Transcriptional refractoriness is dependent on core promoter architecture

Nature Communications

Volumn 6, Issue , 2015, Pages

  Cesbron, François ^a   Oehler, Michael ^a   Ha, Nati ^a   Sancar, Gencer ^a   Brunner, Michael ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II; SERINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR WHITE COLLAR COMPLEX; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; FRQ PROTEIN, NEUROSPORA CRASSA; FUNGAL PROTEIN; MESSENGER RNA; VVD PROTEIN, NEUROSPORA CRASSA; WC-1 PROTEIN, NEUROSPORA CRASSA; WHITE COLLAR 2 PROTEIN, NEUROSPORA;

FUNGUS; GENE EXPRESSION; GENOME; LIGHT EFFECT; RNA;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION SYSTEM; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; MEMORY; NEUROSPORA; NONHUMAN; PROMOTER REGION; RNA SEQUENCE; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; FEEDBACK SYSTEM; GENE EXPRESSION; GENETICS; LIGHT; METABOLISM; NEUROSPORA CRASSA; PHOSPHORYLATION; PHYSIOLOGY;

NEUROSPORA;

DNA-BINDING PROTEINS; FEEDBACK, PHYSIOLOGICAL; FUNGAL PROTEINS; GENE EXPRESSION; LIGHT; NEUROSPORA CRASSA; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84926683733     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7753     Document Type: Article

References (69)

