Cell-to-cell diversity in protein levels of a gene driven by a tetracycline inducible promoter

BMC Molecular Biology

Volumn 12, Issue , 2011, Pages

  Smolander, Olli Pekka ^a   Kandhavelu, Meenakshisundaram ^a   Mannerström, Henrik ^a   Lihavainen, Eero ^a   Kalaichelvan, Shanmugapriya ^a   Healy, Shannon ^a,b   Yli Harja, Olli ^a,c   Karp, Matti ^a,d   Ribeiro, Andre S ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b UNIVERSITY OF MANITOBA   (Canada)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^d Biosensors Competence Centre   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANHYDROTETRACYCLINE; GREEN FLUORESCENT PROTEIN; RNA; ANTIINFECTIVE AGENT; TETRACYCLINE;

ARTICLE; BINDING SITE; CELL POPULATION; CELL STRUCTURE; CELL TO CELL DIVERSITY; COMPLEX FORMATION; GENE; GENETIC CODE; GENOME; NONHUMAN; PHENOTYPIC VARIATION; POISSON DISTRIBUTION; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA TRANSCRIPTION; DRUG EFFECT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS;

ESCHERICHIA COLI;

ANTI-BACTERIAL AGENTS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GREEN FLUORESCENT PROTEINS; PROMOTER REGIONS, GENETIC; TETRACYCLINE;

EID: 79955810592     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-12-21     Document Type: Article

References (45)

