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A requiem to the nuclear matrix: from a controversial concept to 3D organization of the nucleus

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Abstract

The first papers coining the term “nuclear matrix” were published 40 years ago. Here, we review the data obtained during the nuclear matrix studies and discuss the contribution of this controversial concept to our current understanding of nuclear architecture and three-dimensional organization of genome.

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References

  • Albrethsen J, Knol JC, Jimenez CR (2009) Unravelling the nuclear matrix proteome. J Proteomics 72:71–81

    CAS  PubMed  Google Scholar 

  • Amankwah KS, De Boni U (1994) Ultrastructural localization of filamentous actin within neuronal interphase nuclei in situ. Exp Cell Res 210:315–325

    CAS  PubMed  Google Scholar 

  • Amati BB, Gasser SM (1988) Chromosomal ARS and CEN elements bind specifically to the yeast nuclear scaffold. Cell 54:967–978

    CAS  PubMed  Google Scholar 

  • Barboro P, D'Arrigo C, Diaspro A, Mormino M, Alberti I, Parodi S, Patrone E, Balbi C (2002) Unraveling the organization of the internal nuclear matrix: RNA-dependent anchoring of NuMA to a lamin scaffold. Exp Cell Res 279:202–218

    CAS  PubMed  Google Scholar 

  • Barboro P, D'Arrigo C, Mormino M, Coradeghini R, Parodi S, Patrone E, Balbi C (2003) An intranuclear frame for chromatin compartmentalization and higher-order folding. J Cell Biochem 88:113–120

    CAS  PubMed  Google Scholar 

  • Berezney R (1980) Fractionation of the nuclear matrix. I. Partial separation into matrix protein fibrils and a residual ribonucleoprotein fraction. J Cell Biol 85:641–650

    CAS  PubMed  Google Scholar 

  • Berezney R, Buchholtz LA (1981) Isolation and characterization of rat liver nuclear matrices containing high molecular weight deoxyribonucleic acid. Biochemistry 20:4995–5002

    CAS  PubMed  Google Scholar 

  • Berezney R, Coffey D (1974) Identification of a nuclear protein matrix. Biochem Biophys Res Commun 60:1410–1419

    CAS  PubMed  Google Scholar 

  • Berezney R, Coffey DS (1975) Nuclear protein matrix: association with newly synthesized DNA. Science 189:291–293

    CAS  PubMed  Google Scholar 

  • Berezney R, Coffey DS (1977) Nuclear matrix: isolation and characterization of a framework structure from rat liver nuclei. J Cell Biol 73:616–637

    CAS  PubMed Central  PubMed  Google Scholar 

  • Berezney R, Mortillaro MJ, Ma H, Wei X, Samarabandu J (1995) The nuclear matrix: a structural milieu for genomic function. Int Rev Cytol 1–65

  • Berrios M, Osheroff N, Fisher PA (1985) In situ localization of DNA topoisomerase II, a major polypeptide component of the Drosophila nuclear matrix fraction. Proc Natl Acad Sci U S A 82:4142–4146

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bickmore WA (2013) The spatial organization of the human genome. Ann Rev Genomics Human Genet 14:67–84

    CAS  Google Scholar 

  • Bodnar JW (1988) A domain model for eukaryotic DNA organization: a molecular basis for cell differentiation and chromosome evolution. J Theor Biol 132:479–507

    CAS  PubMed  Google Scholar 

  • Boulikas T (1993) Nature of DNA sequences at the attachment regions of genes to the nuclear matrix. J Cell Biochem 52:14–22

    CAS  PubMed  Google Scholar 

  • Brun C, Dang Q, Miassod R (1990) Studies of an 800-kilobase DNA stretch of the Drosophila X chromosome: comapping of a subclass of scaffold-attached regions with sequences able to replicate autonomously in Saccharomyces cerevisiae. Mol Cell Biol 10:5455–5463

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buongiorno-Nardelli M, Micheli G, Carri MT, Marilley M (1982) A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298:100–102

    CAS  PubMed  Google Scholar 

  • Cavalli G, Misteli T (2013) Functional implications of genome topology. Nat Struct Mol Biol 20:290–299

    CAS  PubMed  Google Scholar 

  • Cisse II, Izeddin I, Causse SZ, Boudarene L, Senecal A, Muresan L, Dugast-Darzacq C, Hajj B, Dahan M, Darzacq X (2013) Real-time dynamics of RNA polymerase II clustering in live human cells. Science 341:664–667

