Single-cell analysis of transcription kinetics across the cell cycle

eLife

Volumn 5, Issue JANUARY2016, 2016, Pages

  Skinner, Samuel O ^a,b,c   Xu, Heng ^a,b,c   Nagarkar Jaiswal, Sonal ^a   Freire, Pablo R ^a   Zwaka, Thomas P ^a,d   Golding, Ido ^a,b,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b RICE UNIVERSITY   (United States)

^c University of Illinois at Urbana Champaign   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MESSENGER RNA; NANOG PROTEIN, MOUSE; OCTAMER TRANSCRIPTION FACTOR 4; POU5F1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR NANOG;

ARTICLE; CELL CULTURE; CELL CYCLE PROGRESSION; CELL FUNCTION; CELL PERMEABILIZATION; CELL PROLIFERATION ASSAY; CELL SEGMENTATION; CONTROLLED STUDY; COPY NUMBER VARIATION; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENCE MICROSCOPY; GENE ACTIVITY; GENE EXPRESSION; GENE REPLICATION; HUMAN; HUMAN CELL; QUANTITATIVE ANALYSIS; SINGLE CELL ANALYSIS; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; CELL CYCLE; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; MOUSE;

ANIMALS; CELL CYCLE; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; MICE; NANOG HOMEOBOX PROTEIN; OCTAMER TRANSCRIPTION FACTOR-3; RNA, MESSENGER; SINGLE-CELL ANALYSIS; TRANSCRIPTION, GENETIC;

EID: 84961285137     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12175.001     Document Type: Article

References (65)

