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PMID: 20713708 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Tracking, tuning, and terminating microbial physiology using synthetic riboregulators.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 107 ·No. 36 ·2010-09-07 ·Pages 15898-903

Callura JM, Dwyer DJ, Isaacs FJ, Cantor CR, Collins JJ

Abstract

The development of biomolecular devices that interface with biological systems to reveal new insights and produce novel functions is one of the defining goals of synthetic biology. Our lab previously described a synthetic, riboregulator system that affords for modular, tunable, and tight control of gene expression in vivo. Here we highlight several experimental advantages unique to this RNA-based system, including physiologically relevant protein production, component modularity, leakage minimization, rapid response time, tunable gene expression, and independent regulation of multiple genes. We demonstrate this utility in four sets of in vivo experiments with various microbial systems. Specifically, we show that the synthetic riboregulator is well suited for GFP fusion protein tracking in wild-type cells, tight regulation of toxic protein expression, and sensitive perturbation of stress response networks. We also show that the system can be used for logic-based computing of multiple, orthogonal inputs, resulting in the development of a programmable kill switch for bacteria. This work establishes a broad, easy-to-use synthetic biology platform for microbiology experiments and biotechnology applications.

MeSH Terms
Bacterial Physiological Phenomena Ribonucleotides/physiology
Chemicals
Ribonucleotides
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Callura Jarred M
Howard Hughes Medical Institute, Boston University, MA 02215, USA.
Dwyer Daniel J
Isaacs Farren J
Cantor Charles R
Collins James J
References (48)
48 references, click to expand
  1. Engineering a ligand-dependent RNA transcriptional activator.
    Chem Biol. 2004 Aug;11(8):1157-63 PMID: 15324817
  2. Engineered riboregulators enable post-transcriptional control of gene expression.
    Nat Biotechnol. 2004 Jul;22(7):841-7 PMID: 15208640
  3. Green fluorescent protein functions as a reporter for protein localization in Escherichia coli.
    J Bacteriol. 2000 Jul;182(14):4068-76 PMID: 10869087
  4. Holins: the protein clocks of bacteriophage infections.
    Annu Rev Microbiol. 2000;54:799-825 PMID: 11018145
  5. Nucleotide sequence of the lexA gene of Escherichia coli K-12.
    Nucleic Acids Res. 1981 Aug 25;9(16):4149-61 PMID: 6272195
  6. Synthetic biology: new engineering rules for an emerging discipline.
    Mol Syst Biol. 2006;2:2006.0028 PMID: 16738572
  7. A theophylline responsive riboswitch based on helix slipping controls gene expression in vivo.
    Nucleic Acids Res. 2004 Mar 05;32(4):1610-4 PMID: 15004248
  8. Engineered gene circuits.
    Nature. 2002 Nov 14;420(6912):224-30 PMID: 12432407
  9. Control of the ccd operon in plasmid F.
    J Bacteriol. 1989 May;171(5):2353-60 PMID: 2651399
  10. Cell lysis by induction of cloned lambda lysis genes.
    Mol Gen Genet. 1981;182(2):326-31 PMID: 6457237
  11. RegulonDB (version 5.0): Escherichia coli K-12 transcriptional regulatory network, operon organization, and growth conditions.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D394-7 PMID: 16381895
  12. Recent advances in mammalian synthetic biology-design of synthetic transgene control networks.
    Curr Opin Biotechnol. 2009 Aug;20(4):449-60 PMID: 19762224
  13. Design of the linkers which effectively separate domains of a bifunctional fusion protein.
    Protein Eng. 2001 Aug;14(8):529-32 PMID: 11579220
  14. Negative co-dominant inhibition of recA protein function. Biochemical properties of the recA1, recA13 and recA56 proteins and the effect of recA56 protein on the activities of the wild-type recA protein function in vitro.
    J Mol Biol. 1993 Nov 5;234(1):72-86 PMID: 8230208
  15. TonB-dependent energy transduction between outer and cytoplasmic membranes.
    Biometals. 2007 Jun;20(3-4):453-65 PMID: 17225934
  16. A synthetic oscillatory network of transcriptional regulators.
    Nature. 2000 Jan 20;403(6767):335-8 PMID: 10659856
  17. Structure, function, and mechanism of ribonucleotide reductases.
