Teasing Apart Translational and Transcriptional Components of Stochastic Variations in Eukaryotic Gene Expression

PLoS Computational Biology

Volumn 8, Issue 8, 2012, Pages

  Salari, Raheleh ^a,f   Wojtowicz, Damian ^a,b   Zheng, Jie ^c   Levens, David ^d   Pilpel, Yitzhak ^e   Przytycka, Teresa M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF WARSAW   (Poland)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d NATIONAL CANCER INSTITUTE   (United States)

^e WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^f Stanford University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STOCHASTIC MODELS; STOCHASTIC SYSTEMS; TRANSCRIPTION;

CELL-TO-CELL VARIATION; CODON USAGE; EUKARYOTIC GENE EXPRESSION; GENES EXPRESSION; NOISE STRENGTH; SEQUENCE FEATURES; SINGLE CELLS ANALYSIS; STOCHASTIC VARIATION; STOCHASTICITY; TATA BOX;

PROTEINS;

RIBOSOME PROTEIN; TRANSFER RNA;

5' UNTRANSLATED REGION; ARTICLE; CODON USAGE; EUKARYOTE; GENE EXPRESSION; RIBOSOME; RNA STRUCTURE; RNA TRANSCRIPTION; RNA TRANSLATION; TATA BOX; THEORETICAL MODEL;

EUKARYOTA;

EID: 84866082847     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002644     Document Type: Article

References (59)