    CAS  PubMed  Google Scholar 

  • Cockerill PN, Garrard WT (1986a) Chromosomal loop anchorage sites appear to be evolutionarily conserved. FEBS Lett 204:5–7

    CAS  PubMed  Google Scholar 

  • Cockerill PN, Garrard WT (1986b) Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell 44:273–282

    CAS  PubMed  Google Scholar 

  • Cook PR, Brazell IA (1976) Conformational constraints in nuclear DNA. J Cell Sci 22:287–302

    CAS  PubMed  Google Scholar 

  • Cook PR, Brazell IA (1980) Mapping sequences in loops of nuclear DNA by their progressive detachment from the nuclear cage. Nucleic acids Res 8:2895–2906

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cook PR, Brazell IA, Jost E (1976) Characterization of nuclear structures containing superhelical DNA. J Cell Sci 22:303–324

    CAS  PubMed  Google Scholar 

  • Cook PR, Lang J, Hayday A, Lania L, Fried M, Chiswell DJ, Wyke A (1982) 1982. Active viral genes in transformed cells lie close to the nuclear cage. EMBO J 1:447–452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cremer T, Cremer M (2010) Chromosome territories. Cold Spring Harbor Perspect Biol 2:a003889

    Google Scholar 

  • Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schrock E, Speicher MR, Mathieu U, Jauch A, Emmerich P et al (1993) Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harbor Symp Quant Biol 58:777–792

    CAS  PubMed  Google Scholar 

  • Cremer M, von Hase J, Volm T, Brero A, Kreth G, Walter J, Fischer C, Solovei I, Cremer C, Cremer T (2001) Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosom Res 9:541–567

    CAS  Google Scholar 

  • Dion V, Gasser SM (2013) Chromatin movement in the maintenance of genome stability. Cell 152:1355–1364

    CAS  PubMed  Google Scholar 

  • Dostie J, Bickmore WA (2012) Chromosome organization in the nucleus - charting new territory across the Hi-Cs. Curr Opin Genet Dev 22:125–131

    CAS  PubMed  Google Scholar 

  • Eivazova ER, Gavrilov A, Pirozhkova I, Petrov A, Iarovaia OV, Razin SV, Lipinski M, Vassetzky YS (2009) Interaction in vivo between the two matrix attachment regions flanking a single chromatin loop. J Mol Biol 386:929–937

    CAS  PubMed  Google Scholar 

  • Feister HA, Onyia JE, Miles RR, Yang X, Galvin R, Hock JM, Bidwell JP (2000) The expression of the nuclear matrix proteins NuMA, topoisomerase II-alpha, and -beta in bone and osseous cell culture: regulation by parathyroid hormone. Bone 26:227–234

    CAS  PubMed  Google Scholar 

  • Fielding P, Fox CF (1970) Evidence for stable attachment of DNA to membrane at the replication origin of Escherichia coli. Biochem Biophys Res Commun 41:157–162

    CAS  PubMed  Google Scholar 

  • Gasser SM, Laemmli UK (1986a) Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell 46:521–530

    CAS  PubMed  Google Scholar 

  • Gasser SM, Laemmli UK (1986b) The organization of chromatin loops : characterization of a scaffold attachment site. EMBO J 5:511–518

    CAS  PubMed Central  PubMed  Google Scholar 

  • Georgiev GP, Chentsov IS (1963) On ultrastructure of the nucleus on the basis of electron microscopy of isolated nuclei subjected to salt extracts. Biofizika 8:50–57

    CAS  PubMed  Google Scholar 

  • Gerner C, Holzmann K, Meissner M, Gotzmann J, Grimm R, Sauermann G (1999) Reassembling proteins and chaperones in human nuclear matrix protein fractions. J Cell Biochem 74:145–151

    CAS  PubMed  Google Scholar 

  • Gromova II, Nielsen OF, Razin SV (1995) Long-range fragmentation of the eukaryotic genome by exogenous and endogenous nucleases proceeds in a specific fashion via preferential DNA cleavage at matrix attachment sites. J Biol Chem 270:18685–18690

    CAS  PubMed  Google Scholar 

  • Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W et al (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–951

