Expression profiling in vivo demonstrates rapid changes in liver microRNA levels of whitefish (Coregonus lavaretus) following microcystin-LR exposure

Aquatic Toxicology

Volumn 122-123, Issue , 2012, Pages 188-196

  Brzuzan, P ^a   Wozny M ^a   Wolinska L ^a   Piasecka, A ^b  

^a UNIVERSITY OF WARMIA AND MAZURY IN OLSZTYN   (Poland)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Microcystin LR; MiRNA; MRNA; P53; Whitefish

Indexed keywords

CASPASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DICER; FERRITIN; HISTONE H2A; LET 7C; MESSENGER RNA; MICROCYSTIN LR; MICRORNA; MICRORNA 122; MICRORNA 16A; MICRORNA 21A; MICRORNA 34A; MICRORNA 9B; PROTEIN BAX; PROTEIN P53; RAS PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; CYANOBACTERIUM; FISH; GENE EXPRESSION; METABOLISM; RNA; TOXIN;

AGAR GEL ELECTROPHORESIS; ARTICLE; CELL CYCLE; CONTROLLED STUDY; COREGONUS LAVARETUS; DISSOCIATION; ENVIRONMENTAL STRESS; FATTY ACID METABOLISM; FISH; GENE EXPRESSION PROFILING; IN VIVO STUDY; LIVER TOXICITY; MELTING POINT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WHITEFISH;

ANIMALS; FISH PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIVER; MICROCYSTINS; MICRORNAS; SALMONIDAE; TIME FACTORS; WATER POLLUTANTS, CHEMICAL;

COREGONUS LAVARETUS; CYANOBACTERIA;

EID: 84864046897     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.07.001     Document Type: Article

References (70)

1. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
2. Ason B., Darnell D.K., Wittbrodt B., Berezikov E., Kloosterman W.P., Wittbrodt J., Antin P.B., Plasterk R.H. Differences in vertebrate microRNA expression. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:14385-14389.
3. Asslaber D., Piñón J.D., Seyfried I., Desch P., Stöcher M., Tinhofer I., Egle A., Merkel O., Greil R. microRNA-34a expression correlates with MDM2 SNP309 polymorphism and treatment-free survival in chronic lymphocytic leukemia. Blood 2010, 115:4191-4197.
4. Betel D., Wilson M., Gabow A., Marks D.S., Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Research 2008, 36:D149-D153.
5. Billam M., Mukhi S., Tang L., Gao W., Wang J. Toxic response indicators of microcystin-LR in F344 rats following a single-dose treatment. Toxicon 2008, 51:1068-1080.
6. Brzuzan P., Woźny M., Łuczyński M.K., Góra M. CYP1A gene expression in adipose fin of rainbow trout (Oncorhynchus mykiss Walbaum) exposed to benzo[a]pyrene. Environmental Biotechnology 2007, 3:20-24.
7. Brzuzan P., Woźny M., Ciesielski S., Łuczyński M.K., Góra M., Kuźmiński H., Dobosz S. Microcystin-LR induced apoptosis and mRNA expression of p53 and cdkn1a in liver of whitefish (Coregonus lavaretus L.). Toxicon 2009, 54:170-183.
8. Brzuzan P., Woźny M., Wolińska L., Piasecka A., Łuczyński M.K. MicroRNA expression in liver of whitefish (Coregonus lavaretus) exposed to microcystin-LR. Environmental Biotechnology 2010, 6:53-60.
9. Campos A., Vasconcelos V. Molecular mechanism of microcystin toxicity in animal cells. International Journal of Molecular Sciences 2010, 11:268-287.
10. Carmichael W.W. Cyanobacteria secondary metabolites - the cyanotoxins. Journal of Applied Bacteriology 1992, 72:445-459.
11. Chan J.A., Krichevsky A.M., Kosik K.S. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Research 2005, 65:6029-6033.
12. Chang T.C., Yu D., Lee Y.S., Wentzel E.A., Arking D.E., West K.M., Dang C.V., Thomas-Tikhonenko A., Mendell J.T. Widespread microRNA repression by Myc contributes to tumorigenesis. Nature Genetics 2008, 40:43-50.
13. Chen P.Y., Manninga H., Slanchev K., Chien M., Russo J.J., Ju J., Sheridan R., John B., Marks D.S., Gaidatzis D., Sander C., Zavolan M., Tuschl T. The developmental miRNA profiles of zebrafish as determined by small RNA cloning. Genes and Development 2005, 19:1288-1293.
14. Cimmino A., Calin G.A., Fabbri M., Iorio M.V., Ferracin M., Shimizu M., Wojcik S.E., Aqeilan R.I., Zupo S., Dono M., Rassenti L., Alder H., Volinia S., Liu C.G., Kipps T.J., Negrini M., Croce C.M. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:13944-13949.
15. Dietrich D., Hoeger S. Guidance values for microcystins in water and cyanobacterial supplement products (blue-green algal supplements): a reasonable or misguided approach?. Toxicology and Applied Pharmacology 2005, 203:273-289.
16. Ding W.X., Shen H.M., Ong C.N. Pivotal role of mitochondrial Ca(2+) in microcystin-induced mitochondrial permeability transition in rat hepatocytes. Biochemical and Biophysical Research Communications 2001, 285:1155-1161.
17. Feurstein D., Stemmer K., Kleinteich J., Speicher T., Dietrich D.R. Microcystin congener- and concentration-dependent induction of murine neuron apoptosis and neurite degeneration. Toxicological Sciences 2011, 124:424-431.
18. Fromme H., Köhler A., Krause R., Führling D. Occurrence of cyanobacterial toxins-microcystins and anatoxin-a-in Berlin water bodies with implications to human health and regulations. Environmental Toxicology 2000, 15:120-130.
19. Fu W.Y., Chen J.P., Wang X.M., Xu L.H. Altered expression of p53 Bcl-2 and Bax induced by microcystin-LR in vivo and in vitro. Toxicon 2005, 46:171-177.
20. Fujita S., Ito T., Mizutani T., Minoguchi S., Yamamichi N., Sakurai K., Iba H. miR-21 gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. Journal of Molecular Biology 2008, 378:492-504.
21. Gartel A.L., Ye X., Goufman E., Shianov P., Hay N., Najmabadi F., Tyner A.L. Myc represses the p21(WAF1/CIP1) promoter and interacts with Sp1/Sp3. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:4510-4515.
22. Gehringer M.M. Microcystin-LR and okadaic acid-induced cellular effects: a dualistic response. FEBS Letters 2004, 557:1-8.
