Suv4-20h2 mediates chromatin compaction and is important for cohesion recruitment to heterochromatin

Genes and Development

Volumn 27, Issue 8, 2013, Pages 859-872

  Hahn, Matthias ^a   Dambacher, Silvia ^a   Dulev, Stanimir ^a   Kuznetsova, Anastasia Yurievna ^b   Eck, Simon ^c,d   Wörz, Stefan ^c,d   Sadic, Dennis ^a   Schulte, Maike ^a   Mallm, Jan Philipp ^c,d   Maiser, Andreas ^a,e   Debs, Pierre ^f   von Melchner, Harald ^f   Leonhardt, Heinrich ^a,e   Schermelleh, Lothar ^a,e,g   Rohr, Karl ^c,d   Rippe, Karsten ^c,d   Storchova, Zuzana ^b   Schotta, Gunnar ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e Deutsches Krebsforschungszentrum ^*  (Germany)

^f GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^g UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Chromocenter clustering; Chromosome segregation; Cohesin; Heterochromatin; Suv39h; Suv4 20h2

Indexed keywords

COHESIN; HETEROCHROMATIN PROTEIN 1; HISTONE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE SUV4 20H2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE G0 PHASE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; HETEROCHROMATIN; INTERPHASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; MICE; MUTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

MAMMALIA;

EID: 84876895132     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.210377.112     Document Type: Article

References (42)

