Abstract
The eukaryotic genome is packaged as chromatin within the three-dimensional nuclear space. Decades of cytological studies have revealed that chromosomes and genes are non-randomly localized within the nucleus and such organizations have important roles on genome function. However, several fundamental questions remain to be resolved. For example, what is required for the preferential localization of a gene to a nuclear landmark? What is the mechanism underlying gene repositioning in the nucleus? How does subnuclear gene positioning regulate gene transcription? Recent studies have revealed that several factors such as DNA sequence composition, specific regulatory sequences, epigenetic modifications, chromatin remodelers, post-transcriptional regulators and nuclear architectural proteins can influence chromatin dynamics and gene positioning in a gene-specific manner among organisms from yeast to human. In this review, we discuss some recent findings as well as experimental tools to investigate subnuclear gene positioning and to explore its implications in genome functions.
Similar content being viewed by others
References
Abruzzi K C, Belostotsky D A, Chekanova J A, Dower K, Rosbash M (2006). 3′-end formation signals modulate the association of genes with the nuclear periphery as well as mRNP dot formation. EMBO J, 25(18): 4253–4262
Ahmed S, Brickner D G, Light W H, Cajigas I, McDonough M, Froyshteter A B, Volpe T, Brickner J H (2010). DNA zip codes control an ancient mechanism for gene targeting to the nuclear periphery. Nat Cell Biol, 12(2): 111–118
Andrulis E D, Neiman A M, Zappulla D C, Sternglanz R (1998). Perinuclear localization of chromatin facilitates transcriptional silencing. Nature, 394(6693): 592–595
Ballester M, Kress C, Hue-Beauvais C, Kiêu K, Lehmann G, Adenot P, Devinoy E (2008). The nuclear localization of WAP and CSN genes is modified by lactogenic hormones in HC11 cells. J Cell Biochem, 105(1): 262–270
Belmont A S, Li G, Sudlow G, Robinett C (1999). Visualization of largescale chromatin structure and dynamics using the lac operator/lac repressor reporter system. Methods Cell Biol, 58: 203–222
Berezney R, Dubey D D, Huberman J A (2000). Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci. Chromosoma, 108(8): 471–484
Bian Q, Khanna N, Alvikas J, Belmont A S (2013). β-Globin cis-elements determine differential nuclear targeting through epigenetic modifications. J Cell Biol, 203(5): 767–783
Blobel G (1985). Gene gating: a hypothesis. Proc Natl Acad Sci USA, 82(24): 8527–8529
Boyle S, Gilchrist S, Bridger J M, Mahy N L, Ellis J A, Bickmore W A (2001). The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum Mol Genet, 10(3): 211–219
Branco M R, Pombo A (2006). Intermingling of chromosome territories in interphase suggests role in translocations and transcriptiondependent associations. PLoS Biol, 4(5): e138
Brickner D G, Cajigas I, Fondufe-Mittendorf Y, Ahmed S, Lee P C, Widom J, Brickner J H (2007). H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol, 5(4): e81
Brickner J H, Walter P (2004). Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol, 2(11): e342
Brown C R, Kennedy C J, Delmar V A, Forbes D J, Silver P A (2008a). Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev, 22(5): 627–639
Brown J M, Green J, das Neves R P, Wallace H A, Smith A J, Hughes J, Gray N, Taylor S, Wood W G, Higgs D R, Iborra F J, Buckle V J (2008b). Association between active genes occurs at nuclear speckles and is modulated by chromatin environment. J Cell Biol, 182(6): 1083–1097
Brown J M, Leach J, Reittie J E, Atzberger A, Lee-Prudhoe J, Wood W G, Higgs D R, Iborra F J, Buckle V J (2006). Coregulated human globin genes are frequently in spatial proximity when active. J Cell Biol, 172(2): 177–187
Brown K E, Baxter J, Graf D, Merkenschlager M, Fisher A G (1999). Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell, 3(2): 207–217
Brown K E, Guest S S, Smale S T, Hahm K, Merkenschlager M, Fisher A G (1997). Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell, 91(6): 845–854
Cabal G G, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O, Lesne A, Buc H, Feuerbach-Fournier F, Olivo-Marin J C, Hurt E C, Nehrbass U (2006). SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature, 441(7094): 770–773
Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer M W (2010). Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell, 140(3): 372–383
Casolari J M, Brown C R, Drubin D A, Rando O J, Silver P A (2005). Developmentally induced changes in transcriptional program alter spatial organization across chromosomes. Genes Dev, 19(10): 1188–1198
Casolari J M, Brown C R, Komili S, West J, Hieronymus H, Silver P A (2004). Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell, 117(4): 427–439
Chan E A, Teng G, Corbett E, Choudhury K R, Bassing C H, Schatz D G, Krangel MS (2013). Peripheral subnuclear positioning suppresses Tcrb recombination and segregates Tcrb alleles from RAG2. Proc Natl Acad Sci USA, 110(48): E4628–E4637
Chen B, Gilbert L A, Cimini B A, Schnitzbauer J, Zhang W, Li G W, Park J, Blackburn E H, Weissman J S, Qi L S, Huang B (2013). Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell, 155(7): 1479–1491
Chuang C H, Carpenter A E, Fuchsova B, Johnson T, de Lanerolle P, Belmont A S (2006). Long-range directional movement of an interphase chromosome site. Curr Biol, 16(8): 825–831
Croft J A, Bridger J M, Boyle S, Perry P, Teague P, Bickmore W A (1999). Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol, 145(6): 1119–1131
Csink A K, Henikoff S (1996). Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature, 381(6582): 529–531
de Wit E, de Laat W (2012). A decade of 3C technologies: insights into nuclear organization. Genes Dev, 26(1): 11–24
Dekker J, Rippe K, Dekker M, Kleckner N (2002). Capturing chromosome conformation. Science, 295(5558): 1306–1311
Deng W, Blobel G A (2013). Manipulating nuclear architecture. Curr Opin Genet Dev, 25C: 1–7
Deng W, Lee J, Wang H, Miller J, Reik A, Gregory P D, Dean A, Blobel G A (2012). Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell, 149(6): 1233–1244
Dernburg A F, Broman KW, Fung J C, Marshall WF, Philips J, Agard D A, Sedat J W (1996). Perturbation of nuclear architecture by longdistance chromosome interactions. Cell, 85(5): 745–759
Dieppois G, Iglesias N, Stutz F (2006). Cotranscriptional recruitment to the mRNA export receptor Mex67p contributes to nuclear pore anchoring of activated genes. Mol Cell Biol, 26(21): 7858–7870
Dimitrova D S, Gilbert D M (1999). The spatial position and replication timing of chromosomal domains are both established in early G1 phase. Mol Cell, 4(6): 983–993
Dirks R W, de Pauw E S, Raap A K (1997). Splicing factors associate with nuclear HCMV-IE transcripts after transcriptional activation of the gene, but dissociate upon transcription inhibition: evidence for a dynamic organization of splicing factors. J Cell Sci, 110(Pt 4): 515–522
Dostie J, Richmond T A, Arnaout R A, Selzer R R, Lee WL, Honan T A, Rubio E D, Krumm A, Lamb J, Nusbaum C, Green R D, Dekker J (2006). Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res, 16(10): 1299–1309
Drubin D A, Garakani A M, Silver P A (2006). Motion as a phenotype: the use of live-cell imaging and machine visual screening to characterize transcription-dependent chromosome dynamics. BMC Cell Biol, 7(1): 19
Dundr M, Ospina J K, Sung M H, John S, Upender M, Ried T, Hager G L, Matera A G (2007). Actin-dependent intranuclear repositioning of an active gene locus in vivo. J Cell Biol, 179(6): 1095–1103
Ferrai C, de Castro I J, Lavitas L, Chotalia M, Pombo A (2010). Gene positioning. Cold Spring Harb Perspect Biol, 2(6): a000588
Finlan L E, Sproul D, Thomson I, Boyle S, Kerr E, Perry P, Ylstra B, Chubb J R, Bickmore W A (2008). Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet, 4(3): e1000039
Fraser P, Bickmore W (2007). Nuclear organization of the genome and the potential for gene regulation. Nature, 447(7143): 413–417
Gaj T, Gersbach C A, Barbas C F 3rd (2013). ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol, 31(7): 397–405
Germann S, Juul-Jensen T, Letarnec B, Gaudin V (2006). DamID, a new tool for studying plant chromatin profiling in vivo, and its use to identify putative LHP1 target loci. Plant J, 48(1): 153–163