1. Zenklusen, D., Larson, D. R. & Singer, R. H. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat. Struct. Mol. Biol. 15, 1263-1271 (2008).
2. Holstege, F. C. et al. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717-728 (1998).
3. Schwanhausser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337-342 (2011).
4. Golding, I., Paulsson, J., Zawilski, S. M. & Cox, E. C. Real-time kinetics of gene activity in individual bacteria. Cell 123, 1025-1036 (2005).
5. Chubb, J. R., Trcek, T., Shenoy, S. M. & Singer, R. H. Transcriptional pulsing of a developmental gene. Curr. Biol. 16, 1018-1025 (2006).
6. Raj, A., Peskin, C. S., Tranchina, D., Vargas, D. Y. & Tyagi, S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 4, e309 (2006).
7. Hornung, G. et al. Noise-mean relationship in mutated promoters. Genome Res. 22, 2409-2417 (2012).
8. Dadiani, M. et al. Two DNA-encoded strategies for increasing expression with opposing effects on promoter dynamics and transcriptional noise. Genome Res. 23, 966-976 (2013).
9. To, T. L. & Maheshri, N. Noise can induce bimodality in positive transcriptional feedback loops without bistability. Science 327, 1142-1145 (2010).
10. Murphy, K. F., Balazsi, G. & Collins, J. J. Combinatorial promoter design for engineering noisy gene expression. Proc. Natl Acad. Sci. USA 104, 12726-12731 (2007).
11. Sanchez, A. & Golding, I. Genetic determinants and cellular constraints in noisy gene expression. Science 342, 1188-1193 (2013).
12. Suter, D. M. et al. Mammalian genes are transcribed with widely different bursting kinetics. Science 332, 472-474 (2011).
13. Bar-Even, A. et al. Noise in protein expression scales with natural protein abundance. Nat. Genet. 38, 636-643 (2006).
14. Carey, L. B., van Dijk, D., Sloot, P. M., Kaandorp, J. A. & Segal, E. Promoter sequence determines the relationship between expression level and noise. PLoS Biol. 11, e1001528 (2013).
15. Taniguchi, Y. et al. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329, 533-538 (2010).
16. So, L. H. et al. General properties of transcriptional time series in Escherichia coli. Nat. Genet. 43, 554-560 (2011).
17. Skupsky, R., Burnett, J. C., Foley, J. E., Schaffer, D. V. & Arkin, A. P. HIV promoter integration site primarily modulates transcriptional burst size rather than frequency. PLoS Comput. Biol. 6, e1000952 (2010).
18. Dar, R. D. et al. Transcriptional burst frequency and burst size are equally modulated across the human genome. Proc. Natl Acad. Sci. U S A 109, 17454-17459 (2012).
19. Larson, D. R. et al. Direct observation of frequency modulated transcription in single cells using light activation. Elife 2, e00750 (2013).
20. Raj, A. & van Oudenaarden, A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226 (2008).
21. Voss, T. C. et al. Combinatorial probabilistic chromatin interactions produce transcriptional heterogeneity. J. Cell Sci. 122, 345-356 (2009).
22. Molina, N. et al. Stimulus-induced modulation of transcriptional bursting in a single mammalian gene. Proc. Natl Acad. Sci. USA 110, 20563-20568 (2013).
23. Harper, C. V. et al. Dynamic analysis of stochastic transcription cycles. PLoS Biol. 9, e1000607 (2011).
24. Baker, C. L., Loros, J. J. & Dunlap, J. C. The circadian clock of Neurospora crassa. FEMS Microbiol. Rev. 36, 95-110 (2012).
25. Schafmeier, T. & Diernfellner, A. C. Light input and processing in the circadian clock of Neurospora. FEBS Lett. 585, 1467-1473 (2011).
26. Xue, Z. et al. Transcriptional interference by antisense RNA is required for circadian clock function. Nature 514, 650-653 (2014).
27. Malzahn, E., Ciprianidis, S., Kaldi, K., Schafmeier, T. & Brunner, M. Photoadaptation in Neurospora by competitive interaction of activating and inhibitory LOV domains. Cell 142, 762-772 (2010).
28. Froehlich, A. C., Loros, J. J. & Dunlap, J. C. Rhythmic binding of a WHITE COLLAR-containing complex to the frequency promoter is inhibited by FREQUENCY. Proc. Natl Acad. Sci. USA 100, 5914-5919 (2003).
29. Froehlich, A. C., Liu, Y., Loros, J. J. & Dunlap, J. C. White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297, 815-819 (2002).
30. Zoltowski, B. D., Vaccaro, B. & Crane, B. R. Mechanism-based tuning of a LOV domain photoreceptor. Nat. Chem. Biol. 5, 827-834 (2009).
31. He, Q. & Liu, Y. Molecular mechanism of light responses in Neurospora: from light-induced transcription to photoadaptation. Genes Dev. 19, 2888-2899 (2005).
32. Schafmeier, T. et al. Transcriptional feedback of Neurospora circadian clock gene by phosphorylation-dependent inactivation of its transcription factor. Cell 122, 235-246 (2005).
33. Mayer, A. et al. Uniform transitions of the general RNA polymerase II transcription complex. Nat. Struct. Mol. Biol. 17, 1272-1278 (2010).
34. Phatnani, H. P. & Greenleaf, A. L. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20, 2922-2936 (2006).
