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Genes to Cells (2008) 13, 1127-1140. doi:10.1111/j.1365-2443.2008.01233.x
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Crystal structure of Methanococcus jannaschii TATA box-binding protein

 Naruhiko Adachi1,2,3, Miki Senda3, Ryo Natsume3, Toshiya Senda4,* and Masami Horikoshi1,2,*

1 Horikoshi Gene Selector Project, Exploratory Research for Advanced Technology (ERATO), Japan Science and Technology Corporation (JST), 5-9-6 Tokodai, Tsukuba-shi, Ibaraki 300-2635, Japan
2 Laboratory of Developmental Biology, Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan
3 Protein Structural Information Analysis Team, Japan Biological Informatics Consortium (JBIC), 2-42 Aomi, Koto-ku, Tokyo 135-0064, Japan
4 Biomedicinal Information Research Center (BIRC), National Institute of Advanced Industrial Science and Technology (AIST), 2-42 Aomi, Koto-ku, Tokyo 135-0064, Japan


   Abstract
Top
 Abstract
Introduction
 Results
 Discussion
 Experimental procedures
 References
 
As the archaeal transcription system consists of a eukaryotic-type transcription apparatus and bacterial-type regulatory transcription factors, analyses of the molecular interface between the transcription apparatus and regulatory transcription factors are critical to reveal the evolutionary change of the transcription system. TATA box-binding protein (TBP), the central components of the transcription apparatus are classified into three groups: eukaryotic, archaeal-I and archaeal-II TBPs. Thus, comparative functional analysis of these three groups of TBP is important for the study of the evolution of the transcription system. Here, we present the first crystal structure of an archaeal-II TBP from Methanococcus jannaschii. The highly conserved and group-specific conserved surfaces of TBP bind to DNA and TFIIB/TFB, respectively. The phylogenetic trees of TBP and TFIIB/TFB revealed that they evolved in a coupled manner. The diversified surface of TBP is negatively charged in the archaeal-II TBP, which is completely different from the case of eukaryotic and archaeal-I TBPs, which are positively charged and biphasic, respectively. This difference is responsible for the diversification of the regulatory functions of TBP during evolution.


   Introduction
Top
 Abstract
 Introduction
Results
 Discussion
 Experimental procedures
 References
 
There are three biological kingdoms on earth: eukaryotes, archaea, and bacteria (Woese et al. 1990). Morphologically, archaea are similar to bacteria. Archaea and bacteria are of similar size and each have a single large circular plasmid and a small genome (most are in the range of 1.5–4.0 x 106 bp) (Woese et al. 1990). In addition, archaeal and bacterial cells lack a nuclear envelope and subcellular organelles (e.g. mitochondria, lysosome, and endoplasmic reticula) (Woese et al. 1990). In contrast, the molecular organization of archaea is more closely related to that in eukaryotes than to that in bacteria. Archaeal replication and translation are carried out by eukaryotic-type components (e.g. DNA polymerase family B and 16S rRNA, respectively) rather than bacterial-type ones (Bell & Jackson 1998; Reeve 2003; Barry & Bell 2006). Most archaea have eukaryotic-type chromatin factors (e.g. histones), but bacteria do not.

The archaeal transcription reaction is carried out by a eukaryotic-type transcription apparatus, which contains transcription enzyme(s) and initiation factor(s) (Supporting Information Table S1) (Geiduschek & Ouhammouch 2005; Li et al. 2007). The subunit structure of archaeal RNA polymerase, a transcription enzyme, closely resembles that of eukaryotic RNA polymerase II rather than that of bacterial RNA polymerase (Zillig et al. 1978) (Supporting Information Table S1). The primary structures of transcription initiation factors in the archaeal system, TATA box-binding protein (TBP) (Marsh et al. 1994; Rowlands et al. 1994), TFB (corresponding to eukaryotic TFIIB) (Ouzounis & Sander 1992), and TFE (corresponding to eukaryotic TFIIE{alpha}) (Bell et al. 2001; Hanzelka et al. 2001), are also similar to those in the eukaryotic RNA polymerase II system (Supporting Information Table S1). As archaea have no bacterial-type transcription initiation factor ({sigma} factor), it is believed that the archaeal transcription system is more similar to the eukaryotic one than to the bacterial one, though archaea lack several eukaryotic-type subunits of RNA polymerase II (Rpb8 and Rpb9), transcription initiation factors in the RNA polymerase II system (TFIIA, TFIIEβ, TFIIF, TFIIH, and TAFs) and the factors in the RNA polymerase I and III systems examined thus far (Bell & Jackson 2001; Geiduschek & Ouhammouch 2005).

Although the archaeal transcription apparatus is similar to the eukaryotic one, archaea have only a few eukaryotic-type regulatory transcription factors (Bell & Jackson 2001; Geiduschek & Ouhammouch 2005). In addition, there are few archaea-specific-type regulatory transcription factors. Most archaeal regulatory transcription factors are of the bacterial-type (Aravind & Koonin 1999; Kyrpides & Ouzounis 1999). Archaea mainly utilize bacterial helix-turn-helix (HTH)-type regulatory transcription factors (i.e. DtxR family protein (MJ0568), PbsX family protein (MJ0272), Lrp/AsnC family protein (MJ0151 and MJ0723), ArsR family protein (MJ1325 and MJ1553), and LysR family protein (MJ0300 and MJ1120)) (Aravind & Koonin 1999; Kyrpides & Ouzounis 1999). The bacterial ribbon-helix-helix-type regulatory transcription factors also exist in archaea (i.e. Arc/MetJ family protein (MJ0080, MJ0549, and MJ0767)) (Aravind & Koonin 1999; Kyrpides & Ouzounis 1999).

As the archaeal transcription system is a "hybrid" of eukaryotic and bacterial systems, the interaction between the eukaryotic-type transcription apparatus and bacterial-type regulatory transcription factors in archaea should be different from that within eukaryotes or bacteria. A study with an in vitro reconstituted transcription system of Methanococcus jannaschii (Mj) by Ouhammouch and Geiduschek showed that the eukaryotic-type TBP binds to the TATA box and the complex is stabilized by the bacterial-type regulatory transcription factor (MjPtr2) which binds to its DNA recognition element (Ouhammouch et al. 2003). This complex activates the transcription initiation reaction (Ouhammouch et al. 2003), suggesting that archaeal TBP contains two distinct surfaces: an evolutionarily conserved surface for the transcription apparatus and an evolutionarily diversified surface for regulatory transcription factors (Kornberg 2007).

Recently, we classified TBP into three groups based on their primary structure: three groups of TBPs are defined as eukaryotic, archaeal-I, and archaeal-II TBPs (Adachi et al. 2004). This classification was also supported by the following analyses. First, a pairwise comparison of the primary structures of TBP indicated that eukaryotic TBP is distinct from archaeal-I and -II TBPs. The TBP core domain is highly conserved among eukaryotes (approximately 80% identity on average) (Fig. 1A and Supporting Information Fig. S1). In contrast, the identity between eukaryotic and archaeal-I TBPs (approximately 40% identity on average) is relatively low and is nearly the same as that between eukaryotic and archaeal-II TBPs (approximately 40% identity on average). The identity between archaeal-I and archaeal-II TBPs is also relatively low (approximately 40% identity on average), suggesting that archaeal-I and archaeal-II TBPs belong to distinct groups. Second each TBP group has its characteristic N- and C-tail regions. As shown in Fig. 1B, the N- and C-tail regions show differences among the groups. The N-tail region of eukaryotic TBP varies in amino acid sequence and length depending on the species (17–160 amino acids long) (Supporting Information Fig. S2). Archaeal-I TBP has a 2–7 amino-acid-long N-tail region and a glutamate-rich C-tail region. Archaeal-II TBP has almost no N- and C-tail regions, and shows a minimum composition of only the core domain. Thirdly, each group has its characteristic ratio of acidic residues to all charged residues (Adachi et al. 2004) (Fig. 1C), suggesting that the electrostatic potential differs from group to group. Indeed, the crystal structures showed that the surface electrostatic potentials of eukaryotic TBP (positively charged) and archaeal-I TBP (biphasic) differ significantly, although their structures are essentially the same (Fig. 1D and Supporting Information Fig. S3) (Nikolov et al. 1992; Chasman et al. 1993; DeDecker et al. 1996; Kosa et al. 1997; Littlefield et al. 1999; Koike et al. 2004).


Figure 1
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  		Figure 1  Classification of TATA box-binding protein (TBP). (A) The average values of the sequence identity ratios calculated by the pairwise sequence comparisons. The results of these comparisons fell into six categories. The average value and standard deviation in each category were calculated and shown in the graph. The six categories of the comparison are as follows: comparisons within the eukaryote group, within the archaea-I group, within the archaea-II group, between the eukaryote and archaea-I groups (eu x arc-I), between the eukaryote and archaea-II groups (eu x arc-II), and between the archaea-I and archaea-II groups (arc-I x arc-II). The gene IDs of the sequences used in these calculations are shown in Supporting Information Table S2. Only amino acid sequences of the core domains were used for the calculations. (B) Domain structure of TBP. Arrows indicate the direct repeats of the core domain of TBP. Hs, Homo sapiens; At, Arabidopsis thaliana; Sc, Saccharomyces cerevisiae; Sa, Sulfolobus acidocaldarius; Pw, Pyrococcus woesei; Mj, Methanococcus jannaschii. (C) Histogram showing the acidic residue ratios in the core domain of TBP. Blue, grey and red bars represent eukaryotic, archaeal-I, and archaeal-II TBPs, respectively. (D) Electrostatic potential of HsTBP and SaTBP. The upper and lower panels show the results for HsTBP and SaTBP, respectively. The left panel shows the "front" view. The panels beside the left panel provide the back, top, and bottom views, respectively. Arrowheads indicate the negatively charged surface.

