General organisational principles of the transcriptional regulation system: a tree or a circle?

Recent advances of systemic approaches to gene expression and cellular metabolism provide unforeseen opportunities for relating and integrating extensive datasets describing the transcriptional regulation system as a whole. However, due to the multifaceted nature of the phenomenon, these datasets often contain logically distinct types of information determined by underlying approach and adopted methodology of data analysis. Consequently, to integrate the datasets comprising information on the states of chromatin structure, transcriptional regulatory network and cellular metabolism, a novel methodology enabling interconversion of logically distinct types of information is required. Here we provide a holistic conceptual framework for analysis of global transcriptional regulation as a system coordinated by structural coupling between the transcription machinery and DNA topology, acting as interdependent sensors and determinants of metabolic functions. In this operationally closed system any transition in physiological state represents an emergent property determined by shifts in structural coupling, whereas genetic regulation acts as a genuine device converting one logical type of information into the other.

[1]  A. Travers,et al.  FIS modulates growth phase‐dependent topological transitions of DNA in Escherichia coli , 1997, Molecular microbiology.

[2]  The gyr genes of Salmonella enterica serovar Typhimurium are repressed by the factor for inversion stimulation, Fis , 2003, Molecular Genetics and Genomics.

[3]  C. Dorman,et al.  Expression of the Fis protein is sustained in late‐exponential‐ and stationary‐phase cultures of Salmonella enterica serovar Typhimurium grown in the absence of aeration , 2007, Molecular microbiology.

[4]  G. Muskhelishvili,et al.  A systematic in vitro study of nucleoprotein complexes formed by bacterial nucleoid-associated proteins revealing novel types of DNA organization. , 2009, Journal of molecular biology.

[5]  Henri Buc,et al.  RNA polymerases as molecular motors , 2009 .

[6]  L. Hsieh,et al.  Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock , 1991, Journal of bacteriology.

[7]  R. T. Dame,et al.  The role of nucleoid‐associated proteins in the organization and compaction of bacterial chromatin , 2005, Molecular microbiology.

[8]  S. Altuvia,et al.  Differential regulation of Escherichia coli topoisomerase I by Fis , 2007, Molecular microbiology.

[9]  A. Travers,et al.  A common topology for bacterial and eukaryotic transcription initiation? , 2007, EMBO reports.

[10]  S Brunak,et al.  A DNA structural atlas for Escherichia coli. , 2000, Journal of molecular biology.

[11]  A. Emili,et al.  Interaction network containing conserved and essential protein complexes in Escherichia coli , 2005, Nature.

[12]  Andrew Travers,et al.  DNA supercoiling — a global transcriptional regulator for enterobacterial growth? , 2005, Nature Reviews Microbiology.

[13]  Regine Hengge,et al.  Differential ability of σs and σ70 of Escherichia coli to utilize promoters containing half or full UP‐element sites , 2004 .

[14]  R. J. Franco,et al.  Rifampin and rpoB mutations can alter DNA supercoiling in Escherichia coli , 1988, Journal of bacteriology.

[15]  M. Babu,et al.  High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes , 2007, Nucleic acids research.

[16]  Marc-Thorsten Hütt,et al.  Dissecting the logical types of network control in gene expression profiles , 2008, BMC Systems Biology.

[17]  R. Hengge-aronis,et al.  Role for the histone-like protein H-NS in growth phase-dependent and osmotic regulation of sigma S and many sigma S-dependent genes in Escherichia coli , 1995, Journal of bacteriology.

[18]  J. Collado-Vides,et al.  Conservation of DNA curvature signals in regulatory regions of prokaryotic genes. , 2003, Nucleic acids research.

[19]  A. Travers,et al.  RNA polymerase and an activator form discrete subcomplexes in a transcription initiation complex , 2006, The EMBO journal.

[20]  D. Lilley,et al.  Superhelical torsion in cellular DNA responds directly to environmental and genetic factors. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[21]  C. Calladine,et al.  Understanding DNA: The Molecule & How It Works , 1992 .

