Nuclear matrix – structure, function and pathogenesis
Piotr Wasąg 1 , Robert Lenartowski 2Abstract
The nuclear matrix (NM), or nuclear skeleton, is the non-chromatin, ribonucleoproteinaceous framework that is resistant to high ionic strength buffers, nonionic detergents, and nucleolytic enzymes. The NM fulfills a structural role in eukaryotic cells and is responsible for maintaining the shape of the nucleus and the spatial organization of chromatin. Moreover, the NM participates in several cellular processes, such as DNA replication/repair, gene expression, RNA transport, cell signaling and differentiation, cell cycle regulation, apoptosis and carcinogenesis. Short nucleotide sequences called scaffold/matrix attachment regions (S/MAR) anchor the chromatin loops to the NM proteins (NMP). The NMP composition is dynamic and depends on the cell type and differentiation stage or metabolic activity. Alterations in the NMP composition affect anchoring of the S/MARs and thus alter gene expression.This review aims to systematize information about the skeletal structure of the nucleus, with particular emphasis on the organization of the NM and its role in selected cellular processes. We also discuss several diseases that are caused by aberrant NM structure or dysfunction of individual NM elements.
References
- 1. Agrelo R., Souabni A., Novatchkova M., Haslinger C., Leeb M.,Komnenovic V., Kishimoto H., Gresh L., Kohwi-Shigematsu T., KennerL., Wutz A.: SATB1 defines the developmental context for genesilencing by Xist in lymphoma and embryonic cells. Dev. Cell, 2009;16: 507-516
Google Scholar - 2. Amati B., Gasser S.M.: Drosophila scaffold-attached regions bindnuclear scaffolds and can function as ARS elements in both buddingand fission yeasts. Mol. Cell. Biol., 1990; 10: 5442-5454
Google Scholar - 3. Barboro P., D’Arrigo C., Diaspro A., Mormino M., Alberti I., ParodiS., Patrone E., Balbi C.: Unraveling the organization of the internalnuclear matrix: RNA-dependent anchoring of NuMA to a lamin scaffold.Exp. Cell Res., 2002; 279: 202-218
Google Scholar - 4. Barboro P., D’Arrigo C., Repaci E., Bagnasco L., Orecchia P., CarnemollaB., Patrone E., Balbi C.: Proteomic analysis of the nuclearmatrix in the early stages of rat liver carcinogenesis: identificationof differentially expressed and MAR-binding proteins. Exp. Cell Res.,2009; 315: 226-239
Google Scholar - 5. Barboro P., Repaci E., D’Arrigo C., Balbi C.: The role of nuclearmatrix proteins binding to matrix attachment regions (MARs) inprostate cancer cell differentiation. PLoS One, 2012; 7: e40617
Google Scholar - 6. Barboro P., Rubagotti A., Orecchia P., Spina B., Truini M., RepaciE., Carmignani G., Romagnoli A., Introini C., Boccardo F., CarnemollaB., Balbi C.: Differential proteomic analysis of nuclear matrix inmuscle-invasive bladder cancer: potential to improve diagnosis andprognosis. Cell. Oncol., 2008; 30: 13-26
Google Scholar - 7. Barry G., Briggs J.A., Vanichkina D.P., Poth E.M., Beveridge N.J.,Ratnu V.S., Nayler S.P., Nones K., Hu J., Bredy T.W., Nakagawa S.,Rigo F., Taft R.J., Cairns M.J., Blackshaw S.: The long non-codingRNA Gomafu is acutely regulated in response to neuronal activationand involved in schizophrenia-associated alternative splicing. Mol.Psychiatry, 2014; 19: 486-494
Google Scholar - 8. Berezney R., Coffey D.S.: Identification of a nuclear protein matrix.Biochem. Biophys. Res. Commun., 1974; 60: 1410-1417
Google Scholar - 9. Berezney R., Coffey D.S.: Nuclear matrix. Isolation and characterizationof a framework structure from rat liver nuclei. J. Cell Biol.,1977; 73: 616-637
Google Scholar - 10. Bergmann J.H., Spector D.L.: Long non-coding RNAs: modulatorsof nuclear structure and function. Curr. Opin. Cell Biol., 2014;26: 10-18
Google Scholar - 11. Blencowe B.J., Issner R., Nickerson J.A., Sharp P.A.: A coactivatorof pre-mRNA splicing. Genes Dev., 1998; 12: 996-1009
