Giant proteins that move DNA: bullies of the genomic playground

As genetic material DNA is wonderful, but as a macromolecule it is unruly, voluminous and fragile. Without the action of DNA replicases, topoisomerases, helicases, translocases and recombinases, the genome would collapse into a topologically entangled random coil that would be useless to the cell. We discuss the organization, movement and energetics of these proteins that are crucial to the preservation of a molecule that has such beautiful biological but challenging physical properties.

[1]  A. Grossman,et al.  Movement of replicating DNA through a stationary replisome. , 2000, Molecular cell.

[2]  G. Orphanides,et al.  Evidence for a conformational change in the DNA gyrase-DNA complex from hydroxyl radical footprinting. , 1994, Nucleic acids research.

[3]  A. Varshavsky,et al.  Arrest of segregation leads to accumulation of highly intertwined catenated dimers: Dissection of the final stages of SV40 DNA replication , 1981, Cell.

[4]  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.

[5]  J. Wang,et al.  Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. , 2000, Science.

[6]  Cees Dekker,et al.  Real-time observation of DNA translocation by the type I restriction modification enzyme EcoR124I , 2004, Nature Structural &Molecular Biology.

[7]  B. Tye.  MCM proteins in DNA replication. , 1999, Annual review of biochemistry.

[8]  T. Harkins,et al.  Pre-steady-state analysis of ATP hydrolysis by Saccharomyces cerevisiae DNA topoisomerase II. 2. Kinetic mechanism for the sequential hydrolysis of two ATP. , 1998, Biochemistry.

[9]  P. Brown,et al.  A sign inversion mechanism for enzymatic supercoiling of DNA. , 1979, Science.

[10]  M. Sheetz,et al.  Transcription by single molecules of RNA polymerase observed by light microscopy , 1991, Nature.

[11]  J. Champoux.  DNA topoisomerases: structure, function, and mechanism. , 2001, Annual review of biochemistry.

[12]  J. Lindsley,et al.  Yeast Topoisomerase II Is Inhibited by Etoposide After Hydrolyzing the First ATP and Before Releasing the Second ADP* , 1999, The Journal of Biological Chemistry.

[13]  J. Errington,et al.  Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. , 1999, Molecular cell.

[14]  A. Worcel,et al.  On the structure of the folded chromosome of Escherichia coli. , 1972, Journal of molecular biology.

[15]  R. B. Jensen,et al.  A moving DNA replication factory in Caulobacter crescentus , 2001, The EMBO journal.

[16]  Michael D. Stone,et al.  Mechanochemical analysis of DNA gyrase using rotor bead tracking , 2006, Nature.

[17]  B. Strauss,et al.  A model for replication repair in mammalian cells. , 1976, Journal of molecular biology.

[18]  N. Cozzarelli,et al.  Closing the ring: links between SMC proteins and chromosome partitioning, condensation, and supercoiling. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Sherratt,et al.  Spatial and temporal organization of replicating Escherichia coli chromosomes , 2003, Molecular microbiology.

[20]  N. Cozzarelli,et al.  Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Omar A Saleh,et al.  Analysis of DNA supercoil induction by FtsK indicates translocation without groove-tracking , 2005, Nature Structural &Molecular Biology.

[22]  N. Friedman,et al.  Stochastic protein expression in individual cells at the single molecule level , 2006, Nature.

[23]  H. Smith,et al.  Mechanism of DNA degradation by the ATP-dependent DNase from Hemophilus influenzae Rd. , 1976, The Journal of biological chemistry.

[24]  X. Xie,et al.  Probing Gene Expression in Live Cells, One Protein Molecule at a Time , 2006, Science.

[25]  W. Donachie,et al.  FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli , 1998, Molecular microbiology.

[26]  Jeff Gore,et al.  Sequence-Directed DNA Translocation by Purified FtsK , 2005, Science.

[27]  S. Bell,et al.  ATPase switches controlling DNA replication initiation. , 2000, Current opinion in cell biology.

[28]  K. Pogliano,et al.  Role of Cell-Specific SpoIIIE Assembly in Polarity of DNA Transfer , 2002, Science.

[29]  P. Hanawalt,et al.  Title Evolution of the SNF 2 family of proteins : Subfamilies with distinct sequences and functions Permalink , 2022 .

[30]  Tania A. Baker,et al.  Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines , 2005, Nature.

[31]  S. Ben-Yehuda,et al.  A Checkpoint Protein That Scans the Chromosome for Damage at the Start of Sporulation in Bacillus subtilis , 2006, Cell.

[32]  R. Losick,et al.  Does RNA polymerase help drive chromosome segregation in bacteria? , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  James H. White.  Self-Linking and the Gauss Integral in Higher Dimensions , 1969 .

[34]  E. Schrödinger.  What Is Life , 1946 .

[35]  Meriem El Karoui,et al.  KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase , 2005, The EMBO journal.

