Integrated mRNA and micro RNA profiling reveals epigenetic mechanism of differential sensitivity of Jurkat T cells to AgNPs and Ag ions

Toxicology Letters

Volumn 229, Issue 1, 2014, Pages 311-318

  Eom, Hyun Jeong ^a   Chatterjee, Nivedita ^a   Lee, Jeongsoo ^b   Choi, Jinhee ^a  

^a University of Seoul   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Epigenetic mechanism; Integrated analysis; MiR 219 5p; MiR 654 3p; Silver nanoparticles

Indexed keywords

ENDONUCLEASE G; ENDONUCLEASE G LIKE 1; MESSENGER RNA; METALLOTHIONEIN; METALLOTHIONEIN 1A; METALLOTHIONEIN 1F; METALLOTHIONEIN 1H; METALLOTHIONEIN II; MICRORNA; MICRORNA 219 5P; MICRORNA 302; MICRORNA 33; MICRORNA 504; MICRORNA 654 3P; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN; PROTEIN P53; SILVER; SILVER NANOPARTICLE; TRIBBLES HOMOLOG 3 PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; JURKAT CELL LINE; MESSENGER RNA MICROARRAY; MICROARRAY ANALYSIS; MICRORNA MICROARRAY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; UPREGULATION;

EPIGENETIC MECHANISM; INTEGRATED ANALYSIS; MIR-219-5P; MIR-654-3P; SILVER NANOPARTICLES;

APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; EPIGENESIS, GENETIC; GENE EXPRESSION; HUMANS; JURKAT CELLS; METAL NANOPARTICLES; MICROARRAY ANALYSIS; MICRORNAS; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SILVER;

EID: 84903828714     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.05.019     Document Type: Article

References (73)