Google Scholar - 12. Blencowe B.J., Nickerson J.A., Issner R., Penman S., Sharp P.A.:Association of nuclear matrix antigens with exon-containing splicingcomplexes. J. Cell Biol., 1994; 127: 593-607
Google Scholar - 13. Bode J., Goetze S., Heng H., Krawetz S.A., Benham C.: From DNAstructure to gene expression: mediators of nuclear compartmentalizationand dynamics. Chromosome Res., 2003; 11: 435-445
Google Scholar - 14. Bonne G., Quijano-Roy S.: Emery-Dreifuss muscular dystrophy,laminopathies, and other nuclear envelopathies. Handb. Clin. Neurol.2013; 113: 1367-1376
Google Scholar - 15. Boulikas T.: Chromatin domains and prediction of MAR sequences.Int. Rev. Cytol., 1995; 162A: 279-388
Google Scholar - 16. Burke B., Stewart C.L.: Functional architecture of the cell’s nucleusin development, aging, and disease. Curr. Top. Dev. Biol., 2014; 109: 1-52
Google Scholar - 17. Burute M., Gottimukkala K., Galande S.: Chromatin organizerSATB1 is an important determinant of T-cell differentiation. Immunol.Cell Biol., 2012; 90: 852-859
Google Scholar - 18. Calikowski T.T., Meulia T., Meier I.: A proteomic study of the arabidopsisnuclear matrix. J. Cell. Biochem. 2003; 90: 361-378
Google Scholar - 19. Carvalho C., Pereira H.M., Ferreira J., Pina C., Mendonça D., RosaA.C., Carmo-Fonseca M.: Chromosomal G-dark bands determine thespatial organization of centromeric heterochromatin in the nucleus.Mol. Biol. Cell, 2001; 12: 3563-3572
Google Scholar - 20. Cau P., Navarro C., Harhouri K., Roll P., Sigaudy S., Kaspi E., PerrinS., De Sandre-Giovannoli A., Lévy N.: Nuclear matrix, nuclear envelopeand premature aging syndromes in a translational researchperspective. Semin. Cell Dev. Biol. 2014; 29: 125-147
Google Scholar - 21. Ceci M., Offenhäuser N., Marchisio P.C., Biffo S.: Formation ofnuclear matrix filaments by p27BBP/eIF6. Biochem. Biophys. Res.Commun., 2002; 295: 295-299
Google Scholar - 22. Chattopadhyay S., Kaul R., Charest A., Housman D., Chen J.:SMAR1, a novel, alternatively spliced gene product, binds the Scaffold/Matrix-associatedregion at the T cell receptor beta locus. Genomics,2000; 68: 93-96
Google Scholar - 23. Chavali P.L., Funa K., Chavali S.: Cis-regulation of microRNAexpression by scaffold/matrix-attachment regions. Nucleic AcidsRes., 2011; 39: 6908-6918
Google Scholar - 24. Chemmannur S., Chattopadhyay S.: Role of nuclear matrix associatedregion (MAR) binding proteins in the regulation of T helpercell differentiation. Proc. Indian Natn. Sci. Acad., 2014; 80: 269-288
Google Scholar - 25. Chemmannur S.V., Badhwar A.J., Mirlekar B., Malonia S.K., GuptaM., Wadhwa N., Bopanna R., Mabalirajan U., Majumdar S., Ghosh B.,Chattopadhyay S.: Nuclear matrix binding protein SMAR1 regulatesT-cell differentiation and allergic airway disease. Mucosal Immunol.,2015; 8: 1201-1211
Google Scholar - 26. Ciejek E.M., Tsai M.J., O’Malley B.W.: Actively transcribed genesare associated with the nuclear matrix. Nature, 1983; 306: 607-609
Google Scholar - 27. Ciska M., Moreno Diaz de la Espina S.: The intriguing plantnuclear lamina. Front. Plant Sci., 2014; 5: 166
Google Scholar - 28. Cockerill P.N.: Nuclear matrix attachment occurs in several regionsof the IgH locus. Nucleic Acids Res., 1990; 18: 2643-2648
Google Scholar - 29. Cockerill P.N., Garrard W.T.: Chromosomal loop anchorage ofthe kappa immunoglobulin gene occurs next to the enhancer ina region containing topoisomerase II sites. Cell, 1986; 44: 273-282
Google Scholar - 30. Coffinier C., Chang S.Y., Nobumori C., Tu Y., Farber E.A., TothJ.I., Fong L.G., Young S.G.: Abnormal development of the cerebralcortex and cerebellum in the setting of lamin B2 deficiency. Proc.Natl. Acad. Sci. USA, 2010; 107: 5076-5081
