Molecular responses to toxicological stressors: Profiling microRNAs in wild atlantic salmon (salmo salar) exposed to acidic aluminum-rich water

Aquatic Toxicology

Volumn 138-139, Issue , 2013, Pages 98-104

  Kure, Elin H ^a,b   Sæbø, Mona ^a   Stangeland, Astrid M ^b   Hamfjord, Julian ^b   Hytterød, Sigurd ^c   Heggenes, Jan ^a   Lydersen, Espen ^a  

^a UNIVERSITY OF SOUTH EASTERN NORWAY   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

Acid aluminum water; Atlantic salmon; High throughput sequencing; MicroRNA responses; Salmo salar; Toxicological stress

Indexed keywords

ALUMINUM; CARBON DIOXIDE; CATECHOLAMINE; CHLORIDE ION; CORTICOSTEROID; FRESH WATER; GLUCOSE; HYDROCORTISONE; MICRORNA; SODIUM ION;

ACIDITY; ALUMINUM; BIOMARKER; DOSE-RESPONSE RELATIONSHIP; GENE EXPRESSION; GENETIC ANALYSIS; IDENTIFICATION METHOD; MOLECULAR ANALYSIS; PHYSIOLOGICAL RESPONSE; POLLUTION EFFECT; POLLUTION EXPOSURE; RNA; SALMONID; TOXICOLOGY;

ACID RAIN; ANIMAL TISSUE; ARTICLE; ATLANTIC SALMON; BIOINFORMATICS; CARBON DIOXIDE TENSION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; GENETIC CONSERVATION; GLUCOSE BLOOD LEVEL; HEMATOCRIT; HIGH THROUGHPUT SEQUENCING; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ANALYSIS; STRESS; UPREGULATION; WATER ACIDIFICATION; WATER POLLUTION; ZEBRA FISH;

ALUMINUM; ANIMALS; BASE SEQUENCE; BIOLOGICAL MARKERS; BLOOD GLUCOSE; CARBON DIOXIDE; CHLORIDES; GENE EXPRESSION REGULATION; HEMATOCRIT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HYDROGEN-ION CONCENTRATION; MICRORNAS; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; SALMO SALAR; SODIUM; WATER POLLUTANTS, CHEMICAL;

ATLANTIC OCEAN;

ANIMALIA; DANIO RERIO; SALMO SALAR;

EID: 84879423232     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.04.004     Document Type: Article

References (76)

1. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
2. Amin I., Patil B.L., Briddon R.W., Mansoor S., Fauquet C.M. A common set of developmental miRNAs are upregulated in Nicotiana benthamiana by diverse begomoviruses. Virology Journal 2011, 8.
3. Anders S., Huber W. Differential expression analysis for sequence count data. Genome Biology 2010, 11:R106.
4. Andreassen R., Lunner S., Hoyheim B. Characterization of full-length sequenced cDNA inserts (FLIcs) from Atlantic salmon (Salmo salar). BMC Genomics 2009, 10:502.
5. Andreassen R., Lunner S., Hoyheim B. Characterization of full-length sequenced cDNA inserts (FLIcs) from Atlantic salmon (Salmo salar). BMC Genomics 2009, 10.
6. Barton B.A. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology 2002, 42:517-525.
7. Baumgart M., Groth M., Priebe S., Appelt J., Guthke R., Platzer M., Cellerino A. Age-dependent regulation of tumor-related microRNAs in the brain of the annual fish Nothobranchius furzeri. Mechanisms of Ageing and Development 2012, 133:226-233.
8. Benjamini Y., Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 1995, 57:289-300.
9. Berezikov E., Thuemmler F., van Laake L.W., Kondova I., Bontrop R., Cuppen E., Plasterk R.H. Diversity of microRNAs in human and chimpanzee brain. Nature Genetics 2006, 38:1375-1377.
10. Bonga S.E.W. The stress response in fish. Physiological Reviews 1997, 77:591-625.
11. Cameron J.N. Branchial ion uptake in arctic grayling: resting values and effects of acid-base disturbance. Journal of Experimental Biology 1976, 64:711-725.
12. Chi W., Tong C.B., Gan X.N., He S.P. Characterization and comparative profiling of miRNA transcriptomes in bighead carp and silver carp. PLoS ONE 2011, 6.
13. Cronan C.S., Schofield C.L. Aluminum leaching response to acid precipitation - effects on high-elevation watersheds in the northeast. Science 1979, 204:304-306.
14. Davidson W.S., Koop B.F., Jones S.J., Iturra P., Vidal R., Maass A., Jonassen I., Lien S., Omholt S.W. Sequencing the genome of the Atlantic salmon (Salmo salar). Genome Biology 2010, 11:403.
15. Dougan W.K., Wilson A.L. The absorptiometric determination of aluminium in water. A comparison of some chromogenic reagents and the development of an improved method. Analyst 1974, 99:413-430.
16. Driscoll C.T., Baker J.P., Bisogni J.J., Schofield C.L. Effect of aluminum speciation on fish in dilute acidified waters. Nature 1980, 284:161-164.
17. Farazi T.A., Spitzer J.I., Morozov P., Tuschl T. miRNAs in human cancer. Journal of Pathology 2011, 223:102-115.
18. Fu Y.S., Shi Z.Y., Wu M.L., Zhang J.L., Jia L., Chen X.W. Identification and differential expression of microRNAs during metamorphosis of the Japanese flounder (Paralichthys olivaceus). PLoS ONE 2011, 6.
19. Gaidatzis D., van Nimwegen E., Hausser J., Zavolan M. Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 2007, 8.
20. Grande M., Muniz I.P., Andersen S. Relative tolerance of some salmonids to acid waters. Verhandlungen des Internationalen Verein Limnologie 1978, 20:2076-2084.
21. Green R.E., Krause J., Ptak S.E., Briggs A.W., Ronan M.T., Simons J.F., Du L., Egholm M., Rothberg J.M., Paunovic M., Paabo S. Analysis of one million base pairs of Neanderthal DNA. Nature 2006, 444:330-336.
22. Griffiths-Jones S., Saini H., van Dongen S., Enright A. miRBase: tools for microRNA genomics. Nucleic Acids Research 2008, D154-D158.
23. Ha M., Pang M.X., Agarwal V., Chen Z.J. Interspecies regulation of microRNAs and their targets. Biochimica Biophysica Acta - Gene Regulatory Mechanisms 2008, 1779:735-742.
24. Hackenberg M., Sturm M., Langenberger D., Falcon-Perez J.M., Aransay A.M. miRanalyzer: a microRNA detection and analysis tool for next-generation sequencing experiments. Nucleic Acids Research 2009, 37:W68-W76.
25. Hesthagen T., Hansen L.P. Estimates of the annual loss Atlantic salmon, Salmo salar L., in Norway due to acidification. Aquatic Research and Fish Management 1991, 22:85-91.
26. Hou L., Wang D., Baccarelli A. Environmental chemicals and microRNAs. Mutation Research 2011, 714:105-112.
27. Howells G., Dalziel T.R.K., Reader J.P., Solbé J.F. In Water Quality for Freshwater Fish. Further Advisory Criteria 1994, 55-115. Gordon and Breach Science Publishers.
28. Hudder A., Novak R.F. miRNAs: effectors of environmental influences on gene expression and disease. Toxicological Sciences 2008, 103:228-240.
29. Johansen S.D., Karlsen B.O., Furmanek T., Andreassen M., Jørgensen T.E., Bizuayehu T.T., Breines R., Emblem Å., Kettunen P., Luukko K., Edvardsen R.B., Nordeide J.T., Coucheron D.H., Moum T. RNA deep sequencing of the Atlantic cod transcriptome. Comparative Biochemistry and Physiology D 2011, 6:18-22.
