Engineering dynamic cell cycle control with synthetic small molecule-responsive RNA devices

Journal of Biological Engineering

Volumn 9, Issue 1, 2015, Pages

  Wei, Kathy Y ^a   Smolke, Christina D ^a  

^a Stanford University   (United States)

Author keywords

Cell cycle; Cellular devices; RNA engineering; Synthetic biology

Indexed keywords

RNA;

ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CELL POPULATION; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE SWITCHING; GENETIC ENGINEERING; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROCESS OPTIMIZATION; RELIABILITY; RNA SYNTHESIS; SYNTHETIC BIOLOGY;

EID: 84947564362     PISSN: None     EISSN: 17541611     Source Type: Journal    
DOI: 10.1186/s13036-015-0019-7     Document Type: Article

References (55)

1. Salis HM, Mirsky EA, Voigt CA. Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol. 2009;27(10):946-50. doi: 10.1038/nbt.1568.
2. Gardner TS, Cantor CR, Collins JJ. Construction of a genetic toggle switch in Escherichia coli. Nature. 2000;403(6767):339-42. doi: 10.1038/35002131.
3. Friedland AE, Lu TK, Wang X, Shi D, Church G, Collins JJ. Synthetic gene networks that count. Science. 2009;324(5931):1199-202. doi: 10.1126/science.1172005.
4. Tabor JJ, Salis HM, Simpson ZB, Chevalier AA, Levskaya A, Marcotte EM, et al. A synthetic genetic edge detection program. Cell. 2009;137(7):1272-81. doi: 10.1016/j.cell.2009.04.048.
5. Bonnet J, Yin P, Ortiz ME, Subsoontorn P, Endy D. Amplifying genetic logic gates. Science. 2013;340(6132):599-603. doi: 10.1126/science.1232758.
6. Zalatan JG, Lee ME, Almeida R, Gilbert LA, Whitehead EH, La Russa M, et al. Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell. 2015;160(1-2):339-50. doi: 10.1016/j.cell.2014.11.052.
7. Wang YH, Wei KY, Smolke CD. Synthetic biology: advancing the design of diverse genetic systems. Annual review of chemical and biomolecular engineering. 2013;4:69-102. doi: 10.1146/annurev-chembioeng-061312-103351.
8. Galloway KE, Franco E, Smolke CD. Dynamically reshaping signaling networks to program cell fate via genetic controllers. Science. 2013;341(6152):1235005. doi: 10.1126/science.1235005.
9. Bashor CJ, Helman NC, Yan S, Lim WA. Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics. Science. 2008;319(5869):1539-43. doi: 10.1126/science.1151153.
10. Xie Z, Wroblewska L, Prochazka L, Weiss R, Benenson Y. Multi-input RNAi-based logic circuit for identification of specific cancer cells. Science. 2011;333(6047):1307-11. doi: 10.1126/science.1205527.
11. Ye H, Daoud-El Baba M, Peng RW, Fussenegger M. A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science. 2011;332(6037):1565-8. doi: 10.1126/science.1203535.
12. Chen YY, Jensen MC, Smolke CD. Genetic control of mammalian T-cell proliferation with synthetic RNA regulatory systems. Proc Natl Acad Sci U S A. 2010;107(19):8531-6. doi: 10.1073/pnas.1001721107.
13. Tigges M, Marquez-Lago TT, Stelling J, Fussenegger M. A tunable synthetic mammalian oscillator. Nature. 2009;457(7227):309-12. doi: 10.1038/nature07616.
14. Haynes KA, Silver PA. Synthetic reversal of epigenetic silencing. J Biol Chem. 2011;286(31):27176-82. doi: 10.1074/jbc.C111.229567.
15. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-74. doi: 10.1016/j.cell.2011.02.013.
16. Fussenegger M, Schlatter S, Datwyler D, Mazur X, Bailey JE. Controlled proliferation by multigene metabolic engineering enhances the productivity of Chinese hamster ovary cells. Nat Biotechnol. 1998;16(5):468-72. doi: 10.1038/nbt0598-468.