Google Scholar - 31. Conner J.R., Hornick J.L.: SATB2 is a novel marker of osteoblasticdifferentiation in bone and soft tissue tumours. Histopathology,2013; 63: 36-49
Google Scholar - 32. Courbet S., Gay S., Arnoult N., Wronka G., Anglana M., Brison O.,Debatisse M.: Replication fork movement sets chromatin loop sizeand origin choice in mammalian cells. Nature, 2008; 455: 557-560
Google Scholar - 33. Cremer T., Cremer C.: Chromosome territories, nuclear architectureand gene regulation in mammalian cells. Nat. Rev. Genet.,2001; 2: 292-301
Google Scholar - 34. Cremer T., Dietzel S., Eils R., Lichter P., Cremer C.: Chromosometerritories, nuclear matrix filaments and inter-chromatin channels:a topological view on nuclear architecture and function. W: KewChromosome Conference IV, red.: P.E. Brandharn, M.D. Bennett.Royal Botanic Gardens, Kew 1995, 63-81
Google Scholar - 35. Das R., Yu J., Zhang Z., Gygi M.P., Krainer A.R., Gygi S.P., Reed R.:SR proteins function in coupling RNAP II transcription to pre-mRNAsplicing. Mol. Cell, 2007; 26: 867-881
Google Scholar - 36. Davidovich C., Zheng L., Goodrich K.J., Cech T.R.: PromiscuousRNA binding by Polycomb repressive complex 2. Nat. Struct. Mol.Biol., 2013; 20: 1250-1257
Google Scholar - 37. de Lange T.: Human telomeres are attached to the nuclear matrix.EMBO J., 1992; 11: 717-724
Google Scholar - 38. De Sandre-Giovannoli A., Bernard R., Cau P., Navarro C., AmielJ., Boccaccio I., Lyonnet S., Stewart C.L., Munnich A., Le Merrer M.,Lévy N.: Lamin a truncation in Hutchinson-Gilford progeria. Science,2003; 300: 2055
Google Scholar - 39. De Sandre-Giovannoli A., Chaouch M., Kozlov S., Vallat J.M., TazirM., Kassouri N., Szepetowski P., Hammadouche T., Vandenberghe A.,Stewart C.L., Grid D., Lévy N.: Homozygous defects in LMNA, encodinglamin A/C nuclear-envelope proteins, cause autosomal recessiveaxonal neuropathy in human (Charcot-Marie-Tooth disordertype 2) and mouse. Am. J. Hum. Genet.. 2002; 70: 726-736
Google Scholar - 40. Debald M., Franken S., Heukamp L.C., Linke A., Wolfgarten M.,Walgenbach K.J., Braun M., Rudlowski C., Gieselmann V., Kuhn W.,Hartmann G., Walgenbach-Brünagel G.: Identification of specificnuclear structural protein alterations in human breast cancer. J.Cell. Biochem., 2011; 112: 3176-3184
Google Scholar - 41. Edelman L.B., Fraser P.: Transcription factories: genetic programmingin three dimensions. Curr. Opin. Genet. Dev., 2012; 22:110-114
Google Scholar - 42. Eivazova E.R., Markov S.A., Pirozhkova I., Lipinski M., VassetzkyY.S.: Recruitment of RNA polymerase II in the Ifng gene promotercorrelates with the nuclear matrix association in activated T helpercells. J. Mol. Biol., 2007; 371: 317-322
Google Scholar - 43. Engelke R., Riede J., Hegermann J., Wuerch A., Eimer S., DengjelJ., Mittler G.: The quantitative nuclear matrix proteome as a biochemicalsnapshot of nuclear organization. J. Proteome Res., 2014;13: 3940-3956
Google Scholar - 44. Enukashvily N.I., Lobov I.B., Kukalev A., Podgornaya O.I.: A nuclearmatrix protein related to intermediate filaments proteins isa member of the complex binding alphoid DNA in vitro. Cell Biol.Int., 2000; 24: 483-492
Google Scholar - 45. Ferreira J., Paolella G., Ramos C., Lamond A.I.: Spatial organizationof large-scale chromatin domains in the nucleus: a magnifiedview of single chromosome territories. J. Cell Biol., 1997; 139:1597-1610
Google Scholar - 46. Fey E.G., Krochmalnic G., Penman S.: The nonchromatin substructuresof the nucleus: the ribonucleoprotein (RNP)-containingand RNP-depleted matrices analyzed by sequential fractionationand resinless section electron microscopy. J. Cell Biol., 1986; 102:1654-1665
Google Scholar - 47. Gabriel D., Roedl D., Gordon L.B., Djabali K.: Sulforaphane enhancesprogerin clearance in Hutchinson-Gilford progeria fibroblasts.Aging Cell, 2015; 14: 78-91