Geyer P K, Vitalini M W, Wallrath L L (2011). Nuclear organization: taking a position on gene expression. Curr Opin Cell Biol, 23(3): 354–359
Gilbert D M (2001). Nuclear position leaves its mark on replication timing. J Cell Biol, 152(2): F11–F15
Green EM, Jiang Y, Joyner R, Weis K (2012). A negative feedback loop at the nuclear periphery regulates GAL gene expression. Mol Biol Cell, 23(7): 1367–1375
Guelen L, Pagie L, Brasset E, Meuleman W, Faza M B, Talhout W, Eussen B H, de Klein A, Wessels L, de Laat W, van Steensel B (2008). Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature, 453(7197): 948–951
Haaf T, Schmid M (1991). Chromosome topology in mammalian interphase nuclei. Exp Cell Res, 192(2): 325–332
Hepperger C, Mannes A, Merz J, Peters J, Dietzel S (2008). Threedimensional positioning of genes in mouse cell nuclei. Chromosoma, 117(6): 535–551
Hewitt S L, High F A, Reiner S L, Fisher A G, Merkenschlager M (2004). Nuclear repositioning marks the selective exclusion of lineage-inappropriate transcription factor loci during T helper cell differentiation. Eur J Immunol, 34(12): 3604–3613
Hofmann W A, Johnson T, Klapczynski M, Fan J L, de Lanerolle P (2006). From transcription to transport: emerging roles for nuclear myosin I. Biochem Cell Biol, 84(4): 418–426
Horike S, Cai S, Miyano M, Cheng J F, Kohwi-Shigematsu T (2005). Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat Genet, 37(1): 31–40
Ishii K, Arib G, Lin C, Van Houwe G, Laemmli U K (2002). Chromatin boundaries in budding yeast: the nuclear pore connection. Cell, 109(5): 551–562
Isogai Y, Tjian R (2003). Targeting genes and transcription factors to segregated nuclear compartments. Curr Opin Cell Biol, 15(3): 296–303
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna J A, Charpentier E (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096): 816–821
Jost K L, Haase S, Smeets D, Schrode N, Schmiedel J M, Bertulat B, Herzel H, Cremer M, Cardoso M C (2011). 3D-Image analysis platform monitoring relocation of pluripotency genes during reprogramming. Nucleic Acids Res, 39(17): e113
Kalverda B, Fornerod M (2010). Characterization of genome-nucleoporin interactions in Drosophila links chromatin insulators to the nuclear pore complex. Cell Cycle, 9(24): 4812–4817
Kalverda B, Pickersgill H, Shloma V V, Fornerod M (2010). Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell, 140(3): 360–371
Kind J, Pagie L, Ortabozkoyun H, Boyle S, de Vries S S, Janssen H, Amendola M, Nolen L D, Bickmore W A, van Steensel B (2013). Single-cell dynamics of genome-nuclear lamina interactions. Cell, 153(1): 178–192
Kind J, van Steensel B (2010). Genome-nuclear lamina interactions and gene regulation. Curr Opin Cell Biol, 22(3): 320–325
Kohwi M, Lupton J R, Lai S L, Miller M R, Doe C Q (2013). Developmentally regulated subnuclear genome reorganization restricts neural progenitor competence in Drosophila. Cell, 152(1–2): 97–108
Kosak S T, Skok J A, Medina K L, Riblet R, Le Beau M M, Fisher A G, Singh H (2002). Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science, 296(5565): 158–162
Kouzine F, Liu J, Sanford S, Chung H J, Levens D (2004). The dynamic response of upstream DNA to transcription-generated torsional stress. Nat Struct Mol Biol, 11(11): 1092–1100
Kress C, Kiêu K, Droineau S, Galio L, Devinoy E (2011). Specific positioning of the casein gene cluster in active nuclear domains in luminal mammary epithelial cells. Chromosome Res, 19(8): 979–997
Kumaran R I, Spector D L (2008). A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J Cell Biol, 180(1): 51–65
Kundu S, Horn P J, Peterson C L (2007). SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster. Genes Dev, 21(8): 997–1004
Lamond A I, Sleeman J E (2003). Nuclear substructure and dynamics. Curr Biol, 13(21): R825–R828
Lanctôt C, Cheutin T, Cremer M, Cavalli G, Cremer T (2007). Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat Rev Genet, 8(2): 104–115
Lawrence J B, Clemson C M (2008). Gene associations: true romance or chance meeting in a nuclear neighborhood? J Cell Biol, 182(6): 1035–1038
Lee H, Quinn J C, Prasanth K V, Swiss V A, Economides K D, Camacho M M, Spector D L, Abate-Shen C (2006). PIAS1 confers DNAbinding specificity on the Msx1 homeoprotein. Genes Dev, 20(7): 784–794