    CAS  PubMed  Google Scholar 

  • Gueth-Hallonet C, Wang J, Harborth J, Weber K, Osborn M (1998) Induction of a regular nuclear lattice by overexpression of NuMA. Exp Cell Res 243:434–452

    CAS  PubMed  Google Scholar 

  • Hacisuleyman, E., Goff, L.A., Trapnell, C., Williams, A., Henao-Mejia, J., Sun, L., McClanahan, P., Hendrickson, D.G., Sauvageau, M., Kelley, D.R., et al. (2014). Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nature structural & molecular biology

  • Hancock R (1982) Topological organisation of interphase DNA: the nuclear matrix and other skeletal structures. Biol Cell 46:105–122

    CAS  Google Scholar 

  • Hancock R (2000) A new look at the nuclear matrix. Chromosoma 109:219–225

    CAS  PubMed  Google Scholar 

  • Hancock R (2004) Internal organisation of the nucleus: assembly of compartments by macromolecular crowding and the nuclear matrix model. Biol Cell 96:595–601

    CAS  PubMed  Google Scholar 

  • Hancock R (2014) The crowded nucleus. Int Rev Mol Biol 307:15–26

    Google Scholar 

  • Hartwig M (1982) The size of independently supercoiled domains in nuclear DNA from normal human lymphocytes and leukemic lymphoblasts. Biochim Biophys Acta 698:214–217

    CAS  PubMed  Google Scholar 

  • He DC, Martin T, Penman S (1991) Localization of heterogeneous nuclear ribonucleoprotein in the interphase nuclear matrix core filaments and on perichromosomal filaments at mitosis. Proc Natl Acad Sci U S A 88:7469–7473

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hempel K, Stratling WH (1996) The chicken lysozyme gene 5' MAR and the Drosophila histone SAR are electroelutable from encapsulated and digested nuclei. J Cell Sci 109(Pt 6):1459–1469

    CAS  PubMed  Google Scholar 

  • Hozak P, Hassan AB, Jakson DA, Cook PR (1993) Visualization of replication factories attached to a nucleoskeleton. Cell 73:361–373

    CAS  PubMed  Google Scholar 

  • Hozak P, Sasseville AM, Raymond Y, Cook PR (1995) Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J Cell Sci 108:635–644

    CAS  PubMed  Google Scholar 

  • Hunt BF, Vogelstein B (1981) Association of newly replicated DNA with the nuclear matrix of Physarum polycephalum. Nucleic acids Res 9:349–363

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iarovaia O, Hancock R, Lagarkova M, Miassod R, Razin SV (1996) Mapping of genomic DNA loop organization in a 500-kilobase region of the Drosophila X chromosome by the topoisomerase II-mediated DNA loop excision protocol. Mol Cell Biol 16:302–308

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iarovaia OV, Bystritskiy A, Ravcheev D, Hancock R, Razin SV (2004) Visualization of individual DNA loops and a map of loop domains in the human dystrophin gene. Nucleic acids Res 32:2079–2086

    CAS  PubMed Central  PubMed  Google Scholar 

  • Infante AA, Firshein W, Hobart P, Murray L (1976) A nuclear membrane-associated DNA complex in cultured mammalian cells capable of synthesizing DNA in vitro. Biochemistry 15:4810–4817

    CAS  PubMed  Google Scholar 

  • Jack RS, Eggert H (1992) The elusive nuclear matrix. Eur J Biochem 209:503–509

    CAS  PubMed  Google Scholar 

  • Jackson DA, Cook PR (1985) Transcription occurs at a nucleoskeleton. EMBO J 4:919–925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jackson D, Cook P (1988) Visualization of a filamentous nucleoskeleton with a 23 nm axial repeat. EMBO J 7:3667–3677

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jackson DA, Cook PR (1995) The structural basis of nuclear function. Int Rev Cytol 162A:125–149

    CAS  PubMed  Google Scholar 

  • Jackson DA, McCready SJ, Cook PR (1981) RNA is synthesized at the nuclear cage. Nature 292:552–555

    CAS  PubMed  Google Scholar 

  • Jost J-P, Seldran M (1984) Association of transcriptionally active vitellogenin II gene with the nuclear matrix of chicken liver. EMBO J 3:2205–2208

    Google Scholar 

  • Kaufmann SH, Shaper JH (1991) Association of topoisomerase II with the hepatoma cell nuclear matrix: the role of intermolecular disulfide bond formation. Exp Cell Res 192:511–523