Google Scholar - 48. Galande S., Purbey P.K., Notani D., Kumar P.P.: The third dimensionof gene regulation: organization of dynamic chromatin loopscapeby SATB1. Curr. Opin. Genet. Dev., 2007; 17: 408-414
Google Scholar - 49. Gasser S.M., Laemmli U.K.: The organisation of chromatin loops:characterization of a scaffold attachment site. EMBO J., 1986;5: 511-518
Google Scholar - 50. Gerace L., Blum A., Blobel G.: Immunocytochemical localizationof the major polypeptides of the nuclear pore complex-laminafraction. Interphase and mitotic distribution. J. Cell Biol., 1978;79: 546-566
Google Scholar - 51. Gerner C., Holzmann K., Meissner M., Gotzmann J., Grimm R.,Sauermann G.: Reassembling proteins and chaperones in humannuclear matrix protein fractions. J. Cell. Biochem., 1999; 74: 145-151
Google Scholar - 52. Getzenberg R.H.: Nuclear matrix and the regulation of geneexpression: tissue specificity. J. Cell. Biochem., 1994; 55: 22-31
Google Scholar - 53. Girard-Reydet C., Grégoire D., Vassetzky Y., Méchali M.: DNAreplication initiates at domains overlapping with nuclear matrixattachment regions in the xenopus and mouse c-myc promoter.Gene, 2004; 332: 129-138
Google Scholar - 54. Guo B., Odgren P.R., van Wijnen A.J., Last T.J., Nickerson J., PenmanS., Lian J.B., Stein J.L., Stein G.S.: The nuclear matrix proteinNMP-1 is the transcription factor YY1. Proc. Natl. Acad. Sci. USA,1995; 92: 10526-10530
Google Scholar - 55. Hacisuleyman E., Goff L.A., Trapnell C., Williams A., Henao-MejiaJ., Sun L., McClanahan P., Hendrickson D.G., Sauvageau M., Kelley D.R.,Morse M., Engreitz J., Lander E.S., Guttman M., Lodish H.F. i wsp.: Topologicalorganization of multichromosomal regions by the long intergenicnoncoding RNA Firre. Nat. Struct. Mol. Biol., 2014; 21: 198-206
Google Scholar - 56. Hasegawa Y., Brockdorff N., Kawano S., Tsutui K., Tsutui K., NakagawaS.: The matrix protein hnRNP U is required for chromosomallocalization of Xist RNA. Dev. Cell, 2010; 19: 469-476
Google Scholar - 57. He D.C., Martin T., Penman S.: Localization of heterogeneousnuclear ribonucleoprotein in the interphase nuclear matrix corefilaments and on perichromosomal filaments at mitosis. Proc. Natl.Acad. Sci. USA, 1991; 88: 7469-7473
Google Scholar - 58. He D.C., Nickerson J.A., Penman S.: Core filaments of the nuclearmatrix. J. Cell Biol., 1990; 110: 569-580
Google Scholar - 59. Hirano Y., Ishii K., Kumeta M., Furukawa K., Takeyasu K., HorigomeT.: Proteomic and targeted analytical identification of BXDC1and EBNA1BP2 as dynamic scaffold proteins in the nucleolus. GenesCells, 2009; 14: 155-166
Google Scholar - 60. Hozák P.: The nucleoskeleton and attached activities. Exp. CellRes., 1996; 229: 267-271
Google Scholar - 61. Hozák P., Cook P.R., Schöfer C., Mosgöller W., Wachtler F.: Siteof transcription of ribosomal RNA and intranucleolar structure inHeLa cells. J. Cell Sci., 1994; 107: 639-648
Google Scholar - 62. Hozák P., Hassan A.B., Jackson D.A., Cook P.R.: Visualization of replicationfactories attached to nucleoskeleton. Cell, 1993; 73: 361-373
Google Scholar - 63. Hozák P., Jackson D.A., Cook P.R.: Replication factories and nuclearbodies: the ultrastructural characterization of replication sitesduring the cell cycle. J. Cell Sci., 1994; 107: 2191-2202
Google Scholar - 64. Ioudinkova E., Razin S.V., Borunova V., de Conto F., Rynditch A.,Scherrer K.: RNA-dependent nuclear matrix contains a 33 kb globinfull domain transcript as well as prosomes but no 26S proteasomes.J. Cell. Biochem., 2005; 94: 529-539
Google Scholar - 65. Jackson D.A., Cook P.R.: Replication occurs at a nucleoskeleton.EMBO J., 1986; 5: 1403-1410
Google Scholar - 66. Jackson D.A., Cook P.R.: Transcription occurs at a nucleoskeleton.EMBO J., 1985; 4: 919-925
Google Scholar - 67. Jackson DA, Cook P.R.: Visualization of a filamentous nucleoskeletonwith a 23 nm axial repeat. EMBO J., 1988; 7: 3667-3677
