How does exposure to nickel and cadmium affect the transcriptome of yellow perch (Perca flavescens) - Results from a 1000 candidate-gene microarray

Aquatic Toxicology

Volumn 142-143, Issue , 2013, Pages 355-364

  Bougas, Bérénice ^a,b   Normandeau, Eric ^b   Pierron, Fabien ^c,d   Campbell, Peter G C ^a   Bernatchez, Louis ^b   Couture, Patrice ^a  

^a CENTRE EAU TERRE ENVIRONNEMENT   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d UNIVERSITÉ BORDEAUX 1   (France)

Author keywords

Cadmium; Ecotoxicology; Microarrays; Nickel; Yellow perch

Indexed keywords

CADMIUM; CALCIUM; IRON; NICKEL; OXYGEN; TRANSCRIPTOME; VITAMIN;

BIOMARKER; CADMIUM; CONCENTRATION (COMPOSITION); ECOTOXICOLOGY; ENVIRONMENTAL FACTOR; GENE; METABOLISM; NICKEL; PERCIFORM; TOXICITY;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CLOTTING; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIETARY INTAKE; ECOTOXICOLOGY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; GENE FUNCTION; GENETIC TRANSCRIPTION; IRON METABOLISM; MICROARRAY ANALYSIS; NONHUMAN; PERCA FLAVESCENS; PRIORITY JOURNAL; RNA SEQUENCE; RNA TRANSLATION; TEMPERATURE STRESS; TRANSCRIPTOMICS; VITAMIN METABOLISM; WATER CONTAMINATION;

CADMIUM; ECOTOXICOLOGY; MICROARRAYS; NICKEL; YELLOW PERCH;

ANIMALS; CADMIUM; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION REGULATION; LIVER; NICKEL; PERCHES; PROTEIN ARRAY ANALYSIS; TEMPERATURE; TRANSCRIPTOME; WATER POLLUTANTS, CHEMICAL;

EID: 84884730033     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.09.009     Document Type: Article

References (82)

