Specifying peripheral heterochromatin during nuclear lamina reassembly

Nucleus (United States)

Volumn 5, Issue 1, 2014, Pages 32-39

  Poleshko, Andrey ^a   Katz, Richard A ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

Heterochromatin; Heterochromatin protein 1; Nuclear envelope; Nuclear lamina; Proline Rich 14

Indexed keywords

AURORA B KINASE; LAMIN B;

ANAPHASE; ARTICLE; CHROMOSOME; GENE EXPRESSION; GENE SILENCING; HETEROCHROMATIN; HUMAN; ISOELECTRIC POINT; MITOSIS; NONHUMAN; NUCLEAR LAMINA; PHENOTYPE; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TELOPHASE;

EID: 84897483294     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.28167     Document Type: Article

References (60)

1. Bickmore WA, van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 2013; 152:1270-84; PMID:23498936; http://dx.doi.org/10.1016/j.cell.2013.02.001
2. Cavalli G, Misteli T. Functional implications of genome topology. Nat Struct Mol Biol 2013; 20:290-9; PMID:23463314; http://dx.doi.org/10.1038/nsmb.2474
3. Collas P, Lund EG, Oldenburg AR. Closing the (nuclear) envelope on the genome: how nuclear lamins interact with promoters and modulate gene expression. Bioessays 2014; 36:75-83; PMID:24272858; http://dx.doi.org/10.1002/bies.201300138
4. Bank EM, Gruenbaum Y. The nuclear lamina and heterochromatin: a complex relationship. Biochem Soc Trans 2011; 39:1705-9; PMID:22103511; http://dx.doi.org/10.1042/BST20110603
5. Geyer PK, Vitalini M W, Wallrath LL. Nuclear organization: taking a position on gene expression. Curr Opin Cell Biol 2011; 23:354-9; PMID:21450447; http://dx.doi.org/10.1016/j.ceb.2011.03.002
6. Meister P, Mango SE, Gasser SM. Locking the genome: nuclear organization and cell fate. Curr Opin Genet Dev 2011; 21:167-74; PMID:21345665; http://dx.doi.org/10.1016/j.gde.2011.01.023
7. Reddy KL, Zullo JM, Bertolino E, Singh H. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 2008; 452:243-7; PMID:18272965; http://dx.doi.org/10.1038/nature06727
8. Shevelyov YY, Nurminsky DI. The nuclear lamina as a gene-silencing hub. Curr Issues Mol Biol 2012; 14:27-38; PMID:21795760
9. Towbin BD, González-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser SM. Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 2012; 150:934-47; PMID:22939621; http://dx.doi.org/10.1016/j.cell.2012.06.051
10. Zhou V W, Goren A, Bernstein BE. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 2011; 12:7-18;PMID:21116306; http://dx.doi.org/10.1038/nrg2905
11. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I, Brugman W, Gräf S, Flicek P, Kerkhoven RM, van Lohuizen M, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell 2010; 38:603-13; PMID:20513434; http://dx.doi.org/10.1016/j.molcel.2010.03.016
12. Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD. Nuclear lamins. Cold Spring Harb Perspect Biol 2010; 2:a000547; PMID:20826548; http://dx.doi.org/10.1101/cshperspect.a000547
13. Dittmer TA, Misteli T. The lamin protein family. Genome Biol 2011; 12:222; PMID:21639948; http://dx.doi.org/10.1186/gb-2011-12-5-222
14. Simon DN, Wilson KL. The nucleoskeleton as a genome-associated dynamic 'network of net work s'. Nat Rev Mol Cell Biol 2011; 12:695-708; PMID:21971041; http://dx.doi.org/10.1038/nrm3207