1. Bulut-Karslioglu A, Perrera V, Scaranaro M, de la Rosa-Velazquez IA, van de Nobelen S, Shukeir N, Popow J, Gerle B, Opravil S, Pagani M, et al. 2012. A transcription factor-based mechanism for mouse heterochromatin formation. Nat Struct Mol Biol 19: 1023-1030.
2. Cheutin T, McNairn AJ, Jenuwein T, Gilbert DM, Singh PB, Misteli T. 2003. Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299: 721-725.
3. Degner SC, Verma-Gaur J, Wong TP, Bossen C, Iverson GM, Torkamani A, Vettermann C, Lin YC, Ju Z, Schulz D, et al. 2011. CCCTC-binding factor (CTCF) and cohesin influence the genomic architecture of the Igh locus and antisense transcription in pro-B cells. Proc Natl Acad Sci 108: 9566-9571.
4. Eckert CA, Gravdahl DJ, Megee PC. 2007. The enhancement of pericentromeric cohesin association by conserved kinetochore components promotes high-fidelity chromosome segregation and is sensitive to microtubule-based tension. Genes Dev 21: 278-291.
5. Fan Y, Nikitina T, Zhao J, Fleury TJ, Bhattacharyya R, Bouhassira EE, Stein A, Woodcock CL, Skoultchi AI. 2005. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123: 1199-1212.
6. Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, Schotta G, Bonaldi T, Haydon C, Ropero S, Petrie K, et al. 2005. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 37: 391-400.
7. Gause M, Misulovin Z, Bilyeu A, Dorsett D. 2010. Dosagesensitive regulation of cohesin chromosome binding and dynamics by Nipped-B, Pds5, and Wapl. Mol Cell Biol 30: 4940-4951.
8. Gilbert N, Thomson I, Boyle S, Allan J, Ramsahoye B, Bickmore WA. 2007. DNA methylation affects nuclear organization, histone modifications, and linker histone binding but not chromatin compaction. J Cell Biol 177: 401-411.
9. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Lobrich M, Jeggo PA. 2008. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 31: 167-177.
10. Guenatri M, Bailly D, Maison C, Almouzni G. 2004. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol 166: 493-505.
11. Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, Fraser P, Fisher AG, Merkenschlager M. 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460: 410-413.
12. Hahn M, Dambacher S, Schotta G. 2010. Heterochromatin dysregulation in human diseases. J Appl Physiol 109: 232-242.
13. Hauf S, Waizenegger IC, Peters JM. 2001. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293: 1320-1323.
14. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, et al. 2010. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435.
15. Koch B, Kueng S, Ruckenbauer C, Wendt KS, Peters JM. 2008. The Suv39h-HP1 histone methylation pathway is dispensable for enrichment and protection of cohesin at centromeres in mammalian cells. Chromosoma 117: 199-210.
16. Kueng S, Hegemann B, Peters BH, Lipp JJ, Schleiffer A, Mechtler K, Peters JM. 2006. Wapl controls the dynamic association of cohesin with chromatin. Cell 127: 955-967.
17. Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F. 2004. Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430: 573-578.
18. Markaki Y, Smeets D, Cremer M, Schermelleh L. 2013. Fluorescence in situ hybridization applications for super-resolution 3D structured illumination microscopy. Methods Mol Biol 950: 43-64.
19. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. 2006. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10: 105-116.
20. Muller KP, Erdel F, Caudron-Herger M, Marth C, Fodor BD, Richter M, Scaranaro M, Beaudouin J, Wachsmuth M, Rippe K. 2009. Multiscale analysis of dynamics and interactions of heterochromatin protein 1 by fluorescence fluctuation microscopy. Biophys J 97: 2876-2885.
21. Nasmyth K. 2011. Cohesin: A catenase with separate entry and exit gates? Nat Cell Biol 13: 1170-1177.
22. Nicetto D, Hahn M, Jung J, Schneider TD, Straub T, David R, Schotta G, Rupp RA. 2013. Suv4-20h histone methyltransferases promote neuroectodermal differentiation by silencing the pluripotency-associated oct-25 gene. PLoS Genet 9: e1003188.
23. Nonaka N, Kitajima T, Yokobayashi S, Xiao G, Yamamoto M, Grewal SI, Watanabe Y. 2002. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 4: 89-93.
24. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, et al. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132: 422-433.
25. Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, et al. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107: 323-337.
26. Rubio ED, Reiss DJ, Welcsh PL, Disteche CM, Filippova GN, Baliga NS, Aebersold R, Ranish JA, Krumm A. 2008. CTCF physically links cohesin to chromatin. Proc Natl Acad Sci 105: 8309-8314.
27. Salic A, Waters JC, Mitchison TJ. 2004. Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 118: 567-578.
28. Samoshkin A, Dulev S, Loukinov D, Rosenfeld JA, Strunnikov AV. 2012. Condensin dysfunction in human cells induces nonrandom chromosomal breaks in anaphase, with distinct patterns for both unique and repeated genomic regions. Chromosoma 121: 191-199.
29. Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, Kner P, Burke B, Cardoso MC, Agard DA, Gustafsson MG, et al. 2008. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320: 1332-1336.
30. Schneider AC, Heukamp LC, Rogenhofer S, Fechner G, Bastian PJ, von Ruecker A, Muller SC, Ellinger J. 2011. Global histone H4K20 trimethylation predicts cancer-specific survival in patients with muscle-invasive bladder cancer. BJU Int 108: E290-E296.
31. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T. 2004. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18: 1251-1262.
32. Schotta G, Sengupta R, Kubicek S, Malin S, Kauer M, Callen E, Celeste A, Pagani M, Opravil S, De La Rosa-Velazquez IA, et al. 2008. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev 22: 2048-2061.
33. Seitan VC, Merkenschlager M. 2012. Cohesin and chromatin organisation. Curr Opin Genet Dev 22: 93-100.
34. Souza PP, Volkel P, Trinel D, Vandamme J, Rosnoblet C, Heliot L, Angrand PO. 2009. The histone methyltransferase SUV420H2 and heterochromatin proteins HP1 interact but show different dynamic behaviours. BMC Cell Biol 10: 41.
35. Tang Z, Sun Y, Harley SE, Zou H, Yu H. 2004. Human Bub1 protects centromeric sister-chromatid cohesion through Shugoshin during mitosis. Proc Natl Acad Sci 101: 18012-18017.
36. Thompson SL, Bakhoum SF, Compton DA. 2010. Mechanisms of chromosomal instability. Curr Biol 20: R285-R295.
37. Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, Contino G, Deshpande V, Iafrate AJ, Letovsky S, et al. 2011. Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 331: 593-596.
38. Van Den Broeck A, Brambilla E, Moro-Sibilot D, Lantuejoul S, Brambilla C, Eymin B, Khochbin S, Gazzeri S. 2008. Loss of histone H4K20 trimethylation occurs in preneoplasia and influences prognosis of non-small cell lung cancer. Clin Cancer Res 14: 7237-7245.
39. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, et al. 2010. Quantitative interaction proteomics and genomewide profiling of epigenetic histone marks and their readers. Cell 142: 967-980.
40. Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters JM. 2006. Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol 16: 863-874.
41. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, et al. 2008. Cohesin mediates transcriptional insulation by CCCTCbinding factor. Nature 451: 796-801.
42. Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, Nederlof PM, Gage FH, Verma IM. 2011. BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 477: 179-184.