Control of heterochromatin localization and silencing by the nuclear membrane protein Lem2

Genes and Development

Volumn 30, Issue 2, 2016, Pages 133-148

  Barrales, Ramón Ramos ^a   Forn, Marta ^a   Georgescu, Paula Raluca ^a   Sarkadi, Zsuzsa ^a   Braun, Sigurd ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b MPI of Biochemistry   (Germany)

Author keywords

Heterochromatin; Lamin associated proteins; LEM; Nuclear periphery; Perinuclear silencing; Tethering

Indexed keywords

HISTONE DEACETYLASE; MEMBRANE PROTEIN; NUCLEAR MEMBRANE PROTEIN LEM2; TRANSCRIPTION FACTOR SNF; UNCLASSIFIED DRUG; EPE1 PROTEIN, S POMBE; HETEROCHROMATIN; NUCLEAR PROTEIN; PROTEIN BINDING; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; CELLULAR DISTRIBUTION; CENTROMERE; GENE DELETION; GENE SILENCING; HETEROCHROMATIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; SCHIZOSACCHAROMYCES POMBE; TELOMERE; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES;

GENE DELETION; GENE SILENCING; HETEROCHROMATIN; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 84954554188     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.271288.115     Document Type: Article

References (48)

1. Alfredsson-Timmins J, Kristell C, Henningson F, Lyckman S, Bjerling P. 2009. Reorganization of chromatin is an early response to nitrogen starvation in Schizosaccharomyces pombe. Chromosoma 118: 99-112.
2. Allshire RC, Ekwall K. 2015. Epigenetic regulation of chromatin states in Schizosaccharomyces pombe. Cold Spring Harb Perspect Biol 7: a018770.
3. Al-Sady B, Madhani HD, Narlikar GJ. 2013. Division of labor between the chromodomains of HP1 and Suv39 methylase enables coordination of heterochromatin spread. Mol Cell 51: 80-91.
4. Amendola M, van Steensel B. 2014. Mechanisms and dynamics of nuclear lamina-genome interactions. Curr Opin Cell Biol 28C: 61-68.
5. Audergon P, Catania S, Kagansky A, Tong P, Shukla M, Pidoux A, Allshire RC. 2015. Restricted epigenetic inheritance of H3K9 methylation. Science 348: 128-132.
6. Barton LJ, Soshnev AA, Geyer PK. 2015. Networking in the nucleus: a spotlight on LEM-domain proteins. Curr Opin Cell Biol 34: 1-8.
7. Brachner A, Foisner R. 2011. Evolvement of LEM proteins as chromatin tethers at the nuclear periphery. Biochem Soc Trans 39: 1735-1741.
8. Braun S, Garcia JF, Rowley M, Rougemaille M, Shankar S, Madhani HD. 2011. The Cul4-Ddb1(Cdt)² ubiquitin ligase inhibits invasion of a boundary-associated antisilencing factor into heterochromatin. Cell 144: 41-54.
9. Caputo S, Couprie J, Duband-Goulet I, Kondé E, Lin F, Braud S, Gondry M, Gilquin B, Worman HJ, Zinn-Justin S. 2006. The carboxyl-terminal nucleoplasmic region of MAN1 exhibits a DNA binding winged helix domain. J Biol Chem 281: 18208-18215.
10. Chan JNY, Poon BPK, Salvi J, Olsen JB, Emili A, Mekhail K. 2011. Perinuclear cohibin complexes maintain replicative life span via roles at distinct silent chromatin domains. Dev Cell 20: 867-879.
11. Chikashige Y, Yamane M, Okamasa K, Tsutsumi C, Kojidani T, Sato M, Haraguchi T, Hiraoka Y. 2009. Membrane proteins Bqt3 and -4 anchor telomeres to the nuclear envelope to ensure chromosomal bouquet formation. J Cell Biol 187: 413-427.
12. Demmerle J, Koch AJ, Holaska JM. 2012. The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J Biol Chem 287: 22080-22088.
13. Ekwall K, Nimmo ER, Javerzat JP, Borgstrøm B, Egel R, Cranston G, Allshire R. 1996. Mutations in the fission yeast silencing factors clr4+ and rik1+ disrupt the localisation of the chromo domain protein Swi6p and impair centromere function. J Cell Sci 109: 2637-2648.
14. Ekwall K, Cranston G, Allshire RC. 1999. Fission yeast mutants that alleviate transcriptional silencing in centromeric flanking repeats and disrupt chromosome segregation. Genetics 153: 1153-1169.
15. Gonzalez Y, Saito A, Sazer S. 2012. Fission yeast Lem2 and Man1 perform fundamental functions of the animal cell nuclear lamina. Nucleus 3: 60-76.
16. Gonzalez-Sandoval A, Towbin BD, Kalck V, Cabianca DS, Gaidatzis D, Hauer MH, Geng L, Wang L, Yang T, Wang X, et al. 2015. Perinuclear anchoring of H3K9-methylated chromatin stabilizes induced cell fate in C. elegans embryos. Cell 163: 1333-1347.
17. Grewal SI. 2010. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 20: 134-141
18. Grund SE, Fischer T, Cabal GG, Antúnez O, Pérez-Ortín JE, Hurt E. 2008. The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. J Cell Biol 182: 897-910.
19. Gudise S, Figueroa RA, Lindberg R, Larsson V, Hallberg E. 2011. Samp1 is functionally associated with the LINC complex and A-type lamina networks. J Cell Sci 124: 2077-2085
20. Hall IM, Noma K, Grewal SIS. 2003. RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc Natl Acad Sci 100: 193-198.