1. Neubauerz Z, Calef E. Immunity phase-shift in defective lysogens: non-mutational hereditary change of early regulation of lambda prophage. Journal of Molecular Biology 1970, 51:1-13. 10.1016/0022-2836(70)90265-2, 4921249.
2. Arkin A, Ross J, McAdams HM. Stochastic kinetic analysis of developmental pathway bifurcation in phage λ-infected Escherichia coli cells. Genetics 1998, 149:1633-1648. 1460268, 9691025.
3. Acar M, Mettetal J, van Oudenaarden. A stochastic switching as a survival strategy in fluctuating environments. Nature Genetics 2008, 40:471-475. 10.1038/ng.110, 18362885.
4. Lee HH, Molla MN, Cantor CR, Collins JJ. Bacterial charity work leads to population-wide resistance. Nature 2010, 467:82-86. 10.1038/nature09354, 2936489, 20811456.
5. von Hippel P, Bear D, Morgan W, McSwiggen J. Protein-nucleic acid interactions in transcription: A molecular analysis. Annual Review of Biochemistry 1984, 53:389. 10.1146/annurev.bi.53.070184.002133, 6206781.
6. McClure WR. Rate-limiting steps in RNA chain initiation. PNAS 1980, 77:5634-5638. 10.1073/pnas.77.10.5634, 350123, 6160577.
7. Yu J, Xiao J, Ren X, Lao K, Xie S. Probing gene expression in live cells, one protein molecule at a time. Science 2006, 311:1600-1603. 10.1126/science.1119623, 16543458.
8. Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie S. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 2001, 329:533-538.
9. Kaern M, Elston TR, Blake WJ, Collins JJ. Stochasticity in gene expression. Nature Reviews Genetics 2005, 6:451-464. 10.1038/nrg1615, 15883588.
10. Hillen W, Berens C. Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Annual Review of Microbiology 1994, 48:345-369. 10.1146/annurev.mi.48.100194.002021, 7826010.
11. McClure WR. Mechanism and control of transcription initiation in prokaryotes. Annual Review of Biochemistry 1985, 54:171-120. 10.1146/annurev.bi.54.070185.001131, 3896120.
12. Lutz R, Bujard H. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Research 1997, 25:1203-1210. 10.1093/nar/25.6.1203, 146584, 9092630.
13. Ashcroft M, Kubbutat M, Vousden K. Regulation of p53 Function and Stability by Phosphorylation. Molecular Cell Biology 1999, 19:1751-1758.
14. Dai X, Healy S, Yli-Harja O, Ribeiro AS. Tuning cell differentiation patterns and single cell dynamics by regulating proteins' functionalities in a Toggle Switch. Journal of Theoretical Biology 2009, 261(3):441-448. 10.1016/j.jtbi.2009.08.024, 19712686.
15. Buc H, McClure WR. Kinetics of open complex formation between Escherichia coli RNA polymerase and the lac UV5 promoter. Evidence for a sequential mechanism involving three steps. Biochemistry 1985, 24:2712-2723. 10.1021/bi00332a018, 3896304.
16. Lutz R, Lozinski T, Ellinger T, Bujard H. Dissecting the functional program of Escherichia coli promoters: the combined mode of action of Lac repressor and AraC activator. Nucleic Acids Research 2001, 29:3873-3881. 10.1093/nar/29.18.3873, 55909, 11557820.
17. Ribeiro AS, Häkkinen A, Mannerström H, Lloyd-Price J, Yli-Harja O. Effects of the promoter open complex formation on gene expression dynamics. Physical Review E 2010, 81:011912.
18. Ribeiro AS. Effects of coupling strength and space on the dynamics of coupled toggle switches in stochastic gene networks with multiple-delayed reactions. Physical Review E 2007, 75:061903.
19. Golding I, Paulsson J, Zawilski SM, Cox EC. Real-time kinetics of gene activity in individual bacteria. Cell 2005, 123:1025-1036. 10.1016/j.cell.2005.09.031, 16360033.
20. Le TT, Harlepp S, Guet CC, Dittmar K, Emonet T, Pan T, Cluzel P. Real-time RNA profiling within a single bacterium. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9160-9164.
21. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6640-6645. 10.1073/pnas.120163297, 18686, 10829079.
22. Andersen JB, Sternberg C, Poulsen LK, Bjørn SP, Givskov M, Molin S. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Applied Environmental Microbiology 1998, 64:2240-2246.
23. Elowitz MB, Leibler S. A synthetic oscillatory network of transcriptional regulators. Nature 2000, 403:335-338. 10.1038/35002125, 10659856.
24. Skerra A. Use of the tetracycline promoter for the tightly regulated production of a murine antibody fragment in Escherichia coli. Gene 1994, 151:131-135. 10.1016/0378-1119(94)90643-2, 7828861.
25. Korpela MT, Kurittu JS, Karvinen JT, Karp MT. A recombinant Escherichia coli sensor strain for the detection of tetracyclines. Analytical Chemistry 1998, 70:4457-4462. 10.1021/ac980740e, 9823708.
26. Hansson MD, Rzeznicka K, Rosenbäck M, Hansson M, Sirijovski N. PCR-mediated deletion of plasmid DNA. Analytical Biochemistry 2008, 15:373-375.
27. Maniatis T, Fritsch EF, Sambrook J. Molecular Cloning: A Laboratory Manual 1982, New York: Cold Spring Harbor Laboratory, New York.
28. Soille P. Morphological Image Analysis: Principles and Applications 1999, Springer-Verlag.
29. Chen TB, Lu H, Lee Y-S, Lan H-J. Segmentation of cDNA microarray images by kernel density estimation. Journal of Biomedical Informatics 2008, 41:1021-1027. 10.1016/j.jbi.2008.02.007, 18395494.
30. Otsu N. A threshold selection method from gray-level histograms. IEEE Transactions on Systems, Man, Cybernetics 1979, 9:62-66.
31. Ribeiro AS, Zhu R, Kauffman SA. A general modeling strategy for gene regulatory networks with stochastic dynamics. Journal of Computational Biology 2007, 13:1630-1639.
32. Roussel M, Zhu R. Validation of an algorithm for delay stochastic simulation of transcription and translation in prokaryotic gene expression. Physical Biology 2006, 3:274-284. 10.1088/1478-3975/3/4/005, 17200603.
33. Zhu R, Ribeiro S, Salahub D, Kauffman SA. Studying genetic regulatory networks at the molecular level: de-layed reaction stochastic models. Journal of Theoretical Biology 2007, 246:725-745. 10.1016/j.jtbi.2007.01.021, 17350653.
34. Ribeiro AS, Lloyd-Price J. SGNSim, a stochastic genetic networks simulator. Bioinformatics 2007, 23:777-779. 10.1093/bioinformatics/btm004, 17267430.
35. Gillespie DT. Exact stochastic simulation of coupled chemical reactions. Journal of Physical Chemistry 1977, 81:2340-2361.
36. Ribeiro AS, Smolander OP, Rajala T, Häkkinen A, Yli-Harja O. Delayed stochastic model of transcription at the single nucleotide level. Journal of Computational Biology 2009, 16:539-553. 10.1089/cmb.2008.0153, 19361326.
37. Kleinschmidt C, Tovar K, Hillen W, Porschke D. Dynamics of repressor-operator recognition: the Tn10-encoded tetracycline resistance control. Biochemistry 1988, 27:1094-104. 10.1021/bi00404a003, 2835082.
38. Kamionka A, Bogdanska-Urbaniak J, Scholz O, Hillen W. Two mutations in the tetracycline repressor change the inducer anhydrotetracycline to a corepressor. Nucleic Acids Research 2004, 32:842-847. 10.1093/nar/gkh200, 373327, 14764926.
39. Cormack BP, Valdivia RH, Falkow S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 1996, 173:33-38. 10.1016/0378-1119(95)00685-0, 8707053.
40. Zhu R, Salahub D. Delay stochastic simulation of single-gene expression reveals a detailed relationship between protein noise and mean abundance. FEBS Letters 2008, 582:2905-291. 10.1016/j.febslet.2008.07.028, 18656472.
41. Paulsson J. Summing up the noise in gene networks. Nature 2004, 29:415-418.
42. Landick R. The regulatory roles and mechanism of transcriptional pausing. Biochemical Society Transactions 2006, 34:1062-1066.
43. 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. Nature Genetics 2006, 38:636-643. 10.1038/ng1807, 16715097.
44. Ribeiro AS. Stochastic and delayed stochastic models of gene expression and regulation. Mathematical Biosciences 2010, 223:1-11. 10.1016/j.mbs.2009.10.007, 19883665.
45. Greive SJ, von Hippel PH. Thinking quantitatively about transcriptional regulation. Nature Reviews Molecular Cell Biology 2005, 6:221-32.