1. Alsop D., Wood C.M. Metal uptake and acute toxicity in zebrafish: common mechanisms across multiple metals. Aquatic Toxicology 2011, 105:385-393.
2. Altenburger R., Scholz S., Schmitt-Jansen M., Busch W., Escher B.I. Mixture toxicity revisited from a toxicogenomic perspective. Environmental Science & Technology 2012, 46:2508-2522.
3. Amara U., Rittirsch D., Flierl M., Bruckner U., Klos A., Gebhard F., Lambris J.D., et al. Interaction between the coagulation and complement system 2 serine protease systems. Current Topic in Complement II 2008, 71-79. Springer Science+Business Media, Berlin. J.D. Lambris (Ed.).
4. Audet D., Couture P. Seasonal variations in tissue metabolic capacities of yellow perch (Perca flavescens) from clean and metal-contaminated environments. Canadian Journal of Fisheries and Aquatic Sciences 2003, 60:269-278.
5. Bélanger-Déchêsnes S., Couture P., Campbell P.G.C., Bernatchez L. Evolutionary change driven by metal exposure as revealed by coding SNP genome scan in wild yellow perch (Perca flavescens). Ecotoxicology 2013, (Online early publication). 10.1007/s10646-013-1083-8.
6. Braun A.P., Schulman H. The multifuncional calcium/calmodulin-dependent protein kinase: from form to function. Annual Review of Physiology 1995, 57:417-445.
7. Buckley B.A., Gracey A.Y., Somero G.N. The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. Journal of Experimental Biology 2006, 209:2660-2677.
8. Bowden T.J. Modulation of the immune system of fish by their environment. Fish & Shellfish Immunology 2008, 25:373-383.
9. Chen H., Davidson T., Singleton S., Garrick M.D., Costa M. Nickel decreases cellular iron level and converts cytosolic aconitase to iron-regulatory protein 1 in A549 cells. Toxicology and Applied Pharmacology 2005, 206:275-287.
10. Choi G., Schultz M.J., Levi M., van der Poll T. The relationship between inflammation and the coagulation system. Swiss Medical Weekly 2006, 136:139-144.
11. Chua A.C.G., Graham R.M., Trinder D., Olynyk J.K. The regulation of cellular iron metabolism. Clinical Laboratory Sciences 2007, 44:413-459.
12. Conesa A., Götz S., García-Gómez J.M., Terol J., Talón M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
13. Couture P., Busby P., Gauthier C., Rajotte J., Pyle G. Seasonal and regional variations of metal contamination and condition indicators in yellow perch (Perca flavescens) along two polymetallic gradients. I. Factors influencing tissue metal concentrations. Human and Ecological Risk Assessment: HERA 2008, 14:97-125.
14. Cui X., Hwang J.T.G., Qiu J., Blades N.J., Churchill G.A. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 2005, 6:59-75.
15. Davidson T., Chen H., Garrick M.D., D'Angelo G., Costa M. Soluble nickel interferes with cellular iron homeostasis. Molecular and Cellular Biochemistry 2005, 279:157-162.
16. Defo M.A., Pierron F., Spear P.A., Bernatchez L., Campbell P.G.C., Couture P. Evidence for metabolic imbalance of vitamin A(2) in wild fish chronically exposed to metals. Ecotoxicology and Environmental Safety 2012, 85:88-95.
17. Dios S., Romero A., Chamorro R., Figueras A., Novoa B. Effect of the temperature during antiviral immune response ontogeny in teleosts. Fish and Shellfish Immunology 2010, 29:1019-1027.
18. Dominguez M., Takemura A., Tsuchiya M., Nakamura S. Impact of different environmental factors on the circulating immunoglobulin levels in the Nile tilapia, Oreochromis niloticus. Aquaculture 2004, 241:491-500.
19. Fedorenkova A., Vonk J.A., Lenders H.J.R., Ouborg N.J., Breure A.M., Jan H.A. Ecotoxicogenomics: bridging the gap between genes and populations. Environmental Science & Technology 2010, 44:9239-9240.
20. Feng S., Tillier E.R.M. A fast and flexible approach to oligonucleotide probe design for genomes and gene families. Bioinformatics 2007, 23:1195-1202.
21. Forbes V.E., Palmqvist A., Bach L. The use and misuse of biomarkers in ecotoxicology. Environmental Toxicology and Chemistry 2006, 25:272-280.
22. Fraser J., de Mello L.V., Ward D., Rees H.H., Williams D.R., Fang Y., Fang Y., et al. Hypoxia-inducible myoglobin expression in nonmuscle tissues. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:2977-2981.