[22]  John von Neumann,et al.  The Computer and the Brain , 1960 .

[23]  C. D. Hardy,et al.  Topological domain structure of the Escherichia coli chromosome. , 2004, Genes & development.

[24]  Y. Tse‐Dinh,et al.  Direct Interaction between Escherichia coli RNA Polymerase and the Zinc Ribbon Domains of DNA Topoisomerase I* , 2003, Journal of Biological Chemistry.

[25]  N. Fujita,et al.  Promoter selectivity of Escherichia coli RNA polymerase E sigma 70 and E sigma 38 holoenzymes. Effect of DNA supercoiling. , 1996, The Journal of biological chemistry.

[26]  C. Dorman,et al.  Flexible response: DNA supercoiling, transcription and bacterial adaptation to environmental stress. , 1996, Trends in microbiology.

[27]  A. Travers,et al.  Conserved features of coordinately regulated E. coli promoters. , 1984, Nucleic acids research.

[28]  Anthony Wilden.  System and Structure: Essays in Communication and Exchange , 1972 .

[29]  T. Nyström,et al.  Negative regulation by RpoS: a case of sigma factor competition , 1998, Molecular microbiology.

[30]  T. Nyström,et al.  ppGpp: a global regulator in Escherichia coli. , 2005, Trends in microbiology.

[31]  G. Bateson,et al.  Mind and Nature: A Necessary Unity , 1979 .

[32]  A. Travers,et al.  A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli , 1999, Molecular microbiology.

[33]  R. Gourse,et al.  DksA Is Required for Growth Phase-Dependent Regulation, Growth Rate-Dependent Control, and Stringent Control of fis Expression in Escherichia coli , 2006, Journal of bacteriology.

[34]  A. Travers,et al.  DNA supercoiling and transcription in Escherichia coli: The FIS connection. , 2001, Biochimie.

[35]  A. Emili,et al.  Global Functional Atlas of Escherichia coli Encompassing Previously Uncharacterized Proteins , 2009, PLoS biology.

[36]  J. Gralla,et al.  Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli , 1987, Journal of bacteriology.

[37]  S. Busby,et al.  Selective repression by Fis and H‐NS at the Escherichia coli dps promoter , 2008, Molecular microbiology.

[38]  R. Hengge,et al.  The molecular basis of selective promoter activation by the σS subunit of RNA polymerase , 2007, Molecular microbiology.

[39]  A. Ishihama,et al.  Twelve Species of the Nucleoid-associated Protein from Escherichia coli , 1999, The Journal of Biological Chemistry.

[40]  V. Nagaraja,et al.  A complex of DNA gyrase and RNA polymerase fosters transcription in Mycobacterium smegmatis. , 2006, Biochemical and biophysical research communications.

[41]  A. Kolb,et al.  DNA supercoiling contributes to disconnect σS accumulation from σS‐dependent transcription in Escherichia coli , 2003 .

[42]  S. Adhya,et al.  Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[43]  R. Hengge-aronis,et al.  The Escherichia coli histone‐like protein HU regulates rpoS translation , 2001, Molecular microbiology.

[44]  M. Gerstein,et al.  Genomic analysis of regulatory network dynamics reveals large topological changes , 2004, Nature.

[45]  C. D. Hardy,et al.  A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure , 2005, Molecular microbiology.

[46]  R Kahmann,et al.  Regulation of crp transcription by oscillation between distinct nucleoprotein complexes , 1998, The EMBO journal.

[47]  S. Ueda,et al.  Growth Phase-Dependent Variation in Protein Composition of the Escherichia coli Nucleoid , 1999, Journal of bacteriology.

[48]  A. Travers,et al.  Coordination of genomic structure and transcription by the main bacterial nucleoid‐associated protein HU , 2010, EMBO reports.

[49]  I. Tessman,et al.  Regulation of DNA superhelicity by rpoB mutations that suppress defective Rho-mediated transcription termination in Escherichia coli , 1988, Journal of bacteriology.

