Cell-Cycle Dependence of Transcription Dominates Noise in Gene Expression

PLoS Computational Biology

Volumn 9, Issue 7, 2013, Pages

  Zopf, C J ^a   Quinn, Katie ^a   Zeidman, Joshua ^a   Maheshri, Narendra ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; PROTEINS; STOCHASTIC MODELS; STOCHASTIC SYSTEMS;

CELL CYCLE; DYNAMIC MEASUREMENT; EXPRESSION LEVELS; GENES EXPRESSION; MRNA LEVELS; PROTEIN LEVEL; RANDOM PERIODS; SINGLE CELLS; STATIC MEASUREMENTS; STATICS AND DYNAMICS;

TRANSCRIPTION;

MESSENGER RNA;

ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL DIVISION; CELL GROWTH; CONTROLLED STUDY; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; NONHUMAN; PROMOTER REGION; SACCHAROMYCES CEREVISIAE;

EID: 84880815428     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003161     Document Type: Article

References (69)

1. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S, (2006) Stochastic mRNA synthesis in mammalian cells. PLoS Biology 4: e309 OP.
2. To TL, Maheshri N, (2010) Noise can induce bimodality in positive transcriptional feedback loops without bistability. Science 327: 1142-1145.
3. 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.
4. Raj A, van Oudenaarden A, (2009) Single-molecule approaches to stochastic gene expression. Annu Rev Biophys 38: 255-270.
5. 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.
6. Peccoud J, Ycart B, (1995) Markovian modeling of gene-product synthesis. Theor Popul Biol 48: 222-234.
7. Shahrezaei V, Swain PS, (2008) Analytical distributions for stochastic gene expression. Proc Natl Acad Sci U S A 105: 17256-17261.
8. Golding I, Paulsson J, Zawilski SM, Cox EC, (2005/12/16) Real-time kinetics of gene activity in individual bacteria. Cell 123: 1025-1036.
9. Maiuri P, Knezevich A, De Marco A, Mazza D, Kula A, et al. (2011) Fast transcription rates of RNA polymerase II in human cells. EMBO Rep 12: 1280-1285.
10. Chubb JR, Trcek T, Shenoy SM, Singer RH, (2006/5/23) Transcriptional pulsing of a developmental gene. Current Biology 16: 1018-1025.
11. Muramoto T, Cannon D, Gierlinski M, Corrigan A, Barton GJ, et al. (2012) Live imaging of nascent RNA dynamics reveals distinct types of transcriptional pulse regulation. Proc Natl Acad Sci U S A 109: 7350-7355.
12. Larson DR, Zenklusen D, Wu B, Chao JA, Singer RH, (2011) Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 332: 475-478.
13. Choi PJ, Cai L, Frieda K, Xie XS, (2008) A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 322: 442-446.
14. 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.
15. 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.
16. Tan RZ, van Oudenaarden A, (2010) Transcript counting in single cells reveals dynamics of rDNA transcription. Mol Syst Biol 6: 358.
17. Munsky B, Neuert G, van Oudenaarden A, (2012) Using gene expression noise to understand gene regulation. Science 336: 183-187.
18. Elowitz MB, Levine AJ, Siggia ED, Swain PS, (2002) Stochastic gene expression in a single cell. Science 297: 1183.
19. Raser JM, O'Shea EK, (2004) Control of stochasticity in eukaryotic gene expression. Science 304: 1811-1814.
20. Volfson D, Marciniak J, Blake WJ, Ostroff N, Tsimring LS, et al. (2006) Origins of extrinsic variability in eukaryotic gene expression. Nature 439: 861-864.
21. Pedraza JM, van Oudenaarden A, (2005) Noise propagation in gene networks. Science 307: 1965-1969.
22. Colman-Lerner A, Gordon A, Serra E, Chin T, Resnekov O, et al. (2005) Regulated cell-to-cell variation in a cell-fate decision system. Nature 437: 699-706.
23. Hilfinger A, Paulsson J, (2011) Separating intrinsic from extrinsic fluctuations in dynamic biological systems. Proc Natl Acad Sci U S A 108: 12167-12172.
24. Huh D, Paulsson J, (2011) Non-genetic heterogeneity from stochastic partitioning at cell division. Nat Genet 43: 95-100.
25. Trcek T, Larson DR, Moldon A, Query CC, Singer RH, (2011) Single-molecule mRNA decay measurements reveal promoter- regulated mRNA stability in yeast. Cell 147: 1484-1497.
26. Gordon A, Colman-Lerner A, Chin TE, Benjamin KR, Yu RC, et al. (2007) Single-cell quantification of molecules and rates using open-source microscope-based cytometry. Nat Methods 4: 175-181.
27. Cookson NA, Cookson SW, Tsimring LS, Hasty J, (2010) Cell cycle-dependent variations in protein concentration. Nucleic Acids Res 38: 2676-2681.
28. Goranov AI, Cook MF, Ricicova MF, Ben-Ari GF, Gonzalez CF, et al. (2009) The rate of cell growth is governed by cell cycle stage. Genes Dev 23: 1408-1422.
29. Boehlke KW, Friesen JD, (1975) Cellular content of ribonucleic acid and protein in saccharomyces cerevisiae as a function of exponential growth rate: Calculation of the apparent peptide chain elongation rate. J Bacteriol 121: 429-433.
30. Larson DR, Singer RH, Zenklusen D, (2009) A single molecule view of gene expression. Trends Cell Biol 19: 630-637.
31. 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.
32. Paulsson J, Berg OG, Ehrenberg M, (2000) Stochastic focusing: Fluctuation-enhanced sensitivity of intracellular regulation. Proceedings of the National Academy of Sciences of the United States of America 97: 7148-7153.
