hnRNP A1 Relocalization to the Stress Granules Reflects a Role in the Stress Response

REFERENCES

• Allemand, E., S. Guil, M. Myers, J. Moscat, J. F. Caceres, and A. R. Krainer. 2005. Regulation of heterogenous nuclear ribonucleoprotein A1 transport by phosphorylation in cells stressed by osmotic shock. Proc. Natl. Acad. Sci. USA 102:3605–3610.
   PubMedGoogle Scholar
• Biamonti, G. 2004. Nuclear stress bodies: a heterochromatin affair? Nat. Rev. Mol. Cell Biol. 5:493–498.
   PubMedGoogle Scholar
• Biamonti, G., M. Buvoli, M. T. Bassi, C. Morandi, F. Cobianchi, and S. Riva. 1989. Isolation of an active gene encoding human hnRNP protein A1. Evidence for alternative splicing. J. Mol. Biol. 207:491–503.
   PubMed Web of Science ®Google Scholar
• Bond, U. 1988. Heat shock but not other stress inducers leads to the disruption of a sub-set of snRNPs and inhibition of in vitro splicing in HeLa cells. EMBO J. 7:3509–3518.
   PubMed Web of Science ®Google Scholar
• Bonnal, S., F. Pileur, C. Orsini, F. Parker, F. Pujol, A. C. Prats, and S. Vagner. 2005. Heterogeneous nuclear ribonucleoprotein A1 is a novel internal ribosome entry site trans-acting factor that modulates alternative initiation of translation of the fibroblast growth factor 2 mRNA. J. Biol. Chem. 280:4144–4153.
   PubMed Web of Science ®Google Scholar
• Buxade, M., J. L. Parra, S. Rousseau, N. Shpiro, R. Marquez, N. Morrice, J. Bain, E. Espel, and C. G. Proud. 2005. The Mnks are novel components in the control of TNFalpha biosynthesis and phosphorylate and regulate hnRNP A1. Immunity 23:177–189.
   PubMed Web of Science ®Google Scholar
• Caceres, J. F., T. Misteli, G. R. Screaton, D. L. Spector, and A. R. Krainer. 1997. Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell Biol. 138:225–238.
   PubMed Web of Science ®Google Scholar
• Caceres, J. F., S. Stamm, D. M. Helfman, and A. R. Krainer. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265:1706–1709.
   PubMed Web of Science ®Google Scholar
• Cazalla, D., K. Newton, and J. F. Caceres. 2005. A novel SR-related protein is required for the second step of pre-mRNA splicing. Mol. Cell. Biol. 25:2969–2980.
   PubMedGoogle Scholar
• Cougot, N., S. Babajko, and B. Seraphin. 2004. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165:31–40.
   PubMed Web of Science ®Google Scholar
• Daoud, R., G. Mies, A. Smialowska, L. Olah, K. A. Hossmann, and S. Stamm. 2002. Ischemia induces a translocation of the splicing factor tra2-beta 1 and changes alternative splicing patterns in the brain. J. Neurosci. 22:5889–5899.
   PubMedGoogle Scholar
• Davis, R. J. 1994. MAPKs: new JNK expands the group. Trends Biochem. Sci. 19:470–473.
   PubMed Web of Science ®Google Scholar
• Denegri, M., I. Chiodi, M. Corioni, F. Cobianchi, S. Riva, and G. Biamonti. 2001. Stress-induced nuclear bodies are sites of accumulation of pre-mRNA processing factors. Mol. Biol. Cell 12:3502–3514.
   PubMed Web of Science ®Google Scholar
• Denegri, M., D. Moralli, M. Rocchi, M. Biggiogera, E. Raimondi, F. Cobianchi, L. De Carli, S. Riva, and G. Biamonti. 2002. Human chromosomes 9, 12, and 15 contain the nucleation sites of stress-induced nuclear bodies. Mol. Biol. Cell 13:2069–2079.
   PubMed Web of Science ®Google Scholar
• Dreyfuss, G., V. N. Kim, and N. Kataoka. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3:195–205.
