#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

hnRNP K Coordinates Transcriptional Silencing by SETDB1 in Embryonic Stem Cells


Retroelements, including endogenous retroviruses (ERVs), pose a significant threat to genome stability. In mouse embryonic stem (ES) cells, the enzyme SETDB1 safeguards the genome against transcription of specific ERVs by depositing a repressive mark H3K9 trimethylation (H3K9me3). Although SETDB1 is recruited to ERVs by its binding partner KAP1, the molecular basis of this silencing pathway is not clear. Using biochemical and genetic approaches, we identified hnRNP K as a novel component of this silencing pathway that facilitates the recruitment of SETDB1 to ERVs to promote their repression. HnRNP K binds to ERV sequences via KAP1 and subsequently promotes SETDB1 binding. Together, our results reveal a novel function for hnRNP K in transcriptional silencing of ERVs and demonstrate a new regulatory mechanism governing the deposition of H3K9me3 by SETDB1 in ES cells.


Vyšlo v časopise: hnRNP K Coordinates Transcriptional Silencing by SETDB1 in Embryonic Stem Cells. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004933
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004933

Souhrn

Retroelements, including endogenous retroviruses (ERVs), pose a significant threat to genome stability. In mouse embryonic stem (ES) cells, the enzyme SETDB1 safeguards the genome against transcription of specific ERVs by depositing a repressive mark H3K9 trimethylation (H3K9me3). Although SETDB1 is recruited to ERVs by its binding partner KAP1, the molecular basis of this silencing pathway is not clear. Using biochemical and genetic approaches, we identified hnRNP K as a novel component of this silencing pathway that facilitates the recruitment of SETDB1 to ERVs to promote their repression. HnRNP K binds to ERV sequences via KAP1 and subsequently promotes SETDB1 binding. Together, our results reveal a novel function for hnRNP K in transcriptional silencing of ERVs and demonstrate a new regulatory mechanism governing the deposition of H3K9me3 by SETDB1 in ES cells.


Zdroje

1. Stocking C, Kozak C a (2008) Murine endogenous retroviruses. Cell Mol Life Sci 65: 3383–3398. Available: http://www.ncbi.nlm.nih.gov/pubmed/18818872. Accessed 26 May 2014. doi: 10.1007/s00018-008-8497-0 18818872

2. Maksakova I a, Romanish MT, Gagnier L, Dunn C a, van de Lagemaat LN, et al. (2006) Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet 2: e2. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1331978&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1371/journal.pgen.0020002 16440055

3. Peaston AE, Evsikov A V, Graber JH, de Vries WN, Holbrook AE, et al. (2004) Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 7: 597–606. Available: http://www.ncbi.nlm.nih.gov/pubmed/15469847. doi: 10.1016/j.devcel.2004.09.004 15469847

4. Leung DC, Lorincz MC (2012) Silencing of endogenous retroviruses: when and why do histone marks predominate? Trends Biochem Sci 37: 127–133. Available: http://www.ncbi.nlm.nih.gov/pubmed/22178137. Accessed 30 May 2014. doi: 10.1016/j.tibs.2011.11.006 22178137

5. Walsh CP, Chaillet JR, Bestor TH (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20: 116–117. Available: http://www.ncbi.nlm.nih.gov/pubmed/9771701. doi: 10.1038/2413 9771701

6. Hutnick LK, Huang X, Loo T-C, Ma Z, Fan G (2010) Repression of retrotransposal elements in mouse embryonic stem cells is primarily mediated by a DNA methylation-independent mechanism. J Biol Chem 285: 21082–21091. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2898347&tool=pmcentrez&rendertype=abstract. Accessed 31 May 2014. doi: 10.1074/jbc.M110.125674 20404320

7. Lupo A, Cesaro E, Montano G, Zurlo D, Izzo P, et al. (2013) KRAB-Zinc Finger Proteins : A Repressor Family Displaying Multiple Bio- logical Functions: 268–278.