17. Conklin JF, Sage J. Keeping an eye on retinoblastoma control of human embryonic stem cells. J Cell Biochem. 2009;108(5):1023-30. doi: 10.1002/jcb.22342.
18. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature. 2001;411(6835):366-74. doi: 10.1038/35077232.
19. Kymalainen H, Appelt JU, Giordano FA, Davies AF, Ogilvie CM, Ahmed SG, et al. Long-term episomal transgene expression from mitotically stable integration-deficient lentiviral vectors. Hum Gene Ther. 2014;25(5):428-42. doi: 10.1089/hum.2013.172.
20. Rosner M, Schipany K, Hengstschlager M. Merging high-quality biochemical fractionation with a refined flow cytometry approach to monitor nucleocytoplasmic protein expression throughout the unperturbed mammalian cell cycle. Nat Protoc. 2013;8(3):602-26. doi: 10.1038/nprot.2013.011.
21. Carothers JM, Goler JA, Juminaga D, Keasling JD. Model-driven engineering of RNA devices to quantitatively program gene expression. Science. 2011;334(6063):1716-9. doi: 10.1126/science.1212209.
22. Bell CL, Yu D, Smolke CD, Geall AJ, Beard CW, Mason PW. Control of alphavirus-based gene expression using engineered riboswitches. Virology. 2015;483:302-11. doi: 10.1016/j.virol.2015.04.023.
23. Michener JK, Smolke CD. High-throughput enzyme evolution in Saccharomyces cerevisiae using a synthetic RNA switch. Metab Eng. 2012;14(4):306-16. doi: 10.1016/j.ymben.2012.04.004.
24. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. Control of gene expression by a natural metabolite-responsive ribozyme. Nature. 2004;428(6980):281-6. doi: 10.1038/nature02362.
25. Strovas TJ, Rosenberg AB, Kuypers BE, Muscat RA, Seelig G. MicroRNA-based single-gene circuits buffer protein synthesis rates against perturbations. ACS Synth Biol. 2014;3(5):324-31. doi: 10.1021/sb4001867.
26. Khvorova A, Lescoute A, Westhof E, Jayasena SD. Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat Struct Biol. 2003;10(9):708-12. doi: 10.1038/nsb959.
27. Stoltenburg R, Reinemann C, Strehlitz B. SELEX--a (r)evolutionary method to generate high-affinity nucleic acid ligands. Biomol Eng. 2007;24(4):381-403. doi: 10.1016/j.bioeng.2007.06.001.
28. Hermann T, Patel DJ. Adaptive recognition by nucleic acid aptamers. Science. 2000;287(5454):820-5.
29. Win MN, Smolke CD. A modular and extensible RNA-based gene-regulatory platform for engineering cellular function. Proc Natl Acad Sci U S A. 2007;104(36):14283-8. doi: 10.1073/pnas.0703961104.
30. Liang JC, Chang AL, Kennedy AB, Smolke CD. A high-throughput, quantitative cell-based screen for efficient tailoring of RNA device activity. Nucleic Acids Res. 2012;40(20), e154. doi: 10.1093/nar/gks636.
31. Townshend B, Kennedy AB, Xiang JS, Smolke CD. High-throughput cellular RNA device engineering. Nat Methods. 2015;12(10):989-94. doi: 10.1038/nmeth.3486.
32. Wei KY, Chen YY, Smolke CD. A yeast-based rapid prototype platform for gene control elements in mammalian cells. Biotechnol Bioeng. 2013;110(4):1201-10. doi: 10.1002/bit.24792.
33. Ketzer P, Kaufmann JK, Engelhardt S, Bossow S, von Kalle C, Hartig JS, et al. Artificial riboswitches for gene expression and replication control of DNA and RNA viruses. Proc Natl Acad Sci U S A. 2014;111(5):E554-62. doi: 10.1073/pnas.1318563111.
34. Lukas J, Herzinger T, Hansen K, Moroni MC, Resnitzky D, Helin K, et al. Cyclin E-induced S phase without activation of the pRb/E2F pathway. Genes Dev. 1997;11(11):1479-92.
35. Hsu JY, Reimann JD, Sorensen CS, Lukas J, Jackson PK. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APC(Cdh1). Nat Cell Biol. 2002;4(5):358-66. doi: 10.1038/ncb785.