1. Elowitz MB, Levine AJ, Siggia ED, Swain PS, (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186.
2. Raser JM, O'Shea EK, (2005) Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013.
3. Kaern M, Elston TC, Blake WJ, Collins JJ, (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6: 451-464.
4. Fraser HB, Hirsh AE, Giaever G, Kumm J, Eisen MB, (2004) Noise minimization in eukaryotic gene expression. PLoS Biol 2: e137.
5. Bahar R, Hartmann CH, Rodriguez KA, Denny AD, Busuttil RA, et al. (2006) Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 441: 1011-1014.
6. Lehner B, (2008) Selection to minimise noise in living systems and its implications for the evolution of gene expression. Mol Syst Biol 4: 170.
7. Becskei A, Serrano L, (2000) Engineering stability in gene networks by autoregulation. Nature 405: 590-593.
8. Acar M, Becskei A, van Oudenaarden A, (2005) Enhancement of cellular memory by reducing stochastic transitions. Nature 435: 228-232.
9. Chang HH, Hemberg M, Barahona M, Ingber DE, Huang S, (2008) Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453: 544-547.
10. Janes KA, Wang C-C, Holmberg KJ, Cabral K, Brugge JS, (2010) Identifying single-cell molecular programs by stochastic profiling. Nat Meth 7: 311-317.
11. Becskei A, Seraphin B, Serrano L, (2001) Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion. EMBO J 20: 2528-2535.
12. Rao CV, Wolf DM, Arkin AP, (2002) Control, exploitation and tolerance of intracellular noise. Nature 420: 231-237.
13. Kramer BP, Fussenegger M, (2005) Hysteresis in a synthetic mammalian gene network. Proc Natl Acad Sci U S A 102: 9517-9522.
14. Guido NJ, Wang X, Adalsteinsson D, McMillen D, Hasty J, et al. (2006) A bottom-up approach to gene regulation. Nature 439: 856-860.
15. Zhang Z, Qian W, Zhang J, (2009) Positive selection for elevated gene expression noise in yeast. Mol Syst Biol 5: 299.
16. Wang Z, Zhang J, (2011) Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc Natl Acad Sci U S A 108: E67-76.
17. Thattai M, van Oudenaarden A, (2001) Intrinsic noise in gene regulatory networks. Proc Natl Acad Sci U S A 98: 8614-8619.
18. Osella M, Bosia C, Cora D, Caselle M, (2011) The role of incoherent microRNA-mediated feedforward loops in noise buffering. PLoS Comput Biol 7: e1001101.
19. Kittisopikul M, Suel GM, (2010) Biological role of noise encoded in a genetic network motif. Proc Natl Acad Sci U S A 107: 13300-13305.
20. Rodriguez Martinez M, Soriano J, Tlusty T, Pilpel Y, Furman I, (2010) Messenger RNA fluctuations and regulatory RNAs shape the dynamics of a negative feedback loop. Phys Rev E Stat Nonlin Soft Matter Phys 81: 031924.
21. Jothi R, Balaji S, Wuster A, Grochow JA, Gsponer J, et al. (2009) Genomic analysis reveals a tight link between transcription factor dynamics and regulatory network architecture. Mol Syst Biol 5: 294.
22. Li J, Min R, Vizeacoumar FJ, Jin K, Xin X, et al. (2010) Exploiting the determinants of stochastic gene expression in Saccharomyces cerevisiae for genome-wide prediction of expression noise. Proc Natl Acad Sci U S A 107: 10472-10477.
23. Swain PS, Elowitz MB, Siggia ED, (2002) Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc Natl Acad Sci U S A 99: 12795-12800.
24. Hilfinger A, Paulsson J, (2011) Separating intrinsic from extrinsic fluctuations in dynamic biological systems. Proc Natl Acad Sci U S A 108: 12167-12172.
25. Maheshri N, O'Shea EK, (2007) Living with noisy genes: how cells function reliably with inherent variability in gene expression. Annu Rev Biophys Biomol Struct 36: 413-434.
26. Raser JM, O'Shea EK, (2004) Control of Stochasticity in Eukaryotic Gene Expression. Science 304: 1811-1814.
27. Maamar H, Raj A, Dubnau D, (2007) Noise in Gene Expression Determines Cell Fate in Bacillus subtilis. Science 317: 526-529.
28. Mao C, Brown CR, Falkovskaia E, Dong S, Hrabeta-Robinson E, et al. (2010) Quantitative analysis of the transcription control mechanism. Mol Syst Biol 6: 431.
29. Newman JR, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, et al. (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441: 840-846.
30. 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.
31. Blake WJ, M KA, Cantor CR, Collins JJ, (2003) Noise in eukaryotic gene expression. Nature 422: 633-637.
32. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E, et al. (2006) Noise in protein expression scales with natural protein abundance. Nat Genet 38: 636-643.
33. Golding I, Paulsson J, Zawilski SM, Cox EC, (2005) Real-time kinetics of gene activity in individual bacteria. Cell 123: 1025-1036.
34. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S, (2006) Stochastic mRNA synthesis in mammalian cells. PLoS Biol 4: e309.
35. Suter DM, Molina N, Gatfield D, Schneider K, Schibler U, et al. (2011) Mammalian Genes Are Transcribed with Widely Different Bursting Kinetics. Science 332: 472-474.
36. Cai L, Friedman N, Xie XS, (2006) Stochastic protein expression in individual cells at the single molecule level. Nature 440: 358-362.
37. Silander OK, Nikolic N, Zaslaver A, Bren A, Kikoin I, et al. (2012) A Genome-Wide Analysis of Promoter-Mediated Phenotypic Noise in Escherichia coli. PLoS Genet 8: e1002443.
38. Pilpel Y, (2011) Noise in biological systems: pros, cons, and mechanisms of control. Methods Mol Biol 759: 407-425.
39. Grantham R, Gautier C, Gouy M, Jacobzone M, Mercier R, (1981) Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res 9: r43-74.
40. Bennetzen JL, Hall BD, (1982) Codon selection in yeast. J Biol Chem 257: 3026-3031.
41. Gouy M, Gautier C, (1982) Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10: 7055-7074.
42. Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, et al. (2010) Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329: 533-538.
43. Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, et al. (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature 467: 103-107.
44. Pestova TV, Kolupaeva VG, (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16: 2906-2922.
45. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS, (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-223.
46. Kudla G, Murray AW, Tollervey D, Plotkin JB, (2009) Coding-sequence determinants of gene expression in Escherichia coli. Science 324: 255-258.
47. de Smit MH, van Duin J, (1990) Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. Proc Natl Acad Sci U S A 87: 7668-7672.
48. Ringner M, Krogh M, (2005) Folding free energies of 5′-UTRs impact post-transcriptional regulation on a genomic scale in yeast. PLoS Comput Biol 1: e72.
49. dos Reis M, Wernisch L, Savva R, (2003) Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome. Nucleic Acids Res 31: 6976-6985.
50. Alhabshan F, Smallhorn JF, Golding F, Musewe N, Freedom RM, et al. (2005) Extent of myocardial non-compaction: comparison between MRI and echocardiographic evaluation. Pediatr Radiol 35: 1147-1151.
51. Gu W, Zhou T, Wilke CO, (2010) A universal trend of reduced mRNA stability near the translation-initiation site in prokaryotes and eukaryotes. PLoS Comput Biol 6: e1000664.
52. Friedman N, Cai L, Xie XS, (2006) Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Phys Rev Lett 97: 168302.
53. Paulsson J, Ehrenberg M, (2000) Random signal fluctuations can reduce random fluctuations in regulated components of chemical regulatory networks. Phys Rev Lett 84: 5447-5450.
54. Blake WJ, Balazsi G, Kohanski MA, Isaacs FJ, Murphy KF, et al. (2006) Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell 24: 853-865.
55. Mogno I, Vallania F, Mitra RD, Cohen BA, (2010) TATA is a modular component of synthetic promoters. Genome Res 20: 1391-1397.
56. Basehoar AD, Zanton SJ, Pugh BF, (2004) Identification and distinct regulation of yeast TATA box-containing genes. Cell 116: 699-709.
57. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, et al. (2010) An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141: 344-354.
58. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996-1006.
59. Bernhart SH, Hofacker IL, Stadler PF, (2006) Local RNA base pairing probabilities in large sequences. Bioinformatics 22: 614-615.