Determinants of Specific Binding of HMGB1 Protein to Hemicatenated DNA Loops
Identifieur interne : 001E07 ( Main/Exploration ); précédent : 001E06; suivant : 001E08Determinants of Specific Binding of HMGB1 Protein to Hemicatenated DNA Loops
Auteurs : Sandrine Jaouen [France] ; Leanne De Koning [France] ; Claire Gaillard [France] ; Eva Muselíková-Polanská [République tchèque] ; Michal Štros [République tchèque] ; François Strauss [France]Source :
- Journal of Molecular Biology [ 0022-2836 ] ; 2005.
English descriptors
- mix :
Abstract
Protein HMGB1 has long been known as one of the most abundant non-histone proteins in the nucleus of mammalian cells, and has regained interest recently for its function as an extracellular cytokine. As a DNA-binding protein, HMGB1 facilitates DNA–protein interactions by increasing the flexibility of the double helix, and binds specifically to distorted DNA structures. We have previously observed that HMGB1 binds with extremely high affinity to a novel DNA structure, hemicatenated DNA loops (hcDNA), in which double-stranded DNA fragments containing a tract of poly(CA)·poly(TG) form a loop maintained at its base by a hemicatenane. Here, we show that the single HMGB1 domains A and B, the HMG-box domain of sex determination factor SRY, as well as the prokaryotic HMGB1-like protein HU, specifically interact with hcDNA (Kd0.5 nM). However, the affinity of full-length HMGB1 for hcDNA is three orders of magnitude higher (Kd<0.5 pM) and requires the simultaneous presence of both HMG-box domains A and B plus the acidic C-terminal tail on the molecule. Interestingly, the high affinity of the full-length protein for hcDNA does not decrease in the presence of magnesium. Experiments including a comparison of HMGB1 binding to hcDNA and to minicircles containing the CA/TG sequence, binding studies with HMGB1 mutated at intercalating amino acid residues (involved in recognition of distorted DNA structures), and exonuclease III footprinting, strongly suggest that the hemicatenane, not the DNA loop, is the main determinant of the affinity of HMGB1 for hcDNA. Experiments with supercoiled CA/TG-minicircles did not reveal any involvement of left-handed Z-DNA in HMGB1 binding. Our results point to a tight structural fit between HMGB1 and DNA hemicatenanes under physiological conditions, and suggest that one of the nuclear functions of HMGB1 could be linked to the possible presence of hemicatenanes in the cell.
Url:
DOI: 10.1016/j.jmb.2005.08.073
Affiliations:
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Le document en format XML
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<affiliation wicri:level="1"><hal:affiliation type="laboratory" xml:id="struct-1131" status="OLD"> <idno type="RNSR">199712638E</idno>
<idno type="IdRef">026536412</idno>
<orgName>Institut Jacques Monod</orgName>
<orgName type="acronym">IJM (UMR_7592)</orgName>
<date type="end">2019-12-31</date>
<desc> <address> <addrLine>Université Paris Diderot, Bât. Buffon, 15 rue Hélène Brion, 75205 Paris cédex 13</addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://www.ijm.fr/</ref>
</desc>
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<relation name="UMR_7592" active="#struct-441569" type="direct"></relation>
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<idno type="IdRef">027542084</idno>
<orgName>Université Paris Diderot - Paris 7</orgName>
<orgName type="acronym">UPD7</orgName>
<desc> <address> <addrLine>5 rue Thomas-Mann - 75205 Paris cedex 13</addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://www.univ-paris-diderot.fr</ref>
</desc>
</org>
</tutelle>
<tutelle name="UMR_7592" active="#struct-441569" type="direct"><org type="institution" xml:id="struct-441569" status="VALID"> <idno type="IdRef">02636817X</idno>
<idno type="ISNI">0000000122597504</idno>
<orgName>Centre National de la Recherche Scientifique</orgName>
<orgName type="acronym">CNRS</orgName>