8. Friedman JR, Fredericks WJ, Jensen DE, Speicher DW, Huang XP, et al. (1996) KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev 10: 2067–2078. Available: http://www.genesdev.org/cgi/doi/10.1101/gad.10.16.2067. Accessed 24 May 2014. doi: 10.1101/gad.10.16.2067 8769649

9. Wolf D, Goff SP (2009) Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 458: 1201–1204. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2676211&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1038/nature07844 19270682

10. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ (2002) 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 16: 919–932. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=152359&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1101/gad.973302 11959841

11. Matsui T, Leung D, Miyashita H, Maksakova I a, Miyachi H, et al. (2010) Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927–931. Available: http://www.ncbi.nlm.nih.gov/pubmed/20164836. Accessed 30 May 2014. doi: 10.1038/nature08858 20164836

12. Lukic S, Nicolas J-C, Levine a J (2014) The diversity of zinc-finger genes on human chromosome 19 provides an evolutionary mechanism for defense against inherited endogenous retroviruses. Cell Death Differ 21: 381–387. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3921586&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014. doi: 10.1038/cdd.2013.150 24162661

13. Schlesinger S, Lee AH, Wang GZ, Green L, Goff SP (2013) Proviral silencing in embryonic cells is regulated by Yin Yang 1. Cell Rep 4: 50–58. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3771693&tool=pmcentrez&rendertype=abstract. Accessed 5 June 2014. doi: 10.1016/j.celrep.2013.06.003 23810560

14. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, et al. (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237–240. Available: http://www.ncbi.nlm.nih.gov/pubmed/20075919. Accessed 30 May 2014. doi: 10.1038/nature08674 20075919

15. Liu S, Brind’Amour J, Karimi MM, Shirane K, Bogutz A, et al. (2014) Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells. Genes Dev 28: 2041–2055. Available: http://www.ncbi.nlm.nih.gov/pubmed/25228647. Accessed 18 September 2014. doi: 10.1101/gad.244848.114 25228647

16. Leung D, Du T, Wagner U, Xie W, Lee AY, et al. (2014) Regulation of DNA methylation turnover at LTR retrotransposons and imprinted loci by the histone methyltransferase Setdb1. Proc Natl Acad Sci U S A 111: 6690–6695. Available: http://www.ncbi.nlm.nih.gov/pubmed/24757056. Accessed 26 May 2014. doi: 10.1073/pnas.1322273111 24757056

17. Karimi MM, Goyal P, Maksakova I a, Bilenky M, Leung D, et al. (2011) DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8: 676–687. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3857791&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1016/j.stem.2011.04.004 21624812

18. Ivanov A V, Peng H, Yurchenko V, Yap KL, Negorev DG, et al. (2007) PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 28: 823–837. Available: http://www.ncbi.nlm.nih.gov/pubmed/18082607. Accessed 30 May 2014. doi: 10.1016/j.molcel.2007.11.012 18082607

19. Lee Y-K, Thomas SN, Yang AJ, Ann DK (2007) Doxorubicin down-regulates Kruppel-associated box domain-associated protein 1 sumoylation that relieves its transcription repression on p21WAF1/CIP1 in breast cancer MCF-7 cells. J Biol Chem 282: 1595–1606. Available: http://www.ncbi.nlm.nih.gov/pubmed/17079232. Accessed 30 May 2014. doi: 10.1074/jbc.M606306200 17079232

20. Li X, Lee Y-K, Jeng J-C, Yen Y, Schultz DC, et al. (2007) Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J Biol Chem 282: 36177–36189. Available: http://www.ncbi.nlm.nih.gov/pubmed/17942393. Accessed 30 May 2014. doi: 10.1074/jbc.M706912200 17942393

21. Garvin AJ, Densham RM, Blair-Reid S a, Pratt KM, Stone HR, et al. (2013) The deSUMOylase SENP7 promotes chromatin relaxation for homologous recombination DNA repair. EMBO Rep 14: 975–983. Available: http://www.ncbi.nlm.nih.gov/pubmed/24018422. Accessed 10 June 2014. doi: 10.1038/embor.2013.141 24018422

22. Tang F, Barbacioru C, Nordman E, Bao S, Lee C, et al. (2011) Deterministic and stochastic allele specific gene expression in single mouse blastomeres. PLoS One 6: e21208. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3121735&tool=pmcentrez&rendertype=abstract. Accessed 22 March 2012. doi: 10.1371/journal.pone.0021208 21731673

23. Bilodeau S, Kagey MH, Frampton GM, Rahl PB, Young R a (2009) SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev 23: 2484–2489. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2779743&tool=pmcentrez&rendertype=abstract. Accessed 26 May 2014. doi: 10.1101/gad.1837309 19884255

24. Wang H, An W, Cao R, Xia L, Erdjument-bromage H, et al. (2003) mAM Facilitates Conversion by ESET of Dimethyl to Trimethyl Lysine 9 of Histone H3 to Cause Transcriptional Repression University of North Carolina at Chapel Hill. 12: 475–487.