1. Ambs S., Prueitt R.L., Yi M., Hudson R.S., Howe T.M., Petrocca F., Wallace T.A., Liu C.G., Volinia S., Calin G.A., Yfantis H.G., Stephens R.M., Croce C.M. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res. 2008, 68:6162-6170.
2. An J., Pan Y., Yan Z., Li W., Cui J., Yuan J., Tian L., Xing R., Lu Y. MiR-23a in amplified 19p13.13 loci targets metallothionein 2A and promotes growth in gastric cancer cells. J. Cell. Biochem. 2013, 114:2160-2169.
3. Avissar-Whiting M., Veiga K.R., Uhl K.M., Maccani M.A., Gagne L.A., Moen E.L., Marsit C.J. Bisphenol A exposure leads to specific microRNA alterations in placental cells. Reprod. Toxicol. 2010, 29:401-406.
4. Barroso-delJesus A., Lucena-Aguilar G., Sanchez L., Ligero G., Gutierrez-Aranda I., Menendez P. The Nodal inhibitor Lefty is negatively modulated by the microRNA miR-302 in human embryonic stem cells. FASEB J. 2011, 25:1497-1508.
5. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
6. Benn T.M., Westerhoff P. Nanoparticle silver released into water from commercially available sock fabrics. Environ. Sci. Technol. 2008, 42:4133-4139.
7. Bilberg K., Hovgaard M.B., Besenbacher F., Baatrup E. In vivo toxicity of silver nanoparticles and silver ions in zebrafish (Danio rerio). J. Toxicol. 2012, 2012:293784.
8. Bollati V., Marinelli B., Apostoli P., Bonzini M., Nordio F., Hoxha M., Pegoraro V., Motta V., Tarantini L., Cantone L., Schwartz J., Bertazzi P.A., Baccarelli A. Exposure to metal-rich particulate matter modifies the expression of candidate microRNAs in peripheral blood leukocytes. Environ. Health Perspect. 2010, 18:763-768.
9. Chan M.C., Hilyard A.C., Wu C., Davis B.N., Hill N.S., Lal A., Lieberman J., Lagna G., Hata A. Molecular basis for antagonism between PDGF and the TGFbeta family of signalling pathways by control of miR-24 expression. EMBO J. 2010, 29:559-573.
10. Cirera-Salinas D., Pauta M., Allen R.M., Salerno A.G., Ramírez C.M., Chamorro-Jorganes A., Wanschel A.C., Lasuncion M.A., Morales-Ruiz M., Suarez Y., Baldan Á., Esplugues E., Fernández-Hernando C. Mir-33 regulates cell proliferation and cell cycle progression. Cell Cycle 2012, 11:922-933.
11. Ding J.X., Kato S., Du K.Y. PI3K activates negative and positive signals to regulate TRB3 expression in hepatic cells. Exp. Cell Res. 2008, 314:1566-1574.
12. Elyakim E., Sitbon E., Faerman A., Tabak S., Montia E., Belanis L., Dov A., Marcusson E.G., Bennett C.F., Chajut A., Cohen D., Yerushalmi N. hsa-miR-191 is a candidate oncogene target for hepatocellular carcinoma therapy. Cancer Res. 2010, 70:8077-8087.
13. Enright A.J., John B., Gaul U., Tuschl T., Sander C., Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 2003, 5:R1.
14. Eom H.J., Ahn J.M., Kim Y., Choi J. Hypoxia inducible factor-1 (HIF-1)-flavin containing monooxygenase-2 (FMO-2) signaling acts in silver nanoparticles and silver ion toxicity in the nematode, Caenorhabditis elegans. Toxicol. Appl. Pharmacol. 2013, 270:106-113.
15. Eom H.J., Choi J. p38 MAPK activation, DNA damage, cell cycle arrest and apoptosis as mechanisms of toxicity of silver nanoparticles in Jurkat T cells. Environ. Sci. Technol. 2010, 44:8337-8342.
16. Fabrega J., Fawcett S.R., Renshaw J.C., Lead J.R. Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ. Sci. Technol. 2009, 43:7285-7290.
17. Foldbjerg R., Dang D.A., Autrup H. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch. Toxicol. 2011, 85:743-750.
18. Foldbjerg R., Irving E.S., Hayashi Y., Sutherland D.S., Thorsen K., Autrup H., Beer C. Global gene expression profiling of human lung epithelial cells after exposure to nanosilver. Toxicol. Sci. 2012, 130:145-157.
19. Foldbjerg R., Olesen P., Hougaard M., Dang D.A., Hoffmann H.J., Autrup H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicol. Lett. 2009, 190:156-162.
