Raf1 is a DCAF for the Rik1 DDB1-like protein and has separable roles in siRNA generation and chromatin modification

PLoS Genetics

Volumn 8, Issue 2, 2012, Pages

  Buscaino, Alessia ^a   White, Sharon A ^a   Houston, Douglas R ^a   Lejeune, Erwan ^a   Simmer, Femke ^a,c   de Lima Alves, Flavia ^a   Diyora, Piyush T ^a   Urano, Takeshi ^b   Bayne, Elizabeth H ^a,d   Rappsilber, Juri ^a   Allshire, Robin C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CHROMOSOME PROTEIN; HISTONE H3; HISTONE METHYLTRANSFERASE; PROTEIN CLRC; PROTEIN RAF1; RIK1 DDB1 LIKE PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CLR4 PROTEIN, S POMBE; CLR7 PROTEIN, S POMBE; DDB1 PROTEIN, S POMBE; DNA BINDING PROTEIN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; METHYLTRANSFERASE; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN; RAF PROTEIN; RIK1 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN; SLP1 PROTEIN, S POMBE; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CENTROMERE; CHROMATIN; GENE AMPLIFICATION; GENE MUTATION; GENETIC TRANSCRIPTION; HISTONE METHYLATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN MOTIF; RNA INTERFERENCE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETICS; HETEROCHROMATIN; HUMAN; METABOLISM; METHYLATION; MUTATION; PROTEIN PROCESSING; SCHIZOSACCHAROMYCES; STRUCTURAL HOMOLOGY; UBIQUITINATION;

SCHIZOSACCHAROMYCETACEAE;

CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; METHYLATION; METHYLTRANSFERASES; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-RAF; RNA, SMALL INTERFERING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84859166140     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002499     Document Type: Article

References (56)

