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Article ; Online ; Conference proceedings: The First Annual Winter q-bio Meeting: quantitative biology on the Hawaiian Islands.

Prindle, Arthur / Stanton, Brynne C

ACS synthetic biology

2013 Volume 2, Issue 4, Page(s) 170–172

MeSH term(s)	Humans ; Models, Biological ; Synthetic Biology/methods ; Systems Biology/methods
Language	English
Publishing date	2013-04-19
Publishing country	United States
Document type	Congresses
ISSN	2161-5063
ISSN (online)	2161-5063
DOI	10.1021/sb400023u
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Article ; Online: Targets of the Sex Inducer homeodomain proteins are required for fungal development and virulence in Cryptococcus neoformans.

Mead, Matthew E / Stanton, Brynne C / Kruzel, Emilia K / Hull, Christina M

Molecular microbiology

2015 Volume 95, Issue 5, Page(s) 804–818

Abstract: In the yeast Saccharomyces cerevisiae, the regulation of cell types by homeodomain transcription factors is a key paradigm; however, many questions remain regarding this class of developmental regulators in other fungi. In the human fungal pathogen ... ...

Abstract	In the yeast Saccharomyces cerevisiae, the regulation of cell types by homeodomain transcription factors is a key paradigm; however, many questions remain regarding this class of developmental regulators in other fungi. In the human fungal pathogen Cryptococcus neoformans, the homeodomain transcription factors Sxi1α and Sxi2a are required for sexual development that produces infectious spores, but the molecular mechanisms by which they drive this process are unknown. To better understand homeodomain control of fungal development, we determined the targets of the Sxi2a-Sxi1α heterodimer using whole genome expression analyses paired with in silico and in vitro binding site identification methods. We identified Sxi-regulated genes that contained a site bound directly by the Sxi proteins that is required for full regulation in vivo. Among the targets of the Sxi2a-Sxi1α complex were many genes known to be involved in sexual reproduction, as well as several well-studied virulence genes. Our findings suggest that genes involved in sexual development are also important in mammalian disease. Our work advances the understanding of how homeodomain transcription factors control complex developmental events and suggests an intimate link between fungal development and virulence.
MeSH term(s)	Binding Sites ; Computational Biology ; Computer Simulation ; Cryptococcus neoformans/growth & development ; Cryptococcus neoformans/pathogenicity ; Gene Expression ; Gene Expression Regulation, Fungal ; Genes, Fungal ; Genome, Fungal ; Homeodomain Proteins/chemistry ; Homeodomain Proteins/metabolism ; Humans ; Transcription Factors/chemistry ; Transcription Factors/metabolism ; Virulence
Chemical Substances	Homeodomain Proteins ; Transcription Factors
Language	English
Publishing date	2015-01-16
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/mmi.12898
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Article ; Online: Genomic mining of prokaryotic repressors for orthogonal logic gates.

Stanton, Brynne C / Nielsen, Alec A K / Tamsir, Alvin / Clancy, Kevin / Peterson, Todd / Voigt, Christopher A

Nature chemical biology

2013 Volume 10, Issue 2, Page(s) 99–105

Abstract: Genetic circuits perform computational operations based on interactions between freely diffusing molecules within a cell. When transcription factors are combined to build a circuit, unintended interactions can disrupt its function. Here, we apply 'part ... ...

Abstract	Genetic circuits perform computational operations based on interactions between freely diffusing molecules within a cell. When transcription factors are combined to build a circuit, unintended interactions can disrupt its function. Here, we apply 'part mining' to build a library of 73 TetR-family repressors gleaned from prokaryotic genomes. The operators of a subset were determined using an in vitro method, and this information was used to build synthetic promoters. The promoters and repressors were screened for cross-reactions. Of these, 16 were identified that both strongly repress their cognate promoter (5- to 207-fold) and exhibit minimal interactions with other promoters. Each repressor-promoter pair was converted to a NOT gate and characterized. Used as a set of 16 NOT/NOR gates, there are >10(54) circuits that could be built by changing the pattern of input and output promoters. This represents a large set of compatible gates that can be used to construct user-defined circuits.
MeSH term(s)	Base Sequence ; Gene Regulatory Networks/genetics ; Genome, Bacterial/genetics ; Genomics ; Operator Regions, Genetic ; Prokaryotic Cells ; Promoter Regions, Genetic/genetics ; Repressor Proteins/genetics ; Small Molecule Libraries
Chemical Substances	Repressor Proteins ; Small Molecule Libraries
Language	English
Publishing date	2013-12-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2202962-X
ISSN	1552-4469 ; 1552-4450
ISSN (online)	1552-4469
ISSN	1552-4450
DOI	10.1038/nchembio.1411
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Article ; Online: Genetic programs constructed from layered logic gates in single cells.

