The C. Elegans dosage compensation complex mediates interphase X chromosome compaction

Epigenetics and Chromatin

Volumn 7, Issue 1, 2014, Pages

  Lau, Alyssa C ^a   Nabeshima, Kentaro ^b   Csankovszki, Györgyi ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Caenorhabditis elegans; Chromatin; Chromosome condensation; Condensin; Dosage compensation; Epigenetics; Gene expression; Interphase chromosome

Indexed keywords

CONDENSIN; CONDENSIN I; CONDENSIN II; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE; CHROMOSOME 1; CHROMOSOME CONDENSATION; CHROMOSOME SIZE; CHROMOSOME STRUCTURE; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE REPRESSION; HISTONE MODIFICATION; INTERPHASE; MALE; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; X CHROMOSOME COMPACTION;

EID: 84988958100     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-7-31     Document Type: Article

References (78)

1. Ohno S: Sex Chromosomes and Sex-Linked Genes. Berlin: Springer; 1967:1-140.
2. Conrad T, Akhtar A: Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat Rev Genet 2011, 13:123-134.
3. Ferrari F, Alekseyenko AA, Park PJ, Kuroda MI: Transcriptional control of a whole chromosome: emerging models for dosage compensation. Nat Struct Mol Biol 2014, 21:118-125.
4. Deng X, Berletch JB, Ma W, Nguyen DK, Hiatt JB, Noble WS, Shendure J, Disteche CM: Mammalian X upregulation is associated with enhanced transcription initiation, RNA half-life, and MOF-mediated H4K16 acetylation. Dev Cell 2013, 25:55-68.
5. Deng X, Hiatt JB, Nguyen DK, Ercan S, Sturgill D, Hillier LW, Schlesinger F, Davis CA, Reinke VJ, Gingeras TR, Shendure J, Waterston RH, Oliver B, Lieb JD, Disteche CM: Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat Genet 2011, 43:1179-1185.
6. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, Dudko OK, Malley JD, Eastman PS, Oliver B: Global analysis of X-chromosome dosage compensation. J Biol 2006, 5:3.
7. Lin H, Gupta V, Vermilyea MD, Falciani F, Lee JT, O'Neill LP, Turner BM: Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol 2007, 5:e326.
8. Lin H, Halsall JA, Antczak P, O'Neill LP, Falciani F, Turner BM: Relative overexpression of X-linked genes in mouse embryonic stem cells is consistent with Ohno's hypothesis. Nat Genet 2011, 43:1169-1170. author reply 1171-1162.
9. Barakat TS, Gribnau J: X chromosome inactivation in the cycle of life. Development 2012, 139:2085-2089.
10. Heard E, Disteche CM: Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 2006, 20:1848-1867.
11. Payer B, Lee JT: X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 2008, 42:733-772.
12. Csankovszki G, Petty EL, Collette KS: The worm solution: a chromosomefull of condensin helps gene expression go down. Chromosome Res 2009, 17:621-635.
13. Meyer BJ: Targeting X chromosomes for repression. Curr Opin Genet Dev 2010, 20:179-189.
14. Chuang PT, Albertson DG, Meyer BJ: DPY-27:a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 1994, 79:459-474.
15. Csankovszki G, Collette K, Spahl K, Carey J, Snyder M, Petty E, Patel U, Tabuchi T, Liu H, McLeod I, Thompson J, Sarkeshik A, Yates J, Meyer BJ, Hagstrom K: Three distinct condensin complexes control C. elegans chromosome dynamics. Curr Biol 2009, 19:9-19.
16. Lieb JD, Albrecht MR, Chuang PT, Meyer BJ: MIX-1: an essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation. Cell 1998, 92:265-277.
17. Lieb JD, Capowski EE, Meneely P, Meyer BJ: DPY-26, a link between dosage compensation and meiotic chromosome segregation in the nematode. Science 1996, 274:1732-1736.
18. Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ: Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev 2008, 22:194-211.
19. Hsu DR, Meyer BJ: The dpy-30 gene encodes an essential component of the Caenorhabditis elegans dosage compensation machinery. Genetics 1994, 137:999-1018.
20. Yonker SA, Meyer BJ: Recruitment of C. elegans dosage compensation proteins for gene-specific versus chromosome-wide repression. Development 2003, 130:6519-6532.
21. Mets DG, Meyer BJ: Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 2009, 139:73-86.
22. Hirano T: Condensins: universal organizers of chromosomes with diverse functions. Genes Dev 2012, 26:1659-1678.
23. Green LC, Kalitsis P, Chang TM, Cipetic M, Kim JH, Marshall O, Turnbull L, Whitchurch CB, Vagnarelli P, Samejima K, Earnshaw WC, Choo KH, Hudson DF: Contrasting roles of condensin I and condensin II in mitotic chromosome formation. J Cell Sci 2012, 125:1591-1604.
24. Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM: Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 2004, 117:6435-6445.
25. Ono T, Losada A, Hirano M, Myers MP, Neuwald AF, Hirano T: Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 2003, 115:109-121.
26. Shintomi K, Hirano T: The relative ratio of condensin I to II determines chromosome shapes. Genes Dev 2011, 25:1464-1469.
27. Freeman L, Aragon-Alcaide L, Strunnikov A: The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J Cell Biol 2000, 149:811-824.
28. Hirano T, Kobayashi R, Hirano M: Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 1997, 89:511-521.
29. Hirano T, Mitchison TJ: A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 1994, 79:449-458.
30. Sutani T, Yuasa T, Tomonaga T, Dohmae N, Takio K, Yanagida M: Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev 1999, 13:2271-2283.
31. Hagstrom KA, Holmes VF, Cozzarelli NR, Meyer BJ: C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev 2002, 16:729-742.
32. Collette KS, Petty EL, Golenberg N, Bembenek JN, Csankovszki G: Different roles for Aurora B in condensin targeting during mitosis and meiosis. J Cell Sci 2011, 124:3684-3694.
33. Gerlich D, Hirota T, Koch B, Peters JM, Ellenberg J: Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr Biol 2006, 16:333-344.
34. Ono T, Fang Y, Spector DL, Hirano T: Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 2004, 15:3296-3308.
35. Buster DW, Daniel SG, Nguyen HQ, Windler SL, Skwarek LC, Peterson M, Roberts M, Meserve JH, Hartl T, Klebba JE, Bilder D, Bosco G, Rogers GC: SCFSlimb ubiquitin ligase suppresses condensin II-mediated nuclear reorganization by degrading Cap-H2. J Cell Biol 2013, 201:49-63.
36. Hartl TA, Smith HF, Bosco G: Chromosome alignment and transvection are antagonized by condensin II. Science 2008, 322:1384-1387.
37. Hartl TA, Sweeney SJ, Knepler PJ, Bosco G: Condensin II resolves chromosomal associations to enable anaphase I segregation in Drosophila male meiosis. PLoS Genet 2008, 4:e1000228.
38. Joyce EF, Williams BR, Xie T, Wu CT: Identification of genes that promote or antagonize somatic homolog pairing using a high-throughput FISHbased screen. PLoS Genet 2012, 8:e1002667.
39. Bauer CR, Hartl TA, Bosco G: Condensin II promotes the formation of chromosome territories by inducing axial compaction of polyploid interphase chromosomes. PLoS Genet 2012, 8:e1002873.
40. Rawlings JS, Gatzka M, Thomas PG, Ihle JN: Chromatin condensation via the condensin II complex is required for peripheral T-cell quiescence. EMBO J 2011, 30:263-276.
41. Fazzio TG, Panning B: Condensin complexes regulate mitotic progression and interphase chromatin structure in embryonic stem cells. J Cell Biol 2010, 188:491-503.
42. Haeusler RA, Pratt-Hyatt M, Good PD, Gipson TA, Engelke DR: Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev 2008, 22:2204-2214.
43. Iwasaki O, Tanaka A, Tanizawa H, Grewal SI, Noma K: Centromeric localization of dispersed Pol III genes in fission yeast. Mol Biol Cell 2010, 21:254-265.
44. Rice JC, Nishioka K, Sarma K, Steward R, Reinberg D, Allis CD: Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev 2002, 16:2225-2230.
45. Wilkins BJ, Rall NA, Ostwal Y, Kruitwagen T, Hiragami-Hamada K, Winkler M, Barral Y, Fischle W, Neumann H: A cascade of histone modifications induces chromatin condensation in mitosis. Science 2014, 343:77-80.
46. Oda H, Okamoto I, Murphy N, Chu J, Price SM, Shen MM, Torres-Padilla ME, Heard E, Reinberg D: Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol Cell Biol 2009, 29:2278-2295.
47. Nishioka K, Rice JC, Sarma K, Erdjument-Bromage H, Werner J, Wang Y, Chuikov S, Valenzuela P, Tempst P, Steward R, Lis JT, Allis CD, Reinberg D: PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 2002, 9:1201-1213.
48. Vielle A, Lang J, Dong Y, Ercan S, Kotwaliwale C, Rechtsteiner A, Appert A, Chen QB, Dose A, Egelhofer T, Kimura H, Stempor P, Dernburg A, Lieb JD, Strome S, Ahringer J: H4K20me1 contributes to downregulation of X-linked genes for C. elegans dosage compensation. PLoS Genet 2012, 8:e1002933.
49. Wells MB, Snyder MJ, Custer LM, Csankovszki G: Caenorhabditis elegans dosage compensation regulates histone H4 chromatin state on X chromosomes. Mol Cell Biol 2012, 32:1710-1719.
