MRNA stability changes precede changes in steady-state mRNA amounts during hyperosmotic stress

RNA

Volumn 15, Issue 4, 2009, Pages 600-614

  Molin, Claes ^a   Jauhiainen, Alexandra ^a,b   Warringer, Jonas ^a   Nerman, Olle ^a,b   Sunnerhagen, P E R ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Hoc pathway; Mrna turnover; Saccharomyces cerevisiae; Stress activated map kinase

Indexed keywords

MESSENGER RNA;

ARTICLE; BACTERIAL CELL; GENETIC TRANSCRIPTION; HYPEROSMOTIC STRESS; NONHUMAN; PRIORITY JOURNAL; RNA STABILITY; SACCHAROMYCES CEREVISIAE; STEADY STATE;

MITOGEN-ACTIVATED PROTEIN KINASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSMOSIS; PROTEIN-SERINE-THREONINE KINASES; RNA STABILITY; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 62549149882     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1403509     Document Type: Article

References (53)

1. Albertyn, J., Hohmann, S., Thevelein, J.M., and Prior, B.A, 1994. GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol. Cell. Biol. 14: 4135-4144.
2. Arikawa, E., Sun, Y., Wang, J., Zhou, Q., Ning, B., Dial, S.L., Guo, L., and Yang, J, 2008. Cross-platform comparison of SYBR Green real-time PCR with TaqMan PCR, microarrays and other gene expression measurement technologies evaluated in the MicroArray Quality Control (MAQC) study. BMC Genomics 9: 328. doi: 10.1186/1471-2164-9-328.
3. Asp, E., Nilsson, D., and Sunnerhagen, P. 2008. Fission yeast mitogen- activated protein kinase Styl interacts with translation factors. Eukaryot. Cell 7: 328-338.
4. Bilsland, E., Molin, C, Swaminathan, S., Ramne, A., and Sunnerhagen, P. 2004. Rckl and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol. Microbiol. 53: 1743-1756.
5. Bilsland, E., Hult, M., Bell, S.D., Sunnerhagen, P., and Downs, J.A. 2007. The Bre5/Ubp3 ubiquitin protease complex from budding yeast contributes to the cellular response to DNA damage. DNA Repair (Amst.) 6: 1471-1484.
6. Bilsland-Marchesan, E., Arino, J., Saito, FL, Sunnerhagen, P., and Posas, F. 2000. Rck2 kinase is a substrate for the osmotic stress activated mitogen-activated protein kinase Hogl. Mol. Cell. Biol. 20: 3887-3895.
7. Brewster, J.L., de Valoir, T., Dwyer, N.D., Winter, E., and Gustin, M.C. 1993. An osmosensing signal transduction pathway in yeast. Science 259: 1760-1763.
8. Brown, A.J.P. 1994. Measurement of mRNA stability. In Molecular genetics of yeast: A practical approach (ed. J.R. Johnston), pp. 147- 160. Oxford University Press, Oxford, UK.
9. Canales, R.D., Luo, Y., Willey, J.C, Austermiller, B., Barbacioru, C.C., Boysen, C, Hunkapiller, K., Jensen, R.V., Knight, C.R., Lee, K.Y., et al. 2006. Evaluation of DNA microarray results with quantitative gene expression platforms. Nat. Biotechnol. 24: 1115-1122.
10. Causton, H.C., Ren, B., Koh, S.S., Harbison, C.T., Kanin, E., Jennings, E.G., Lee, T.I., True, H.L., Lander, E.S., and Young, R.A. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol Biol. Cell 12: 323-337.
11. Chen, C.Y., Gherzi, R., Andersen, J.S., Gaietta, G., Jurchott, K., Royer, H.D., Mann, M., and Karin, M. 2000. Nucleolin and YB- 1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes ©Dev. 14: 1236-1248.
12. 2 arrest essential for cell survival at high osmolarity. EMBO J. 25: 2338-2346.
13. de Nadal, E., Casadome, L., and Posas, F. 2003. Targeting the MEF2- like transcription factor Smpl by the stress-activated Hogl mitogen-activated protein kinase. Mol. Cell. Biol. 23: 229-237.
14. de Nadal, E., Zapater, M., Alepuz, P.M., Sumoy, L., Mas, G., and Posas, F. 2004. The MAPK Hogl recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 427: 370-374.