    CAS  PubMed  Google Scholar 

  • Kaufmann SH, Coffey DS, Shaper JH (1981) Considerations in the isolation of rat liver nuclear matrix, nuclear envelope, and pore complex lamina. Exp Cell Res 132:105–123

    CAS  PubMed  Google Scholar 

  • Kind J, Pagie L, Ortabozkoyun H, Boyle S, de Vries SS, Janssen H, Amendola M, Nolen LD, Bickmore WA, van Steensel B (2013) Single-cell dynamics of genome-nuclear lamina interactions. Cell 153:178–192

    CAS  PubMed  Google Scholar 

  • Kitamura E, Blow JJ, Tanaka TU (2006) Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories. Cell 125:1297–1308

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lagarkova MA, Svetlova E, Giacca M, Falaschi A, Razin SV (1998) DNA loop anchorage region colocalizes with the replication origin located downstream to the human gene encoding lamin B2. J Cell Biochem 69:13–18

    CAS  PubMed  Google Scholar 

  • Lebkowski JS, Laemmli UK (1982) Evidence for two levels of DNA folding in histone-depleted HeLa interphase nuclei. J Mol Biol 156:309–324

    CAS  PubMed  Google Scholar 

  • Legartova, S., Stixova, L., Laur, O., Kozubek, S., Sehnalova, P., and Bartova, E. (2013). Nuclear structures surrounding internal lamin invaginations. J Cell Biochem

  • Lemaitre JM, Danis E, Pasero P, Vassetzky Y, Mechali M (2005) Mitotic remodeling of the replicon and chromosome structure. Cell 123:787–801

    CAS  PubMed  Google Scholar 

  • Levi V, Ruan Q, Plutz M, Belmont AS, Gratton E (2005) Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys J 89:4275–4285

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lewis CD, Lebkowski JS, Daly AK, Laemmli UK (1984) Interphase nuclear matrix and metaphase scaffolding structures. J Sci Suppl 1:103–122

    CAS  Google Scholar 

  • Long BH, Huang CY, Pogo AO (1979) Isolation and characterization of the nuclear matrix in Friend erythroleukemia cells: chromatin and hnRNA interactions with the nuclear matrix. Cell 18:1079–1090

    CAS  PubMed  Google Scholar 

  • Ma H, Siegel AJ, Berezney R (1999) Association of chromosome territories with the nuclear matrix. Disruption of human chromosome territories correlates with the release of a subset of nuclear matrix proteins. J Cell Biol 146:531–542

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marshall WF (2002) Order and disorder in the nucleus. Curr Biol 12:R185–R192

    CAS  PubMed  Google Scholar 

  • Marshall WF, Straight A, Marko JF, Swedlow J, Dernburg A, Belmont A, Murray AW, Agard DA, Sedat JW (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol 7:930–939

    CAS  PubMed  Google Scholar 

  • Martelli AM, Falcieri E, Gobbi P, Manzoli L, Gilmour RS, Cocco L (1991) Heat-induced stabilization of the nuclear matrix: a morphological and biochemical analysis in murine erythroleukemia cells. Exp Cell Res 196:216–225

    CAS  PubMed  Google Scholar 

  • Martelli AM, Manzoli L, Rubbini S, Billi AM, Bareggi R, Cocco L (1995) The protein composition of Friend cell nuclear matrix stabilized by various treatments. Different recovery of nucleolar proteins B23 and C23 and nuclear lamins. Biol Cell 83:15–22

    CAS  PubMed  Google Scholar 

  • Mattern KA, Humbel BM, Muijsers AO, de Jong L, van Driel R (1996) hnRNP proteins and B23 are the major proteins of the internal nuclear matrix of HeLa S3 cells. J Cell Biochem 62:275–289

    CAS  PubMed  Google Scholar 

  • Mattern KA, van Goethem RE, de Jong L, van Driel R (1997) Major internal nuclear matrix proteins are common to different human cell types. J Cell Biochem 65:42–52

    CAS  PubMed  Google Scholar 

  • McCready SJ, Godwin J, Mason DW, Brazell IA, Cook PR (1980) DNA is replicated at the nuclear cage. J Cell Sci 46:365–386

