-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Fis Protein Insulates the Gene from Uncontrolled Transcription
The Escherichia coli curved DNA binding protein A (CbpA) is a poorly characterised nucleoid associated factor and co-chaperone. It is expressed at high levels as cells enter stationary phase. Using genetics, biochemistry, and genomics, we have examined regulation of, and DNA binding by, CbpA. We show that Fis, the dominant growth-phase nucleoid protein, prevents CbpA expression in growing cells. Regulation by Fis involves an unusual “insulation” mechanism. Thus, Fis protects cbpA from the effects of a distal promoter, located in an adjacent gene. In stationary phase, when Fis levels are low, CbpA binds the E. coli chromosome with a preference for the intrinsically curved Ter macrodomain. Disruption of the cbpA gene prompts dramatic changes in DNA topology. Thus, our work identifies a novel role for Fis and incorporates CbpA into the growing network of factors that mediate bacterial chromosome structure.
Vyšlo v časopise: Fis Protein Insulates the Gene from Uncontrolled Transcription. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003152
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003152Souhrn
The Escherichia coli curved DNA binding protein A (CbpA) is a poorly characterised nucleoid associated factor and co-chaperone. It is expressed at high levels as cells enter stationary phase. Using genetics, biochemistry, and genomics, we have examined regulation of, and DNA binding by, CbpA. We show that Fis, the dominant growth-phase nucleoid protein, prevents CbpA expression in growing cells. Regulation by Fis involves an unusual “insulation” mechanism. Thus, Fis protects cbpA from the effects of a distal promoter, located in an adjacent gene. In stationary phase, when Fis levels are low, CbpA binds the E. coli chromosome with a preference for the intrinsically curved Ter macrodomain. Disruption of the cbpA gene prompts dramatic changes in DNA topology. Thus, our work identifies a novel role for Fis and incorporates CbpA into the growing network of factors that mediate bacterial chromosome structure.
Zdroje
1. DillonSC, DormanCJ (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8 : 185–195.
2. DormanCJ, BarrGC, Ni BhriainN, HigginsCF (1988) DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol 6 : 2816–2826.
3. SobetzkoP, TraversA, MuskhelishviliG (2012) Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc Natl Acad Sci 109: E42–E50.
4. AzamTA, IwataA, NishimuraA, UedaS, IshihamaA (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181 : 6361–6370.
5. AlmirónM, LinkAJ, FurlongD, KolterR (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6 : 2646–2654.
6. WolfSG, FrenkielD, AradT, FinkelSE, KolterR, et al. (1999) DNA protection by stress-induced biocrystallization. Nature 400 : 83–85.
7. CalhounLN, KwonYM (2011) Structure, function and regulation of the DNA-binding protein Dps and its role in acid and oxidative stress resistance in Escherichia coli: a review. J Appl Microbiol 110 : 375–386.
8. GraingerDC, GoldbergMD, LeeDJ, BusbySJ (2008) Selective repression by Fis and H-NS at the Escherichia coli dps promoter. Mol Microbiol 68 : 1366–1377.
9. UeguchiC, KakedaM, YamadaH, MizunoT (1994) An analogue of the DnaJ molecular chaperone in Escherichia coli. Proc Natl Acad Sci 91 : 1054–1058.
10. AzamTA, IshihamaA (1999) Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J Biol Chem 274 : 33105–33113.
11. BirdJG, SharmaS, RoshwalbSC, HoskinsJR, WicknerS (2006) Functional analysis of CbpA, a DnaJ homolog and nucleoid-associated DNA-binding protein. J Biol Chem 281 : 34349–34356.
12. ChintakayalaK, GraingerDC (2011) A conserved acidic amino acid mediates the interaction between modulators and co-chaperones in enterobacteria. J Mol Biol 411 : 313–320.
13. ChaeC, SharmaS, HoskinsJR, WicknerS (2004) CbpA, a DnaJ homolog, is a DnaK co-chaperone, and its activity is modulated by CbpM. J Biol Chem 279 : 33147–33153.
14. SarrafNS, BaardsnesJ, ChengJ, O'Connor-McCourtM, CyglerM, et al. (2010) Structural basis of the regulation of the CbpA co-chaperone by its specific modulator CbpM. J Mol Biol 398 : 111–121.
