Discrete nuclear domains of poly(A) RNA and their relationship to the functional organization of the nucleus

doi:10.1083/jcb.115.5.1191

This Article

Full Text (PDF, 3327K)

Alert me when this article is cited

Citation Map

Services

Email this article

Similar articles in this journal

Similar articles in PubMed

Alert me to new content in the JCB

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via CrossRef

Citing Articles via Google Scholar

Google Scholar

Articles by Carter, K. C.

Articles by Lawrence, J. B.

Search for Related Content

PubMed

PubMed Citation

Articles by Carter, K. C.

Articles by Lawrence, J. B.

Pubmed/NCBI databases

Compound via MeSH
Substance via MeSH

Social Bookmarking

What's this?

ARTICLES

Discrete nuclear domains of poly(A) RNA and their relationship to the functional organization of the nucleus

KC Carter, KL Taneja and JB Lawrence
Department of Cell Biology, University of Massachusetts Medical Center, Worcester 01655.

The functional organization of the nucleus was studied using a fluorescence microscopy approach which allowed integration of positional information for RNA, DNA, and proteins. In cells from sea urchin to human, nuclear poly(A) RNA was found concentrated primarily within several discrete "transcript domains" which often surrounded nucleoli. Concentrations of poly(A) RNA were coincident with snRNP antigen clusters, providing evidence for the localization of pre-mRNA splicing at these sites. The spatial relationship of transcript domains with respect to various classes of DNA was established, in that the poly(A) RNA-rich regions coincided with discrete regions of low DNA density and were non-randomly distributed with respect to specific DNA sequences. Centromeric DNA and late-replicating DNA did not overlap transcript domains, whereas a subset of early-replicating DNA may. Results indicate that transcript domains do not result directly from a simple clustering of chromatin corresponding to metaphase chromosomes bands. Finally, observations on the reassembly of these domains after mitosis suggest that the clustering of snRNP antigens may be dependent on the reappearance of pol II transcription. Implications of these findings for overall nuclear structure and function are considered, including a discussion of whether transcript domains may be sites of polymerase II transcription reflecting a clustering of active genes.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Hurt, J. A., Obar, R. A., Zhai, B., Farny, N. G., Gygi, S. P., Silver, P. A. (2009). A conserved CCCH-type zinc finger protein regulates mRNA nuclear adenylation and export. JCB 185: 265-277 [Abstract] [Full Text]
Pfeifer, I., Elsby, R., Fernandez, M., Faria, P. A., Nussenzveig, D. R., Lossos, I. S., Fontoura, B. M. A., Martin, W. D., Barber, G. N. (2008). NFAR-1 and -2 modulate translation and are required for efficient host defense. Proc. Natl. Acad. Sci. USA 105: 4173-4178 [Abstract] [Full Text]
Smith, K. P., Byron, M., Johnson, C., Xing, Y., Lawrence, J. B. (2007). Defining early steps in mRNA transport: mutant mRNA in myotonic dystrophy type I is blocked at entry into SC-35 domains. JCB 178: 951-964 [Abstract] [Full Text]
Sone, M., Hayashi, T., Tarui, H., Agata, K., Takeichi, M., Nakagawa, S. (2007). The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J. Cell Sci. 120: 2498-2506 [Abstract] [Full Text]
Royo, H., Basyuk, E., Marty, V., Marques, M., Bertrand, E., Cavaille, J. (2007). Bsr, a Nuclear-retained RNA with Monoallelic Expression. Mol. Biol. Cell 18: 2817-2827 [Abstract] [Full Text]
Prasanth, K. V., Spector, D. L. (2007). Eukaryotic regulatory RNAs: an answer to the 'genome complexity' conundrum. Genes Dev. 21: 11-42 [Abstract] [Full Text]
Schmidt, U., Richter, K., Berger, A. B., Lichter, P. (2006). In vivo BiFC analysis of Y14 and NXF1 mRNA export complexes: preferential localization within and around SC35 domains. JCB 172: 373-381 [Abstract] [Full Text]
Iborra, F. J., Jackson, D. A., Cook, P. R. (2004). The case for nuclear translation. J. Cell Sci. 117: 5713-5720 [Abstract] [Full Text]
Molenaar, C., Abdulle, A., Gena, A., Tanke, H. J., Dirks, R. W. (2004). Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells. JCB 165: 191-202 [Abstract] [Full Text]