30. Johnsen B.O., Jensen A.J. The Gyrodactylus story in Norway. Aquaculture 1991, 98:289-302.
31. Johnston I.A., Lee H.T., Macqueen D.J., Paranthaman K., Kawashima C., Anwar A., Kinghorn J.R., Dalmay T. Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. Journal of Experimental Biology 2009, 212:1781-1793.
32. Jung J.H., Seo P.J., Park C.M. MicroRNA biogenesis and function in higher plants. Plant Biotechnology Report 2009, 3:111-126.
33. Kantar M., Lucas S.J., Budak H. miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 2011, 233:471-484.
34. Kulshreshtha R., Ferracin M., Wojcik S.E., Garzon R., Alder H., Agosto-Perez F.J., Davuluri R., Liu C.G., Croce C.M., Negrini M., Calin G.A., Ivan M. A microRNA signature of hypoxia. Molecular and Cellular Biology 2007, 27:1859-1867.
35. Lacroix G.L., Townsend D.R. Responses of Juvenile Atlantic Salmon (Salmo-Salar) to Episodic Increases in Acidity of Nova-Scotia Rivers. Canadian Journal of Fisheries and Aquatic Sciences 1987, 44:1475-1484.
36. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Radmark O., Kim S., Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
37. Lema C., Cunningham M.J. MicroRNAs and their implications in toxicological research. Toxicology Letters 2010, 198:100-105.
38. Li S.C., Chan W.C., Hu L.Y., Lay C.H., Hsu C.N., Lin W. Identification of homologous microRNAs in 56 animal genomes. Genomics 2010, 96:1-9.
39. Li B.S., Qin Y.R., Duan H., Yin W.L., Xia X.L. Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. Journal of Experimental Botany 2011, 62:3765-3779.
40. Liu H.H., Tian X., Li Y.J., Wu C.A., Zheng C.C. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 2008, 14:836-843.
41. Lu S., Sun Y.H., Chiang V.L. Stress-responsive microRNAs in Populus. Plant Journal 2008, 55:131-151.
42. Lydersen E., Lofgren S., Arnesen R.T. Metals in Scandinavian surface waters: effects of acidification, liming, and potential reacidification. Critical Reviews in Environment Science and Technology 2002, 32:73-295.
43. + fluxes. Journal of Experimental Biology 1983, 102:123-140.
44. Mcdonald D.G., Walker R.L., Wilkes P.R.H. The interaction of environmental calcium and low pH on the physiology of the rainbow-trout, Salmo gairdneri. 2. Branchial ionoregulatory mechanisms. Journal of Experimental Biology 1983, 102:141-155.
45. Mello C.C., Conte D. Revealing the world of RNA interference. Nature 2004, 431:338-342.
46. Melo S.A., Esteller M. Dysregulation of microRNAs in cancer: playing with fire. FEBS Letters 2011, 585:2087-2099.
47. Monette M.Y., McCormick D. Impacts of short-term acid and aluminum exposure on Atlantic salmon (Salmo salar) physiology: a direct comparison of parr and smolts. Aquatic Toxicology 2008, 86:216-226.
48. Mommsen T.P., Vijayan M.M., Moon T.W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Reviews in Fish Biology and Fisheries 1999, 9:211-268.
49. Murani E., Ponsuksili S., D'Eath R.B., Turner S.P., Evans G., Tholking L., Kurt E., Klont R., Foury A., Mormede P., Wimmers K. Differential mRNA expression of genes in the porcine adrenal gland associated with psychosocial stress. Journal of Molecular Endocrinology 2011, 46:165-174.
50. Neville C.M. Physiological response of juvenile rainbow-trout, Salmo gairdneri, to acid and aluminum - prediction of field responses from laboratory data. Canadian Journal of Fisheries and Aquatic Sciences 1985, 42:2004-2019.
51. Neville C.M., Campbell P.G.C. Possible mechanisms of aluminum toxicity in a dilute, acidic environment to fingerlings and older life stages of salmonids. Water, Air, and Soil Pollution 1988, 42:311-327.
52. Nilsen T.W. Mechanisms of microRNA-mediated gene regulation in animal cells. Trends in Genetics 2007, 23:243-249.
53. Niwa R., Slack F.J. The evolution of animal microRNA function. Current Opinion in Genetics and Development 2007, 17:145-150.
54. Pan Q., Shai O., Lee L.J., Frey B.J., Blencowe B.J. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nature Genetics 2008, 40:1413-1415.
55. Paul S., Kim S.J., Park H.W., Lee S.Y., An Y.R., Oh M.J., Jung J.W., Ryu J.C., Hwang S.Y. Impact of miRNA deregulation on mRNA expression profiles in response to environmental toxicant, nonylphenol. Molecular and Cellular Toxicology 2011, 7:259-269.
56. Poleo A.B.S., Ostbye K., Oxnevad S.A., Andersen R.A., Heibo E., Vollestad L.A. Toxicity of acid aluminium-rich water to seven freshwater fish species: a comparative laboratory study. Environmental Pollution 1997, 96:129-139.