15. CosgriffS, ChintakayalaK, ChimYT, ChenX, AllenS, et al. (2010) Dimerization and DNA-dependent aggregation of the Escherichia coli nucleoid protein and chaperone CbpA. Mol Microbiol 77 : 1289–1300.
16. SinghSS, TypasA, HenggeR, GraingerDC (2011) Escherichia coli σ70 senses sequence and conformation of the promoter spacer region. Nucleic Acids Res 39 : 5109–5118.
17. AzamTA, HiragaS, IshihamaA (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid. Genes Cells 5 : 613–626.
18. BrowningDF, ColeJA, BusbySJ (2004) Transcription activation by remodelling of a nucleoprotein assembly: the role of NarL at the FNR-dependent Escherichia coli nir promoter. Mol Microbiol 53 : 203–215.
19. HengenPN, BartramSL, StewartLE, SchneiderTD (1997) Information analysis of Fis binding sites. Nucleic Acids Res 25 : 4994–5002.
20. HirvonenCA, RossW, WozniakCE, MarascoE, AnthonyJR, et al. (2001) Contributions of UP elements and the transcription factor FIS to expression from the seven rrn P1 promoters in Escherichia coli. J Bacteriol 183 : 6305–6314.
21. ShaoY, Feldman-CohenLS, OsunaR (2008) Functional characterisation of the Escherichia coli Fis-DNA binding sequence. J Mol Biol 376 : 771–785.
22. GraingerDC, HurdD, GoldbergMD, BusbySJ (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34 : 4642–4652.
23. ChoBK, KnightEM, BarrettCL, PalssonBØ (2008) Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res 18 : 900–910.
24. KahramanoglouC, SeshasayeeAS, PrietoAI, IbbersonD, SchmidtS, et al. (2011) Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res 39 : 2073–2091.
25. AtteyA, BelyaevaT, SaveryN, HoggettJ, FujitaN, et al. (1994) Interactions between the cyclic AMP receptor protein and the alpha subunit of RNA polymerase at the Escherichia coli galactose operon P1 promoter. Nucleic Acids Res 22 : 4375–4380.
26. XuM, BusbySJ, BrowningDF (2009) Activation and repression at the Escherichia coli ynfEFGHI operon promoter. J Bacteriol 191 : 3172–3176.
27. SquireDJ, XuM, ColeJA, BusbySJ, BrowningDF (2009) Competition between NarL-dependent activation and Fis-dependent repression controls expression from the Escherichia coli yeaR and ogt promoters. Biochem J 420 : 249–257.
28. HollandsK, LeeDJ, LloydGS, BusbySJ (2010) Activation of sigma 28-dependent transcription in Escherichia coli by the cyclic AMP receptor protein requires an unusual promoter organization. Mol Microbiol 75 : 1098–1111.
29. PedersenAG, JensenLJ, BrunakS, StaerfeldtHH, UsseryDW (2000) A DNA structural atlas for Escherichia coli. J Mol Biol 299 : 907–930.
30. ConterA (2003) Plasmid DNA supercoiling and survival in long-term cultures of Escherichia coli: role of NaCl. J Bacteriol 185 : 5324–5327.
31. ConterA, MenchonC, GutierrezC (1997) Role of DNA supercoiling and rpoS sigma factor in the osmotic and growth phase-dependent induction of the gene osmE of Escherichia coli K12. J Mol Biol 273 : 75–83.
32. YamashinoT, KakedaM, UeguchiC, MizunoT (1994) An analogue of the DnaJ molecular chaperone whose expression is controlled by σS during the stationary phase and phosphate starvation in Escherichia coli. Mol Microbiol 13 : 475–483.
33. DornenburgJE, DevitaAM, PalumboMJ, WadeJT (2010) Widespread antisense transcription in Escherichia coli. mBio 1(1): e00024–10 doi:10.1128/mBio.00024-10.
34. SharmaCM, HoffmannS, DarfeuilleF, ReignierJ, FindeissS, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464 : 250–255.
