Coordinate H3K9 and DNA methylation silencing of ZNFs in toxicant-induced malignant transformation

Epigenetics

Volumn 8, Issue 10, 2013, Pages 1080-1088

  Severson, Paul L ^a   Tokar, Erik J ^b   Vrba, Lukas ^c   Waalkes, Michael P ^b   Futscher, Bernard W ^a,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Arsenic; C2H2 zinc finger genes; DNA methylation; Epigenetics; H3K27me3; H3K4me3; H3K9me3; Malignant transformation

Indexed keywords

ARSENIC; BRAIN DERIVED NEUROTROPHIC FACTOR; OSTEONECTIN; TOXIC SUBSTANCE;

ANXA6 GENE; ARTICLE; C2H2 ZINC FINGER GENE; CARCINOGENESIS; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME 19; DNA ISOLATION; DNA METHYLATION; DNA MICROARRAY; DOWN REGULATION; EMBRYONIC STEM CELL; ENDOGENOUS RETROVIRUS; FGF5 GENE; GENE; GENE CLUSTER; GENE EXPRESSION; GENE SILENCING; HISTONE H3 LYSINE 27 TRIMETHYLATION; HISTONE H3 LYSINE 9 TRIMETHYLATION; HUMAN; HUMAN CELL; LAMB2 GENE; MALIGNANT TRANSFORMATION; NUCLEOTIDE SEQUENCE; PROSTATE EPITHELIUM; PTGS2 GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SLC4A11 GENE; TRANSCRIPTION INITIATION SITE; UCHL1 GENE; UPREGULATION;

ARSENIC; C2H2 ZINC FINGER GENES; DNA METHYLATION; EPIGENETICS; H3K27ME3; H3K4ME3; H3K9ME3; MALIGNANT TRANSFORMATION;

ARSENITES; CARRIER PROTEINS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; DNA METHYLATION; GENE ONTOLOGY; GENE SILENCING; HISTONES; HUMANS; LYSINE; NUCLEAR PROTEINS; ZINC FINGERS;

EID: 84884961634     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.25926     Document Type: Article

References (55)

