Cohesin proteins promote ribosomal RNA production and protein translation in yeast and human cells

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Bose, Tania ^a   Lee, Kenneth K ^a   Lu, Shuai ^a,b   Xu, Baoshan ^a   Harris, Bethany ^a   Slaughter, Brian ^a   Unruh, Jay ^a   Garrett, Alexander ^a   McDowell, William ^a   Box, Andrew ^a   Li, Hua ^a   Peak, Allison ^a   Ramachandran, Sree ^a   Seidel, Chris ^a   Gerton, Jennifer L ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; INITIATION FACTOR 2; METHIONINE; RIBOSOME RNA; SULFUR 35; TRANSCRIPTION FACTOR GCN4; ACYLTRANSFERASE; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CELL CYCLE PROTEIN; COHESINS; ECO1 PROTEIN, S CEREVISIAE; GCN4 PROTEIN, S CEREVISIAE; NONHISTONE PROTEIN; NUCLEAR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; STRUCTURAL MAINTENANCE OF CHROMOSOME PROTEIN 1;

ARTICLE; BIOGENESIS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; FIBROBLAST CULTURE; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCUS; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RIBOSOME; RNA GENE; RNA SYNTHESIS; ROBERTS SYNDROME; UPREGULATION; YEAST CELL; BIOSYNTHESIS; CELL LINE; CRANIOFACIAL MALFORMATION; FIBROBLAST; GENETICS; HYPERTELORISM; METABOLISM; MUTATION; PHOCOMELIA; POLYSOME; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCETALES;

ACETYLTRANSFERASES; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL CYCLE PROTEINS; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; CRANIOFACIAL ABNORMALITIES; ECTROMELIA; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; HYPERTELORISM; MUTATION; NUCLEAR PROTEINS; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84864051677     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002749     Document Type: Article

References (69)

1. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, et al. (2000) Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5: 243-254.
2. Gillespie PJ, Hirano T, (2004) Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol 14: 1598-1603.
3. Takahashi TS, Yiu P, Chou MF, Gygi S, Walter JC, (2004) Recruitment of Xenopus Scc2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol 6: 991-996.
4. Ben-Shahar TR, Heeger S, Lehane C, East P, Flynn H, et al. (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321: 563-566.
5. Zhang J, Shi X, Li Y, Kim BJ, Jia J, et al. (2008) Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell 31: 143-151.
6. Rowland BD, Roig MB, Nishino T, Kurze A, Uluocak P, et al. (2009) Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity. Mol Cell 33: 763-774.
7. Hartman T, Stead K, Koshland D, Guacci V, (2000) Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae. J Cell Biol 151: 613-626.
8. Panizza S, Tanaka T, Hochwagen A, Eisenhaber F, Nasmyth K, (2000) Pds5 cooperates with cohesin in maintaining sister chromatid cohesion. Curr Biol 10: 1557-1564.
9. Deardorff MA, Kaur M, Yaeger D, Rampuria A, Korolev S, et al. (2007) Mutations in cohesin complex members SMC3 and SMC1A cause a mild variant of cornelia de Lange syndrome with predominant mental retardation. Am J Hum Genet 80: 485-494.
10. Musio A, Selicorni A, Focarelli ML, Gervasini C, Milani D, et al. (2006) X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet 38: 528-530.
11. Krantz ID, McCallum J, DeScipio C, Kaur M, Gillis LA, et al. (2004) Cornelia de Lange syndrome is caused by mutations in NIPBL, the human homolog of Drosophila melanogaster Nipped-B. Nat Genet 36: 631-635.
12. Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T, (2004) NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet 36: 636-641.
13. Vega H, Waisfisz Q, Gordillo M, Sakai N, Yanagihara I, et al. (2005) Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat Genet 37: 468-470.
14. Liu J, Krantz ID, (2008) Cohesin and human disease. Annu Rev Genomics Hum Genet 9: 303-320.
15. Schule B, Oviedo A, Johnston K, Pai S, Francke U, (2005) Inactivating mutations in ESCO2 cause SC phocomelia and Roberts syndrome: no phenotype-genotype correlation. Am J Hum Genet 77: 1117-1128.
16. Gard S, Light W, Xiong B, Bose T, McNairn AJ, et al. (2009) Cohesinopathy mutations disrupt the subnuclear organization of chromatin. Journal of Cell Biology 187: 455-462.
17. Lu S, Goering M, Gard S, Xiong B, McNairn AJ, et al. (2010) Eco1 is important for DNA damage repair in S. cerevisiae. Cell Cycle 9.
18. Xiong B, Lu S, Gerton JL, (2010) Hos1 is a lysine deacetylase for the Smc3 subunit of cohesin. Curr Biol 20: 1660-1665.
19. D'Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, et al. (2008) Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22: 2215-2227.
20. Laferte A, Favry E, Sentenac A, Riva M, Carles C, et al. (2006) The transcriptional activity of RNA polymerase I is a key determinant for the level of all ribosome components. Genes Dev 20: 2030-2040.
21. Wang L, Haeusler RA, Good PD, Thompson M, Nagar S, et al. (2005) Silencing near tRNA genes requires nucleolar localization. J Biol Chem 280: 8637-8639.
22. Conesa C, Ruotolo R, Soularue P, Simms TA, Donze D, et al. (2005) Modulation of yeast genome expression in response to defective RNA polymerase III-dependent transcription. Mol Cell Biol 25: 8631-8642.
23. Berriz GF, Beaver JE, Cenik C, Tasan M, Roth FP, (2009) Next generation software for functional trend analysis. Bioinformatics 25: 3043-3044.
24. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
25. Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, et al. (2001) Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol Cell Biol 21: 4347-4368.
26. Lieb JD, Liu X, Botstein D, Brown PO, (2001) Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat Genet 28: 327-334.
27. Dever TE, (1997) Using GCN4 as a reporter of eIF2 alpha phosphorylation and translational regulation in yeast. Methods 11: 403-417.
28. Hinnebusch AG, (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59: 407-450.
29. Mueller PP, Harashima S, Hinnebusch AG, (1987) A segment of GCN4 mRNA containing the upstream AUG codons confers translational control upon a heterologous yeast transcript. Proc Natl Acad Sci U S A 84: 2863-2867.
30. Dever TE, Feng L, Wek RC, Cigan AM, Donahue TF, et al. (1992) Phosphorylation of initiation factor 2 alpha by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68: 585-596.
31. Lee B, Udagawa T, Singh CR, Asano K, (2007) Yeast phenotypic assays on translational control. Methods Enzymol 429: 105-137.
32. Asano K, Krishnamoorthy T, Phan L, Pavitt GD, Hinnebusch AG, (1999) Conserved bipartite motifs in yeast eIF5 and eIF2Bepsilon, GTPase-activating and GDP-GTP exchange factors in translation initiation, mediate binding to their common substrate eIF2. EMBO J 18: 1673-1688.
33. Hurt E, Hannus S, Schmelzl B, Lau D, Tollervey D, et al. (1999) A novel in vivo assay reveals inhibition of ribosomal nuclear export in ran-cycle and nucleoporin mutants. J Cell Biol 144: 389-401.
34. Li Z, Lee I, Moradi E, Hung NJ, Johnson AW, et al. (2009) Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS Biol 7: e1000213 doi:10.1371/journal.pbio.1000213.