35. KawanoM, StorzG, RaoBS, RosnerJL, MartinRG (2005) Detection of low-level promoter activity within open reading frame sequences of Escherichia coli. Nucleic Acids Res 33 : 6268–6276.
36. OhniwaRL, MorikawaK, KimJ, OhtaT, IshihamaA, et al. (2006) Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J 25 : 5591–5602.
37. Miller J (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
38. LloydGS, HollandsK, GodfreyRE, BusbySJ (2008) Transcription initiation in the Escherichia coli K-12 malI-malX intergenic region and the role of the cyclic AMP receptor protein. FEMS Microbiol Lett 288 : 250–7.
39. KolbA, KotlarzD, KusanoS, IshihamaA (1995) Selectivity of the Escherichia coli RNA polymerase E sigma 38 for overlapping promoters and ability to support CRP activation. Nucleic Acids Res 23 : 819–826.
40. GraingerDC, OvertonTW, ReppasN, WadeJT, TamaiE, et al. (2004) Genomic studies with Escherichia coli MelR protein: applications of chromatin immunoprecipitation and microarrays. J Bacteriol 186 : 6938–6943.
41. CarverT, ThomsonN, BleasbyA, BerrimanM, ParkhillJ (2009) DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25 : 119–120.
42. ShpigelmanES, TrifonovEN, BolshoyA (1993) CURVATURE: software for the analysis of curved DNA. Comput Appl Biosci 9 : 435–440.
43. BallCA, OsunaR, FergusonKC, JohnsonRC (1992) Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli.. J Bacteriol 174 : 8043–8056.
Štítky
Genetika Reprodukčná medicína
Článek Comparative Genome Structure, Secondary Metabolite, and Effector Coding Capacity across PathogensČlánek TATES: Efficient Multivariate Genotype-Phenotype Analysis for Genome-Wide Association StudiesČlánek Secondary Metabolism and Development Is Mediated by LlmF Control of VeA Subcellular Localization inČlánek Human Disease-Associated Genetic Variation Impacts Large Intergenic Non-Coding RNA ExpressionČlánek The Roles of Whole-Genome and Small-Scale Duplications in the Functional Specialization of GenesČlánek The Role of Autophagy in Genome Stability through Suppression of Abnormal Mitosis under Starvation
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2013 Číslo 1- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- A Model of High Sugar Diet-Induced Cardiomyopathy
- Comparative Genome Structure, Secondary Metabolite, and Effector Coding Capacity across Pathogens
- Emerging Function of Fat Mass and Obesity-Associated Protein (Fto)
- Positional Cloning Reveals Strain-Dependent Expression of to Alter Susceptibility to Bleomycin-Induced Pulmonary Fibrosis in Mice
- Genetics of Ribosomal Proteins: “Curiouser and Curiouser”
- Transposable Elements Re-Wire and Fine-Tune the Transcriptome
- Function and Regulation of , a Gene Implicated in Autism and Human Evolution
- MAML1 Enhances the Transcriptional Activity of Runx2 and Plays a Role in Bone Development
- Predicting Mendelian Disease-Causing Non-Synonymous Single Nucleotide Variants in Exome Sequencing Studies
- A Systematic Mapping Approach of 16q12.2/ and BMI in More Than 20,000 African Americans Narrows in on the Underlying Functional Variation: Results from the Population Architecture using Genomics and Epidemiology (PAGE) Study
- Transcription of the Major microRNA–Like Small RNAs Relies on RNA Polymerase III
- Histone H3K56 Acetylation, Rad52, and Non-DNA Repair Factors Control Double-Strand Break Repair Choice with the Sister Chromatid
- Genome-Wide Association Study Identifies a Novel Susceptibility Locus at 12q23.1 for Lung Squamous Cell Carcinoma in Han Chinese
- Genetic Disruption of the Copulatory Plug in Mice Leads to Severely Reduced Fertility
- The [] Prion Exists as a Dynamic Cloud of Variants
- Adult Onset Global Loss of the Gene Alters Body Composition and Metabolism in the Mouse
- Fis Protein Insulates the Gene from Uncontrolled Transcription
- The Meiotic Nuclear Lamina Regulates Chromosome Dynamics and Promotes Efficient Homologous Recombination in the Mouse
