A novel class of mRNA-containing cytoplasmic granules are produced in response to UV-irradiation

Molecular Biology of the Cell

Volumn 19, Issue 11, 2008, Pages 4980-4992

  Gaillard, Hélène ^a   Aguilera, Andrés ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E; INITIATION FACTOR 4G; MESSENGER RNA; SODIUM CHLORIDE; GAL1 PROTEIN, S CEREVISIAE; GALACTOKINASE; NITROGEN; POLYADENYLIC ACID; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL GRANULE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; HEAT SHOCK; NONHUMAN; PRIORITY JOURNAL; RNA DEGRADATION; ULTRAVIOLET IRRADIATION; AUTOPHAGY; CYTOLOGY; DRUG EFFECT; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; POLYSOME; RADIATION EXPOSURE; RADIATION RESPONSE; RNA STABILITY; SACCHAROMYCES CEREVISIAE; ULTRAVIOLET RADIATION;

EUKARYOTA;

AUTOPHAGY; CYTOPLASMIC GRANULES; DOSE-RESPONSE RELATIONSHIP, RADIATION; ENDOCYTOSIS; GALACTOKINASE; GENE EXPRESSION REGULATION, FUNGAL; HEAT-SHOCK RESPONSE; NITROGEN; POLY A; POLYRIBOSOMES; RNA STABILITY; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SODIUM CHLORIDE; ULTRAVIOLET RAYS;

EID: 58149300223     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-02-0193     Document Type: Article

References (73)