35. Guacci V, Koshland D, Strunnikov A, (1997) A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91: 47-57.
36. Sjogren C, Nasmyth K, (2001) Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr Biol 11: 991-995.
37. D'Ambrosio C, Kelly G, Shirahige K, Uhlmann F, (2008) Condensin-dependent rDNA decatenation introduces a temporal pattern to chromosome segregation. Curr Biol 18: 1084-1089.
38. Clemente-Blanco A, Mayan-Santos M, Schneider DA, Machin F, Jarmuz A, et al. (2009) Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature 458: 219-222.
39. Ide S, Miyazaki T, Maki H, Kobayashi T, (2010) Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327: 693-696.
40. Zou H, Rothstein R, (1997) Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 90: 87-96.
41. Laloraya S, Guacci V, Koshland D, (2000) Chromosomal addresses of the cohesin component Mcd1p. J Cell Biol 151: 1047-1056.
42. Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, et al. (2004) Genome-Wide Mapping of the Cohesin Complex in the Yeast Saccharomyces cerevisiae. PLoS Biol 2: e259 doi:10.1371/journal.pbio.0020259.
43. Dammann R, Lucchini R, Koller T, Sogo JM, (1993) Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res 21: 2331-2338.
44. Tan RZ, van Oudenaarden A, (2010) Transcript counting in single cells reveals dynamics of rDNA transcription. Mol Syst Biol 6: 358.
45. van der Lelij P, Godthelp BC, van Zon W, van Gosliga D, Oostra AB, et al. (2009) The cellular phenotype of Roberts syndrome fibroblasts as revealed by ectopic expression of ESCO2. PLoS ONE 4: e6936 doi:10.1371/journal.pone.0006936.
46. Schaaf CA, Misulovin Z, Sahota G, Siddiqui AM, Schwartz YB, et al. (2009) Regulation of the Drosophila Enhancer of split and invected-engrailed gene complexes by sister chromatid cohesion proteins. PLoS ONE 4: e6202 doi:10.1371/journal.pone.0006202.
47. Liu J, Zhang Z, Bando M, Itoh T, Deardorff MA, et al. (2009) Transcriptional dysregulation in NIPBL and cohesin mutant human cells. PLoS Biol 7: e1000119 doi:10.1371/journal.pbio.1000119.
48. Kawauchi S, Calof AL, Santos R, Lopez-Burks ME, Young CM, et al. (2009) Multiple organ system defects and transcriptional dysregulation in the Nipbl(+/-) mouse, a model of Cornelia de Lange Syndrome. PLoS Genet 5: e1000650 doi:10.1371/journal.pgen.1000650.
49. Rhodes JM, Bentley FK, Print CG, Dorsett D, Misulovin Z, et al. (2010) Positive regulation of c-Myc by cohesin is direct, and evolutionarily conserved. Dev Biol.
50. Wendt KS, Peters JM, (2009) How cohesin and CTCF cooperate in regulating gene expression. Chromosome Res 17: 201-214.
51. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature.
52. Rollins RA, Morcillo P, Dorsett D, (1999) Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152: 577-593.
53. Fay A, Misulovin Z, Li J, Schaaf CA, Gause M, et al. (2011) Cohesin selectively binds and regulates genes with paused RNA polymerase. Curr Biol 21: 1624-1634.
54. Skibbens RV, Marzillier J, Eastman L, (2010) Cohesins coordinate gene transcriptions of related function within Saccharomyces cerevisiae. Cell Cycle 9.
55. Monnich M, Kuriger Z, Print CG, Horsfield JA, (2011) A zebrafish model of Roberts syndrome reveals that Esco2 depletion interferes with development by disrupting the cell cycle. PLoS ONE 6: e20051 doi:10.1371/journal.pone.0020051.
56. Narla A, Ebert BL, (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood 115: 3196-3205.
57. Mayan M, Aragon L, (2010) Cis-interactions between non-coding ribosomal spacers dependent on RNAP-II separate RNAP-I and RNAP-III transcription domains. Cell Cycle 9: 4328-4337.
58. Terret M-E, Sherwood R, Rahman S, Qin J, Jallepalli PV, (2009) Cohesin acetylation speeds the replication fork. Nature 462: 231-234.
59. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
60. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
61. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108-110.
62. Kel AE, Gossling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, et al. (2003) MATCH: A tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31: 3576-3579.
63. Ramirez M, Wek RC, Hinnebusch AG, (1991) Ribosome association of GCN2 protein kinase, a translational activator of the GCN4 gene of Saccharomyces cerevisiae. Mol Cell Biol 11: 3027-3036.
64. Hillenmeyer ME, Ericson E, Davis RW, Nislow C, Koller D, et al. (2010) Systematic analysis of genome-wide fitness data in yeast reveals novel gene function and drug action. Genome Biol 11: R30.
65. Zhang Y, Sikes ML, Beyer AL, Schneider DA, (2009) The Paf1 complex is required for efficient transcription elongation by RNA polymerase I. Proc Natl Acad Sci U S A 106: 2153-2158.
66. Kang HA, Hershey JW, (1994) Effect of initiation factor eIF-5A depletion on protein synthesis and proliferation of Saccharomyces cerevisiae. J Biol Chem 269: 3934-3940.
67. Smith JS, Boeke JD, (1997) An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev 11: 241-254.
68. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, et al. (2010) Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468: 321-325.
69. Wang BD, Eyre D, Basrai M, Lichten M, Strunnikov A, (2005) Condensin binding at distinct and specific chromosomal sites in the Saccharomyces cerevisiae genome. Mol Cell Biol 25: 7216-7225.