- Genome-Wide Haplotype Analysis of Expression Quantitative Trait Loci in Monocytes
- TATES: Efficient Multivariate Genotype-Phenotype Analysis for Genome-Wide Association Studies
- Structural Basis of a Histone H3 Lysine 4 Demethylase Required for Stem Elongation in Rice
- The Ecm11-Gmc2 Complex Promotes Synaptonemal Complex Formation through Assembly of Transverse Filaments in Budding Yeast
- MCM8 Is Required for a Pathway of Meiotic Double-Strand Break Repair Independent of DMC1 in
- Comparative Genomic Analysis of the Endosymbionts of Herbivorous Insects Reveals Eco-Environmental Adaptations: Biotechnology Applications
- Integration of Nodal and BMP Signals in the Heart Requires FoxH1 to Create Left–Right Differences in Cell Migration Rates That Direct Cardiac Asymmetry
- Pharmacodynamics, Population Dynamics, and the Evolution of Persistence in
- A Hybrid Likelihood Model for Sequence-Based Disease Association Studies
- Aberration in DNA Methylation in B-Cell Lymphomas Has a Complex Origin and Increases with Disease Severity
- Multiple Opposing Constraints Govern Chromosome Interactions during Meiosis
- Transcriptional Dynamics Elicited by a Short Pulse of Notch Activation Involves Feed-Forward Regulation by Genes
- Dynamic Large-Scale Chromosomal Rearrangements Fuel Rapid Adaptation in Yeast Populations
- Heterologous Gln/Asn-Rich Proteins Impede the Propagation of Yeast Prions by Altering Chaperone Availability
- Gene Copy-Number Polymorphism Caused by Retrotransposition in Humans
- An Incompatibility between a Mitochondrial tRNA and Its Nuclear-Encoded tRNA Synthetase Compromises Development and Fitness in
- Secondary Metabolism and Development Is Mediated by LlmF Control of VeA Subcellular Localization in
- Single-Stranded Annealing Induced by Re-Initiation of Replication Origins Provides a Novel and Efficient Mechanism for Generating Copy Number Expansion via Non-Allelic Homologous Recombination
- Tbx2 Controls Lung Growth by Direct Repression of the Cell Cycle Inhibitor Genes and
- Suv4-20h Histone Methyltransferases Promote Neuroectodermal Differentiation by Silencing the Pluripotency-Associated Oct-25 Gene
- A Conserved Helicase Processivity Factor Is Needed for Conjugation and Replication of an Integrative and Conjugative Element
- Telomerase-Null Survivor Screening Identifies Novel Telomere Recombination Regulators
- Genome-Wide Analysis Reveals Selection for Important Traits in Domestic Horse Breeds
- Coordinated Degradation of Replisome Components Ensures Genome Stability upon Replication Stress in the Absence of the Replication Fork Protection Complex
- Nkx6.1 Controls a Gene Regulatory Network Required for Establishing and Maintaining Pancreatic Beta Cell Identity
- HIF- and Non-HIF-Regulated Hypoxic Responses Require the Estrogen-Related Receptor in
- Delineating a Conserved Genetic Cassette Promoting Outgrowth of Body Appendages
- The Telomere Capping Complex CST Has an Unusual Stoichiometry, Makes Multipartite Interaction with G-Tails, and Unfolds Higher-Order G-Tail Structures
- Comprehensive Methylome Characterization of and at Single-Base Resolution
- Loci Associated with -Glycosylation of Human Immunoglobulin G Show Pleiotropy with Autoimmune Diseases and Haematological Cancers
- Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol
- Centromere-Like Regions in the Budding Yeast Genome
- Sequencing of Loci from the Elephant Shark Reveals a Family of Genes in Vertebrate Genomes, Forged by Ancient Duplications and Divergences
- Mendelian and Non-Mendelian Regulation of Gene Expression in Maize
- Mutational Spectrum Drives the Rise of Mutator Bacteria
- Human Disease-Associated Genetic Variation Impacts Large Intergenic Non-Coding RNA Expression
- The Roles of Whole-Genome and Small-Scale Duplications in the Functional Specialization of Genes
