The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective.

The bacterial genome is folded into a compact structure called the nucleoid. Considerable compaction of the DNA molecule is required in order to reduce its volume below that of the cell. Several mechanisms, such as molecular crowding and DNA supercoiling contribute to the compactness of the nucleoid. Besides these mechanisms, a number of architectural proteins associate with the chromosomal DNA and cause it to fold into a compact structure by bridging, bending or wrapping DNA. In this review, we provide an overview of the major nucleoid-associated proteins from a structural perspective and we discuss their possible roles in dynamically shaping the bacterial nucleoid.

[1]  Leroy F. Liu,et al.  Transcription generates positively and negatively supercoiled domains in the template , 1988, Cell.

[2]  P. Graumann.  SMC proteins in bacteria: condensation motors for chromosome segregation? , 2001, Biochimie.

[3]  N. Friedman,et al.  Modulation of DNA conformations through the formation of alternative high-order HU-DNA complexes. , 2004, Journal of molecular biology.

[4]  Reid C. Johnson,et al.  DNA Looping by Saccharomyces cerevisiae High Mobility Group Proteins NHP6A/B , 1995, The Journal of Biological Chemistry.

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

[6]  T. Yamazaki,et al.  Identification of the DNA binding surface of H‐NS protein from Escherichia coli by heteronuclear NMR spectroscopy , 1999, FEBS letters.

[7]  Jasper Akerboom,et al.  Structural insight into gene transcriptional regulation and effector binding by the Lrp/AsnC family , 2006, Nucleic acids research.

[8]  T. Hirano,et al.  Dynamic molecular linkers of the genome: the first decade of SMC proteins. , 2005, Genes & development.

[9]  C. Gualerzi,et al.  Lethal overproduction of the Escherichia coli nucleoid protein H-NS: ultramicroscopic and molecular autopsy , 2004, Molecular and General Genetics MGG.

[10]  H. Niki,et al.  Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli , 1999, The EMBO journal.

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

[12]  Ying Zhang,et al.  Flexible DNA bending in HU–DNA cocrystal structures , 2003, The EMBO journal.

[13]  J. Calvo,et al.  The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli , 1994, Microbiological reviews.

[14]  J. Geiselmann,et al.  In vivo interaction of the Escherichia coli integration host factor with its specific binding sites. , 1995, Nucleic acids research.

[15]  C. Wyman,et al.  H-NS mediated compaction of DNA visualised by atomic force microscopy. , 2000, Nucleic acids research.

[16]  C. Dorman.  H-NS: a universal regulator for a dynamic genome , 2004, Nature Reviews Microbiology.

[17]  R. C. Johnson,et al.  Variable structures of Fis-DNA complexes determined by flanking DNA-protein contacts. , 1996, Journal of molecular biology.

[18]  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.

[19]  G. Bullerjahn,et al.  The DpsA Protein of Synechococcus sp. Strain PCC7942 Is a DNA-binding Hemoprotein , 1995, The Journal of Biological Chemistry.

[20]  A. Strunnikov.  SMC complexes in bacterial chromosome condensation and segregation. , 2006, Plasmid.

[21]  D. Pettijohn,et al.  Supercoils in prokaryotic DNA restrained in vivo. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Thijs J. G. Ettema,et al.  The Lrp family of transcriptional regulators , 2003, Molecular microbiology.

[23]  C. Bustamante,et al.  Wrapping of DNA around the E.coli RNA polymerase open promoter complex , 1999, The EMBO journal.

[24]  F. Imamoto,et al.  Requirement of integration host factor (IHF) for growth of Escherichia coli deficient in HU protein. , 1990, Gene.

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

[26]  Reid C. Johnson,et al.  Major Nucleoid Proteins in the Structure and Function of the Escherichia coli Chromosome , 2005 .

[27]  R. Kolter,et al.  DNA protection by stress-induced biocrystallization , 1999, Nature.

[28]  S. Wolf,et al.  Nucleoid restructuring in stationary‐state bacteria , 2004, Molecular microbiology.

[29]  W. D. de Vos,et al.  Crystal structure of the Lrp‐like transcriptional regulator from the archaeon Pyrococcus furiosus , 2001, The EMBO journal.

[30]  C. Pon,et al.  Proteins from the prokaryotic nucleoid: primary and quaternary structure of the 15‐kD Escherichia coli DNA binding protein H‐NS , 1988, Molecular microbiology.

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

[32]  C. Wyman,et al.  Structural basis for preferential binding of H-NS to curved DNA. , 2001, Biochimie.

[33]  T. Mizuno,et al.  Solution structure of the DNA binding domain of a nucleoid‐associated protein, H‐NS, from Escherichia coli , 1995, FEBS letters.

[34]  R. Stein,et al.  Domain Behavior and Supercoil Dynamics in Bacterial Chromosomes , 2005 .

[35]  E. Chiancone,et al.  DNA condensation and self-aggregation of Escherichia coli Dps are coupled phenomena related to the properties of the N-terminus. , 2004, Nucleic acids research.

[36]  C. Higgins,et al.  Oligomerization of the chromatin‐structuring protein H‐NS , 2000, Molecular microbiology.

[37]  A. Travers,et al.  An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. , 2001, Nucleic acids research.

[38]  E. Shimoni,et al.  Stress, order and survival , 2002, Nature Reviews Molecular Cell Biology.

[39]  C. Higgins,et al.  H-NS oligomerization domain structure reveals the mechanism for high order self-association of the intact protein. , 2002, Journal of molecular biology.