15. Reddy KL, Feinberg AP. Higher order chromatin organization in cancer. Semin Cancer Biol 2013; 23:109-15; PMID:23266653; http://dx.doi.org/10.1016/j.semcancer.2012.12.001
16. Davidson PM, Lammerding J. Broken nuclei - lamins, nuclear mechanics, and disease. Trends Cell Biol 2013; PMID:24309562; http://dx.doi.org/10.1016/j.tcb.2013.11.004
17. Burtner CR, Kennedy BK. Progeria syndromes and ageing: what is the connection? Nat Rev Mol Cell Biol 2010; 11:567-78;PMID:20651707; http://dx.doi.org/10.1038/nrm2944
18. Cruickshanks HA, McBryan T, Nelson DM, Van der kraats ND, Shah PP, van Tuyn J, Singh Rai T, Brock C, Donahue G, Dunican DS, et al. Senescent cells harbour features of the cancer epigenome. Nat Cell Biol 2013; 15:1495-506; PMID:24270890; http://dx.doi.org/10.1038/ncb2879
19. Sadaie M, Salama R, Carroll T, Tomimatsu K, Chandra T, Young AR, Narita M, Pérez-Mancera PA, Bennett DC, Chong H, et al. Redistribution of the Lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev 2013; 27:1800-8; PMID:23964094; http://dx.doi.org/10.1101/gad.217281.113
20. Shah PP, Donahue G, Otte GL, Capell BC, Nelson DM, Cao K, Aggarwala V, Cruickshanks HA, Rai TS, McBryan T, et al. Lamin B1 depletion in senescent cells triggers large-scale changes in gene expression and the chromatin landscape. Genes Dev 2013; 27:1787-99; PMID:23934658; http://dx.doi.org/10.1101/gad.223834.113
21. Butin-Israeli V, Adam SA, Goldman AE, Goldman RD. Nuclear lamin functions and disease. Trends Genet 2012; 28:464-71; PMID:22795640; http://dx.doi.org/10.101/j.tig.2012.06.001
22. Gordon LB, Cao K, Collins FS. Progeria: translational insights from cell biology. J Cell Biol 2012; 199:9-13; PMID:23027899; http://dx.doi.org/10.1083/jcb.201207072
23. Worman HJ, Ostlund C, Wang Y. Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol 2010; 2:a000760;PMID: 20182615; http://dx.doi.org/10.1101/cshperspect.a000760
24. Kubben N, Adriaens M, Meuleman W, Voncken J W, van Steensel B, Misteli T. Mapping of lamin A and progerin-interacting genome regions. Chromosoma 2012; 121:447-64; PMID:22610065; http://dx.doi.org/10.1007/s00412-012-0376-7
25. Montes de Oca R, Shoemaker CJ, Gucek M, Cole RN, Wilson KL. Barrier-to-autointegration factor proteome reveals chromatin-regulatory partners. PLoS One 2009; 4:e7050; PMID:19759913; http://dx.doi.org/10.1371/journal.pone.0007050
26. Olins AL, Rhodes G, Welch DB, Zwerger M, Olins DE. Lamin B receptor: multi-tasking at the nuclear envelope. Nucleus 2010; 1:53-70; PMID:21327105
27. Zullo JM, Demarco IA, Piqué-Regi R, Gaffney DJ, Epstein CB, Spooner CJ, Luperchio TR, Bernstein BE, Pritchard JK, Reddy KL, et al. DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 2012; 149:1474-87; PMID:22726435; http://dx.doi.org/10.1016/j.cell.2012.04.035
28. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008; 453:948-51; PMID:18463634; http://dx.doi.org/10.1038/nature06947
29. Kind J, van Steensel B. Genome-nuclear lamina interactions and gene regulation. Curr Opin Cell Biol 2010; 22:320-5; PMID:20444586; http://dx.doi.org/10.1016/j.ceb.2010.04.002
30. Lund E, Oldenburg AR, Delbarre E, Freberg CT, Duband-Goulet I, Eskeland R, Buendia B, Collas P. Lamin A/C-promoter interactions specify chromatin state-dependent transcription outcomes. Genome Res 2013; 23:1580-9; PMID:23861385; http://dx.doi.org/10.1101/gr.159400.113