57. Poleo A.B.S., Schjolden J., Hansen H., Bakke T.A., Mo T.A., Rosseland B.O., Lydersen E. The effect of various metals on Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon (Salmo salar). Parasitology 2004, 128:169-177.
58. Reid S.G., Bernier N.J., Perry S.F. The adrenergic stress response in fish: control of catecholamine storage and release. Comparative Biochemistry and Physiology 1998, 120C:1-27.
59. Rogeberg E.J.S., Henriksen A. An automatic method for fratctionation and determination of aluminium species in fresh water. Vatten 1985, 41:48-53.
60. Schecher W.D., Dricoll C.T. An evaluation of uncertainty associated with aluminium equilibrium calculations. Water Resources Research 1987, 23:525-534.
61. Schecher W.D., Dricoll C.T. An evaluation of the equilibrium calculations within acidification models: the effects of uncertainty in measured chemical comopunds. Water Resources Research 1988, 24:533-540.
62. Soleng A., Poleo A.B.S., Alstad N.E.W., Bakke T.A. Aqueous aluminium eliminates Gyrodactylus salaris (Platyhelminthes, Monogenea) infections in Atlantic salmon. Parasitology 1999, 119:19-25.
63. Staurnes M., Blix P., Reite O.B. Effects of acid water and aluminium on parr-smolt transformation and seawater tolerance in Atlantic salmon, Salmo salar. Canadian Journal of Fisheries and Aquatic Sciences 1993, 50:1816-1827.
64. Sultan M., Schulz M.H., Richard H., Magen A., Klingenhoff A., Scherf M., Seifert M., Borodina T., Soldatov A., Parkhomchuk D., Schmidt D., O'Keeffe S., Haas S., Vingron M., Lehrach H., Yaspo M.L. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 2008, 321:956-960.
65. Takacs C.M., Giraldez A.J. MicroRNAs as genetic sculptors: fishing for clues. Seminars in Cell and Developmental Biology 2010, 21:760-767.
66. Thomas R.K., Baker A.C., Debiasi R.M., Winckler W., Laframboise T., Lin W.M., Wang M., Feng W., Zander T., MacConaill L., Lee J.C., Nicoletti R., Hatton C., Goyette M., Girard L., Majmudar K., Ziaugra L., Wong K.K., Gabriel S., Beroukhim R., Peyton M., Barretina J., Dutt A., Emery C., Greulich H., Shah K., Sasaki H., Gazdar A., Minna J., Armstrong S.A., Mellinghoff I.K., Hodi F.S., Dranoff G., Mischel P.S., Cloughesy T.F., Nelson S.F., Liau L.M., Mertz K., Rubin M.A., Moch H., Loda M., Catalona W., Fletcher J., Signoretti S., Kaye F., Anderson K.C., Demetri G.D., Dummer R., Wagner S., Herlyn M., Sellers W.R., Meyerson M., Garraway L.A. High-throughput oncogene mutation profiling in human cancer. Nature Genetics 2007, 39:347-351.
67. Thomas R.K., Nickerson E., Simons J.F., Janne P.A., Tengs T., Yuza Y., Garraway L.A., LaFramboise T., Lee J.C., Shah K., O'Neill K., Sasaki H., Lindeman N., Wong K.K., Borras A.M., Gutmann E.J., Dragnev K.H., DeBiasi R., Chen T.H., Glatt K.A., Greulich H., Desany B., Lubeski C.K., Brockman W., Alvarez P., Hutchison S.K., Leamon J.H., Ronan M.T., Turenchalk G.S., Egholm M., Sellers W.R., Rothberg J.M., Meyerson M. Sensitive mutation detection in heterogeneous cancer specimens by massively parallel picoliter reactor sequencing. Nature Medicine 2006, 12:852-855.
68. Tijsterman M., Plasterk R.H. Dicers at RISC; the mechanism of RNAi. Cell 2004, 117:1-3.
69. Wang T.Z., Chen L., Zhao M.G., Tian Q.Y., Zhang W.H. Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 2011, 12.
70. Wheeler D.A., Srinivasan M., Egholm M., Shen Y., Chen L., McGuire A., He W., Chen Y.J., Makhijani V., Roth G.T., Gomes X., Tartaro K., Niazi F., Turcotte C.L., Irzyk G.P., Lupski J.R., Chinault C., Song X.Z., Liu Y., Yuan Y., Nazareth L., Qin X., Muzny D.M., Margulies M., Weinstock G.M., Gibbs R.A., Rothberg J.M. The complete genome of an individual by massively parallel DNA sequencing. Nature 2008, 452:872-876.
71. Wienholds E., Plasterk R.H.A. MicroRNA function in animal development. FEBS Letters 2005, 579:5911-5922.
72. Xia J.H., He X.P., Bai Z.Y., Yue G.H. Identification and characterization of 63 microRNAs in the Asian seabass lates calcarifer. PLoS ONE 2011, 6.
73. Yokoi T., Nakajima M. Toxicological implications of modulation of gene expression by microRNAs. Toxicological Sciences 2011, 123:1-14.
74. Zeng L., Childs S.J. The smooth muscle microRNA miR-145 regulates gut epithelial development via a paracrine mechanism. Developmental Biology 2012, 367:178-186.
75. Zhang B.H., Wang Q.L., Pan X.P. MicroRNAs and their regulatory roles in animals and plants. Journal of Cellular Physiology 2007, 210:279-289.
76. Zhang L., Li Y.Y., Zeng H.C., Wei J., Wan Y.J., Chen J., Xu S.Q. MicroRNA expression changes during zebrafish development induced by perfluorooctane sulfonate. Journal of Applied Toxicology 2011, 31:210-222.