Levsky J M, Singer R H (2003). Fluorescence in situ hybridization: past, present and future. J Cell Sci, 116(Pt 14): 2833–2838
Lieberman-Aiden E, van Berkum N L, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie B R, Sabo P J, Dorschner M O, Sandstrom R, Bernstein B, Bender M A, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny L A, Lander E S, Dekker J (2009). Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326(5950): 289–293
Lionnet T, Czaplinski K, Darzacq X, Shav-Tal Y, Wells A L, Chao J A, Park H Y, de Turris V, Lopez-Jones M, Singer R H (2011). A transgenic mouse for in vivo detection of endogenous labeled mRNA. Nat Methods, 8(2): 165–170
Luperchio T R, Wong X, Reddy K L (2014). Genome regulation at the peripheral zone: lamina associated domains in development and disease. Curr Opin Genet Dev, 25C: 50–61
Luthra R, Kerr S C, Harreman MT, Apponi L H, Fasken MB, Ramineni S, Chaurasia S, Valentini S R, Corbett A H (2007). Actively transcribed GAL genes can be physically linked to the nuclear pore by the SAGA chromatin modifying complex. J Biol Chem, 282(5): 3042–3049
Marko J F, Poirier M G (2003). Micromechanics of chromatin and chromosomes. Biochem Cell Biol, 81(3): 209–220
Mattout A, Meshorer E (2010). Chromatin plasticity and genome organization in pluripotent embryonic stem cells. Curr Opin Cell Biol, 22(3): 334–341
Matzke A J, Huettel B, van der Winden J, Matzke M(2005). Use of twocolor fluorescence-tagged transgenes to study interphase chromosomes in living plants. Plant Physiol, 139(4): 1586–1596
Meaburn K J, Gudla P R, Khan S, Lockett S J, Misteli T (2009). Diseasespecific gene repositioning in breast cancer. J Cell Biol, 187(6): 801–812
Meaburn K J, Misteli T (2008). Locus-specific and activity-independent gene repositioning during early tumorigenesis. J Cell Biol, 180(1): 39–50
Meister P, Towbin B D, Pike B L, Ponti A, Gasser S M (2010). The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev, 24(8): 766–782
Meuleman W, Peric-Hupkes D, Kind J, Beaudry J B, Pagie L, Kellis M, Reinders M, Wessels L, van Steensel B (2013). Constitutive nuclear lamina-genome interactions are highly conserved and associated with A/T-rich sequence. Genome Res, 23(2): 270–280
Mewborn S K, Puckelwartz M J, Abuisneineh F, Fahrenbach J P, Zhang Y, MacLeod H, Dellefave L, Pytel P, Selig S, Labno C M, Reddy K, Singh H, McNally E (2010). Altered chromosomal positioning, compaction, and gene expression with a lamin A/C gene mutation. PLoS ONE, 5(12): e14342
Misteli T (2007). Beyond the sequence: cellular organization of genome function. Cell, 128(4): 787–800
Miyanari Y, Ziegler-Birling C, Torres-Padilla M E (2013). Live visualization of chromatin dynamics with fluorescent TALEs. Nat Struct Mol Biol, 20(11): 1321–1324
Moen P T Jr, Johnson C V, Byron M, Shopland L S, de la Serna I L, Imbalzano A N, Lawrence J B (2004). Repositioning of musclespecific genes relative to the periphery of SC-35 domains during skeletal myogenesis. Mol Biol Cell, 15(1): 197–206
Nagano T, Lubling Y, Stevens T J, Schoenfelder S, Yaffe E, Dean W, Laue E D, Tanay A, Fraser P (2013). Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature, 502(7469): 59–64
Naumova N, Smith E M, Zhan Y, Dekker J (2012). Analysis of longrange chromatin interactions using Chromosome Conformation Capture. Methods, 58(3): 192–203
Németh A, Conesa A, Santoyo-Lopez J, Medina I, Montaner D, Péterfia B, Solovei I, Cremer T, Dopazo J, Längst G (2010). Initial genomics of the human nucleolus. PLoS Genet, 6(3): e1000889
Neumann F R, Dion V, Gehlen L R, Tsai-Pflugfelder M, Schmid R, Taddei A, Gasser S M (2012). Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev, 26(4): 369–383
O’Gorman S, Fox D T, Wahl G M (1991). Recombinase-mediated gene activation and site-specific integration in mammalian cells. Science, 251(4999): 1351–1355
Osborne C S, Chakalova L, Brown K E, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell J A, Lopes S, Reik W, Fraser P (2004). Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet, 36(10): 1065–1071
Osborne C S, Chakalova L, Mitchell J A, Horton A, Wood A L, Bolland D J, Corcoran A E, Fraser P (2007). Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol, 5(8): e192