23. Garcia-Reyero N., Poynton H.C., Kennedy A.J., Guan X., Escalon B.L., Chang B., Varshavsky J., et al. Biomarker discovery and transcriptomic responses in Daphnia magna exposed to munitions constituents. Environmental Science & Technology 2009, 43:4188-4193.
24. Gauthier C., Campbell P.G.C., Couture P. Physiological correlates of growth and condition in the yellow perch (Perca flavescens). Comparative Biochemistry and Physiology Part A 2008, 151:526-532.
25. Giguère A., Campbell P.G.C., Hare L., McDonald D.G., Rasmussen J.B. Influence of lake chemistry and fish age on cadmium, copper, and zinc concentrations in various organs of indigenous yellow perch (Perca flavescens). Canadian Journal of Fisheries and Aquatic Sciences 2004, 61:1702-1716.
26. Gracey A.Y., Fraser E.J., Li W., Fang Y., Taylor R.R., Rogers J., Brass A., et al. Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:16970-16975.
27. Gracey A.Y. Interpreting physiological responses to environmental change through gene expression profiling. Journal of Experimental Biology 2007, 210:1584-1592.
28. Guinot D., Ureña R., Pastor A., Varó I., del Ramo J., Torreblanca A. Long-term effect of temperature on bioaccumulation of dietary metals and metallothionein induction in Sparus aurata. Chemosphere 2012, 87:1215-1221.
29. Handy R.D., Depledge M.H. Physiological responses: their measurement and use as environmental biomarkers in ecotoxicology. Ecotoxicology 1999, 8:329-349.
30. Heugens E.H.W., Jager T., Creyghton R., Kraak M.H.S., Hendriks a.J., Van Straalen N.M., Admiraal W. Temperature-dependent effects of cadmium on Daphnia magna: accumulation versus sensitivity. Environmental Science & Technology 2003, 37:2145-2151.
31. Heugens E.H.W., Tokkie L.T.B., Kraak M.H.S., Hendriks A.J., Van Straalen N.M., Admiraal W. Population growth of Daphnia magna under multiple stress conditions: joint effects of temperature, food, and cadmium. Environmental Science & Technology 2006, 25:1399-1407.
32. Higuchi M., Celino F.T., Shimizu-Yamaguchi S., Miura C., Miura T. Taurine plays an important role in the protection of spermatogonia from oxidative stress. Amino Acids 2012, 10.1007/s00726-012-1316-9.
33. Jeffries M.K.S., Mehinto A.C., Carter B.J., Denslow N.D., Kolok A.S. Taking microarrays to the field: differential hepatic gene expression of caged fathead minnows from Nebraska watersheds. Environmental Science & Technology 2012, 46:1877-1885.
34. Johnston I., Guderley H., Franklin C., Crockford T., Kamunde C. Are mitochondria subject to evolutionary temperature adaptation?. Journal of Experimental Biology 1994, 195:293-306.
35. Ju Z., Dunham R.A., Liu Z. Differential gene expression in the brain of channel catfish (Ictalurus punctatus) in response to cold acclimation. Molecular Genetics and Genomics 2002, 268:87-95.
36. Ju Z., Wells M.C., Heater S.J., Walter R.B. Multiple tissue gene expression analyses in Japanese medaka (Oryzias latipes) exposed to hypoxia. Comparative Biochemistry and Physiology Part C 2007, 145:134-144.
37. Kassahn K.S., Caley M.J., Ward A.C., Connolly A.R., Stone G., Crozier R.H. Heterologous microarray experiments used to identify the early gene response to heat stress in a coral reef fish. Molecular Ecology 2007, 16:1749-1763.
38. Karaytug S., Sevgiler Y., Karayakar F. Comparison of the protective effects of antioxidant compounds in the liver and kidney of Cd- and Cr-exposed common carp. Environmental Toxicology 2011, 1-9. 10.1002/tox.
39. Kerr M.K., Martin M., Churchill G.A. Analysis of variance for gene expression microarray data. Journal of Computational Biology: A Journal of Computational Molecular Cell Biology 2000, 7:819-837.
40. Kerr M.K., Afshari C.A., Bennett L., Bushel P., Martinez J., Walker N.J., Churchill G.A. Statistical analysis of a gene expression microarray experiment with replication. Statistica Sinica 2002, 12:203-217.
41. Kogenaru S., Yan Q., Guo Y., Wang N. RNA-seq and microarray complement each other in transcriptome profiling. BMC Genomics 2012, 13:629.
