Role of microRNAs and DNA methyltransferases in transmitting induced genomic instability between cell generations

Frontiers in Public Health

Volumn 2, Issue SEP, 2014, Pages

  Huumonen, Katriina ^a   Korkalainen, Merja ^b   Viluksela, Matti ^a,b   Lahtinen, Tapani ^c   Naarala, Jonne ^a   Juutilainen, Jukka ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Cadmium; DNA methyltransferases; Epigenetics; Induced genomic instability; MicroRNA; TCDD

Indexed keywords

EID: 84969517408     PISSN: None     EISSN: 22962565     Source Type: Journal    
DOI: 10.3389/fpubh.2014.00139     Document Type: Article

References (78)

1. Kadhim MA,Macdonald DA, Goodhead DT, Lorimore SA,Marsden SJ,Wright EG. Transmission of chromosomal instability after plutonium alpha-particle irradiation. Nature (1992) 355(6362):738-40. doi:10.1038/355738a0
2. Wright EG. Radiation-induced genomic instability in haemopoietic cells. Int J Radiat Biol (1998) 74(6):681-7. doi:10.1080/095530098140943
3. MorganWF. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res (2003) 159(5):567-80. doi:10.1667/0033-7587(2003)159[0581:NADEOE]2. 0.CO;2
4. Baverstock K, Ronkko M. Epigenetic regulation of the mammalian cell. PLoS One (2008) 3(6):e2290. doi:10.1371/journal.pone.0002290
5. Aypar U, Morgan WF, Baulch JE. Radiation-induced genomic instability: are epigenetic mechanisms the missing link?. Int J Radiat Biol (2011) 87(2):179-91. doi:10.3109/09553002.2010.522686
6. Ilnytskyy Y, Kovalchuk O. Non-targeted radiation effects-an epigenetic connec-tion. Mutat Res (2011) 714(1-2):113-25. doi:10.1016/j.mrfmmm.2011.06.014
7. Baverstock K. Radiation-induced genomic instability: a paradigm-breaking phe-nomenon and its relevance to environmentally induced cancer.Mutat Res (2000) 454(1-2):89-109. doi:10.1016/S0027-5107(00)00100-7
8. Korkalainen M, Huumonen K, Naarala J, Viluksela M, Juutilainen J. Dioxin induces genomic instability in mouse embryonic fibroblasts. PLoS One (2012) 7(5):e37895. doi:10.1371/journal.pone.0037895
9. Coen N, Mothersill C, Kadhim M, Wright EG. Heavy metals of relevance to human health induce genomic instability. J Pathol (2001) 195(3):293-9. doi:10.1002/path.950
10. Phillipson RP, Tobi SE, Morris JA, McMillan TJ. UV-A induces persistent genomic instability in human keratinocytes through an oxidative stress mech-anism. Free Radic Biol Med (2002) 32(5):474-80. doi:10.1016/S0891-5849(01) 00829-2
11. Limoli CL, Kaplan MI, Phillips JW, Adair GM,MorganWF. Differential induc-tion of chromosomal instability by DNA strand-breaking agents. Cancer Res (1997) 57(18):4048-56.
12. Glen CD, Dubrova YE. Exposure to anticancer drugs can result in trans-generational genomic instability in mice. Proc Natl Acad Sci U S A (2012) 109(8):2984-8. doi:10.1073/pnas.1119396109
13. Dubrova YE, HickenbothamP,Glen CD,Monger K,WongHP, Barber RC. Pater-nal exposure to ethylnitrosourea results in transgenerational genomic instability in mice. Environ Mol Mutagen (2008) 49(4):308-11. doi:10.1002/em.20385
14. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature (2001) 411(6835):366-74. doi:10.1038/35077232
15. Cassidy LD, Venkitaraman AR. Genome instability mechanisms and the struc-ture of cancer genomes. Curr Opin Genet Dev (2012) 22(1):10-3. doi:10.1016/ j.gde.2012.02.003
16. Sieber OM, Heinimann K, Tomlinson IP. Genomic instability -the engine of tumorigenesis?. Nat Rev Cancer (2003) 3(9):701-8. doi:10.1038/nrc1170
