Phenotypic noise: Effects of post-transcriptional regulatory processes affecting mRNA

Wiley Interdisciplinary Reviews: RNA

Volumn 5, Issue 2, 2014, Pages 197-207

  Arbel Goren, Rinat ^a   Tal, Asaf ^a   Stavans, Joel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; UNTRANSLATED RNA;

ALTERNATIVE RNA SPLICING; CELL INTERACTION; EUKARYOTE; GENE CONTROL; HUMAN; MOLECULAR BIOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROKARYOTE; REGULATORY MECHANISM; REVIEW; RNA INTERFERENCE; RNA PROCESSING; RNA TRANSCRIPTION;

ANIMALS; HUMANS; RNA INTERFERENCE; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA, UNTRANSLATED;

EID: 84893738397     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1209     Document Type: Review

References (89)

1. Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie XS. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 2010, 329:533-538.
2. Maheshri N, O'Shea EK. Living with noisy genes: how cells function reliably with inherent variability in gene expression. Annu Rev Biophys Biomol Struct 2007, 36:413-434.
3. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E, Pilpel Y, Barkai N. Noise in protein expression scales with natural protein abundance. Nat Genet 2006, 38:636-643.
4. Ellis EL, Delbruck M. The growth of bacteriophage. J Gen Physiol 1939, 22:365-384.
5. Eldar A, Elowitz MB. Functional roles for noise in genetic circuits. Nature 2010, 467:167-173.
6. Balazsi G, van Oudenaarden A, Collins JJ. Cellular decision making and biological noise: from microbes to mammals. Cell 2011, 144:910-925.
7. Elowitz MB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
8. Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S. Switches in bacteriophage λ development. Annu Rev Genet 2005, 39:409-429.
9. Zeng L, Skinner SO, Zong C, Sippy J, Feiss M, Golding I. Decision making at a subcellular level determines the outcome of bacteriophage infection. Cell 2010, 141:682-691.
10. Weinberger LS, Burnett JC, Toettcher JE, Arkin AP, Schaffer DV. Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell 2005, 122:169-182.
11. Suel GM, Kulkarni RP, Dworkin J, Garcia-Ojalvo J, Elowitz MB. Tunability and noise dependence in differentiation dynamics. Science 2007, 315:1716-1719.
12. Gregor T, Tank DW, Wieschaus EF, Bialek W. Probing the limits to positional information. Cell 2007, 130:153-164.
13. Zernicka-Goetz M, Morris SA, Bruce AW. Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo. Nat Rev Genet 2009, 10:467-477.
14. Booth IR. Stress and the single cell: intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. Int J Food Microbiol 2002, 78:19-30.
15. Pigliucci M, Murren CJ. Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 2003, 57:1455-1464.
16. Lopez-Maury L, Marguerat S, Bahler J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 2008, 9:583-593.
17. Fraser D, Kaern M. A chance at survival: gene expression noise and phenotypic diversification strategies. Mol Microbiol 2009, 71:1333-1340.
18. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science 2004, 305:1622-1625.
19. Slack MD, Martinez ED, Wu LF, Altschuler SJ. Characterizing heterogeneous cellular responses to perturbations. Proc Natl Acad Sci U S A 2008, 105:19306-19311.
20. Swain PS, Elowitz MB, Siggia ED. Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc Natl Acad Sci U S A 2002, 99:12795-12800.
21. Volfson D, Marciniak J, Blake WJ, Ostroff N, Tsimring LS, Hasty J. Origins of extrinsic variability in eukaryotic gene expression. Nature 2006, 439:861-864.
22. Cai L, Friedman N, Xie XS. Stochastic protein expression in individual cells at the single molecule level. Nature 2006, 440:358-362.
23. Becskei A, Kaufmann BB, van Oudenaarden A. Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat Genet 2005, 37:937-944.
24. Blake WJ, Balazsi G, Kohanski MA, Isaacs FJ, Murphy KF, Kuang Y, Cantor CR, Walt DR, Collins JJ. Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell 2006, 24:853-865.
25. Jacob F, Monod J. Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 1961, 3:318-356.
26. Gottesman S, Storz G. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 2011, 3:a003798.
27. Beisel CL, Storz G. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 2010, 34:866-882.
28. Storz G, Vogel J, Wassarman KM. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 2011, 43:880-891.