- Sex-Specific Signaling in the Blood–Brain Barrier Is Required for Male Courtship in
- A Newly Uncovered Group of Distantly Related Lysine Methyltransferases Preferentially Interact with Molecular Chaperones to Regulate Their Activity
- Is Required for Leptin-Mediated Depolarization of POMC Neurons in the Hypothalamic Arcuate Nucleus in Mice
- Unlocking the Bottleneck in Forward Genetics Using Whole-Genome Sequencing and Identity by Descent to Isolate Causative Mutations
- The Role of Autophagy in Genome Stability through Suppression of Abnormal Mitosis under Starvation
- MTERF3 Regulates Mitochondrial Ribosome Biogenesis in Invertebrates and Mammals
- Downregulation and Altered Splicing by in a Mouse Model of Facioscapulohumeral Muscular Dystrophy (FSHD)
- NBR1-Mediated Selective Autophagy Targets Insoluble Ubiquitinated Protein Aggregates in Plant Stress Responses
- Retroactive Maintains Cuticle Integrity by Promoting the Trafficking of Knickkopf into the Procuticle of
- Phenome-Wide Association Study (PheWAS) for Detection of Pleiotropy within the Population Architecture using Genomics and Epidemiology (PAGE) Network
- Genetic and Functional Modularity of Activities in the Specification of Limb-Innervating Motor Neurons
- A Population Genetic Model for the Maintenance of R2 Retrotransposons in rRNA Gene Loci
- A Quartet of PIF bHLH Factors Provides a Transcriptionally Centered Signaling Hub That Regulates Seedling Morphogenesis through Differential Expression-Patterning of Shared Target Genes in
- A Genome-Wide Integrative Genomic Study Localizes Genetic Factors Influencing Antibodies against Epstein-Barr Virus Nuclear Antigen 1 (EBNA-1)
- Mutation of the Diamond-Blackfan Anemia Gene in Mouse Results in Morphological and Neuroanatomical Phenotypes
- Life, the Universe, and Everything: An Interview with David Haussler
- Alternative Oxidase Expression in the Mouse Enables Bypassing Cytochrome Oxidase Blockade and Limits Mitochondrial ROS Overproduction
- An Evolutionarily Conserved Synthetic Lethal Interaction Network Identifies FEN1 as a Broad-Spectrum Target for Anticancer Therapeutic Development
- The Flowering Repressor Underlies a Novel QTL Interacting with the Genetic Background
- Telomerase Is Required for Zebrafish Lifespan
- and Diversified Expression of the Gene Family Bolster the Floral Stem Cell Network
- Susceptibility Loci Associated with Specific and Shared Subtypes of Lymphoid Malignancies
- An Insertion in 5′ Flanking Region of Causes Blue Eggshell in the Chicken
- Increased Maternal Genome Dosage Bypasses the Requirement of the FIS Polycomb Repressive Complex 2 in Arabidopsis Seed Development
- WNK1/HSN2 Mutation in Human Peripheral Neuropathy Deregulates Expression and Posterior Lateral Line Development in Zebrafish ()
- Synergistic Interaction of Rnf8 and p53 in the Protection against Genomic Instability and Tumorigenesis
- Dot1-Dependent Histone H3K79 Methylation Promotes Activation of the Mek1 Meiotic Checkpoint Effector Kinase by Regulating the Hop1 Adaptor
- A Heterogeneous Mixture of F-Series Prostaglandins Promotes Sperm Guidance in the Reproductive Tract
- Starvation, Together with the SOS Response, Mediates High Biofilm-Specific Tolerance to the Fluoroquinolone Ofloxacin
- Directed Evolution of a Model Primordial Enzyme Provides Insights into the Development of the Genetic Code
- Genome-Wide Screens for Tinman Binding Sites Identify Cardiac Enhancers with Diverse Functional Architectures
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Function and Regulation of , a Gene Implicated in Autism and Human Evolution
- An Insertion in 5′ Flanking Region of Causes Blue Eggshell in the Chicken
- Comprehensive Methylome Characterization of and at Single-Base Resolution
- Susceptibility Loci Associated with Specific and Shared Subtypes of Lymphoid Malignancies
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy