Abstract
A strikingly large number of the proteins involved in DNA metabolism adopt a toroidal ? or ring-shaped ? quaternary structure, even though they have completely unrelated functions. Given that these proteins all use DNA as a substrate, their convergence to one shape is probably not a coincidence. Ring-forming proteins may have been selected during evolution for advantages conferred by the toroidal shape on their interactions with DNA.
Key Points
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A strikingly large number of proteins that interact with DNA assume a toroidal, or ring-shaped structure. These include sliding clamp proteins, which increase the lifetime of other proteins on DNA, helicases that unwind DNA, topisomerases that alter DNA structure, and many other proteins that mediate the processes of DNA replication, repair and recombination.
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A common feature of these proteins is that their subunits are arranged in a closed ring, the centre of which is able to accommodate single stranded and/or duplex DNA. For many proteins, this property is proposed to allow high processivity on DNA through topological linkage.
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Although some proteins such as human topoisomerase I bind DNA in the central cavity simply by opening up and closing around DNA, others require the help of ?molecular matchmakers? that link toroidal proteins and DNA by ATP-dependent reactions.
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References
Boyer, P. D. The ATP synthase ? a splendid molecular machine. Annu. Rev. Biochem. 66, 717?749 ( 1997).
Sigler, P. B. et al. Structure and function in GroEL-mediated protein folding. Annu. Rev. Biochem. 67, 581?608 (1998).
Bochtler, M., Ditzel, L., Groll, M., Hartmann, C. & Huber, R. The proteasome. Annu. Rev. Biophys. Biomol. Struct. 28, 295?317 ( 1999).
Isaacs, N. W., Cogdell, R. J., Freer, A. A. & Prince, S. M. Light-harvesting mechanisms in purple photosynthetic bacteria. Curr. Opin. Struct. Biol. 5, 794?797 (1995).
Hingorani, M. M. & O'Donnell, M. Toroidal proteins: running rings around DNA. Curr. Biol. 8, R83?R86 (1998).
Hingorani, M. M. & O'Donnell, M. Sliding clamps: a (tail)ored fit. Curr. Biol. 10, R25? R29 (2000).
Baker, T. A. & Bell, S. P. Polymerases and the replisome: machines within machines. Cell 92, 295? 305 (1998).
Fay, P. J., Johanson, K. O., McHenry, C. S. & Bambara, R. A. Size classes of products synthesized processively by DNA polymerase III and DNA polymerase III holoenzyme of Escherichia coli. J. Biol. Chem. 256, 976?983 ( 1981).
Tsurimoto, T. & Stillman, B. Functions of replication factor C and proliferating-cell nuclear antigen: functional similarity of DNA polymerase accessory proteins from human cells and bacteriophage T4. Proc. Natl Acad. Sci. USA 87, 1023?1027 (1990).
Jarvis, T. C., Newport, J. W. & von Hippel, P. H. Stimulation of the processivity of the DNA polymerase of bacteriophage T4 by the polymerase accessory proteins. The role of ATP hydrolysis. J. Biol. Chem. 266, 1830? 1840 (1991).
Stukenberg, P. T., Studwell-Vaughan, P. S. & O'Donnell, M. Mechanism of the sliding beta-clamp of DNA polymerase III holoenzyme. J. Biol. Chem. 266, 11328?11334 (1991). This study predicted that the β clamp encircles DNA before the solution of a crystal structure. This prediction was made on the basis of the observation that β could fall off linear DNA, but not circular DNA.
Kong, X. P., Onrust, R., O'Donnell, M. & Kuriyan, J. Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp. Cell 69, 425?437 (1992).The first crystal structure of a sliding clamp protein clarified greatly the mechanism by which clamps act as processivity factors for polymerase on DNA.
Yao, N. et al. Clamp loading, unloading and intrinsic stability of the PCNA, beta and gp45 sliding clamps of human, E. coli and T4 replicases. Genes Cells 1, 101?113 ( 1996).
Moarefi, I., Jeruzalmi, D., Turner, J., O'Donnell, M. & Kuriyan, J. Crystal structure of the DNA polymerase processivity factor of T4 bacteriophage. J. Mol. Biol. 296, 1215?1223 (2000).
Shamoo, Y. & Steitz, T. A. Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex. Cell 99, 155? 166 (1999).Structure of a sliding clamp in complex with an interacting peptide from the DNA polymerase; this structure represents the first step towards determining the structure of a DNA replisome.