Google Scholar - 68. Jackson D.A., Hassan A.B., Errington R.J., Cook P.R.: Visualizationof focal sites of transcription within human nuclei. EMBO J.,1993; 12: 1059-1065
Google Scholar - 69. Jeon Y., Lee J.T.: YY1 tethers Xist RNA to the inactive X nucleationcenter. Cell, 2011; 146: 119-133
Google Scholar - 70. Jimenez-Escrig A., Gobernado I., Garcia-Villanueva M., Sanchez–Herranz A.: Autosomal recessive Emery-Dreifuss muscular dystrophycaused by a novel mutation (R225Q) in the lamin A/C geneidentified by exome sequencing. Muscle Nerve, 2012; 45: 605-610
Google Scholar - 71. Johnson J.O., Pioro E.P., Boehringer A., Chia R., Feit H., RentonA.E., Pliner H.A., Abramzon Y., Marangi G., Winborn B.J., Gibbs J.R.,Nalls M.A., Morgan S., Shoai M., Hardy J.: Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat. Neurosci.,2014; 17: 664-666
Google Scholar - 72. Kisseljova N.P., Dmitriev P., Katargin A., Kim E., Ezerina D., MarkozashviliD., Malysheva D., Planche E., Lemmers R.J., van der MaarelS.M., Laoudj-Chenivesse D., Lipinski M., Vassetzky Y.S.: DNA polymorphismand epigenetic marks modulate the affinity of a scaffold/matrix attachment region to the nuclear matrix. Eur. J. Hum. Genet.,2014; 22: 1117-1123
Google Scholar - 73. Kramer J.A., Krawetz S.A.: Matrix-associated regions in haploidexpressed domains. Mamm. Genome, 1995; 6: 677-679
Google Scholar - 74. Kulkarni A., Pavithra L., Rampalli S., Mogare D., Babu K., ShiekhG., Ghosh S., Chattopadhyay S.: HIV-1 integration sites are flanked bypotential MARs that alone can act as promoters. Biochem. Biophys.Res. Commun., 2004; 322: 672-677
Google Scholar - 75. Lanktree M., Cao H., Rabkin S.W., Hanna A., Hegele R.A.: NovelLMNA mutations seen in patients with familial partial lipodystrophysubtype 2 (FPLD2; MIM 151660). Clin. Genet., 2007; 71: 183-186
Google Scholar - 76. Lee D.C., Welton K.L., Smith E.D., Kennedy B.K.: A-type nuclearlamins act as transcriptional repressors when targeted to promoters.Exp. Cell Res., 2009; 315: 996-1007
Google Scholar - 77. Legartová S., Stixová L., Laur O., Kozubek S., Sehnalová P., BártováE.: Nuclear structures surrounding internal lamin invaginations.J. Cell. Biochem., 2014; 115: 476-487
Google Scholar - 78. Leman E.S., Madigan M.C., Brünagel G., Takaha N., Coffey D.S.,Getzenberg R.H.: Nuclear matrix localization of high mobility groupprotein I(Y) in a transgenic mouse model for prostate cancer. J. Cell.Biochem., 2003; 88: 599-608
Google Scholar - 79. Lenartowski R., Goc A.: Rola macierzy jądrowej w przestrzennejorganizacji procesów jądrowych. Post. Biochem., 2002; 48: 252-261
Google Scholar - 80. Lieberman-Aiden E., van Berkum N.L., Williams L., ImakaevM., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., DorschnerM.O., Sandstrom R., Bernstein B., Bender M.A., Groudine M., GnirkeA. i wsp.: Comprehensive mapping of long-range interactions revealsfolding principles of the human genome. Science, 2009; 326:289-293
Google Scholar - 81. Linnemann A.K., Platts A.E., Krawetz S.A.: Differential nuclearscaffold/matrix attachment marks expressed genes. Hum. Mol.Genet., 2009; 18: 645-654
Google Scholar - 82. Liu G.H., Suzuki K., Qu J., Sancho-Martinez I., Yi F., Li M., KumarS., Nivet E., Kim J., Soligalla R.D., Dubova I., Goebl A., PlongthongkumN., Fung H.L., Zhang K. i wsp.: Targeted gene correction oflaminopathy-associated LMNA mutations in patient-specific iPSCs.Cell Stem Cell., 2011; 8: 688-694
Google Scholar - 83. Lüftner D., Possinger K.: Nuclear matrix proteins as biomarkersfor breast cancer. Expert. Rev. Mol. Diagn., 2002; 2: 23-31
Google Scholar - 84. Ma H., Siegel A.J., Berezney R.: Association of chromosome territorieswith the nuclear matrix. Disruption of human chromosometerritories correlates with the release of a subset of nuclear matrixproteins. J. Cell Biol., 1999; 146: 531-542
