Noise in gene expression is coupled to growth rate

Genome Research

Volumn 25, Issue 12, 2015, Pages 1893-1902

  Keren, Leeat ^a   Van Dijk, David ^a,b   Weingarten Gabbay, Shira ^a   Davidi, Dan ^a   Jona, Ghil ^a   Weinberger, Adina ^a   Milo, Ron ^a   Segal, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CYCLE; FLOW CYTOMETRY; GENE EXPRESSION; GENE SEQUENCE; GLOBAL CHANGE; GROWTH RATE; NONHUMAN; NUTRITIONAL STATUS; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; BIOLOGICAL MODEL; ENVIRONMENT; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SINGLE CELL ANALYSIS; TRANSCRIPTION INITIATION;

CELL CYCLE; ENVIRONMENT; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; GENE-ENVIRONMENT INTERACTION; MODELS, BIOLOGICAL; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SINGLE-CELL ANALYSIS; TRANSCRIPTIONAL ACTIVATION;

EID: 84944443140     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.191635.115     Document Type: Article

References (63)

1. Acar M, Becskei A, van Oudenaarden A. 2005. Enhancement of cellular memory by reducing stochastic transitions. Nature 435: 228-232.
2. Acar M, Mettetal JT, van Oudenaarden A. 2008. Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40: 471-475.
3. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. 2004. Bacterial persistence as a phenotypic switch. Science 305: 1622-1625.
4. Balázsi G, van Oudenaarden A, Collins JJ. 2011. Cellular decision making and biological noise: from microbes to mammals. Cell 144: 910-925.
5. 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.
6. Basehoar AD, Zanton SJ, Pugh BF. 2004. Identification and distinct regulation of yeast TATA box-containing genes. Cell 116: 699-709.
7. Berthoumieux S, de Jong H, Baptist G, Pinel C, Ranquet C, Ropers D, Geiselmann J. 2013. Shared control of gene expression in bacteria by transcription factors and global physiology of the cell. Mol Syst Biol 9: 634.
8. Blake WJ, Kærn M, Cantor CR, Collins JJ. 2003. Noise in eukaryotic gene expression. Nature 422: 633-637.
9. 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.
10. Brauer MJ, Huttenhower C, Airoldi EM, Rosenstein R, Matese JC, Gresham D, Boer VM, Troyanskaya OG, Botstein D. 2008. Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol Biol Cell 19: 352-367.
11. Bryant GO, Prabhu V, Floer M, Wang X, Spagna D, Schreiber D, Ptashne M. 2008. Activator control of nucleosome occupancy in activation and repression of transcription. PLoS Biol 6: 2928-2939.
12. Carey LB, van Dijk D, Sloot PM, Kaandorp JA, Segal E. 2013. Promoter sequence determines the relationship between expression level and noise. PLoS Biol 11: e1001528.
13. Cohen AA, Geva-Zatorsky N, Eden E, Frenkel-Morgenstern M, Issæva I, Sigal A, Milo R, Cohen-Saidon C, Liron Y, Kam Z, et al. 2008. Dynamic proteomics of individual cancer cells in response to a drug. Science 322: 1511-1516.
14. Colman-Lerner A, Gordon A, Serra E, Chin T, Resnekov O, Endy D, Pesce CG, Brent R. 2005. Regulated cell-to-cell variation in a cell-fate decision system. Nature 437: 699-706.
15. 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.
16. Dar RD, Hosmane NN, Arkin MR, Siliciano RF, Weinberger LS. 2014. Screening for noise in gene expression identifies drug synergies. Science 344: 1392-1396.
17. Das Neves RP, Jones NS, Andreu L, Gupta R, Enver T, Iborra FJ. 2010. Connecting variability in global transcription rate to mitochondrial variability. PLoS Biol 8: e1000560.
18. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297: 1183-1186.
19. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, Lubling Y, Widom J, Segal E. 2008. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 4: e1000216.
20. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
21. Gerosa L, Kochanowski K, Heinemann M, Sauer U. 2013. Dissecting specific and global transcriptional regulation of bacterial gene expression. Mol Syst Biol 9: 658.
22. Grossman AD. 1995. Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu Rev Genet 29: 477-508.
23. Guido NJ, Lee P, Wang X, Elston TC, Collins JJ. 2007. A pathway and genetic factors contributing to elevated gene expression noise in stationary phase. Biophys J 93: L55-L57.
24. 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.
25. Huisinga KL, Pugh BF. 2004. A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiæ. Mol Cell 13: 573-585.
26. Ingraham JL, Maaløe O, Neidhardt FC. 1983. Growth of the bacterial cell. Sinauer Associates, Sunderland, MA.
27. Johnston GC, Ehrhardt CW, Lorincz A, Carter BL. 1979. Regulation of cell size in the yeast Saccharomyces cerevisiæ. J Bacteriol 137: 1-5.
28. Jones DL, Brewster RC, Phillips R. 2014. Promoter architecture dictates cellto-cell variability in gene expression. Science 346: 1533-1536.
