Advertisement

Reverse Gyrase

  • M. Duguet
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 9)

Abstract

Reverse gyrase is a fascinating enzyme for many reasons. Apart from its unique ability to introduce positive supercoils in a closed circular DNA at temperatures up to 100 °C, it is the first example of an ATP-dependent type I topoisomerase. Although it was isolated from hyperthermophiles, organisms considered by several authors as very primitive, close to the root of the tree of life (Woese et al. 1990; Olsen et al. 1994), reverse gyrase appears as an extraordinarily sophisticated enzyme: as developed in this chapter, it is probably composed of two intercommunicating domains, a topoisomerase and a putative helicase, in which several movements and conformational changes take place, promoting DNA cleavage, strand passage and resealing as other topoisomerases, but also supercoiling by a mechanism yet unknown, that may involve a local strand separation by a helicase-like activity.

Keywords

Reverse Gyrase Negative Supercoils Strand Cleavage Sulfolobus Acidocaldarius Positive Supercoiling 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andera L, Mikulik K, Savelyeva ND (1993) Characterization of a reverse gyrase from the extemely thermophilic hydrogen-oxidizing eubacterium Calderobacterium hydrogenophilum. FEMS Microbiol Lett 110:107–112CrossRefGoogle Scholar
  2. Arthur L (1991) Characterisation of a novel eukozyotic topoisomerase (top 3) in saccaromyces cerevisiae that affects recombination and gene expression. PhD Thesis, Columbia University, New YorkGoogle Scholar
  3. Brantl S, Kummer C, Behnke D (1994) Complete nucleotide sequence of plasmid pGB3637, a derivative of the Streptococcus agalactida plasmid pIP501. Gene 142:155–156PubMedCrossRefGoogle Scholar
  4. Bouthier de la Tour C, Portemer C, Nadal M, Stetter KO, Forterre P, Duguet M (1990) Reverse gyrase, a hallmark of the hyperthermophilic archaebacteria. J Bacteriol 172:6803–6808Google Scholar
  5. Bouthier de la Tour C, Portemer C, Huber R, Forterre P, Duguet M (1991) Reverse gyrase in thermophilic eubacteria. J Bacteriol 173:3921–3923Google Scholar
  6. Bouthier de la Tour C, Portemer C, Forterre P, Huber R, Duguet M (1993) ATP-independent DNA topoisomerase from Fervidobacterium islandicum. Biochim Biophys Acta 1216:213–220Google Scholar
  7. Ceglowski P, Boitsov G, Lueder G, Alonso JC (1992) Genebank accession no. X66468Google Scholar
  8. Charbonnier F (1993) Etude de la topologie de l’ADN chez les archaebactéries thermophiles. Thesis Université Paris Sud, OrsayGoogle Scholar
  9. Collin RG (1990) Reverse gyrase from archaebacteria. Thesis, University of Waikato, Hamilton, NZGoogle Scholar
  10. Collin RG, Morgan HW, Musgrave DR, Daniel RM (1988) Distribution of reverse gyrase in representative species of eubacteria and archaebacteria. FEMS Microbiol Lett 55:235–240CrossRefGoogle Scholar
  11. Confalonieri F (1993) Clonage et séquençage du gene de la reverse gyrase de Sulfobolus acidocaldarius: analyse moléculaire de sa séquence ainsi que de celles des régions d’ADN situées de part et d’autre de ce gène. Thesis, Université Paris Sud, OrsayGoogle Scholar
  12. Confalonieri F, Elie C, Nadal M, Bouthier de la Tour C, Forterre P, Duguet M (1993) Reverse gyrase: a helicase-like domain and a type I topoisomerase in the same Polypeptide. Proc Natl Acad Sci USA 90:4753–4757PubMedCrossRefGoogle Scholar
  13. Confalonieri F, Marsault J, Duguet M (1994) SAV, an archaebacterial gene with extensive homology to a family of highly conserved eukaryotic ATPases. J Mol Biol 235:396–401PubMedCrossRefGoogle Scholar
  14. Dalgaard JZ, Garrett RA (1993) Archaeal hyperthermophile genes. In: Kates M, Kusner D, Matheson A (eds) The biochemistry of archaea. New comprehensive biochemistry series, vol 26, Elsevier, AmsterdamGoogle Scholar
  15. De Jong S (1994) Cloning and sequencing of the Topl gene, the gene encoding B. subtilis DNA topoisomerase I. Genebank accession no. L27797Google Scholar
  16. Di Gate RJ, Marians KJ (1989) Molecular cloning and DNA sequence analysis of Escherichia coli topB, the gene encoding topoisomerase III. J Biol Chem 264:17924–17930Google Scholar