Google Scholar - 85. Magnusson K., de Wit M., Brennan D.J., Johnson L.B., McGee S.F.,Lundberg E., Naicker K., Klinger R., Kampf C., Asplund A., WesterK., Gry M., Bjartell A., Gallagher W.M., Rexhepaj E. i wsp.: SATB2 incombination with cytokeratin 20 identifies over 95% of all colorectalcarcinomas. Am. J. Surg. Pathol., 2011; 35: 937-948
Google Scholar - 86. Malhas A., Goulbourne C., Vaux D.J.: The nucleoplasmic reticulum:form and function. Trends Cell Biol., 2011; 21: 362-373
Google Scholar - 87. Mamillapalli A., Pathak R.U., Garapati H.S., Mishra R.K.: Transposableelement ‘roo’ attaches to nuclear matrix of the Drosophilamelanogaster. J. Insect Sci., 2013; 13: 111
Google Scholar - 88. Melnik S., Deng B., Papantonis A., Baboo S., Carr I.M., Cook P.R.:The proteomes of transcription factories containing RNA polymerasesI, II or III. Nat. Methods, 2011; 8: 963-968
Google Scholar - 89. Mercer T.R., Mattick J.S.: Understanding the regulatory andtranscriptional complexity of the genome through structure. GenomeRes., 2013; 23: 1081-1088
Google Scholar - 90. Mirkovitch J., Mirault M.E., Laemmli U.K.: Organization of thehigher-order chromatin loop: specific DNA attachment sites on nuclearscaffold. Cell, 1984; 39: 223-232
Google Scholar - 91. Mirlekar B., Ghorai S., Khetmalas M., Bopanna R., ChattopadhyayS.: Nuclear matrix protein SMAR1 control regulatory T-cell fate during inflammatory bowel disease (IBD). Mucosal Immunol.,2015; 8: 1184-1200
Google Scholar - 92. Moreno Díaz de la Espina S.M.: Nuclear matrix isolated fromplant cells. Int. Rev. Cytol. 1995; 162B: 75-139
Google Scholar - 93. Mortillaro M.J., Blencowe B.J., Wei X., Nakayasu H., Du L., WarrenS.L., Sharp P.A., Berezney R.: A hyperphosphorylated form ofthe large subunit of RNA polymerase II is associated with splicingcomplexes and the nuclear matrix. Proc. Natl. Acad. Sci. USA, 1996;93: 8253-8257
Google Scholar - 94. Muchir A., Bonne G., van der Kooi A.J., van Meegen M., Baas F.,Bolhuis P.A., de Visser M., Schwartz K.: Identification of mutationsin the gene encoding lamins A/C in autosomal dominant limb girdlemuscular dystrophy with atrioventricular conduction disturbances(LGMD1B). Hum. Mol. Genet., 2000; 9: 1453-1459
Google Scholar - 95. Nakagawa S., Prasanth K.V.: eXIST with matrix-associated proteins.Trends Cell Biol., 2011; 21: 321-327
Google Scholar - 96. Nakayasu H., Berezney R.: Mapping replicational sites in theeucaryotic cell nucleus. J. Cell Biol., 1989; 108: 1-11
Google Scholar - 97. Navarro C.L., De Sandre-Giovannoli A., Bernard R., BoccaccioI., Boyer A., Geneviève D., Hadj-Rabia S., Gaudy-Marqueste C., SmittH.S., Vabres P., Faivre L., Verloes A., Van Essen T., Flori E., HennekamR. i wsp.: Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganizationand identify restrictive dermopathy as a lethal neonatallaminopathy. Hum. Mol. Genet., 2004; 13: 2493-2503
Google Scholar - 98. Nickerson J.A., Krochmalnic G., Wan K.M., Penman S.: Chromatinarchitecture and nuclear RNA. Proc. Natl. Acad. Sci. USA, 1989;86: 177-181
Google Scholar - 99. Niu Y., Li J.S., Luo X.R.: Enhancement of expression of survivinpromoter-driven CD/TK double suicide genes by the nuclearmatrix attachment region in transgenic gastric cancer cells. Gene,2014; 534: 177-182
Google Scholar - 100. Novelli G., Muchir A., Sangiuolo F., Helbling-Leclerc A., D’ApiceM.R., Massart C., Capon F., Sbraccia P., Federici M., Lauro R., TudiscoC., Pallotta R., Scarano G., Dallapiccola B., Merlini L. i wsp.: Mandibuloacraldysplasia is caused by a mutation in LMNA-encoding laminA/C. Am. J. Hum. Genet. 2002; 71: 426-431
Google Scholar - 101. Ocampo J., Mondragón R., Roa-Espitia A.L., Chiquete-Félix N.,Salgado Z.O., Mújica A.: Actin, myosin, cytokeratins and spectrinare components of the guinea pig sperm nuclear matrix. TissueCell, 2005; 37: 293-308