50. Nabeshima K, Mlynarczyk-Evans S, Villeneuve AM: Chromosome painting reveals asynaptic full alignment of homologs and HIM-8-dependent remodeling of X chromosome territories during Caenorhabditis elegans meiosis. PLoS Genet 2011, 7:e1002231.
51. Hedgecock EM, White JG: Polyploid tissues in the nematode Caenorhabditis elegans. Dev Biol 1985, 107:128-133.
52. Consortium CeS: Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018.
53. Hsu DR, Chuang PT, Meyer BJ: DPY-30, a nuclear protein essential early in embryogenesis for Caenorhabditis elegans dosage compensation. Development 1995, 121:3323-3334.
54. Pferdehirt RR, Kruesi WS, Meyer BJ: An MLL/COMPASS subunit functions in the C. elegans dosage compensation complex to target X chromosomes for transcriptional regulation of gene expression. Genes Dev 2011, 25:499-515.
55. Sulston JE, Schierenberg E, White JG, Thomson JN: The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983, 100:64-119.
56. Eskeland R, Leeb M, Grimes GR, Kress C, Boyle S, Sproul D, Gilbert N, Fan Y, Skoultchi AI, Wutz A, Bickmore WA: Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol Cell 2010, 38:452-464.
57. Stear JH, Roth MB: Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment. Genes Dev 2002, 16:1498-1508.
58. Chan RC, Severson AF, Meyer BJ: Condensin restructures chromosomes in preparation for meiotic divisions. J Cell Biol 2004, 167:613-625.
59. Jans J, Gladden JM, Ralston EJ, Pickle CS, Michel AH, Pferdehirt RR, Eisen MB, Meyer BJ: A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome. Genes Dev 2009, 23:602-618.
60. Custer LM, Snyder MJ, Flegel K, Csankovszki G: The onset of C. elegans dosage compensation is linked to the loss of developmental plasticity. Dev Biol 2014, 385:279-290.
61. Kimura K, Hirano T: Dual roles of the 11S regulatory subcomplex in condensin functions. Proc Natl Acad Sci U S A 2000, 97:11972-11977.
62. Kimura K, Cuvier O, Hirano T: Chromosome condensation by a human condensin complex in Xenopus egg extracts. J Biol Chem 2001, 276:5417-5420.
63. Kimura K, Hirano T: ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 1997, 90:625-634.
64. St-Pierre J, Douziech M, Bazile F, Pascariu M, Bonneil E, Sauve V, Ratsima H, D'Amours D: Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol Cell 2009, 34:416-426.
65. Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR: 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 1999, 98:239-248.
66. Baxter J, Sen N, Martinez VL, De Carandini ME, Schvartzman JB, Diffley JF, Aragon L: Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Science 2011, 331:1328-1332.
67. Sakai A, Hizume K, Sutani T, Takeyasu K, Yanagida M: Condensin but not cohesin SMC heterodimer induces DNA reannealing through proteinprotein assembly. EMBO J 2003, 22:2764-2775.
68. Cuylen S, Metz J, Haering CH: Condensin structures chromosomal DNA through topological links. Nat Struct Mol Biol 2011, 18:894-901.
69. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL: Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311:844-847.
70. Hamada FN, Park PJ, Gordadze PR, Kuroda MI: Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster. Genes Dev 2005, 19:2289-2294.
71. Straub T, Gilfillan GD, Maier VK, Becker PB: The Drosophila MSL complex activates the transcription of target genes. Genes Dev 2005, 19:2284-2288.
72. Akhtar A, Becker PB: Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol Cell 2000, 5:367-375.
73. Smith ER, Pannuti A, Gu W, Steurnagel A, Cook RG, Allis CD, Lucchesi JC: The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol Cell Biol 2000, 20:312-318.
74. Dunlap D, Yokoyama R, Ling H, Sun HY, McGill K, Cugusi S, Lucchesi JC: Distinct contributions of MSL complex subunits to the transcriptional enhancement responsible for dosage compensation in Drosophila. Nucleic Acids Res 2012, 40:11281-11291.
75. Corona DF, Clapier CR, Becker PB, Tamkun JW: Modulation of ISWI function by site-specific histone acetylation. EMBO Rep 2002, 3:242-247.
76. Brenner S: The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
77. Kamath RS, Ahringer J: Genome-wide RNAi screening in Caenorhabditis elegans. Methods 2003, 30:313-321.
78. Csankovszki G, McDonel P, Meyer BJ: Recruitment and spreading of the C. elegans dosage compensation complex along X chromosomes. Science 2004, 303:1182-1185.