title: A versatile framework for microbial engineering using synthetic non-coding RNAs.
abstract: Synthetic non-coding RNAs have emerged as a versatile class of molecular devices that have a diverse range of programmable functions, including signal sensing, gene regulation and the modulation of molecular interactions. Owing to their small size and the central role of Watson-Crick base pairing in determining their structure, function and interactions, several distinct types of synthetic non-coding RNA regulators that are functional at the DNA, mRNA and protein levels have been experimentally characterized and computationally modelled. These engineered devices can be incorporated into genetic circuits, enabling the more efficient creation of complex synthetic biological systems. In this Review, we summarize recent progress in engineering synthetic non-coding RNA devices and their application to genetic and cellular engineering in a broad range of microorganisms.
authors.affiliation: 1] University of California San Francisco Center for Systems and Synthetic Biology, University of California San Francisco, San Francisco, California 94158, USA. [2] Department of Cellular and Molecular Pharmacology, University of California San Francisco, San Francisco, California 94158, USA. [3] California Institute for Quantitative Biomedical Research, San Francisco, California 94158, USA.
authors.forename: Lei S
authors.initials: LS
authors.lastname: Qi
authors.affiliation: 1] California Institute for Quantitative Biomedical Research, San Francisco, California 94158, USA. [2] Department of Bioengineering, University of California Berkeley, Berkeley, California 94720, USA. [3] Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
authors.forename: Adam P
authors.initials: AP
authors.lastname: Arkin
mesh_terms: D001419:Bacteria / Q000235:genetics*; D001709:Biotechnology; D003198:Computer Simulation; D005658:Fungi / Q000235:genetics*; D005786:Gene Expression Regulation; D053263:Gene Regulatory Networks; D005818:Genetic Engineering / Q000379:methods*; D022661:RNA, Untranslated / Q000737:chemistry / Q000235:genetics*; D015398:Signal Transduction; D058615:Synthetic Biology
chemical_list: D022661:RNA, Untranslated
references.citation: Genetics. 2013 Nov;195(3):1187-91
references.pmid: 23979586
references.citation: Nat Biotechnol. 2007 Jul;25(7):795-801
references.pmid: 17515909
references.citation: Science. 2012 Aug 17;337(6096):816-21
references.pmid: 22745249
references.citation: Biotechniques. 2008 Apr;44(5):613-6
references.pmid: 18474035
references.citation: Cold Spring Harb Symp Quant Biol. 2006;71:269-73
references.pmid: 17381306
references.citation: Nat Methods. 2012 Nov;9(11):1088-94
references.pmid: 23023598
references.citation: Proc Natl Acad Sci U S A. 2013 Aug 20;110(34):14024-9
references.pmid: 23924614
references.citation: RNA. 2011 Mar;17(3):478-88
references.pmid: 21224378
references.citation: Proc Natl Acad Sci U S A. 2012 Sep 18;109(38):15271-6
references.pmid: 22949707
references.citation: Nat Biotechnol. 2013 Mar;31(3):227-9
references.pmid: 23360964
references.citation: Curr Opin Microbiol. 2005 Dec;8(6):685-94
references.pmid: 16256421
references.citation: Mol Syst Biol. 2012;8:620
references.pmid: 23089683
references.citation: Nucleic Acids Res. 2012 Jul;40(12):5775-86
references.pmid: 22383579
references.citation: Science. 2009 Jul 24;325(5939):429-32
references.pmid: 19628860
references.citation: Nat Biotechnol. 2004 Jul;22(7):841-7
references.pmid: 15208640
references.citation: Science. 2011 Sep 2;333(6047):1248-52
references.pmid: 21885773
references.citation: Science. 2008 Oct 17;322(5900):456-60
references.pmid: 18927397
references.citation: Proc Natl Acad Sci U S A. 2011 May 24;108(21):8617-22
references.pmid: 21555549
references.citation: Proc Natl Acad Sci U S A. 2012 Apr 10;109(15):5850-5
references.pmid: 22454498
references.citation: Nat Rev Genet. 2007 Oct;8(10):776-90
references.pmid: 17846637
references.citation: Biotechnol Prog. 1999 Jan-Feb;15(1):58-64
references.pmid: 9933514
references.citation: Methods Mol Biol. 2010;634:355-69
references.pmid: 20676996
references.citation: Cell. 2009 Feb 20;136(4):577-80
references.pmid: 19239877
references.citation: Nat Biotechnol. 2013 Mar;31(3):233-9
references.pmid: 23360965
references.citation: Curr Opin Microbiol. 2008 Dec;11(6):567-73
references.pmid: 18983935
references.citation: Nature. 2012 Nov 8;491(7423):249-53
references.pmid: 23041931