17. Loeb LA. A mutator phenotype in cancer. Cancer Res (2001) 61(8):3230-9.
18. Tamminga J, Kovalchuk O. Role of DNA damage and epigenetic DNA methyla-tion changes in radiation-induced genomic instability and bystander effects in germline in vivo. Curr Mol Pharmacol (2011) 4(2):115-25. doi:10.2174/1874-470211104020115
19. Filkowski JN, Ilnytskyy Y, Tamminga J, Koturbash I, Golubov A, Bagnyukova T, et al. Hypomethylation and genome instability in the germline of exposed parents and their progeny is associated with altered miRNA expression. Car-cinogenesis (2010) 31(6):1110-5. doi:10.1093/carcin/bgp300
20. Kovalchuk O, Baulch JE. Epigenetic changes and nontargeted radiation effects -is there a link?. Environ MolMutagen (2008) 49(1):16-25. doi:10.1002/em.20361
21. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell (2004) 116(2):281-97. doi:10.1016/S0092-8674(04)00045-5
22. Wang Z, Yao H, Lin S, Zhu X, Shen Z, Lu G, et al. Transcriptional and epi-genetic regulation of human microRNAs. Cancer Lett (2013) 331(1):1-10. doi:10.1016/j.canlet.2012.12.006
23. Mendell JT. MicroRNAs: critical regulators of development, cellular physiology and malignancy. Cell Cycle (2005) 4(9):1179-84. doi:10.4161/cc.4.9.2032
24. Ambros V. The functions of animal microRNAs. Nature (2004) 431(7006): 350-5. doi:10.1038/nature02871
25. Kato M, Slack FJ. microRNAs: small molecules with big roles -C. elegans to human cancer. Biol Cell (2008) 100(2):71-81. doi:10.1042/BC20070078
26. JanssonMD, Lund AH.MicroRNA and cancer.Mol Oncol (2012) 6(6):590-610. doi:10.1016/j.molonc.2012.09.006
27. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell (2012) 148(6):1172-87. doi:10.1016/j.cell.2012.02.005
28. Parpart S,Wang XW.microRNA regulation and its consequences in cancer. Curr Pathobiol Rep (2013) 1(1):71-9. doi:10.1007/s40139-012-0002-7
29. Kiani J, Grandjean V, Liebers R, Tuorto F, Ghanbarian H, Lyko F, et al. RNA-mediated epigenetic heredity requires the cytosine methyltransferase Dnmt2. PLoS Genet (2013) 9(5):e1003498. doi:10.1371/journal.pgen.1003498
30. Sato F, Tsuchiya S, Meltzer SJ, Shimizu K. MicroRNAs and epigenetics. FEBS J (2011) 278(10):1598-609. doi:10.1111/j.1742-4658.2011.08089.x
31. Lim JP, Brunet A. Bridging the transgenerational gap with epigenetic memory. Trends Genet (2013) 29(3):176-86. doi:10.1016/j.tig.2012.12.008
32. Skinner MK, Haque CG, Nilsson E, Bhandari R, McCarrey JR. Environ-mentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line. PLoS One (2013) 8(7):e66318. doi:10.1371/journal.pone.0066318
33. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet (2003) 33(Suppl):245-54. doi:10.1038/ng1089
34. Kulis M, Esteller M. DNA methylation and cancer. Adv Genet (2010) 70:27-56. doi:10.1016/B978-0-12-380866-0.60002-2
