DNA supercoiling plays essential role in maintaining proper chromosome structure, as well as the equilibrium between genome dynamics and stability under specific physicochemical and physiological conditions. In mesophilic organisms, DNA is negatively supercoiled and, until recently, positive supercoiling was considered a peculiar mark of (hyper)thermophilic archaea needed to survive high temperatures. However, several lines of evidence suggest that negative and positive supercoiling might coexist in both (hyper)thermophilic and mesophilic organisms, raising the possibility that positive supercoiling might serve as a regulator of various cellular events, such as chromosome condensation, gene expression, mitosis, sister chromatid cohesion, centromere identity and telomere homoeostasis.

Introduction

Maintaining the appropriate sign and density of DNA supercoiling is vital for any cell. DNA supercoiling plays a major role in many cellular functions, including DNA packaging, gene regulation and recombination. Conversely, most DNA activities, as well as internal and environmental factors, may affect DNA topology, raising the need for mechanisms for its homoeostatic control. This is mainly due to the direct action of DNA topoisomerases that modify the DNA linking number enzymatically [1,2] and to several types of DNA-binding proteins that are able to induce non-enzymatic structural modification of DNA, such as bending, wrapping, crossing or compaction [3]; these proteins can indirectly manipulate DNA topology by inducing torsional tensions that can be released by DNA topoisomerases (Figure 1). Changes in superhelicity may have consequences for the local DNA structure and stability, as well as its biological functions. Supercoiled molecules of opposite signs display markedly different physical properties: underwound (negatively supercoiled) DNA facilitates the strand separation required for DNA transactions. In contrast, DNA overwinding (positive supercoiling) may affect the helical repeat, helix melting and/or flexibility, resulting in DNA stabilization.

Mechanisms of positive supercoiling

Figure 1
Mechanisms of positive supercoiling

Top: right-handed DNA wrapping by an architectural protein is a non-covalent conformational modification reversible upon protein release. However, in a topologically closed molecule, such as a circular DNA (as shown), or if topological barriers prevent torsional stress dissipation (not shown), compensatory negative supercoils are formed in protein-free domains. These can be released by a Type I or Type II topoisomerase, resulting in net positive supercoiling. Bottom: reverse gyrase induces covalent modification of the substrate by cleavage of a single DNA strand and unidirectional strand passage towards linking number increase (enlarged in the inset).

Figure 1
Mechanisms of positive supercoiling

Top: right-handed DNA wrapping by an architectural protein is a non-covalent conformational modification reversible upon protein release. However, in a topologically closed molecule, such as a circular DNA (as shown), or if topological barriers prevent torsional stress dissipation (not shown), compensatory negative supercoils are formed in protein-free domains. These can be released by a Type I or Type II topoisomerase, resulting in net positive supercoiling. Bottom: reverse gyrase induces covalent modification of the substrate by cleavage of a single DNA strand and unidirectional strand passage towards linking number increase (enlarged in the inset).

In the vast majority of organisms of the three kingdoms (Archaea, Bacteria and Eukarya) that live at mesophilic temperatures (20–40°C), DNA is negatively supercoiled, whereas positive DNA supercoiling is generally considered to be a by-product of processes involving unwinding of the double helix and/or translocation of protein machines along DNA. In thermophilic and hyperthermophilic organisms, which can live at temperatures as high as 113°C, modulation of the DNA secondary structure is intimately concerned with the problem of stabilization of DNA against heat denaturation while maintaining its metabolic activity. The existence of alternative topological states was demonstrated by the discovery of reverse gyrase, a DNA topoisomerase inducing positive supercoiling (reviewed in [4,5]) and the finding of episomal DNA in relaxed or positively supercoiled form in several hyperthermophilic archaea [6]. These findings suggested that, in each organism, the actual DNA topology is the result of the adaptive pressure to maintain the proper equilibrium between genome dynamics and stability under the physicochemical conditions specific to that particular organism. However, recent findings suggest that the picture might be more complex, and negative and positive supercoiling might coexist in both (hyper)thermophiles and mesophiles.

