Gene repositioning within the cell nucleus is not random and is determined by its genomic neighborhood

Epigenetics and Chromatin

Volumn 8, Issue 1, 2015, Pages

  Jost, K Laurence ^a   Bertulat, Bianca ^a   Rapp, Alexander ^a   Brero, Alessandro ^b   Hardt, Tanja ^b   Domaing, Petra ^b   Gösele, Claudia ^b   Schulz, Herbert ^b   Hübner, Norbert ^b   Cardoso, M Cristina ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

3D FISH measurements; Chromocenters; Gene position; Gene silencing; Genomic context; Heterochromatin proximity; MeCP2; Myogenesis; Nuclear periphery; Transcriptional profiling

Indexed keywords

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMOSOMAL LOCALIZATION; CONTROLLED STUDY; CPG ISLAND; DOWN REGULATION; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOCATION; GENE REARRANGEMENT; GENE SEQUENCE; GENE SILENCING; GENETIC ANALYSIS; GENETIC DISTANCE; GENETIC TRANSCRIPTION; HETEROCHROMATIN; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

EID: 84941912754     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/s13072-015-0025-5     Document Type: Article

References (64)

1. Pennisi E. Mysteries of the cell. Does a gene's location in the nucleus matter? Science. 2011;334(6059):1050-1. doi: 10.1126/science.334.6059.1050.
2. Francastel C, Schubeler D, Martin DI, Groudine M. Nuclear compartmentalization and gene activity. Nat Rev Mol Cell Biol. 2000;1(2):137-43. doi: 10.1038/35040083.
3. Saksouk N, Simboeck E, Dejardin J. Constitutive heterochromatin formation and transcription in mammals. Epigenet Chromatin. 2015;8:3. doi: 10.1186/1756-8935-8-3.
4. Towbin BD, Gonzalez-Sandoval A, Gasser SM. Mechanisms of heterochromatin subnuclear localization. Trends Biochem Sci. 2013;38(7):356-63. doi: 10.1016/j.tibs.2013.04.004.
5. Muller H. Types of visible variations induced by X-rays in Drosophila. J Genet. 1930;22(3):299-334. doi: 10.1007/bf02984195.
6. Karpen GH. Position-effect variegation and the new biology of heterochromatin. Curr Opin Genet Dev. 1994;4(2):281-91.
7. Delaire S, Huang YH, Chan SW, Robey EA. Dynamic repositioning of CD4 and CD8 genes during T cell development. J Exp Med. 2004;200(11):1427-35. doi: 10.1084/jem.20041041.
8. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell. 1997;91(6):845-54.
9. Guenatri M, Bailly D, Maison C, Almouzni G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J Cell Biol. 2004;166(4):493-505. doi: 10.1083/jcb.200403109.
10. Harmon B, Sedat J. Cell-by-cell dissection of gene expression and chromosomal interactions reveals consequences of nuclear reorganization. PLoS Biol. 2005;3(3):e67. doi: 10.1371/journal.pbio.0030067.
11. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM. The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev. 2010;24(8):766-82. doi: 10.1101/gad.559610.
12. Andrulis ED, Neiman AM, Zappulla DC, Sternglanz R. Perinuclear localization of chromatin facilitates transcriptional silencing. Nature. 1998;394(6693):592-5. doi: 10.1038/29100.
13. Simmer F, Buscaino A, Kos-Braun IC, Kagansky A, Boukaba A, Urano T, et al. Hairpin RNA induces secondary small interfering RNA synthesis and silencing in trans in fission yeast. EMBO Rep. 2010;11(2):112-8. doi: 10.1038/embor.2009.273.
14. Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, Thompson JK, et al. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell. 2005;121(1):13-24. doi: 10.1016/j.cell.2005.01.036.
15. Solovei I, Kreysing M, Lanctot C, Kosem S, Peichl L, Cremer T, et al. Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell. 2009;137(2):356-68. doi: 10.1016/j.cell.2009.01.052.
16. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell. 2013;152(3):584-98. doi: 10.1016/j.cell.2013.01.009.
17. Jost KL, Bertulat B, Cardoso MC. Heterochromatin and gene positioning: inside, outside, any side? Chromosoma. 2012;121(6):555-63. doi: 10.1007/s00412-012-0389-2.
18. Brero A, Easwaran HP, Nowak D, Grunewald I, Cremer T, Leonhardt H, et al. Methyl CpG-binding proteins induce large-scale chromatin reorganization during terminal differentiation. J Cell Biol. 2005;169(5):733-43. doi: 10.1083/jcb.200502062.
