C.K.W., Musgrove E.A. Estrogen and progestin regulation of cell cycle progression. J. Mammary Gland Biol. Neoplasia 1998, 1:63-72.
52. Thilagam H., Gopalokrishnan S., Bo J., Wang K.J. Effect of 17β-estradiol on the immunocompetence of Japanese sea bass (Lateolabrax japonicus). Environ. Toxicol. Chem. 2009, 28:1722-1731.
53. Vermeirssen E.L.M., Burki R., Joris C., Peter A., Segner H., Suter M.J.-F., Burkhardt-Holm P. Characterisation of the estrogenicity of Swiss midland rivers using a recombinant yeast bioassay and plasma vitellogenin concentrations in feral male brown trout. Environ. Toxicol. Chem. 2005, 24:2226-2233.
54. Vinuelea A., Snoek L.B., Riksen J.A.G., Kammenga J.E. Gene expression modifications by temperature-toxicvant interactions in Chaneorhabditis elegans. PLoS ONE 2011, 6:e24676.
55. Wahli T., Bernet D., Steiner P.A., Schmidt-Posthaus H. Geographic distribution of Tetracapsuloides bryosalmonae infected fish in Swiss rivers: an update. Aquat. Sci. 2007, 69:3-10.
56. Wahli T., Bernet D., Segner H., Schmidt-Posthaus H. Role of altitude and water temperature as regulating factors for the geographical distribution of Tetracapsuloides bryosalmonae-infected fishes in Switzerland. J. Fish Biol. 2008, 73:2184-2197.
57. Wenger M., Sattler U., Goldschmidt-Clermont E., Segner H. 17Beta-estradiol affects complement components and survival of rainbow trout (Oncorhynchus mykiss) challenged by bacterial (Yersinia ruckeri) infection. Fish Shellfish Immunol. 2011, 31:90-97.
58. Williams T.D., Diab A.M., George S.G., Sabine V., Chipman J.K. Gene expression of European flounder (Platichthys flesus) to 17-β estradiol. Toxicol. Lett. 2007, 168:236-248.