In the present paper, we review current knowledge on mechanisms and factors inducing positive supercoiling in diverse organisms and discuss evidence suggesting that positive supercoiling might play specific roles not only in thermophilic, but also in mesophilic, organisms, raising the possibility that the free energy of positive supercoiling may be exploited as a regulator of cellular events.

Positive supercoiling in mesophiles: always evil?

In the classical view, negative supercoiling is believed to facilitate the fluidity required for DNA transactions, playing a significant role in a wide variety of DNA functions, whereas positive supercoiling may have a detrimental effect on genome dynamics. For instance, eukaryotic nucleosome formation is stimulated by negative supercoiling, whereas it is strongly inhibited by positive supercoiling [7]; in addition, left-handed crossovers allow packaging of DNA into higher-order DNA structures while preventing sticky interactions, whereas right-handed crossovers present in relaxed or positive DNA may have inhibitory effects on such superstructures [8]. Consistently, negative supercoiling is an important conformational property of the genome of mesophilic organisms and is maintained by specific mechanisms. Bacteria bear gyrase, a topoisomerase that actively introduces negative supercoiling in an ATP-dependent reaction, and nucleoid-associated proteins such as HU and HNS (histone-like nucleoid structuring protein) [9]; eukaryotes possess histones that wrap DNA into negative supercoils [10]; most mesophilic archaea hold eukaryotic-like histones [11]. Positive supercoils generated by transcription and replication fork movement are removed by the action of topoisomerases. These are DNA gyrase and topoisomerase IV in bacteria and topoisomerase I and II in eukaryotes; for archaea, it is still not clear which is the topoisomerase in charge of this function [1,2,6]. Malfunctioning or inhibition of topoisomerases induce accumulation of positive superturns ahead of the replication fork, which in turn determines replication block and ultimately cell death. Positive supercoiling also has an inhibitory effect on transcription. In yeast, accumulation of positive helical tension along intracellular DNA can be induced by inactivation of both topoisomerase I and II combined with the ectopic expression of the Escherichia coli topoisomerase IA, which relaxes only negatively supercoiled DNA. As a result, a strong reduction of global transcription occurs [12]. Genome-wide analysis showed a striking positional effect of positive supercoiling induced transcription inhibition: genes located at distal position on chromosomes gradually escaped from the transcription stall, indicating that DNA is not torsionally constrained at the chromosomal ends, although is not clear how helical tension is released [13]. In E. coli, positive supercoiling could be induced in vivo in a mutant carrying an octameric variant of HU, which is dimeric in its wild-type form and induces negative supercoiling. The mutant showed a high degree of DNA condensation and altered global transcription pattern [14]. It therefore appears that mesophilic organisms evolved specific mechanisms to prevent the presence of positive DNA in their genome.

However, recent results suggest that positive supercoiling might exist in organisms living at mesophilic temperatures, at least under particular circumstances, and may have a physiological role either by harnessing the free energy stored in the positively supercoiled molecule or exploiting its structural properties. For instance, in vitro models of replication intermediates of bacterial DNA plasmids showed that the formation of Holliday-like junctions at both forks of a replication bubble creates a positive topological constraint that prevents further regression of the forks. Thus, in this case, accumulation of positive supercoiling provides a possible mechanism to protect DNA molecules against extensive fork reversal in the presence of replication blocking lesions [15].

During telomere resolution in two related spirochaete strains, causing Lyme disease and relapsing fever, covalently closed hairpin telomeres are generated from replication intermediates, due to the action of the telomere resolvase, ResT. Bankhead et al. [16] showed that positive supercoiling promotes cooperative assembly of ResT molecules on the DNA substrate, resulting in significant stimulation of telomere resolution. The authors suggest that positive supercoiling produced during telomere replication may link telomere resolution to replication, providing an elegant mechanism to regulate telomere resolution both temporally and spatially. Interestingly, positive supercoiling was also shown to play a role in telomere homoeostasis in human cells [17]. In this case, the telomeric protein TRF2 (telomere repeat factor 2) was shown to generate positive supercoiling and DNA condensation; although the exact role of this activity was not demonstrated directly, it was suggested that TRF2, by constraining DNA in a right-handed conformation, can modify the twist of the adjacent DNA and facilitate strand invasion, which is an essential step in telomeric t-loop formation.