[36]  S. Halford,et al.  Measurement of the contributions of 1D and 3D pathways to the translocation of a protein along DNA. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Nicholas R. Cozzarelli,et al.  DNA topology and its biological effects , 1990 .

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

[39]  S. Rimsky.  Structure of the histone-like protein H-NS and its role in regulation and genome superstructure. , 2004, Current opinion in microbiology.

[40]  N. Cozzarelli,et al.  Simplification of DNA topology below equilibrium values by type II topoisomerases. , 1997, Science.

[41]  D. Dunlap,et al.  Direct observation of DNA distortion by the RSC complex. , 2006, Molecular cell.

[42]  Michael D. Stone,et al.  Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. Wang,et al.  Supercoiling of the DNA template during transcription. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[44]  M. Kirschner,et al.  Dynamic instability of microtubule growth , 1984, Nature.

[45]  M. O’Donnell,et al.  Cellular DNA replicases: components and dynamics at the replication fork. , 2005, Annual review of biochemistry.

[46]  Michael D. Stone,et al.  Structural transitions and elasticity from torque measurements on DNA , 2003, Nature.

[47]  W. Jencks,et al.  Binding energy, specificity, and enzymic catalysis: the circe effect. , 2006, Advances in enzymology and related areas of molecular biology.

[48]  R. Fuchs,et al.  Uncoupling of Leading- and Lagging-Strand DNA Replication During Lesion Bypass in Vivo , 2003, Science.

[49]  W. Margolin,et al.  Localization of Cell Division Protein FtsK to theEscherichia coli Septum and Identification of a Potential N-Terminal Targeting Domain , 1998, Journal of bacteriology.

[50]  S. M. Sullivan,et al.  Bacterial sporulation: Pole-to-pole protein oscillation , 2000, Current Biology.

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

[52]  R. Losick,et al.  Assembly of the SpoIIIE DNA Translocase Depends on Chromosome Trapping in Bacillus subtilis , 2003, Current Biology.

[53]  G. Călugăreanu.  Sur les classes d'isotopie des noeuds tridimensionnels et leurs invariants , 1961 .

[54]  D. Sherratt,et al.  Asymmetric activation of Xer site‐specific recombination by FtsK , 2004, EMBO reports.

[55]  David Keller,et al.  Single-molecule studies of the effect of template tension on T7 DNA polymerase activity , 2000, Nature.

[56]  D. Sherratt,et al.  Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12 , 1993, Cell.

[57]  N. Cozzarelli,et al.  Independence of replisomes in Escherichia coli chromosomal replication. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[58]  A. Grossman,et al.  Control of Sporulation Gene Expression in Bacillus subtilis by the Chromosome Partitioning Proteins Soj (ParA) and Spo0J (ParB) , 2000, Journal of bacteriology.

[59]  J. Errington,et al.  Compartmentalization of transcription and translation in Bacillus subtilis , 2000, The EMBO journal.

[60]  Christian Lesterlin,et al.  A dual role for the FtsK protein in Escherichia coli chromosome segregation , 2002, EMBO reports.

[61]  J. Errington,et al.  Septal localization of the SpoIIIE chromosome partitioning protein in Bacillus subtilis , 1997, The EMBO journal.

[62]  JAMES C. Wang,et al.  Cellular roles of DNA topoisomerases: a molecular perspective , 2002, Nature Reviews Molecular Cell Biology.

[63]  Hiroyasu Itoh,et al.  Direct observation of DNA rotation during transcription by Escherichia coli RNA polymerase , 2001, Nature.

[64]  J. E. Cabrera,et al.  The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues , 2003, Molecular microbiology.

[65]  Robert Landick,et al.  RNA Polymerase as a Molecular Motor , 1998, Cell.

[66]  N. Cozzarelli,et al.  Preferential relaxation of positively supercoiled DNA by E. coli topoisomerase IV in single-molecule and ensemble measurements. , 2000, Genes & development.

[67]  N. Cozzarelli,et al.  Positive Torsional Strain Causes the Formation of a Four-way Junction at Replication Forks* , 2001, The Journal of Biological Chemistry.

[68]  A. Alexeev,et al.  A Novel Function of Rad54 Protein , 2003, The Journal of Biological Chemistry.

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

[70]  J. Thorner,et al.  Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. , 1994, Genes & development.

[71]  Michael J Rust,et al.  Ligands for Clathrin-Mediated Endocytosis Are Differentially Sorted into Distinct Populations of Early Endosomes , 2006, Cell.

[72]  D. Dressler,et al.  Initiation and reinitiation of DNA synthesis during replication of bacteriophage T7. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[73]  C. Walczak,et al.  Mitotic spindle assembly and chromosome segregation: refocusing on microtubule dynamics. , 2004, Molecular cell.

[74]  P. Cook.  The organization of replication and transcription. , 1999, Science.