19. Bertulat B, De Bonis ML, Della Ragione F, Lehmkuhl A, Milden M, Storm C, et al. MeCP2 dependent heterochromatin reorganization during neural differentiation of a novel Mecp2-deficient embryonic stem cell reporter line. PLoS One. 2012;7(10):e47848. doi: 10.1371/journal.pone.0047848.
20. Baccarini P. Sulle cinesi vegeative del "Cynomorium coccineum L.". Nuovo Girornale botanico italiano Nuova serie. 1908;15(2):189-203.
21. Fransz P, De Jong JH, Lysak M, Castiglione MR, Schubert I. Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci USA. 2002;99(22):14584-9. doi: 10.1073/pnas.212325299.
22. Fransz P, Soppe W, Schubert I. Heterochromatin in interphase nuclei of Arabidopsis thaliana. Chromosome Res Int J Mol Supramol Evol Asp Chromosome Biol. 2003;11(3):227-40.
23. Meaburn KJ, Misteli T. Locus-specific and activity-independent gene repositioning during early tumorigenesis. J Cell Biol. 2008;180(1):39-50. doi: 10.1083/jcb.200708204.
24. Takizawa T, Gudla PR, Guo L, Lockett S, Misteli T. Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev. 2008;22(4):489-98. doi: 10.1101/gad.1634608.
25. Szczerbal I, Foster HA, Bridger JM. The spatial repositioning of adipogenesis genes is correlated with their expression status in a porcine mesenchymal stem cell adipogenesis model system. Chromosoma. 2009;118(5):647-63. doi: 10.1007/s00412-009-0225-5.
26. Reddy KL, Zullo JM, Bertolino E, Singh H. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature. 2008;452(7184):243-7. doi: 10.1038/nature06727.
27. Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E, Perry P, et al. Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet. 2008;4(3):e1000039. doi: 10.1371/journal.pgen.1000039.
28. Takizawa T, Meaburn KJ, Misteli T. The meaning of gene positioning. Cell. 2008;135(1):9-13. doi: 10.1016/J.Cell.2008.09.026.
29. Ferrai C, de Castro IJ, Lavitas L, Chotalia M, Pombo A. Gene positioning. Cold Spring Harb Perspect Biol. 2010;2(6):a000588. doi: 10.1101/cshperspect.a000588.
30. Mayer R, Brero A, von Hase J, Schroeder T, Cremer T, Dietzel S. Common themes and cell type specific variations of higher order chromatin arrangements in the mouse. BMC Cell Biol. 2005;6:44. doi: 10.1186/1471-2121-6-44.
31. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell. 2006;10(1):105-16. doi: 10.1016/j.devcel.2005.10.017.
32. Park SH, Kook MC, Kim EY, Park S, Lim JH. Ultrastructure of human embryonic stem cells and spontaneous and retinoic acid-induced differentiating cells. Ultrastruct Pathol. 2004;28(4):229-38.
33. Jost KL, Haase S, Smeets D, Schrode N, Schmiedel JM, Bertulat B, et al. 3D-Image analysis platform monitoring relocation of pluripotency genes during reprogramming. Nucleic Acids Res. 2011;39(17):e113. doi: 10.1093/nar/gkr486.
34. Irintchev A, Langer M, Zweyer M, Theisen R, Wernig A. Functional improvement of damaged adult mouse muscle by implantation of primary myoblasts. J Physiol. 1997;500(Pt 3):775-85.
35. Kaufmann U, Kirsch J, Irintchev A, Wernig A, Starzinski-Powitz A. The M-cadherin catenin complex interacts with microtubules in skeletal muscle cells: implications for the fusion of myoblasts. J Cell Sci. 1999;112(Pt 1):55-68.
36. Agarwal N, Hardt T, Brero A, Nowak D, Rothbauer U, Becker A, et al. MeCP2 interacts with HP1 and modulates its heterochromatin association during myogenic differentiation. Nucleic Acids Res. 2007;35(16):5402-8. doi: 10.1093/nar/gkm599.
37. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37(1):1-13. doi: 10.1093/nar/gkn923.
38. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57. doi: 10.1038/nprot.2008.211.
39. Colantuoni C, Jeon OH, Hyder K, Chenchik A, Khimani AH, Narayanan V, et al. Gene expression profiling in postmortem Rett syndrome brain: differential gene expression and patient classification. Neurobiol Dis. 2001;8(5):847-65. doi: 10.1006/nbdi.2001.0428.