25. Bomsztyk K, Denisenko O, Ostrowski J (2004) hnRNP K: one protein multiple processes. Bioessays 26: 629–638. Available: http://www.ncbi.nlm.nih.gov/pubmed/15170860. Accessed 5 June 2014. doi: 10.1002/bies.20048 15170860

26. Denisenko ON, O’Neill B, Ostrowski J, Van Seuningen I, Bomsztyk K (1996) Zik1, a transcriptional repressor that interacts with the heterogeneous nuclear ribonucleoprotein particle K protein. J Biol Chem 271: 27701–27706. Available: http://www.ncbi.nlm.nih.gov/pubmed/8910362. doi: 10.1074/jbc.271.44.27701 8910362

27. Sarge KD, Park-Sarge O-K (2009) Detection of Proteins sumoylated in vitro and in vivo. In: Park-Sarge O-K, Curry TE, editors. Molecular Endocrinology: Methods in Molecular Biology. Methods in Molecular Biology. Totowa, NJ: Humana Press, Vol. 590. pp. 265–277. Available: http://link.springer.com/10.1007/978–1–60327–378–7. Accessed 28 May 2014.

28. Yuan P, Han J, Guo G, Orlov YL, Huss M, et al. (2009) Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev 23: 2507–2520. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2779752&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1101/gad.1831909 19884257

29. Germain-Desprez D, Bazinet M, Bouvier M, Aubry M (2003) Oligomerization of transcriptional intermediary factor 1 regulators and interaction with ZNF74 nuclear matrix protein revealed by bioluminescence resonance energy transfer in living cells. J Biol Chem 278: 22367–22373. Available: http://www.ncbi.nlm.nih.gov/pubmed/12684500. Accessed 18 September 2014. doi: 10.1074/jbc.M302234200 12684500

30. Dejgaard K, Leffers H (1996) Characterisation of the nucleic-acid-binding activity of KH domains. Different properties of different domains. Eur J Biochem 241: 425–431. Available: http://www.ncbi.nlm.nih.gov/pubmed/8917439.

31. Ostrowski J, Seuningens I Van, Segern R, Rauchll T, Sleathll PR, et al. (1994) Purification, Cloning, and Expression of a Murine Phosphoprotein That Binds the KB Motif in Vitro Identifies It as the Homolog of the K Protein Human Heterogeneous Nuclear Ribonucleoprotein. J Biol Chem 269: 17626–17634. 8021272

32. Pelisch F, Pozzi B, Risso G, Muñoz MJ, Srebrow A (2012) DNA damage-induced heterogeneous nuclear ribonucleoprotein K sumoylation regulates p53 transcriptional activation. J Biol Chem 287: 30789–30799. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3436322&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1074/jbc.M112.390120 22825850

33. Lee SW, Lee MH, Park JH, Kang SH, Yoo HM, et al. (2012) SUMOylation of hnRNP-K is required for p53-mediated cell-cycle arrest in response to DNA damage. EMBO J 31: 4441–4452. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3512394&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1038/emboj.2012.293 23092970

34. Mahajan R, Gerace L, Melchior F (1998) Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J Cell Biol 140: 259–270. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2132567&tool=pmcentrez&rendertype=abstract. doi: 10.1083/jcb.140.2.259 9442102

35. Rodriguez MS, Desterro JM, Lain S, Midgley C a, Lane DP, et al. (1999) SUMO-1 modification activates the transcriptional response of p53. EMBO J 18: 6455–6461. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1171708&tool=pmcentrez&rendertype=abstract. doi: 10.1093/emboj/18.22.6455 10562557

36. Peng H, Begg GE, Schultz DC, Friedman JR, Jensen DE, et al. (2000) Reconstitution of the KRAB-KAP-1 repressor complex: a model system for defining the molecular anatomy of RING-B box-coiled-coil domain-mediated protein-protein interactions. J Mol Biol 295: 1139–1162. Available: http://www.ncbi.nlm.nih.gov/pubmed/10653693. doi: 10.1006/jmbi.1999.3402 10653693

37. Yang B, O’Herrin SM, Wu J, Reagan-Shaw S, Ma Y, et al. (2007) MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res 67: 9954–9962. Available: http://www.ncbi.nlm.nih.gov/pubmed/17942928. Accessed 2 October 2014. doi: 10.1158/0008-5472.CAN-07-1478 17942928

38. Li X, Lin HH, Chen H, Xu X, Shih H-M, et al. (2010) SUMOylation of the transcriptional co-repressor KAP1 is regulated by the serine and threonine phosphatase PP1. Sci Signal 3: ra32. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3302164&tool=pmcentrez&rendertype=abstract. Accessed 25 September 2014. doi: 10.1126/scisignal.2000781 20424263

