Elongator complex influences telomeric gene silencing and DNA damage response by its role in wobble uridine tRNA modification

PLoS Genetics

Volumn 7, Issue 9, 2011, Pages

  Chen, Changchun ^a   Huang, Bo ^a,b   Eliasson, Mattias ^a   Rydén, Patrik ^a   Byström, Anders S ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATOR COMPLEX; GENE PRODUCT; GLUTAMIC ACID; GLUTAMINE; LYSINE; MUTANT PROTEIN; NUCLEOSIDE; REGULATOR PROTEIN; SIRTUIN 4; TRANSFER RNA; UNCLASSIFIED DRUG; URIDINE; CYCLINE; GLUTAMIC ACID TRANSFER RNA; GLUTAMINE TRANSFER RNA; LYSINE TRANSFER RNA; SILENT INFORMATION REGULATOR PROTEIN; SIR4 PROTEIN, S CEREVISIAE;

ALLELE; ARTICLE; CHROMATIN; DNA DAMAGE; ELP3 GENE; GENE; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; TELOMERE; TRANSFER RNA MODIFICATION; TUC2 GENE; WILD TYPE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MUTATION; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

CHROMATIN; DNA DAMAGE; GENE EXPRESSION REGULATION; GENE SILENCING; HUMANS; MUTATION; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BIOSYNTHESIS; RNA, TRANSFER; RNA, TRANSFER, GLN; RNA, TRANSFER, GLU; RNA, TRANSFER, LYS; SACCHAROMYCES CEREVISIAE; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; TELOMERE;

EID: 80053461006     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002258     Document Type: Article

References (45)

