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Spiral Structure of Escherichia Coli HU Provides Foundation for DNA Supercoiling

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Spiral Structure of Escherichia Coli HU Provides Foundation for DNA Supercoiling Spiral structure of Escherichia coli HU␣␤ provides foundation for DNA supercoiling Fusheng Guo and Sankar Adhya* Laboratory of Molecular Biology, National Cancer Institute, Bethesda, MD 20892-4264 Contributed by Sankar Adhya, January 4, 2007 (sent for review October 5, 2006) We determined the crystal structure of the Escherichia coli nucleoid- Table 1. Statistics of data collection, molecular replacement, associated HU␣␤ protein by x-ray diffraction and observed that the and refinement heterodimers form multimers with octameric units in three potential arrangements, which may serve specialized roles in different DNA Diffraction datasets transaction reactions. It is of special importance that one of the Resolution, Å 2.5 structures forms spiral filaments with left-handed rotations. A neg- Unique reflection 7,730 atively superhelical DNA can be modeled to wrap around this left- Rmerge* (outer bin) 0.039 (0.399) handed HU␣␤ multimer. Whereas the wild-type HU generated neg- Compl., % (outer bin) 92.8 (72.9) ative DNA supercoiling in vitro, an engineered heterodimer with an Redundancy 6.2 altered amino acid residue critical for the formation of the left-handed Refinement spiral protein in the crystal was defective in the process, thus pro- No. of residues 167 viding the structural explanation for the classical property of HU to No. of nonhydrogen atoms 1,068 restrain negative supercoils in DNA. No. of solvents 24 No. of Ni 1 HU-multimers ͉ nucleoid ͉ x-ray crystallography No. of Cl 1 Resolution range, Å 20–2.5 R† (outer) 0.226 (0.357) he bacterial nucleoid is distinguished from the eukaryotic R † (outer) 0.258 (0.405) chromosome structure by the ostensible lack of an ordered free T rmsd bond, Å 0.017 nucleosomal structure, which characteristically influences gene rmsd bond angle, ° 1.514 expression pattern. In Escherichia coli, the 4.6-Mb circular DNA rmsd chiral, ° 0.088 chromosome with a 1.6-mm circumference is condensed 1,000-fold to a diameter of 1 ␮m in the nucleoid (1). Although it has been *Rmerge ϭ Α͉I Ϫ͗I͉͘/ΑI, where I and ͗I͘ are the observed intensity and the mean suggested that DNA compaction in the nucleoid is caused by intensity of the same reflection from multiple measurements. Summation is extensive negative supercoiling, the involvement of several proteins, over all reflections. † ϭ Α ͉ ͉ Ϫ ͉ ͉ Α͉ ͉ e.g., HU, HNS, FIS, and SeqA, also in the compaction is now widely R ( Fo Fc )/ Fo , where Fo is the measured structure factor and Fc is the accepted (1, 2). However, the precise structure of the nucleoid, and calculated structure factor from the model. the exact role of these proteins in the nucleoid formation is unknown. Despite the deficiency in our knowledge about the three different forms, two of which exhibit distinct spiral multimers. nucleoid physical structure and any influence a structure may have The replacement of the ␤-E38 residue, critical for interdimeric on gene expression, it was found that specific amino acid changes interface in the left-handed spiral, by alanine affected the negative in the E. coli HU qualitatively change the morphology and the DNA supercoiling capacity in vitro. We discuss the significance of transcription profile of cells profoundly (3). The latter observation the findings in nucleoid biology. BIOCHEMISTRY suggests that HU may be involved in nucleoid structure in an influential way not appreciated previously. Results HU contains two homologous subunits, ␣ and ␤, 9.5 kDa each. X-Ray Structure. The diffraction data were collected from a crystal HU also exists as ␣␣ and ␤␤ homodimers, in different stages of cell with a tetragonal space group I4 with unit cell dimensions of a ϭ growth (4). Although HU binds to DNA nonspecifically, it shows 1 b ϭ 82.915 Å and c ϭ 61.048 Å with one heterodimer in an a propensity for binding to distorted, bent, or Holliday-junction asymmetric unit. The parameters of data collection and refinement DNA, an ability that may aid DNA compaction (5). HU and are presented in Table 1. The local environments of the residues 12 topoisomerase I acting in concert also regulate DNA supercoiling ␣␤ both in vivo and in vitro (6, 7). In HU-deficient mutants, partially and 13 support the assignment of the heterodimers. In the ␣-subunit, E12 and K13 form two salt bridges with ␤-K18 of an relaxed DNA is compensated by altered levels of topoisomerase I ␤ or DNA gyrase (8, 9). Indeed, E. coli nucleoids in the absence of adjacent dimer and -E34 of the same dimer, respectively (Fig. 1a). In the ␤-subunit, A12 and G13 have no crystal contact (Fig. 1b). HU are significantly enlarged in volume (10). Ϫ ␣ ␣ That specific mutants