39. Ryan RF, Schultz DC, Ayyanathan K, Singh PB, Friedman JR, et al. (1999) KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Krüppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol Cell Biol 19: 4366–4378. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=104396&tool=pmcentrez&rendertype=abstract 10330177

40. Schultz DC, Friedman JR, Rauscher FJ (2001) Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev 15: 428–443. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=312636&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1101/gad.869501 11230151

41. Maksakova I a, Goyal P, Bullwinkel J, Brown JP, Bilenky M, et al. (2011) H3K9me3-binding proteins are dispensable for SETDB1/H3K9me3-dependent retroviral silencing. Epigenetics Chromatin 4: 12. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3169442&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1186/1756-8935-4-12 21774827

42. Maksakova I a, Thompson PJ, Goyal P, Jones SJ, Singh PB, et al. (2013) Distinct roles of KAP1, HP1 and G9a/GLP in silencing of the two-cell-specific retrotransposon MERVL in mouse ES cells. Epigenetics Chromatin 6: 15. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3682905&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1186/1756-8935-6-15 23735015

43. Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, et al. (2006) Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11: 805–814. Available: http://www.ncbi.nlm.nih.gov/pubmed/16824199. Accessed 27 May 2014. doi: 10.1111/j.1365-2443.2006.00984.x 16824199

44. Dinh PX, Das A, Franco R, Pattnaik AK (2013) Heterogeneous nuclear ribonucleoprotein K supports vesicular stomatitis virus replication by regulating cell survival and cellular gene expression. J Virol 87: 10059–10069. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3754001&tool=pmcentrez&rendertype=abstract. Accessed 25 September 2014. doi: 10.1128/JVI.01257-13 23843646

45. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553–560. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2921165&tool=pmcentrez&rendertype=abstract. Accessed 1 March 2012. doi: 10.1038/nature06008 17603471

46. Marks H, Kalkan T, Menafra R, Denissov S, Jones K, et al. (2012) The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149: 590–604. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3398752&tool=pmcentrez&rendertype=abstract. Accessed 26 May 2014. doi: 10.1016/j.cell.2012.03.026 22541430

47. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315–326. Available: http://www.ncbi.nlm.nih.gov/pubmed/16630819. Accessed 13 March 2012. doi: 10.1016/j.cell.2006.02.041 16630819

48. Boyer L a, Plath K, Zeitlinger J, Brambrink T, Medeiros L a, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349–353. Available: http://www.ncbi.nlm.nih.gov/pubmed/16625203. Accessed 23 May 2014. doi: 10.1038/nature04733 16625203

49. Fujikura J, Yamato E, Yonemura S, Hosoda K, Masui S, et al. (2002) Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev 16: 784–789. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=186328&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014. doi: 10.1101/gad.968802 11937486

50. Zhang C, Ye X, Zhang H, Ding M, Deng H (2007) GATA factors induce mouse embryonic stem cell differentiation toward extraembryonic endoderm. Stem Cells Dev 16: 605–613. Available: http://www.ncbi.nlm.nih.gov/pubmed/17784834. Accessed 10 June 2014. doi: 10.1089/scd.2006.0077 17784834

51. Mikula M, Bomsztyk K (2011) Direct recruitment of ERK cascade components to inducible genes is regulated by heterogeneous nuclear ribonucleoprotein (hnRNP) K. J Biol Chem 286: 9763–9775. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3058954&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1074/jbc.M110.213330 21233203

52. Mikula M, Bomsztyk K, Goryca K, Chojnowski K, Ostrowski J (2013) Heterogeneous nuclear ribonucleoprotein (HnRNP) K genome-wide binding survey reveals its role in regulating 3’-end RNA processing and transcription termination at the early growth response 1 (EGR1) gene through XRN2 exonuclease. J Biol Chem 288: 24788–24798. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3750174&tool=pmcentrez&rendertype=abstract. Accessed 26 September 2014. doi: 10.1074/jbc.M113.496679 23857582

53. Zeng L, Yap KL, Ivanov A V, Wang X, Mujtaba S, et al. (2008) Structural insights into human KAP1 PHD finger-bromodomain and its role in gene silencing. Nat Struct Mol Biol 15: 626–633. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3331790&tool=pmcentrez&rendertype=abstract. Accessed 20 September 2014. doi: 10.1038/nsmb.1416 18488044