[40]  K. Nasmyth,et al.  The structure and function of SMC and kleisin complexes. , 2005, Annual review of biochemistry.

[41]  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.

[42]  N. Higgins.  The bacterial chromosome , 2005 .

[43]  Cees Dekker,et al.  Dual architectural roles of HU: formation of flexible hinges and rigid filaments. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  K. Drlica,et al.  Histonelike proteins of bacteria. , 1987, Microbiological reviews.

[45]  K. Swinger,et al.  IHF and HU: flexible architects of bent DNA. , 2004, Current opinion in structural biology.

[46]  E. Le Cam,et al.  Contribution of DNA Conformation and Topology in Right-handed DNA Wrapping by the Bacillus subtilis LrpC Protein* , 2003, The Journal of Biological Chemistry.

[47]  John A. Tainer,et al.  Structural Biology of Rad50 ATPase ATP-Driven Conformational Control in DNA Double-Strand Break Repair and the ABC-ATPase Superfamily , 2000, Cell.

[48]  K. Hopfner,et al.  Structural Biochemistry of ATP-Driven Dimerization and DNA-Stimulated Activation of SMC ATPases , 2004, Current Biology.

[49]  A. Grossman,et al.  Characterization of a prokaryotic SMC protein involved in chromosome partitioning. , 1998, Genes & development.

[50]  H. Craighead,et al.  An Lrp-type transcriptional regulator from Agrobacterium tumefaciens condenses more than 100 nucleotides of DNA into globular nucleoprotein complexes. , 1999, Journal of molecular biology.

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

[52]  H. Buc,et al.  The Degree of Oligomerization of the H-NS Nucleoid Structuring Protein Is Related to Specific Binding to DNA* , 2002, The Journal of Biological Chemistry.

[53]  H. D. Ulrich,et al.  A Prokaryotic Condensin/Cohesin-Like Complex Can Actively Compact Chromosomes from a Single Position on the Nucleoid and Binds to DNA as a Ring-Like Structure , 2003, Molecular and Cellular Biology.

[54]  Reid C. Johnson,et al.  Low-force DNA condensation and discontinuous high-force decondensation reveal a loop-stabilizing function of the protein Fis. , 2005, Physical review letters.

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

[56]  F. Imamoto,et al.  Role of HU proteins in forming and constraining supercoils of chromosomal DNA inEscherichia coli , 1995, Molecular and General Genetics MGG.

[57]  S. Diekmann,et al.  Global structure similarities of intact and nicked DNA complexed with IHF measured in solution by fluorescence resonance energy transfer. , 1999, Nucleic acids research.

[58]  O. Gileadi,et al.  Compaction of single DNA molecules induced by binding of integration host factor (IHF) , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. Hirano,et al.  Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interactions. , 2006, Molecular cell.

[60]  H. Nash,et al.  Comparison of protein binding to DNA in vivo and in vitro: defining an effective intracellular target. , 1995, The EMBO journal.

[61]  D. Ussery,et al.  DNA Binding Is Not Sufficient for H-NS-mediated Repression ofproU Expression* , 1997, The Journal of Biological Chemistry.

[62]  M. Yaniv,et al.  E. coli DNA binding protein HU forms nucleosome-like structure with circular double-stranded DNA , 1979, Cell.

[63]  H. Erickson,et al.  The Symmetrical Structure of Structural Maintenance of Chromosomes (SMC) and MukB Proteins: Long, Antiparallel Coiled Coils, Folded at a Flexible Hinge , 1998, The Journal of cell biology.

[64]  T. Hirano,et al.  Positive and negative regulation of SMC–DNA interactions by ATP and accessory proteins , 2004, The EMBO journal.

[65]  Martijn S. Luijsterburg,et al.  DNA Bridging: a Property Shared among H-NS-Like Proteins , 2005, Journal of bacteriology.

[66]  D. Crothers,et al.  Concerted binding and bending of DNA by Escherichia coli integration host factor. , 2002, Journal of molecular biology.

[67]  M. Simon,et al.  Host protein requirements for in vitro site-specific DNA inversion , 1986, Cell.

[68]  A. Grossman,et al.  Structural Maintenance of Chromosomes Protein of Bacillussubtilis Affects Supercoiling In Vivo , 2002, Journal of bacteriology.

[69]  P. Graumann,et al.  Dynamic assembly, localization and proteolysis of the Bacillus subtilis SMC complex , 2005, BMC Cell Biology.

[70]  J. Löwe,et al.  Distribution of the Escherichia coli structural maintenance of chromosomes (SMC)‐like protein MukB in the cell , 2001, Molecular microbiology.

[71]  Phoebe A Rice,et al.  Crystal Structure of an IHF-DNA Complex: A Protein-Induced DNA U-Turn , 1996, Cell.

[72]  E. Margeat,et al.  The H-NS dimerization domain defines a new fold contributing to DNA recognition , 2003, Nature Structural Biology.

[73]  G D Stormo,et al.  A consensus sequence for binding of Lrp to DNA , 1995, Journal of bacteriology.

[74]  R. Dame,et al.  HU: promoting or counteracting DNA compaction? , 2002, FEBS letters.

[75]  R. C. Johnson,et al.  The nonspecific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. , 1993, Genes & development.

[76]  R. Kolter,et al.  The crystal structure of Dps, a ferritin homolog that binds and protects DNA , 1998, Nature Structural Biology.