Berciano, M. T., Villagra, N. T., Ojeda, J. L., Navascues, J., Gomes, A., Lafarga, M., Carmo-Fonseca, M. (2004). Oculopharyngeal muscular dystrophy-like nuclear inclusions are present in normal magnocellular neurosecretory neurons of the hypothalamus. Hum Mol Genet 13: 829-838 [Abstract] [Full Text]
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 Muscle-specific Genes Relative to the Periphery of SC-35 Domains during Skeletal Myogenesis. Mol. Biol. Cell 15: 197-206 [Abstract] [Full Text]
Shopland, L. S., Johnson, C. V., Byron, M., McNeil, J., Lawrence, J. B. (2003). Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods. JCB 162: 981-990 [Abstract] [Full Text]
Oh, S. W., Pope, R. K., Smith, K. P., Crowley, J. L., Nebl, T., Lawrence, J. B., Luna, E. J. (2003). Archvillin, a muscle-specific isoform of supervillin, is an early expressed component of the costameric membrane skeleton. J. Cell Sci. 116: 2261-2275 [Abstract] [Full Text]
Shiels, C., Islam, S. A., Vatcheva, R., Sasieni, P., Sternberg, M. J. E., Freemont, P. S., Sheer, D. (2002). PML bodies associate specifically with the MHC gene cluster in interphase nuclei. J. Cell Sci. 114: 3705-3716 [Abstract] [Full Text]
Shopland, L. S., Byron, M., Stein, J. L., Lian, J. B., Stein, G. S., Lawrence, J. B. (2001). Replication-dependent Histone Gene Expression Is Related to Cajal Body (CB) Association but Does Not Require Sustained CB Contact. Mol. Biol. Cell 12: 565-576 [Abstract] [Full Text]
Johnson, C., Primorac, D., McKinstry, M., McNeil, J., Rowe, D., Lawrence, J. B. (2000). Tracking Col1a1 RNA in Osteogenesis Imperfecta: Splice-Defective Transcripts Initiate Transport from the Gene but Are Retained within the Sc35 Domain. JCB 150: 417-432 [Abstract] [Full Text]
Leitch, A. R. (2000). Higher Levels of Organization in the Interphase Nucleus of Cycling and Differentiated Cells. Microbiol. Mol. Biol. Rev. 64: 138-152 [Abstract] [Full Text]
JACKSON, D. A., POMBO, A., IBORRA, F. (2000). The balance sheet for transcription: an analysis of nuclear RNA metabolism in mammalian cells. FASEB J. 14: 242-254 [Abstract] [Full Text]
Dostie, J., Lejbkowicz, F., Sonenberg, N. (2000). Nuclear Eukaryotic Initiation Factor 4e (Eif4e) Colocalizes with Splicing Factors in Speckles. JCB 148: 239-246 [Abstract] [Full Text]
Calado, A, Carmo-Fonseca, M (2000). Localization of poly(A)-binding protein 2 (PABP2) in nuclear speckles is independent of import into the nucleus and requires binding to poly(A) RNA. J. Cell Sci. 113: 2309-2318 [Abstract]
Ladomery, M. R., Slight, J., Mc Ghee, S., Hastie, N. D. (1999). Presence of WT1, the Wilm's Tumor Suppressor Gene Product, in Nuclear Poly(A)+ Ribonucleoprotein. J. Biol. Chem. 274: 36520-36526 [Abstract] [Full Text]
Wei, X., Somanathan, S., Samarabandu, J., Berezney, R. (1999). Three-Dimensional Visualization of Transcription Sites and Their Association with Splicing Factor-Rich Nuclear Speckles. JCB 146: 543-558 [Abstract] [Full Text]
Jolly, C., Vourc'h, C., Robert-Nicoud, M., Morimoto, R. I. (1999). Intron-independent Association of Splicing Factors with Active Genes. JCB 145: 1133-1143 [Abstract] [Full Text]
Smith, K. P., Moen, P. T. Jr., Wydner, K. L., Coleman, J. R., Lawrence, J. B. (1999). Processing of Endogenous Pre-mRNAs in Association with SC-35 Domains Is Gene Specific. JCB 144: 617-629 [Abstract] [Full Text]
Snaar, S. P., Vincent, M., Dirks, R. W. (1999). RNA Polymerase II Localizes at Sites of Human Cytomegalovirus Immediate-early RNA Synthesis and Processing. J. Histochem. Cytochem. 47: 245-254 [Abstract] [Full Text]
Gross, S., Loijens, J., Anderson, R. (1999). The casein kinase Ialpha isoform is both physically positioned and functionally competent to regulate multiple events of mRNA metabolism. J. Cell Sci. 112: 2647-2656 [Abstract]
Baer, M., Williams, S. C., Dillner, A., Schwartz, R. C., Johnson, P. F. (1998). Autocrine Signals Control CCAAT/Enhancer Binding Protein beta �Expression, Localization, and Activity in Macrophages. Blood 92: 4353-4365 [Abstract] [Full Text]
Hendzel, M. J., Kruhlak, M. J., Bazett-Jones, D. P. (1998). Organization of Highly Acetylated Chromatin around Sites of Heterogeneous Nuclear RNA Accumulation. Mol. Biol. Cell 9: 2491-2507 [Abstract] [Full Text]