Krishna, T. S., Kong, X. P., Gary, S., Burgers, P. M. & Kuriyan, J. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79, 1233? 1243 (1994).
Gulbis, J. M., Kelman, Z., Hurwitz, J., O'Donnell, M. & Kuriyan, J. Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA. Cell 87, 297? 306 (1996).
Patel, S. S. & Picha, K. M. Structure and function of hexameric helicases. Annu. Rev. Biochem. (in the press).
Lohman, T. M. & Bjornson, K. P. Mechanisms of helicase-catalyzed DNA unwinding. Annu. Rev. Biochem. 65, 169 ?214 (1996).
Karow, J. K., Wu, L. & Hickson, I. D. RecQ family helicases: roles in cancer and aging. Curr. Opin. Genet. Dev. 10, 32?38 (2000).
Reha-Krantz, L. J. & Hurwitz, J. The dnaB gene product of Escherichia coli. I. Purification, homogeneity, and physical properties. J. Biol. Chem. 253, 4043? 4050 (1978).
Finger, L. R. & Richardson, J. P. Stabilization of the hexameric form of Escherichia coli. protein rho under ATP hydrolysis conditions . J. Mol. Biol. 156, 203? 219 (1982).
Egelman, H. H., Yu, X., Wild, R., Hingorani, M. M. & Patel, S. S. Bacteriophage T7 helicase/primase proteins form rings around single-stranded DNA that suggest a general structure for hexameric helicases. Proc. Natl Acad. Sci. USA 92, 3869?3873 (1995). The electron-microscope (EM) structure of a replicative hexameric DNA helicase provided insights into how these enzymes form a ring that encircles single-stranded DNA and catalyse unwinding of duplex DNA.
Sawaya, M. R., Guo, S., Tabor, S., Richardson, C. C. & Ellenberger, T. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7. Cell 99, 167?177 (1999).The first crystal structure of a hexameric DNA helicase.
Dong, F., Gogol, E. P. & von Hippel, P. H. The phage T4-coded DNA replication helicase (gp41) forms a hexamer upon activation by nucleoside triphosphate. J. Biol. Chem. 270, 7462?7473 (1995).
Barcena, M. et al. Polymorphic quaternary organization of the Bacillus subtilis bacteriophage SPP1 replicative helicase (G40 P). J. Mol. Biol. 283, 809?819 ( 1998).
San Martin, M. C., Gruss, C. & Carazo, J. M. Six molecules of SV40 large T antigen assemble in a propeller-shaped particle around a channel. J. Mol. Biol. 268, 15?20 (1997).
Yu, X., Jezewska, M. J., Bujalowski, W. & Egelman, E. H. The hexameric E. coli DnaB helicase can exist in different quaternary states. J. Mol. Biol. 259, 7? 14 (1996).
Yu, X., Horiguchi, T., Shigesada, K. & Egelman, E. H. Three-dimensional reconstruction of transcription termination factor rho: Orientation of the N-terminal domain and visualization of an RNA-binding Site . J. Mol. Biol. 299, 1299? 1307 (2000).
Stasiak, A. et al. The Escherichia coli RuvB branch migration protein forms double hexameric rings around DNA. Proc. Natl Acad. Sci. USA 91, 7618?7622 ( 1994).
Sato, M. et al. Electron microscopic observation and single-stranded DNA binding activity of the Mcm4, 6, 7 complex. J. Mol. Biol. 300 , 421?431 (2000). A first view of the quaternary structure of the human MCM helicase that is required for initiation of DNA replication.
Karow, J. K., Newman, R. H., Freemont, P. S. & Hickson, I. D. Oligomeric ring structure of the Bloom's syndrome helicase. Curr. Biol. 9, 597?600 ( 1999).
Chong, J. P., Hayashi, M. K., Simon, M. N., Xu, R. M. & Stillman, B. A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc. Natl Acad. Sci. USA 97, 1530?1535 (2000).
Yu, X., Hingorani, M. M., Patel, S. S. & Egelman, E. H. DNA is bound within the central hole to one or two of the six subunits of the T7 DNA helicase. Nature Struct. Biol. 3, 740?743 (1996).
Morris, P. D. & Raney, K. D. DNA helicases displace streptavidin from biotin-labeled oligonucleotides. Biochemistry 38, 5164?5171 (1999).