36. Nghiem P, Park PK, Kim Y, Vaziri C, Schreiber SL. ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc Natl Acad Sci U S A. 2001;98(16):9092-7. doi: 10.1073/pnas.161281798.
37. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25(1):25-9. doi: 10.1038/75556.
38. Morgan DO. The cell cycle: principles of control. Primers in biology. London Sunderland, MA: New Science Press in association with Oxford University Press; 2007. Distributed inside North America by Sinauer Associates, Publishers.
39. Rubin SM, Gall AL, Zheng N, Pavletich NP. Structure of the Rb C-terminal domain bound to E2F1-DP1: a mechanism for phosphorylation-induced E2F release. Cell. 2005;123(6):1093-106. doi: 10.1016/j.cell.2005.09.044.
40. Gavet O, Pines J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev Cell. 2010;18(4):533-43. doi: 10.1016/j.devcel.2010.02.013.
41. Mukherji M, Bell R, Supekova L, Wang Y, Orth AP, Batalov S, et al. Genome-wide functional analysis of human cell-cycle regulators. Proc Natl Acad Sci U S A. 2006;103(40):14819-24. doi: 10.1073/pnas.0604320103.
42. Kittler R, Pelletier L, Heninger AK, Slabicki M, Theis M, Miroslaw L, et al. Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat Cell Biol. 2007;9(12):1401-12. doi: 10.1038/ncb1659.
43. Tian J, Andreadis ST. Independent and high-level dual-gene expression in adult stem-progenitor cells from a single lentiviral vector. Gene Ther. 2009;16(7):874-84. doi: 10.1038/gt.2009.46.
44. Wilson C, Bellen HJ, Gehring WJ. Position effects on eukaryotic gene expression. Annu Rev Cell Biol. 1990;6:679-714. doi: 10.1146/annurev.cb.06.110190.003335.
45. Milot E, Fraser P, Grosveld F. Position effects and genetic disease. Trends Genet. 1996;12(4):123-6.
46. Shearwin KE, Callen BP, Egan JB. Transcriptional interference--a crash course. Trends Genet. 2005;21(6):339-45. doi: 10.1016/j.tig.2005.04.009.
47. Eszterhas SK, Bouhassira EE, Martin DI, Fiering S. Transcriptional interference by independently regulated genes occurs in any relative arrangement of the genes and is influenced by chromosomal integration position. Mol Cell Biol. 2002;22(2):469-79.
48. Auslander S, Stucheli P, Rehm C, Auslander D, Hartig JS, Fussenegger M. A general design strategy for protein-responsive riboswitches in mammalian cells. Nat Methods. 2014;11(11):1154-60. doi: 10.1038/nmeth.3136.
49. Culler SJ, Hoff KG, Smolke CD. Reprogramming cellular behavior with RNA controllers responsive to endogenous proteins. Science. 2010;330(6008):1251-5. doi: 10.1126/science.1192128.
50. Kennedy AB, Vowles JV, d'Espaux L, Smolke CD. Protein-responsive ribozyme switches in eukaryotic cells. Nucleic Acids Res. 2014;42(19):12306-21. doi: 10.1093/nar/gku875.
51. Bloom RJ, Winkler SM, Smolke CD. Synthetic feedback control using an RNAi-based gene-regulatory device. J Biol Eng. 2015;9:5. doi: 10.1186/s13036-015-0002-3.
52. Zhang J, Yang PL, Gray NS. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer. 2009;9(1):28-39. doi: 10.1038/nrc2559.
53. Sambrook J, Russell DW. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press; 2001.
54. Pozarowski P, Darzynkiewicz Z. Analysis of cell cycle by flow cytometry. Methods Mol Biol. 2004;281:301-11. doi: 10.1385/1-59259-811-0:301.
55. Kalejta RF, Brideau AD, Banfield BW, Beavis AJ. An integral membrane green fluorescent protein marker, Us9-GFP, is quantitatively retained in cells during propidium iodide-based cell cycle analysis by flow cytometry. Exp Cell Res. 1999;248(1):322-8. doi: 10.1006/excr.1999.4427.