42. Kraemer L.D., Campbell P.G.C., Hare L., Auclair J. A field study examining the relative importance of food and water as sources of cadmium for juvenile yellow perch (Perca flavescens). Canadian Journal of Fisheries and Aquatic Sciences 2006, 63:549-557.
43. 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. Environmental Toxicology and Chemistry 2007, 26:100-109.
44. Kubrak O.I., Husak V.V., Rovenko B.M., Poigner H., Mazepa M.A., Kriews M., Abele D., et al. Tissue specificity in nickel uptake and induction of oxidative stress in kidney and spleen of goldfish Carassius auratus, exposed to waterborne nickel. Aquatic Toxicology 2012, 118-119:88-96.
45. Kumar P., Prasad Y., Patra a.K., Ranjan R., Swarup D., Patra R.C., Pal S. Ascorbic acid, garlic extract and taurine alleviate cadmium-induced oxidative stress in freshwater catfish (Clarias batrachus). Science of the Total Environment 2009, 407:5024-5030.
46. Kwong R.W.M., Niyogi S. The interactions of iron with other divalent metals in the intestinal tract of a freshwater teleost, rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology 2009, 150:442-449.
47. Lam P.K.S. Use of biomarkers in environmental monitoring. Ocean Coastal Management 2009, 52:348-354.
48. Logan C.A., Somero G.N. Transcriptional responses to thermal acclimation in the eurythermal fish Gillichthys mirabilis (Cooper 1864). American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2010, 299:R843-R852.
49. Logan C.A., Somero G.N. Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2011, 300:1373-1383.
50. Long Y., Li L., Li Q., He X., Cui Z. Transcriptomic characterization of temperature stress responses in larval zebrafish. PLoS One 2012, 7:e37209.
51. Lü X., Lu H., Zhao L., Yang Y., Lu Z. Genome-wide pathways analysis of nickel ion-induced differential genes expression in fibroblasts. Biomaterials 2010, 31:1965-1973.
52. Malek R.L., Sajadi H., Abraham J., Grundy M., Gerhard G.S. The effects of temperature reduction on gene expression and oxidative stress in skeletal muscle from adult zebrafish. Comparative Biochemistry and Physiology 2004, 138:363-373.
53. Manna P., Sinha M., Sil P.C. Cadmium induced testicular pathophysiology: prophylactic role of taurine. Reproductive Toxicology 2008, 26:282-291.
54. Manna P., Sinha M., Sil P.C. Taurine plays a beneficial role against cadmium-induced oxidative renal dysfunction. Amino Acids 2009, 36:417-428.
55. McGeer J.C., Niyogi S., Smith D.C. Cadmium. Fish Physiology 2011, vol. 31B:125-184. Academic Press, Elsevier Inc., Waltham.
56. Nielsen F.H., Shuler T.R., McLeod T.G., Zimmerman T.J. Nickel influences iron metabolism through physiologic, pharmacologic and toxicologic mechanisms in the rat. Journal of Nutrition 1984, 114:1280-1288.
57. Pierron F., Bourret V., St-Cyr J., Campbell P.G.C., Bernatchez L., Couture P. Transcriptional responses to environmental metal exposure in wild yellow perch (Perca flavescens) collected in lakes with differing environmental metal concentrations (Cd, Cu, Ni). Ecotoxicology 2009, 18:620-631.
58. Pierron F., Normandeau E., Defo M.A., Campbell P.G.C., Bernatchez L., Couture P. Effects of chronic metal exposure on wild fish populations revealed by high-throughput cDNA sequencing. Ecotoxicology 2011, 20:1388-1399.
59. Podrabsky J.E., Somero G.N. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. Journal of Experimental Biology 2004, 207:2237-2254.
60. Poynton H.C., Varshavsky J.R., Chang S., Holman P.S., Loguinov A.V., Bauer D.J., Komachi K., et al. Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environmental Science & Technology 2007, 41:1044-1050.
61. Poynton H.C., Loguinov A.V., Varshavsky J.R., Chang S., Perkins E.J., Vulpe S.D. Gene expression profiling in Daphnia magna part I: concentration-dependent profiles provide support for the no observed transcriptional effect level. Environmental Science & Technology 2008, 42:6250-6256.
62. Pyle G., Couture P. Nickel. Fish Physiology 2011, vol. 31A:253-289. Academic Press, Elsevier Inc., Waltham.
63. Raos N., Kasprzak K.S. Allosteric binding of nickel (II) to calmodulin. Fundamental and Applied Toxicology 1989, 13:816-822.