Eukaryotic nucleosomes formed by H3/H4 histones wrap DNA in a left-handed manner and induce negative supercoils [10]. The tetramer–dimer equilibrium of H3/H4 histones has important effects on DNA supercoiling: the tetramer forms negatively coiled DNA; however, in the presence of an excess of the histone chaperone NAP1 (nucleosome assembly protein 1), only H3–H4 dimers are obtained, which induce positively supercoiled DNA [18]. Thus DNA topology might be modulated by conformational changes in the H3–H4 complex through variation of NAP1 activity/concentration. Although such a transition has never been observed in a canonical nucleosome, the eukaryotic CenH3 histone variant, which is specific to the centromeric nucleosomes, was shown to induce positive supercoils both in vitro and in yeast cells [19,20]. It was suggested that the presence of positive nucleosomes at the single centromeric location along the chromosome and the mutual incompatibility of nucleosomes with opposite topologies could explain how centromeres are recognized and maintained as unique loci on chromosomes.

Condensins are highly conserved ancient complexes comprising two SMC (structural maintenance of chromosomes) ATPase subunits (Table 1). These proteins are found in nearly all organisms and, in vitro, are able to induce positive supercoiling. Condensin was initially discovered for its role in eukaryotic chromosome condensation during mitosis, suggesting that positive supercoiling might be the key mechanism underlying the compaction of chromatin fibres. More recently, a number of studies extended these results showing that condensin-like complexes have a general role in chromosome architecture in eukaryotes, bacteria and possibly also in archaea, are required for correct folding and segregation of chromosomes in mitosis and meiosis, and play roles in gene regulation and DNA repair, thus pointing to a wide physiological importance of positive supercoiling [21,22].

Table 1
Proteins inducing positive supercoiling

SMC, structural maintenance of chromosomes. See the text for references.

Source Protein Activity Function 
(Hyper)thermophilic archaea and bacteria Reverse gyrase Topoisomerase, ATP-dependent positive supercoiling Regulation of DNA topology; DNA-damage response 
M. smegmatis Topoisomerase II Topoisomerase, ATP-dependent relaxation and positive supercoiling Unknown 
Pisum sativum (pea) Topoisomerase I Topoisomerase, ATP-independent DNA relaxation and positive supercoiling Unknown 
Eukaryotes, bacteria, archaea SMC DNA binding protein, ATP-dependent positive supercoiling DNA condensation; chromosome folding and segregation; gene regulation and DNA repair 
Eukaryotes CenH3 Right-handed DNA wrapping (with other histones) Centromere-specific histone 
Homo sapiens TRF2 DNA-binding protein Telomere homoeostasis; DNA condensation 
H. sapiens DEK DNA-binding protein Chromatin-associated protein; proto-oncogene 
E. coli SeqA DNA-binding protein Negative regulation of replication; chromosome organization 
S. solfataricus Smj12 DNA-binding protein Stabilization of the double helix 
Source Protein Activity Function 
(Hyper)thermophilic archaea and bacteria Reverse gyrase Topoisomerase, ATP-dependent positive supercoiling Regulation of DNA topology; DNA-damage response 
M. smegmatis Topoisomerase II Topoisomerase, ATP-dependent relaxation and positive supercoiling Unknown 
Pisum sativum (pea) Topoisomerase I Topoisomerase, ATP-independent DNA relaxation and positive supercoiling Unknown 
Eukaryotes, bacteria, archaea SMC DNA binding protein, ATP-dependent positive supercoiling DNA condensation; chromosome folding and segregation; gene regulation and DNA repair 
Eukaryotes CenH3 Right-handed DNA wrapping (with other histones) Centromere-specific histone 
Homo sapiens TRF2 DNA-binding protein Telomere homoeostasis; DNA condensation 
H. sapiens DEK DNA-binding protein Chromatin-associated protein; proto-oncogene 
E. coli SeqA DNA-binding protein Negative regulation of replication; chromosome organization 
S. solfataricus Smj12 DNA-binding protein Stabilization of the double helix 