29. Desnoyers G, Morissette A, Prevost K, Masse E. Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J 2009, 28:1551-1561.
30. Arbel-Goren R, Tal A, Friedlander T, Meshner S, Costantino N, Court DL, Stavans J. Effects of post-transcriptional regulation on phenotypic noise in Escherichia coli. Nucleic Acids Res 2013, 41:4825-4834.
31. Gogol EB, Rhodius VA, Papenfort K, Vogel J, Gross CA. Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci U S A 2011, 108:12875-12880.
32. Prevost K, Salvail H, Desnoyers G, Jacques JF, Phaneuf E, Masse E. The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol Microbiol 2007, 64:1260-1273.
33. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S. DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci U S A 1998, 95:12462-12467.
34. Hussein R, Lim HN. Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci U S A 2011, 108:1110-1115.
35. Levine E, Zhang Z, Kuhlman T, Hwa T. Quantitative characteristics of gene regulation by small RNA. PLoS Biol 2007, 5:e229.
36. Elf J, Paulsson J, Berg OG, Eherenberg M. Mesoscopic kinetics and its applications in protein synthesis. In: Alberghina L, Westernhoff HV, eds. Topics in Current Genetics: Systems Biology: Definitions and Perspectives. Berlin: Springer-Verlag; 2005, 95-116.
37. Mehta P, Goyal S, Wingreen NS. A quantitative comparison of sRNA-based and protein-based gene regulation. Mol Syst Biol 2008, 4:221.
38. Jost D, Nowojewski A, Levine E. Regulating the many to benefit the few: role of weak small RNA targets. Biophys J 2013, 104:1773-1782.
39. Shimoni Y, Friedlander G, Hetzroni G, Niv G, Altuvia S, Biham O, Margalit H. Regulation of gene expression by small non-coding RNAs: a quantitative view. Mol Syst Biol 2007, 3:138.
40. Beisel CL, Storz G. The base-pairing RNA spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. Mol Cell 2011, 41:286-297.
41. Osella M, Bosia C, Cora D, Caselle M. The role of incoherent microRNA-mediated feedforward loops in noise buffering. PLoS Comput Biol 2011, 7:e1001101.
42. Ghosh B, Karmakar R, Bose I. Noise characteristics of feed forward loops. Phys Biol 2005, 2:36-45.
43. Ghildiyal M, Zamore PD. Small silencing RNAs: an expanding universe. Nat Rev Genet 2009, 10:94-108.
44. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009, 136:642-655.
45. Mangan S, Alon U. Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci U S A 2003, 100:11980-11985.
46. Hutvagner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002, 297:2056-2060.
47. Flynt AS, Lai EC. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet 2008, 9:831-842.
48. Hagen JW, Lai EC. microRNA control of cell-cell signaling during development and disease. Cell Cycle 2008, 7:2327-2332.
49. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009, 10:704-714.
50. Siciliano V, Garzilli I, Fracassi C, Criscuolo S, Ventre S, di Bernardo D. miRNAs confer phenotypic robustness to gene networks by suppressing biological noise. Nat Commun 2013, 4:2364.
51. Hornstein E, Shomron N. Canalization of development by microRNAs. Nat Genet 2006, 38(suppl):S20-S24.
52. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. Animal microRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 2005, 123:1133-1146.
53. Li X, Cassidy JJ, Reinke CA, Fischboeck S, Carthew RW. A microRNA imparts robustness against environmental fluctuation during development. Cell 2009, 137:273-282.
54. Kim DH, Grun D, van Oudenaarden A. Dampening of expression oscillations by synchronous regulation of a microRNA and its target. Nat Genet 2013, 45:1337-1344.
55. Arvey A, Larsson E, Sander C, Leslie CS, Marks DS. Target mRNA abundance dilutes microRNA and siRNA activity. Mol Syst Biol 2010, 6:363.
56. Loinger A, Shemla Y, Simon I, Margalit H, Biham O. Competition between small RNAs: a quantitative view. Biophys J 2012, 102:1712-1721.
57. Waks Z, Klein AM, Silver PA. Cell-to-cell variability of alternative RNA splicing. Mol Syst Biol 2011, 7:506.
58. Kornblihtt AR, Schor IE, Allo M, Dujardin G, Petrillo E, Munoz MJ. Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol 2013, 14:153-165.
59. Irimia M, Blencowe BJ. Alternative splicing: decoding an expansive regulatory layer. Curr Opin Cell Biol 2012, 24:323-332.
60. Hoskins AA, Moore MJ. The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem Sci 2012, 37:179-188.
