BEND3 represses rDNA transcription by stabilizing a NoRC component via USP21 deubiquitinase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 27, 2015, Pages 8338-8343

  Khan, Abid ^a   Giri, Sumanprava ^a   Wang, Yating ^a   Chakraborty, Arindam ^a   Ghosh, Archit K ^a   Anantharaman, Aparna ^a   Aggarwal, Vasudha ^a   Sathyan, Kizhakke M ^a   Ha, Taekjip ^a,b,c   Prasanth, Kannanganattu V ^a   Prasanth, Supriya G ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

BEND3; NoRC; rDNA; Tip5; Transcription repression

Indexed keywords

BEND3 PROTEIN; DEUBIQUITINASE; NUCLEAR PROTEIN; NUCLEOLAR REMODELING COMPLEX; REPRESSOR PROTEIN; RIBOSOME DNA; UBIQUITIN SPECIFIC PROTEASE 21; UNCLASSIFIED DRUG; BAZ2A PROTEIN, HUMAN; BEND3 PROTEIN, HUMAN; HISTONE; LYSINE; NONHISTONE PROTEIN; PROTEIN BINDING; UBIQUITIN THIOLESTERASE; USP21 PROTEIN, HUMAN;

ACROCENTRIC CHROMOSOME; ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; CHROMOSOME 13; CHROMOSOME 14; CHROMOSOME 15; CHROMOSOME 21; CHROMOSOME 22; CONTROLLED STUDY; CROSS LINKING; DNA TRANSCRIPTION; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC ASSOCIATION; GENETIC STABILITY; HUMAN; IMMUNOPRECIPITATION; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROCESSING; SOUTHERN BLOTTING; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHYLATION; NUCLEOLUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SUMOYLATION; TUMOR CELL LINE; WESTERN BLOTTING;

EUKARYOTA; MAMMALIA;

BLOTTING, WESTERN; CELL LINE, TUMOR; CELL NUCLEOLUS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA, RIBOSOMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; LYSINE; METHYLATION; MICROSCOPY, FLUORESCENCE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SUMOYLATION; UBIQUITIN THIOLESTERASE;

EID: 84935515910     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1424705112     Document Type: Article

References (47)