1. Otero G, Fellows J, Li Y, de Bizemont T, Dirac AM, et al. (1999) Elongator, a multisubunit component of a novel RNA polymerase II holoenzyme for transcriptional elongation. Mol Cell 3: 109-118.
2. Winkler GS, Petrakis TG, Ethelberg S, Tokunaga M, Erdjument-Bromage H, et al. (2001) RNA polymerase II elongator holoenzyme is composed of two discrete subcomplexes. J Biol Chem 276: 32743-32749.
3. Krogan NJ, Greenblatt JF, (2001) Characterization of a six-subunit holo-elongator complex required for the regulated expression of a group of genes in Saccharomyces cerevisiae. Mol Cell Biol 21: 8203-8212.
4. Hawkes NA, Otero G, Winkler GS, Marshall N, Dahmus ME, et al. (2002) Purification and characterization of the human elongator complex. J Biol Chem 277: 3047-3052.
5. Kim JH, Lane WS, Reinberg D, (2002) Human Elongator facilitates RNA polymerase II transcription through chromatin. Proc Natl Acad Sci U S A 99: 1241-1246.
6. Wittschieben BO, Otero G, de Bizemont T, Fellows J, Erdjument-Bromage H, et al. (1999) A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme. Mol Cell 4: 123-128.
7. Winkler GS, Kristjuhan A, Erdjument-Bromage H, Tempst P, Svejstrup JQ, (2002) Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc Natl Acad Sci U S A 99: 3517-3522.
8. Rahl PB, Chen CZ, Collins RN, (2005) Elp1p, the yeast homolog of the FD disease syndrome protein, negatively regulates exocytosis independently of transcriptional elongation. Mol Cell 17: 841-853.
9. Frohloff F, Fichtner L, Jablonowski D, Breunig KD, Schaffrath R, (2001) Saccharomyces cerevisiae Elongator mutations confer resistance to the Kluyveromyces lactis zymocin. EMBO J 20: 1993-2003.
10. Huang B, Johansson MJ, Byström AS, (2005) An early step in wobble uridine tRNA modification requires the Elongator complex. RNA 11: 424-436.
11. Lu J, Huang B, Esberg A, Johansson MJ, Byström AS, (2005) The Kluyveromyces lactis gamma-toxin targets tRNA anticodons. RNA 11: 1648-1654.
12. Johansson MJ, Esberg A, Huang B, Björk GR, Byström AS, (2008) Eukaryotic wobble uridine modifications promote a functionally redundant decoding system. Mol Cell Biol.
13. Chen C, Tuck S, Byström AS, (2009) Defects in tRNA modification associated with neurological and developmental dysfunctions in Caenorhabditis elegans elongator mutants. PLoS Genet 5: e1000561 doi:10.1371/journal.pgen.1000561.
14. Mehlgarten C, Jablonowski D, Wrackmeyer U, Tschitschmann S, Sondermann D, et al. (2010) Elongator function in tRNA wobble uridine modification is conserved between yeast and plants. Mol Microbiol 76: 1082-1094.
15. Esberg A, Huang B, Johansson MJ, Byström AS, (2006) Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol Cell 24: 139-148.
16. Campos EI, Reinberg D, (2009) Histones: annotating chromatin. Annu Rev Genet 43: 559-599.
17. Clapier CR, Cairns BR, (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304.
18. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE, (2001) Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res 29: 1097-1106.
19. Li Q, Fazly AM, Zhou H, Huang S, Zhang Z, et al. (2009) The elongator complex interacts with PCNA and modulates transcriptional silencing and sensitivity to DNA damage agents. PLoS Genet 5: e1000684 doi:10.1371/journal.pgen.1000684.
20. Gottschling DE, Aparicio OM, Billington BL, Zakian VA, (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63: 751-762.
21. Fillingham J, Recht J, Silva AC, Suter B, Emili A, et al. (2008) Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol 28: 4342-4353.
22. Lin LJ, Minard LV, Johnston GC, Singer RA, Schultz MC, (2010) Asf1 can promote trimethylation of H3 K36 by Set2. Mol Cell Biol 30: 1116-1129.
23. Tsubota T, Berndsen CE, Erkmann JA, Smith CL, Yang L, et al. (2007) Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. Mol Cell 25: 703-712.
24. Grant PA, Duggan L, Cote J, Roberts SM, Brownell JE, et al. (1997) Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 11: 1640-1650.
25. Eberharter A, Sterner DE, Schieltz D, Hassan A, Yates JR, 3rd, et al. (1999) The ADA complex is a distinct histone acetyltransferase complex in Saccharomyces cerevisiae. Mol Cell Biol 19: 6621-6631.
26. Wittschieben BO, Fellows J, Du W, Stillman DJ, Svejstrup JQ, (2000) Overlapping roles for the histone acetyltransferase activities of SAGA and elongator in vivo. EMBO J 19: 3060-3068.
27. Keeling KM, Lanier J, Du M, Salas-Marco J, Gao L, et al. (2004) Leaky termination at premature stop codons antagonizes nonsense-mediated mRNA decay in S. cerevisiae. RNA 10: 691-703.
28. Björk GR, Huang B, Persson OP, Byström AS, (2007) A conserved modified wobble nucleoside (mcm5s2U) in lysyl-tRNA is required for viability in yeast. RNA 13: 1245-1255.
29. Pokholok DK, Hannett NM, Young RA, (2002) Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol Cell 9: 799-809.
30. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691.
31. Begley U, Dyavaiah M, Patil A, Rooney JP, DiRenzo D, et al. (2007) Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 28: 860-870.
32. Close P, Hawkes N, Cornez I, Creppe C, Lambert CA, et al. (2006) Transcription impairment and cell migration defects in elongator-depleted cells: implication for familial dysautonomia. Mol Cell 22: 521-531.
33. Holmberg C, Katz S, Lerdrup M, Herdegen T, Jaattela M, et al. (2002) A novel specific role for I kappa B kinase complex-associated protein in cytosolic stress signaling. J Biol Chem 277: 31918-31928.
34. Nelissen H, Fleury D, Bruno L, Robles P, De Veylder L, et al. (2005) The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc Natl Acad Sci U S A 102: 7754-7759.
35. Creppe C, Malinouskaya L, Volvert ML, Gillard M, Close P, et al. (2009) Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136: 551-564.
36. Solinger JA, Paolinelli R, Kloss H, Scorza FB, Marchesi S, et al. (2010) The Caenorhabditis elegans Elongator complex regulates neuronal alpha-tubulin acetylation. PLoS Genet 6: e1000820 doi:10.1371/journal.pgen.1000820.
37. Akella JS, Wloga D, Kim J, Starostina NG, Lyons-Abbott S, et al. (2010) MEC-17 is an alpha-tubulin acetyltransferase. Nature 467: 218-222.
38. Paraskevopoulou C, Fairhurst SA, Lowe DJ, Brick P, Onesti S, (2006) The Elongator subunit Elp3 contains a Fe4S4 cluster and binds S-adenosylmethionine. Mol Microbiol 59: 795-806.
39. Greenwood C, Selth LA, Dirac-Svejstrup AB, Svejstrup JQ, (2009) An iron-sulfur cluster domain in Elp3 important for the structural integrity of elongator. J Biol Chem 284: 141-149.
40. Burke D, Dawson D, Stearns T, (2000) Methods in Yeast Genetics Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
41. Björk GR, Jacobsson K, Nilsson K, Johansson MJ, Byström AS, et al. (2001) A primordial tRNA modification required for the evolution of life? EMBO J 20: 231-239.
42. He F, Amrani N, Johansson MJ, Jacobson A, (2008) Chapter 6. Qualitative and quantitative assessment of the activity of the yeast nonsense-mediated mRNA decay pathway. Methods Enzymol 449: 127-147.
43. Fiorentini P, Huang KN, Tishkoff DX, Kolodner RD, Symington LS, (1997) Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol 17: 2764-2773.
44. Sikorski RS, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
45. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P, (1992) Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.