Moon, Tae Seok / Lou, Chunbo / Tamsir, Alvin / Stanton, Brynne C / Voigt, Christopher A

Nature

2012 Volume 491, Issue 7423, Page(s) 249–253

Abstract: Genetic programs function to integrate environmental sensors, implement signal processing algorithms and control expression dynamics. These programs consist of integrated genetic circuits that individually implement operations ranging from digital logic ... ...

Abstract	Genetic programs function to integrate environmental sensors, implement signal processing algorithms and control expression dynamics. These programs consist of integrated genetic circuits that individually implement operations ranging from digital logic to dynamic circuits, and they have been used in various cellular engineering applications, including the implementation of process control in metabolic networks and the coordination of spatial differentiation in artificial tissues. A key limitation is that the circuits are based on biochemical interactions occurring in the confined volume of the cell, so the size of programs has been limited to a few circuits. Here we apply part mining and directed evolution to build a set of transcriptional AND gates in Escherichia coli. Each AND gate integrates two promoter inputs and controls one promoter output. This allows the gates to be layered by having the output promoter of an upstream circuit serve as the input promoter for a downstream circuit. Each gate consists of a transcription factor that requires a second chaperone protein to activate the output promoter. Multiple activator-chaperone pairs are identified from type III secretion pathways in different strains of bacteria. Directed evolution is applied to increase the dynamic range and orthogonality of the circuits. These gates are connected in different permutations to form programs, the largest of which is a 4-input AND gate that consists of 3 circuits that integrate 4 inducible systems, thus requiring 11 regulatory proteins. Measuring the performance of individual gates is sufficient to capture the behaviour of the complete program. Errors in the output due to delays (faults), a common problem for layered circuits, are not observed. This work demonstrates the successful layering of orthogonal logic gates, a design strategy that could enable the construction of large, integrated circuits in single cells.
MeSH term(s)	Amino Acid Sequence ; DNA-Binding Proteins/metabolism ; Directed Molecular Evolution ; Escherichia coli/cytology ; Escherichia coli/genetics ; Gene Expression Regulation, Bacterial ; Genomic Islands/genetics ; Logic ; Models, Genetic ; Molecular Chaperones/metabolism ; Molecular Sequence Data ; Promoter Regions, Genetic/genetics ; Pseudomonas/genetics ; Salmonella/genetics ; Shigella/genetics ; Single-Cell Analysis ; Synthetic Biology ; Transcription Factors/metabolism ; Transcription, Genetic
Chemical Substances	DNA-Binding Proteins ; Molecular Chaperones ; Transcription Factors
Language	English
Publishing date	2012-10-07
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/nature11516
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Article ; Online: Systematic transfer of prokaryotic sensors and circuits to mammalian cells.

Stanton, Brynne C / Siciliano, Velia / Ghodasara, Amar / Wroblewska, Liliana / Clancy, Kevin / Trefzer, Axel C / Chesnut, Jonathan D / Weiss, Ron / Voigt, Christopher A

ACS synthetic biology

2014 Volume 3, Issue 12, Page(s) 880–891

Abstract: Prokaryotic regulatory proteins respond to diverse signals and represent a rich resource for building synthetic sensors and circuits. The TetR family contains >10(5) members that use a simple mechanism to respond to stimuli and bind distinct DNA ... ...

Abstract	Prokaryotic regulatory proteins respond to diverse signals and represent a rich resource for building synthetic sensors and circuits. The TetR family contains >10(5) members that use a simple mechanism to respond to stimuli and bind distinct DNA operators. We present a platform that enables the transfer of these regulators to mammalian cells, which is demonstrated using human embryonic kidney (HEK293) and Chinese hamster ovary (CHO) cells. The repressors are modified to include nuclear localization signals (NLS) and responsive promoters are built by incorporating multiple operators. Activators are also constructed by modifying the protein to include a VP16 domain. Together, this approach yields 15 new regulators that demonstrate 19- to 551-fold induction and retain both the low levels of crosstalk in DNA binding specificity observed between the parent regulators in Escherichia coli, as well as their dynamic range of activity. By taking advantage of the DAPG small molecule sensing mediated by the PhlF repressor, we introduce a new inducible system with 50-fold induction and a threshold of 0.9 μM DAPG, which is comparable to the classic Dox-induced TetR system. A set of NOT gates is constructed from the new repressors and their response function quantified. Finally, the Dox- and DAPG- inducible systems and two new activators are used to build a synthetic enhancer (fuzzy AND gate), requiring the coordination of 5 transcription factors organized into two layers. This work introduces a generic approach for the development of mammalian genetic sensors and circuits to populate a toolbox that can be applied to diverse applications from biomanufacturing to living therapeutics.
MeSH term(s)	Animals ; CHO Cells ; Cricetinae ; Cricetulus ; Escherichia coli/genetics ; Escherichia coli Proteins/genetics ; Genes, Bacterial/genetics ; Genetic Engineering/methods ; HEK293 Cells ; Humans ; Phloroglucinol/analogs & derivatives ; Promoter Regions, Genetic/genetics ; Synthetic Biology/methods ; Transgenes/genetics
Chemical Substances	Escherichia coli Proteins ; TetR(B) protein, E coli ; 2,4-diacetylphloroglucinol (8XV4YYO3WN) ; Phloroglucinol (DHD7FFG6YS)
Language	English
Publishing date	2014-12-19
Publishing country	United States
Document type	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.
ISSN	2161-5063
ISSN (online)	2161-5063
DOI	10.1021/sb5002856
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Article ; Online: Allelic exchange of pheromones and their receptors reprograms sexual identity in Cryptococcus neoformans.

Stanton, Brynne C / Giles, Steven S / Staudt, Mark W / Kruzel, Emilia K / Hull, Christina M

PLoS genetics

2010 Volume 6, Issue 2, Page(s) e1000860

Abstract: ... by which the C. neoformans sexes are determined, we created strains in which the pheromone and pheromone receptor ... between alpha and alpha(a) strains. These data reveal that cell identity in C. neoformans is controlled ...

Abstract	Cell type specification is a fundamental process that all cells must carry out to ensure appropriate behaviors in response to environmental stimuli. In fungi, cell identity is critical for defining "sexes" known as mating types and is controlled by components of mating type (MAT) loci. MAT-encoded genes function to define sexes via two distinct paradigms: 1) by controlling transcription of components common to both sexes, or 2) by expressing specially encoded factors (pheromones and their receptors) that differ between mating types. The human fungal pathogen Cryptococcus neoformans has two mating types (a and alpha) that are specified by an extremely unusual MAT locus. The complex architecture of this locus makes it impossible to predict which paradigm governs mating type. To identify the mechanism by which the C. neoformans sexes are determined, we created strains in which the pheromone and pheromone receptor from one mating type (a) replaced the pheromone and pheromone receptor of the other (alpha). We discovered that these "alpha(a)" cells effectively adopt a new mating type (that of a cells); they sense and respond to alpha factor, they elicit a mating response from alpha cells, and they fuse with alpha cells. In addition, alpha(a) cells lose the alpha cell type-specific response to pheromone and do not form germ tubes, instead remaining spherical like a cells. Finally, we discovered that exogenous expression of the diploid/dikaryon-specific transcription factor Sxi2a could then promote complete sexual development in crosses between alpha and alpha(a) strains. These data reveal that cell identity in C. neoformans is controlled fully by three kinds of MAT-encoded proteins: pheromones, pheromone receptors, and homeodomain proteins. Our findings establish the mechanisms for maintenance of distinct cell types and subsequent developmental behaviors in this unusual human fungal pathogen.
MeSH term(s)	Alleles ; Blotting, Northern ; Blotting, Southern ; Crosses, Genetic ; Cryptococcus neoformans/cytology ; Cryptococcus neoformans/genetics ; Cryptococcus neoformans/metabolism ; Fruiting Bodies, Fungal/cytology ; Fruiting Bodies, Fungal/metabolism ; Fungal Proteins/genetics ; Fungal Proteins/metabolism ; Gene Expression Regulation, Fungal ; Genes, Mating Type, Fungal/genetics ; Pheromones/metabolism ; Receptors, Pheromone/metabolism ; Reproduction
Chemical Substances	Fungal Proteins ; Pheromones ; Receptors, Pheromone
Language	English
Publishing date	2010-02-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2186725-2
ISSN	1553-7404 ; 1553-7390
ISSN (online)	1553-7404
ISSN	1553-7390
DOI	10.1371/journal.pgen.1000860
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Article: Cognate Site Identifier analysis reveals novel binding properties of the Sex Inducer homeodomain proteins of Cryptococcus neoformans

Stanton, Brynne C / Giles, Steven S / Kruzel, Emilia K / Warren, Christopher L / Ansari, Aseem Z / Hull, Christina M

Molecular microbiology. 2009 June, v. 72, no. 6

2009

Abstract: Homeodomain proteins function in fungi to specify cell types and control sexual development. In the meningoencephalitis-causing fungal pathogen Cryptococcus neoformans, sexual development leads to the production of spores (suspected infectious particles). ...

Abstract	Homeodomain proteins function in fungi to specify cell types and control sexual development. In the meningoencephalitis-causing fungal pathogen Cryptococcus neoformans, sexual development leads to the production of spores (suspected infectious particles). Sexual development is controlled by the homeodomain transcription factors Sxi1α and Sxi2a, but the mechanism by which they act is unknown. To understand how the Sxi proteins regulate development, we characterized their binding properties in vitro, showing that Sxi2a does not require a partner to bind DNA with high affinity. We then utilized a novel approach, Cognate Site Identifier (CSI) arrays, to define a comprehensive DNA-binding profile for Sxi2a, revealing a consensus sequence distinct from those of other fungal homeodomain proteins. Finally, we show that the homeodomains of both Sxi proteins are required for sexual development, a departure from related fungi. Our findings support a model in which Sxi1α and Sxi2a control sexual development in a homeodomain-dependent manner by binding to DNA sequences that differ from those defined in previously established fungal paradigms.
Language	English
Dates of publication	2009-06
Size	p. 1334-1347.
Publisher	Blackwell Publishing Ltd
Publishing place	Oxford, UK
Document type	Article
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/j.1365-2958.2009.06719.x
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Article ; Online: Sexual development in Cryptococcus neoformans requires CLP1, a target of the homeodomain transcription factors Sxi1alpha and Sxi2a.

Ekena, Joanne L / Stanton, Brynne C / Schiebe-Owens, Jessica A / Hull, Christina M

Eukaryotic cell

2007 Volume 7, Issue 1, Page(s) 49–57

Abstract: Sexual development in the human fungal pathogen Cryptococcus neoformans is a multistep process that results in the formation of spores, the likely infectious particles. A critical step in this developmental process is the transition from bud-form growth ... ...

Abstract	Sexual development in the human fungal pathogen Cryptococcus neoformans is a multistep process that results in the formation of spores, the likely infectious particles. A critical step in this developmental process is the transition from bud-form growth to filamentous growth. This transition is controlled by the homeodomain transcription factors Sxi1alpha and Sxi2a, whose targets are largely unknown. Here we describe the discovery of a gene, CLP1, that is regulated by Sxi1alpha and Sxi2a and is essential for sexual development. In vitro binding studies also show that the CLP1 promoter is bound directly by Sxi1alpha and Sxi2a. The deletion of CLP1 leads to a block in sexual development after cell fusion but before filament formation, and cells without CLP1 are unable to grow vegetatively after cell fusion. Our findings lead to a model in which CLP1 is a downstream target of the Sxi proteins that functions to promote growth after mating and to establish the filamentous state, a critical step in the production of spores.
MeSH term(s)	Blotting, Northern ; Blotting, Southern ; Cryptococcus neoformans/growth & development ; Cryptococcus neoformans/pathogenicity ; Diploidy ; Electrophoretic Mobility Shift Assay ; Fruiting Bodies, Fungal ; Fungal Proteins/genetics ; Fungal Proteins/metabolism ; Gene Expression Regulation, Fungal ; Genes, Mating Type, Fungal ; Homeodomain Proteins/genetics ; Homeodomain Proteins/metabolism ; Phenotype ; Promoter Regions, Genetic/genetics ; Transcription Factors/genetics
Chemical Substances	Fungal Proteins ; Homeodomain Proteins ; Transcription Factors
Language	English
Publishing date	2007-11-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2077635-4
ISSN	1535-9786 ; 1535-9778
ISSN (online)	1535-9786
ISSN	1535-9778
DOI	10.1128/EC.00377-07
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Article ; Online: Cognate Site Identifier analysis reveals novel binding properties of the Sex Inducer homeodomain proteins of Cryptococcus neoformans.