Parada L, Misteli T (2002). Chromosome positioning in the interphase nucleus. Trends Cell Biol, 12(9): 425–432
Patel N S, Rhinn M, Semprich C I, Halley P A, Dollé P, Bickmore W A, Storey K G (2013). FGF signalling regulates chromatin organisation during neural differentiation via mechanisms that can be uncoupled from transcription. PLoS Genet, 9(7): e1003614
Pederson T (2002). Dynamics and genome-centricity of interchromatin domains in the nucleus. Nat Cell Biol, 4(12): E287–E291
Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman S W, Solovei I, Brugman W, Gräf S, Flicek P, Kerkhoven R M, van Lohuizen M, Reinders M, Wessels L, van Steensel B (2010). Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell, 38(4): 603–613
Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, van Steensel B (2006). Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet, 38(9): 1005–1014
Ragoczy T, Bender M A, Telling A, Byron R, Groudine M (2006). The locus control region is required for association of the murine betaglobin locus with engaged transcription factories during erythroid maturation. Genes Dev, 20(11): 1447–1457
Reddy K L, Zullo J M, Bertolino E, Singh H (2008). Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature, 452(7184): 243–247
Robinett C C, Straight A, Li G, Willhelm C, Sudlow G, Murray A, Belmont A S (1996). In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J Cell Biol, 135(6 Pt 2): 1685–1700
Rohner S, Kalck V, Wang X, Ikegami K, Lieb J D, Gasser S M, Meister P (2013). Promoter- and RNA polymerase II-dependent hsp-16 gene association with nuclear pores in Caenorhabditis elegans. J Cell Biol, 200(5): 589–604
Sarma N J, Haley TM, Barbara K E, Buford T D, Willis K A, Santangelo G M (2007). Glucose-responsive regulators of gene expression in Saccharomyces cerevisiae function at the nuclear periphery via a reverse recruitment mechanism. Genetics, 175(3): 1127–1135
Schermelleh L, Carlton P M, Haase S, Shao L, Winoto L, Kner P, Burke B, Cardoso M C, Agard D A, Gustafsson M G, Leonhardt H, Sedat J W (2008). Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science, 320(5881): 1332–1336
Schmid M, Arib G, Laemmli C, Nishikawa J, Durussel T, Laemmli U K (2006). Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol Cell, 21(3): 379–391
Schoenfelder S, Sexton T, Chakalova L, Cope N F, Horton A, Andrews S, Kurukuti S, Mitchell J A, Umlauf D, Dimitrova D S, Eskiw C H, Luo Y, Wei C L, Ruan Y, Bieker J J, Fraser P (2010). Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet, 42(1): 53–61
Schröck E, du Manoir S, Veldman T, Schoell B, Wienberg J, Ferguson-Smith M A, Ning Y, Ledbetter D H, Bar-Am I, Soenksen D, Garini Y, Ried T (1996). Multicolor spectral karyotyping of human chromosomes. Science, 273(5274): 494–497
Sexton T, Schober H, Fraser P, Gasser S M (2007). Gene regulation through nuclear organization. Nat Struct Mol Biol, 14(11): 1049–1055
Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, deWit E, van Steensel B, de Laat W (2006). Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet, 38(11): 1348–1354
Simonis M, Kooren J, de Laat W (2007). An evaluation of 3C-based methods to capture DNA interactions. Nat Methods, 4(11): 895–901
Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C, Cmarko D, Cremer C, Fakan S, Cremer T (2002). Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res, 276(1): 10–23
Solovei I, Kreysing M, Lanctôt C, Kösem S, Peichl L, Cremer T, Guck J, Joffe B (2009). Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell, 137(2): 356–368
Spector D L (2001). Nuclear domains. J Cell Sci, 114(Pt 16): 2891–2893
Splinter E, de Wit E, Nora E P, Klous P, van de Werken H J, Zhu Y, Kaaij L J, van Ijcken W, Gribnau J, Heard E, de Laat W (2011). The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev, 25(13): 1371–1383
Steglich B, Filion G J, 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(1): 77–87
Sun H B, Shen J, Yokota H (2000). Size-dependent positioning of human chromosomes in interphase nuclei. Biophys J, 79(1): 184–190
Szczerbal I, Foster H A, Bridger J M (2009). The spatial repositioning of adipogenesis genes is correlated with their expression status in a porcine mesenchymal stem cell adipogenesis model system. Chromosoma, 118(5): 647–663
