A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules

Journal of Cell Science

Volumn 117, Issue 19, 2004, Pages 4551-4558

  Metz, Alexandra ^a   Soret, Johann ^b   Vourc'h, Claire ^a   Tazi, Jamal ^b   Jolly, Caroline ^a  

^a INSTITUT ALBERT BONNIOT   (France)

^b INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

Heat shock; HSFI; Nuclear stress granules; Satellite III transcripts; SR proteins

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; RNA POLYMERASE II; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; CELL DAMAGE; CHROMOSOME 9Q; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE IDENTIFICATION; GENE LOCUS; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SPLICEOSOME;

CELL NUCLEUS STRUCTURES; DNA, SATELLITE; DNA-BINDING PROTEINS; HELA CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA POLYMERASE II; RNA SPLICING; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 5444253157     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01329     Document Type: Article

References (48)

1. Allemand, E., Gattoni, R., Bourbon, H. M., Stevenin, J., Caceres, J. F., Soret, J. and Tazi, J. (2001). Distinctive features of Drosophila alternative splicing factor RS domain: implication for specific phosphorylation, shuttling, and splicing activation. Mol. Cell. Biol. 21, 1345-1359.
2. Allemand, E., Dokudovskaya, S., Bordonne, R. and Tazi, J. (2002). A conserved Drosophila transportin-serine/arginine-rich (SR) protein permits nuclear import of Drosophila SR protein splicing factors and their antagonist repressor splicing factor 1. Mol. Biol. Cell 13, 2436-2447.
3. Amrein, H., Hedley, M. L. and Maniatis, T. (1994). The role of specific protein-RNA and protein-protein interactions in positive and negative control of pre-mRNA splicing by Transformer 2. Cell 76, 735-746.
4. Birney, E., Kumar, S. and Krainer, A. R. (1993). Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21, 5803-5816.
5. Caceres, J. F., Misteli, T., Screaton, G. R., Spector, D. L. and Krainer, A. R. (1997). Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell Biol. 138, 225-238.
6. Chandler, S. D., Mayeda, A., Yeakley, J. M., Krainer, A. R. and Fu, X. D. (1997). RNA splicing specificity determined by the coordinated action of RNA recognition motifs in SR proteins. Proc. Natl. Acad. Sci. USA 94, 3596-3601.
7. Chiodi, I., Biggiogera, M., Denegri, M., Corioni, M., Weighardt, F., Cobianchi, F., Riva, S. and Biamonti, G. (2000). Structure and dynamics of hnRNP-labelled nuclear bodies induced by stress treatments. J. Cell Sci. 113, 4043-4053.
8. Cotto, J., Fox, S. and Morimoto, R. (1997). HSF1 granules: a novel stress-induced nuclear compartment of human cells. J. Cell Sci. 110, 2925-2934.
9. Creancier, L., Prats, H., Zanibellato, C., Amalric, F. and Bugler, B. (1993). Determination of the functional domains involved in nucleolar targeting of nucleolin. Mol. Biol. Cell 4, 1239-1250.
10. Dauksaite, V. and Akusjarvi, G. (2004). The second RNA binding domain of human splicing factor ASF/SF2 is the critical domain controlling adenovirus E1A alternative 5′ splice site selection. Biochem. J. 381, 343-350.
11. Denegri, M., Chiodi, I., Corioni, M., Cobianchi, F., Riva, S. and Biamonti, G. (2001). Stress-induced Nuclear Bodies Are Sites of Accumulation of Pre-mRNA Processing Factors. Mol. Biol. Cell 12 3502-3514.
12. Denegri, M., Moralli, D., Rocchi, M., Biggiogera, M., Raimondi, E., Cobianchi, F., de Carli, L., Riva, S. and Biamonti, G. (2002). Human chromosomes 9, 12, and 15 contain the nucleation sites of stress-induced nuclear bodies. Mol. Biol. Cell 13, 2069-2079.
13. Du, L. and Warren, S. L. (1997). A functional interaction between the carboxy-terminal domain of RNA polymerase II and pre-mRNA splicing. J. Cell Biol. 136, 5-18.
14. Dye, B. T. and Patton, J. G. (2001). An RNA recognition motif (RRM) is required for the localization of PTB- associated splicing factor (PSF) to subnuclear speckles. Exp. Cell Res. 263, 131-144.
15. Hickey, E., Brandon, S. E., Smale, G., Lloyd, D. and Weber, L. A. (1989). Sequence and regulation of a gene encoding a human 89-kilodalton heat shock protein. Mol. Cell. Biol. 9, 2615-2626.
16. Himmelspach, M., Cavaloc, Y., Chebli, K., Stevenin, J. and Gattoni, R. (1995). Titration of serine/arginine (SR) splicing factors during adenoviral infection modulates E1A pre-mRNA alternative splicing. RNA 1, 794-806.
17. Jolly, C., Morimoto, R., Robert-Nicoud, M. and Vourc'h, C. (1997). HSF1 transcription factor concentrates in nuclear foci during heat shock: relationship with transcription sites. J. Cell Sci. 110, 2935-2941.
18. Jolly, C., Usson, Y. and Morimoto, R. I. (1999). Rapid and reversible relocalization of heat shock factor 1 within seconds to nuclear stress granules. Proc. Natl. Acad. Sci. USA 96, 6769-6774.
19. Jolly, C., Konecny, L., Grady, D. L., Kutskova, Y. A., Cotto, J. J., Morimoto, R. I. and Vourc'h, C. (2002). In vivo binding of active heat shock transcription factor 1 to human chromosome 9 heterochromatin during stress. J. Cell Biol. 156, 775-781.
