Holocarboxylase synthetase synergizes with methyl CpG binding protein 2 and DNA methyltransferase 1 in the transcriptional repression of long-terminal repeats

Epigenetics

Volumn 8, Issue 5, 2013, Pages 504-511

  Xue, Jing ^a   Wijeratne, Subhashinee S K ^a   Zempleni, Janos ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Biotin; DNA methyl transferase; Holocarboxylase synthase; Long terminal repeats; Methyl CpG binding protein 2; Methylation; Repression

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HISTONE H3; HOLOCARBOXYLASE SYNTHETASE; LIGASE; MESSENGER RNA; METHYL CPG BINDING PROTEIN 2; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; DNA TRANSCRIPTION; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; LONG TERMINAL REPEAT; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 84877350648     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.24449     Document Type: Article

References (50)

1. Suzuki Y, Aoki Y, Ishida Y, Chiba Y, Iwamatsu A, Kishino T, et al. Isolation and characterization of mutations in the human holocarboxylase synthetase cDNA. Nat Genet 1994; 8:122-8; PMID:7842009; http://dx.doi.org/10.1038/ng1094-122
2. Hiratsuka M, Sakamoto O, Li X, Suzuki Y, Aoki Y, Narisawa K. Identification of holocarboxylase synthetase (HCS) proteins in human placenta. Biochim Biophys Acta 1998; 1385:165-71; PMID:9630604; http://dx.doi.org/10.1016/S0167-4838(98)00032-6
3. Zempleni J, Wijeratne SSK, Kuroishi T. (2012) Biotin, In Present Knowledge in Nutrition (Erdman JW, Jr., Macdonald I, Zeisel SH, Eds.), pp 587-609, International Life Sciences Institute, Washington, DC
4. Bailey LM, Wallace JC, Polyak SW. Holocarboxylase synthetase: correlation of protein localisation with biological function. Arch Biochem Biophys 2010; 496:45-52; PMID:20153287; http://dx.doi.org/10.1016/j. abb.2010.01.015
5. Bao B, Wijeratne SS, Rodriguez-Melendez R, Zempleni J. Human holocarboxylase synthetase with a start site at methionine-58 is the predominant nuclear variant of this protein and has catalytic activity. Biochem Biophys Res Commun 2011; 412:115-20; PMID:21802411; http://dx.doi.org/10.1016/j.bbrc.2011.07.055
6. Camporeale G, Giordano E, Rendina R, Zempleni J, Eissenberg JC. Drosophila melanogaster holocarboxylase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan, and heat tolerance. J Nutr 2006; 136:2735-42; PMID:17056793
7. Singh D, Pannier AK, Zempleni J. Identification of holocarboxylase synthetase chromatin binding sites using the DamID technology. Anal Biochem 2011; 413:55-9; PMID:21303649; http://dx.doi. org/10.1016/j.ab.2011.02.001
8. Bao B, Pestinger V, Hassan YI, Borgstahl GE, Kolar C, Zempleni J. Holocarboxylase synthetase is a chromatin protein and interacts directly with histone H3 to mediate biotinylation of K9 and K18. J Nutr Biochem 2011; 22:470-5; PMID:20688500; http://dx.doi.org/10.1016/j.jnutbio.2010.04.001
9. Chew YC, West JT, Kratzer SJ, Ilvarsonn AM, Eissenberg JC, Dave BJ, et al. Biotinylation of histones represses transposable elements in human and mouse cells and cell lines and in Drosophila melanogaster. J Nutr 2008; 138:2316-22; PMID:19022951 and http://dx.doi.org/10.3945/jn.108.098673
10. Pestinger V, Wijeratne SSK, Rodriguez-Melendez R, Zempleni J. Novel histone biotinylation marks are enriched in repeat regions and participate in repression of transcriptionally competent genes. J Nutr Biochem 2011; 22:328-33; PMID:20691578; http://dx.doi. org/10.1016/j.jnutbio.2010.02.011
11. Rios-Avila L, Pestinger V, Zempleni J. K16-biotinylated histone H4 is overrepresented in repeat regions and participates in the repression of transcriptionally competent genes in human Jurkat lymphoid cells. J Nutr Biochem 2012; 23:1559-64; PMID:22192339; http://dx.doi.org/10.1016/j.jnutbio.2011.10.009