<date type="start">1939-10-19</date>
<desc> <address> <country key="FR"></country>
</address>
<ref type="url">http://www.cnrs.fr/</ref>
</desc>
</org>
</tutelle>
</tutelles>
</hal:affiliation>
<country>France</country>
</affiliation>
</author>
</analytic>
<idno type="DOI">10.1016/j.jmb.2005.08.073</idno>
<series><title level="j">Journal of Molecular Biology</title>
<idno type="ISSN">0022-2836</idno>
<imprint><date type="datePub">2005</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass><keywords scheme="mix" xml:lang="en"><term>DNA knot</term>
<term>DNA topoisomers</term>
<term>HMG-box domain</term>
<term>alternative DNA conformations</term>
<term>chloroquine gels</term>
<term>fractionation</term>
<term>hemicatenane</term>
<term>high-mobility group proteins</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"> <p>Protein HMGB1 has long been known as one of the most abundant non-histone proteins in the nucleus of mammalian cells, and has regained interest recently for its function as an extracellular cytokine. As a DNA-binding protein, HMGB1 facilitates DNA–protein interactions by increasing the flexibility of the double helix, and binds specifically to distorted DNA structures. We have previously observed that HMGB1 binds with extremely high affinity to a novel DNA structure, hemicatenated DNA loops (hcDNA), in which double-stranded DNA fragments containing a tract of poly(CA)·poly(TG) form a loop maintained at its base by a hemicatenane. Here, we show that the single HMGB1 domains A and B, the HMG-box domain of sex determination factor SRY, as well as the prokaryotic HMGB1-like protein HU, specifically interact with hcDNA (Kd0.5 nM). However, the affinity of full-length HMGB1 for hcDNA is three orders of magnitude higher (Kd<0.5 pM) and requires the simultaneous presence of both HMG-box domains A and B plus the acidic C-terminal tail on the molecule. Interestingly, the high affinity of the full-length protein for hcDNA does not decrease in the presence of magnesium. Experiments including a comparison of HMGB1 binding to hcDNA and to minicircles containing the CA/TG sequence, binding studies with HMGB1 mutated at intercalating amino acid residues (involved in recognition of distorted DNA structures), and exonuclease III footprinting, strongly suggest that the hemicatenane, not the DNA loop, is the main determinant of the affinity of HMGB1 for hcDNA. Experiments with supercoiled CA/TG-minicircles did not reveal any involvement of left-handed Z-DNA in HMGB1 binding. Our results point to a tight structural fit between HMGB1 and DNA hemicatenanes under physiological conditions, and suggest that one of the nuclear functions of HMGB1 could be linked to the possible presence of hemicatenanes in the cell.</p>
</div>
</front>
</TEI>
<affiliations><list><country><li>France</li>
<li>République tchèque</li>
</country>
</list>
<tree><country name="France"><noRegion><name sortKey="Jaouen, Sandrine" sort="Jaouen, Sandrine" uniqKey="Jaouen S" first="Sandrine" last="Jaouen">Sandrine Jaouen</name>
</noRegion>
<name sortKey="De Koning, Leanne" sort="De Koning, Leanne" uniqKey="De Koning L" first="Leanne" last="De Koning">Leanne De Koning</name>
<name sortKey="Gaillard, Claire" sort="Gaillard, Claire" uniqKey="Gaillard C" first="Claire" last="Gaillard">Claire Gaillard</name>
<name sortKey="Strauss, Francois" sort="Strauss, Francois" uniqKey="Strauss F" first="François" last="Strauss">François Strauss</name>
</country>
<country name="République tchèque"><noRegion><name sortKey="Muselikova Polanska, Eva" sort="Muselikova Polanska, Eva" uniqKey="Muselikova Polanska E" first="Eva" last="Muselíková-Polanská">Eva Muselíková-Polanská</name>
</noRegion>
<name sortKey="Stros, Michal" sort="Stros, Michal" uniqKey="Stros M" first="Michal" last="Štros">Michal Štros</name>
</country>
</tree>
</affiliations>
</record>
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