64. Rajotte J.W., Couture P. Effects of environmental metal contamination on the condition, swimming performance, and tissue metabolic capacities of wild yellow perch (Perca flavescens). Canadian Journal of Fisheries and Aquatic Sciences 2002, 59:1296-1304.
65. Regoli F. Lysosomal responses as sensitive stress index in biomonitoring heavy metal pollution. Marine Ecology Progress Series 1992, 84:63-69.
66. Reynders H., van der Ven K., Moens L.N., van Remortel P., De Coen W.M., Blust R. Patterns of gene expression in carp liver after exposure to a mixture of waterborne and dietary cadmium using a custom-made microarray. Aquatic Toxicology 2006, 80:180-193.
67. Roberts J.J., Brandt S.B., Fanslow D., Ludsin S.A., Pothoven S.A., Scavia D., Hook T.O. Effects of hypoxia on consumption, growth, and RNA:DNA ratios of young yellow perch. Transactions of the American Fisheries Society 2011, 140:1574-1586.
68. Salem M., Silverstein J., Rexroad C.E., Yao J. Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 2007, 8:328.
69. Schaffer S.W., Azuma J., Mozaffari M. Role of antioxidant activity of taurine in diabetes. Canadian Journal of Physiology and Pharmacology 2009, 87:91-99.
70. Sîrbu A., Kerr G., Crane M., Ruskin H.J. RNA-seq vs dual- and single-channel microarray data: sensitivity analysis for differential expression and clustering. PLoS One 2012, 7:e50986.
71. Smith S., Bernatchez L., Beheregaray L.B. RNA-seq analysis reveals extensive transcriptional plasticity to temperature stress in a freshwater fish species. BMC Genomics 2013, 14. 10.1186/1471-2164-14-375.
72. Stanger O., Wonisch W. Enzymatic and non-enzymatic antioxidative effects of folic acid and its reduced derivates. Water Soluble Vitamins, Clinical Research and Future Applications, Subcellular Biochemistry 2012, vol. 56:151-161. Springer, Netherlands.
73. Soetaert A., Vandenbrouck T., van der Ven K., Maras M., van Remortel P., Blust R., De Coen W.M. Molecular responses during cadmium-induced stress in Daphnia magna: integration of differential gene expression with higher-level effects. Aquatic Toxicology 2007, 83:212-222.
74. Stocker P., Lesgards J.F., Vidal N., Chalier F., Prost M. ESR study of a biological assay on whole blood: antioxidant efficiency of various vitamins. Biochimica et Biophysica Acta 2003, 1621:1-8.
75. Suzuki Y., Chao S., Zysk J.R., Cheung W.Y. Stimulation of calmodulin by cadmium ion. Archives of Toxicology 1985, 57:205-211.
76. Ton C., Stamatiou D., Liew C-C. Gene expression profile of zebrafish exposed to hypoxia during development. Physiological Genomics 2003, 13:97-106.
77. Van Aggelen G., Ankley G.T., Baldwin W.S., Bearden D.W., Benson W.H., Chipman J.K., Collette T.W., et al. Integrating omic technologies into aquatic ecological risk assessment and environmental monitoring: hurdles, achievements, and future outlook. Environmental Health Perspectives 2010, 118:1-5.
78. Vandenbrouck T., Soetaert A., van der Ven K., Blust R., De Coen W. Nickel and binary metal mixture responses in Daphnia magna: molecular fingerprints and (sub)organismal effects. Aquatic Toxicology 2009, 92:18-29.
79. Vandenbrouck T., Dom N., Novais S., Soetaert A., Ferreira A.L.G., Loureiro S., Soares A.M.V.M., et al. Nickel response in function of temperature differences: effects at different levels of biological organization in Daphnia magna. Comparative Biochemistry and Physiology Part D: Genomics Proteomics 2011, 6:271-281.
80. Vergauwen L., Benoot D., Blust R., Knapen D. Long-term warm or cold acclimation elicits a specific transcriptional response and affects energy metabolism in zebrafish. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 2010, 157:149-157.
81. Vornanen M., Hassinen M., Koskinen H., Krasnov A. Steady-state effects of temperature acclimation on the transcriptome of the rainbow trout heart. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2005, 289:R1177-R1184.
82. Wolfinger R.D., Gibson G., Wolfinger E.D., Bennett L., Hamadeh H., Bushel P., Afshari C., et al. Assessing gene significance from cDNA microarray expression data via mixed models. Journal of Computational Biology 2001, 8:625-637.