Intron-independent association of splicing factors with active genes

Journal of Cell Biology

Volumn 145, Issue 6, 1999, Pages 1133-1143

  Jolly, Caroline ^a,b   Vourc'h, Claire ^b   Robert Nicoud, Michel ^b   Morimoto, Richard I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b INSERM   (France)

Author keywords

Heat shock genes; Nuclear organization; Splicing; Transcription

Indexed keywords

AZETIDINE; CADMIUM; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; TRANSCRIPTION FACTOR;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; FIBROBLAST; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEAT SHOCK; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTRON; PRIORITY JOURNAL;

AZETIDINES; CADMIUM; CELLS, CULTURED; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRONS; NUCLEAR PROTEINS; RIBONUCLEOPROTEINS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA POLYMERASE II; RNA SPLICING; RNA, MESSENGER; SPLICEOSOMES; TEMPERATURE; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 0033553878     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.6.1133     Document Type: Article

References (85)

1. Abravaya, K., B. Phillips, and R.I. Morimoto. 1991. Attenuation of the heat shock response in HeLa cells is mediated by the release of bound heat shock transcription factor and is modulated by changes in growth and in heat shock temperatures. Genes Dev. 5: 2117-2127.
2. Al-Shawi, R., J. Kinnaird, J. Burke, and J.O. Bishop. 1990. Expression of a foreign gene in a line of transgenic mice is modulated by a chromosomal position effect. Mol. Cell. Biol. 10: 1192-1198.
3. Banerji, S.S., K. Laing, and R.I. Morimoto. 1984. Erythroid lineage-specific expression and inducibility of the major heat shock protein Hsp70 during avian embryogenesis. Genes Dev. 1: 946-953.
4. Baurén, G., W.-Q. Jiang, K. Bernholm, F. Gu, and L. Wieslander. 1996. Demonstration of a dynamic, transcription-dependent organization of pre-mRNA splicing factors in polytene nuclei. J. Cell Biol. 133: 929-941.
5. Blencowe, B.J., M.J. Mortillaro, X. Wei, H. Nakayasu, L. Du, S.L. Warren, P.A. Sharp, and R. Berezney. 1996. A hyperphosphorylated form of the largest subunit of RNA polymerase II is associated with splicing complexes. Proc. Natl. Acad. Sci USA. 93: 8253-8257.
6. Bregman, D.B., L. Du, S. van der Zee, and S.L. Warren. 1995. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129: 287-298.
7. Bridge, E., D.-X. Xia, M. Carmo-Fonseca, B. Cardinali, A.I. Lamond, and U. Petlersson. 1995. Dynamic organization of splicing factors in adenovirus-infected cells. J. Virol. 69: 281-290.
8. Carmo-Fonseca, M., R. Pepperkok, M.T. Carvalho, and A.I. Lamond. 1992. Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 sn-RNPs in coiled bodies. J. Cell Biol. 117: 1-14.
9. Carter, K.C., K.L. Taneja, and J.B. Lawrence. 1991. Discrete nuclear domains of poly(A) RNA and their relationship to the functional organization of the nucleus. J. Cell Biol. 115: 1191-1202.
10. Carter, K.C., D. Bowman, W. Carrington, K. Fogarty, J.A. McNeil, F.S. Fay, and J.B. Lawrence. 1993. A three-dimensional view of precursor messenger RNA metabolism within the mammalian nucleus. Science. 259: 1330-1335.
11. Cho, E.-J., T. Tagaki, C.R. Moore, and S. Buratowski. 1997. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 11: 3319-3326.
12. Clemson, C.M., and J.B. Lawrence. 1996. Multifunctional compartments in the cell nucleus: insights from DNA and RNA localization. J. Cell. Biochem. 62: 181-190.