1. Farazi TA, Juranek SA, Tuschl T, (2008) The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 135: 1201-1214.
2. Grewal SI, (2010) RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 20: 134-141.
3. Moazed D, (2009) Small RNAs in transcriptional gene silencing and genome defence. Nature 457: 413-420.
4. Guang S, Bochner AF, Burkhart KB, Burton N, Pavelec DM, et al. (2010) Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription. Nature 465: 1097-1101.
5. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, et al. (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908-917.
6. Allshire RC, Javerzat JP, Redhead NJ, Cranston G, (1994) Position effect variegation at fission yeast centromeres. Cell 76: 157-169.
7. Djupedal I, Portoso M, Spahr H, Bonilla C, Gustafsson CM, et al. (2005) RNA Pol II subunit Rpb7 promotes centromeric transcription and RNAi-directed chromatin silencing. Genes Dev 19: 2301-2306.
8. Kato H, Goto DB, Martienssen RA, Urano T, Furukawa K, et al. (2005) RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science 309: 467-469.
9. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, et al. (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837.
10. Bayne EH, White SA, Kagansky A, Bijos DA, Sanchez-Pulido L, et al. (2010) Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140: 666-677.
11. Sadaie M, Iida T, Urano T, Nakayama J, (2004) A chromodomain protein, Chp1, is required for the establishment of heterochromatin in fission yeast. Embo J 23: 3825-3835.
12. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, et al. (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124.
13. Zhang K, Mosch K, Fischle W, Grewal SI, (2008) Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat Struct Mol Biol 15: 381-388.
14. Petrie VJ, Wuitschick JD, Givens CD, Kosinski AM, Partridge JF, (2005) RNA interference (RNAi)-dependent and RNAi-independent association of the Chp1 chromodomain protein with distinct heterochromatic loci in fission yeast. Mol Cell Biol 25: 2331-2346.
15. Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, et al. (2007) SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128: 491-504.
16. Buhler M, Verdel A, Moazed D, (2006) Tethering RITS to a nascent transcript initiates RNAi- and heterochromatin-dependent gene silencing. Cell 125: 873-886.
17. Hong EJ, Villen J, Gerace EL, Gygi SP, Moazed D, (2005) A cullin E3 ubiquitin ligase complex associates with Rik1 and the Clr4 histone H3-K9 methyltransferase and is required for RNAi-mediated heterochromatin formation. RNA Biol 2: 106-111.
18. Motamedi MR, Verdel A, Colmenares SU, Gerber SA, Gygi SP, et al. (2004) Two RNAi complexes, RITS and RDRC, physically interact and localise to noncoding centromeric RNAs. Cell 119: 789-802.
19. Noma K, Sugiyama T, Cam H, Verdel A, Zofall M, et al. (2004) RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat Genet 36: 1174-1180.
20. Djupedal I, Kos-Braun IC, Mosher RA, Soderholm N, Simmer F, et al. (2009) Analysis of small RNA in fission yeast; centromeric siRNAs are potentially generated through a structured RNA. EMBO J 28: 3832-3844.
21. Gerace EL, Halic M, Moazed D, (2010) The methyltransferase activity of Clr4Suv39h triggers RNAi independently of histone H3K9 methylation. Mol Cell 39: 360-372.
22. Jia S, Kobayashi R, Grewal SI, (2005) Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat Cell Biol 7: 1007-1013.
23. Li F, Goto DB, Zaratiegui M, Tang X, Martienssen R, et al. (2005) Two novel proteins, dos1 and dos2, interact with rik1 to regulate heterochromatic RNA interference and histone modification. Curr Biol 15: 1448-1457.
24. Horn PJ, Bastie JN, Peterson CL, (2005) A Rik1-associated, cullin-dependent E3 ubiquitin ligase is essential for heterochromatin formation. Genes Dev 19: 1705-1714.
25. Thon G, Hansen KR, Altes SP, Sidhu D, Singh G, et al. (2005) The Clr7 and Clr8 directionality factors and the Pcu4 cullin mediate heterochromatin formation in the fission yeast Schizosaccharomyces pombe. Genetics 171: 1583-1595.
26. Jackson S, Xiong Y, (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem Sci 34: 562-570.
27. Shilatifard A, (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269.
28. Petroski MD, Deshaies RJ, (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6: 9-20.
29. Kapetanaki MG, Guerrero-Santoro J, Bisi DC, Hsieh CL, Rapic-Otrin V, et al. (2006) The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc Natl Acad Sci U S A 103: 2588-2593.
30. Wang H, Zhai L, Xu J, Joo HY, Jackson S, et al. (2006) Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 22: 383-394.
31. Higa LA, Wu M, Ye T, Kobayashi R, Sun H, et al. (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD-40-repeat proteins and regulates histone methylation. Nat Cell Biol 8: 1277-1283.
32. Jin J, Arias EE, Chen J, Harper JW, Walter JC, (2006) A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol Cell 23: 709-721.
33. Angers S, Li T, Yi X, MacCoss MJ, Moon RT, et al. (2006) Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443: 590-593.
34. He YJ, McCall CM, Hu J, Zeng Y, Xiong Y, (2006) DDB1 functions as a linker to recruit receptor WD-40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev 20: 2949-2954.
35. Liu C, Powell KA, Mundt K, Wu L, Carr AM, et al. (2003) Cop9/signalosome subunits and Pcu4 regulate ribonucleotide reductase by both checkpoint-dependent and-independent mechanisms. Genes Dev 17: 1130-1140.
36. Neuwald AF, Poleksic A, (2000) PSI-BLAST searches using hidden markov models of structural repeats: prediction of an unusual sliding DNA clamp and of beta-propellers in UV-damaged DNA-binding protein. Nucleic Acids Res 28: 3570-3580.
37. Braun S, Garcia JF, Rowley M, Rougemaille M, Shankar S, et al. (2011) The cul4-ddb1(cdt2) ubiquitin ligase inhibits invasion of a boundary-associated antisilencing factor into heterochromatin. Cell 144: 41-54.
38. Pidoux AL, Uzawa S, Perry PE, Cande WZ, Allshire RC, (2000) Live analysis of lagging chromosomes during anaphase and their effect on spindle elongation rate in fission yeast. J Cell Sci 113 Pt 23: 4177-4191.
39. Li F, Huarte M, Zaratiegui M, Vaughn MW, Shi Y, et al. (2008) Lid2 is required for coordinating H3K4 and H3K9 methylation of heterochromatin and euchromatin. Cell 135: 272-283.
40. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, et al. (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294: 2539-2542.
41. Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, et al. (2002) Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 4: 89-93.
42. Ekwall K, Javerzat JP, Lorentz A, Schmidt H, Cranston G, et al. (1995) The chromodomain protein Swi6: a key component at fission yeast centromeres. Science 269: 1429-1431.
43. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, et al. (2002) Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237.
44. Scrima A, Konickova R, Czyzewski BK, Kawasaki Y, Jeffrey PD, et al. (2008) Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135: 1213-1223.
45. Han Z, Guo L, Wang H, Shen Y, Deng XW, et al. (2006) Structural basis for the specific recognition of methylated histone H3 lysine 4 by the WD-40 protein WDR5. Mol Cell 22: 137-144.
46. Couture JF, Collazo E, Trievel RC, (2006) Molecular recognition of histone H3 by the WD-40 protein WDR5. Nat Struct Mol Biol 13: 698-703.
47. Schuetz A, Allali-Hassani A, Martin F, Loppnau P, Vedadi M, et al. (2006) Structural basis for molecular recognition and presentation of histone H3 by WDR5. EMBO J 25: 4245-4252.
48. Zhang K, Fischer T, Porter RL, Dhakshnamoorthy J, Zofall M, et al. (2011) Clr4/Suv39 and RNA quality control factors cooperate to trigger RNAi and suppress antisense RNA. Science 331: 1624-1627.
49. Li F, Martienssen R, Cande WZ, (2011) Coordination of DNA replication and histone modification by the Rik1-Dos2 complex. Nature 475: 244-248.
50. Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, et al. (2008) Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451: 734-737.
51. Kloc A, Zaratiegui M, Nora E, Martienssen R, (2008) RNA interference guides histone modification during the S phase of chromosomal replication. Curr Biol 18: 490-495.
52. Kagansky A, Folco HD, Almeida R, Pidoux AL, Boukaba A, et al. (2009) Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science 324: 1716-1719.
53. Moreno S, Klar A, Nurse P, (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823.
54. Pidoux A, Mellone B, Allshire R, (2004) Analysis of chromatin in fission yeast. Methods 33: 252-259.
55. Oeffinger M, Wei KE, Rogers R, DeGrasse JA, Chait BT, et al. (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat Methods 4: 951-956.
56. Bayne EH, Portoso M, Kagansky A, Kos-Braun IC, Urano T, et al. (2008) Splicing factors facilitate RNAi-directed silencing in fission yeast. Science 322: 602-606.