A few studies reported about other DNA-binding proteins inducing constrained positive supercoiling in bacteria or eukaryotes: the E. coli SeqA protein, which is a negative regulator of chromosome replication and has a role in chromosome organization [23], and the human oncoprotein DEK, an abundant chromatin-associated protein, which introduces positive supercoils both into protein-free DNA and into DNA in chromatin [24].

Finally, two reports described atypical topoisomerases with positive supercoiling activities. A pea topoisomerase I in the absence of Mg2+ ions showed relaxation activity of both positive and negative supercoiled DNA, typical of Type IB topoisomerases; however, in the presence of Mg2+ ions, it introduces positive supercoils [25]. Moreover, a Type II topoisomerase from the bacterium Mycobacterium smegmatis, besides the canonical ATP-dependent DNA relaxation of negatively supercoiled DNA, also introduces positive supercoils into both relaxed and negatively supercoiled substrates [26]. However, neither the reaction mechanism nor the physiological role of these enzymes has been clarified.

Positive supercoiling in (hyper)thermophiles: only good?

Hyperthermophilic organisms may require specific mechanisms inducing positive supercoiling to counteract the denaturing effect of their growth temperature. Indeed, several lines of evidence suggest that DNA is more positive in (hyper)thermophilic archaea as compared with mesophiles: the plasmidic form of SSV1 (Sulfolobus shibatae virus 1) of the archaeon Sulfolobus shibatae (Topt>80°C) is positively supercoiled, and several plasmids from different hyperthermophilic strains were found in relaxed to positively supercoiled form [6,27]. In addition, all hyperthermophiles invariably possess the positive supercoiling inducing topoisomerase, reverse gyrase, which is the only hyperthermophilic-specific protein identified so far [28]. Reverse gyrase is a bimodular enzyme comprising an N-terminal domain structurally similar to SF2 (superfamily 2) helicases, fused to a C-terminal Type IA topoisomerase (Figure 1). Positive supercoiling activity requires ATP, high temperature and both protein domains [4,5]. Analysis of the isolated ATPase and topoisomerase domains of reverse gyrase showed that they form specific physical interactions, and, when combined, co-operate to achieve the ATP-dependent positive supercoiling activity [29]. In S. solfataricus, reverse gyrase participates in DNA-damage response [30,31], interacts with SSB (single-strand-binding protein) [32], and inhibits the translesion DNA polymerase PolY [33]. The relation between reverse gyrase positive supercoiling activity and its role in these processes is not clear. SSB stimulates reverse gyrase positive supercoiling activity [32]; remarkably, this latter is required to inhibit PolY, which has reduced affinity for positive DNA [33]. These results suggest the intriguing hypothesis that positive supercoiling might serve as a general mechanism to regulate DNA-acting enzymes through modification of DNA structure, not only in thermophiles.

In addition to reverse gyrase, S. solfataricus contains the DNA-binding protein Smj12, which belongs to the so-called BA (bacterial–archaeal) family of regulators. Unlike most members of this family, this protein induces positive supercoiling, which can be observed in topological assays in combination with the eukaryotic topoisomerase I [34]. Smj12 is not abundant, suggesting that it is not a general architectural protein, but rather has a specialized function and/or localization.