29. Kærn M, Elston TC, Blake WJ, Collins JJ. 2005. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6: 451-464.
30. Kaufmann BB, Yang Q, Mettetal JT, van Oudenaarden A. 2007. Heritable stochastic switching revealed by single-cell genealogy. PLoS Biol 5: e239.
31. 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.
32. Klumpp S, Hwa T. 2008. Growth-rate-dependent partitioning of RNA polymerases in bacteria. Proc Natl Acad Sci 105: 20245-20250.
33. Klumpp S, Hwa T. 2014. Bacterial growth: global effects on gene expression, growth feedback and proteome partition. Curr Opin Biotechnol 28: 96-102.
34. Klumpp S, Zhang Z, Hwa T. 2009. Growth rate-dependent global effects on gene expression in bacteria. Cell 139: 1366-1375.
35. Lee J, Lee J, Farquhar KS, Yun J, Frankenberger CA, Bevilacqua E, Yeung K, Kim EJ, Balázsi G, Rosner MR. 2014. Network of mutually repressive metastasis regulators can promote cell heterogeneity and metastatic transitions. Proc Natl Acad Sci 111: E364-E373.
36. Levy S, Ihmels J, Carmi M, Weinberger A, Friedlander G, Barkai N. 2007. Strategy of transcription regulation in the budding yeast. PLoS One 2: e250.
37. Levy SF, Ziv N, Siegal ML. 2012. Bet hedging in yeast by heterogeneous, agecorrelated expression of a stress protectant. PLoS Biol 10: e1001325.
38. Maamar H, Raj A, Dubnau D. 2007. Noise in gene expression determines cell fate in Bacillus subtilis. Science 317: 526-529.
39. Miller AW, Befort C, Kerr EO, Dunham MJ. 2013. Design and use of multiplexed chemostat arrays. J Vis Exp e50262.
40. Munsky B, Neuert G, van Oudenaarden A. 2012. Using gene expression noise to understand gene regulation. Science 336: 183-187.
41. Nachman I, Regev A, Ramanathan S. 2007. Dissecting timing variability in yeast meiosis. Cell 131: 544-556.
42. Newman JRS, Ghæmmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL, Weissman JS. 2006. Single-cell proteomic analysis of S. cerevisiæ reveals the architecture of biological noise. Nature 441: 840-846.
43. O'Duibhir E, Lijnzaad P, Benschop JJ, Lenstra TL, van Leenen D, Groot Koerkamp MJ, Margaritis T, Brok MO, Kemmeren P, Holstege FC. 2014. Cell cycle population effects in perturbation studies. Mol Syst Biol 10: 732.
44. Pedersen S, Bloch PL, Reeh S, Neidhardt FC. 1978. Patterns of protein synthesis in E. coli: a catalog of the amount of 140 individual proteins at different growth rates. Cell 14: 179-190.
45. Pedraza JM, van Oudenaarden A. 2005. Noise propagation in gene networks. Science 307: 1965-1969.
46. Raj A, van Oudenaarden A. 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135: 216-226.
47. Rao CV, Wolf DM, Arkin AP. 2002. Control, exploitation and tolerance of intracellular noise. Nature 420: 231-237.
48. Raser JM, O'Shea EK. 2004. Control of stochasticity in eukaryotic gene expression. Science 304: 1811-1814.
49. 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.
50. Regenberg B, Grotkjær T, Winther O, Fausbøll A, Akesson M, Bro C, Hansen LK, Brunak S, Nielsen J. 2006. Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiæ. Genome Biol 7: R107.
51. Sanchez A, Golding I. 2013. Genetic determinants and cellular constraints in noisy gene expression. Science 342: 1188-1193.
52. Schwabe A, Bruggeman FJ. 2014. Contributions of cell growth and biochemical reactions to nongenetic variability of cells. Biophys J 107: 301-313.
53. Slater ML, Sharrow SO, Gart JJ. 1977. Cell cycle of Saccharomyces cerevisiæ in populations growing at different rates. Proc Natl Acad Sci 74: 3850-3854.
54. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiæ by microarray hybridization. Mol Biol Cell 9: 3273-3297.
55. Stewart-Ornstein J, Weissman JS, El-Samad H. 2012. Cellular noise regulons underlie fluctuations in Saccharomyces cerevisiæ. Mol Cell 45: 483-493.
56. Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie XS. 2010. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329: 533-538.
57. Thattai M, van Oudenaarden A. 2001. Intrinsic noise in gene regulatory networks. Proc Natl Acad Sci 98: 8614-8619.
58. Tirosh I, Barkai N. 2008. Two strategies for gene regulation by promoter nucleosomes. Genome Res 18: 1084-1091.
59. Tyson CB, Lord PG, Wheals AE. 1979. Dependency of size of Saccharomyces cerevisiæ cells on growth rate. J Bacteriol 138: 92-98.
60. Vardi N, Levy S, Assaf M, Carmi M, Barkai N. 2013. Budding yeast escape commitment to the phosphate starvation program using gene expression noise. Curr Biol 23: 2051-2057.
61. Volfson D, Marciniak J, Blake WJ, Ostroff N, Tsimring LS, Hasty J. 2006. Origins of extrinsic variability in eukaryotic gene expression. Nature 439: 861-864.
62. 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.
63. Zopf CJ, Quinn K, Zeidman J, Maheshri N. 2013. Cell-cycle dependence of transcription dominates noise in gene expression. PLoS Comput Biol 9: e1003161.