Bujalowski, W. & Jezewska, M. J. Interactions of Escherichia coli primary replicative helicase DnaB protein with single-stranded DNA. The nucleic acid does not wrap around the protein hexamer . Biochemistry 34, 8513? 8519 (1995).
Fouts, E. T., Yu, X., Egelman, E. H. & Botchan, M. R. Biochemical and electron microscopic image analysis of the hexameric E1 helicase. J. Biol. Chem. 274, 4447?4458 (1999).
Mastrangelo, I. A. et al. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication. Nature 338, 658?662 (1989).
Yong, Y. & Romano, L. J. Benzo[a]pyrene-DNA adducts inhibit the DNA helicase activity of the bacteriophage T7 gene 4 protein. Chem. Res. Toxicol. 9, 179?187 (1996).
Hacker, K. J. & Johnson, K. A. A hexameric helicase encircles one DNA strand and excludes the other during DNA unwinding. Biochemistry 36, 14080?14087 ( 1997).
Raney, K. D., Carver, T. E. & Benkovic, S. J. Stoichiometry and DNA unwinding by the bacteriophage T4 41:59 helicase. J. Biol. Chem. 271, 14074 ?14081 (1996).
Nakai, H. & Richardson, C. C. Interactions of the DNA polymerase and gene 4 protein of bacteriophage T7. Protein?protein and protein?DNA interactions involved in RNA-primed DNA synthesis. J. Biol. Chem. 261, 15208?15216 ( 1986).
Kim, S., Dallmann, H. G., McHenry, C. S. & Marians, K. J. Coupling of a replicative polymerase and helicase: a tau-DnaB interaction mediates rapid replication fork movement. Cell 84, 643?650 (1996).
Yuzhakov, A., Turner, J. & O'Donnell, M. Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell 86, 877?886 (1996).
Hingorani, M. M. & Patel, S. S. Interactions of bacteriophage T7 DNA primase/helicase protein with single-stranded and double-stranded DNAs. Biochemistry 32, 12478 ?12487 (1993).
Jezewska, M. J., Kim, U. S. & Bujalowski, W. Binding of Escherichia coli primary replicative helicase DnaB protein to single-stranded DNA. Long-range allosteric conformational changes within the protein hexamer. Biochemistry 35 , 2129?2145 (1996).
Hingorani, M. M., Washington, M. T., Moore, K. C. & Patel, S. S. The dTTPase mechanism of T7 DNA helicase resembles the binding change mechanism of the F1-ATPase. Proc. Natl Acad. Sci. USA 94, 5012?5017 (1997). Rapid kinetic analysis of the NTPase activity of a hexameric helicase yielded a model mechanism for helicase-catalysed sequential TTP hydrolysis (similar to F 1 -ATPase) that may be coupled to stepwise DNA unwinding.
Stitt, B. L. & Xu, Y. Sequential hydrolysis of ATP molecules bound in interacting catalytic sites of Escherichia coli transcription termination protein Rho. J. Biol. Chem. 273, 26477?26486 (1998).
Kovall, R. & Matthews, B. W. Toroidal structure of lambda-exonuclease . Science 277, 1824?1827 (1997).
Passy, S. I., Yu, X., Li, Z., Radding, C. M. & Egelman, E. H. Rings and filaments of beta protein from bacteriophage lambda suggest a superfamily of recombination proteins. Proc. Natl Acad. Sci. USA 96, 4279?4284 (1999).
Mythili, E., Kumar, K. A. & Muniyappa, K. Characterization of the DNA-binding domain of beta protein, a component of phage lambda red-pathway, by UV catalyzed cross-linking. Gene 182, 81?87 ( 1996).
Poteete, A. R., Sauer, R. T. & Hendrix, R. W. Domain structure and quaternary organization of the bacteriophage P22 Erf protein. J. Mol. Biol. 171, 401?418 (1983).
Thresher, R. J., Makhov, A. M., Hall, S. D., Kolodner, R. & Griffith, J. D. Electron microscopic visualization of RecT protein and its complexes with DNA. J. Mol. Biol. 254, 364?371 (1995).
Ando, R. A. & Morrical, S. W. Single-stranded DNA binding properties of the UvsX recombinase of bacteriophage T4: binding parameters and effects of nucleotides. J. Mol. Biol. 283, 785?796 (1998).