Despite the presence of these positive supercoiling inducing factors in (hyper)thermophiles, a complex picture concerning the genome topology of these organisms is emerging from several lines of evidence. Indeed, some hyperthermophilic bacteria [35] and archaea [36] possess both gyrase and reverse gyrase; in these organisms, plasmids are highly negatively supercoiled [27]; in addition, the knockout mutant of the reverse gyrase in the archaeon Thermococcus kodakaraensis was viable [37], although it was less thermotolerant than the wild-type, and the actual DNA topology in this mutant was not determined. Furthermore, a number of proteins in hyperthermophiles have been shown to induce negative supercoiling: these include Alba, a protein present in all archaea, whose activity is controlled by acetylation [38,39], and Sul7d, one of the main chromatin components of Sulfolobales, which also inhibits reverse gyrase activity [40]. Collectively, these data suggest that positive and negative supercoiled DNA might coexist in (hyper)thermophiles. Indeed, systems inducing negative supercoiling in (hyper)thermophiles might be needed locally or transiently in response to environmental or physiological changes (e.g. growth conditions, heat/cold shock, DNA damage and so on) and the actual topology under each physiological condition might depend on the interplay among multiple cellular and environmental factors. For instance, transient changes in DNA supercoiling might be essential to generate the temperature-stress response by regulating the expression of specific genes, but they could also be a consequence of the physical effects of temperature on cellular components [41].

In addition, (hyper)thermophilic archaea belonging to the subdomain Euryarchaeota contain tetrameric eukaryotic-like histones (reviewed in [42]), which display dual behaviour: they wrap DNA into positive supercoils at high salt concentrations, but into negative supercoils in low salt conditions [43,44]. Since internal salt concentrations are increased following temperature increase, temperature fluctuations could also be accommodated by changes in nucleosome topology. Archaeal histone mutants with residue replacements at sites responsible for dimer–dimer interactions wrap DNA into positive supercoils under all salt conditions [45]. Therefore the DNA topology in archaeal histone–DNA complexes might be controlled by regulating the histone dimer–tetramer equilibrium.

In S. solfataricus, multiple mechanisms appear to modify chromatin composition after DNA damage: UV irradiation induces recruitment of reverse gyrase to the chromatin [30], whereas the alkylating agent MMS (methyl methanesulfonate) induces reverse gyrase degradation and translocation of both Smj12 and Sul7d from the chromatin to the cytosol [31]; although the physiological meaning of these events is not clearly understood, they are likely to affect profoundly chromosome topology.

Finally, reverse gyrase might be viewed as a model of interaction of topoisomerases and helicases. For instance, RecQ helicases form, together with topoisomerase III, complexes involved in the maintenance of genome integrity that are strikingly conserved through the evolution, from bacteria to humans (reviewed in [46,47]). Interestingly, the yeast Sgs1 and Top3 complex was suggested to act as a potential eukaryotic reverse gyrase [48]; it will be thus interesting to test directly whether the combination of these enzymes with reverse gyrase modules might recapitulate the positive supercoiling activity.

Molecular Biology of Archaea II: A Biochemical Society Focused Meeting held at Robinson College, Cambridge, U.K., 16–18 August 2010. Organized and Edited by Stephen Bell (Oxford, U.K.) and Finn Werner (University College London, U.K.).

Abbreviations

     
  • NAP1

    nucleosome assembly protein 1

  •  
  • SSB

    single-strand-binding protein

  •  
  • TRF2

    telomere repeat factor 2

Funding

Work in our laboratory is partially supported by Agenzia Spaziale Italiana Project MoMa [grant number 1/014/06/0].