   PubMed Web of Science ®Google Scholar
• Duncan, R. F., H. Peterson, and A. Sevanian. 2005. Signal transduction pathways leading to increased eIF4E phosphorylation caused by oxidative stress. Free Radic. Biol. Med. 38:631–643.
   PubMedGoogle Scholar
• Eystathioy, T., A. Jakymiw, E. K. Chan, B. Seraphin, N. Cougot, and M. J. Fritzler. 2003. The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA 9:1171–1173.
   PubMedGoogle Scholar
• Fillman, C., and J. Lykke-Andersen. 2005. RNA decapping inside and outside of processing bodies. Curr. Opin. Cell Biol. 17:326–331.
   PubMedGoogle Scholar
• Forch, P., O. Puig, N. Kedersha, C. Martinez, S. Granneman, B. Seraphin, P. Anderson, and J. Valcarcel. 2000. The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol. Cell 6:1089–1098.
   PubMed Web of Science ®Google Scholar
• Gallouzi, I. E., C. M. Brennan, M. G. Stenberg, M. S. Swanson, A. Eversole, N. Maizels, and J. A. Steitz. 2000. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA 97:3073–3078.
   PubMedGoogle Scholar
• Gatto-Konczak, F., C. F. Bourgeois, C. Le Guiner, L. Kister, M. C. Gesnel, J. Stevenin, and R. Breathnach. 2000. The RNA-binding protein TIA-1 is a novel mammalian splicing regulator acting through intron sequences adjacent to a 5′ splice site. Mol. Cell. Biol. 20:6287–6299.
   PubMedGoogle Scholar
• Gilbert, W., C. W. Siebel, and C. Guthrie. 2001. Phosphorylation by Sky1p promotes Npl3p shuttling and mRNA dissociation. RNA 7:302–313.
   PubMedGoogle Scholar
• Hamilton, B. J., C. M. Burns, R. C. Nichols, and W. F. Rigby. 1997. Modulation of AUUUA response element binding by heterogeneous nuclear ribonucleoprotein A1 in human T lymphocytes. The roles of cytoplasmic location, transcription, and phosphorylation. J. Biol. Chem. 272:28732–28741.
   PubMedGoogle Scholar
• He, Y., M. A. Brown, J. A. Rothnagel, N. A. Saunders, and R. Smith. 2005. Roles of heterogeneous nuclear ribonucleoproteins A and B in cell proliferation. J. Cell Sci. 118:3173–3183.
   PubMed Web of Science ®Google Scholar
• Iervolino, A., G. Santilli, R. Trotta, C. Guerzoni, V. Cesi, A. Bergamaschi, C. Gambacorti-Passerini, B. Calabretta, and D. Perrotti. 2002. hnRNP A1 nucleocytoplasmic shuttling activity is required for normal myelopoiesis and BCR/ABL leukemogenesis. Mol. Cell. Biol. 22:2255–2266.
   PubMed Web of Science ®Google Scholar
• Ingelfinger, D., D. J. Arndt-Jovin, R. Luhrmann, and T. Achsel. 2002. The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8:1489–1501.
   PubMed Web of Science ®Google Scholar
• Izaurralde, E., A. Jarmolowski, C. Beisel, I. W. Mattaj, G. Dreyfuss, and U. Fischer. 1997. A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export. J. Cell Biol. 137:27–35.
   PubMedGoogle Scholar
• Izquierdo, J. M., N. Majos, S. Bonnal, C. Martinez, R. Castelo, R. Guigo, D. Bilbao, and J. Valcarcel. 2005. Regulation of Fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition. Mol. Cell 19:475–484.
   PubMed Web of Science ®Google Scholar
• Jolly, C., A. Metz, J. Govin, M. Vigneron, B. M. Turner, S. Khochbin, and C. Vourc'h. 2004. Stress-induced transcription of satellite III repeats. J. Cell Biol. 164:25–33.
   PubMed Web of Science ®Google Scholar
• Kamath, R. V., D. J. Leary, and S. Huang. 2001. Nucleocytoplasmic shuttling of polypyrimidine tract-binding protein is uncoupled from RNA export. Mol. Biol. Cell 12:3808–3820.
   PubMedGoogle Scholar
• Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963–969.
   PubMed Web of Science ®Google Scholar
• Kedersha, N., S. Chen, N. Gilks, W. Li, I. J. Miller, J. Stahl, and P. Anderson. 2002. Evidence that ternary complex (eIF2-GTP-tRNA(i) (Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 13:195–210.
   PubMed Web of Science ®Google Scholar
• Kedersha, N., M. R. Cho, W. Li, P. W. Yacono, S. Chen, N. Gilks, D. E. Golan, and P. Anderson. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151:1257–1268.
   PubMed Web of Science ®Google Scholar
• Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M. J. Fitzler, D. Scheuner, R. J. Kaufman, D. E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871–884.
   PubMed Web of Science ®Google Scholar
• Kyriakis, J. M., and J. Avruch. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:807–869.
   PubMed Web of Science ®Google Scholar
• Lai, M. C., H. W. Kuo, W. C. Chang, and W. Y. Tarn. 2003. A novel splicing regulator shares a nuclear import pathway with SR proteins. EMBO J. 22:1359–1369.
   PubMed Web of Science ®Google Scholar
• López de Silanes, I., S. Galban, J. L. Martindale, X. Yang, K. Mazan-Mamczarz, F. E. Indig, G. Falco, M. Zhan, and M. Gorospe. 2005. Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol. Cell. Biol. 25:9520–9531.
   PubMed Web of Science ®Google Scholar
• Lu, L., A. P. Han, and J. J. Chen. 2001. Translation initiation control by heme-regulated eukaryotic initiation factor 2α kinase in erythroid cells under cytoplasmic stresses. Mol. Cell. Biol. 21:7971–7980.
   PubMed Web of Science ®Google Scholar
• Martinez-Contreras, R., J. F. Fisette, F. U. Nasim, R. Madden, M. Cordeau, and B. Chabot. 2006. Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing. PLoS Biol. 4:e21.
   PubMed Web of Science ®Google Scholar
• Mayeda, A., and A. R. Krainer. 1992. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68:365–375.
   PubMed Web of Science ®Google Scholar
• Mayeda, A., S. H. Munroe, J. F. Caceres, and A. R. Krainer. 1994. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 13:5483–5495.
   PubMed Web of Science ®Google Scholar
• Metz, A., J. Soret, C. Vourc'h, J. Tazi, and C. Jolly. 2004. A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J. Cell Sci. 117:4551–4558.
   PubMed Web of Science ®Google Scholar
• Michael, W. M., M. Choi, and G. Dreyfuss. 1995. A nuclear export signal in hnRNP A1: a signal-mediated, temperature-dependent nuclear protein export pathway. Cell 83:415–422.
   PubMed Web of Science ®Google Scholar
• New, L., Y. Jiang, M. Zhao, K. Liu, W. Zhu, L. J. Flood, Y. Kato, G. C. Parry, and J. Han. 1998. PRAK, a novel protein kinase regulated by the p38 MAP kinase. EMBO J. 17:3372–3384.
   PubMed Web of Science ®Google Scholar
• Patry, C., L. Bouchard, P. Labrecque, D. Gendron, B. Lemieux, J. Toutant, E. Lapointe, R. Wellinger, and B. Chabot. 2003. Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticle A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines. Cancer Res. 63:7679–7688.
   PubMed Web of Science ®Google Scholar
• Pinol-Roma, S., Y. D. Choi, M. J. Matunis, and G. Dreyfuss. 1988. Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins. Genes Dev. 2:215–227.
   PubMed Web of Science ®Google Scholar
• Pinol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730–732.
   PubMed Web of Science ®Google Scholar
• Pyronnet, S., H. Imataka, A. C. Gingras, R. Fukunaga, T. Hunter, and N. Sonenberg. 1999. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J. 18:270–279.
   PubMed Web of Science ®Google Scholar
• Sanford, J. R., J. D. Ellis, D. Cazalla, and J. F. Caceres. 2005. Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc. Natl. Acad. Sci. USA 102:15042–15047.