13. Dirks, R.W., E.S.D. de Pauw, and A.K. Raap. 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.
14. Du, L., and S.L. Warren. 1997. A functional interaction between the carboxy-terminal domain of RNA polymerase II and pre-mRNA splicing. J. Cell Biol. 136: 5-18.
15. Durkin, A.S., D.R. Maglott, N.C. Vamvakopoulos, H.Y. Zoghbi, and W.C. Nierman. 1993. Assignment of an intron-containing human heat-shock protein gene (hsp90β, HSPCB) to chromosome 6 near TCTE1 (6p21) and two intronless pseudogenes to chromosomes 4 and 15 by polymerase chain reaction amplification from a panel of hybrid cell lines. Genomics. 18: 452-454.
16. Fakan, S. 1994. Perichromatin fibrils are in situ forms of nascent transcripts. Trends Cell Biol. 4: 86-90.
17. Fay, F.S., K.L. Taneja, S. Shenoy, L. Lifshitz, and R.H. Singer. 1997. Quantitative digital analysis of diffuse and concentrated nuclear distributions of nascent transcripts. SC35 and poly(A). Exp. Cell Res. 231: 27-37.
18. Fort, P., L. Marty, M. Piechaczyk, S. El Sabrouty, C. Dani, P. Jeanteur, and J.M. Blanchard. 1985. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate dehydrogenase multigenic family. Nucleic Acids Res. 13: 1431-1442.
19. Fu, X.-D., and T. Maniatis. 1990. Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature. 343: 437-441.
20. Gough, N.M. 1988. Rapid and quantitative preparation of cytoplasmic RNA from small number of cells. Anal. Biochem. 15: 93-95.
21. Harrison, G.S., H.A. Drabkin, F.T. Kao, J. Hartz, I.M. Hart, E.H.Y. Chu, B.J. Wu, and R.I. Morimoto. 1987. Chromosomal location of human genes encoding major heat-shock protein HSP70. Somat. Cell. Mol. Genet. 13: 119-130.
22. Hickey, E., S.E. Brandon, S. Sadis, G. Smale, and L.A. Weber. 1986. Molecular cloning of sequences encoding the human heat shock proteins and their expression during hyperthermia. Gene. 43: 147-154.
23. Huang, S., and D.L. Spector. 1991. Nascent pre-mRNA transcripts are associated with nuclear regions enriched in spicing factors. Genes Dev. 5: 2288-2302.
24. Huang, S., and D.L. Spector. 1996a. Dynamic organization of pre-mRNA splicing factors. J. Cell. Biochem. 62: 191-197.
25. Huang, S., and D.L. Spector. 1996b. Intron-dependent recruitment of pre-mRNA splicing factors to sites of transcription. J. Cell Biol. 133: 719-732.
26. Jiménez-Garcia, L.F., and D.L. Spector. 1993. In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell. 73: 47-59.
27. Jolly, C., and R.I. Morimoto. 1999. Stress and the cell nucleus: dynamics of gene expression and structural reorganization. Gene Expr. In press.
28. Jolly, C., F. Mongelard, M. Robert-Nicoud, and C. Vourc'h. 1997a. Optimization of nuclear transcripts detection by FISH and combination with fluorescence immunocytochemical detection of transcription factors. J. Histochem. Cytochem. 45: 1585-1592.
29. Jolly, C., R.I. Morimoto, M. Robert-Nicoud, and C. Vourc'h. 1997b. Nuclear foci enriched in HSF1 transcription factor: relationship with heat shock gene transcription sites. J. Cell Sci. 110: 2935-2941.
30. Jolly, C., S. Michelland, M. Rocchi, M. Robert-Nicoud, and C. Vourc'h. 1997c. Analysis of the transcriptional activity of amplified genes in tumor cells by fluorescence in situ hybridization. Hum. Genet. 101: 81-87.
31. Jolly, C., M. Robert-Nicoud, and C. Vourc'h. 1998. Contribution of the growing RNA molecules to the nuclear transcripts foci observed by FISH. Exp. Cell Res. 238: 299-304.