54. Fukuda I, Ito A, Hirai G, Nishimura S, Kawasaki H, et al. (2009) Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate. Chem Biol 16: 133–140. Available: http://www.ncbi.nlm.nih.gov/pubmed/19246003. Accessed 29 May 2014. doi: 10.1016/j.chembiol.2009.01.009 19246003

55. Balasubramanyam K, Swaminathan V, Ranganathan A, Kundu TK (2003) Small molecule modulators of histone acetyltransferase p300. J Biol Chem 278: 19134–19140. Available: http://www.ncbi.nlm.nih.gov/pubmed/12624111. Accessed 9 June 2014. doi: 10.1074/jbc.M301580200 12624111

56. Nacerddine K, Lehembre F, Bhaumik M, Artus J, Cohen-Tannoudji M, et al. (2005) The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell 9: 769–779. Available: http://www.ncbi.nlm.nih.gov/pubmed/16326389. Accessed 30 May 2014. doi: 10.1016/j.devcel.2005.10.007 16326389

57. Tan X, Xu X, Elkenani M, Smorag L, Zechner U, et al. (2013) Zfp819, a novel KRAB-zinc finger protein, interacts with KAP1 and functions in genomic integrity maintenance of mouse embryonic stem cells. Stem Cell Res 11: 1045–1059. Available: http://www.ncbi.nlm.nih.gov/pubmed/23954693. Accessed 10 June 2014. doi: 10.1016/j.scr.2013.07.006 23954693

58. Charroux B, Angelats C, Fasano L, Kerridge S, Vola C (1999) The levels of the bancal product, a Drosophila homologue of vertebrate hnRNP K protein, affect cell proliferation and apoptosis in imaginal disc cells. Mol Cell Biol 19: 7846–7856. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=84859&tool=pmcentrez&rendertype=abstract 10523673

59. Denisenko O, Bomsztyk K (2002) Yeast hnRNP K-Like Genes Are Involved in Regulation of the Telomeric Position Effect and Telomere Length Yeast hnRNP K-Like Genes Are Involved in Regulation of the Telomeric Position Effect and Telomere Length. 22.

60. Denisenko ON, Bomsztyk K (1997) The product of the murine homolog of the Drosophila extra sex combs gene displays transcriptional repressor activity. The Product of the Murine Homolog of the Drosophila extra sex combs Gene Displays Transcriptional Repressor Activity. Mol Cell Biol 17: 4707–4717.

61. Ichimura T, Watanabe S, Sakamoto Y, Aoto T, Fujita N, et al. (2005) Transcriptional repression and heterochromatin formation by MBD1 and MCAF/AM family proteins. J Biol Chem 280: 13928–13935. Available: http://www.ncbi.nlm.nih.gov/pubmed/15691849. Accessed 26 June 2014. doi: 10.1074/jbc.M413654200 15691849

62. Neyret-Kahn H, Benhamed M, Ye T, Le Gras S, Cossec J-C, et al. (2013) Sumoylation at chromatin governs coordinated repression of a transcriptional program essential for cell growth and proliferation. Genome Res 23: 1563–1579. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3787255&tool=pmcentrez&rendertype=abstract. Accessed 30 May 2014. doi: 10.1101/gr.154872.113 23893515

63. Iyengar S, Ivanov A V, Jin VX, Rauscher FJ, Farnham PJ (2011) Functional analysis of KAP1 genomic recruitment. Mol Cell Biol 31: 1833–1847. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3133220&tool=pmcentrez&rendertype=abstract. Accessed 30 May 2014. doi: 10.1128/MCB.01331-10 21343339

64. Kuo C-Y, Li X, Kong X-Q, Luo C, Chang C-C, et al. (2014) An Arginine-rich Motif of Ring Finger Protein 4 (RNF4) Oversees the Recruitment and Degradation of the Phosphorylated and SUMOylated Krüppel-associated Box Domain-associated Protein 1 (KAP1)/TRIM28 Protein during Genotoxic Stress. J Biol Chem 289: 20757–20772. Available: http://www.ncbi.nlm.nih.gov/pubmed/24907272. Accessed 26 September 2014. doi: 10.1074/jbc.M114.555672 24907272

65. Seki Y, Kurisaki A, Watanabe-susaki K, Nakajima Y, Nakanishi M (2010) TIF1 β regulates the pluripotency of embryonic stem cells in a phosphorylation-dependent manner.