12. Camporeale G, Oommen AM, Griffin JB, Sarath G, Zempleni J. K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J Nutr Biochem 2007; 18:760-8; PMID:17434721; http://dx.doi.org/10.1016/j.jnutbio.2006.12.014
13. Wijeratne SS, Camporeale G, Zempleni J. K12-biotinylated histone H4 is enriched in telomeric repeats from human lung IMR-90 fibroblasts. J Nutr Biochem 2010; 21:310-6; PMID:19369050; http://dx.doi. org/10.1016/j.jnutbio.2009.01.010
14. Stanley JS, Griffin JB, Zempleni J. Biotinylation of histones in human cells. Effects of cell proliferation. Eur J Biochem 2001; 268:5424-9; PMID:11606205; http://dx.doi.org/10.1046/j.0014-2956.2001.02481.x
15. Bailey LM, Ivanov RA, Wallace JC, Polyak SW. Artifactual detection of biotin on histones by streptavidin. Anal Biochem 2008; 373:71-7; PMID:17920026; http://dx.doi.org/10.1016/j.ab.2007.09.003
16. Kuroishi T, Rios-Avila L, Pestinger V, Wijeratne SS, Zempleni J. Biotinylation is a natural, albeit rare, modification of human histones. Mol Genet Metab 2011; 104:537-45; PMID:21930408; http://dx.doi. org/10.1016/j.ymgme.2011.08.030
17. Li Y, Hassan YI, Moriyama H, Zempleni J. Holocarboxylase synthetase interacts physically with euchromatic histone-lysine N-methyltransferase, linking biotinylation with histone methylation. J Nutr Biochem 2013; In press; PMID:23337344; http://dx.doi.org/10.1016/j.jnutbio.2012.12.003
18. Kouzarides T, Berger SL. (2007) Chromatin modifications and their mechanism of action, In Epigenetics (Allis CD, Jenuwein T, Reinberg D, Eds.), pp 191-209, Cold Spring Harbor Press, Cold Spring Harbor, NY
19. Gralla M, Camporeale G, Zempleni J. Holocarboxylase synthetase regulates expression of biotin transporters by chromatin remodeling events at the SMVT locus. J Nutr Biochem 2008; 19:400-8; PMID:17904341; http://dx.doi.org/10.1016/j.jnutbio.2007.06.002
20. Schermelleh L, Haemmer A, Spada F, Rösing N, Meilinger D, Rothbauer U, et al. Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucleic Acids Res 2007; 35:4301-12; PMID:17576694; http://dx.doi.org/10.1093/nar/gkm432
21. Li E, Bird A. (2007) DNA methylation in mammals, In Epigenetics (Allis CD, Jenuwein T, Reinberg D, Eds.), pp 341-56, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
22. Bogdanović O, Veenstra GJ. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 2009; 118:549-65; PMID:19506892; http://dx.doi.org/10.1007/s00412-009-0221-9
23. Kolker E, Higdon R, Haynes W, Welch D, Broomall W, Lancet D, et al. MOPED: Model Organism Protein Expression Database. Nucleic Acids Res 2012; 40(Database issue):D1093-9; PMID:22139914; http://dx.doi.org/10.1093/nar/gkr1177
24. Brenet F, Moh M, Funk P, Feierstein E, Viale AJ, Socci ND, et al. DNA methylation of the first exon is tightly linked to transcriptional silencing. PLoS ONE 2011; 6:e14524; PMID:21267076; http://dx.doi. org/10.1371/journal.pone.0014524
25. Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 2005; 24:800-12; PMID:15678104; http://dx.doi.org/10.1038/sj.emboj.7600545
26. Buzdin A, Kovalskaya-Alexandrova E, Gogvadze E, Sverdlov E. GREM, a technique for genome-wide isolation and quantitative analysis of promoter active repeats. Nucleic Acids Res 2006; 34:e67; PMID:16698959; http://dx.doi.org/10.1093/nar/gkl335
27. Kazazian HH Jr. Mobile elements: drivers of genome evolution. Science 2004; 303:1626-32; PMID:15016989; http://dx.doi.org/10.1126/science. 1089670
28. Jaenisch R, Schnieke A, Harbers K. Treatment of mice with 5-azacytidine efficiently activates silent retroviral genomes in different tissues. Proc Natl Acad Sci USA 1985; 82:1451-5; PMID:2579397; http://dx.doi. org/10.1073/pnas.82.5.1451
29. Jähner D, Stuhlmann H, Stewart CL, Harbers K, Löhler J, Simon I, et al. De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature 1982; 298:623-8; PMID:6285203; http://dx.doi.org/10.1038/298623a0
