Probing the effect of promoters on noise in gene expression using thousands of designed sequences

Genome Research

Volumn 24, Issue 10, 2014, Pages 1698-1706

  Sharon, Eilon ^a,d   Van Dijk, David ^a   Kalma, Yael ^a   Keren, Leeat ^a   Manor, Ohad ^a   Yakhini, Zohar ^b,c   Segal, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b AGILENT LABORATORIES   (United States)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; MESSENGER RNA; TRANSCRIPTION FACTOR; DNA; SACCHAROMYCES CEREVISIAE PROTEIN;

ALLOSTERISM; ARTICLE; BINDING SITE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; ELASTIC TISSUE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE LIBRARY; GENE SEQUENCE; HIGH THROUGHPUT SEQUENCING; KINETICS; NOISE; NOISE MEASUREMENT; NONHUMAN; NUCLEOSOME; PROMOTER REGION; PROTEIN DEGRADATION; REPORTER GENE; REPRODUCIBILITY; TATA BOX; TRANSCRIPTION INITIATION; BIOLOGY; FUNGAL GENE; GENETICS; METABOLISM; MOLECULAR GENETICS; PROCEDURES; SACCHAROMYCES CEREVISIAE; STATISTICAL MODEL;

BINDING SITES; COMPUTATIONAL BIOLOGY; DNA; GENE EXPRESSION; GENES, FUNGAL; LINEAR MODELS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84907527856     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.168773.113     Document Type: Article

References (53)