of HU protein qualitatively change the cell The 2Fo Fc omit map of -E12 and -K13 shows apparent transcription profile suggests that the HU-mediated DNA struc- electron density at the site of the deleted residues at cutoff of 1.0 Ϫ tural change results in a defined architecture (topological or oth- and the corresponding Fo Fc omit map shows positive electron erwise) that guides the transcription pattern in cell. Although HU also plays specific roles in many DNA metabolic reactions (11–14), Author contributions: F.G. and S.A. designed research; F.G. performed research; F.G. and by well studied mechanisms, a relation between an HU-influenced S.A. analyzed data; and F.G. and S.A. wrote the paper. nucleoid structure and global gene expression profile is elusive. It The authors declare no conflict of interest. was also suggested that HU antagonizes, not aids, DNA supercoil- Data deposition: The structure factors have been deposited in the Protein Data Bank, ing (15). www.pdb.org (PDB ID code 2O97). ␣␤ We report here the structure of the E. coli HU heterodimer *To whom correspondence should be addressed at: National Cancer Institute, 37 Convent crystals determined by x-ray diffraction. The crystal structure of the Drive, Room 5138, Bethesda, MD 20892-4264. E-mail: [email protected]. heterodimer, unlike the structures of HU homodimers from E. coli This article contains supporting information online at www.pnas.org/cgi/content/full/ and other bacteria, show stacked dimers with octameric repeats in 0611686104/DC1. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0611686104 PNAS ͉ March 13, 2007 ͉ vol. 104 ͉ no. 11 ͉ 4309–4314 Downloaded by guest on October 1, 2021 Fig. 2. Residues that contribute to the hydrophobic core of E. coli HU. Those in red directly contribute to dimerization. The underlined residues are differ- ent in ␣ and ␤ chains. The italicized residues are those whose counterparts in the opposite chain are polar or charged. ␣-K18, ␣-K73, ␤-K9, ␤-D15, ␤-K18, ␤-K75, and ␤-K83 are invisible. Although required for crystallization, the DNA fragment was missing in the electron density map. The crystals when dissolved in buffer showed a spectrum with significant OD at 260 nm, whereas pure HU␣␤ solution had no distinct absorbance at that wavelength. It is possible that a trace amount of DNase activity, intrinsic or extraneous, in the HU preparation damaged the DNA so as not to show any ordered electron density. Indeed, we detected a very low DNase activity in the preparation when a 32P-labeled pBR332 plasmid DNA was incubated overnight at 37°C with the HU preparation supplemented with 10 mM MgCl2. Because different DNA duplexes (SI Table 2) used in crystallization enabled HU␣␤ to form the same type of crystals, perhaps DNA molecules acted as a ‘‘general salt’’ in crystallization. General Structure. The secondary structural elements of the HU␣␤ heterodimer are comparable to the previously reported structures of HU homodimers of Thermotoga maritima, Bacillus stearother- mophilus, Anabaena, and HU␣␣ of E. coli (16–20). The superim- position of the structures of the ␣- and the ␤-subunits gives an rms deviation (rmsd) of 0.895 Å per 69 C␣ atoms. The structures of the E. coli HU␣␤ heterodimer reported here and that of the ␣␣ homodimer (16) are superimposable with an rmsd of 0.807 Å per 140 C␣ atoms. The superimposition of two ␣␤ heterodimers, when the ␣- and ␤-subunits of one dimer are reversed, gave an rmsd of 0.905 Å per 139 C␣ atoms. Both ␣ and ␤ chains in the heterodimer consist of three helices and three antiparallel strands: helix 1 (residues 2–13), helix 2 (17–38), helix 3 (82–90), strand 1 (40–45), strand 2 (47–54), and strand 3 (75–81). The B-factor profiles indicate that the ␤-subunit residues, par- ticularly the first 20 and the last 10, are slightly less ordered than the ones in the ␣-subunit in the crystal packing environment. The folding of a monomer is maintained by core hydrophobic residues; Fig. 1. Snapshots of electron density maps of residues 12 and 13 as finger residues L6, I7, I10, A11, A21, and L25 interact with each other to prints of the ␣ and ␤ chains. (a) E12 and K13 of the ␣-subunit. (b) A12 and G13 generate a V-shape between helix 1 and helix 2, whereas residues ␤ Ϫ of .(c) The same region of a with E12 and K13 omitted. The 2Fo Fc map ␣-I32 (␤-V32), L36, V42, F50, V52, and P77 hold helix 2 and the Ϫ cutoff at 1 is in green. The positive Fo Fc map cutoff at 3 is in red. The red and three strands in a given conformation in both subunits. Most of blue text indicates separate HU dimer molecules. these residues also participate in dimerization (see below), making the formation of monomers and dimers interdependent. density at cutoff of 3.0, especially on the location of the side chain Dimerization. The two monomers interwind into a dimer as a unit. ␣ ⌲ of - 13 (Fig.
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