20. Fukushima T., Hamada Y., Yamada H., Horii I. Changes of micro-RNA expression in rat liver treated by acetaminophen or carbon tetrachloride - regulating role of micro-RNA for RNA expression. J. Toxicol. Sci. 2007, 32:401-409.
21. Gagné F., André C., Skirrow R., Gélinas M., Auclair J., van Aggelen G., Turcotte P., Gagnon C. Toxicity of silver nanoparticles to rainbow trout: a toxicogenomic approach. Chemosphere 2012, 89:615-622.
22. Gocek E., Wang X., Liu X., Liu C.G., Studzinski G.P. MicroRNA-32 upregulation by 1,25-dihydroxyvitamin D3 in human myeloid leukemia cells leads to Bim targeting and inhibition of AraC-induced apoptosis. Cancer Res. 2011, 71:6230-6239.
23. Griffiths-Jones S., Grocock R.J., van Dongen S., Bateman A., Enright A.J. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 2006, 34(Database issue):D140-D144.
24. Guo X.B., Jing C.Q., Li L.P., Zhang L., Shi Y.L., Wang J.S., Liu J.L., Li C.S. Down-regulation of miR-622 in gastric cancer promotes cellular invasion and tumor metastasis by targeting ING1 gene. World J. Gastroenterol. 2011, 17:1895-1902.
25. Hafner M., Landthaler M., Burger L., Khorshid M., Hausser J., Berninger P., Rothballer A., Ascano M., Jungkamp A.C., Munschauer M., Ulrich A., Wardle G.S., Dewell S., Zavolan M., Tuschl T. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141:129-141.
26. Han Z., Yang Q., Liu B., Wu J., Li Y., Yang C., Jiang Y. MicroRNA-622 functions as a tumor suppressor by targeting K-Ras and enhancing the anticarcinogenic effect of resveratrol. Carcinogenesis 2012, 33:131-139.
27. Hu W., Chan C.S., Wu R., Zhang C., Sun Y., Song J.S., Tang L.H., Levine A.J., Feng Z. Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol. Cell 2010, 38:689-699.
28. Hua F., Mu R., Liu J., Xue J., Wang Z., Lin H., Yang H., Chen X., Hu Z. TRB3 interacts with SMAD3 promoting tumor cell migration and invasion. J. Cell Sci. 2011, 124:3235-3246.
29. Huang W., Li M.D. Differential allelic expression of dopamine D1 receptor gene (DRD1) is modulated by microRNA miR-504. Biol. Psychiatry. 2009, 65:702-705.
30. Huang N., Lin J., Ruan J., Su N., Qing R., Liu F., He B., Lv C., Zheng D., Luo R. MiR-219-5p inhibits hepatocellular carcinoma cell proliferation by targeting glypican-3. FEBS Lett. 2012, 586:884-891.
31. Hudder A., Novak R.F. miRNAs: effectors of environmental influences on gene expression and disease. Toxicol. Sci. 2008, 103:228-240.
32. Ji Q., Hao X., Meng Y., Zhang M., Desano J., Fan D., Xu L. Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer 2008, 8:266.
33. Izzotti A., Calin G.A., Arrigo P., Steele V.E., Croce C.M., De Flora S. Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J. 2009, 23:806-812.
34. Kaveh R., Li Y.S., Ranjbar S., Tehrani R., Brueck C.L., Van Aken B. Changes in Arabidopsis thaliana Gene expression in response to silver nanoparticles and silver ions. Environ. Sci. Technol. 2013, 47:10637-10644.
35. Kawata K., Osawa M., Okabe S. In vitro toxicity of silver nanoparticles at noncytotoxic doses to HepG2 human hepatoma cells. Environ. Sci. Technol. 2009, 43:6046-6451.
36. Kim J.S., Kuk E., Yu K.N., Kim J.H., Park S.J., Lee H.J., Kim S.H., Park Y.K., Park Y.H., Hwang C.Y., Kim Y.K., Lee Y.S., Jeong D.H., Cho M.H. Antimicrobial effects of silver nanoparticles. Nanomedicine 2007, 3:95-101.
37. Kiss-Toth E., Bagstaff S.M., Sung H.Y., Jozsa V., Dempsey C., Caunt J.C., Oxley K.M., Wyllie D.H., Polgar T., Harte M., O'neill L.A., Qwarnstrom E.E., Dower S.K. Human tribbles, a protein family controlling mitogen-activated protein kinase cascades. J. Biol. Chem. 2004, 279:42703-42708.
38. Kloosterman W.P., Plasterk R.H. The diverse functions of microRNAs in animal development and disease. Dev. Cell 2006, 11:441-450.