61. Vargas DY, Shah K, Batish M, Levandoski M, Sinha S, Marras SA, Schedl P, Tyagi S. Single-molecule imaging of transcriptionally coupled and uncoupled splicing. Cell 2011, 147:1054-1065.
62. Cramer P, Pesce CG, Baralle FE, Kornblihtt AR. Functional association between promoter structure and transcript alternative splicing. Proc Natl Acad Sci U S A 1997, 94:11456-11460.
63. Braunschweig U, Gueroussov S, Plocik AM, Graveley BR, Blencowe BJ. Dynamic integration of splicing within gene regulatory pathways. Cell 2013, 152:1252-1269.
64. Schmidt U, Basyuk E, Robert MC, Yoshida M, Villemin JP, Auboeuf D, Aitken S, Bertrand E. Real-time imaging of cotranscriptional splicing reveals a kinetic model that reduces noise: implications for alternative splicing regulation. J Cell Biol 2011, 193:819-829.
65. Bhatt DM, Pandya-Jones A, Tong AJ, Barozzi I, Lissner MM, Natoli G, Black DL, Smale ST. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 2012, 150:279-290.
66. Zraly CB, Dingwall AK. The chromatin remodeling and mRNA splicing functions of the Brahma (SWI/SNF) complex are mediated by the SNR1/SNF5 regulatory subunit. Nucleic Acids Res 2012, 40:5975-5987.
67. Skotheim RI, Nees M. Alternative splicing in cancer: noise, functional, or systematic? Int J Biochem Cell Biol 2007, 39:1432-1449.
68. Melamud E, Moult J. Stochastic noise in splicing machinery. Nucleic Acids Res 2009, 37:4873-4886.
69. Pickrell JK, Pai AA, Gilad Y, Pritchard JK. Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet 2010, 6:e1001236.
70. Gurskaya NG, Staroverov DB, Zhang L, Fradkov AF, Markina NM, Pereverzev AP, Lukyanov KA. Analysis of alternative splicing of cassette exons at single-cell level using two fluorescent proteins. Nucleic Acids Res 2012, 40:e57.
71. Saltzman AL, Kim YK, Pan Q, Fagnani MM, Maquat LE, Blencowe BJ. Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol Cell Biol 2008, 28:4320-4330.
72. Shalek AK, Satija R, Adiconis X, Gertner RS, Gaublomme JT, Raychowdhury R, Schwartz S, Yosef N, Malboeuf C, Lu D, et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 2013, 498:236-240.
73. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476.
74. Shearwin KE, Callen BP, Egan JB. Transcriptional interference-a crash course. Trends Genet 2005, 21:339-345.
75. Schmitt S, Prestel M, Paro R. Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev 2005, 19:697-708.
76. Abarrategui I, Krangel MS. Noncoding transcription controls downstream promoters to regulate T-cell receptor α recombination. EMBO J 2007, 26:4380-4390.
77. Lenasi T, Contreras X, Peterlin BM. Transcriptional interference antagonizes proviral gene expression to promote HIV latency. Cell Host Microbe 2008, 4:123-133.
78. Sneppen K, Dodd IB, Shearwin KE, Palmer AC, Schubert RA, Callen BP, Egan JB. A mathematical model for transcriptional interference by RNA polymerase traffic in Escherichia coli. J Mol Biol 2005, 346:399-409.
79. Golding I, Paulsson J, Zawilski SM, Cox EC. Real-time kinetics of gene activity in individual bacteria. Cell 2005, 123:1025-1036.
80. Mitarai N, Dodd IB, Crooks MT, Sneppen K. The generation of promoter-mediated transcriptional noise in bacteria. PLoS Comput Biol 2008, 4:e1000109.
81. Buetti-Dinh A, Ungricht R, Kelemen JZ, Shetty C, Ratna P, Becskei A. Control and signal processing by transcriptional interference. Mol Syst Biol 2009, 5:300.
82. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 2009, 459:428-432.
83. Brock A, Chang H, Huang S. Non-genetic heterogeneity-a mutation-independent driving force for the somatic evolution of tumours. Nat Rev Genet 2009, 10:336-342.
84. Berenbaum MC. In vivo determination of the fractional kill of human tumor cells by chemotherapeutic agents. Cancer Chemother Rep 1972, 56:563-571.
85. Arraiano CM, Andrade JM, Domingues S, Guinote IB, Malecki M, Matos RG, Moreira RN, Pobre V, Reis FP, Saramago M, et al. The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol Rev 2010, 34:883-923.
86. Elkon R, Ugalde AP, Agami R. Alternative cleavage and polyadenylation: extent, regulation and function. Nat Rev Genet 2013, 14:496-506.
87. Swain PS. Efficient attenuation of stochasticity in gene expression through post-transcriptional control. J Mol Biol 2004, 344:965-976.
88. Blumenthal T. Operons in eukaryotes. Brief Funct Genomic Proteomic 2004, 3:199-211.
89. Yoon JH, Abdelmohsen K, Gorospe M. Posttranscriptional gene regulation by long noncoding RNA. J Mol Biol 2012, 425:3723-3730.