1. Aas, P. A., Otterlei, M., Falnes, P. O., Vagbo, C. B., Skorpen, F., Akbari, M., Sundheim, O., Bjoras, M., Slupphaug, G., Seeberg, E., and Krokan, H. E. (2003). Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421, 859-863.
2. Anderson, J. T., Paddy, M. R., and Swanson, M. S. (1993). PUB1 is a major nuclear and cytoplasmic polyadenylated RNA-binding protein in Saccharo-myces cerevisiae. Mol. Cell. Biol. 13, 6102-6113.
3. Anderson, P., and Kedersha, N. (2006). RNA granules. J. Cell Biol. 172, 803-808.
4. Anderson, P., and Kedersha, N. (2008). Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141-150.
5. Baltimore, D. (2001). Our genome unveiled. Nature 409, 814-816.
6. Beelman, C. A., and Parker, R. (1994). Differential effects of translational inhibition in cis and in trans on the decay of the unstable yeast MFA2 mRNA. J. Biol. Chem. 269, 9687-9692.
7. Bellacosa, A., and Moss, E. G. (2003). RNA repair: damage control. Curr. Biol. 13, R482-R484.
8. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I., and Filipowicz, W. (2006). Stress-induced reversal of microRNA repression and mRNA P-body localization in human cells. Cold Spring Harb. Symp. Quant. Biol. 71, 513-521.
9. Bollig, F., Winzen, R., Kracht, M., Ghebremedhin, B., Ritter, B., Wilhelm, A., Resch, K., and Holtmann, H. (2002). Evidence for general stabilization of mRNAs in response to UV light. Eur. J. Biochem. 269, 5830-5839.
10. Bouveret,E., Rigaut,G., Shevchenko, A.,Wilm, M., and Seraphin, B. (2000). A Sm-like protein complex that participates in mRNA degradation. EMBO J. 19, 1661-1671.
11. Bregeon, D., and Sarasin, A. (2005). Hypothetical role of RNA damage avoidance in preventing human disease. Mutat. Res. 577, 293-302.
12. Brengues, M., and Parker, R. (2007). Accumulation of polyadenylated mRNA, Pab1p, eIF4E, and eIF4G with P-bodies in Saccharomyces cerevisiae. Mol. Biol. Cell 18, 2592-2602.
13. Brengues, M., Teixeira, D., and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310, 486-489.
14. Cole, C. N., Heath, C. V., Hodge, C. A., Hammell, C. M., and Amberg, D. C. (2002). Analysis of RNA export. Methods Enzymol. 351, 568-587.
15. Cougot, N., Babajko, S., and Seraphin, B. (2004). Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165, 31-40.
16. Decker, C. J., and Parker, R. (1993). A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 7, 1632-1643.
17. Decker, C. J., and Parker, R. (2006). CAR-1 and trailer hitch: driving mRNP granule function at the ER? J. Cell Biol. 173, 159-163.
18. Del Gatto-Konczak, F., Bourgeois, C. F., Le Guiner, C., Kister, L., Gesnel, M. C., Stevenin, J., and Breathnach,R. (2000). The RNA-bindingprotein TIA-1 is a novel mammalian splicing regulator acting through intron sequences adjacent to a 5' splice site. Mol. Cell. Biol. 20, 6287-6299.
19. Doma, M. K., and Parker, R. (2006). Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440, 561-564.
20. Dunand-Sauthier, I., Walker, C., Wilkinson, C., Gordon, C., Crane, R., Norbury, C., and Humphrey, T. (2002). Sum1, a component of the fission yeast eIF3 translation initiation complex, is rapidly relocalized during environmental stress and interacts with components of the 26S proteasome. Mol. Biol. Cell 13, 1626-1640.
21. Duttagupta, R., Tian, B., Wilusz, C. J., Khounh, D. T., Soteropoulos, P., Ouyang,M.,Dougherty,J. P., and Peltz,S. W. (2005). Global analysis ofPub1p targets reveals a coordinate control of gene expression through modulation of binding and stability. Mol. Cell. Biol. 25, 5499-5513.
22. Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007). P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8, 9-22.
23. Falnes, P. O., Klungland, A., and Alseth, I. (2007). Repair of methyl lesions in DNA and RNA by oxidative demethylation. Neuroscience 145, 1222-1232.
24. Forch, P., Puig, O., Kedersha, N., Martinez, C., Granneman, S., Seraphin, B., Anderson, P., and Valcarcel, J. (2000). The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol. Cell 6, 1089-1098.
25. Gaillard, H., Wellinger, R. E., and Aguilera, A. (2007). A new connection of mRNP biogenesis and export with transcription-coupled repair. Nucleic Acids Res. 35, 3893-3906.
26. Gowrishankar,G.,Winzen,R.,Bollig,F.,Ghebremedhin,B.,Redich,N.,Ritter, B., Resch, K., Kracht, M., and Holtmann, H. (2005). Inhibition of mRNA deadenylation and degradation by ultraviolet light. Biol. Chem. 386, 1287-1293.
27. Gowrishankar, G., Winzen, R., Dittrich-Breiholz, O., Redich, N., Kracht, M., and Holtmann, H. (2006). Inhibition of mRNA deadenylation and degradation by different types of cell stress. Biol. Chem. 387, 323-327.
28. Grigull, J., Mnaimneh, S., Pootoolal, J., Robinson, M. D., and Hughes, T. R. (2004). Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24, 5534-5547.
29. Heminger, K. A., Hartson, S. D., Rogers, J., and Matts, R. L. (1997). Cisplatin inhibits protein synthesis in rabbit reticulocyte lysate by causing an arrest in elongation. Arch. Biochem. Biophys. 344, 200-207.
30. Herrick, D., Parker, R., and Jacobson, A. (1990). Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 2269-2284.
31. Hieronymus, H., Yu, M. C., and Silver, P. A. (2004). Genome-wide mRNA surveillance is coupled to mRNA export. Genes Dev. 18, 2652-2662.
32. Hilgers, V., Teixeira, D., and Parker, R. (2006). Translation-independent inhibition of mRNA deadenylation during stress in Saccharomyces cerevisiae. RNA 12, 1835-1845.
33. Hollams, E. M., Giles, K. M., Thomson, A. M., and Leedman, P. J. (2002). MRNA stability and the control of gene expression: implications for human disease. Neurochem. Res. 27, 957-980.
34. Hoyle, N. P., Castelli, L. M., Campbell, S. G., Holmes, L. E., and Ashe, M. P. (2007). Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J. Cell Biol. 179, 65-74.
35. Hurter, J., Gordon, M. P., Kirwan, J. P., and McLaren, A. D. (1974). In vitro photoreactivation of ultraviolet-inactivated ribonucleic acid from tobacco mosaic virus. Photochem. Photobiol. 19, 185-190.
36. Kedersha, N., and Anderson, P. (2002). Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30, 963-969.
37. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M. J., Scheuner, D., Kaufman, R. J., Golan, D. E., and Anderson, P. (2005). Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169, 871-884.
38. Kedersha, N. L., Gupta, M., Li, W., Miller, I., and Anderson, P. (1999). RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 147, 1431-1442.
39. Kimball, S. R., Horetsky, R. L., Ron, D., Jefferson, L. S., and Harding, H. P. (2003). Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am. J. Physiol. Cell Physiol. 284, C273-C284.
40. Klionsky, D. J. (2005a). Autophagy. Curr. Biol. 15, R282-R283.
41. Klionsky, D. J. (2005b). The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118, 7-18.
42. Kressler, D., de la Cruz, J., Rojo, M., and Linder, P. (1997). Fal1p is an essential DEAD-box protein involved in 40S-ribosomal-subunit biogenesis in Saccharo-myces cerevisiae. Mol. Cell. Biol. 17, 7283-7294.
43. Kuai, L., Das, B., and Sherman, F. (2005). A nuclear degradation pathway controls the abundance of normal mRNAs in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 102, 13962-13967.
44. Mason, P. B., and Struhl, K. (2003). The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol. Cell. Biol. 23, 8323-8333.
45. Masta, A., Gray, P. J., and Phillips, D. R. (1995). Nitrogen mustard inhibits transcription and translation in a cell free system. Nucleic Acids Res. 23, 3508-3515.
46. Matunis, M. J., Matunis, E. L., and Dreyfuss, G. (1993). PUB 1, a major yeast poly(A)+ RNA-binding protein. Mol. Cell. Biol. 13, 6114-6123.
47. Merriam, V., and Gordon, M. P. (1965). Photoreactivation of tobacco mosaic virus ribonucleic acid following near ultraviolet irradiation. Proc. Natl. Acad. Sci. USA 54, 1261-1268.
48. Muhlrad, D., Decker, C. J., and Parker, R. (1994). Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5' - >3' digestion of the transcript. Genes Dev. 8, 855-866.
49. Murphy, T. M., and Gordon, M. P. (1971). Light-mediated regulation of TMV-RNA photoreactivation. Photochem. Photobiol. 13, 45-55.
50. Nakagawa, T., and Ogawa, H. (1999). The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control in meiosis. EMBO J. 18, 5714-5723.
51. Nunomura, A., Honda, K., Takeda, A., Hirai, K., Zhu, X., Smith, M. A., and Perry, G. (2006). Oxidative damage to RNA in neurodegenerative diseases. J. Biomed. Biotechnol. 2006, 82323
52. Ogawa, H., Johzuka, K., Nakagawa, T., Leem, S. H., and Hagihara, A. H. (1995). Functions of the yeast meiotic recombination genes, MRE11 and MRE2. Adv. Biophys. 31, 67-76.
53. Ougland, R., Zhang, C. M., Liiv, A., Johansen, R. F., Seeberg, E., Hou, Y. M., Remme, J., and Falnes, P. O. (2004). AlkB restores the biological function of mRNA and tRNA inactivated by chemical methylation. Mol. Cell 16, 107-116.
54. Parker, R., and Sheth, U. (2007). P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646.
55. Puig, O., Gottschalk, A., Fabrizio, P., and Seraphin, B. (1999). Interaction of the U1 snRNP with nonconserved intronic sequences affects 5' splice site selection. Genes Dev. 13, 569-580.
56. Reagan, M. S., and Friedberg, E. C. (1997). Recovery of RNA polymerase II synthesis following DNA damage in mutants of Saccharomyces cerevisiae defective in nucleotide excision repair. Nucleic Acids Res. 25, 4257-4263.
57. Revenkova, E., Masson, J., Koncz, C., Afsar, K., Jakovleva, L., and Paszkowski, J. (1999). Involvement of Arabidopsis thaliana ribosomal protein S27 in mRNA degradation triggered by genotoxic stress. EMBO J. 18, 490-499.
58. Rosenberg, J., and Sato, P. (1988). Messenger RNA loses the ability to direct in vitro peptide synthesis following incubation with cisplatin. Mol. Pharmacol. 33, 611-616.
59. Ruiz-Echevarria, M. J., and Peltz, S. W. (2000). The RNA binding protein Pub1 modulates the stability of transcripts containing upstream open reading frames. Cell 101, 741-751.
60. Rycyna, R. E., and Alderfer, J. L. (1988). Ultraviolet irradiation of nucleic acids: formation, purification, and solution conformational analyses of the cis-syn and trans-syn photodimers of UpU. Biochemistry 27, 3142-3151.
61. Saavedra, C., Tung, K. S., Amberg, D. C., Hopper, A. K., and Cole, C. N. (1996). Regulation of mRNA export in response to stress in Saccharomyces cerevisiae. Genes Dev. 10, 1608-1620.
62. Sheth, U., and Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300, 805-808.
63. Smerdon, M. J., Bedoyan, J., and Thoma, F. (1990). DNA repair in a small yeast plasmid folded into chromatin. Nucleic Acids Res. 18, 2045-2051.
64. St Johnston, D. (2005). Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 6, 363-375.
65. Stimac, E., Groppi, V. E., Jr., and Coffino, P. (1984). Inhibition of protein synthesis stabilizes histone mRNA. Mol. Cell. Biol. 4, 2082-2090.
66. Tani, T., Derby, R. J., Hiraoka, Y., and Spector, D. L. (1995). Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport. Mol. Biol. Cell 6, 1515-1534.
67. Teixeira, D., Sheth, U., Valencia-Sanchez, M. A., Brengues, M., and Parker, R. (2005). Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11, 371-382.
68. Tharun, S., He, W., Mayes, A. E., Lennertz, P., Beggs, J. D., and Parker, R. (2000). Yeast Sm-like proteins function in mRNA decapping and decay. Nature 404, 515-518.
69. Tharun, S., and Parker, R. (1999). Analysis of mutations in the yeast mRNA decapping enzyme. Genetics 151, 1273-1285.
70. Trautwein, M., Dengjel, J., Schirle, M., and Spang, A. (2004). Arf1p provides an unexpected link between COPI vesicles and mRNA in Saccharomyces cerevisiae. Mol. Biol. Cell 15, 5021-5037.
71. Vasudevan, S., and Peltz, S. W. (2001). Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. Mol. Cell 7, 1191-1200.
72. Wilczynska, A., Aigueperse, C., Kress, M., Dautry, F., and Weil, D. (2005). The translational regulator CPEB1 provides a link between dcp1 bodies and stress granules. J. Cell Sci. 118, 981-992.
73. Yoshida, J., and Tani, T. (2005). Hsp16p is required for thermotolerance in nuclear mRNA export in fission yeast Schizosaccharomyces pombe. Cell Struct. Funct. 29, 125-138.