    CAS  PubMed  Google Scholar 

  • Meister P, Taddei A (2013) Building silent compartments at the nuclear periphery: a recurrent theme. Curr Opin Genet Dev 23:96–103

    CAS  PubMed  Google Scholar 

  • Menz K, Radomski N, Jost E (1996) INMP, a novel intranuclear matrix protein related to the family of intermediate filament-like proteins: molecular cloning and sequence analysis. Biochim Biophys Acta 1309:14–20

    CAS  PubMed  Google Scholar 

  • Mika S, Rost B (2005) NMPdb: database of nuclear matrix proteins. Nucleic acids Res 33:D160–D163

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mirkovitch J, Mirault ME, Laemmli UK (1984) Organization of the higher-order chromatin loop : specific DNA attachment sites on nuclear scaffold. Cell 39:223–232

    CAS  PubMed  Google Scholar 

  • Mullenders LH, van Zeeland AA, Natarajan AT (1983) Comparison of DNA loop size and super-coiled domain size in human cells. Mutat Res 112:245–252

    CAS  PubMed  Google Scholar 

  • Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E, Dean W, Laue ED, Tanay A, Fraser P (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502:59–64

    CAS  PubMed  Google Scholar 

  • Nakagomi K, Kohwi Y, Dickinson LA, Kohwishigematsu T (1994) A novel DNA-binding motif in the nuclear matrix attachment DNA-binding protein SATB1. Mol Cell Biol 14:1852–1860

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakayasu H, Berezney R (1991) Nuclear matrins: identification of the major nuclear matrix proteins. Proc Natl Acad Sci U S A 88:10312–10316

    CAS  PubMed Central  PubMed  Google Scholar 

  • Narayan KS, Steele WJ, Smetana K, Busch H (1967) Ultrastructural aspects of the ribonucleo-protein network in nuclei of Walker tumor and rat liver. Exp Cell Res 46:65–77

    CAS  PubMed  Google Scholar 

  • Neri LM, Bortul R, Zweyer M, Tabellini G, Borgatti P, Marchisio M, Bareggi R, Capitani S, Martelli AM (1999) Influence of different metal ions on the ultrastructure, biochemical properties, and protein localization of the K562 cell nuclear matrix. J Cell Biochem 73:342–354

    CAS  PubMed  Google Scholar 

  • Nickerson J (2001) Experimental observations of a nuclear matrix. J Cell Sci 114:463–474

    CAS  PubMed  Google Scholar 

  • Nickerson JA, Krochmalnic G, Wan KM, Penman S (1989) Chromatin architecture and nuclear RNA. Proc Natl Acad Sci U S A 86:177–181

    CAS  PubMed Central  PubMed  Google Scholar 

  • O'Brien RL, Sanyal AB, Stanton RH (1972) Association of DNA replication with the nuclear membrane of HeLa cells. Exp Cell Res 70:106–112

    PubMed  Google Scholar 

  • Ohlsson R, Bartkuhn M, Renkawitz R (2010) CTCF shapes chromatin by multiple mechanisms: the impact of 20 years of CTCF research on understanding the workings of chromatin. Chromosoma 119:351–360

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paulson JR, Laemmli UK (1977) The structure of histone-depleted metaphase chromosomes. Cell 12:817–825

    CAS  PubMed  Google Scholar 

  • Pederson T (1998) Thinking about a nuclear matrix. J Mol Biol 277:147–159

    CAS  PubMed  Google Scholar 

  • Pederson T (2000) Half a century of “the nuclear matrix”. Mol Biol Cell 11:799–805

    CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips-Cremins JE, Sauria ME, Sanyal A, Gerasimova TI, Lajoie BR, Bell JS, Ong CT, Hookway TA, Guo C, Sun Y et al (2013) Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153:1281–1295

    CAS  PubMed  Google Scholar 

  • Pliss A, Malyavantham KS, Bhattacharya S, Berezney R (2013) Chromatin dynamics in living cells: identification of oscillatory motion. J Cell Physiol 228:609–616

    CAS  PubMed  Google Scholar 

  • Politz JC, Scalzo D, Groudine M (2013) Something silent this way forms: the functional organization of the repressive nuclear compartment. Ann Rev cell Dev Biol 29:241–270

    CAS  Google Scholar 

  • Razin SV (1987) DNA interactions with the nuclear matrix and spatial organization of replication and transcription. Bio Essays 6:19–23