66. Koch CM, Honemann-Capito M, Egger-Adam D, Wodarz A (2009) Windei, the Drosophila homolog of mAM/MCAF1, is an essential cofactor of the H3K9 methyl transferase dSETDB1/Eggless in germ line development. PLoS Genet 5: e1000644. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2730569&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1371/journal.pgen.1000644 19750210

67. Wen F, Shen A, Shanas R, Bhattacharyya A, Lian F, et al. (2010) Higher expression of the heterogeneous nuclear ribonucleoprotein k in melanoma. Ann Surg Oncol 17: 2619–2627. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2943057&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1245/s10434-010-1121-1 20499280

68. Ceol CJ, Houvras Y, Jane-Valbuena J, Bilodeau S, Orlando D a, et al. (2011) The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 471: 513–517. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3348545&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1038/nature09806 21430779

69. Barboro P, Repaci E, Rubagotti a, Salvi S, Boccardo S, et al. (2009) Heterogeneous nuclear ribonucleoprotein K: altered pattern of expression associated with diagnosis and prognosis of prostate cancer. Br J Cancer 100: 1608–1616. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2696760&tool=pmcentrez&rendertype=abstract. Accessed 11 June 2014. doi: 10.1038/sj.bjc.6605057 19401687

70. Sun Y, Wei M, Ren S-C, Chen R, Xu W-D, et al. (2014) Histone methyltransferase SETDB1 is required for prostate cancer cell proliferation, migration and invasion. Asian J Androl 16: 319–324. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3955348&tool=pmcentrez&rendertype=abstract. Accessed 11 June 2014. doi: 10.4103/1008-682X.122812 24556744

71. Tang F, Li W, Chen Y, Wang D, Han J, et al. (2014) Downregulation of hnRNP K by RNAi inhibits growth of human lung carcinoma cells. Oncol Lett 7: 1073–1077. Available: http://www.ncbi.nlm.nih.gov/pubmed/24944671. Accessed 20 June 2014. doi: 10.3892/ol.2014.1832 24944671

72. Rodriguez-Paredes M, Martinez de Paz a, Simó-Riudalbas L, Sayols S, Moutinho C, et al. (2014) Gene amplification of the histone methyltransferase SETDB1 contributes to human lung tumorigenesis. Oncogene 33: 2807–2813. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4031636&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1038/onc.2013.239 23770855

73. Chan QWT, Howes CG, Foster LJ (2006) Quantitative comparison of caste differences in honeybee hemolymph. Mol Cell Proteomics 5: 2252–2262. Available: http://www.ncbi.nlm.nih.gov/pubmed/16920818. Accessed 4 June 2014. doi: 10.1074/mcp.M600197-MCP200 16920818

74. Kristensen AR, Gsponer J, Foster LJ (2013) Protein synthesis rate is the predominant regulator of protein expression during differentiation. Mol Syst Biol 9: 689. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3792347&tool=pmcentrez&rendertype=abstract. Accessed 24 May 2014. doi: 10.1038/msb.2013.47 24045637

75. Yang L, Xia L, Wu DY, Wang H, Chansky HA, et al. (2002) Molecular cloning of ESET, a novel histone H3-specific methyltransferase that interacts with ERG transcription factor: 148–152.

76. Ostareck DH, Ostareck-Lederer a, Wilm M, Thiele BJ, Mann M, et al. (1997) mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3’ end. Cell 89: 597–606. Available: http://www.ncbi.nlm.nih.gov/pubmed/9160751. doi: 10.1016/S0092-8674(00)80241-X 9160751

77. Han M-H, Lin C, Meng S, Wang X (2010) Proteomics analysis reveals overlapping functions of clustered protocadherins. Mol Cell Proteomics 9: 71–83. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2808268&tool=pmcentrez&rendertype=abstract. Accessed 11 June 2014. doi: 10.1074/mcp.M900343-MCP200 19843561

78. Tanese N (1997) Small-scale density gradient sedimentation to separate and analyze multiprotein complexes. Methods 12: 224–234. Available: http://www.ncbi.nlm.nih.gov/pubmed/9237167. doi: 10.1006/meth.1997.0475 9237167

79. Abruzzi KC, Lacadie S, Rosbash M (2004) Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes. EMBO J 23: 2620–2631. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=449771&tool=pmcentrez&rendertype=abstract. Accessed 10 June 2014. doi: 10.1038/sj.emboj.7600261 15192704

80. Matunis MJ, Michael WM, Dreyfuss G (1992) Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein. Mol Cell Biol 12: 164–171. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=364080&tool=pmcentrez&rendertype=abstract 1729596

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#