1. Abranches E, Bekman E, Henrique D. 2013. Generation and characterization of a novel mouse embryonic stem cell line with a dynamic reporter of nanog expression. PLoS ONE 8:e59928. doi: 10.1371/journal.pone.0059928
2. Abranches E, Guedes AMV, Moravec M, Maamar H, Svoboda P, Raj A, Henrique D. 2014. Stochastic NANOG fluctuations allow mouse embryonic stem cells to explore pluripotency. Development 141:2770-2779. doi: 10.1242/dev.108910
3. Bahar Halpern K, Caspi I, Lemze D, Levy M, Landen S, Elinav E, Ulitsky I, Itzkovitz S. 2015a. Nuclear retention of mRNA in mammalian tissues. Cell Reports 13:2653-2662. doi: 10.1016/j.celrep.2015.11.036
4. Bahar Halpern K, Tanami S, Landen S, Chapal M, Szlak L, Hutzler A, Nizhberg A, Itzkovitz S. 2015b. Bursty gene expression in the intact mammalian liver. Molecular Cell 58:147-156. doi: 10.1016/j.molcel.2015.01.027
5. Battich N, Stoeger T, Pelkmans L. 2015. Control of transcript variability in single mammalian cells. Cell 163:1596-­1610. doi: 10.1016/j.cell.2015.11.018
6. Cahan P, Daley GQ. 2013. Origins and implications of pluripotent stem cell variability and heterogeneity. Nature Reviews Molecular Cell Biology 14:357-368. doi: 10.1038/nrm3584
7. Cartwright P, McLean C, Sheppard A, Rivett D, Jones K, Dalton S. 2005. LIF/STAT3 controls ES cell self-renewal and pluripotency by a myc-dependent mechanism. Development 132:885-896. doi: 10.1242/dev.01670
8. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. 2003. Functional expression cloning of nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643-655. doi: 10.1016/S0092-8674(03)00392-1
9. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A. 2007. Nanog safeguards pluripotency and mediates germline development. Nature 450:1230-1234. doi: 10.1038/nature06403
10. Chen H, Shiroguchi K, Ge H, Xie XS. 2015. Genome-wide study of mRNA degradation and transcript elongation in escherichia coli. Molecular Systems Biology 11:781. doi: 10.15252/msb.20145794
11. Coulon A, Ferguson ML, de Turris V, Palangat M, Chow CC, Larson DR. 2014. Kinetic competition during the transcription cycle results in stochastic RNA processing. eLife 3. doi: 10.7554/eLife.03939
12. Elowitz MB, Levine AJ, Siggia ED, Swain PS. 2002. Stochastic gene expression in a single cell. Science 297:1183-­1186. doi: 10.1126/science.1070919
13. Faddah DA, Wang H, Cheng AW, Katz Y, Buganim Y, Jaenisch R. 2013. Single-cell analysis reveals that expression of nanog is biallelic and equally variable as that of other pluripotency factors in mouse ESCs. Cell Stem Cell 13:23-29. doi: 10.1016/j.stem.2013.04.019
14. Femino AM, Fay FS, Fogarty K, Singer RH. 1998. Visualization of single RNA transcripts in situ. Science 280:585-­590. doi: 10.1126/science.280.5363.585
15. Filipczyk A, Gkatzis K, Fu J, Hoppe PS, Lickert H, Anastassiadis K, Schroeder T. 2013. Biallelic expression of nanog protein in mouse embryonic stem cells. Cell Stem Cell 13:12-13. doi: 10.1016/j.stem.2013.04.025
16. FitzPatrick DR, Ramsay J, McGill NI, Shade M, Carothers AD, Hastie ND. 2002. Transcriptome analysis of human autosomal trisomy. Human Molecular Genetics 11:3249-3256. doi: 10.1093/hmg/11.26.3249
17. Friedman N, Cai L, Xie XS. 2006. Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Physical Review Letters 97. doi: 10.1103/PhysRevLett.97.168302
18. Gillespie DT. 1977. Exact stochastic simulation of coupled chemical reactions. The Journal of Physical Chemistry 81:2340-2361. doi: 10.1021/j100540a008
19. Golding I, Paulsson J, Zawilski SM, Cox EC. 2005. Real-time kinetics of gene activity in individual bacteria. Cell 123:1025-1036. doi: 10.1016/j.cell.2005.09.031
20. Gonzales KAU, Liang H, Lim Y-S, Chan Y-S, Yeo J-C, Tan C-P, Gao B, Le B, Tan Z-Y, Low K-Y, Liou Y-C, Bard F, Ng H-H. 2015. Deterministic restriction on pluripotent state dissolution by cell-cycle pathways. Cell 162:564-­579. doi: 10.1016/j.cell.2015.07.001
21. GrUn D, Kester L, van Oudenaarden A. 2014. Validation of noise models for single-cell transcriptomics. Nature Methods 11:637-640. doi: 10.1038/nmeth.2930
22. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, Dudko O, Malley J, Eastman PS, Oliver B. 2006. Global analysis of x-chromosome dosage compensation. Journal of Biology 5:3. doi: 10.1186/jbiol30
23. Hansen CH, van Oudenaarden A. 2013. Allele-specific detection of single mRNA molecules in situ. Nature Methods 10:869-871. doi: 10.1038/nmeth.2601
24. Heard E, Clerc P, Avner P. 1997. X chromosome inactivation in mammals. Annual Review of Genetics 31:571-­610. doi: 10.1146/annurev.genet.31.1.571
25. Hoyle NP, Ish-Horowicz D. 2013. Transcript processing and export kinetics are rate-limiting steps in expressing vertebrate segmentation clock genes. Proceedings of the National Academy of Sciences of the United States of America 110:E4316-E4324. doi: 10.1073/pnas.1308811110
26. Huh D, Paulsson J. 2011. Non-genetic heterogeneity from stochastic partitioning at cell division. Nature Genetics 43:95-100. doi: 10.1038/ng.729
27. Johnston DA, Allen White R, Barlogie B. 1978. Automatic processing and interpretation of DNA distributions: comparison of several techniques. Computers and Biomedical Research 11:393-404. doi: 10.1016/0010-4809(78)90020-4
28. Jones DL, Brewster RC, Phillips R. 2014. Promoter architecture dictates cell-to-cell variability in gene expression. Science 346:1533-1536. doi: 10.1126/science.1255301
29. Kafri R, Levy J, Ginzberg MB, Oh S, Lahav G, Kirschner MW. 2013. Dynamics extracted from fixed cells reveal feedback linking cell growth to cell cycle. Nature 494:480-483. doi: 10.1038/nature11897
30. Kalmar T, Lim C, Hayward P, Mufñoz-Descalzo S, Nichols J, Garcia-Ojalvo J, Martinez Arias A. 2009. Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biology 7:e1000149. doi: 10.1371/journal.pbio.1000149
31. Levesque MJ, Ginart P, Wei Y, Raj A. 2013. Visualizing SNVs to quantify allele-specific expression in single cells. Nature Methods 10:865-867. doi: 10.1038/nmeth.2589
32. Martin RM, Rino J, Carvalho C, Kirchhausen T, Carmo-Fonseca M. 2013. Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity. Cell Reports 4:1144-1155. doi: 10.1016/j.celrep.2013.08.013
33. Muüoz Descalzo S, Rue P, Faunes F, Hayward P, Jakt LM, Balayo T, Garcia-Ojalvo J, Martinez Arias A. 2013. A competitive protein interaction network buffers Oct4-mediated differentiation to promote pluripotency in embryonic stem cells. Molecular Systems Biology 9. doi: 10.1038/msb.2013.49
34. Munsky B, Khammash M. 2006. The finite state projection algorithm for the solution of the chemical master equation. The Journal of Chemical Physics 124:044104. doi: 10.1063/1.2145882
35. Neuert G, Munsky B, Tan RZ, Teytelman L, Khammash M, van Oudenaarden A. 2013. Systematic identification of signal-activated stochastic gene regulation. Science 339:584-587. doi: 10.1126/science.1231456
36. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199 doi: 10.1016/0378-1119(91)90434-D.
37. Niwa H, Smith AG, Miyazaki Jun-ichi. 2000. Quantitative expression of oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 24:372-376. doi: 10.1038/74199
38. Ochiai H, Sugawara T, Sakuma T, Yamamoto T. 2014. Stochastic promoter activation affects nanog expression variability in mouse embryonic stem cells. Scientific Reports 4:7125. doi: 10.1038/srep07125
39. Padovan-Merhar O, Nair GP, Biaesch AG, Mayer A, Scarfone S, Foley SW, Wu AR, Churchman LS, Singh A, Raj A. 2015. Single mammalian cells compensate for differences in cellular volume and DNA copy number through independent global transcriptional mechanisms. Molecular Cell 58:339-352. doi: 10.1016/j.molcel.2015.03.005
40. Pauklin S, Vallier L. 2013. The cell-cycle state of stem cells determines cell fate propensity. Cell 155:135-147. doi: 10.1016/j.cell.2013.08.031
41. Pesce M, Wang X, Wolgemuth DJ, Scholer HR. 1998. Differential expression of the oct-4 transcription factor during mouse germ cell differentiation. Mechanisms of Development 71:89-98. doi: 10.1016/S0925-4773(98)00002-1
42. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S. 2006. Stochastic mRNA synthesis in mammalian cells. PLoS Biology 4:e309. doi: 10.1371/journal.pbio.0040309
43. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S. 2008. Imaging individual mRNA molecules using multiple singly labeled probes. Nature Methods 5:877-879. doi: 10.1038/nmeth.1253
44. Raj A, van Oudenaarden A. 2008. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135:216-226. doi: 10.1016/j.cell.2008.09.050