1. Acar M, Mettetal JT, van Oudenaarden A. 2008. Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40: 471-475.
2. Amit R, Garcia HG, Phillips R, Fraser SE. 2011. Building enhancers from the ground up: a synthetic biology approach. Cell 146: 105-118.
3. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E, Pilpel Y, Barkai N. 2006. Noise in protein expression scales with natural protein abundance. Nat Genet 38: 636-643.
4. Basehoar AD, Zanton SJ, Pugh BF. 2004. Identification and distinct regulation of yeast TATA box-containing genes. Cell 116: 699-709.
5. Batenchuk C, St-Pierre S, Tepliakova L, Adiga S, Szuto A, Kabbani N, Bell JC, Baetz K, KærnM. 2011. Chromosomal position effects are linked to sir2-mediated variation in transcriptional burst size. Biophys J 100: L56-L58.
6. Beaumont HJE, Gallie J, Kost C, Ferguson GC, Rainey PB. 2009. Experimental evolution of bet hedging. Nature 462: 90-93.
7. Blake WJ, Kærn M, Cantor CR, Collins JJ. 2003. Noise in eukaryotic gene expression. Nature 422: 633-637.
8. Blake WJ, Balázsi G, Kohanski MA, Isaacs FJ, Murphy KF, Kuang Y, Cantor CR, Walt DR, Collins JJ. 2006. Phenotypic consequences of promotermediated transcriptional noise. Mol Cell 24: 853-865.
9. Cai L, Friedman N, Xie XS. 2006. Stochastic protein expression in individual cells at the single molecule level. Nature 440: 358-362.
10. Carey LB, van Dijk D, Sloot PMA, Kaandorp JA, Segal E. 2013. Promoter sequence determines the relationship between expression level and noise. PLoS Biol 11: e1001528.
11. Choi JK, Kim YJ. 2009. Intrinsic variability of gene expression encoded in nucleosome positioning sequences. Nat Genet 41: 498-503.
12. Dadiani M, van Dijk D, Segal B, Field Y, Ben-Artzi G, Raveh-Sadka T, Levo M, Kaplow I,Weinberger A, Segal E. 2013. Two DNA-encoded strategies for increasing expression with opposing effects on promoter dynamics and transcriptional noise. Genome Res 23: 966-976.
13. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297: 1183-1186.
14. Friedman N, Cai L, Xie XS. 2006. Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Phys Rev Lett 97: 168302.
15. Gertz J, Siggia ED, Cohen BA. 2009. Analysis of combinatorial cis-regulation in synthetic and genomic promoters. Nature 457: 215-218.
16. Gillespie DT. 1977. Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81: 2340-2361.
17. Giniger E, Ptashne M. 1988. Cooperative DNA binding of the yeast transcriptional activator GAL4. Proc Natl Acad Sci 85: 382-386.
18. Gotea V, Visel A,Westlund JM, Nobrega MA, Pennacchio LA, Ovcharenko I. 2010. Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res 20: 565-577.
19. Hammar P, Leroy P, Mahmutovic A,Marklund EG, Berg OG, Elf J. 2012. The lac repressor displays facilitated diffusion in living cells. Science 336: 1595-1598.
20. Hornung G, Bar-Ziv R, Rosin D, Tokuriki N, Tawfik DS, Oren M, Barkai N. 2012. Noise-mean relationship in mutated promoters. Genome Res 22: 2409-2417.
21. Keren L, Zackay O, Lotan-Pompan M, Barenholz U, Dekel E, Sasson V, Aidelberg G, Bren A, Zeevi D, Weinberger A, et al. 2013. Promoters maintain their relative activity levels under different growth conditions. Mol Syst Biol 9: 701.
22. Khazanov N, Marcovitz A, Levy Y. 2013. Asymmetric DNA-search dynamics by symmetric dimeric proteins. Biochemistry 52: 5335-5344.
23. Kim S, Broströmer E, Xing D, Jin J, Chong S, Ge H, Wang S, Gu C, Yang L, Gao YQ, et al. 2013. Probing allostery through DNA. Science 339: 816-819.
24. Lehner B. 2010. Conflict between noise and plasticity in yeast. PLoS Genet 6: e1001185.
25. LeProust EM, Peck BJ, Spirin K, McCuen HB, Moore B, Namsaraev E, Caruthers MH. 2010. Synthesis of high-quality libraries of long (150mer) oligonucleotides by a novel depurination controlled process. Nucleic Acids Res 38: 2522-2540.
26. Li GW, Berg OG, Elf J. 2009. Effects of macromolecular crowding and DNA looping on gene regulation kinetics. Nat Phys 5: 294-297.
27. MacIsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD, Fraenkel E. 2006. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7: 113.
28. Miller JA, Widom J. 2003. Collaborative competition mechanism for gene activation in vivo. Mol Cell Biol 23: 1623-1632.
29. Mogno I, Vallania F, Mitra RD, Cohen BA. 2010. TATA is a modular component of synthetic promoters. Genome Res 20: 1391-1397.
30. Munsky B, Neuert G, van Oudenaarden A. 2012. Using gene expression noise to understand gene regulation. Science 336: 183-187.
31. Murphy KF, Balázsi G, Collins JJ. 2007. Combinatorial promoter design for engineering noisy gene expression. Proc Natl Acad Sci 104: 12726-12731.
32. Newman JRS, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, Weissman JS. 2006. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441: 840-846.
33. Ozbudak EM, Thattai M, Kurtser I, Grossman AD, van Oudenaarden A. 2002. Regulation of noise in the expression of a single gene. Nat Genet 31: 69-73.
34. Pachkov M, Balwierz PJ, Arnold P, Ozonov E, van Nimwegen E. 2013. SwissRegulon, a database of genome-wide annotations of regulatory sites: recent updates. Nucleic Acids Res 41: D214-D220.
35. Paulsson J. 2004. Summing up the noise in gene networks. Nature 427: 415-418.
36. Pedraza JM, Paulsson J. 2008. Effects of molecular memory and bursting on fluctuations in gene expression. Science 319: 339-343.
37. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A. 2010. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105-D110.
38. Rainey PB, Beaumont HJE, Ferguson GC, Gallie J, Kost C, Libby E, Zhang XX. 2011. The evolutionary emergence of stochastic phenotype switching in bacteria. Microb Cell Fact (Suppl 1) 10: S14.
39. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S. 2006. Stochastic mRNA synthesis in mammalian cells. PLoS Biol 4: e309.
40. Raser JM, O'Shea EK. 2004. Control of stochasticity in eukaryotic gene expression. Science 304: 1811-1814.
41. Raveh-Sadka T, Levo M, Shabi U, Shany B, Keren L, Lotan-Pompan M, Zeevi D, Sharon E, Weinberger A, Segal E. 2012. Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nat Genet 44: 743-750.
42. Sanchez A, Garcia HG, Jones D, Phillips R, Kondev J. 2011. Effect of promoter architecture on the cell-to-cell variability in gene expression. PLoS Comput Biol 7: e1001100.
43. Sharon E, Kalma Y, Sharp A, Raveh-Sadka T, Levo M, Zeevi D, Keren L, Yakhini Z, Weinberger A, Segal E. 2012. Inferring gene regulatory logic from high-throughput measurements of thousands of systematically designed promoters. Nat Biotechnol 30: 521-530.
44. Sherman MS, Cohen BA. 2014. A computational framework for analyzing stochasticity in gene expression. PLoS Comput Biol 10: e1003596.
45. So LH, Ghosh A, Zong C, Sepúlveda LA, Segev R, Golding I. 2011. General properties of transcriptional time series in Escherichia coli. Nat Genet 43: 554-560.
46. Stewart-Ornstein J,Weissman JS, El-Samad H. 2012. Cellular noise regulons underlie fluctuations in Saccharomyces cerevisiae. Mol Cell 45: 483-493.
47. Tirosh I, Barkai N. 2008. Two strategies for gene regulation by promoter nucleosomes. Genome Res 18: 1084-1091.
48. Venters BJ,Wachi S, Mavrich TN, Andersen BE, Jena P, Sinnamon AJ, Jain P, Rolleri NS, Jiang C, Hemeryck-Walsh C, et al. 2011. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell 41: 480-492.
49. Weinberger LS, Burnett JC, Toettcher JE, Arkin AP, Schaffer DV. 2005. Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell 122: 169-182.
50. Weingarten-Gabbay S, Segal E. 2014. The grammar of transcriptional regulation. Hum Genet 133: 701-711.
51. Wunderlich Z,Mirny LA. 2009. Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet 25: 434-440.
52. Zenklusen D, Larson DR, Singer RH. 2008. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat Struct Mol Biol 15: 1263-1271.
53. Zou H, Hastie T. 2005. Regularization and variable selection via the elastic net. Stat Methodol 67: 301-320.