20. Jolly, C., Metz, A., Govin, J., Vigneron, M., Turner, B. M., Khochbin, S. and Vourc'h, C. (2004). Stress-induced transcription of satellite III repeats. J. Cell Biol. 164, 25-33.
21. Kim, E., Du, L., Bregman, D. B. and Warren, S. L. (1997). Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J. Cell Biol. 136, 19-28.
22. Kohtz, J. D., Jamison, S. F., Will, C. L., Zuo, P., Luhrmann, R., Garcia-Blanco, M. A. and Manley, J. L. (1994). Protein-protein interactions and 5′-splice-site recognition in mammalian mRNA precursors. Nature 368, 119-124.
23. Lindquist, S. (1986). The heat-shock response. Annu. Rev. Biochem. 55,1151-1191.
24. Mathew, S., Behm, F., Dalton, J. and Raimondi, S. (1999). Comparison of cytogenetics, Southern blotting, and fluorescence in situ hybridization as methods for detecting MLL gene rearrangements in children with acute leukemia and with 11q23 abnormalities. Leukemia 13, 1713-1720.
25. Mayeda, A. and Krainer, A. R. (1992). Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68, 365-375.
26. Mayeda, A., Munroe, S. H., Xu, R. M. and Krainer, A. R. (1998). Distinct functions of the closely related tandem RNA-recognition motifs of hnRNP A1. RNA 4, 1111-1123.
27. Mayeda, A., Screaton, G. R., Chandler, S. D., Fu, X. D. and Krainer, A. R. (1999). Substrate specificities of SR proteins in constitutive splicing are determined by their RNA recognition motifs and composite pre-mRNA exonic elements. Mol. Cell. Biol. 19, 1853-1863.
28. McCracken, S., Fong, N., Yankulov, K., Ballantyne, S., Pan, G., Greenblatt, J., Patterson, S. D., Wickens, M. and Bentley, D. L. (1997). The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385, 357-361.
29. Morimoto, R. I. (1998). Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788-3796.
30. Mortillaro, M. J., Blencowe, B. J., Wei, X., Nakayasu, H., Du, L., Warren, S. L., Sharp, P. A. and Berezney, R. (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.
31. Nyman, U., Hallman, H., Hadlaczky, G., Petterson, I., Sharp, G. and Ringertz, N. R. (1986). Intranuclear localization of snRNP antigens. J. Cell Biol. 102, 137-144.
32. Pelham, H. R. (1984). Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J. 3, 3095-3100.
33. Pirkkala, L., Nykanen, P. and Sistonen, L. (2001). Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15, 1118-1131.
34. Prasanth, K. V., Rajendra, T. K., Lal, A. K. and Lakhotia, S. C. (2000). Omega speckles - a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. J. Cell Sci. 113, 3485-3497.
35. Rizzi, N., Denegri, M., Chiodi, I., Corioni, M., Valgardsdottir, R., Cobianchi, F., Riva, S. and Biamonti, G. (2004). Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock. Mol. Biol. Cell 15 543-551.
36. Sanford, J. R., Longman, D. and Caceres, J. F. (2003). Multiple roles of the SR protein family in splicing regulation. Prog. Mol. Subcell. Biol. 31, 33-58.
37. Sarge, K. D., Murphy, S. P. and Morimoto, R. I. (1993). Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol. Cell. Biol. 13, 1392-1407.
38. Shi, H. and Xu, R. M. (2003). Crystal structure of the Drosophila Mago nashi-Y14 complex. Genes Dev. 17, 971-976.
39. Shi, Y., Mosser, D. D. and Morimoto, R. I. (1998). Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev. 12, 654-666.
40. Timchenko, N. A., Welm, A. L., Lu, X. and Timchenko, L. T. (1999). CUG repeat binding protein (CUGBP1) interacts with the 5′ region of C/EBPbeta mRNA and regulates translation of C/EBPbeta isoforms. Nucleic Acids Res. 27, 4517-4525.
41. van Der Houven van Oordt, W., Newton, K., Screaton, G. R. and Caceres, J. F. (2000). Role of SR protein modular domains in alternative splicing specificity in vivo. Nucleic Acids Res. 28 4822-4831.
42. Wang, S. M., Khandekar, J. D., Kaul, K. L., Winchester, D. J. and Morimoto, R. I. (1999). A method for the quantitative analysis of human heat shock gene expression using a multiplex RT-PCR assay. Cell Stress Chaperones 4, 153-161.
43. Weighardt, F., Cobianchi, F., Cartegni, L., Chiodi, I., Villa, A., Riva, S. and Biamonti, G. (1999). A novel hnRNP protein (HAP/SAF-B) enters a subset of hnRNP complexes and relocates in nuclear granules in response to heat shock. J. Cell Sci. 112, 1465-1476.
44. Welch, W. J. and Feramisco, J. R. (1984). Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells. J. Biol. Chem. 259, 4501-4513.
45. Wu, B. J. and Morimoto, R. I. (1985). Transcription of the human hsp70 gene is induced by serum stimulation. Proc. Natl. Acad. Sci. USA 82, 6070-6074.
46. Wu, J. Y. and Maniatis, T. (1993). Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75, 1061-1070.
47. Yuryev, A., Patturajan, M., Litingtung, Y., Joshi, R. V., Gentile, C., Gebara, M. and Corden, J. L. (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.
48. Zhu, J. and Krainer, A. R. (2000). Pre-mRNA splicing in the absence of an SR protein RS domain. Genes Dev. 14, 3166-3178.