Taddei A (2007). Active genes at the nuclear pore complex. Curr Opin Cell Biol, 19(3): 305–310
Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F, Schober H, Gasser S M (2006). Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature, 441(7094): 774–778
Takizawa T, Gudla P R, Guo L, Lockett S, Misteli T (2008a). Allelespecific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev, 22(4): 489–498
Takizawa T, Meaburn K J, Misteli T (2008b). The meaning of gene positioning. Cell, 135(1): 9–13
Tanabe H, Müller S, Neusser M, von Hase J, Calcagno E, Cremer M, Solovei I, Cremer C, Cremer T (2002). Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci USA, 99(7): 4424–4429
Tolhuis B, Blom M, Kerkhoven R M, Pagie L, Teunissen H, Nieuwland M, Simonis M, de Laat W, van Lohuizen M, van Steensel B (2011). Interactions among Polycomb domains are guided by chromosome architecture. PLoS Genet, 7(3): e1001343
Towbin B D, González-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser S M (2012). Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell, 150(5): 934–947
Towbin B D, Meister P, Pike B L, Gasser S M (2010). Repetitive transgenes in C. elegans accumulate heterochromatic marks and are sequestered at the nuclear envelope in a copy-number- and lamindependent manner. Cold Spring Harb Symp Quant Biol, 75(0): 555–565
Tumbar T, Belmont A S (2001). Interphase movements of a DNA chromosome region modulated by VP16 transcriptional activator. Nat Cell Biol, 3(2): 134–139
van Koningsbruggen S, Gierlinski M, Schofield P, Martin D, Barton G J, Ariyurek Y, den Dunnen J T, Lamond A I (2010). High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol Biol Cell, 21(21): 3735–3748
van Steensel B, Dekker J (2010). Genomics tools for unraveling chromosome architecture. Nat Biotechnol, 28(10): 1089–1095
van Steensel B, Henikoff S (2000). Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase. Nat Biotechnol, 18(4): 424–428
Vaquerizas J M, Suyama R, Kind J, Miura K, Luscombe N M, Akhtar A (2010). Nuclear pore proteins nup153 and megator define transcriptionally active regions in the Drosophila genome. PLoS Genet, 6(2): e1000846
Vermeulen M, Mulder K W, Denissov S, Pijnappel W W, van Schaik F M, Varier R A, Baltissen M P, Stunnenberg H G, Mann M, Timmers H T (2007). Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell, 131(1): 58–69
Vodala S, Abruzzi K C, Rosbash M (2008). The nuclear exosome and adenylation regulate posttranscriptional tethering of yeast GAL genes to the nuclear periphery. Mol Cell, 31(1): 104–113
Vogel M J, Peric-Hupkes D, van Steensel B (2007). Detection of in vivo protein-DNA interactions using DamID in mammalian cells. Nat Protoc, 2(6): 1467–1478
Williams R R, Azuara V, Perry P, Sauer S, Dvorkina M, Jørgensen H, Roix J, McQueen P, Misteli T, Merkenschlager M, Fisher A G (2006). Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J Cell Sci, 119(Pt 1): 132–140
Wu F, Yao J (2013). Spatial compartmentalization at the nuclear periphery characterized by genome-wide mapping. BMC Genomics, 14(1): 591
Xing Y, Johnson C V, Moen P T Jr, McNeil J A, Lawrence J (1995). Nonrandom gene organization: structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains. J Cell Biol, 131(6 Pt 2): 1635–1647
Yao J, Fetter R D, Hu P, Betzig E, Tjian R (2011). Subnuclear segregation of genes and core promoter factors in myogenesis. Genes Dev, 25(6): 569–580
Zink D, Amaral M D, Englmann A, Lang S, Clarke L A, Rudolph C, Alt F, Luther K, Braz C, Sadoni N, Rosenecker J, Schindelhauer D (2004). Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei. J Cell Biol, 166(6): 815–825
Zullo J M, Demarco I A, Piqué-Regi R, Gaffney D J, Epstein C B, Spooner C J, Luperchio T R, Bernstein B E, Pritchard J K, Reddy K L, Singh H (2012). DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell, 149(7): 1474–1487
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vishnoi, N., Yao, J. Gene positioning and genome function. Front. Biol. 9, 255–268 (2014). https://doi.org/10.1007/s11515-014-1313-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11515-014-1313-3