References

References
1
Champoux
J.J.
DNA topoisomerases: structure, function, and mechanism
Annu. Rev. Biochem.
2001
, vol. 
70
 (pg. 
369
-
413
)
2
Wang
J.C.
Cellular roles of DNA topoisomerases: a molecular perspective
Nat. Rev. Mol. Cell Biol.
2002
, vol. 
3
 (pg. 
430
-
440
)
3
Luijsterburg
M.S.
White
M.F.
van Driel
R.
Dame
R.T.
The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes
Crit. Rev. Biochem. Mol. Biol.
2008
, vol. 
43
 (pg. 
393
-
418
)
4
Nadal
M.
Reverse gyrase, an insight into the role of DNA-topoisomerases
Biochimie
2007
, vol. 
89
 (pg. 
447
-
455
)
5
Perugino
G.
Valenti
A.
D'Amaro
A.
Rossi
M.
Ciaramella
M.
Reverse gyrase and genome stability in hyperthermophilic organisms
Biochem. Soc. Trans.
2009
, vol. 
37
 (pg. 
69
-
73
)
6
Forterre
P.
Bergerat
A.
Lopez-Garcia
P.
The unique DNA topology and DNA topoisomerases of hyperthermophilic archaea
FEMS Microbiol. Rev.
1996
, vol. 
18
 (pg. 
237
-
248
)
7
Gupta
P.
Zlatanova
J.
Tomschik
M.
Nucleosome assembly depends on the torsion in the DNA molecule: a magnetic tweezers study
Biophys. J.
2009
, vol. 
97
 (pg. 
3150
-
3157
)
8
Timsit
Y.
Várnai
P.
Helical chirality: a link between local interactions and global topology in DNA
PLoS ONE
2010
, vol. 
19
 pg. 
e9326
 
