Regulation of glucose-dependent gene expression by the RNA helicase Dbp2 in Saccharomyces cerevisiae

Genetics

Volumn 198, Issue 3, 2014, Pages 1001-1014

  Beck, Zachary T ^a   Cloutier, Sara C ^a   Schipma, Matthew J ^c   Petell, Christopher J ^a   Ma, Wai Kit ^a   Tran, Elizabeth J ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b Purdue University   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; DEAD BOX PROTEIN 2; GLUCOSE; GLUCOSE TRANSPORTER; RNA HELICASE; UNCLASSIFIED DRUG; DBP2 PROTEIN, S CEREVISIAE; MESSENGER RNA; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOGENESIS; CARBON SOURCE; CELLULAR DISTRIBUTION; CYTOPLASM; CYTOSOL; ENERGY BALANCE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE REPRESSION; GENETIC ASSOCIATION; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOTIDE SEQUENCE; NUTRITIONAL STATUS; PROTEIN METABOLISM; PROTEIN STABILITY; RNA SEQUENCE; RNA STRUCTURE; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE; UPREGULATION; CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION; DOWN REGULATION; DRUG EFFECTS; ENZYMOLOGY; EXTRACELLULAR SPACE; FUNGAL GENE; GENE REGULATORY NETWORK; GENETICS; METABOLISM; PROTEIN TRANSPORT; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION; DEAD-BOX RNA HELICASES; DOWN-REGULATION; EXTRACELLULAR SPACE; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENES, FUNGAL; GLUCOSE; PROTEIN TRANSPORT; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84908658486     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.170019     Document Type: Article

References (67)