35. Koturbash I, Pogribny I, Kovalchuk O. Stable loss of global DNA methyla-tion in the radiation-target tissue -a possible mechanism contributing to radiation carcinogenesis?. Biochem Biophys Res Commun (2005) 337(2):526-33. doi:10.1016/j.bbrc.2005.09.084
36. Bergman Y, Cedar H. DNA methylation dynamics in health and disease. Nat Struct Mol Biol (2013) 20(3):274-81. doi:10.1038/nsmb1013-1236a
37. Suva ML, Riggi N, Bernstein BE. Epigenetic reprogramming in cancer. Science (2013) 339(6127):1567-70. doi:10.1126/science.1230184
38. Friso S, Udali S, Guarini P, Pellegrini C, Pattini P,Moruzzi S, et al. Global DNA hypomethylation in peripheral blood mononuclear cells as a biomarker of can-cer risk. Cancer Epidemiol Biomarkers Prev (2013) 22(3):348-55. doi:10.1158/ 1055-9965.EPI-12-0859
39. Torano EG, Petrus S, Fernandez AF, Fraga MF. Global DNA hypomethylation in cancer: review of validated methods and clinical significance. Clin Chem Lab Med (2012) 50(10):1733-42. doi:10.1515/cclm-2011-0902
40. Rugo RE, Mutamba JT, Mohan KN, Yee T, Chaillet JR, Greenberger JS, et al. Methyltransferases mediate cell memory of a genotoxic insult. Oncogene (2011) 30(6):751-6. doi:10.1038/onc.2010.480
41. Armstrong CA, Jones GD, Anderson R, Iyer P, Narayanan D, Sandhu J, et al. DNMTs are required for delayed genome instability caused by radiation. Epige-netics (2012) 7(8):892-902. doi:10.4161/epi.21094
42. Khoddami V, Cairns BR. Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol (2013) 31(5):458-64. doi:10.1038/nbt.2566
43. Hernandez LG, van Steeg H, Luijten M, van Benthem J. Mechanisms of non-genotoxic carcinogens and importance of a weight of evidence approach.Mutat Res (2009) 682(2-3):94-109. doi:10.1016/j.mrrev.2009.07.002
44. Katic J,Cemeli E,BaumgartnerA,Laubenthal J,Bassano I, Stolevik SB, et al. Eval-uation of the genotoxicity of 10 selected dietary/environmental compoundswith the in vitromicronucleus cytokinesis-block assay in an interlaboratory compar-ison. Food Chem Toxicol (2010) 48(10):2612-23. doi:10.1016/j.fct.2010.06.030
45. Huumonen K, Korkalainen M, Boman E, Heikkilä J, Höytö A, Lahtinen T, et al. Dose-and time-dependent changes ofmicronucleus frequency and gene expres-sion in the progeny of irradiated cells: two components in radiation-induced genomic instability?. Mutat Res Fundam Mol Mech Mutagen (2014) 765:32-9. doi:10.1026/j.mrfmmm.2014.04.010
46. Falt S, Holmberg K, Lambert B, Wennborg A. Long-term global gene expression patterns in irradiated human lymphocytes. Carcinogenesis (2003) 24(11):1837-45. doi:10.1093/carcin/bgg134
47. Huumonen K, Immonen HK, Baverstock K,HiltunenM, KorkalainenM, Lahti-nen T, et al. Radiation-induced genomic instability in Caenorhabditis elegans. Mutat Res (2012) 748(1-2):36-41. doi:10.1016/j.mrgentox.2012.06.010
48. Reznikoff CA, Brankow DW, Heidelberger C. Establishment and characteriza-tion of a cloned line of C3H mouse embryo cells sensitive to postconfluence inhibition of division. Cancer Res (1973) 33(12):3231-8.