9
Johnson
R.C.
Johnson
L.M.
Schmidt
J.
Gardner
J.F.
Higgins
N.P.
Higgins
N.P.
Major nucleoid proteins in the structure and function of the Escherichia coli chromosome
The Bacterial Chromosome
2005
Washington, DC
ASM Press
10
Luger
K.
Mader
A.W.
Richmond
R.K.
Sargent
D.F.
Richmond
T.J.
Crystal structure of the nucleosome core particle at 2.8 Å resolution
Nature
1997
, vol. 
389
 (pg. 
251
-
260
)
11
Sandman
K.
Reeve
J.N.
Archaeal chromatin proteins: different structures but common function?
Curr. Opin. Microbiol.
2005
, vol. 
8
 (pg. 
656
-
661
)
12
Gartenberg
M.R.
Wang
J.C.
Positive supercoiling of DNA greatly diminishes mRNA synthesis in yeast
Proc. Natl. Acad. Sci. U.S.A.
1992
, vol. 
89
 (pg. 
11461
-
11465
)
13
Joshi
R.S.
Pin
B.
Roca
J.
Positional dependence of transcriptional inhibition by DNA torsional stress in yeast chromosomes
EMBO J.
2010
, vol. 
29
 (pg. 
740
-
748
)
14
Kar
S.
Choi
E.J.
Guo
F.
Dimitriadis
E.K.
Kotova
S.L.
Adhya
S.
Right-handed DNA supercoiling by an octameric form of histone-like protein HU: modulation of cellular transcription
J. Biol. Chem.
2006
, vol. 
281
 (pg. 
40144
-
40153
)
15
Fierro-Fernández
M.
Hernández
P.
Krimer
D.B.
Stasiak
A.
Schvartzman
J.B.
Topological locking restrains replication fork reversal
Proc. Natl. Acad. Sci. U.S.A.
2007
, vol. 
104
 (pg. 
1500
-
1505
)
16
Bankhead
T.
Kobryn
K.
Chaconas
G.
Unexpected twist: harnessing the energy in positive supercoils to control telomere resolution
Mol. Microbiol.
2006
, vol. 
62
 (pg. 
895
-
905
)
17
Amiard
S.
Doudeau
M.
Pinte
S.
Poulet
A
Lenain
C.
Faivre-Moskalenko
C.
Angelov
D.
Hug
N.
Vindigni
A.
Bouvet
P.
, et al. 
A topological mechanism for TRF2-enhanced strand invasion
Nat. Struct. Mol. Biol.
2007
, vol. 
14
 (pg. 
147
-
54
)
18
Peterson
S.
Danowit
R.
Wunsch
A.
Jackson
V.
NAP1 catalyzes the formation of either positive or negative supercoils on DNA on basis of the dimer–tetramer equilibrium of histones H3/H4
Biochemistry
2007
, vol. 
46
 (pg. 
8634
-
8646
)
19
Furuyama
T.
Henikoff
S.
Centromeric nucleosomes induce positive DNA supercoils
Cell
2009
, vol. 
138
 (pg. 
104
-
113
)
20
Lavelle
C.
Recouvreux
P.
Wong
H.
Bancaud
A.
Viovy
J.L.
Prunell
A.
Victor
J.M.
Right-handed nucleosome: myth or reality?
Cell
2009
, vol. 
139
 (pg. 
1216
-
1217
)
21
Hudson
D.F.
Marshall
K.M.
Earnshaw
W.C.
Condensin: architect of mitotic chromosomes
Chromosome Res.
2009
, vol. 
17
 (pg. 
131
-
144
)
22
Lindow
J.C.
Britton
R.A.
Grossman
A.D.
Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo
J. Bacteriol.
2002
, vol. 
184
 (pg. 
5317
-
5322
)
23
Klungsøyr
H.K.
Skarstad
K.
Positive supercoiling is generated in the presence of Escherichia coli SeqA protein
Mol. Microbiol.
2004
, vol. 
54
 (pg. 
123
-
131
)
24
Waldmann
T.
Eckerich
C.
Baack
M.
Gruss
C.
The ubiquitous chromatin protein DEK alters the structure of DNA by introducing positive supercoils
J. Biol. Chem.
2002
, vol. 
277
 (pg. 
24988
-
24994
)
25
Reddy
M.K.
Nair
S.
Tewari
K.K.
Cloning, expression and characterization of a gene which encodes a topoisomerase I with positive supercoiling activity in pea
Plant Mol. Biol.
1998
, vol. 
37
 (pg. 
773
-
784
)
26
Jain
P.
Nagaraja
V.
An atypical type II topoisomerase from Mycobacterium smegmatis with positive supercoiling activity
Mol. Microbiol.
2005
, vol. 
58
 (pg. 
1392
-
1405
)
27
Charbonnier
F.
Forterre
P.
Comparison of plasmid DNA topology among mesophilic and thermophilic eubacteria and archaebacteria
J. Bacteriol.
1994
, vol. 
176
 (pg. 
1251
-
1259
)
28
Brochier-Armanet
C.
Forterre
P.
Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggest a complex hystory of vertical inheritance and lateral gene transfers
Archaea
2006
, vol. 
2
 (pg. 
i
-
xi
)
29
Valenti
A.
Perugino
G.
D'Amaro
A.
Cacace
A.
Napoli
A.
Rossi
M.