23. Girard M., Jacquemin E., Munnich A., Lyonnet S., Henrion-Caude A. miR-122, a paradigm for the role of microRNAs in the liver. Journal of Hepatology 2008, 48:648-656.
24. Guzman R.E., Solter P.F., Runnegar M.T. Inhibition of nuclear protein phosphatase activity in mouse hepatocytes by the cyanobacterial toxin microcystin-LR. Toxicon 2003, 41:773-781.
25. He X., He L., Hannon G.J. The guardian's little helper: microRNAs in the p53 tumor suppressor network. Cancer Research 2007, 67:11099-11101.
26. Honkanen R.E., Zwiller J., Moore R.E., Daily S.L., Khatra B.S., Dukelow M., Boynton A.L. Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. Journal of Biological Chemistry 1990, 265:19401-19404.
27. Hudder A., Novak R.F. miRNAs: effectors of environmental influences on gene expression and disease. Toxicological Sciences 2008, 103:228-240.
28. Johnson S.M., Grosshans H., Shingara J., Byrom M., Jarvis R., Cheng A., Labourier E., Reinert K.L., Brown D., Slack F.J. RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-647.
29. Kazuń K., Siwicki A.K. Propiscin - a safe new anestetic for fish. Archives of Polish Fisheries 2001, 9:183-190.
30. Kortner T.M., Valen E.C., Kortner H., Marjara I.S., Krogdahl Å., Bakke A.M. Candidate reference genes for quantitative real-time PCR (qPCR) assays during development of a diet-related enteropathy in Atlantic salmon (Salmo salar L.) and the potential pitfalls of uncritical use of normalization software tools. Aquaculture 2011, 318:355-363.
31. Koscianska E., Baev V., Skreka K., Oikonomaki K., Rusinov V., Tabler M., Kalantidis K. Prediction and preliminary validation of oncogene regulation by miRNAs. BMC Molecular Biology 2007, 8:79.
32. Krützfeldt J., Rajewsky N., Braich R., Rajeev K.G., Tuschl T., Manoharan M., Stoffel M. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005, 438:685-689.
33. Le M.T.N., Teh C., Shyh-Chang N., Xie H., Zhou B., Korzh V., Lodish H.F., Lim B. MicroRNA-125b is a novel negative regulator of p53. Genes and Development 2009, 23:862-876.
34. Li H.H., Cai X., Shouse G.P., Piluso L.G., Liu X. A specific PP2A regulatory subunit B56γ, mediates DNA damage-induced dephosphorylation of p53 at Thr55. EMBO Journal 2007, 26:402-411.
35. Li Y., Sheng J., Sha J., Han X. The toxic effects of microcystin-LR on the reproductive system of male rats in vivo and in vitro. Reproductive Toxicology 2008, 26:239-245.
36. Li H., Xie P., Li G., Hao L., Xiong Q. In vivo study on the effects of microcystin extracts on the expression profiles of proto-oncogenes (c-fos, c-jun and c-myc) in liver, kidney and testis of male Wistar rats injected i.v. with toxins. Toxicon 2009, 53:169-175.
37. Liang Y., Ridzon D., Wong L., Chen C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 2007, 8:166.
38. Liu L., Cash T.P., Jones R.G., Keith B., Thompson C.B., Simon M.C. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Molecular Cell 2006, 21:521-531.
39. Liu M., Tee C., Zeng F., Sherry J.P., Dixon B., Bols N.C., Duncker B.P. Characterization of p53 expression in rainbow trout. Comparative Biochemistry and Physiology. Part C, Toxicology & Pharmacology 2011, 154:326-332.
40. Malbrouck C., Kestemont P. Effects of microcystins on fish. Environmental Toxicology and Chemistry 2006, 25:72-86.
41. Marsit C.J., Eddy K., Kelsey K.T. MicroRNA responses to cellular stress. Cancer Research 2006, 66:10843-10848.
42. Meister G., Tuschl T. Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431:343-349.
43. Mishra P.K., Tyagi N., Kundu S., Tyagi S.C. MicroRNAs are involved in homocysteine-induced cardiac remodeling. Cell Biochemistry and Biophysics 2009, 55:153-162.
44. Nong Q., Komatsu M., Izumo K., Indo H.P., Xu B., Aoyama K., Majima H.J., Horiuchi M., Morimoto K., Takeuchi T. Involvement of reactive oxygen species in Microcystin-LR-induced cytogenotoxicity. Free Radical Research 2007, 41:1326-1337.
45. Orino K., Lehman L., Tsuji Y., Ayaki H., Torti S.V., Torti F.M. Ferritin and the response to oxidative stress. Biochemical Journal 2001, 357:241-247.
46. Østbye T.K., Kjær M.A., Rørå A.M.B., Torstensen B., Ruyter B. High n-3 HUFA levels in the diet of Atlantic salmon affect muscle and mitochondrial membrane lipids and their susceptibility to oxidative stress. Aquaculture Nutrition 2011, 17:177-190.
47. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 2001, 29:e45.
48. 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 Research 2002, 30:e36.
49. Pfaffl M.W., Tichopad A., Prgomet C., Neuvians T.P. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - excel-based tool using pair-wise correlations. Biotechnology Letters 2004, 26:509-515.
50. Pichardo S., Jos A., Zurita J.L., Salguero M., Cameán A.M., Repetto G. Acute and subacute toxic effects produced by microcystin-YR on the fish cell lines RTG-2 and PLHC-1. Toxicology In Vitro 2007, 21:1460-1467.
51. Pillai R.S., Bhattacharyya S.N., Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms?. Trends in Cell Biology 2007, 17:118-126.
52. Pluquet O., Hainaut P. Genotoxic and non-genotoxic pathways of p53 induction. Cancer Letters 2001, 174:1-15.
53. Rau E.M., Billiard S.M., Di Giulio R.T. Lack of p53 induction in fish cells by model chemotherapeutics. Oncogene 2006, 25:2004-2010.
54. Qiu T., Xie P., Liu Y., Li G., Xiong Q., Hao L., Li H. The profound effects of microcystin on cardiac antioxidant enzymes, mitochondrial function and cardiac toxicity in rat. Toxicology 2009, 257:86-94.
55. Ramachandra R.K., Salem M., Gahr S., Rexroad C.E., Yao J. Cloning and characterization of microRNAs from rainbow trout (Oncorhynchus mykiss): their expression during early embryonic development. BMC Developmental Biology 2008, 8:41.
56. Rotkrua P., Akiyama Y., Hashimoto Y., Otsubo T., Yuasa Y. MiR-9 downregulates CDX2 expression in gastric cancer cells. International Journal of Cancer 2011, 129:2611-2620.
57. Salem M., Xiao C., Womack J., Rexroad C.E., Yao J. MicroRNA repertoire for functional genome research in rainbow trout (Oncorhynchus mykiss). Marine Biotechnology 2010, 12:410-429.
58. Sedan D., Andrinolo D., Telese L., Giannuzzi L., de Alaniz M.J.T., Marra C.A. Alteration and recovery of the antioxidant system induced by sub-chronic exposure to microcystin-LR in mice: its relation to liver lipid composition. Toxicon 2010, 55:333-342.
59. Sunkar R., Kapoor A., Zhu J.K. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 2006, 18:2051-2065.
60. Tarasov V., Jung P., Verdoodt B., Lodygin D., Epanchintsev A., Menssen A., Meister G., Hermeking H. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007, 6:1586-1593.
61. van Apeldoorn M.E., van Egmond H.P., Speijers G.J.A., Bakker G.J.I. Toxins of cyanobacteria. Molecular Nutrition & Food Research 2007, 51:7-60.
62. Vousden K.H., Lu X. Live or let die: the cell's response to p53. Nature Reviews Cancer 2002, 2:594-604.
63. Wang M., Chan L.L., Si M., Hong H., Wang D. Proteomic analysis of hepatic tissue of zebrafish (Danio rerio) experimentally exposed to chronic Microcystin-LR. Toxicological Sciences 2010, 113:60-69.
64. Wei Y., Weng D., Li F., Zou X., Young D.O., Ji J., Shen P. Involvement of JNK regulation in oxidative stress-mediated murine liver injury by microcystin-LR. Apoptosis 2008, 13:1031-1042.
65. WHO Guidelines for Drinking-Water Quality, vol. 1. Recommendations 2004, World Health Organization Publishing, Geneva, Switzerland. 3rd edition.
66. Woźny, M., Brzuzan, P., Wolińska, L., Góra, M., Łuczyński, M.K., 2012. Differential gene expression in rainbow trout (Oncorhynchus mykiss) liver and ovary after exposure to zearalenone. Comparative Biochemistry and Physiology. Part C, Toxicology & Pharmacology, in press. doi:10.1016/j.cbpc.2012.05.005.
67. Xu B., Huang Y. Histone H2a mRNA interacts with Lin28 and contains a Lin28-dependent posttranscriptional regulatory element. Nucleic Acids Research 2009, 37:4256-4263.
68. Žegura B., Filipič M., Šuput D., Lah T., Sedmak B. In vitro genotoxicity of microcystin-RR on primary cultured rat hepatocytes and Hep G2 cell line detected by Comet assay. Radiology and Oncology 2002, 36:159-161.
69. Žegura B., Zajc I., Lah T.T., Filipič M. Patterns of microcystin-LR induced alteration of the expression of genes involved in response to DNA damage and apoptosis. Toxicon 2008, 51:615-623.
70. Zhao Y., Xiong Q., Xie P. Analysis of microRNA expression in embryonic developmental toxicity induced by MC-RR. PLoS ONE 2011, 6:e22676.