49. Liu SG, Qin XG, Zhao BS, Qi B, Yao WJ, Wang TY, et al. Differential expres-sion of miRNAs in esophageal cancer tissue. Oncol Lett (2013) 5(5):1639-42. doi:10.3892/ol.2013.1251
50. Sakurai K, Furukawa C, Haraguchi T, Inada K, Shiogama K, Tagawa T, et al. MicroRNAs miR-199a-5p and -3p target the Brm subunit of SWI/SNF to gen-erate a double-negative feedback loop in a variety of human cancers. Cancer Res (2011) 71(5):1680-9. doi:10.1158/0008-5472.CAN-10-2345
51. Yang L, Li N, Wang H, Jia X, Wang X, Luo J. Altered microRNA expression in cisplatin-resistant ovarian cancer cells and upregulation of miR-130a asso-ciated with MDR1/P-glycoprotein-mediated drug resistance. Oncol Rep (2012) 28(2):592-600. doi:10.3892/or.2012.1823
52. Santarpia L,Calin GA,AdamL,Ye L, Fusco A,Giunti S, et al. AmiRNA signature associated with human metastatic medullary thyroid carcinoma. Endocr Relat Cancer (2013) 20(6):809-23. doi:10.1530/ERC-13-0357
53. Walter BA,ValeraVA,Pinto PA,MerinoMJ.ComprehensivemicroRNAprofiling of prostate cancer. J Cancer (2013) 4(5):350-7. doi:10.7150/jca.6394
54. Schmitt MJ, Margue C, Behrmann I, Kreis S. MiRNA-29: a microRNA family with tumor-suppressing and immune-modulating properties. Curr Mol Med (2013) 13(4):572-85. doi:10.2174/1566524011313040009
55. Wang Y, Zhang X, Li H,Yu J, Ren X. The role of miRNA-29 family in cancer. Eur J Cell Biol (2013) 92(3):123-8. doi:10.1016/j.ejcb.2012.11.004
56. Laurila EM, Kallioniemi A. The diverse role of miR-31 in regulating cancer associated phenotypes. Genes Chromosomes Cancer (2013) 52(12):1103-13. doi:10.1002/gcc.22107
57. Vosa U, Vooder T, Kolde R, Vilo J, Metspalu A, Annilo T. Meta-analysis of microRNA expression in lung cancer. Int J Cancer (2013) 132(12):2884-93. doi:10.1002/ijc.27981
58. Daikoku T, Hirota Y, Tranguch S, Joshi AR, DeMayo FJ, Lydon JP, et al. Conditional loss of uterine Pten unfailingly and rapidly induces endometrial cancer in mice. Cancer Res (2008) 68(14):5619-27. doi:10.1158/0008-5472. CAN-08-1274
59. Davalos V, Esteller M. MicroRNAs and cancer epigenetics: a macrorevolution. Curr Opin Oncol (2010) 22(1):35-45. doi:10.1097/CCO.0b013e328333dcbb
60. Guo X, Liu Q,Wang G, Zhu S, Gao L, HongW, et al. microRNA-29b is a novel mediator of Sox2 function in the regulation of somatic cell reprogramming. Cell Res (2013) 23(1):142-56. doi:10.1038/cr.2012.180
61. Koturbash I,Zemp FJ,Pogribny I,KovalchukO. Smallmoleculeswith big effects: the role of the microRNAome in cancer and carcinogenesis. Mutat Res (2011) 722(2):94-105. doi:10.1016/j.mrgentox.2010.05.006
62. Yoshioka W, Higashiyama W, Tohyama C. Involvement of microRNAs in dioxin-induced liver damage in the mouse. Toxicol Sci (2011) 122(2):457-65. doi:10.1093/toxsci/kfr130
63. Varambally S, Cao Q,Mani RS, Shankar S,Wang X, Ateeq B, et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science (2008) 322(5908):1695-9. doi:10.1126/science.1165395
64. Wei X, Xiang T, Ren G, Tan C, Liu R, Xu X, et al. miR-101 is down-regulated by the hepatitis B virus x protein and induces aberrant DNA methylation by targeting DNA methyltransferase 3A. Cell Signal (2013) 25(2):439-46. doi:10.1016/j.cellsig.2012.10.013
65. Asangani IA, Harms PW, Dodson L, Pandhi M, Kunju LP, Maher CA, et al. Genetic and epigenetic loss of microRNA-31 leads to feed-forward expression of EZH2 in melanoma. Oncotarget (2012) 3(9):1011-25.
