Slow-growing cells within isogenic populations have increased RNA polymerase error rates and DNA damage

Nature Communications

Volumn 6, Issue , 2015, Pages

  Van Dijk, David ^a,b   Dhar, Riddhiman ^c,d   Missarova, Alsu M ^d   Espinar, Lorena ^d   Blevins, William R ^d   Lehner, Ben ^c,d,e   Carey, Lucas B ^d  

^a Department of Biological Sciences Columbia University ^*  (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d UNIVERSITAT POMPEU FABRA   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE; FUNGAL PROTEIN; FUNGAL RNA;

ANTIBIOTICS; CELLS AND CELL COMPONENTS; CHROMOSOME; DNA; ENDOGENOUS GROWTH; ENZYME; PHENOTYPE; RNA; SUBPOPULATION;

ANTIBIOTIC SENSITIVITY; ARTICLE; CELL CULTURE; CELL GROWTH; CHEMOTHERAPY; DNA DAMAGE; ENVIRONMENT; GENE EXPRESSION; GENETIC VARIABILITY; GROWTH RATE; ISOGENIC CELL; NONHUMAN; OXIDATIVE STRESS; POPULATION GROWTH; SINGLE CELL ANALYSIS; SLOW GROWING CELL; TRANSPOSON; UPREGULATION; YEAST; CELL PROLIFERATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROCEDURES;

CELL PROLIFERATION; DNA DAMAGE; DNA-DIRECTED RNA POLYMERASES; FLOW CYTOMETRY; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; RNA, FUNGAL; YEASTS;

EID: 84939168337     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8972     Document Type: Article

References (53)

1. Orr, H. A. Fitness and its role in evolutionary genetics. Nat. Rev. Genet. 10, 531-539 (2009).
2. Kiviet, D. J. et al. Stochasticity of metabolism and growth at the single-cell level. Nature 514, 376-379 (2014).
3. Wakamoto, Y. et al. Dynamic persistence of antibiotic-stressed mycobacteria. Science 339, 91-95 (2013).
4. Balaban, N. Q., Gerdes, K., Lewis, K. & McKinney, J. D. A problem of persistence: still more questions than answers? Nat. Rev. Microbiol. 11, 587-591 (2013).
5. Fridman, O., Goldberg, A., Ronin, I., Shoresh, N. & Balaban, N. Q. Optimization of lag time underlies antibiotic tolerance in evolved bacterial populations. Nature 513, 418-421 (2014).
6. Gupta, P. B. et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146, 633-644 (2011).
7. Brown, R., Curry, E., Magnani, L., Wilhelm-Benartzi, C. S. & Borley, J. Poised epigenetic states and acquired drug resistance in cancer. Nat. Rev. Cancer 14, 747-753 (2014).
8. Marusyk, A., Almendro, V. & Polyak, K. Intra-tumour heterogeneity: a looking glass for cancer? Nat. Rev. Cancer 12, 323-334 (2012).
9. Brauer, M. J. et al. Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast. Mol. Biol. Cell 19, 352-367 (2008).
10. Kemmeren, P. et al. Large-scale genetic perturbations reveal regulatory networks and an abundance of gene-specific repressors. Cell 157, 740-752.
11. O'Duibhir, E. et al. Cell cycle population effects in perturbation studies. Mol. Syst. Biol. 10, 732-732 (2014).
12. Ihssen, J. & Egli, T. Global physiological analysis of carbon-and energy-limited growing Escherichia coli confirms a high degree of catabolic flexibility and preparedness for mixed substrate utilization. Environ. Microbiol. 7, 1568-1581 (2005).
13. Ihssen, J. & Egli, T. Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology 150, 1637-1648 (2004).
14. Lubeck, E. & Cai, L. Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nat. Methods 9, 743-748 (2012).
15. Elowitz, M. B., Levine, A. J., Siggia, E. D. & Swain, P. S. Stochastic gene expression in a single cell. Science 297, 1183-1186 (2002).
16. Levy, S. F., Ziv, N. & Siegal, M. L. Bet hedging in yeast by heterogeneous, agecorrelated expression of a stress protectant. PLoS Biol. 10, e1001325-e1001325 (2012).
17. Ziv, N., Siegal, M. L. & Gresham, D. Genetic and non-genetic determinants of cell-growth variation assessed by high-throughput microscopy. Mol. Biol. Evol. 30, 2568-2578 (2013).
18. Cabib, E. & Arroyo, J. How carbohydrates sculpt cells: chemical control of morphogenesis in the yeast cell wall. Nat. Rev. Microbiol. 11, 648-655 (2013).
19. Neymotin, B., Athanasiadou, R. & Gresham, D. Determination of in vivo RNA kinetics using RATE-seq. RNA 20, 1645-1652 (2014).
20. Hillenmeyer, M. E. et al. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320, 362-365 (2008).
21. Roberts, G. G. & Hudson, A. P. Transcriptome profiling of Saccharomyces cerevisiae during a transition from fermentative to glycerol-based respiratory growth reveals extensive metabolic and structural remodeling. Mol. Genet. Genomics 276, 170-186 (2006).
22. Ebina, H. & Levin, H. L. Stress management: how cells take control of their transposons. Mol. Cell 27, 180-181 (2007).
23. Feng, G., Leem, Y. E. & Levin, H. L. Transposon integration enhances expression of stress response genes. Nucleic Acids Res. 41, 775-789 (2012).
24. Galhardo, R. S., Hastings, P. J. & Rosenberg, S. M. Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 42, 399-435 (2007).
25. Hastings, P. J., Slack, A., Petrosino, J. F. & Rosenberg, S. M. Adaptive amplification and point mutation are independent mechanisms: evidence for various stress-inducible mutation mechanisms. PLoS Biol. 2, e399-e399 (2004).
26. Gasch, A. P. et al. Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol. Biol. Cell 12, 2987-3003 (2001).
27. Fikus, M. U. et al. The product of the DNA damage-inducible gene of Saccharomyces cerevisiae, DIN7, specifically functions in mitochondria. Genetics 154, 73-81 (2000).
28. Lisby, M., Mortensen, U. H. & Rothstein, R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5, 572-577 (2003).
29. Cooke, M. S., Evans, M. D., Dizdaroglu, M. & Lunec, J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 17, 1195-1214 (2003).
30. McClintock, B. The significance of responses of the genome to challenge. Science 226, 792-801 (1984).
31. Gordon, A. J. E., Satory, D., Halliday, J. A. & Herman, C. Heritable change caused by transient transcription errors. PLoS Genet. 9, e1003595-e1003595 (2013).
32. Baker, L. A. et al. The yeast Snt2 protein coordinates the transcriptional response to hydrogen peroxide-mediated oxidative stress. Mol. Cell. Biol. 33, 3735-3748 (2013).
33. Nookaew, I. et al. A comprehensive comparison of RNA-Seq-based transcriptome analysis from reads to differential gene expression and crosscomparison with microarrays: a case study in Saccharomyces cerevisiae. Nucleic Acids Res. 40, 10084-10097 (2012).
34. Schieber, M. & Chandel, N. S. TOR signaling couples oxygen sensing to lifespan in C. elegans. Cell Rep. 9, 9-15 (2014).
35. Lang, G. I. & Murray, A. W. Estimating the per-base-pair mutation rate in the yeast Saccharomyces cerevisiae. Genetics 178, 67-82 (2008).
36. Nesser, N. K., Peterson, D. O. & Hawley, D. K. RNA polymerase II subunit Rpb9 is important for transcriptional fidelity in vivo. Proc. Natl Acad. Sci. USA 103, 3268-3273 (2006).
37. Gout, J.-F., Thomas, W. K., Smith, Z., Okamoto, K. & Lynch, M. Large-scale detection of in vivo transcription errors. Proc. Natl Acad. Sci. USA 110, 18584-18589 (2013).
38. Koonin, E. V. & Wolf, Y. I. Evolution of microbes and viruses: a paradigm shift in evolutionary biology? Front. Cell. Infect. Microbiol. 2, 119-119 (2012).
39. Kushnir, A. S., Davido, D. J. & Schaffer, P. A. Role of nuclear factor Y in stress-induced activation of the herpes simplex virus type 1 ICP0 promoter. J. Virol. 84, 188-200 (2010).
40. Volcy, K. & Fraser, N. W. DNA damage promotes herpes simplex virus-1 protein expression in a neuroblastoma cell line. J. Neurovirol. 19, 57-64 (2013).
41. Pelet, S. et al. Transient activation of the HOG MAPK pathway regulates bimodal gene expression. Science 332, 732-735 (2011).
42. Alvaro, D., Lisby, M. & Rothstein, R. Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet. 3, e228 (2007).
43. Shor, E., Fox, C. A. & Broach, J. R. The yeast environmental stress response regulates mutagenesis induced by proteotoxic stress. PLoS Genet. 9, e1003680 (2013).
44. Roth, J. R., Kugelberg, E., Reams, A. B., Kofoid, E. & Andersson, D. I. Origin of mutations under selection: the adaptive mutation controversy. Annu. Rev. Microbiol. 60, 477-501 (2006).
45. Weiss, E. L. Mitotic exit and separation of mother and daughter cells. Genetics 192, 1165-1202 (2012).
46. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7, 562-578 (2012).
47. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
48. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
49. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
50. Eden, E., Navon, R., Steinfeld, I., Lipson, D. & Yakhini, Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10, 48 (2009).
51. Pogliano, J., Pogliano, K., Weiss, D. S., Losick, R. & Beckwith, J. Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. Proc. Natl Acad. Sci. USA 94, 559-564 (1997).
52. Elowitz, M. B., Surette, M. G., Wolf, P. E., Stock, J. & Leibler, S. Photoactivation turns green fluorescent protein red. Curr. Biol. 7, 809-812 (1997).
53. Wapinski, I., Pfeffer, A., Friedman, N. & Regev, A. Natural history and evolutionary principles of gene duplication in fungi. Nature 449, 54-61 (2007).