Ciaramella
M.
Dissection of reverse gyrase activities: insight into the evolution of a thermostable molecular machine
Nucleic Acids Res.
2008
, vol. 
36
 (pg. 
4587
-
4597
)
30
Napoli
A.
Valenti
A.
Salerno
V.
Nadal
M.
Garnier
F.
Rossi
M.
Ciaramella
M.
Reverse gyrase recruitment to DNA after UV light irradiation in Sulfolobus solfataricus
J. Biol. Chem.
2004
, vol. 
279
 (pg. 
33192
-
33198
)
31
Valenti
A.
Napoli
A.
Ferrara
M.C.
Nadal
M.
Rossi
M.
Ciaramella
M.
Selective degradation of reverse gyrase and DNA fragmentation induced by alkylating agent in the archaeon Sulfolobus solfataricus
Nucleic Acids Res.
2006
, vol. 
34
 (pg. 
2098
-
2108
)
32
Napoli
A.
Valenti
A.
Salerno
V.
Nadal
M.
Garnier
F.
Rossi
M.
Ciaramella
M.
Functional interaction of reverse gyrase with single-strand binding protein of the archaeon Sulfolobus
Nucleic Acids Res.
2005
, vol. 
33
 (pg. 
564
-
576
)
33
Valenti
A.
Perugino
G.
Nohmi
T.
Rossi
M.
Ciaramella
M.
Inhibition of translesion DNA polymerase by archaeal reverse gyrase
Nucleic Acids Res.
2009
, vol. 
37
 (pg. 
4287
-
4295
)
34
Napoli
A.
Kvaratskelia
M.
White
M.F.
Rossi
M.
Ciaramella
M.
A novel member of the bacterial–archaeal regulator family is a nonspecific DNA-binding protein and induces positive supercoiling
J. Biol. Chem.
2001
, vol. 
276
 (pg. 
10745
-
10752
)
35
Guipaud
O.
Marguet
E.
Noll
K.M.
de la Tour
C.B.
Forterre
P.
Both DNA gyrase and reverse gyrase are present in the hyperthermophilic bacterium Thermotoga maritima
Proc. Natl. Acad. Sci. U.S.A.
1997
, vol. 
94
 (pg. 
10606
-
10611
)
36
Forterre
P.
Gribaldo
S.
Gadelle
D.
Serre
M.C.
Origin and evolution of DNA topoisomerases
Biochimie
2007
, vol. 
89
 (pg. 
427
-
446
)
37
Atomi
H.
Matsumi
R.
Imanaka
T.
Reverse gyrase is not a prerequisite for hyperthermophilic life
J. Bacteriol.
2004
, vol. 
186
 (pg. 
4829
-
4833
)
38
Xue
H.
Guo
R.
Wen
Y.
Liu
D.
Huang
L.
An abundant DNA binding protein from the hyperthermophilic archaeon Sulfolobus shibatae affects DNA supercoiling in a temperature-dependent fashion
J. Bacteriol.
2000
, vol. 
182
 (pg. 
3929
-
3933
)
39
Bell
S.D.
Botting
C.H.
Wardleworth
B.N.
Jackson
S.P.
White
M.F.
The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation
Science
2002
, vol. 
29
 (pg. 
148
-
151
)
40
Napoli
A.
Zivanovic
Y.
Bocs
C.
Buhler
C.
Rossi
M.
Forterre
P.
Ciaramella
M.
DNA bending, compaction and negative supercoiling by the architectural protein Sso7d of Sulfolobus solfataricus
Nucleic Acids Res.
2002
, vol. 
30
 (pg. 
2656
-
2662
)
41
López-García
P.
Forterre
P.
DNA topology and the thermal stress response, a tale from mesophiles and hyperthermophiles
BioEssays
2000
, vol. 
22
 (pg. 
738
-
746
)
42
Reeve
J.N.
Bailey
K.A.
Li
W.T.
Marc
F.
Sandman
K.
Soares
D.J.
Archaeal histones: structures, stability and DNA binding
Biochem. Soc. Trans.
2004
, vol. 
32
 (pg. 
227
-
230
)
43
Musgrave
D.
Sandman
K.M.
Reeve
J.N.
DNA binding by the archaeal histone HMf results in positive supercoiling
Proc. Natl. Acad. Sci. U.S.A.
1991
, vol. 
88
 (pg. 
10397
-
10401
)
44
Musgrave
D.
Forterre
P.
Slesarev
A.
Negative constrained DNA supercoiling in archaeal nucleosomes
Mol. Microbiol.
2000
, vol. 
35
 (pg. 
341
-
349
)
45
Marc
F.
Sandman
K.
Lurz
R.
Reeve
J.N.
Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling
J. Biol. Chem.
2002
, vol. 
277
 (pg. 
30879
-
30886
)
46
Cobb
J.A.
Bjergbaek
L.
RecQ helicases: lessons from model organisms
Nucleic Acids Res.
2006
, vol. 
34
 (pg. 
4106
-
4114
)
47
Vindigni
A.
Hickson
I.D.
RecQ helicases: multiple structures for multiple functions?
HFSP J.
2009
, vol. 
3
 (pg. 
153
-
164
)
48
Gangloff
S.
McDonald
J.P.
Bendixen
C.
Arthur
L.
Rothstein
R.
The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase
Mol. Cell. Biol.
1994
, vol. 
14
 (pg. 
8391
-
8398
)