66. Chan YT, Lin YC, Lin RJ, Kuo HH, Thang WC, Chiu KP, et al. Concordant and discordant regulation of target genes by miR-31 and its isoforms. PLoS One (2013) 8(3):e58169. doi:10.1371/journal.pone.0058169
67. Earle JS, Luthra R, Romans A, Abraham R, Ensor J, Yao H, et al. Associa-tion of microRNA expression with microsatellite instability status in colorectal adenocarcinoma. J Mol Diagn (2010) 12(4):433-40. doi:10.2353/jmoldx.2010. 090154
68. Kovaleva V, Mora R, Park YJ, Plass C, Chiramel AI, Bartenschlager R, et al. miRNA-130a targets ATG2B and DICER1 to inhibit autophagy and trigger killing of chronic lymphocytic leukemia cells. Cancer Res (2012) 72(7):1763-72. doi:10.1158/0008-5472.CAN-11-3671
69. Tamminga J,Kathiria P,Koturbash I,KovalchukO.DNAdamage-induced upreg-ulation of miR-709 in the germline downregulates BORIS to counteract aber-rant DNA hypomethylation. Cell Cycle (2008) 7(23):3731-6. doi:10.4161/cc.7. 23.7186
70. Kraemer A, Anastasov N, Angermeier M, Winkler K, Atkinson MJ, Moertl S. MicroRNA-mediated processes are essential for the cellular radiation response. Radiat Res (2011) 176(5):575-86. doi:10.1667/RR2638.1
71. Templin T, Paul S, Amundson SA, Young EF, Barker CA, Wolden SL, et al. Radiation-induced micro-RNA expression changes in peripheral blood cells of radiotherapy patients. Int J Radiat Oncol Biol Phys (2011) 80(2):549-57. doi:10.1016/j.ijrobp.2010.12.061
72. Jaksik R, Lalik A, Skonieczna M, Cieslar-Pobuda A, Student S, Rzeszowska-Wolny J. MicroRNAs and reactive oxygen species: are they in the same regulatory circuit?. Mutat Res (2014) 764-765:64-71. doi:10.1016/j.mrgentox. 2013.09.003
73. Singh NP, Singh UP, Guan H, Nagarkatti P, Nagarkatti M. Prenatal exposure to TCDD triggers significant modulation of microRNA expression profile in the thymus that affects consequent gene expression. PLoS One (2012) 7(9):e45054. doi:10.1371/journal.pone.0045054
74. Moffat ID, Boutros PC, Celius T, Linden J, Pohjanvirta R, Okey AB. microR-NAs in adult rodent liver are refractory to dioxin treatment. Toxicol Sci (2007) 99(2):470-87. doi:10.1093/toxsci/kfm189
75. Fabbri M,Urani C, Sacco MG, Procaccianti C, Gribaldo L.Whole genome analy-sis and microRNAs regulation in HepG2 cells exposed to cadmium. ALTEX (2012) 29(2):173-82. doi:10.14573/altex.2012.2.173
76. Doi T, Puri P,McCannA,Bannigan J,Thompson J. Epigenetic effect of cadmium on global de novo DNA hypomethylation in the cadmium-induced ventral body wall defect (VBWD) in the chickmodel. Toxicol Sci (2011) 120(2):475-80. doi:10.1093/toxsci/kfr022
77. Takiguchi M, Achanzar WE, Qu W, Li G, Waalkes MP. Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation sta-tus during cadmium-induced cellular transformation. Exp Cell Res (2003) 286(2):355-65. doi:10.1016/S0014-4827(03)00062-4
78. Wang B, Li Y, Shao C, Tan Y, Cai L. Cadmium and its epigenetic effects. Curr Med Chem (2012) 19(16):2611-20. doi:10.2174/092986712800492913