Shinohara, A., Ogawa, H. & Ogawa, T. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69, 457?470 (1992); erratum in Cell 71, 180 (1992).
Bianco, P. R., Tracy, R. B. & Kowalczykowski, S. C. DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci. 3, D570? D603 (1998).
Yu, X. & Egelman, E. H. The RecA hexamer is a structural homologue of ring helicases. Nature Struct. Biol. 4 , 101?104 (1997).
Baumann, P., Benson, F. E., Hajibagheri, N. & West, S. C. Purification of human Rad51 protein by selective spermidine precipitation . Mutat. Res. 384, 65?72 (1997).
Passy, S. I. et al. Human Dmc1 protein binds DNA as an octameric ring. Proc. Natl Acad. Sci. USA 96, 10684? 10688 (1999).EM structure of this ring-shaped human RecA homologue opens up new possible mechanisms of action of RecA-like proteins in homologous recombination or other metabolic processes.
Stasiak, A. Z. et al. The human Rad52 protein exists as a heptameric ring. Curr. Biol. 10, 337?340 (2000).
Rattray, A. J. & Symington, L. S. Multiple pathways for homologous recombination in Saccharomyces cerevisiae. Genetics 139, 45?56 ( 1995).
Baumann, P. & West, S. C. Heteroduplex formation by human Rad51 protein: effects of DNA end-structure, hRPA and hRad52. J. Mol. Biol. 291, 363?374 (1999).
Sung, P. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272, 28194?28197 (1997).
New, J. H., Sugiyama, T., Zaitseva, E. & Kowalczykowski, S. C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391, 407?410 (1998).
Wang, J. C. DNA topoisomerases. Annu. Rev. Biochem. 65, 635?692 (1996).
Lima, C. D., Wang, J. C. & Mondragon, A. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367, 138?146 (1994).
Mondragon, A. & DiGate, R. The structure of Escherichia coli DNA topoisomerase III. Structure Fold. Des. 7, 1373?1383 (1999).
Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J. & Hol, W. G. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504?1513 (1998).
Stewart, L., Redinbo, M. R., Qiu, X., Hol, W. G. & Champoux, J. J. A model for the mechanism of human topoisomerase I. Science 279, 1534?1541 (1998).The series of crystal structures of human topoisomerase I in references 68 and 69 provide detailed snapshots of the process by which this enzyme catalyses changes in the topology of DNA.
Berger, J. M. Type II DNA topoisomerases. Curr. Opin. Struct. Biol. 8, 26?32 (1998).
Baird, C. L., Harkins, T. T., Morris, S. K. & Lindsley, J. E. Topoisomerase II drives DNA transport by hydrolyzing one ATP. Proc. Natl Acad. Sci. USA 96, 13685? 13690 (1999).A rapid kinetic study of the topoisomerase II reaction yields a model mechanism by which this enzyme couples ATP binding and hydrolysis to catenation or decatenation of duplex DNA.
Berger, J. M., Gamblin, S. J., Harrison, S. C. & Wang, J. C. Structure and mechanism of DNA topoisomerase II. Nature 379, 225?232 (1996).
Lee, J. Y. et al. Crystal structure of NAD+-dependent DNA ligase: modular architecture and functional implications. EMBO J. 19, 1119?1129 (2000).
Antson, A. A. et al. Structure of the trp RNA-binding attenuation protein, TRAP, bound to RNA. Nature 401, 235? 242 (1999).
Valpuesta, J. M., Fernandez, J. J., Carazo, J. M. & Carrascosa, J. L. The three-dimensional structure of a DNA translocating machine at 10 Å resolution. Structure Fold. Des. 7, 289? 296 (1999).
Kasai, M. et al. The translin ring specifically recognizes DNA ends at recombination hot spots in the human genome. J. Biol. Chem. 272, 11402?11407 (1997).
Valle, M., Valpuesta, J. M., Carrascosa, J. L., Tamayo, J. & Garcia, R. The interaction of DNA with bacteriophage phi 29 connector: a study by AFM and TEM. J. Struct. Biol. 116, 390?398 (1996).
Turnquist, S., Simon, M., Egelman, E. & Anderson, D. Supercoiled DNA wraps around the bacteriophage phi 29 head?tail connector. Proc. Natl Acad. Sci. USA 89, 10479? 10483 (1992).