[50]  S. Busby,et al.  Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome , 2006, Nucleic acids research.

[51]  G. W. Hatfield,et al.  DNA topology-mediated control of global gene expression in Escherichia coli. , 2002, Annual review of genetics.

[52]  S Brunak,et al.  Genome organisation and chromatin structure in Escherichia coli. , 2001, Biochimie.

[53]  Peter Ruhdal Jensen,et al.  DNA supercoiling in Escherichia coli is under tight and subtle homeostatic control, involving gene-expression and metabolic regulation of both topoisomerase I and DNA gyrase. , 2002, European journal of biochemistry.

[54]  A. Travers,et al.  The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA , 2000, Molecular microbiology.

[55]  H. Westerhoff,et al.  DNA supercoiling depends on the phosphorylation potential in Escherichia coli , 1996, Molecular microbiology.

[56]  Richard A Stein,et al.  Organization of supercoil domains and their reorganization by transcription , 2005, Molecular microbiology.

[57]  Anthony Maxwell,et al.  Energy coupling in type II topoisomerases: why do they hydrolyze ATP? , 2007, Biochemistry.

[58]  Charles J. Dorman,et al.  Bacterial DNA topology and infectious disease , 2008, Nucleic acids research.

[59]  W. McClure,et al.  Searching for and predicting the activity of sites for DNA binding proteins: compilation and analysis of the binding sites for Escherichia coli integration host factor (IHF). , 1990, Nucleic acids research.

[60]  K. Drlica,et al.  Cross-talk between topoisomerase I and HU in Escherichia coli. , 1996, Journal of molecular biology.

[61]  C. Dorman,et al.  Regulation of gene expression by histone-like proteins in bacteria. , 2003, Current opinion in genetics & development.

[62]  F. Leng,et al.  Transcription-coupled hypernegative supercoiling of plasmid DNA by T7 RNA polymerase in Escherichia coli topoisomerase I-deficient strains. , 2007, Journal of molecular biology.

[63]  T. Elliott,et al.  Fis Regulates Transcriptional Induction of RpoS in Salmonella enterica , 2005, Journal of bacteriology.

[64]  J. E. Cabrera,et al.  Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. , 2006, Journal of structural biology.

[65]  D. Jin,et al.  The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like "stringent" RNA polymerases in Escherichia coli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[66]  H. Bergson.  Time and Free Will , 1889 .

[67]  Marcel Geertz,et al.  Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome , 2006, EMBO reports.

[68]  Y. Tse‐Dinh,et al.  DNA supercoiling and bacterial adaptation: thermotolerance and thermoresistance. , 1997, Trends in microbiology.

[69]  Sarath Chandra Janga,et al.  Transcriptional regulation shapes the organization of genes on bacterial chromosomes , 2009, Nucleic acids research.

[70]  Malcolm Buckle,et al.  Mechanism of transcriptional activation by FIS: role of core promoter structure and DNA topology. , 2003, Journal of molecular biology.

[71]  M. Rossignol,et al.  Macrodomain organization of the Escherichia coli chromosome , 2004, The EMBO journal.

[72]  G. Bateson,et al.  Mind and Nature , 1980 .

[73]  K. Drlica,et al.  Histone-like protein HU and bacterial DNA topology: suppression of an HU deficiency by gyrase mutations. , 1996, Journal of molecular biology.

[74]  H. Choy,et al.  DNA looping-mediated repression by histone-like protein H-NS: specific requirement of Esigma70 as a cofactor for looping. , 2005, Genes & development.

[75]  A. Travers,et al.  DNA microloops and microdomains: a general mechanism for transcription activation by torsional transmission. , 1998, Journal of molecular biology.

[76]  Kathleen Marchal,et al.  The Condition‐Dependent Transcriptional Network in Escherichia coli , 2009, Annals of the New York Academy of Sciences.

[77]  D. Thieffry,et al.  Functional organisation of Escherichia coli transcriptional regulatory network , 2008, Journal of molecular biology.