21. Hediger F, Taddei A, Neumann FR, Gasser SM. 2004. Methods for visualizing chromatin dynamics in living yeast. Methods Enzymol 375: 345-365.
22. Hirano Y, Hizume K, Kimura H, Takeyasu K, Haraguchi T, Hiraoka Y. 2012. Lamin B receptor recognizes specific modifications of histone H4 in heterochromatin formation. J Biol Chem 287: 42654-42663.
23. Hiraoka Y, Maekawa H, Asakawa H, Chikashige Y, Kojidani T, Osakada H, Matsuda A, Haraguchi T. 2011. Inner nuclear membrane protein Ima1 is dispensable for intranuclear positioning of centromeres. Genes Cells 16: 1000-1011.
24. Hou H, Zhou Z, Wang Y, Wang J, Kallgren SP, Kurchuk T, Miller EA, Chang F, Jia S. 2012. Csi1 links centromeres to the nuclear envelope for centromere clustering. J Cell Biol 199: 735-744
25. Ikegami K, Egelhofer TA, Strome S, Lieb JD. 2010. Caenorhabditis elegans chromosome arms are anchored to the nuclear membrane via discontinuous association with LEM-2. Genome Biol 11: R120.
26. Kawakami K, Hayashi A, Nakayama J-I, Murakami Y. 2012. A novel RNAi protein, Dsh1, assembles RNAi machinery on chromatin to amplify heterochromatic siRNA. Genes Dev 26: 1811-1824.
27. Mans B, Anantharaman V, Aravind L, Koonin EV. 2004. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3: 1625-1650
28. Margalit A, Brachner A, Gotzmann J, Foisner R, Gruenbaum Y. 2007. Barrier-to-autointegration factor-a BAFfling little protein. Trends Cell Biol 17: 202-208.
29. Mattout A, Pike BL, Towbin BD, Bank EM, Gonzalez-Sandoval A, Stadler MB, Meister P, Gruenbaum Y, Gasser SM. 2011. An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle integrity. Curr Biol 21: 1603-1614.
30. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM. 2010. The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev 24: 766-782.
31. Mekhail K, Seebacher J, Gygi SP, Moazed D. 2008. Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456: 667-670.
32. Poleshko A, Mansfield KM, Burlingame CC, Andrake MD, Shah NR, Katz RA. 2013. The human protein PRR14 tethers hetero-chromatin to the nuclear lamina during interphase and mitotic exit. Cell Rep 5: 292-301.
33. Ragunathan K, Jih G, Moazed D. 2015. Epigenetic inheritance uncoupled from sequence-specific recruitment. Science 348: 1258699-1258699.
34. Shimada A, Dohke K, Sadaie M, Shinmyozu K, Nakayama J-I, Urano T, Murakami Y. 2009. Phosphorylation of Swi6/HP1 regulates transcriptional gene silencing at heterochromatin. Genes Dev 23: 18-23.
35. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen TV, Devys D, Foisner R, Peichl L, et al. 2013. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152: 584-598.
36. Somech R, Shaklai S, Geller O, Amariglio N, Simon AJ, Rechavi G, Gal-Yam EN. 2005. The nuclear-envelope protein and transcriptional repressor LAP2β interacts with HDAC3 at the nuclear periphery, and induces histone H4 deacetylation. J Cell Sci 118: 4017-4025.
37. Steglich B, Filion GJ, van Steensel B, Ekwall K. 2012. The inner nuclear membrane proteins Man1 and Ima1 link to two different types of chromatin at the nuclear periphery in S. pombe. Nucleus 3: 77-87.
38. Sugiyama T, Cam HP, Sugiyama R, Noma K-I, Zofall M, Kobayashi R, Grewal SIS. 2007. SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128: 491-504
39. Taddei A, Gasser SM. 2012. Structure and function in the budding yeast nucleus. Genetics 192: 107-129.
40. Taddei A, Hediger F, Neumann FR, Bauer C, Gasser SM. 2004. Separation of silencing from perinuclear anchoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO J 23: 1301-1312
41. Taddei A, Van Houwe G, Nagai S, Erb I, van Nimwegen E, Gasser SM. 2009. The functional importance of telomere clustering: global changes in gene expression result from SIR factor dispersion. Genome Res 19: 611-625.
42. Tadeo X, Wang J, Kallgren SP, Liu J, Reddy BD, Qiao F, Jia S. 2013. Elimination of shelterin components bypasses RNAi for pericentric heterochromatin assembly. Genes Dev 27: 2489-2499
43. Towbin BD, González-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser SM. 2012. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150: 934-947.
44. Towbin BD, Gonzalez-Sandoval A, Gasser SM. 2013. Mechanisms of heterochromatin subnuclear localization. Trends Biochem Sci 38: 356-363.
45. Trewick SC, Minc E, Antonelli R, Urano T, Allshire RC. 2007. The JmjC domain protein Epe1 prevents unregulated assembly and disassembly of heterochromatin. EMBO J 26: 4670-4682.
46. Verrier L, Taglini F, Barrales RR, Webb S, Urano T, Braun S, Bayne EH. 2015. Global regulation of heterochromatin spreading by Leo1. Open Biol 5: 150045-150045.
47. Zofall M, Grewal SIS. 2006. Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol Cell 22: 681-692.
48. Zuleger N, Boyle S, Kelly DA, las Heras de JI, Lazou V, Korfali N, Batrakou DG, Randles KN, Morris GE, Harrison DJ, et al. 2013. Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery. Genome Biol 14: R14.