  17. Drlica K (1992) Control of bacterial DNA supercoiling. Mol Microbiol 6:425–433PubMedCrossRefGoogle Scholar
  18. Duguet M (1993) The helical repeat of DNA at high temperature. Nucleic Acids Res 21:463–468PubMedCrossRefGoogle Scholar
  19. Erdmann R, Wiebel FF, Flessau A, Rytka J, Beyer A, Fröhlich KU, Kunau WH (1991) PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell 64:499–510PubMedCrossRefGoogle Scholar
  20. Firth N, Ridgeway KP, Byrne ME, Fink PD, Johnson L, Paulsen IT, Skurray RA (1993) Analysis of a transfer region from the staphylococcal plasmid pSK41. Gene 136:13–25PubMedCrossRefGoogle Scholar
  21. Forterre P, Mirambeau G, Jaxel C, Nadal M, Duguet M (1985) High positive supercoiling in vitro catalyzed by an ATP and polyethylene glycol-stimulated topoisomerase from Sulfolobus acidocaldarius. EMBO J 4:2123–2128PubMedGoogle Scholar
  22. Forterre P, Charbonnier F, Marguet E, Harper F, Henckes G (1992) Chromosome structure and DNA topology in extremely thermophilic archaebacteria. Biochem Soc Symp 58:99–112PubMedGoogle Scholar
  23. Forterre P, Confalonieri F, Charbonnier F, Duguet M (1995) Speculations on the origin of life and thermophily: review of available information on reverse gyrase suggests that hyperthermophilic procaryotes are not so primitive. Origins of life and Evolution of the biosphere 25:235–249PubMedCrossRefGoogle Scholar
  24. Fouet A, Sirard JC, Mock M (1994) Bacillus anthracis pX01 virulence plasmid encodes a type 1 DNA topoisomerase. Mol Microbiol 11:471–479PubMedCrossRefGoogle Scholar
  25. Frölich KU, Fries HW, Rüdiger M, Erdmann R, Botstein D, Mecke D (1991) Yeast cell cycle protein CDC48p shows full-length homology to the mammalian protein VCP and is a member of a protein family involved in secretion, peroxisome formation, and gene expression. J Cell Biol 114:443–453CrossRefGoogle Scholar
  26. Gabay C, Hassidim M, Hurwitz-Lieman J, Marco E, Kaplan A (1993) Modification of topA in Synecoccus PCC 7942. Genebank accession no. X72391Google Scholar
  27. Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothestein R (1994) The yeast type I topoisomerase, Top 3, interacts with Sgs1, a DNA helicase homologue: a potential eucaryotic reverse gyrase. Mol Cell Biol 14:8391–8398PubMedGoogle Scholar
  28. Jaxel C, Nadal M, Mirambeau G, Forterre P, Takahashi M, Duguet M (1989) Reverse gyrase binding to DNA alters the double helix structure and produces single-strand cleavage in the absence of ATP. EMBO J 8:3135–3139PubMedGoogle Scholar
  29. Kikuchi A (1990) Reverse gyrase and other archaebacterial topoisomerases. In: Cozzarelli N, Wang J (eds) DNA topology and its biological effects. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 285–298Google Scholar
  30. Kikuchi A, Asai K (1984) Reverse gyrase — a topoisomerase which introduces positive superhelical turns into DNA. Nature 309:677–681PubMedCrossRefGoogle Scholar
  31. Kikuchi A, Shibata T, Kakasu S (1986) Reverse gyrase and DNA supercoiling in Sulfolobus. Syst Appl Microbiol 7:72–78CrossRefGoogle Scholar
  32. Koo HS, Lau K, Wu HY, Liu LF (1992) Identification of a DNA supercoiling activity in Saccharomyces cerevisiae. Nucleic Acids Res 20:5067–5072PubMedCrossRefGoogle Scholar
  33. Kosyavkin SA, Krah R, Geliert M, Stetter KO, Lake JA, Slesarev AI (1994) A reverse gyrase with an unusual structure. A type I topoisomerase from the hyperthermophile Methanopyrus kandleri is a two-subunit protein. J Biol Chem 269:11081–11089Google Scholar
  34. Kovalsky OI, Kozyavkin SA, Slesarev AI (1990) Archaebacterial reverse gyrase cleavage-site specificity is similar to that of eubacterial DNA topoisomerases I. Nucleic Acids Res 18:2801–2805PubMedCrossRefGoogle Scholar
  35. Kwon H, Imbalzano AN, Khavari PA, Kingston RE, Green MR (1994) Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370:477–481PubMedCrossRefGoogle Scholar
  36. Lima CD, Wang JC, Mondragon A (1994) Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367:138–146PubMedCrossRefGoogle Scholar
  37. Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84:7024–7027PubMedCrossRefGoogle Scholar
  38. Mirambeau G, Duguet M, Forterre P (1984) ATP-dependent DNA topoisomerase from the archaebacterum Sulfolobus acidocaldarius — relaxation of supercoiled DNA at high temperature. J Mol Biol 179:559–563PubMedCrossRefGoogle Scholar