   PubMed Web of Science ®Google Scholar
• Scheper, G. C., N. A. Morrice, M. Kleijn, and C. G. Proud. 2001. The mitogen-activated protein kinase signal-integrating kinase Mnk2 is a eukaryotic initiation factor 4E kinase with high levels of basal activity in mammalian cells. Mol. Cell. Biol. 21:743–754.
   PubMed Web of Science ®Google Scholar
• Shin, C., Y. Feng, and J. L. Manley. 2004. Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature 427:553–558.
   PubMed Web of Science ®Google Scholar
• Shin, C., and J. L. Manley. 2004. Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell Biol. 5:727–738.
   PubMed Web of Science ®Google Scholar
• Shomron, N., M. Alberstein, M. Reznik, and G. Ast. 2005. Stress alters the subcellular distribution of hSlu7 and thus modulates alternative splicing. J. Cell Sci. 118:1151–1159.
   PubMed Web of Science ®Google Scholar
• Siomi, H., and G. Dreyfuss. 1995. A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129:551–560.
   PubMed Web of Science ®Google Scholar
• Stamm, S. 2002. Signals and their transduction pathways regulating alternative splicing: a new dimension of the human genome. Hum. Mol. Genet. 11:2409–2416.
   PubMed Web of Science ®Google Scholar
• Stokoe, D., D. G. Campbell, S. Nakielny, H. Hidaka, S. J. Leevers, C. Marshall, and P. Cohen. 1992. MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase. EMBO J. 11:3985–3994.
   PubMedGoogle Scholar
• Svitkin, Y. V., L. P. Ovchinnikov, G. Dreyfuss, and N. Sonenberg. 1996. General RNA binding proteins render translation cap dependent. EMBO J. 15:7147–7155.
   PubMed Web of Science ®Google Scholar
• Tourriere, H., K. Chebli, L. Zekri, B. Courselaud, J. M. Blanchard, E. Bertrand, and J. Tazi. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160:823–831.
   PubMed Web of Science ®Google Scholar
• van Der Houven Van Oordt, W., M. T. Diaz-Meco, J. Lozano, A. R. Krainer, J. Moscat, and J. F. Caceres. 2000. The MKK(3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J. Cell Biol. 149:307–316.
   PubMed Web of Science ®Google Scholar
• Waskiewicz, A. J., A. Flynn, C. G. Proud, and J. A. Cooper. 1997. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J. 16:1909–1920.
   PubMed Web of Science ®Google Scholar
• Waskiewicz, A. J., J. C. Johnson, B. Penn, M. Mahalingam, S. R. Kimball, and J. A. Cooper. 1999. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol. Cell. Biol. 19:1871–1880.
   PubMed Web of Science ®Google Scholar
• Weighardt, F., G. Biamonti, and S. Riva. 1995. Nucleo-cytoplasmic distribution of human hnRNP proteins: a search for the targeting domains in hnRNP A1. J. Cell Sci. 108:545–555.
   PubMed Web of Science ®Google Scholar
• Wilusz, C. J., and J. Wilusz. 2004. Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet. 20:491–497.
   PubMed Web of Science ®Google Scholar
• Windgassen, M., D. Sturm, I. J. Cajigas, C. I. Gonzalez, M. Seedorf, H. Bastians, and H. Krebber. 2004. Yeast shuttling SR proteins Npl3p, Gbp2p, and Hrb1p are part of the translating mRNPs, and Npl3p can function as a translational repressor. Mol. Cell. Biol. 24:10479–10491.
   PubMed Web of Science ®Google Scholar
• Xie, J., J. A. Lee, T. L. Kress, K. L. Mowry, and D. L. Black. 2003. Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein. Proc. Natl. Acad. Sci. USA 100:8776–8781.
   PubMed Web of Science ®Google Scholar
• Yang, X., M. R. Bani, S. J. Lu, S. Rowan, Y. Ben David, and B. Chabot. 1994. The A1 and A1B proteins of heterogeneous nuclear ribonucleoparticles modulate 5′ splice site selection in vivo. Proc. Natl. Acad. Sci. USA 91:6924–6928.
   PubMedGoogle Scholar