40. Tudor M, Akbarian S, Chen RZ, Jaenisch R. Transcriptional profiling of a mouse model for Rett syndrome reveals subtle transcriptional changes in the brain. Proc Natl Acad Sci USA. 2002;99(24):15536-41. doi: 10.1073/pnas.242566899.
41. Ballestar E, Ropero S, Alaminos M, Armstrong J, Setien F, Agrelo R, et al. The impact of MECP2 mutations in the expression patterns of Rett syndrome patients. Hum Genet. 2005;116(1-2):91-104. doi: 10.1007/s00439-004-1200-0.
42. Delgado IJ, Kim DS, Thatcher KN, LaSalle JM, Van den Veyver IB. Expression profiling of clonal lymphocyte cell cultures from Rett syndrome patients. BMC Med Genet. 2006;7:61. doi: 10.1186/1471-2350-7-61.
43. Sabbattini P, Lundgren M, Georgiou A, Chow C, Warnes G, Dillon N. Binding of Ikaros to the lambda5 promoter silences transcription through a mechanism that does not require heterochromatin formation. EMBO J. 2001;20(11):2812-22. doi: 10.1093/emboj/20.11.2812.
44. Kosak ST, Skok JA, Medina KL, Riblet R, Le Beau MM, Fisher AG, et al. Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science. 2002;296(5565):158-62. doi: 10.1126/science.1068768.
45. Kumaran RI, Spector DL. A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J Cell Biol. 2008;180(1):51-65. doi: 10.1083/jcb.200706060.
46. Sadoni N, Targosz BS, Englmann A, Fesser S, Koch J, Schindelhauer D, et al. Transcription-dependent spatial arrangements of CFTR and conserved adjacent loci are not conserved in human and murine nuclei. Chromosoma. 2008;117(4):381-97. doi: 10.1007/s00412-008-0157-5.
47. Zink D, Amaral MD, Englmann A, Lang S, Clarke LA, Rudolph C, et al. Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei. J Cell Biol. 2004;166(6):815-25. doi: 10.1083/jcb.200404107.
48. Blobel G. Gene gating: a hypothesis. Proc Natl Acad Sci USA. 1985;82(24):8527-9.
49. Akhtar A, Gasser SM. The nuclear envelope and transcriptional control. Nat Rev Genet. 2007;8(7):507-17. doi: 10.1038/nrg2122.
50. Bi X. Heterochromatin structure: lessons from the budding yeast. IUBMB Life. 2014;66(10):657-66. doi: 10.1002/iub.1322.
51. Egecioglu D, Brickner JH. Gene positioning and expression. Curr Opin Cell Biol. 2011;23(3):338-45. doi: 10.1016/j.ceb.2011.01.001.
52. Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci USA. 2002;99(6):3740-5. doi: 10.1073/pnas.052410099.
53. Saxonov S, Berg P, Brutlag DL. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci USA. 2006;103(5):1412-7. doi: 10.1073/pnas.0510310103.
54. Mouse Genome Sequencing C, Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, et al. Initial sequencing and comparative analysis of the mouse genome. Nature. 2002;420(6915):520-62. doi: 10.1038/nature01262.
55. Britten RJ, Davidson EH. Gene regulation for higher cells: a theory. Science. 1969;165(891):349-57.
56. Jacob F, Monod J. Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol. 1961;3:318-56.
57. Chueh AC, Northrop EL, Brettingham-Moore KH, Choo KH, Wong LH. LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin. PLoS Genet. 2009;5(1):e1000354. doi: 10.1371/journal.pgen.1000354.
58. Caron H, van Schaik B, van der Mee M, Baas F, Riggins G, van Sluis P, et al. The human transcriptome map: clustering of highly expressed genes in chromosomal domains. Science. 2001;291(5507):1289-92. doi: 10.1126/science.1056794.
59. Lercher MJ, Urrutia AO, Hurst LD. Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat Genet. 2002;31(2):180-3. doi: 10.1038/ng887.
60. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249-64. doi: 10.1093/biostatistics/4.2.249.
61. Jost KL, Rottach A, Milden M, Bertulat B, Becker A, Wolf P, et al. Generation and characterization of rat and mouse monoclonal antibodies specific for MeCP2 and their use in X-inactivation studies. PLoS One. 2011;6(11):e26499. doi: 10.1371/journal.pone.0026499.
62. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Chen Y, et al. Ensembl 2011. Nucleic Acids Res. 2011;39(Database issue):D800-6. doi: 10.1093/nar/gkq1064.
63. Smit AFA, Hubley R, Grenn P. RepeatMasker Open-4.0. 2013-2015. http://www.repeatmasker.org.
64. Team RC. A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2015.