West, S. C. Processing of recombination intermediates by the RuvABC proteins. Annu. Rev. Genet. 31, 213?244 (1997).
Aoki, K., Suzuki, K., Ishida, R. & Kasai, M. The DNA binding activity of Translin is mediated by a basic region in the ring-shaped structure conserved in evolution. FEBS Lett. 443, 363?366 (1999).
Redinbo, M. R., Stewart, L., Champoux, J. J. & Hol, W. G. Structural flexibility in human topoisomerase I revealed in multiple non-isomorphous crystal structures. J. Mol. Biol. 292, 685 ?696 (1999).
Turner, J., Hingorani, M. M., Kelman, Z. & O'Donnell, M. The internal workings of a DNA polymerase clamp-loading machine. EMBO J. 18, 771?783 ( 1999).
Kaboord, B. F. & Benkovic, S. J. Accessory proteins function as matchmakers in the assembly of the T4 DNA polymerase holoenzyme. Curr. Biol. 5, 149? 157 (1995).
Mossi, R. & Hubscher, U. Clamping down on clamps and clamp loaders ? the eukaryotic replication factor C. Eur. J. Biochem. 254, 209?216 ( 1998).
Hingorani, M. M. & O'Donnell, M. ATP binding to the Escherichia coli clamp loader powers opening of the ring-shaped clamp of DNA polymerase III holoenzyme. J. Biol. Chem. 273, 24550?24563 (1998).
Naktinis, V., Onrust, R., Fang, L. & O'Donnell, M. Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. II. Intermediate complex between the clamp loader and its clamp. J. Biol. Chem. 270, 13358?13365 (1995).
Hingorani, M. M., Bloom, L. B., Goodman, M. F. & O'Donnell, M. Division of labor-sequential ATP hydrolysis drives assembly of a DNA polymerase sliding clamp around DNA. EMBO J. 18, 5131 ?5144 (1999).
Ahnert, P., Moore Picha, K. & Patel, S. S. A ring-opening mechanism for single-stranded DNA binding in the central channel of T7 helicase?primase protein. EMBO J. 19, 3418?3427 ( 2000).
Tarumi, K. & Yonesaki, T. Functional interactions of gene 32, 41, and 59 proteins of bacteriophage T4. J. Biol. Chem. 270, 2614?2619 (1995).
Allen, G. C. Jr & Kornberg, A. Fine balance in the regulation of DnaB helicase by DnaC protein in replication in Escherichia coli. J. Biol. Chem. 266, 22096? 22101 (1991).
Perkins, G. & Diffley, J. F. Nucleotide-dependent prereplicative complex assembly by Cdc6p, a homolog of eukaryotic and prokaryotic clamp-loaders . Mol. Cell 2, 23?32 (1998).
Herbig, U., Marlar, C. A. & Fanning, E. The Cdc6 nucleotide-binding site regulates its activity in DNA replication in human cells. Mol. Biol. Cell 10, 2631?2645 (1999).
Morrical, S. W., Hempstead, K. & Morrical, M. D. The gene 59 protein of bacteriophage T4 modulates the intrinsic and single-stranded DNA-stimulated ATPase activities of gene 41 protein, the T4 replicative DNA helicase. J. Biol. Chem. 269, 33069?33081 (1994).
Learn, B. A., Um, S. J., Huang, L. & McMacken, R. Cryptic single-stranded-DNA binding activities of the phage lambda P and Escherichia coli DnaC replication initiation proteins facilitate the transfer of E. coli DnaB helicase onto DNA. Proc. Natl Acad. Sci. USA 94 , 1154?1159 (1997).
Carter, D. M. & Radding, C. M. The role of exonuclease and beta protein of phage lambda in genetic recombination. II. Substrate specificity and the mode of action of lambda exonuclease. J. Biol. Chem. 246, 2502?2512 (1971).
Fang, L., Davey, M. J. & O'Donnell, M. Replisome assembly at oriC, the replication origin of E. coli, reveals an explanation for initiation sites outside an origin . Mol. Cell 4, 541?553 (1999).
Dutta, A. & Bell, S. P. Initiation of DNA replication in eukaryotic cells. Annu. Rev. Cell Biol. 13, 293?332 (1997).
Mechanic, L. E., Hall, M. C. & Matson, S. W. Escherichia coli DNA helicase II is active as a monomer. J. Biol. Chem. 274, 12488? 12498 (1999).