Google Scholar - 102. Ostermeier G.C., Liu Z., Martins R.P., Bharadwaj R.R., Ellis J.,Draghici S., Krawetz S.A.: Nuclear matrix association of the humanbeta-globin locus utilizing a novel approach to quantitative real-timePCR. Nucleic Acids Res., 2003; 31: 3257-3266
Google Scholar - 103. Parada L.A., McQueen P.G., Misteli T.: Tissue-specific spatialorganization of genomes. Genome Biol., 2004; 5: R44
Google Scholar - 104. Parnaik V.K., Chaturvedi P., Muralikrishna B.: Lamins, laminopathiesand disease mechanisms: possible role for proteasomaldegradation of key regulatory proteins. J. Biosci., 2011; 36: 471-479
Google Scholar - 105. Pathak R.U., Mamillapalli A., Rangaraj N., Kumar R.P., VasanthiD., Mishra K., Mishra R.K.: AAGAG repeat RNA is an essential componentof nuclear matrix in Drosophila. RNA Biol., 2013; 10: 564-571
Google Scholar - 106. Petrov A., Allinne J., Pirozhkova I., Laoudj D., Lipinski M., VassetzkyY.S.: A nuclear matrix attachment site in the 4q35 locus hasan enhancer-blocking activity in vivo: implications for the facio-scapulo-humeraldystrophy. Genome Res., 2008; 18: 39-45
Google Scholar - 107. Petrov A., Pirozhkova I., Carnac G., Laoudj D., Lipinski M., VassetzkyY.S.: Chromatin loop domain organization within the 4q35locus in facioscapulohumeral dystrophy patients versus normalhuman myoblasts. Proc. Natl. Acad. Sci. USA, 2006; 103: 6982-6987
Google Scholar - 108. Raffaele Di Barletta M., Ricci E., Galluzzi G., Tonali P., Mora M.,Morandi L., Romorini A., Voit T., Orstavik K.H., Merlini L., Trevisan C., Biancalana V., Hausmanowa-Petrusewicz I., Bione S., Ricotti R. i wsp.:Different mutations in the LMNA gene cause autosomal dominantand autosomal recessive Emery-Dreifuss muscular dystrophy. Am.J. Hum. Genet., 2000; 66: 1407-1412
Google Scholar - 109. Rappsilber J., Ryder U., Lamond A.I., Mann M.: Large-scaleproteomic analysis of the human spliceosome. Genome Res., 2002;12: 1231-1245
Google Scholar - 110. Razin S.V., Gromova I.I.: The channels model of nuclear matrixstructure. Bioessays, 1995; 17: 443-450
Google Scholar - 111. Reyes J.C., Muchardt C., Yaniv M.: Components of the humanSWI/SNF complex are enriched in active chromatin and are associatedwith the nuclear matrix. J. Cell Biol., 1997; 137: 263-274
Google Scholar - 112. Rinn J.L., Kertesz M., Wang J.K., Squazzo S.L., Xu X., BrugmannS.A., Goodnough L.H., Helms J.A., Farnham P.J., Segal E., Chang H.Y.:Functional demarcation of active and silent chromatin domainsin human HOX loci by noncoding RNAs. Cell, 2007; 129: 1311-1323
Google Scholar - 113. Rivera-Mulia J.C., Hernández-Muñoz R., Martínez F., ArandaAnzaldoA.: DNA moves sequentially towards the nuclear matrixduring DNA replication in vivo. BMC Cell Biol., 2011; 12: 3
Google Scholar - 114. Scharner J., Brown C.A., Bower M., Iannaccone S.T., Khatri I.A.,Escolar D., Gordon E., Felice K., Crowe C.A., Grosmann C., MeriggioliM.N., Asamoah A., Gordon O., Gnocchi V.F., Ellis J.A. i wsp.: NovelLMNA mutations in patients with Emery-Dreifuss muscular dystrophyand functional characterization of four LMNA mutations. Hum.Mutat., 2011; 32: 152-167
Google Scholar - 115. Scharner J., Figeac N., Ellis J.A., Zammit P.S.: Amelioratingpathogenesis by removing an exon containing a missense mutation:a potential exon-skipping therapy for laminopathies. GeneTher., 2015; 22: 503-515
Google Scholar - 116. Senderek J., Garvey S.M., Krieger M., Guergueltcheva V., UrtizbereaA., Roos A., Elbracht M., Stendel C., Tournev I., MihailovaV., Feit H., Tramonte J., Hedera P., Crooks K., Bergmann C. i wsp.:Autosomal-dominant distal myopathy associated with a recurrentmissense mutation in the gene encoding the nuclear matrix protein,matrin 3. Am. J. Hum. Genet., 2009; 84: 511-518
Google Scholar - 117. Shiue C.N., Nematollahi-Mahani A., Wright A.P.: Myc-inducedanchorage of the rDNA IGS region to nucleolar matrix modulatesgrowth-stimulated changes in higher-order rDNA architecture. NucleicAcids Res., 2014; 42: 5505-5517