39. Kocerha J., Faghihi M.A., Lopez-Toledano M.A., Huang J., Ramsey A.J., Caron M.G., Sales N., Willoughby D., Elmen J., Hansen H.F., Orum H., Kauppinen S., Kenny P.J., Wahlestedt C. MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc. Natl. Acad. Sci. USA. 2009, 106:3507-3512.
40. Lee N.S., Kim J.S., Cho W.J., Lee M.R., Steiner R., Gompers A., Ling D., Zhang J., Strom P., Behlke M., Moon S.H., Salvaterra P.M., Jove R., Kim K.S. miR-302b maintains "stemness" of human embryonal carcinoma cells by post-transcriptional regulation of Cyclin D2 expression. Biochem. Biophys. Res. Commun. 2008, 377:434-440.
41. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
42. Li S.S., Yu S.L., Kao L.P., Tsai Z.Y., Singh S., Chen B.Z., Ho B.C., Liu Y.H., Yang P.C. Target identification of microRNAs expressed highly in human embryonic stem cells. J. Cell Biochem. 2009, 106:1020-1030.
43. Lin S.L., Chang D.C., Ying S.Y., Leu D., Wu D.T. MicroRNA miR-302 inhibits the tumorigenecity of human pluripotent stem cells by coordinate suppression of the CDK2 and CDK4/6 cell cycle pathways. Cancer Res. 2010, 70:9473-9482.
44. Luoma S.N. Silver Nanotechnologies and the Environment: Old Problems or New Challenges? 2008, Woodrow Wilson International Center for Scholars, Washington, DC.
45. Miura N., Shinohara Y. Cytotoxic effect and apoptosis induction by silver nanoparticles in HeLa cells. Biochem. Biophys. Res. Commun. 2009, 390:733-737.
46. Murray M.J., Halsall D.J., Hook C.E., Williams D.M., Nicholson J.C., Coleman N. Identification of microRNAs from the miR-371-373 and miR-302 clusters as potential serum biomarkers of malignant germ cell tumors. Am. J. Clin. Pathol. 2011, 135:119-125.
47. Najafi-Shoushtari S.H., Kristo F., Li Y., Shioda T., Cohen D.E., Gerszten R.E., Näär A.M. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 2010, 328:1566-1569.
48. Pal S., Tak Y.K., Song J.M. Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle?. A study of the gram-negative bacterium Escherichia coli. Appl. Environ. Microb. 2007, 73:1712-1720.
49. Papadopoulos G.L., Alexiou P., Maragkakis M., Reczko M., Hatzigeorgiou A.G. DIANA-mirPath: integrating human and mouse microRNAs in pathways. Bioinformatics 2009, 25:1991-1993.
50. Peeters A., Fraisl P., van den Berg S., Ver Loren van Themaat E., Van Kampen A., Rider M.H., Takemori H., van Dijk K.W., Van Veldhoven P.P., Carmeliet P., Baes M. Carbohydrate metabolism is perturbed in peroxisome-deficient hepatocytes due to mitochondrial dysfunction, AMP-activated protein kinase (AMPK) activation, and peroxisome proliferator-activated receptor γ coactivator 1α (PGC-1α) suppression. J. Biol. Chem. 2011, 286:42162-42179.
51. Pichiorri F., Suh S.S., Ladetto M., Kuehl M., Palumbo T., Drandi D., Taccioli C., Zanesi N., Alder H., Hagan J.P., Munker R., Volinia S., Boccadoro M., Garzon R., Palumbo A., Aqeilan R.I., Croce C.M. MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc. Natl. Acad. Sci. USA. 2008, 105:12885-12890.
52. Poynton H.C., Lazorchak J.M., Impellitteri C.A., Blalock B.J., Rogers K., Allen H.J., Loguinov A., Heckman J.L., Govindasmawy S. Toxicogenomic responses of nanotoxicity in Daphnia magna exposed to silver nitrate and coated silver nanoparticles. Environ. Sci. Technol. 2012, 46:6288-6296.
53. Prabhu S., Poulose E. Silver nanoparticles: mechanism of antimicrobial action, synthesis, medical applications, and toxicity effects. Int. Nano Lett. 2012, 2:32.
54. Rademakers R., Eriksen J.L., Baker M., Robinson T., Ahmed Z., Lincoln S.J., Finch N., Rutherford N.J., Crook R.J., Josephs K.A., Boeve B.F., Knopman D.S., Petersen R.C., Parisi J.E., Caselli R.J., Wszolek Z.K., Uitti R.J., Feldman H., Hutton M.L., Mackenzie I.R., Graff-Radford N.R., Dickson D.W. Common variation in the miR-659 binding-site of GRN is a major risk factor for TDP43-positive frontotemporal dementia. Hum. Mol. Genet. 2008, 17:3631-3642.