1. Grummt I (2003) Life on a planet of its own: Regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17(14):1691-1702.
2. Grummt I (2007) Different epigenetic layers engage in complex crosstalk to define the epigenetic state of mammalian rRNA genes. Hum Mol Genet 16(Spec No 1):R21-R27.
3. Grummt I, Pikaard CS (2003) Epigenetic silencing of RNA polymerase I transcription. Nat Rev Mol Cell Biol 4(8):641-649.
4. Lawrence RJ, Pikaard CS (2004) Chromatin turn ons and turn offs of ribosomal RNA genes. Cell Cycle 3(7):880-883.
5. McStay B (2006) Nucleolar dominance: A model for rRNA gene silencing. Genes Dev 20(10):1207-1214.
6. McStay B, Grummt I (2008) The epigenetics of rRNA genes: From molecular to chromosome biology. Annu Rev Cell Dev Biol 24:131-157.
7. Strohner R, et al. (2001) NoRC: A novel member of mammalian ISWI-containing chromatin remodeling machines. EMBO J 20(17):4892-4900.
8. Strohner R, et al. (2004) Recruitment of the nucleolar remodeling complex NoRC establishes ribosomal DNA silencing in chromatin. Mol Cell Biol 24(4):1791-1798.
9. Santoro R, Li J, Grummt I (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet 32(3):393-396.
10. Zhou Y, Santoro R, Grummt I (2002) The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J 21(17):4632-4640.
11. Sathyan KM, Shen Z, Tripathi V, Prasanth KV, Prasanth SG (2011) A BEN-domaincontaining protein associates with heterochromatin and represses transcription. J Cell Sci 124(Pt 18):3149-3163.
12. Abhiman S, Iyer LM, Aravind L (2008) BEN: A novel domain in chromatin factors and DNA viral proteins. Bioinformatics 24(4):458-461.
13. Korutla L, Degnan R, Wang P, Mackler SA (2007) NAC1, a cocaine-regulated POZ/BTB protein interacts with CoREST. J Neurochem 101(3):611-618.
14. Sreenath K, et al. (2010) Nuclear matrix protein SMAR1 represses HIV-1 LTR mediated transcription through chromatin remodeling. Virology 400(1):76-85.
15. Saksouk N, et al. (2014) Redundant mechanisms to form silent chromatin at pericentromeric regions rely on BEND3 and DNA methylation. Mol Cell 56(4):580-594.
16. Dai Q, et al. (2013) BEND6 is a nuclear antagonist of Notch signaling during selfrenewal of neural stem cells. Development 140(9):1892-1902.
17. Dai Q, et al. (2013) The BEN domain is a novel sequence-specific DNA-binding domain conserved in neural transcriptional repressors. Genes Dev 27(6):602-614.
18. Santoro R, Grummt I (2001) Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol Cell 8(3):719-725.
19. Conconi A, Widmer RM, Koller T, Sogo JM (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57(5):753-761.
20. Mayer C, Neubert M, Grummt I (2008) The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep 9(8):774-780.
21. Guetg C, Scheifele F, Rosenthal F, Hottiger MO, Santoro R (2012) Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol Cell 45(6):790-800.
22. Sowa ME, Bennett EJ, Gygi SP, Harper JW (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138(2):389-403.
23. Giri S, et al. (2015) The preRC protein ORCA organizes heterochromatin by assembling histone H3 lysine 9 methyltransferases on chromatin. eLife 4:4.
24. Jain A, et al. (2011) Probing cellular protein complexes using single-molecule pulldown. Nature 473(7348):484-488.
25. Narlikar GJ, Fan HY, Kingston RE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108(4):475-487.
26. Grewal SI, Elgin SC (2007) Transcription and RNA interference in the formation of heterochromatin. Nature 447(7143):399-406.
27. Grewal SI, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8(1):35-46.
28. Guetg C, et al. (2010) The NoRC complex mediates the heterochromatin formation and stability of silent rRNA genes and centromeric repeats. EMBO J 29(13):2135-2146.
29. Komander D, Clague MJ, Urbé S (2009) Breaking the chains: Structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10(8):550-563.
30. Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363-397.
31. Reyes-Turcu FE, Wilkinson KD (2009) Polyubiquitin binding and disassembly by deubiquitinating enzymes. Chem Rev 109(4):1495-1508.
32. Ye Y, Scheel H, Hofmann K, Komander D (2009) Dissection of USP catalytic domains reveals five common insertion points. Mol Biosyst 5(12):1797-1808.
33. Nijman SM, et al. (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123(5):773-786.
34. Nakagawa T, et al. (2008) Deubiquitylation of histone H2A activates transcriptional initiation via trans-histone cross-talk with H3K4 di- and trimethylation. Genes Dev 22(1):37-49.
35. Fan Y, et al. (2014) USP21 negatively regulates antiviral response by acting as a RIG-I deubiquitinase. J Exp Med 211(2):313-328.
36. Zhang J, et al. (2013) Identification of the E3 deubiquitinase ubiquitin-specific peptidase 21 (USP21) as a positive regulator of the transcription factor GATA3. J Biol Chem 288(13):9373-9382.
37. Xu G, et al. (2010) Ubiquitin-specific peptidase 21 inhibits tumor necrosis factor alphainduced nuclear factor kappaB activation via binding to and deubiquitinating receptor-interacting protein 1. J Biol Chem 285(2):969-978.
38. Kessler BM, Edelmann MJ (2011) PTMs in conversation: Activity and function of deubiquitinating enzymes regulated via post-translational modifications. Cell Biochem Biophys 60(1-2):21-38.
39. Postepska-Igielska A, Grummt I (2014) NoRC silences rRNA genes, telomeres, and centromeres. Cell Cycle 13(4):493-494.
40. Mayer C, Schmitz KM, Li J, Grummt I, Santoro R (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 22(3):351-361.
41. Frescas D, Guardavaccaro D, Bassermann F, Koyama-Nasu R, Pagano M (2007) JHDM1B/FBXL10 is a nucleolar protein that represses transcription of ribosomal RNA genes. Nature 450(7167):309-313.
42. Tripathi V, et al. (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39(6): 925-938.
43. Pietrzak M, Rempala G, Nelson PT, Zheng JJ, Hetman M (2011) Epigenetic silencing of nucleolar rRNA genes in Alzheimer's disease. PLoS ONE 6(7):e22585.
44. Tan BC, et al. (2012) Epigeneitc silencing of ribosomal RNA genes by Mybbp1a. J Biomed Sci 19:57.
45. Zentner GE, Saiakhova A, Manaenkov P, Adams MD, Scacheri PC (2011) Integrative genomic analysis of human ribosomal DNA. Nucleic Acids Res 39(12):4949-4960.
46. Gagnon-Kugler T, Langlois F, Stefanovsky V, Lessard F, Moss T (2009) Loss of human ribosomal gene CpG methylation enhances cryptic RNA polymerase II transcription and disrupts ribosomal RNA processing. Mol Cell 35(4):414-425.
47. Cong R, et al. (2012) Interaction of nucleolin with ribosomal RNA genes and its role in RNA polymerase I transcription. Nucleic Acids Res 40(19):9441-9454.