45. Raser JM, O'Shea EK. 2005. Noise in gene expression: origins, consequences, and control. Science 309:2010­-2013. doi: 10.1126/science.1105891
46. Rosenfeld N, Young JW, Alon U, Swain PS, Elowitz MB. 2005. Gene regulation at the single-cell level. Science 307:1962-1965. doi: 10.1126/science.1106914
47. Sanchez A, Choubey S, Kondev J. 2013. Regulation of noise in gene expression. Annual Review of Biophysics 42: 469-491. doi: 10.1146/annurev-biophys-083012-130401
48. Sanchez A, Golding I. 2013. Genetic determinants and cellular constraints in noisy gene expression. Science 342: 1188-1193. doi: 10.1126/science.1242975
49. Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. 2011. Global quantification of mammalian gene expression control. Nature 473:337-342. doi: 10.1038/nature10098
50. Senecal A, Munsky B, Proux F, Ly N, Braye FE, Zimmer C, Mueller F, Darzacq X. 2014. Transcription factors modulate c-fos transcriptional bursts. Cell Reports 8:75-83. doi: 10.1016/j.celrep.2014.05.053
51. Shahrezaei V, Swain PS. 2008. Analytical distributions for stochastic gene expression. Proceedings of the National Academy of Sciences of the United States of America 105:17256-17261. doi: 10.1073/pnas.0803850105
52. Sharova LV, Sharov AA, Nedorezov T, Piao Y, Shaik N, Ko MSH. 2009. Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Research 16:45-58. doi: 10.1093/dnares/dsn030
53. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, Barrandon O, Wray J, Yamanaka S, Chambers I, Smith A. 2009. Nanog is the gateway to the pluripotent ground state. Cell 138:722-737. doi: 10.1016/j.cell.2009.07.039
54. Singer ZS, Yong J, Tischler J, Hackett JA, Altinok A, Surani MA, Cai L, Elowitz MB. 2014. Dynamic heterogeneity and DNA methylation in embryonic stem cells. Molecular Cell 55:319-331. doi: 10.1016/j.molcel.2014.06.029
55. Singh AM, Chappell J, Trost R, Lin L, Wang T, Tang J, Matlock BK, Weller KP, Wu H, Zhao S, Jin P, Dalton S. 2013. Cell-cycle control of developmentally regulated transcription factors accounts for heterogeneity in human pluripotent cells. Stem Cell Reports 1:532-544. doi: 10.1016/j.stemcr.2013.10.009
56. Skinner SO, Sepulveda LA, Xu H, Golding I. 2013. Measuring mRNA copy number in individual escherichia coli cells using single-molecule fluorescent in situ hybridization. Nature Protocols 8:1100-1113. doi: 10.1038/nprot.2013.066
57. So Lok-hang, Ghosh A, Zong C, Sepulveda LA, Segev R, Golding I. 2011. General properties of transcriptional time series in escherichia coli. Nature Genetics 43:554-560. doi: 10.1038/ng.821
58. Thattai M, van Oudenaarden A. 2001. Intrinsic noise in gene regulatory networks. Proceedings of the National Academy of Sciences of the United States of America 98:8614-8619. doi: 10.1073/pnas.151588598
59. Torres-Padilla M-E, Chambers I. 2014. Transcription factor heterogeneity in pluripotent stem cells: a stochastic advantage. Development 141:2173-2181. doi: 10.1242/dev.102624
60. Vargas DY, Shah K, Batish M, Levandoski M, Sinha S, Marras SAE, Schedl P, Tyagi S. 2011. Single-molecule imaging of transcriptionally coupled and uncoupled splicing. Cell 147:1054-1065. doi: 10.1016/j.cell.2011.10.024
61. Vintersten K, Monetti C, Gertsenstein M, Zhang P, Laszlo L, Biechele S, Nagy A. 2004. Mouse in red: red fluorescent protein expression in mouse ES cells, embryos, and adult animals. Genesis 40:241-246. doi: 10.1002/gene.20095
62. Xu H, Sepulveda LA, Figard L, Sokac AM, Golding I. 2015. Combining protein and mRNA quantification to decipher transcriptional regulation. Nature Methods 12:739-742. doi: 10.1038/nmeth.3446
63. Young RA. 2011. Control of the embryonic stem cell state. Cell 144:940-954. doi: 10.1016/j.cell.2011.01.032 Zenklusen D, Larson DR, Singer RH. 2008. Single-RNA counting reveals alternative modes of gene expression in yeast. Nature Structural & Molecular Biology 15:1263-1271. doi: 10.1038/nsmb.1514
64. Zong C, So Lok-hang, Sepulveda LA, Skinner SO, Golding I. 2010. Lysogen stability is determined by the frequency of activity bursts from the fate-determining gene. Molecular Systems Biology 6. doi: 10.1038/msb.2010.96
65. Zopf CJ, Quinn K, Zeidman J, Maheshri N. 2013. Cell-cycle dependence of transcription dominates noise in gene expression. PLoS Computational Biology 9:e1003161. doi: 10.1371/journal.pcbi.1003161