    CAS  Google Scholar 

  • Razin SV (1996) Functional architecture of chromosomal DNA domains. Crit Rev Eukaryot Gene Expr 6:247–269

    CAS  PubMed  Google Scholar 

  • Razin SV, Gromova II (1995) The channels model of nuclear matrix structure. Bioessays 17:443–450

    CAS  PubMed  Google Scholar 

  • Razin SV, Mantieva VL, Georgiev GP (1978) DNA adjacent to attachment points of deoxyribonucleoprotein fibril to chromosomal axial structure is enriched in reiterated base sequences. Nucleic acids Res 5:4737–4751

    CAS  PubMed Central  PubMed  Google Scholar 

  • Razin SV, Mantieva VL, Georgiev GP (1979) The similarity of DNA sequences remaining bound to scaffold upon nuclease treatment of interphase nuclei and metaphase chromosomes. Nucleic acids Res 7:1713–1735

    CAS  PubMed Central  PubMed  Google Scholar 

  • Razin SV, Rzeszowska WJ, Moreau J, Scherrer K (1985) Localization of regions of DNA attachment to the nuclear matrix within the chicken alpha-globin genes in functionally active and functionally inactive nuclei. Molekularnaya Biologia 19:456–466

    CAS  Google Scholar 

  • Razin SV, Kekelidze MG, Lukanidin EM, Scherrer K, Georgiev GP (1986) Replication origins are attached to the nuclear skeleton. Nucleic acids Res 14:8189–8207

    CAS  PubMed Central  PubMed  Google Scholar 

  • Razin SV, Petrov P, Hancock R (1991) Precise localization of the alpha-globin gene cluster within one of the 20- to 300-kilobase DNA fragments released by cleavage of chicken chromosomal DNA at topoisomerase II sites in vivo: evidence that the fragments are DNA loops or domains. Proc Natl Acad Sci U S A 88:8515–8519

    CAS  PubMed Central  PubMed  Google Scholar 

  • Razin SV, Hancock R, Iarovaia O, Westergaard O, Gromova I, Georgiev GP (1993) Structural-functional organization of chromosomal DNA domains. Cold Spring Harb Symp Quant Bio3 58:25–35

    CAS  Google Scholar 

  • Razin SV, Gavrilov AA, Ioudinkova ES, Iarovaia OV (2013) Communication of genome regulatory elements in a folded chromosome. FEBS Lett 587:1840–1847

    CAS  PubMed  Google Scholar 

  • Robinson SI, Nelkin BD, Volgelstein B (1982) The ovalbumin gene is associated with the nuclear matrix of chicken oviduct cells. Cell 28:99–106

    CAS  PubMed  Google Scholar 

  • Robinson SI, Small D, Idzerda R, McKnight GS, Vogelstein B (1983) The association of active genes with the nuclear matrix of the chicken oviduct. Nucl Acids Res 15:5113–5130

    Google Scholar 

  • Rzeszowska-Wolny J, Razin S, Puvion E, Moreau J, Scherrer K (1988) Isolation and characterization of stable nuclear matrix preparations and associated DNA from avian erythroblasts. Biol Cell 64:13–22

    CAS  PubMed  Google Scholar 

  • Saner N, Karschau J, Natsume T, Gierlinski M, Retkute R, Hawkins M, Nieduszynski CA, Blow JJ, de Moura AP, Tanaka TU (2013) Stochastic association of neighboring replicons creates replication factories in budding yeast. J Cell Biol 202:1001–1012

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saredi A, Howard L, Compton DA (1996) NuMA assembles into an extensive filamentous structure when expressed in the cell cytoplasm. J Cell Sci 109(Pt 3):619–630

    CAS  PubMed  Google Scholar 

  • Small D, Nelkin B, Vogelstein B (1985) The association of transcribed genes with the nuclear matrix of Drosophila cells during heat shock. Nucl Acids Res 13:2413–2431

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sofueva S, Hadjur S (2012) Cohesin-mediated chromatin interactions—into the third dimension of gene regulation. Brief Funct Genomics 11:205–216

    CAS  PubMed  Google Scholar 

  • Sofueva S, Yaffe E, Chan WC, Georgopoulou D, Vietri Rudan M, Mira-Bontenbal H, Pollard SM, Schroth GP, Tanay A, Hadjur S (2013) Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J 32:3119–3129