1. Epsztejn-Litman S, Feldman N, Abu-Remaileh M, Shufaro Y, Gerson A, Ueda J, et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat Struct Mol Biol 2008; 15: 1176-83; PMID: 18953337; http://dx. doi. org/10. 1038/nsmb. 1476
2. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 2003; 13: 1192-200; PMID: 12867029; http://dx. doi. org/10. 1016/S0960-9822(03)00432-9
3. Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439: 871-4; PMID: 16357870; http://dx. doi. org/10. 1038/nature04431
4. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39: 232-6; PMID: 17200670; http://dx. doi. org/10. 1038/ng1950
5. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007; 448: 714-7; PMID: 17687327; http://dx. doi. org/10. 1038/nature05987
6. Rowe HM, Friedli M, Offner S, Verp S, Mesnard D, Marquis J, et al. De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET. Development 2013; 140: 519-29; http://dx. doi. org/10. 1242/dev. 087585; PMID: 23293284
7. Quenneville S, Turelli P, Bojkowska K, Raclot C, Offner S, Kapopoulou A, et al. The KRAB-ZFP/KAP1 system contributes to the early embryonic establishment of site-specific DNA methylation patterns maintained during development. Cell Rep 2012; 2: 766-73; http://dx. doi. org/10. 1016/j. celrep. 2012. 08. 043; PMID: 23041315
8. Groner AC, Meylan S, Ciuffi A, Zangger N, Ambrosini G, Dénervaud N, et al. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet 2010; 6: e1000869; http://dx. doi. org/10. 1371/journal. pgen. 1000869; PMID: 20221260
9. Huang X, Yuan W, Huang W, Bai Y, Deng Y, Zhu C, et al. ZNF569, a novel KRAB-containing zinc finger protein, suppresses MAPK signaling pathway. Biochem Biophys Res Commun 2006; 346: 621-8; PMID: 16793018; http://dx. doi. org/10. 1016/j. bbrc. 2006. 05. 109
10. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, et al. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 2010; 463: 237-40; http://dx. doi. org/10. 1038/nature08674; PMID: 20075919
11. Jensen TJ, Novak P, Eblin KE, Gandolfi AJ, Futscher BW. Epigenetic remodeling during arsenicalinduced malignant transformation. Carcinogenesis 2008; 29: 1500-8; PMID: 18448484; http://dx. doi. org/10. 1093/carcin/bgn102
12. Jensen TJ, Novak P, Wnek SM, Gandolfi AJ, Futscher BW. Arsenicals produce stable progressive changes in DNA methylation patterns that are linked to malignant transformation of immortalized urothelial cells. Toxicol Appl Pharmacol 2009; 241: 221-9; PMID: 19716837; http://dx. doi. org/10. 1016/j. taap. 2009. 08. 019
13. Wnek SM, Jensen TJ, Severson PL, Futscher BW, Gandolfi AJ. Monomethylarsonous acid produces irreversible events resulting in malignant transformation of a human bladder cell line following 12 weeks of low-level exposure. Toxicol Sci 2010; 116: 44-57; PMID: 20375083; http://dx. doi. org/10. 1093/toxsci/kfq106
14. Severson PL, Tokar EJ, Vrba L, Waalkes MP, Futscher BW. Agglomerates of aberrant DNA methylation are associated with toxicant-induced malignant transformation. Epigenetics 2012; 7: 1238-48; http://dx. doi. org/10. 4161/epi. 22163; PMID: 22976526
15. Blahnik KR, Dou L, Echipare L, Iyengar S, O'Geen H, Sanchez E, et al. Characterization of the contradictory chromatin signatures at the 3' exons of zinc finger genes. PLoS One 2011; 6: e17121; http://dx. doi. org/10. 1371/journal. pone. 0017121; PMID: 21347206
16. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, et al. Epigenetic stem cell signature in cancer. Nat Genet 2007; 39: 157-8; PMID: 17200673; http://dx. doi. org/10. 1038/ng1941
17. O'Geen H, Squazzo SL, Iyengar S, Blahnik K, Rinn JL, Chang HY, et al. Genome-wide analysis of KAP1 binding suggests autoregulation of KRAB-ZNFs. PLoS Genet 2007; 3: e89; PMID: 17542650; http://dx. doi. org/10. 1371/journal. pgen. 0030089
18. Vogel MJ, Guelen L, de Wit E, Peric-Hupkes D, Lodén M, Talhout W, et al. Human heterochromatin proteins form large domains containing KRAB-ZNF genes. Genome Res 2006; 16: 1493-504; PMID: 17038565; http://dx. doi. org/10. 1101/gr. 5391806
19. Cheng Y, Geng H, Cheng SH, Liang P, Bai Y, Li J, et al. KRAB zinc finger protein ZNF382 is a proapoptotic tumor suppressor that represses multiple oncogenes and is commonly silenced in multiple carcinomas. Cancer Res 2010; 70: 6516-26; http://dx. doi. org/10. 1158/0008-5472. CAN-09-4566; PMID: 20682794