30. Stewart CL, Stuhlmann H, Jähner D, Jaenisch R. De novo methylation, expression, and infectivity of retroviral genomes introduced into embryonal carcinoma cells. Proc Natl Acad Sci USA 1982; 79:4098-102; PMID:6955793; http://dx.doi.org/10.1073/pnas.79.13.4098
31. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003; 300:455; PMID:12702868; http://dx.doi.org/10.1126/science. 1083557
32. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, et al. Induction of tumors in mice by genomic hypomethylation. Science 2003; 300:489-92; PMID:12702876; http://dx.doi.org/10.1126/science. 1083558
33. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, et al.; Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature 2002; 420:520-62; PMID:12466850; http://dx.doi.org/10.1038/nature01262
34. Chazin WJ. (2007) Chazin Lab Protocols, http://www. ihcworld.com/_protocols/lab_protocols/chazin-labprotocols. htm (accessed 1/20/2009)
35. Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 1998; 12:949-57; PMID:9707167
36. Stover PJ. One-carbon metabolism-genome interactions in folate-associated pathologies. J Nutr 2009; 139:2402-5; PMID:19812215; http://dx.doi. org/10.3945/jn.109.113670
37. Zeisel SH. Is maternal diet supplementation beneficial? Optimal development of infant depends on mother's diet. Am J Clin Nutr 2009; 89:685S-7S; PMID:19116319; http://dx.doi.org/10.3945/ajcn.2008.26811F
38. Wen YD, Perissi V, Staszewski LM, Yang WM, Krones A, Glass CK, et al. The histone deacetylase-3 complex contains nuclear receptor corepressors. Proc Natl Acad Sci USA 2000; 97:7202-7; PMID:10860984; http://dx.doi.org/10.1073/pnas.97.13.7202
39. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138:1019-31; PMID:19698979; http://dx.doi.org/10.1016/j.cell.2009.06.049
40. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007; 448:553-60; PMID:17603471; http://dx.doi.org/10.1038/nature06008
41. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008; 454:766-70; PMID:18600261
42. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ 3rd. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 2002; 16:919-32; PMID:11959841; http://dx.doi. org/10.1101/gad.973302
43. Yang L, Xia L, Wu DY, Wang H, Chansky HA, Schubach WH, et al. Molecular cloning of ESET, a novel histone H3-specific methyltransferase that interacts with ERG transcription factor. Oncogene 2002; 21:148-52; PMID:11791185; http://dx.doi. org/10.1038/sj.onc.1204998
44. Esaki S, Malkaram SA, Zempleni J. Effects of singlenucleotide polymorphisms in the human holocarboxylase synthetase gene on enzyme catalysis. Eur J Hum Genet 2012; 20:428-33; PMID:22027809; http://dx.doi.org/10.1038/ejhg.2011.198
45. Chew YC, Camporeale G, Kothapalli N, Sarath G, Zempleni J. Lysine residues in N-and C-terminal regions of human histone H2A are targets for biotinylation by biotinidase. J Nutr Biochem 2006; 17:225-33; PMID:16109483; http://dx.doi.org/10.1016/j. jnutbio.2005.05.003
46. Dahl JA, Collas P. MicroChIP--a rapid micro chromatin immunoprecipitation assay for small cell samples and biopsies. Nucleic Acids Res 2007; 36:e15; PMID:18202078; http://dx.doi.org/10.1093/nar/gkm1158
47. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, et al. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 2009; 10:R130; PMID:19919682; http://dx.doi.org/10.1186/gb-2009-10-11-r130
48. SAS Institute. (2008) SAS/STAT 9.2 User's Guide, SAS Institute, Cary, NC
49. McDonald JH. (2009) Handbook of Biological Statistics, 2nd. ed., Sparky House Publishing, Baltimore, MD
50. Kovalskaya E, Buzdin A, Gogvadze E, Vinogradova T, Sverdlov E. Functional human endogenous retroviral LTR transcription start sites are located between the R and U5 regions. Virology 2006; 346:373-8; PMID:16337666; http://dx.doi.org/10.1016/j. virol.2005.11.007