    CAS  PubMed  Google Scholar 

  • Sueoka N, Quinn WG (1968) Membrane attachment of the chromosome replication origin in Bacillus subtilis. Cold Spring Harbor Symp Quant Biol 33:695–705

    CAS  PubMed  Google Scholar 

  • Tan JH, Wooley JC, LeStourgeon WM (2000) Nuclear matrix-like filaments and fibrogranular complexes form through the rearrangement of specific nuclear ribonucleoproteins. Mol Biol Cell 11:1547–1554

    CAS  PubMed Central  PubMed  Google Scholar 

  • Valkov NI, Gump JL, Sullivan DM (1997) Quantitative immunofluorescence and immunoelectron microscopy of the topoisomerase II alpha associated with nuclear matrices from wild-type and drug-resistant Chinese hamster ovary cell lines. J Cell Biochem 67:112–130

    CAS  PubMed  Google Scholar 

  • Vassetzky YS, Dang Q, Benedetti P, Gasser SM (1994) Topoisomerase II forms multimers in vitro: effects of metals, beta-glycerophosphate, and phosphorylation of its C-terminal domain. Mol Cell Biol 14:6962–6974

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vassetzky Y, Hair A, Mechali M (2000) Rearrangement of chromatin domains during development in Xenopus. Genes Dev 14:1541–1552

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vaughn JP, Dijkwel PA, Mullenders L, Hamlin JL (1990) Replication forks are associated with the nuclear matrix. Nucl Acids Res 18:1965–1969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Verheijen R, Van VT, Remaekers F (1988) The nuclear matrix : structure and composition. J Cell Sci 90:11–36

    PubMed  Google Scholar 

  • Visser AE, Jaunin F, Fakan S, Aten JA (2000) High resolution analysis of interphase chromosome domains. J Cell Sci 113:2585–2593

    CAS  PubMed  Google Scholar 

  • Vogelstein B, Pardoll DM, Coffey DS (1980) Supercoiled loops and eucaryotic DNA replication. Cell 22:79–85

    CAS  PubMed  Google Scholar 

  • Weintraub, H., and Groudine, M. (1976). Chromosomal subunits in active genes have an altered conformation. Science 93

  • Zbarsky IB, Debov SS (1949) On the proteins of the cell nuclei. Proc of the USSR Acad Sci 62:795–798

    Google Scholar 

  • Zeitz MJ, Malyavantham KS, Seifert B, Berezney R (2009) Matrin 3: chromosomal distribution and protein interactions. J Cell Biochem 108:125–133

    CAS  PubMed  Google Scholar 

  • Zeng C, He D, Brinkley BR (1994) Localization of NuMA protein isoforms in the nuclear matrix of mammalian cells. Cell Motil Cytoskeleton 29:167–176

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Presidium of the Russian Academy of Sciences (MCB grant to SVR), RFBR grants (12-04-93109, 14-04-00010 to SVR, and 13-04-93105 to OVI) and grants from INCa (ERABL) and ANRS (No 1154) to YSV.

Conflict of interests

The authors declare no conflict of interests.

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Authors and Affiliations

  1. Institute of Gene Biology of the Russian Academy of Sciences, 119334, Moscow, Russia

    S. V. Razin & O. V. Iarovaia

  2. LIA 1066 French-Russian Joint Cancer Research Laboratory 94805 Villejuif, France, 119334, Moscow, Russia

    S. V. Razin, O. V. Iarovaia & Y. S. Vassetzky

  3. Faculty of Biology, M.V. Lomonosov Moscow State University, 119992, Moscow, Russia

    S. V. Razin

  4. UMR8126, Université Paris-Sud, CNRS, Institut de cancérologie Gustave Roussy, 94805, Villejuif, France

    Y. S. Vassetzky

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  1. S. V. Razin
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  2. O. V. Iarovaia
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  3. Y. S. Vassetzky
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Correspondence to Y. S. Vassetzky.

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Razin, S.V., Iarovaia, O.V. & Vassetzky, Y.S. A requiem to the nuclear matrix: from a controversial concept to 3D organization of the nucleus. Chromosoma 123, 217–224 (2014). https://doi.org/10.1007/s00412-014-0459-8

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  • DOI: https://doi.org/10.1007/s00412-014-0459-8

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