20. Omura N, Li CP, Li A, Hong SM, Walter K, Jimeno A, et al. Genome-wide profiling of methylated promoters in pancreatic adenocarcinoma. Cancer Biol Ther 2008; 7: 1146-56; PMID: 18535405; http://dx. doi. org/10. 4161/cbt. 7. 7. 6208
21. Yamashita S, Tsujino Y, Moriguchi K, Tatematsu M, Ushijima T. Chemical genomic screening for methylation-silenced genes in gastric cancer cell lines using 5-aza-2'-deoxycytidine treatment and oligonucleotide microarray. Cancer Sci 2006; 97: 64-71; PMID: 16367923; http://dx. doi. org/10. 1111/j. 1349-7006. 2006. 00136. x
22. Mori Y, Olaru AV, Cheng Y, Agarwal R, Yang J, Luvsanjav D, et al. Novel candidate colorectal cancer biomarkers identified by methylation microarray-based scanning. Endocr Relat Cancer 2011; 18: 465-78; PMID: 21636702; http://dx. doi. org/10. 1530/ERC-11-0083
23. Lleras RA, Adrien LR, Smith RV, Brown B, Jivraj N, Keller C, et al. Hypermethylation of a cluster of Krüppel-type zinc finger protein genes on chromosome 19q13 in oropharyngeal squamous cell carcinoma. Am J Pathol 2011; 178: 1965-74; PMID: 21514414; http://dx. doi. org/10. 1016/j. ajpath. 2011. 01. 049
24. Andresen K, Boberg KM, Vedeld HM, Honne H, Hektoen M, Wadsworth CA, et al. Novel target genes and a valid biomarker panel identified for cholangiocarcinoma. Epigenetics 2012; 7: 1249-57; PMID: 22983262; http://dx. doi. org/10. 4161/epi. 22191
25. Morris MR, Ricketts CJ, Gentle D, McRonald F, Carli N, Khalili H, et al. Genome-wide methylation analysis identifies epigenetically inactivated candidate tumour suppressor genes in renal cell carcinoma. Oncogene 2011; 30: 1390-401; PMID: 21132003; http://dx. doi. org/10. 1038/onc. 2010. 525
26. Oka D, Yamashita S, Tomioka T, Nakanishi Y, Kato H, Kaminishi M, et al. The presence of aberrant DNA methylation in noncancerous esophageal mucosae in association with smoking history: a target for risk diagnosis and prevention of esophageal cancers. Cancer 2009; 115: 3412-26; PMID: 19472401; http://dx. doi. org/10. 1002/cncr. 24394
27. Mihara M, Yoshida Y, Tsukamoto T, Inada K, Nakanishi Y, Yagi Y, et al. Methylation of multiple genes in gastric glands with intestinal metaplasia: A disorder with polyclonal origins. Am J Pathol 2006; 169: 1643-51; PMID: 17071588; http://dx. doi. org/10. 2353/ajpath. 2006. 060552
28. Du Plessis L, Dietzsch E, Van Gele M, Van Roy N, Van Helden P, Parker MI, et al. Mapping of novel regions of DNA gain and loss by comparative genomic hybridization in esophageal carcinoma in the Black and Colored populations of South Africa. Cancer Res 1999; 59: 1877-83; PMID: 10213495
29. Shao JY, Huang XM, Yu XJ, Huang LX, Wu QL, Xia JC, et al. Loss of heterozygosity and its correlation with clinical outcome and Epstein-Barr virus infection in nasopharyngeal carcinoma. Anticancer Res 2001; 21(4B): 3021-9; PMID: 11712805
30. Tsuda H, Takarabe T, Okada S, Uchida H, Kasamatsu T, Yamada T, et al. Different pattern of loss of heterozygosity among endocervical-type adenocarcinoma, endometrioid-type adenocarcinoma and adenoma malignum of the uterine cervix. Int J Cancer 2002; 98: 713-7; PMID: 11920640; http://dx. doi. org/10. 1002/ijc. 10228
31. Xiang Z, Yuan W, Luo N, Wang Y, Tan K, Deng Y, et al. A novel human zinc finger protein ZNF540 interacts with MVP and inhibits transcriptional activities of the ERK signal pathway. Biochem Biophys Res Commun 2006; 347: 288-96; PMID: 16815308; http://dx. doi. org/10. 1016/j. bbrc. 2006. 06. 076
32. Cao L, Wang Z, Zhu C, Zhao Y, Yuan W, Li J, et al. ZNF383, a novel KRAB-containing zinc finger protein, suppresses MAPK signaling pathway. Biochem Biophys Res Commun 2005; 333: 1050-9; PMID: 15964543; http://dx. doi. org/10. 1016/j. bbrc. 2005. 05. 193
33. Li Y, Wang Y, Zhang C, Yuan W, Wang J, Zhu C, et al. ZNF322, a novel human C2H2 Kruppel-like zinc-finger protein, regulates transcriptional activation in MAPK signaling pathways. Biochem Biophys Res Commun 2004; 325: 1383-92; PMID: 15555580; http://dx. doi. org/10. 1016/j. bbrc. 2004. 10. 183
34. Li Y, Yang D, Bai Y, Mo X, Huang W, Yuan W, et al. ZNF418, a novel human KRAB/C2H2 zinc finger protein, suppresses MAPK signaling pathway. Mol Cell Biochem 2008; 310: 141-51; PMID: 18084723; http://dx. doi. org/10. 1007/s11010-007-9674-4
35. Liu F, Zhu C, Xiao J, Wang Y, Tang W, Yuan W, et al. A novel human KRAB-containing zinc-finger gene ZNF446 inhibits transcriptional activities of SRE and AP-1. Biochem Biophys Res Commun 2005; 333: 5-13; PMID: 15936718; http://dx. doi. org/10. 1016/j. bbrc. 2005. 05. 069