  39. Nadal M (1990) La réverse gyrase de Sulfolubus: surenroulement positif de l’ADN in vivo et in vitro. Thesis, Université Pierre et Marie Curie, ParisGoogle Scholar
  40. Nadal M, Mirambeau G, Forterre P, Reiter WD, Duguet M (1986) Positively supercoiled DNA in a virus-like particle of an archaebacterium. Nature 321:256–258CrossRefGoogle Scholar
  41. Nadal M, Jaxel C, Portemer C, Forterre P, Mirambeau G, Duguet M (1988) Reverse gyrase of Sulfolobus: purification to homogeneity and characterization. Biochemistry 27:9102–9108PubMedCrossRefGoogle Scholar
  42. Nadal M, Couderc E, Duguet M, Jaxel C (1994) Purification and characterization of reverse gyrase from Sulfolobus shibatae. Its proteolytic product appears as an ATP-independent topoisomerase. J Biol Chem 269:5255–5263PubMedGoogle Scholar
  43. Nakasu S, Kikuchi A (1985) Reverse gyrase; ATP-dependent type I topoisomerase from Sulfolobus. EMBO J 4:2705–2710PubMedGoogle Scholar
  44. Nielson JP, Trachsel H (1988) The mouse protein synthesis initiation factor 4A gene family includes two related functional genes which are differentially expressed. EMBO J 7:2097–2105Google Scholar
  45. Nurse P, DiGate RJ, Zavitz KH, Marians KJ (1990) Molecular cloning and DNA sequence analysis of Escherichia coli priA, the gene encoding the primosomal protein replication factor Y. Proc Natl Acad Sci USA 87:4615–4619PubMedCrossRefGoogle Scholar
  46. Olsen GJ, Woese CR, Overbeek R (1994) The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 176:1–6PubMedGoogle Scholar
  47. Omichinski JG, Clore GM, Schaad O, Felsenfeld G, Trainor C, Appella E, Stahl SJ, Gronenborn AM (1993) NMR structure of a specific DNA complex of Zn containing DNA binding domain of GATA-1. Science 261:438–446PubMedCrossRefGoogle Scholar
  48. Romeo AM, Kleff S, Sternglanz R (1992) Genebank accession no. L07870Google Scholar
  49. Sandman K, Krzycki JA, Dobrinski B, Lurz R, Reeve JN (1990) HMF, a DNA-binding protein isolated from the hyperthermophilic archeon Methanothermus fervidus, is most closely related to histones. Proc Natl Acad Sci USA 87:5788–5791PubMedCrossRefGoogle Scholar
  50. Schmid SR, Linder P (1992) D-E-A-D protein family of putative RNA helicases. Mol Microbiol 6:283–292PubMedCrossRefGoogle Scholar
  51. Searcy DG (1986) The Archaebacterial Historie HTa. In: Gualerzi CO, Pon CL (eds) Bacterial chromatin. Springer, Berlin Heidelberg New York, pp 175, 184CrossRefGoogle Scholar
  52. Shibata T, Nakasu S, Yasui K, Kikuchi A (1987) Intrinsic DNA-dependent ATPase. activity of reverse gyrase. J Biol Chem 262:10419–10421Google Scholar
  53. Slesarev AI (1988) Positive supercoiling catalyzed in vitro by ATP-dependent topoisomerase from Desulfurococcus amylolyticus. Eur J Biochem 173:395–399PubMedCrossRefGoogle Scholar
  54. Slesarev AI, Zaitzev DA, Kopylov VM, Stetter KO, Kozyavkin SA (1991) DNA topoisomerase III from extremely thermophilic archaebacteria. J Biol Chem 266:12321–12328PubMedGoogle Scholar
  55. Strack B, Lanka E (1993) Nucleotide sequence of TraE gene of IncP plasmid RP4. Genebank accession no. L10329Google Scholar
  56. Swinfield TJ, Jannière L, Ehrlich SD Minton NP (1991) Characterization of a region of the Enterococcus foecalis plasmid pAMβ1 which enhances the segregational stability of pAMβ1-derived cloning vectors in B. subtilis. Plasmid 26:209–221PubMedCrossRefGoogle Scholar
  57. Tse-Dinh YC, KirKegaard K, Wang JC (1980) Covalent bonds between protein and DNA. J Biol Chem 255:5560–5565Google Scholar
  58. Tse-Dinh YC, Wang JC (1986) Complete nucleotide sequence of the topA gene encoding Escherichia coli topoisomerase I. J Mol Biol 191:321–331PubMedCrossRefGoogle Scholar
  59. Wallis JW, Chrebet G, Brodsky G, Rolfe M, Rothstein R (1989) A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58:409–419PubMedCrossRefGoogle Scholar
  60. Woese CR, Kandier O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains archaebacteria, and eucarya. Proc Natl Acad Sci USA 87:4576–4579PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • M. Duguet
    • 1
  1. 1.Laboratoire d’Enzymologie des Acides Nucléiques, Institut de Génétique et Microbiologie, URA 1354 CNRSUniversité Paris SudOrsayFrance

Personalised recommendations