33. Charvin G, Cross FR, Siggia ED, (2008) A microfluidic device for temporally controlled gene expression and long-term fluorescent imaging in unperturbed dividing yeast cells. PLoS One 3: e1468.
34. O'Neill EM, Kaffman A, Jolly ER, O'Shea EK, (1996) Regulation of PHO4 nuclear localization by the PHO80-PHO85 cyclin-CDK complex. Science 271: 209-212.
35. 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.
36. Gari E, Piedrafita L, Aldea M, Herrero E, (1997) A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in saccharomyces cerevisiae. Yeast 13: 837-848.
37. Granovskaia MV, Jensen LJ, Ritchie ME, Toedling J, Ning Y, et al. (2010) High-resolution transcription atlas of the mitotic cell cycle in budding yeast. Genome Biol 11: R24-2010-11-3-r24.
38. Bean JM, Siggia ED, Cross FR, (2006) Coherence and timing of cell cycle start examined at single-cell resolution. Mol Cell 21: 3-14.
39. Di Talia S, Skotheim JM, Bean JM, Siggia ED, Cross FR, (2007) The effects of molecular noise and size control on variability in the budding yeast cell cycle. Nature 448: 947-951.
40. Zhurinsky J, Leonhard K, Watt S, Marguerat S, Bahler J, et al. (2010) A coordinated global control over cellular transcription. Curr Biol 20: 2010-2015.
41. Wyart M, Botstein D, Wingreen NS, (2010) Evaluating gene expression dynamics using pairwise RNA FISH data. PLoS Comput Biol 6: e1000979.
42. Silverman SJ, Petti AA, Slavov N, Parsons L, Briehof R, et al. (2010) Metabolic cycling in single yeast cells from unsynchronized steady-state populations limited on glucose or phosphate. Proc Natl Acad Sci U S A 107: 6946-6951.
43. Muramoto T, Müller I, Thomas G, Melvin A, Chubb JR, (2010) Methylation of H3K4 is required for inheritance of active transcriptional states. Current Biology 20: 397-406.
44. Weijer CJ, Duschl G, David CN, (1984) A revision of the dictyostelium discoideum cell cycle. J Cell Sci 70: 111-131.
45. Weeks G, Weijer CJ, (1994) The dictyostelium cell cycle and its relationship to differentiation. FEMS Microbiol Lett 124: 123-130.
46. Dynlacht BD, (1997) Regulation of transcription by proteins that control the cell cycle. Nature 389: 149-152.
47. Wolffe AP, (1991) Implications of DNA replication for eukaryotic gene expression. J Cell Sci 99: 201-206.
48. Crowe AJ, Piechan JL, Sang L, Barton MC, (2000) S-phase progression mediates activation of a silenced gene in synthetic nuclei. Mol Cell Biol 20: 4169-4180.
49. Fisher D, Mechali M, (2003) Vertebrate HoxB gene expression requires DNA replication. EMBO J 22: 3737-3748.
50. Kirchmaier AL, Rine J, (2001) DNA replication-independent silencing in S. cerevisiae. Science 291: 646-650.
51. Li YC, Cheng TH, Gartenberg MR, (2001) Establishment of transcriptional silencing in the absence of DNA replication. Science 291: 650-653.
52. Wilson AC, Patient RK, (1993) DNA replication facilitates the action of transcriptional enhancers in transient expression assays. Nucleic Acids Res 21: 4296-4304.
53. Williams RD, Lee BA, Jackson SP, Proudfoot NJ, (1996) Activation domains of transcription factors mediate replication dependent transcription from a minimal HIV-1 promoter. Nucleic Acids Res 24: 549-557.
54. Kamakaka RT, Bulger M, Kadonaga JT, (1993) Potentiation of RNA polymerase II transcription by Gal4-VP16 during but not after DNA replication and chromatin assembly. Genes Dev 7: 1779-1795.
55. Chymkowitch P, Eldholm V, Lorenz S, Zimmermann C, Lindvall JM, et al. (2012) Cdc28 kinase activity regulates the basal transcription machinery at a subset of genes. Proc Natl Acad Sci U S A 109: 10450-10455.
56. Annunziato AT, (2012) Assembling chromatin: The long and winding road. Biochim Biophys Acta 1819: 196-210.
57. Shilatifard A, (2006) Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269.
58. Gottesfeld JM, Forbes DJ, (1997) Mitotic repression of the transcriptional machinery. Trends Biochem Sci 22: 197-202.
59. Elliott SG, McLaughlin CS, (1978) Rate of macromolecular synthesis through the cell cycle of the yeast saccharomyces cerevisiae. Proc Natl Acad Sci U S A 75: 4384-4388.
60. Clemente-Blanco A, Mayan-Santos M, Schneider DA, Machin F, Jarmuz A, et al. (2009) Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature 458: 219-222.
61. Rosenfeld N, Young JW, Alon U, Swain PS, Elowitz MB, (2005) Gene regulation at the single-cell level. Science 307: 1962-1965.
62. Shahrezaei V, Ollivier JF, Swain PS, (2008) Colored extrinsic fluctuations and stochastic gene expression. Mol Syst Biol 4: 196.
63. Thomas BJ, Rothstein R, (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56: 619-630.
64. Guthrie C, Fink GR. (2004) Guide to yeast genetics and molecular and cell biology. part A. Amsterdam: Elsevier Academic Press.
65. Rizzo MA, Springer GH, Granada B, Piston DW, (2004) An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22: 445-449.
66. Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, et al. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20: 87-90.
67. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
68. Zopf CJ, Maheshri N, (2013) Acquiring fluorescence time-lapse movies of budding yeast and analyzing single-cell dynamics using GRAFTS. J Vis Exp pp. e50456.
69. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S, (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877-879.