35. Cesbron, F., Brunner, M. & Diernfellner, A. C. Light-dependent and circadian transcription dynamics in vivo recorded with a destabilized luciferase reporter in Neurospora . PLoS ONE 8, e83660 (2013).
36. Coulon, A., Chow, C. C., Singer, R. H. & Larson, D. R. Eukaryotic transcriptional dynamics: from single molecules to cell populations. Nat. Rev. Genet. 14, 572-584 (2013).
37. Hager, G. L., McNally, J. G. & Misteli, T. Transcription dynamics. Mol. Cell. 35, 741-753 (2009).
38. Lickwar, C. R., Mueller, F., Hanlon, S. E., McNally, J. G. & Lieb, J. D. Genome-wide protein-DNA binding dynamics suggest a molecular clutch for transcription factor function. Nature 484, 251-255 (2012).
39. Poorey, K. et al. Measuring chromatin interaction dynamics on the second time scale at single-copy genes. Science 342, 369-372 (2013).
40. Larson, D. R., Zenklusen, D., Wu, B., Chao, J. A. & Singer, R. H. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 332, 475-478 (2011).
41. Kennedy, M. J. et al. Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods. 7, 973-975 (2010).
42. Wang, X., Chen, X. & Yang, Y. Spatiotemporal control of gene expression by a light-switchable transgene system. Nat. Methods 9, 266-269 (2012).
43. Polstein, L. R. & Gersbach, C. A. Light-inducible spatiotemporal control of gene activation by customizable zinc finger transcription factors. J. Am. Chem. Soc. 134, 16480-16483 (2012).
44. Konermann, S. et al. Optical control of mammalian endogenous transcription and epigenetic states. Nature 500, 472-476 (2013).
45. Motta-Mena, L. B. et al. An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat. Chem. Biol. 10, 196-202 (2014).
46. Fuda, N. J., Ardehali, M. B. & Lis, J. T. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461, 186-192 (2009).
47. Remenyi, A., Scholer, H. R. & Wilmanns, M. Combinatorial control of gene expression. Nat. Struct. Mol. Biol. 11, 812-815 (2004).
48. Lelli, K. M., Slattery, M. & Mann, R. S. Disentangling the many layers of eukaryotic transcriptional regulation. Annu. Rev. Genet. 46, 43-68 (2012).
49. Sera, T. Zinc-finger-based artificial transcription factors and their applications. Adv. Drug. Deliv. Rev. 61, 513-526 (2009).
50. Struhl, K. & Segal, E. Determinants of nucleosome positioning. Nat. Struct. Mol. Biol. 20, 267-273 (2013).
51. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007).
52. Malik, S. & Roeder, R. G. The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat. Rev. Genet. 11, 761-772 (2010).
53. Lariviere, L., Seizl, M. & Cramer, P. A structural perspective on Mediator function. Curr. Opin. Cell. Biol. 24, 305-313 (2012).
54. Ansari, S. A. & Morse, R. H. Mechanisms of Mediator complex action in transcriptional activation. Cell.Mol. Life Sci. 70, 2743-2756 (2013).
55. Thomas, M. C. & Chiang, C. M. The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 41, 105-178 (2006).
56. Carey, M. PICking apart Pol II initiation. Nat. Struct. Mol. Biol. 19, 737-738 (2012).
57. Grunberg, S., Warfield, L. & Hahn, S. Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening. Nat. Struct. Mol. Biol. 19, 788-796 (2012).
58. Yudkovsky, N., Ranish, J. A. & Hahn, S. A transcription reinitiation intermediate that is stabilized by activator. Nature 408, 225-229 (2000).
59. Little, S. C., Tikhonov, M. & Gregor, T. Precise developmental gene expression arises from globally stochastic transcriptional activity. Cell 154, 789-800 (2013).
60. Chong, S., Chen, C., Ge, H. & Xie, X. S. Mechanism of transcriptional bursting in bacteria. Cell 158, 314-326 (2014).
61. Stratmann, M., Suter, D. M., Molina, N., Naef, F. & Schibler, U. Circadian Dbp transcription relies on highly dynamic BMAL1-CLOCK interaction with E boxes and requires the proteasome. Mol. Cell. 48, 277-287 (2012).
62. Pennington, K. L., Marr, S. K., Chirn, G. W. & Marr, 2nd M. T. Holo-TFIID controls the magnitude of a transcription burst and fine-tuning of transcription. Proc. Natl Acad. Sci. USA 110, 7678-7683 (2013).
63. Belden, W. J. et al. The band mutation in Neurospora crassa is a dominant allele of ras-1 implicating RAS signaling in circadian output. Genes Dev. 21, 1494-1505 (2007).
64. Smith, K. M. et al. Transcription factors in light and circadian clock signaling networks revealed by genomewide mapping of direct targets for neurospora white collar complex. Eukaryot. Cell 9, 1549-1556 (2010).
65. Talora, C., Franchi, L., Linden, H., Ballario, P. & Macino, G. Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO J. 18, 4961-4968 (1999).
66. Johnson, L., Cao, X. & Jacobsen, S. Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360-1367 (2002).
67. Gorl, M. et al. A PEST-like element in FREQUENCY determines the length of the circadian period in Neurospora crassa. EMBO J. 20, 7074-7084 (2001).
68. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome. Biol. 10, R25 (2009).
69. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).