1. Barta, I., and R. Iggo, 1995 Autoregulation of expression of the yeast Dbp2p’DEAD-box’ protein is mediated by sequences in the conserved DBP2 intron. EMBO J. 14: 3800-3808.
2. Bermejo, C., F. Haerizadeh, H. Takanaga, D. Chermak, and W. B. Frommer, 2010 Dynamic analysis of cytosolic glucose and ATP levels in yeast using optical sensors. Biochem. J. 432: 399-406.
3. Berriz, G. F., J. E. Beaver, C. Cenik, M. Tasan, and F. P. Roth, 2009 Next generation software for functional trend analysis. Bioinformatics 25: 3043-3044.
4. Bhaskaran, H., and R. Russell, 2007 Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 449: 1014-1018.
5. Boer, V. M., C. A. Crutchfield, P. H. Bradley, D. Botstein, and J. D. Rabinowitz, 2010 Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations. Mol. Biol. Cell 21: 198-211.
6. Bohnsack, M. T., R. Martin, S. Granneman, M. Ruprecht, E. Schleiff et al., 2009 Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol. Cell 36: 583-592.
7. Bond, A. T., D. A. Mangus, F. He, and A. Jacobson, 2001 Absence of Dbp2p alters both nonsense-mediated mRNA decay and rRNA processing. Mol. Cell. Biol. 21: 7366-7379.
8. Bowers, H. A., P. A. Maroney, M. E. Fairman, B. Kastner, R. Luhrmann et al., 2006 Discriminatory RNP remodeling by the DEAD-box protein DED1. RNA 12: 903-912.
9. Broach, J. R., 2012 Nutritional control of growth and development in yeast. Genetics 192: 73-105.
10. Buszczak, M., and A. C. Spradling, 2006 The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin. Genes Dev. 20: 977-989.
11. Camats, M., S. Guil, M. Kokolo, and M. Bach-Elias, 2008 P68 RNA helicase (DDX5) alters activity of cis- and trans-acting factors of the alternative splicing of H-Ras. PLoS ONE 3: e2926.
12. Caretti, G., R. L. Schiltz, F. J. Dilworth, M. Di Padova, P. Zhao et al., 2006 The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev. Cell 11: 547-560.
13. Carrieri, C., L. Cimatti, M. Biagioli, A. Beugnet, S. Zucchelli et al., 2012 Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491: 454-457.
14. Castelnuovo, M., S. Rahman, E. Guffanti, V. Infantino, F. Stutz et al., 2013 Bimodal expression of PHO84 is modulated by early termination of antisense transcription. Nat. Struct. Mol. Biol. 20: 851-858.
15. Castoralova, M., D. Brezinova, M. Sveda, J. Lipov, T. Ruml et al., 2012 SUMO-2/3 conjugates accumulating under heat shock or MG132 treatment result largely from new protein synthesis. Biochim. Biophys. Acta 1823: 911-919.
16. Clark, E. L., A. Coulson, C. Dalgliesh, P. Rajan, S. M. Nicol et al., 2008 The RNA helicase p68 is a novel androgen receptor coactivator involved in splicing and is overexpressed in prostate cancer. Cancer Res. 68: 7938-7946.
17. Cloutier, S. C., W. K. Ma, L. T. Nguyen, and E. J. Tran, 2012 The DEAD- box RNA helicase Dbp2 connects RNA quality control with repression of aberrant transcription. J. Biol. Chem. 287: 26155-26166.
18. Cloutier, S. C., S. Wang, W. K. Ma, C. J. Petell, and E. J. Tran, 2013 Long noncoding RNAs promote transcriptional poising of inducible genes. PLoS Biol. 11: e1001715.
19. Del Campo, M., S. Mohr, Y. Jiang, H. Jia, E. Jankowsky et al., 2009 Unwinding by local strand separation is critical for the function of DEAD-box proteins as RNA chaperones. J. Mol. Biol. 389: 674-693.
20. De Vit, M. J., J. A. Waddle, and M. Johnston, 1997 Regulated nuclear translocation of the Mig1 glucose repressor. Mol. Biol. Cell 8: 1603-1618.
21. DeVit, M. J., and M. Johnston, 1999 The nuclear exportin Msn5 is required for nuclear export of the Mig1 glucose repressor of Saccharomyces cerevisiae. Curr. Biol. 9: 1231-1241.
22. Fatica, A., and I. Bozzoni, 2014 Long non-coding RNAs: new players in cell differentiation and development. Nat. Rev. Genet. 15: 7-21.
23. Fuller-Pace, F. V., and H. C. Moore, 2011 RNA helicases p68 and p72: multifunctional proteins with important implications for cancer development. Future Oncol. 7: 239-251.
24. Gancedo, J. M., 1998 Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 62: 334-361.
25. Geisler, S., L. Lojek, A. M. Khalil, K. E. Baker, and J. Coller, 2012 Decapping of long noncoding RNAs regulates inducible genes. Mol. Cell 45: 279-291.
26. Hardie, D. G., F. A. Ross, and S. A. Hawley, 2012 AMP-activated protein kinase: a target for drugs both ancient and modern. Chem. Biol. 19: 1222-1236.
27. Horak, J., 2013 Regulations of sugar transporters: insights from yeast. Curr. Genet. 59: 1-31.
28. Houseley, J., L. Rubbi, M. Grunstein, D. Tollervey, and M. Vogelauer, 2008 A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Mol. Cell 32: 685-695.
29. Jalal, C., H. Uhlmann-Schiffler, and H. Stahl, 2007 Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res. 35: 3590-3601.
30. Jankowsky, E., 2011 RNA helicases at work: binding and rear- ranging. Trends Biochem. Sci. 36: 19-29.
31. Johnson, J. M., S. Edwards, D. Shoemaker, and E. E. Schadt, 2005 Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments. Trends Genet. 21: 93-102.
32. Johnston, M., and J. H. Kim, 2005 Glucose as a hormone: receptor-mediated glucose sensing in the yeast Saccharomyces cerevisiae. Biochem. Soc. Trans. 33: 247-252.
33. Jorgensen, P., I. Rupes, J. R. Sharom, L. Schneper, J. R. Broach et al., 2004 A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev. 18: 2491-2505.
34. Kovalev, N., D. Barajas, and P. D. Nagy, 2012 Similar roles for yeast Dbp2 and Arabidopsis RH20 DEAD-box RNA helicases to Ded1 helicase in tombusvirus plus-strand synthesis. Virology 432: 470-484.