    Biochim Biophys Acta. 2004 Jun 1;1699(1-2):1-34 PMID: 15158709
  18. Synthesis of orthogonal transcription-translation networks.
    Proc Natl Acad Sci U S A. 2009 May 26;106(21):8477-82 PMID: 19443689
  19. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
    Nat Genet. 2000 May;25(1):25-9 PMID: 10802651
  20. The Gene Ontology Annotation (GOA) Database: sharing knowledge in Uniprot with Gene Ontology.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D262-6 PMID: 14681408
  21. The gamma delta sequence of F is an insertion sequence.
    J Mol Biol. 1978 Dec 15;126(3):347-65 PMID: 745233
  22. Mechanism of specific LexA cleavage: autodigestion and the role of RecA coprotease.
    Biochimie. 1991 Apr;73(4):411-21 PMID: 1911941
  23. SOS induction by thermosensitive replication mutants of miniF plasmid.
    Mol Gen Genet. 1985;198(3):456-64 PMID: 3159950
  24. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli.
    Genetics. 2001 May;158(1):41-64 PMID: 11333217
  25. Synthetic gene networks that count.
    Science. 2009 May 29;324(5931):1199-202 PMID: 19478183
  26. Synthetic RNA circuits.
    Nat Chem Biol. 2007 Jan;3(1):23-8 PMID: 17173026
  27. Molecular control of bacterial death and lysis.
    Microbiol Mol Biol Rev. 2008 Mar;72(1):85-109, table of contents PMID: 18322035
  28. Synthetic biology: understanding biological design from synthetic circuits.
    Nat Rev Genet. 2009 Dec;10(12):859-71 PMID: 19898500
  29. Aerobic regulation of the Escherichia coli tonB gene by changes in iron availability and the fur locus.
    J Bacteriol. 1990 May;172(5):2287-93 PMID: 2139645
  30. Modulation of DNA supercoiling activity of Escherichia coli DNA gyrase by F plasmid proteins. Antagonistic actions of LetA (CcdA) and LetD (CcdB) proteins.
    J Biol Chem. 1992 Jun 15;267(17):12244-51 PMID: 1318314
  31. Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli.
    Mol Syst Biol. 2007;3:91 PMID: 17353933
  32. RNA synthetic biology.
    Nat Biotechnol. 2006 May;24(5):545-54 PMID: 16680139
  33. Exogenous control of mammalian gene expression through modulation of RNA self-cleavage.
    Nature. 2004 Sep 23;431(7007):471-6 PMID: 15386015
  34. RNA sequences that work as transcriptional activating regions.
    Nucleic Acids Res. 2003 Mar 1;31(5):1565-70 PMID: 12595565
  35. Bacterial iron homeostasis.
    FEMS Microbiol Rev. 2003 Jun;27(2-3):215-37 PMID: 12829269
  36. Large-scale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles.
    PLoS Biol. 2007 Jan;5(1):e8 PMID: 17214507
  37. Transposition mutagenesis of bacteriophage lambda: a new gene affecting cell lysis.
    J Mol Biol. 1979 Aug 15;132(3):307-22 PMID: 160463
  38. Construction of a genetic toggle switch in Escherichia coli.
    Nature. 2000 Jan 20;403(6767):339-42 PMID: 10659857
  39. Programmable ligand-controlled riboregulators of eukaryotic gene expression.
    Nat Biotechnol. 2005 Mar;23(3):337-43 PMID: 15723047
  40. A modular and extensible RNA-based gene-regulatory platform for engineering cellular function.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14283-8 PMID: 17709748
  41. Bacterial death by DNA gyrase poisoning.
    Trends Microbiol. 1998 Jul;6(7):269-75 PMID: 9717215
  42. Insight from TonB hybrid proteins into the mechanism of iron transport through the outer membrane.
    J Bacteriol. 2008 Jun;190(11):4001-16 PMID: 18390658
  43. Effects of the ccd function of the F plasmid on bacterial growth.
    J Bacteriol. 1985 Sep;163(3):841-9 PMID: 3897195
  44. Riboswitches in unexpected places--a synthetic riboswitch in a protein coding region.
    RNA. 2008 Dec;14(12):2498-503 PMID: 18945803
  45. Synthetic biology: applications come of age.
    Nat Rev Genet. 2010 May;11(5):367-79 PMID: 20395970
  46. Lethal action of bacteriophage lambda S gene.
    J Virol. 1982 Dec;44(3):886-92 PMID: 6217351
  47. Next-generation synthetic gene networks.
    Nat Biotechnol. 2009 Dec;27(12):1139-50 PMID: 20010597
  48. 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 Res. 1997 Mar 15;25(6):1203-10 PMID: 9092630
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2010-09-07
Epub
2010-00-16
Pages
15898-903
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2936621
Subset
IM
Grants
NIH HHS · DP1 OD003644 · United States
Howard Hughes Medical Institute · United States
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