Topological consequences of cc-dsDNA binding to a protein and a model
for the binding of cc-dsDNA to Mhr1. The extension and associated
untwisting of cc-dsDNA that are required for homologous pairing are induced by
RecA/Rad51 binding (29) and
generate positive (or left-handed) supercoils in the remaining part of the
cc-dsDNA (DNA 2). This type of untwisting is observed as the
formation of negatively supercoiled cc-dsDNA by the topoisomerase I treatment
of cc-dsDNA bound to RecA/Rad51, followed by the removal of proteins (DNA
5). When the substrate cc-dsDNA for homologous pairing is negatively
supercoiled, the positive supercoils that are generated during the reaction
are neutralized, and thus, the negative supercoils stimulate homologous
pairing by RecA (11). On the
other hand, the right-handed wrapping around a protein generates negative (or
right-handed) supercoils (DNA 3). This is observed as the generation
of positively supercoiled cc-dsDNA, when the cc-dsDNA bound to human Rad52 is
treated with topoisomerase I and the proteins are removed (DNA 6)
(41). The positive supercoils
generated by untwisting can be canceled by the negative supercoils generated
by the right-handed wrapping (DNA 4). If the substrate cc-dsDNA is
negatively supercoiled, then the negative supercoils prevent right-handed
wrapping. These phenomena explain our finding that the negative supercoils of
cc-dsDNA prevent homologous pairing by Mhr1 (Figs.
3,
4,
6, and
7) and that the treatment of
the cc-dsDNA-Mhr1 complex with topoisomerase generates neither positive nor
negative supercoils, as shown in Fig.
8B. The cancellation of the positive supercoils and the
negative supercoils is not necessarily complete. In the case of the
Rad52-cc-dsDNA complex, the negative supercoils generated by the wrapping are
larger than the positive supercoils generated by the untwisting. This figure
represents the change by a single unit of supercoil or twist, caused by the
binding of originally relaxed cc-dsDNA (DNA 1) to a protein for simplicity.
W, writhing number of the entire cc-dsDNA; Wn,
local writhing number; ΔWn, local changes in writhe
(positive values, left-handed supercoiling or right-handed wrapping);
ΔTn, local change in twist (negative values,
untwisting) in region n. Subscripts 1 and 2
indicate the protein-bound region of the DNA molecule and the remaining region
of the DNA (where ΔT2 = 0), respectively. The
subscript p indicates the values after topoisomerase treatment.
Before topoisomerase treatment, the sum of the local changes in writhe and
twist is zero, because there is no change in the linking number. If the
substrate dsDNA is relaxed (W = 0), then W2 is
equal to ΔW2. The treatment of the protein-DNA
complex by topoisomerase I results in the relaxing of W2 (to become
0). After the removal of proteins, Wp, which is the sum of
W1 and W2 (equal to 0), is equal to
the sum of ΔT1 and
ΔW1.