32. Kim, E., L. Du, D.B. Bregman, and S.L. Warren. 1997. Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J. Cell Biol. 136: 19-28.
33. Kontermann, R.E., Z. Liu, R.A. Schulze, K.A. Sommer, I. Queitsch, S. Dubel, S.M. Kipriyanov, F. Breitling, and E.K. Bautz. 1995. Characterization of the epitope recognized by a monoclonal antibody directed against the largest subunit of Drosophila RNA polymerase II. Biol. Chem. Hoppe-Seyler. 376: 473-481.
34. Krämer, A., R. Haars, R. Kabisch, H. Will, F.A. Bautz, and E.K. Bautz. 1980. Monoclonal antibody directed against RNA polymerase II of Drosophila melanogaster. Mol. Gen. Genet. 180: 193-199.
35. Krause, S., S. Fakan, K. Weis, and E. Wahle. 1994. Immunodetection of poly(A) binding protein II in the cell nucleus. Exp. Cell Res. 214: 75-82.
36. Lamond, A.I., and W.C. Earnshaw. 1998. Structure and function in the nucleus. Science. 280: 547-553.
37. Lampel, S., J.M. Bridger, R.M. Zirbel, U.R. Mathieu, and P. Lichter. 1997. Nuclear RNA accumulations contain released transcripts and exhibit specific distributions with respect to Sm antigen foci. DNA Cell Biol. 16: 1133-1142.
38. Lawrence, J.B., K.C. Carter, and X. Xing. 1993. Probing functional organization within the nucleus: is genome structure integrated with RNA metabolism? Cold Spring Harbor Symp. Quant. Biol. 58: 807-818.
39. Lerner, E.A., M.R. Lerner, C.A.J. Janeway, and J.A. Steitz. 1981. Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc. Natl. Acad. Sci. USA. 78: 2737-2741.
40. Lichter, P., T. Cremer, J. Borden, L. Manuelidis, and D.C. Ward. 1988. Delineation of individual chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum. Genet. 80: 224-234.
41. Martin, T.E., S.C. Barghusen, G.P. Leser, and P.G. Spear. 1987. Redistribution of nuclear ribonucleoprotein antigens during herpes simplex virus infection. J. Cell Biol. 105: 2069-2082.
42. Matera, A.G. 1998. Of coiled bodies, gems, and salmon. J. Cell. Biochem. 70: 181-192.
43. Mattaj, I.W., W.J. Habets, and W.J. van Venrooij. 1986. Monospecific antibodies reveal details of U2 snRNP structure and interaction between U1 and U2 snRNPs. EMBO (Eur. Mol. Biol. Org.) J. 5: 997-1002.
44. McCracken, S., N. Fong, E. Rosonina, K. Yankulov, G. Brothers, D. Siderovski, A. Hessel, S. Foster, S. Shuman, and D.L. Bentley. 1997a. 5'-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 11: 3306-3318.
45. McCracken, S., N. Fong, K. Yankulov, S. Ballantyne, G. Pan, J. Greenblatt, S.D. Patterson, M. Wickens, and D.L. Bentley. 1997b. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature. 385: 357-361.
46. Misteli, T., and D.L. Spector. 1998. The cellular organization of gene expression. Curr. Opin. Cell Biol. 10: 322-331.
47. Misteli, T., J.F. Cáceres, and D.L. Spector. 1997. The dynamics of a pre-mRNA splicing factor in living cells. Nature. 387: 523-527.
48. Misteli, T., J.F. Cáceres, J.Q. Clement, A.R. Krainer, M.F. Wilkinson, and D.L. Spector. 1998. Serine phosphorylation of SR proteins is required for their recruitment to sites of transcription in vivo. J. Cell Biol. 143: 297-307.
49. Moen, P.T., Jr., K.P. Smith, and J.B. Lawrence. 1995. Compartmentalization of specific pre-mRNA metabolism: an emerging view. Hum. Mol. Genet. 4: 1779-1789.
50. Monier, K., Y. Usson, F. Mongelard, P. Szepetowski, M. Robert-Nicoud, and C. Vourc'h. 1996. Metaphase and interphase mapping by FISH: improvement of chromosome banding and signal resolution in interphase nuclei by means of iterative deconvolution. Cytogenel. Cell Genet. 72: 200-204.