31. McCord R P, Nazario-Toole A, Zhang H, Chines PS, Zhan Y, Erdos MR, Collins FS, Dekker J, Cao K. Correlated alterations in genome organization, histone methylation, and DNA-lamin A/C interactions in Hutchinson-Gilford progeria syndrome. Genome Res 2013; 23:260-9;PMID: 2 3152449; http://dx.doi.org/10.1101/gr.138032.112
32. Meister P, Taddei A. Building silent compartments at the nuclear periphery: a recurrent theme. Curr Opin Genet Dev 2013; 23:96-103; PMID:23312840; http://dx.doi.org/10.1016/j.gde.2012.12.001
33. Towbin BD, Gonzalez-Sandoval A, Gasser SM. Mechanisms of heterochromatin subnuclear localization. Trends Biochem Sci 2013; 38:356-63;PMID: 23746617; http://dx.doi.org/10.1016/j.tibs.2013.04.004
34. Kind J, Pagie L, Ortabozkoyun H, Boyle S, de Vries SS, Janssen H, Amendola M, Nolen LD, Bickmore WA, van Steensel B. Single-cell dynamics of genome-nuclear lamina interactions. Cell 2013; 153:178-92; PMID:23523135; http://dx.doi.org/10.1016/j.cell.2013.02.028
35. Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, McDonald OG, Wen B, Wu H, Liu Y, Diep D, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet 2011; 43:768-75; PMID:21706001; http://dx.doi.org/10.1038/ng.865
36. Jørgensen HF, Fisher AG. LOCKing in Cellular Potential. Cell Stem Cell 2009; 4:192-4; PMID:19265653; http://dx.doi.org/10.1016/j.stem.2009.02.007
37. Ye Q, Worman HJ. Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J Biol Chem 1996; 271:14653-6; PMID:8663349; http://dx.doi.org/10.1074/jbc.271.25.14653
38. Poleshko A, Mansfield KM, Burlingame CC, Andrake MD, Shah NR, Katz RA. The human protein PRR14 tethers heterochromatin to the nuclear lamina during interphase and mitotic exit. Cell Rep 2013; 5:292-301; PMID:24209742; http://dx.doi.org/10.1016/j.celrep.2013.09.024
39. Poleshko A, Einarson MB, Shalginskikh N, Zhang R, Adams PD, Skalka AM, Katz RA. Identification of a functional network of human epigenetic silencing factors. J Biol Chem 2010; 285:422-33;PMID: 19880521; http://dx.doi.org/10.1074/jbc.M109.064667
40. Kubben N, Voncken JW, Demmers J, Calis C, van Almen G, Pinto Y, Misteli T. Identification of differential protein interactors of lamin A and progerin. Nucleus 2010; 1:513-25; PMID:21327095
41. Roux KJ, Kim DI, Raida M, Burke B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol 2012; 196:801-10; PMID:22412018; http://dx.doi.org/10.1083/jcb.201112098
42. Nozawa RS, Nagao K, Masuda HT, Iwasaki O, Hirota T, Nozaki N, Kimura H, Obuse C. Human POGZ modulates dissociation of HP1alpha from mitotic chromosome arms through Aurora B activation. Nat Cell Biol 2010; 12:719-27; PMID:20562864; http://dx.doi.org/10.1038/ncb2075
43. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature 2005; 437:11 73-8;PMID: 16189514; http://dx.doi.org/10.1038/nature04209
44. Zeng W, Ball AR Jr., Yokomori K. HP1: heterochromatin binding proteins working the genome. Epigenetics 2010; 5:287-92; PMID: 20421743; http://dx.doi.org/10.4161/epi.5.4.11683
45. Lechner MS, Schultz DC, Negorev D, Maul GG, Rauscher FJ 3rd. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem Biophys Res Commun 2005; 331:929-37; PMID:15882967; http://dx.doiorg/10.1016/j.bbrc.2005.04.016
46. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen T V, Devys D, Foisner R, Peichl L, et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 2013; 152:584-98; PMID:23374351; http://dx.doi.org/10.1016/j.cell.2013.01.009
47. Sugimoto K, Tasaka H, Dotsu M. Molecular behavior in living mitotic cells of human centromere heterochromatin protein HPLalpha ectopically expressed as a fusion to red fluorescent protein. Cell Struct Funct 2001; 26:705-18;PMID:11942629; http://dx.doi.org/10.1247/csf.26.705
48. Wang F, Higgins JM. Histone modifications and mitosis: countermarks, landmarks, and bookmarks. Trends Cell Biol 2013; 23:175-84; PMID:23246430; http://dx.doi.org/10.1016/j.tcb.2012.11.005
49. Hirota T, Lipp JJ, Toh BH, Peters JM. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 2005; 438:1176-80; PMID:16222244; http://dx.doi.org/10.1038/nature04254
50. Zaidi SK, Young DW, Montecino MA, Lian JB, van Wijnen AJ, Stein JL, Stein GS. Mitotic bookmarking of genes: a novel dimension to epigenetic control. Nat Rev Genet 2010; 11:583-9; PMID:20628351; http://dx.doi.org/10.1038/nrg2827
51. Wandke C, Kutay U. Enclosing chromatin: reassembly of the nucleus after open mitosis. Cell 2013; 152:1222-5; PMID:23498932; http://dx.doi.org/10.1016/j.cell.2013.02.046
52. Haraguchi T, Kojidani T, Koujin T, Shimi T, Osakada H, Mori C, Yamamoto A, Hiraoka Y. Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J Cell Sci 2008; 121:2540-54; PMID:18628300; http://dx.doi.org/10.1242/jcs.033597
53. Naumova N, Imakaev M, Fudenberg G, Zhan Y, Lajoie BR, Mirny LA, Dekker J. Organization of the mitotic chromosome. Science 2013; 342:948-53; PMID:24200812; http://dx.doi.org/10.1126/science.1236083
54. Guo G, Huss M, Tong GQ, Wang C, Li Sun L, Clarke ND, Robson P. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 2010; 18:675-85; PMID:20412781; http://dx.doi.org/10.1016/j.devcel.2010.02.012
55. Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, Lao K, Surani MA. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell 2010; 6:468-78; PMID:20452321; http://dx.doi.org/10.1016/j.stem.2010.03.015
56. Herzog F, Kahraman A, Boehringer D, Mak R, Bracher A, Walzthoeni T, Leitner A, Beck M, Hartl FU, Ban N, et al. Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 2012; 337:1348-52; PMID:22984071; http://dx.doi.org/10.1126/science.1221483
57. Asencio C, Davidson IF, Santarella-Mellwig R, Ly-Hartig TB, Mall M, Wa llenfa ng MR, Mattaj I W, Gorjánácz M. Coordination of kinase and phosphatase activities by Lem4 enables nuclear envelope reassembly during mitosis. Cell 2012; 15 0:122-35; PMID:22770216; http://dx.doi.org/10.1016/j.cell.2012.04.043
58. Gorjánácz M. LEM-4 promotes rapid dephosphorylation of BAF during mitotic exit. Nucleus 2013; 4:14-7; PMID:23211644; http://dx.doi.org/10.4161/nucl.22961
59. Broers JL, Ramaekers FC, Bonne G, Yaou RB, Hutchison CJ. Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 2006; 86:967-1008; PMID:16816143; http://dx.doi.org/10.1152/physrev.00047.2005
60. Fricker M, Hollinshead M, White N, Vaux D. Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J Cell Biol 1997; 136:531-44; PMID:9024685; http://dx.doi.org/10.1083/jcb.136.3.531