references.citation: Cell. 2013 May 9;153(4):910-8
references.pmid: 23643243
references.citation: J Am Chem Soc. 2008 Dec 3;130(48):16310-5
references.pmid: 18998646
references.citation: Cold Spring Harb Perspect Biol. 2011 Dec 01;3(12):
references.pmid: 20980440
references.citation: Nat Biotechnol. 2012 Nov;30(11):1137-42
references.pmid: 23034349
references.citation: Nature. 2008 Jan 3;451(7174):86-9
references.pmid: 18172501
references.citation: Microbiol Mol Biol Rev. 2008 Dec;72(4):579-89, Table of Contents
references.pmid: 19052321
references.citation: Nucleic Acids Res. 2012 Nov 1;40(20):e154
references.pmid: 22810204
references.citation: Sci Am. 2004 Oct;291(4):60-7
references.pmid: 15487671
references.citation: Gene. 2005 Nov 21;361:13-37
references.pmid: 16213112
references.citation: Nucleic Acids Res. 2013 Aug;41(15):7429-37
references.pmid: 23761437
references.citation: Nat Biotechnol. 2002 Feb;20(2):135-41
references.pmid: 11821858
references.citation: Nat Chem. 2011 Oct 30;3(12):954-62
references.pmid: 22109276
references.citation: Cell. 2009 Jun 26;137(7):1272-81
references.pmid: 19563759
references.citation: J Am Chem Soc. 2007 Nov 14;129(45):13814-5
references.pmid: 17944473
references.citation: Nature. 2012 Feb 15;482(7385):331-8
references.pmid: 22337052
references.citation: Science. 2011 Jul 22;333(6041):470-4
references.pmid: 21700839
references.citation: Nature. 2014 Jan 30;505(7485):696-700
references.pmid: 24270811
references.citation: Nature. 2000 Jan 20;403(6767):335-8
references.pmid: 10659856
references.citation: Science. 2010 Nov 26;330(6008):1251-5
references.pmid: 21109673
references.citation: Nat Protoc. 2013 Nov;8(11):2180-96
references.pmid: 24136345
references.citation: PLoS One. 2012;7(8):e42296
references.pmid: 22927924
references.citation: Science. 2011 Sep 2;333(6047):1307-11
references.pmid: 21885784
references.citation: Nat Rev Genet. 2010 Mar;11(3):181-90
references.pmid: 20125085
references.citation: Appl Environ Microbiol. 2010 Dec;76(23):7881-4
references.pmid: 20935124
references.citation: ACS Synth Biol. 2012 Jan 20;1(1):6-13
references.pmid: 23651005
references.citation: Nature. 2010 Jan 28;463(7280):559-62
references.pmid: 20111002
references.citation: Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18090-5
references.pmid: 23071327
references.citation: Science. 1990 Aug 3;249(4968):505-10
references.pmid: 2200121
references.citation: Mol Cell. 2011 Sep 16;43(6):915-26
references.pmid: 21925380
references.citation: Science. 2007 Mar 23;315(5819):1709-12
references.pmid: 17379808
references.citation: Nature. 2014 Jan 30;505(7485):701-5
references.pmid: 24336214
references.citation: Nat Biotechnol. 2012 Mar 25;30(4):354-9
references.pmid: 22446695
references.citation: Annu Rev Chem Biomol Eng. 2013;4:69-102
references.pmid: 23413816
references.citation: Nat Biotechnol. 2012 Oct;30(10):1002-6
references.pmid: 22983090
references.citation: Proc Natl Acad Sci U S A. 2010 May 11;107(19):8531-6
references.pmid: 20421500
references.citation: Science. 2009 May 29;324(5931):1199-202
references.pmid: 19478183
references.citation: Annu Rev Biochem. 2009;78:305-34
references.pmid: 19298181
references.citation: Nucleic Acids Res. 2003 Jul 1;31(13):3406-15
references.pmid: 12824337
references.citation: Nat Chem Biol. 2012 Mar 25;8(5):447-54
references.pmid: 22446835
references.citation: Science. 2013 Sep 20;341(6152):1235005
references.pmid: 23950497
references.citation: Science. 2011 Dec 23;334(6063):1716-9
references.pmid: 22194579
references.citation: Nucleic Acids Res. 2013 Dec;41(22):10449-61
references.pmid: 23999097
references.citation: Mol Divers. 1998-1999;4(2):75-89
references.pmid: 10425631
references.citation: Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):11063-8
references.pmid: 21642531
references.citation: Nature. 2012 Aug 16;488(7411):384-8
references.pmid: 22820255
references.citation: Phys Biol. 2009 Jul 01;6(2):025007
references.pmid: 19571368
references.citation: Science. 2011 Jun 3;332(6034):1196-201
references.pmid: 21636773
references.citation: PLoS Comput Biol. 2009 Dec;5(12):e1000620
references.pmid: 20041206
references.citation: Nat Chem Biol. 2007 Jan;3(1):23-8
references.pmid: 17173026
references.citation: Nature. 2002 Jul 11;418(6894):244-51
references.pmid: 12110901
references.citation: Nature. 1990 Aug 30;346(6287):818-22
references.pmid: 1697402
references.citation: Cell. 2013 Feb 28;152(5):1173-83