51. Morimoto, R.I. 1993. Cells in stress: transcriptional regulation of heat shock genes. Science. 259: 1409-1410.
52. Morimoto, R.I., P.E. Kroeger, and J.J. Cotto. 1996. The transcriptional regulation of heat shock genes: a plethora of heat shock factors and regulatory conditions. In Stress-inducible Cellular Responses. U. Feige, R.I. Morimoto, I. Yahara, and B.S. Polla, editors. Birkhaüser Verlag, Basel, Switzerland. 139-163.
53. Mortillaro, M.J., B.J. Blencowe, X. Wei, H. Nakayasu, L. Du, S.L. Warren, P.A. Sharp, and R. Berezney. 1996. A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc. Natl. Acad. Sci. USA. 93: 8253-8257.
54. Mosser, D., N.G. Theodorakis, and R.I. Morimoto. 1988. Coordinate changes in heat shock element binding activity and hsp70 gene transcription rates in human cells. Mol. Cell. Biol. 8: 4736-4744.
55. O'Keefe, R.T., A. Mayeda, C.L. Sadowski, A.R. Krainer, and D.L. Spector. 1994. Disruption of pre-mRNA splicing in vivo results in reorganization of splicing factors. J. Cell Biol. 124: 249-260.
56. Patturajan, M., R.J. Schulte, B.M. Sefton, R. Berezney, M. Vincent, O. Bensaude, S.L. Warren, and J.L. Corden. 1998. Growth-related changes in phosphorylation of yeast RNA polymerase II. J. Biol. Chem. 273: 4689-4694.
57. Pombo, A., and P.R. Cook. 1996. The localization of sites containing nascent RNA and splicing factors. Exp. Cell Res. 229: 201-203.
58. Pombo, A., J. Ferreira, E. Bridge, and M. Carmo-Fonseca. 1994. Adenovirus replication and transcription sites are spatially separated in the nucleus of infected cells. EMBO (Eur. Mol. Biol. Org.) J. 13: 5075-5085.
59. Puvion, E., and F. Puvion-Dutilleul. 1996. Ultrastructure of the nucleus in relation to transcription and splicing: roles of perichromatin fibrils and interchromatin granules. Exp. Cell Res. 229: 217-225.
60. Puvion-Dutilleul, F., J.-P. Bachellerie, N. Visa, and E. Puvion. 1994. Rearrangements of intranuclear structures involved in RNA processing in response to adenovirus infection. J. Cell Sci. 107: 1457-1468.
61. Raap, A.K., F.M. van de Rijke, R.W. Dirks, C.J. Sol, R. Boom, and M. van der Ploeg. 1991. Bicolor fluorescence in situ hybridization to intron and exon mRN A sequences. Exp. Cell Res. 197: 319-322.
62. Schul, W., L. de Jong, and R. van Driel. 1998a. Nuclear neighbours: the spatial and functional organization of genes and nuclear domains. J. Cell. Biochem. 70: 159-171.
63. Schul, W., R. van Driel, and L. de Jong. 1998b. A subset of poly( A) polymerase is concentrated at sites of RNA synthesis and is associated with domains enriched in splicing factors and poly(A) RNA. Exp. Cell Res. 238: 1-12.
64. Shi, Y., D.D. Mosser, and R.I. Morimoto. 1998. Molecular chaperones as HSFI-specific transcriptional repressors. Genes Dev. 12: 654-666.
65. Shukla, R.R., Z. Dominski, T. Zwierzynski, and R. Kole. 1990. Inactivation of splicing factors in HeLa cells subjected to heat shock. J. Biol. Chem. 265: 20377-20383.
66. Smith, K.P., P.T. Moen, Jr., K.L. Wydner, J.R. Coleman, and J.B. Lawrence. 1999. Processing of endogenous pre-mRNAs in association with SC-35 domains is gene-specific. J. Cell Biol. 144: 617-629.
67. Spector, D.L., X.-D. Fu, and T. Maniatis. 1991. Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO (Eur. Mol. Biol. Org.) J. 10: 3467-3481.