Velankar, S. S., Soultanas, P., Dillingham, M. S., Subramanya, H. S. & Wigley, D. B. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97, 75? 84 (1999).
Petit, M. A. et al. PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling-circle replication. Mol. Microbiol. 29, 261?273 (1998).
Zuccola, H. J., Filman, D. J., Coen, D. M. & Hogle, J. M. The crystal structure of an unusual processivity factor, herpes simplex virus UL42, bound to the C terminus of its cognate polymerase. Mol. Cell 5, 267?278 ( 2000).
Fan, L., Sanschagrin, P. C., Kaguni, L. S. & Kuhn, L. A. The accessory subunit of mtDNA polymerase shares structural homology with aminoacyl-tRNA synthetases: implications for a dual role as a primer recognition factor and processivity clamp. Proc. Natl Acad. Sci. USA 96, 9527?9532 (1999).
Doublie, S. & Ellenberger, T. The mechanism of action of T7 DNA polymerase. Curr. Opin. Struct. Biol. 8, 704?712 (1998).
Johnson, A. A., Tsai, Y., Graves, S. W. & Johnson, K. A. Human mitochondrial DNA polymerase holoenzyme: reconstitution and characterization. Biochemistry 39, 1702?1708 (2000).
Sanders, G. M., Kassavetis, G. A. & Geiduschek, E. P. Dual targets of a transcriptional activator that tracks on DNA. EMBO J. 16, 3124? 3132 (1997).
Leipe, D. D., Aravind, L., Grishin, N. V. & Koonin, E. V. The bacterial replicative helicase DnaB evolved from a RecA duplication. Genome Res. 10, 5?16 ( 2000).A comprehensive phylogenetic and structural analysis of RecA-like proteins and the DnaB family of hexameric helicases indicates that these proteins share a common ancestor that had the ability to form oligomeric rings and undergo NTP-driven conformational changes.
Egelman, E. A ubiquitous structural core. Trends Biochem. Sci. 25, 183?184 (2000).
Acknowledgements
We thank all researchers who provided images, including J. Kuriyan and D. Jeruzalmi (E. coli β clamp, yPCNA, T4 gp45); Y. Shamoo and T. Steitz (RB69 clamp and polymerase); T. Ellenberger (T7 gp4); E. Gogol (T4 gp41); E. Egelman (E. coli DnaB, RuvB, rho, BPV E1, phage λ β protein, hDmc1, hRad52); C. San Martin (SV40 T antigen); I. Hickson (BLM helicase); J. Chong and B. Stillman (M. th MCM); Y. Ishimi (human MCM); P. Ahnert (T7 gp4 on DNA); R. Kovall and B. Matthews (phage λ exonuclease); M. Redinbo and W. Hol (human topoI); A. Mondragón (E. coli topoI and topoIII); J. Wang (yeast topoII); J. Y. Lee and S. W. Suh (DNA ligase); A. Anston (TRAP); J. Carrascosa (φ29 connector) and M. Kasai (human translin). We also thank M. Davey and K. Picha for discussions. Work supported by a grant from the NIH to M.O.
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Glossary
- PROCESSIVITY
-
The ability of an enzyme to catalyse more than one turnover before releasing the substrate or product of the reaction.
- REPLISOME
-
The multi-protein assembly at the junction of the DNA replication fork.
- STRAND EXCHANGE
-
The process by which a single DNA strand switches from one duplex DNA molecule to base pair with a complementary strand from a second, homologous duplex DNA molecule.
- HOMOLOGOUS RECOMBINATION
-
The process by which segments of DNA are exchanged between two DNA duplexes that share high sequence similarity.
- CATENATION/DECATENATION
-
Topoisomerases catenate (join) or decatenate (separate) two circular DNA molecules by cutting one DNA strand, passing a second strand through the break, and resealing the break in DNA.
- MOLECULAR MATCHMAKER
-
A macromolecule that increases the affinity of two or more other molecules for each other, usually through a reaction using energy from ATP binding and hydrolysis.
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Hingorani, M., O'Donnell, M. A tale of toroids in DNA metabolism. Nat Rev Mol Cell Biol 1, 22–30 (2000). https://doi.org/10.1038/35036044
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DOI: https://doi.org/10.1038/35036044
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