35. Kresnowati, M. T., W. A. van Winden, M. J. Almering, A. ten Pierick, C. Ras et al., 2006 When transcriptome meets metabolome: fast cellular responses of yeast to sudden relief of glucose limitation. Mol. Syst. Biol. 2: 49.
36. Laxman, S., B. M. Sutter, and B. P. Tu, 2010 Behavior of a metabolic cycling population at the single cell level as visualized by fluorescent gene expression reporters. PLoS ONE 5: e12595.
37. Lempiainen, H., and D. Shore, 2009 Growth control and ribosome biogenesis. Curr. Opin. Cell Biol. 21: 855-863.
38. Lohr, D., P. Venkov, and J. Zlatanova, 1995 Transcriptional regulation in the yeast GAL gene family: a complex genetic network. FASEB J. 9: 777-787.
39. Ma, W. K., S. C. Cloutier, and E. J. Tran, 2013 The DEAD-box protein Dbp2 functions with the RNA-binding protein Yra1 to promote mRNP assembly. J. Mol. Biol. 425: 3824-3838.
40. Mitchell, S. F., S. Jain, M. She, and R. Parker, 2013 Global analysis of yeast mRNPs. Nat. Struct. Mol. Biol. 20: 127-133.
41. Munchel, S. E., R. K. Shultzaberger, N. Takizawa, and K. Weis, 2011 Dynamic profiling of mRNA turnover reveals gene- specific and system-wide regulation of mRNA decay. Mol. Biol. Cell 22: 2787-2795.
42. Ochocki, J. D., and M. C. Simon, 2013 Nutrient-sensing pathways and metabolic regulation in stem cells. J. Cell Biol. 203: 23-33.
43. Palsson-McDermott, E. M., and L. A. O’Neill, 2013 The Warburg effect then and now: from cancer to inflammatory diseases. BioEssays 35: 965-973.
44. Pelechano, V., and L. M. Steinmetz, 2013 Gene regulation by antisense transcription. Nat. Rev. Genet. 14: 880-893.
45. Perocchi, F., Z. Xu, S. Clauder-Munster, and L. M. Steinmetz, 2007 Antisense artifacts in transcriptome microarray experiments are resolved by actinomycin D. Nucleic Acids Res. 35: e128.
46. Pfaffl, M. W., 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
47. Piao, H., J. MacLean Freed, and P. Mayinger, 2012 Metabolic activation of the HOG MAP kinase pathway by Snf1/AMPK regulates lipid signaling at the Golgi. Traffic 13: 1522-1531.
48. Pinskaya, M., S. Gourvennec, and A. Morillon, 2009 H3 lysine 4- di- and tri-methylation deposited by cryptic transcription attenuates promoter activation. EMBO J. 28: 1697-1707.
49. Powers, T., and P. Walter, 1999 Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 10: 987-1000.
50. Putnam, A. A., and E. Jankowsky, 2013a AMP sensing by DEAD- box RNA helicases. J. Mol. Biol. 425: 3839-3845.
51. Putnam, A. A., and E. Jankowsky, 2013b DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Biochim. Biophys. Acta 1829: 884-893.
52. Ruiz-Echevarria, M. J., C. I. Gonzalez, and S. W. Peltz, 1998 Identifying the right stop: determining how the surveillance complex recognizes and degrades an aberrant mRNA. EMBO J. 17: 575-589.
53. Salzman, D. W., J. Shubert-Coleman, and H. Furneaux, 2007 P68 RNA helicase unwinds the human let-7 microRNA precursor duplex and is required for let-7-directed silencing of gene expression. J. Biol. Chem. 282: 32773-32779.
54. Sellick, C. A., R. N. Campbell and R. J. Reece, 2008 Galactose metabolism in yeast-structure and regulation of the leloir pathway enzymes and the genes encoding them. Int. Rev. Cell Mol. Biol. 269: 111-150.
55. Traven, A., B. Jelicic, and M. Sopta, 2006 Yeast Gal4: a transcriptional paradigm revisited. EMBO Rep. 7: 496-499.
56. van Dijk, E. L., C. L. Chen, Y. d’Aubenton-Carafa, S. Gourvennec, M. Kwapisz et al., 2011 XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475: 114-117.
57. Verwaal, R., J. W. Paalman, A. Hogenkamp, A. J. Verkleij, C. T. Verrips et al., 2002 HXT5 expression is determined by growth rates in Saccharomyces cerevisiae. Yeast 19: 1029-1038.
58. Wang, J., C. Gong, and L. E. Maquat, 2013 Control of myogenesis by rodent SINE-containing lncRNAs. Genes Dev. 27: 793-804.
59. Warner, J. R., 1999 The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24: 437-440.
60. Westfall, P. J., D. R. Ballon, and J. Thorner, 2004 When the stress of your environment makes you go HOG wild. Science 306: 1511-1512.
61. Wilson, B. J., G. J. Bates, S. M. Nicol, D. J. Gregory, N. D. Perkins et al., 2004 The p68 and p72 DEAD box RNA helicases interact with HDAC1 and repress transcription in a promoter-specific manner. BMC Mol. Biol. 5: 11.
62. Wilson, W. A., S. A. Hawley, and D. G. Hardie, 1996 Glucose repression/ derepression in budding yeast: SNF1 protein kinase is activated by phosphorylation under derepressing conditions, and this correlates with a high AMP:ATP ratio. Curr. Biol. 6: 1426-1434.
63. Woods, A., M. R. Munday, J. Scott, X. Yang, M. Carlson et al., 1994 Yeast SNF1 is functionally related to mammalian AMP- activated protein kinase and regulates acetyl-CoA carboxylase in vivo. J. Biol. Chem. 269: 19509-19515.
64. Wullschleger, S., R. Loewith, and M. N. Hall, 2006 TOR signaling in growth and metabolism. Cell 124: 471-484.
65. Xu, Z., W. Wei, J. Gagneur, F. Perocchi, S. Clauder-Munster et al., 2009 Bidirectional promoters generate pervasive transcription in yeast. Nature 457: 1033-1037.
66. Yang, Q., M. Del Campo, A. M. Lambowitz, and E. Jankowsky, 2007 DEAD-box proteins unwind duplexes by local strand separation. Mol. Cell 28: 253-263.
67. Yang, Q., and E. Jankowsky, 2005 ATP- and ADP-dependent modulation of RNA unwinding and strand annealing activities by the DEAD-box protein DED1. Biochemistry 44: 13591-13601.