Stanton, Brynne C / Giles, Steven S / Kruzel, Emilia K / Warren, Christopher L / Ansari, Aseem Z / Hull, Christina M

Molecular microbiology

2009 Volume 72, Issue 6, Page(s) 1334–1347

Abstract	Homeodomain proteins function in fungi to specify cell types and control sexual development. In the meningoencephalitis-causing fungal pathogen Cryptococcus neoformans, sexual development leads to the production of spores (suspected infectious particles). Sexual development is controlled by the homeodomain transcription factors Sxi1alpha and Sxi2a, but the mechanism by which they act is unknown. To understand how the Sxi proteins regulate development, we characterized their binding properties in vitro, showing that Sxi2a does not require a partner to bind DNA with high affinity. We then utilized a novel approach, Cognate Site Identifier (CSI) arrays, to define a comprehensive DNA-binding profile for Sxi2a, revealing a consensus sequence distinct from those of other fungal homeodomain proteins. Finally, we show that the homeodomains of both Sxi proteins are required for sexual development, a departure from related fungi. Our findings support a model in which Sxi1alpha and Sxi2a control sexual development in a homeodomain-dependent manner by binding to DNA sequences that differ from those defined in previously established fungal paradigms.
MeSH term(s)	Consensus Sequence ; Cryptococcus neoformans/genetics ; Cryptococcus neoformans/metabolism ; DNA, Fungal/genetics ; Electrophoretic Mobility Shift Assay ; Fungal Proteins/genetics ; Fungal Proteins/metabolism ; Gene Expression Regulation, Fungal ; Genetic Complementation Test ; Homeodomain Proteins/genetics ; Homeodomain Proteins/metabolism ; Mutagenesis, Site-Directed ; Oligonucleotide Array Sequence Analysis ; Protein Binding ; Substrate Specificity ; Transcription Factors/genetics ; Transcription Factors/metabolism
Chemical Substances	DNA, Fungal ; Fungal Proteins ; Homeodomain Proteins ; Transcription Factors
Language	English
Publishing date	2009-05-25
Publishing country	England
Document type	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.
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/j.1365-2958.2009.06719.x
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Article ; Online: Ribozyme-based insulator parts buffer synthetic circuits from genetic context.

Lou, Chunbo / Stanton, Brynne / Chen, Ying-Ja / Munsky, Brian / Voigt, Christopher A

Nature biotechnology

2012 Volume 30, Issue 11, Page(s) 1137–1142

Abstract: Synthetic genetic programs are built from circuits that integrate sensors and implement temporal control of gene expression. Transcriptional circuits are layered by using promoters to carry the signal between circuits. In other words, the output promoter ...

Abstract	Synthetic genetic programs are built from circuits that integrate sensors and implement temporal control of gene expression. Transcriptional circuits are layered by using promoters to carry the signal between circuits. In other words, the output promoter of one circuit serves as the input promoter to the next. Thus, connecting circuits requires physically connecting a promoter to the next circuit. We show that the sequence at the junction between the input promoter and circuit can affect the input-output response (transfer function) of the circuit. A library of putative sequences that might reduce (or buffer) such context effects, which we refer to as 'insulator parts', is screened in Escherichia coli. We find that ribozymes that cleave the 5' untranslated region (5'-UTR) of the mRNA are effective insulators. They generate quantitatively identical transfer functions, irrespective of the identity of the input promoter. When these insulators are used to join synthetic gene circuits, the behavior of layered circuits can be predicted using a mathematical model. The inclusion of insulators will be critical in reliably permuting circuits to build different programs.
MeSH term(s)	Computer Simulation ; Escherichia coli/genetics ; Gene Regulatory Networks/genetics ; Models, Genetic ; Promoter Regions, Genetic/genetics ; RNA, Catalytic/genetics ; Transcriptional Activation/genetics
Chemical Substances	RNA, Catalytic
Language	English
Publishing date	2012-10-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1311932-1
ISSN	1546-1696 ; 1087-0156
ISSN (online)	1546-1696
ISSN	1087-0156
DOI	10.1038/nbt.2401
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