Google Scholar - 118. Simon D.N., Wilson K.L.: The nucleoskeleton as a genomeassociateddynamic ‘network of networks’. Nat. Rev. Mol. Cell Biol.,2011; 12: 695-708
Google Scholar - 119. Sjakste N.I., Sjakste T.G.: Enzyme activities of nuclear matrix.Biochemistry, 1994; 59: 1239-1246
Google Scholar - 120. Sone M., Hayashi T., Tarui H., Agata K., Takeichi M., NakagawaS.: The mRNA-like noncoding RNA Gomafu constitutes a novel nucleardomain in a subset of neurons. J. Cell Sci., 2007; 120: 2498-2506
Google Scholar - 121. Sreenath K., Pavithra L., Singh S., Sinha S., Dash P.K., SiddappaN.B., Ranga U., Mitra D., Chattopadhyay S.: Nuclear matrix proteinSMAR1 represses HIV-1 LTR mediated transcription through chromatinremodeling. Virology, 2010; 400: 76-85
Google Scholar - 122. Trentani A., Testillano P.S., Risueño M.C., Biggiogera M.: Visualizationof transcription sites at the electron microscope. Eur. J.Histochem., 2003; 47: 195-200
Google Scholar - 123. Tripathi V., Song D.Y., Zong X., Shevtsov S.P., Hearn S., FuX.D., Dundr M., Prasanth K.V.: SRSF1 regulates the assembly of premRNAprocessing factors in nuclear speckles. Mol. Biol. Cell, 2012;23: 3694-3706
Google Scholar - 124. Tsutsui K.M., Sano K., Tsutsui K.: Dynamic view of the nuclearmatrix. Acta Med. Okayama, 2005; 59: 113-120
Google Scholar - 125. van Wijnen A.J., Bidwell J.P., Fey E.G., Penman S., Lian J.B., SteinJ.L., Stein G.S.: Nuclear matrix association of multiple sequencespecificDNA binding activities related to SP-1, ATF, CCAAT, C/EBP,OCT-1, and AP-1. Biochemistry, 1993; 32: 8397-8402
Google Scholar - 126. Wagner S., Chiosea S., Nickerson J.A.: The spatial targetingand nuclear matrix binding domains of SRm160. Proc. Natl. AcadSci. USA, 2003; 100: 3269-3274
Google Scholar - 127. Wei X., Somanathan S., Samarabandu J., Berezney R.: Three-dimensionalvisualization of transcription sites and their associationwith splicing factor-rich nuclear speckles. J. Cell Biol., 1999; 146: 543-558
Google Scholar - 128. Wilson R.H., Coverley D.: Relationship between DNA replicationand the nuclear matrix. Genes Cells, 2013; 18: 17-31
Google Scholar - 129. Worman H.J., Bonne G.: “Laminopathies”: a wide spectrum ofhuman diseases. Exp. Cell Res., 2007; 313: 2121-2133
Google Scholar - 130. Xiao R., Tang P., Yang B, Huang J., Zhou Y., Shao C., Li H., SunH., Zhang Y., Fu X.D.: Nuclear matrix factor hnRNP U/SAF-A exertsa global control of alternative splicing by regulating U2 snRNP maturation.Mol. Cell, 2012; 45: 656-668
Google Scholar - 131. Xing Y.G., Lawrence J.B.: Preservation of specific RNA distributionwithin the chromatin-depleted nuclear substructure demonstratedby in situ hybridization coupled with biochemical fractionation.J. Cell Biol., 1991; 112: 1055-1063
Google Scholar - 132. Xylinas E., Kluth L.A., Rieken M., Karakiewicz P.I., Lotan Y.,Shariat S.F.: Urine markers for detection and surveillance of bladdercancer. Urol. Oncol., 2014; 32: 222-229
Google Scholar - 133. Yanagisawa J., Ando J., Nakayama J., Kohwi Y., Kohwi-ShigematsuT.: A matrix attachment region (MAR)-binding activity dueto a p114 kilodalton protein is found only in human breast carcinomasand not in normal and benign breast disease tissues. CancerRes., 1996; 56: 457-462
Google Scholar - 134. Yokota T., Kanakura Y.: Role of tissue-specific AT-rich DNAsequence-binding proteins in lymphocyte differentiation. Int. J.Hematol., 2014; 100: 238-245
Google Scholar - 135. Zaremba-Czogalla M., Dubińska-Magiera M., Rzepecki R.: Nowefunkcje lamin – starzy znajomi w nowym świetle. Postępy Biol. Kom.,2010; 37: 507-524
Google Scholar - 136. Zeitlin S., Parent A., Silverstein S., Efstratiadis A.: Pre-mRNAsplicing and the nuclear matrix. Mol. Cell. Biol., 1987; 7: 111-120
Google Scholar