Politz, J. C., Browne, E. S., Wolf, D. E., Pederson, T. (1998). Intranuclear diffusion and hybridization state of oligonucleotides measured by fluorescence correlation spectroscopy in living cells. Proc. Natl. Acad. Sci. USA 95: 6043-6048 [Abstract] [Full Text]
Lamond, A. I., Earnshaw, W. C. (1998). Structure and Function in the Nucleus. Science 280: 547-553 [Abstract] [Full Text]
Blencowe, B. J., Issner, R., Nickerson, J. A., Sharp, P. A. (1998). A coactivator of pre-mRNA�splicing. Genes Dev. 12: 996-1009 [Abstract] [Full Text]
Bridger, J., Herrmann, H, Munkel, C, Lichter, P (1998). Identification of an interchromosomal compartment by polymerization of nuclear-targeted vimentin. J. Cell Sci. 111: 1241-1253 [Abstract]
Grondin, B., Cote, F., Bazinet, M., Vincent, M., Aubry, M. (1997). Direct Interaction of the KRAB/Cys2-His2 Zinc Finger Protein ZNF74 with a Hyperphosphorylated Form of the RNA Polymerase II Largest Subunit. J. Biol. Chem. 272: 27877-27885 [Abstract] [Full Text]
Ishov, A. M., Stenberg, R. M., Maul, G. G. (1997). Human Cytomegalovirus Immediate Early Interaction with Host Nuclear Structures: Definition of an Immediate Transcript Environment. JCB 138: 5-16 [Abstract] [Full Text]
Gama-Carvalho, M., Krauss, R. D., Chiang, L., Valcarcel, J., Green, M. R., Carmo-Fonseca, M. (1997). Targeting of U2AF65 to Sites of Active Splicing in the Nucleus. JCB 137: 975-987 [Abstract] [Full Text]
Dirks, R., de Pauw, E., Raap, A. (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: 515-522 [Abstract]
Strouboulis, J, Wolffe, A. (1996). Functional compartmentalization of the nucleus. J. Cell Sci. 109: 1991-2000 [Abstract]
Trump, B. F. (1995). Mechanisms of Toxicity and Carcinogenesis. Toxicol Pathol 23: 775-827
Chadee, D. N., Taylor, W. R., Hurta, R. A. R., Allis, C. D., Wright, J. A., Davie, J. R. (1995). Increased Phosphorylation of Histone H1 in Mouse Fibroblasts Transformed with Oncogenes or Constitutively Active Mitogen-activated Protein Kinase Kinase. J. Biol. Chem. 270: 20098-20105 [Abstract] [Full Text]
Bisotto, S, Lauriault, P, Duval, M, Vincent, M (1995). Colocalization of a high molecular mass phosphoprotein of the nuclear matrix (p255) with spliceosomes. J. Cell Sci. 108: 1873-1882 [Abstract]
Beven, A., Simpson, G., Brown, J., Shaw, P. (1995). The organization of spliceosomal components in the nuclei of higher plants. J. Cell Sci. 108: 509-518 [Abstract]
Bregman, D., Du, L, Li, Y, Ribisi, S, Warren, S. (1994). Cytostellin distributes to nuclear regions enriched with splicing factors. J. Cell Sci. 107: 387-396 [Abstract]
Neel, H, Weil, D, Giansante, C, Dautry, F (1993). In vivo cooperation between introns during pre-mRNA processing.. Genes Dev. 7: 2194-2205 [Abstract]
Xing, Y, Johnson, C., Dobner, P., Lawrence, J. (1993). Higher level organization of individual gene transcription and RNA splicing. Science 259: 1326-1330 [Abstract]
Carter, K., Bowman, D, Carrington, W, Fogarty, K, McNeil, J., Fay, F., Lawrence, J. (1993). A three-dimensional view of precursor messenger RNA metabolism within the mammalian nucleus. Science 259: 1330-1335 [Abstract]
Jackson, D., Cook, P. (1993). Transcriptionally active minichromosomes are attached transiently in nuclei through transcription units. J. Cell Sci. 105: 1143-1150 [Abstract]
Sahlas, D., Milankov, K, Park, P., De Boni, U (1993). Distribution of snRNPs, splicing factor SC-35 and actin in interphase nuclei: immunocytochemical evidence for differential distribution during changes in functional states. J. Cell Sci. 105: 347-357 [Abstract]
Cremer, T., Kurz, A., Zirbel, R., Dietzel, S., Rinke, B., Schrock, E., Speicher, M.R., Mathieu, U., Jauch, A., Emmerich, P., Scherthan, H., Ried, T., Cremer, C., Lichter, P. (1993). Role of Chromosome Territories in the Functional Compartmentalization of the Cell Nucleus. Cold Spring Harb Symp Quant Biol 58: 777-792 [Abstract]
Spector, D.L., O'Keefe, R.T., Jimenez-Garcia, L.F. (1993). Dynamics of Transcription and Pre-mRNA Splicing within the Mammalian Cell Nucleus. Cold Spring Harb Symp Quant Biol 58: 799-805 [Abstract]
Lawrence, J.B., Carter, K.C., Xing, X. (1993). Probing Functional Organization within the Nucleus: Is Genome Structure Integrated with RNA Metabolism?. Cold Spring Harb Symp Quant Biol 58: 807-818 [Abstract]