15. Dunand-Sauthier, I., Walker, C.A., Narasimhan, J., Pearce, A.K., Wek, R.C., and Humphrey, T.C 2005. Stress-activated protein kinase pathway functions to support protein synthesis and trans- lational adaptation in response to environmental stress in fission yeast. Eukaryot. Cell 4: 1785-1793.
16. Duttagupta, R., Tian, B., Wilusz, C.J., Khounh, D.T., Soteropoulos, P., Ouyang, M., Dougherty, J.P., and Peltz, S.W. 2005. Global analysis of Publp targets reveals a coordinate control of gene expression through modulation of binding and stability. Mol. Cell Biol. 25: 5499-5513.
17. Escote, X., Zapater, M., Clotet, J., and Posas, F. 2004. Hogl mediates cell-cycle arrest in Gl phase by the dual targeting of Sicl. Nat. Cell Biol. 6: 997-1002.
18. Garcia-Martinez, J., Aranda, A., and Perez-Ortin, J.E. 2004. Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms. Mol. Cell 15: 303-313.
19. Gasch, A.P., Spellman, P.T., Kao, CM., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D., and Brown, P.O. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol. Cell 11: 4241-4257.
20. Gerber, A.P., Herschlag, D., and Brown, P.O. 2004. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol. 2: E79. doi: 10.1371/journal.pbio. 0020079.
21. Grigull, J., Mnaimneh, 8, Pootoolal, J., Robinson, M.D., and Hughes, T.R. 2004. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttran- scriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24: 5534-5547.
22. Hitti, E., Iakovleva, T., Brook, M., Deppenmeier, S., Gruber, A.D., Radzioch, D., Clark, A.R, Blackshear, P.J, Kotlyarov, A., and Gaestel, M. 2006. Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenine/uridine-rich element. Mol. Cell. Biol. 26: 2399-2407.
23. Ihmels, J., Friedlander, G., Bergmann, S, Sarig, O., Ziv, Y., and Barkai, N. 2002. Revealing modular organization in the yeast transcriptional network. Nat. Genet. 31: 370-377.
24. Ihmels, J, Bergmann, S, Gerami-Nejad, M., Yanai, I., McClellan, M., Berman, J., and Barkai, N. 2005. Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 309: 938-940.
25. Jorgensen, P., Rupes, I., Sharom, J.R., Schneper, L., Broach, J.R., and Tyers, M. 2004. A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes ©Dev. 18: 2491-2505.
26. Kontoyiannis, D., Kodyarov, A, Carballo, E., Alexopoulou, L, Blackshear, P.J., Gaestel, M., Davis, R., Flavell, R., and Kollias, G. 2001. Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J. 20: 3760-3770.
27. Krantz, M., Nordlander, B, Valadi, H., Johansson, M., Gustafsson, L, and Hohmann, S. 2004. Anaerobicity prepares Saccharomyces cerevisiae cells for faster adaptation to osmotic shock. Eukaryot. Cell 3: 1381-1390.
28. Lackner, D.H., Beilharz, T.H., Marguerat, S., Mata, J., Watt, S., Schubert, F, Preiss, T, and Bahler, J. 2007. A network of multiple regulatory layers shapes gene expression in fission yeast. Mol. Cell 26: 145-155.
29. MACQ Consortium. 2006. The MicroArray Quality Control (MAQC) Project shows inter- and intraplatform reproducibility of gene expression measurements. Nat. Biotechnol. 24: 1151-1161.
30. Maeda, T., Wurgler-Murphy, S.M., and Saito, PI. 1994. A two- component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245.
31. Mager, W.H. and Varela, J.C. 1993. Osmostress response of the yeast Saccharomyces. Mol. Microbiol. 10: 253-258.
32. Marquez, J.A. and Serrano, R. 1996. Multiple transduction pathways regulate the sodium-extrusion gene PMR2/ENA1 during salt stress in yeast. FEBS Lett. 382: 89-92.
33. Melamed, D, Pnueli, L., and Arava, Y. 2008. Yeast translational response to high salinity: Global analysis reveals regulation at multiple levels. RNA 14: 1337-1351.
34. Molina-Navarro, M.M., Castells-Roca, L., Belli, G., Garcia- Martinez, J., Marin-Navarro, J., Moreno, J., Perez-Ortin, J.E., and Herrero, E. 2008. Comprehensive transcriptional analysis of the oxidative response in yeast. J. Biol. Chem. 283: 17908-17918.