36. Liu H, Zhu C, Luo J, Wang Y, Li D, Li Y, et al. ZNF411, a novel KRAB-containing zinc-finger protein, suppresses MAP kinase signaling pathway. Biochem Biophys Res Commun 2004; 320: 45-53; PMID: 15207700; http://dx. doi. org/10. 1016/j. bbrc. 2004. 05. 130
37. Yang H, Yuan W, Wang Y, Zhu C, Liu B, Wang Y, et al. ZNF649, a novel Kruppel type zinc-finger protein, functions as a transcriptional suppressor. Biochem Biophys Res Commun 2005; 333: 206-15; PMID: 15950191; http://dx. doi. org/10. 1016/j. bbrc. 2005. 05. 101
38. Guallar D, Pérez-Palacios R, Climent M, Martínez-Abadía I, Larraga A, Fernández-Juan M, et al. Expression of endogenous retroviruses is negatively regulated by the pluripotency marker Rex1/Zfp42. Nucleic Acids Res 2012; 40: 8993-9007; http://dx. doi. org/10. 1093/nar/gks686; PMID: 22844087
39. Rowe HM, Trono D. Dynamic control of endogenous retroviruses during development. Virology 2011; 411: 273-87; http://dx. doi. org/10. 1016/j. virol. 2010. 12. 007; PMID: 21251689
40. Thomas JH, Schneider S. Coevolution of retroelements and tandem zinc finger genes. Genome Res 2011; 21: 1800-12; http://dx. doi. org/10. 1101/gr. 121749. 111; PMID: 21784874
41. Romanish MT, Cohen CJ, Mager DL. Potential mechanisms of endogenous retroviral-mediated genomic instability in human cancer. Semin Cancer Biol 2010; 20: 246-53; http://dx. doi. org/10. 1016/j. semcancer. 2010. 05. 005; PMID: 20685251
42. Zampieri M, Guastafierro T, Calabrese R, Ciccarone F, Bacalini MG, Reale A, et al. ADP-ribose polymers localized on Ctcf-Parp1-Dnmt1 complex prevent methylation of Ctcf target sites. Biochem J 2012; 441: 645-52; http://dx. doi. org/10. 1042/BJ20111417; PMID: 21985173
43. Witcher M, Emerson BM. Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol Cell 2009; 34: 271-84; http://dx. doi. org/10. 1016/j. molcel. 2009. 04. 001; PMID: 19450526
44. Wang F, Zhou X, Liu W, Sun X, Chen C, Hudson LG, et al. Arsenite-induced ROS/RNS generation causes zinc loss and inhibits the activity of poly(ADPribose) polymerase-1. Free Radic Biol Med 2013; 61C: 249-56; http://dx. doi. org/10. 1016/j. freeradbiomed. 2013. 04. 019; PMID: 23602911
45. Guastafierro T, Catizone A, Calabrese R, Zampieri M, Martella O, Bacalini MG, et al. ADP-ribose polymer depletion leads to nuclear Ctcf re-localization and chromatin rearrangement(1). Biochem J 2013; 449: 623-30; http://dx. doi. org/10. 1042/BJ20121429; PMID: 23116180
46. Bello D, Webber MM, Kleinman HK, Wartinger DD, Rhim JS. Androgen responsive adult human prostatic epithelial cell lines immortalized by human papillomavirus 18. Carcinogenesis 1997; 18: 1215-23; PMID: 9214605; http://dx. doi. org/10. 1093/carcin/18. 6. 1215
47. Achanzar WE, Brambila EM, Diwan BA, Webber MM, Waalkes MP. Inorganic arsenite-induced malignant transformation of human prostate epithelial cells. J Natl Cancer Inst 2002; 94: 1888-91; PMID: 12488483; http://dx. doi. org/10. 1093/jnci/94. 24. 1888
48. Benbrahim-Tallaa L, Waterland RA, Styblo M, Achanzar WE, Webber MM, Waalkes MP. Molecular events associated with arsenic-induced malignant transformation of human prostatic epithelial cells: aberrant genomic DNA methylation and K-ras oncogene activation. Toxicol Appl Pharmacol 2005; 206: 288-98; PMID: 16039940; http://dx. doi. org/10. 1016/j. taap. 2004. 11. 017
49. Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, et al. Chromosome-wide and promoterspecific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 2005; 37: 853-62; PMID: 16007088; http://dx. doi. org/10. 1038/ng1598
50. R_Development_Core_Team. R: A language and environment for statistical computing. 2010.
51. Vrba L, Garbe JC, Stampfer MR, Futscher BW. Epigenetic regulation of normal human mammary cell type-specific miRNAs. Genome Res 2011; 21: 2026-37; PMID: 21873453; http://dx. doi. org/10. 1101/gr. 123935. 111
52. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 2007; 23: 257-8; PMID: 17098774; http://dx. doi. org/10. 1093/bioinformatics/btl567
53. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003; 31: e15; PMID: 12582260; http://dx. doi. org/10. 1093/nar/gng015
54. Bengtsson H, Simpson K, Bullard J, Hansen K. Aroma. affymetrix: A generic framework in R for analyzing small to very large affymetrix data sets in bounded memory. 2008.
55. Smyth GK. Limma: Linear models for microarray data. 2005: 397-420.