68. Spector, D.L., R.T. O'Keefe, and L.F. Jiménez-Garcia. 1993. Dynamics of transcription and pre-mRNA splicing within the mammalian cell nucleus. Cold Spring Harbor Symp. Quant. Biol. 58: 799-805.
69. Thibodeau, A., and M. Vincent. 1991. Monoclonal antibody CC-3 recognizes phosphoproteins in interphase and mitolic cells. Exp. Cell Res. 195: 145-153.
70. Vincent, M., P. Lauriault, M.-F. Dubois, S. Lavoie, O. Bensaude, and B. Chabot. 1996. The nuclear matrix protein p255 is a highly phosphorylated form of RNA polymerase II largest subunit which associates with spliceosomes. Nucleic Acids Res. 24: 4649-4652.
71. Visa, N., F. Puvion-Dutilleul, F. Harper, J.P. Bachellerie, and E. Puvion. 1993. Intranuclear distribution of poly(A) RNA determined by electron microscope in situ hybridization. Exp. Cell Res. 208: 19-34.
72. Wang, J., L.-G. Cao, Y.-L. Wang, and T. Pederson. 1991. Localization of pre-messenger RNA at discrete nuclear sites. Proc. Natl. Acad. Sci. USA. 88: 7391-7395.
73. Wang, S.M., J.D. Khandekar, K.L. Kaul, D.J. Winchester, and R.I. Morimoto. 1999. A method for the quantitative analysis of human heat shock gene expression using a multiplex RT-PCR assay. Cell Stress Chaperones. In press.
74. Wansink, D.O., W. Schul, I. van der Kraan, B. van Steensel, R. van Driel, and L. de Jong. 1993. Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J. Cell Biol. 122: 283-293.
75. Watowich, S.S., and R.I. Morimoto. 1988. Complex regulation of heat shock- and glucose-responsive genes in human cells. Mol. Cell. Biol. 8: 393-405.
76. Wei, X., J. Samarabandu, R.S. Devdhar, A.J. Siegel, R. Acharya, and R. Berezney. 1998. Segregation of transcription and replication sites into higher order domains. Science. 281: 1502-1505.
77. Williams, G.T., and R.I. Morimoto. 1990. Maximal stress-induced transcription of the human HSP70 promoter involves interactions with the basal promoter independent of rotational alignment. Mol. Cell. Biol. 10: 3125-3146.
78. Wu, B., C. Hunt, and R.I. Morimoto. 1985. Structure and expression of the human gene encoding major heat shock protein hsp70. Mol. Cell. Biol. 5: 330-341.
79. Wu, Z.A., C. Murphy, H.G. Callan, and J.G. Gall. 1991. Small nuclear ribonucleoproteins and heterogeneous nuclear ribonucleoproteins in the amphibian germinal vesicle: loops, spheres, and snurposomes. J. Cell Biol. 113: 465-483.
80. Wuarin, J., and U. Schibler. 1994. Physical isolation of nascent RNA chains transcribed by RNA polymerase II: evidence for cotranscriptional splicing. Mol. Cell. Biol. 14: 7219-7225.
81. Xing, Y., C.V. Johnson, P.R. Dobner, and J.B. Lawrence. 1993. Higher level organization of individual gene transcription and RNA splicing. Science. 259: 1326-1329.
82. Xing, Y., C.V. Johnson, P.T. Moen, Jr., J.A. McNeil, and J.B. Lawrence. 1995. Nonrandom gene organization: structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains. J. Cell Biol. 131: 1635-1647.
83. Yuryev, A., M. Patturajan, Y. Litingtung, R.V. Joshi, C. Gentile, M. Gebara, and J.L. Corden. 1996. The C-terminal domain of the largest subunit of RNA polymerase II interacts with a novel set of serine/arginine-rich proteins. Proc. Natl. Acad. Sci. USA. 93: 6975-6980.
84. Zeng, C.Q., E. Kim, S.L. Warren, and S.M. Berget. 1997. Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO (Eur. Mol. Biol. Org.) J. 16: 1401-1412.
85. Zhang, G., K.L. Taneja, R.H. Singer, and M.R. Green. 1994. Localization of pre-mRNA splicing in mammalian nuclei. Nature. 372: 809-812.