references.pmid: 23452860
references.citation: Nucleic Acids Res. 2009 Jan;37(1):184-92
references.pmid: 19033367
references.citation: Nat Biotechnol. 2006 May;24(5):545-54
references.pmid: 16680139
references.citation: Science. 2003 Sep 26;301(5641):1904-8
references.pmid: 14512628
references.citation: Cell. 2013 Sep 12;154(6):1370-9
references.pmid: 23992847
references.citation: Cell. 2007 Sep 21;130(6):1019-31
references.pmid: 17889647
references.citation: Nature. 2008 Nov 27;456(7221):516-9
references.pmid: 18971928
references.citation: Nat Methods. 2013 Apr;10(4):347-53
references.pmid: 23474467
references.citation: Cell. 2013 Jul 18;154(2):442-51
references.pmid: 23849981
references.citation: Nature. 2000 Jan 20;403(6767):339-42
references.pmid: 10659857
references.citation: Nat Biotechnol. 2005 Mar;23(3):337-43
references.pmid: 15723047
references.citation: Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14283-8
references.pmid: 17709748
references.citation: Nat Methods. 2013 Apr;10(4):354-60
references.pmid: 23474465
references.citation: Science. 2008 Aug 15;321(5891):960-4
references.pmid: 18703739
references.citation: Annu Rev Microbiol. 2005;59:487-517
references.pmid: 16153177
references.citation: Nat Rev Microbiol. 2006 Aug;4(8):588-96
references.pmid: 16845429
references.citation: Cell. 1989 Oct 20;59(2):395-404
references.pmid: 2478296
references.citation: Nat Biotechnol. 2009 Aug;27(8):753-9
references.pmid: 19648908
references.citation: Biochemistry. 2013 Dec 3;52(48):8777-85
references.pmid: 24215455
references.citation: Mol Syst Biol. 2008;4:161
references.pmid: 18277378
references.citation: Nat Methods. 2013 Nov;10(11):1116-21
references.pmid: 24076762
references.citation: Annu Rev Biophys Biomol Struct. 2001;30:457-75
references.pmid: 11441810
references.citation: Nature. 2010 Jan 21;463(7279):326-30
references.pmid: 20090747
references.citation: J Mol Biol. 1995 Mar 10;246(5):585-94
references.pmid: 7877178
references.citation: Nat Rev Genet. 2004 Apr;5(4):316-23
references.pmid: 15131654
references.citation: Nature. 2010 Jan 28;463(7280):568-71
references.pmid: 20072129
references.citation: Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):11069-74
references.pmid: 21642536
references.citation: Cell. 1983 Sep;34(2):683-91
references.pmid: 6311438
references.citation: Nucleic Acids Res. 2013 Aug;41(15):7577-88
references.pmid: 23761434
references.citation: Genes Dev. 1994 Dec 15;8(24):3021-31
references.pmid: 8001821
references.citation: Nat Rev Microbiol. 2009 Oct;7(10):715-23
references.pmid: 19756010
references.citation: Nucleic Acids Res. 2013 Apr;41(7):4336-43
references.pmid: 23460208
references.citation: Nature. 2012 Aug 16;488(7411):320-8
references.pmid: 22895337
references.citation: Science. 2013 Feb 15;339(6121):823-6
references.pmid: 23287722
references.citation: Nature. 2011 Mar 31;471(7340):602-7
references.pmid: 21455174
references.citation: Curr Opin Biotechnol. 2006 Oct;17(5):548-57
references.pmid: 16978856
references.citation: J Bacteriol. 2002 May;184(10):2740-7
references.pmid: 11976303
references.citation: Nature. 2011 Jan 20;469(7330):368-73
references.pmid: 21248844
references.citation: FEMS Microbiol Rev. 2003 Apr;27(1):75-97
references.pmid: 12697343
references.citation: Cell. 2009 Nov 25;139(5):945-56
references.pmid: 19945378
references.citation: Nature. 2009 May 21;459(7245):414-8
references.pmid: 19458720
references.citation: Nature. 2006 Apr 13;440(7086):940-3
references.pmid: 16612385
references.citation: Proc Natl Acad Sci U S A. 2005 Mar 8;102(10):3581-6
references.pmid: 15738412
references.citation: Nat Rev Microbiol. 2011 Jun;9(6):467-77
references.pmid: 21552286
references.citation: Science. 2013 Feb 15;339(6121):819-23
references.pmid: 23287718
references.citation: ACS Synth Biol. 2013 Oct 18;2(10):604-13
references.pmid: 23977949
references.citation: Elife. 2013 Jan 29;2:e00471
references.pmid: 23386978
references.citation: Proc Natl Acad Sci U S A. 2013 Nov 19;110(47):19012-7
references.pmid: 24191015
references.citation: Nat Biotechnol. 2013 Aug;31(8):686-8
references.pmid: 23929338
references.citation: Biotechnol J. 2013 Dec;8(12):1379-95
references.pmid: 24124015
references.citation: PLoS Comput Biol. 2013;9(8):e1003172
references.pmid: 23935479
references.citation: J Am Chem Soc. 2011 Dec 14;133(49):19878-88
references.pmid: 21981600
references.citation: Nature. 2009 Jan 15;457(7227):309-12
references.pmid: 19148099