55. Rayner K.J., Suárez Y., Dávalos A., Parathath S., Fitzgerald M.L., Tamehiro N., Fisher E.A., Moore K.J., Fernández-Hernando C. MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010, 328:1570-1573.
56. Roh J.Y., Sim S.J., Yi J., Park K., Chung K.H., Ryu D.Y., Choi J. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ. Sci. Technol. 2009, 43:3933-3940.
57. Rzymski T., Paantjens A., Bod J., Harris A.L. Multiple pathways are involved in the anoxia response of SKIP3 including HuR-regulated RNA stability, NF-kappaB and ATF4. Oncogene 2008, 27:4532-4543.
58. Sarachana T., Zhou R., Chen G., Manji H.K., Hu V.W. Investigation of post-transcriptional gene regulatory networks associated with autism spectrum disorders by microRNA expression profiling of lymphoblastoid cell lines. Genome Med. 2010, 2:23.
59. Scheel A.H., Beyer U., Agami R., Dobbelstein M. Immunofluorescence-based screening identifies germ cell associated microRNA 302 as an antagonist to p63 expression. Cell Cycle 2009, 8:1426-1432.
60. Shahverdi A.R., Fakhimi A., Shahverdi H.R., Minaian S. Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomedicine 2007, 3:168-171.
61. Thomas M., Lange-Grünweller K., Weirauch U., Gutsch D., Aigner A., Grünweller A., Hartmann R.K. The proto-oncogene Pim-1 is a target of miR-33a. Oncogene 2012, 31:918-928.
62. Tsai Z.Y., Singh S., Yu S.L., Kao L.P., Chen B.Z., Ho B.C., Yang P.C., Li S.S. Identification of microRNAs regulated by activin A in human embryonic stem cells. J. Cell Biochem. 2010, 109:93-102.
63. Tsai Z.Y., Chou C.H., Lu C.Y., Singh S., Yu S.L., Li S.S. Proteomic comparison of human embryonic stem cells with their differentiated fibroblasts: Identification of 206 genes targeted by hES cell-specific microRNAs. Kaohsiung J. Med. Sci. 2011, 27:299-306.
64. Völker C., Oetken M., Oehlmann J. The biological effects and possible modes of action of nanosilver. Rev. Environ. Contam. Toxicol. 2013, 223:81-106.
65. Wang L., Pal S., Sif S. Protein arginine methyltransferase 5 suppresses the transcription of the RB family of tumor suppressors in leukemia and lymphoma cells. Mol. Cell Biol. 2008, 28:6262-6277.
66. Wu M., Xu L.G., Zhai Z.H., Shu H.B. SINK is a p65-interacting negative regulator of NF-kappa B-dependent transcription. J. Biol. Chem. 2003, 278:27072-27079.
67. Wu S., Huang S., Ding J., Zhao Y., Liang L., Liu T., Zhan R., He X. Multiple microRNAs modulate p21Cip1/Waf1 expression by directly targeting its 3' untranslated region. Oncogene 2010, 29:2302-2308.
68. Wu W., Yang J., Feng X., Wang H., Ye S., Yang P., Tan W., Wei G., Zhou Y. MicroRNA-32 (miR-32) regulates phosphatase and tensin homologue (PTEN) expression and promotes growth, migration, and invasion in colorectal carcinoma cells. Mol. Cancer 2013, 12:30.
69. Xiong J., Yu D., Wei N., Fu H., Cai T., Huang Y., Wu C., Zheng X., Du Q., Lin D., Liang Z. An estrogen receptor alpha suppressor, microRNA-22, is downregulated in estrogen receptor alpha-positive human breast cancer cell lines and clinical samples. FEBS J. 2010, 277:1684-1694.
70. Xu L., Li X., Takemura T., Hanagata N., Wu G., Chou L.L. Genotoxicity and molecular response of silver nanoparticle (NP)-based hydrogel. J. Nanobiotechnol. 2012, 10:16.
71. Yang X., Gondikas A.P., Marinakos S.M., Auffan M., Liu J., Hsu-Kim H., Meyer J.N. Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ. Sci. Technol. 2012, 46:1119-1127.
72. Yauk C.L., Jackson K., Malowany M., Williams A. Lack of change in microRNA expression in adult mouse liver following treatment with benzo(a)pyrene despite robust mRNA transcriptional response. Mutat. Res. 2011, 722:131-139.
73. Ye W., Lv Q., Wong C.K., Hu S., Fu C., Hua Z., Cai G., Li G., Yang B.B., Zhang Y. The effect of central loops in miRNA:MRE duplexes on the efficiency of miRNA-mediated gene regulation. PLoS One 2008, 3(3):e1719.