35. Norbeck, J. and Blomberg, A. 1998. Amino acid uptake is strongly affected during exponential growth of Saccharomyces cerevisiae in 0.7 M NaCl medium. FEMS Microbiol. Lett. 158: 121-126.
36. O'Rourke, S.M. and Herskowitz, I. 1998. The Hogl MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes ©Dev. 12: 2874-2886.
37. Pandey, G, Yoshikawa, K., Hirasawa, T, Nagahisa, K., Katakura, Y., Furusawa, C, Shimizu, H., and Shioya, S. 2007. Extracting the hidden features in saline osmotic tolerance in Saccharomyces cerevisiae from DNA microarray data using the self-organizing map: Biosynthesis of amino acids. Appl. Microbiol. Biotechnol. 75: 415-126.
38. Posas, F., Chambers, J.R., Heyman, J.A., Hoeffler, J.P., de Nadal, E., and Arino, J. 2000. The transcriptional response of yeast to saline stress. J. Biol. Chem. 275: 17249-17255.
39. Proft, M. and Struhl, K. 2004. MAP kinase-mediated stress relief that precedes and regulates the timing of transcriptional induction. Cell 118: 351-361.
40. Proft, M., Pascual-Ahuir, A., de Nadal, E., Arino, J., Serrano, R., and Posas, F. 2001. Regulation of the Skol transcriptional repressor by the Hogl MAP kinase in response to osmotic stress. EMBO J. 20: 1123-1133.
41. Puig, S., Askeland, E., and Thiele, D.J. 2005. Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 120: 99-110.
42. Rep, M., Reiser, V., Gartner, U., Thevelein, J.M., Hohmann, S., Ammerer, G., and Ruis, H. 1999. Osmotic stress-induced gene expression in Saccharomyces cerevisiae requires Msnlp and the novel nuclear factor Hotlp. Mol. Cell. Biol. 19: 5474-5485.
43. Rep, M., Krantz, M., Thevelein, J.M., and Hohmann, S. 2000. The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hotlp and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathway-dependent genes. J. Biol. Chem. 275: 8290-8300.
44. Rodriguez-Gabriel, M.A., Burns, G., McDonald, W.H., Martin, V., Yates 3rd, J.R., Bahler, J., and Russell, P. 2003. RNA-binding protein Csxl mediates global control of gene expression in response to oxidative stress. EMBO f. 22: 6256-6266.
45. Schuller, C, Brewster, J.L., Alexander, M.R., Gustin, M.C., and Ruis, H. 1994. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J. 13: 4382-4389.
46. Shalem, O., Dahan, O., Levo, M., Martinez, M.R., Furman, I., Segal, E., and Pilpel, Y. 2008. Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation. Mol. Syst. Biol 4: 223. doi: 10.1037/ msb.2008.59.
47. Smyth, G.K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl Genet. Mol Biol 3: Article 3. http://www.bepress.com/sagmb/vol3/issl/art3.
48. Swaminathan, 8., Masek, T., Molin, C, Pospisek, M., and Sunnerhagen, P. 2006. Rck2 is required for reprogramming of ribosomes during oxidative stress. Mol. Biol Cell 17: 1472- 1482.
49. Teige, M., Scheikl, E., Reiser, V., Ruis, FL, and Ammerer, G. 2001. Rck2, a member of the calmodulin-protein kinase family, links protein synthesis to high osmolarity MAP kinase signaling in budding yeast. Proc. Natl Acad. Sci. 98: 5625-5630.
50. Wang, Y., Liu, C.L., Storey, J.D., Tibshirani, R.J., Herschlag, D., and Brown, P.O. 2002. Precision and functional specificity in mRNA decay. Proc. Natl. Acad. Sci. 99: 5860-5865.
51. Warner, J.R. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24: 437-440.
52. Winzen, R., Kracht, M., Ritter, B., Wilhelm, A. Chen, C.Y., Shyu, A.B., Muller, M., Gaestel, M., Resch, K., and Holtmann, H. 1999. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18: 4969-4980.
53. Yale, J. and Bohnert, H.J. 2001. Transcript expression in Saccharomyces cerevisiae at high salinity. J. Biol Chem. 276: 15996-16007.