 
For a comparative functional study of the molecular interactions between TBP and the transcription apparatuses/ regulatory transcription factors in the respective groups at the atomic level, tertiary structural information of TBP in all groups is required. However, no tertiary structures of archaeal-II TBP have been reported. Here, we determined the crystal structure of an archaeal-II TBP (MjTBP) at 1.9 Å resolution for the first time. MjTBP has a structure similar to eukaryotic (At and Sc) and archaeal-I (Pw and Sa) TBPs. The surface of MjTBP is negatively charged, which is very different from the case of eukaryotic and archaeal-I TBPs surfaces. A structural comparison of the three groups of TBP revealed that the DNA- and TFIIB/TFB-binding residues of TBP form conserved surfaces, but other residues form diversified surfaces. These analyses seem to provide a reasonable solution to problems raised from conserved and diversified interactions within the archaeal transcription system.


   Results
Top
 Abstract
 Introduction
 Results
Discussion
 Experimental procedures
 References
 
Crystal structure of Methanococcus jannaschii TBP

Methanococcus jannaschii TBP (MjTBP), which is evolutionarily far from the structurally known TBPs, belongs to the archaeal-II group. As M. jannaschii is the only archaea whose in vitro reconstituted transcription system has been developed (Werner & Weinzierl 2002; Ouhammouch et al. 2003), MjTBP is a good source for further investigation of the evolutionary differences in the regulatory mechanisms of transcription initiation.

The crystal structure of the full-length MjTBP was determined at 1.9 Å resolution by the molecular replacement method using the crystal structure of Sulfolobus acidocaldarius TBP (SaTBP) as a search model (Koike et al. 2004) (Fig. 2A). The asymmetric unit contains four TBP monomers (chains A, B, P, and Q) with 251 water molecules (chains P and Q are shown in Fig. 2B; data collection and refinement statistics are shown in Table 1). This is the first crystal structure of an archaeal-II TBP. The crystal structure showed that MjTBP has a structure similar to other TBPs (At, Sc, Sa and PwTBPs). Least-squares fittings of these structures gave root mean square distances (RMSDs) of 1.41–2.60 Å for 172 C{alpha} atoms in the core domain (Table 2A). As observed in At, Sc, Sa, and PwTBPs, MjTBP forms a dimer in the crystal through the interaction with their second stirrup regions of the core domain (Fig. 2B) (Nikolov et al. 1992; Chasman et al. 1993; DeDecker et al. 1996; Koike et al. 2004).


Figure 2
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  		Figure 2  Crystal structure of Methanococcus jannaschii TATA box-binding protein (MjTBP). (A) 2Fo-Fc electron density map of MjTBP. (B) Ribbon drawing of MjTBP showing two molecules in the asymmetric unit. Chains P and Q are shown in magenta and yellow, respectively. The asymmetric unit contains two TBP dimers (chains A–B and P–Q). The N- and C-terminals of each chain and helices H2 and H2' are labeled. (C) Superposition of the H2 helices (corresponding to the region from Lys69 to Ile146 of MjTBP) of At, Sc, Sa, Pw and MjTBP, which are shown in green, magenta, salmon, yellow and cyan, respectively. When the five N-terminal residues of helix H2 (corresponding to Lys69–Glu73 in MjTBP; right side) are superposed, the position of the C-terminal residue of helix H2 (corresponding to Lys84 in MjTBP; left side) deviates within the range of 0.89–1.80 Å in the comparison of the residues between eukaryotic and archaeal-I TBPs. However, the deviation of the position of the C-terminal residues of helix H2 is 3.43–5.00 Å when MjTBP and other TBPs are compared. The view is in the same orientation as the "top" view of Fig. 1D.

 

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  		Table 1  Data collection and refinement statistics
 

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  		Table 2  RMSD values [Å] derived from the least-squares fittings using the various regions of TBP
 
The major structural difference between MjTBP and eukaryotic/archaeal-I TBP is observed in the helices H2 and H2' on the convex surface (Fig. 2B). Helix H2 is nearly straight in the eukaryotic and archaeal-I TBPs (green (At), magenta (Sc), salmon (Sa), and yellow (Pw) in Fig. 2C). However, helix H2 of MjTBP shows a curved structure (cyan (Mj) in Fig. 2C). This curved helix may be one of the specific features of archaeal-II TBP. Helix H2' of the eukaryotic TBP is kinked at the proline residue, which corresponds to Asp172 in MjTBP. In the archaeal-I and -II TBPs, helix H2' is not kinked. As the helices H2 and H2' of TBP may function as a target surface of regulatory transcription factors in archaea (also described in the section of "Interface with regulatory transcription factors—diversified surfaces —"), these structural differences of helix H2 and H2' may provide structural and functional variations of the convex surface of TBP.

Negatively charged surface of MjTBP

As predicted from the differences in the amino acid compositions of various TBP species, the electrostatic potential of MjTBP (an archaeal-II TBP) is totally different from those of the previously solved structures of eukaryotic and archaeal-I TBPs (Nikolov et al. 1992; Chasman et al. 1993; DeDecker et al. 1996; Koike et al. 2004). The molecular surfaces of the eukaryotic TBP are positively charged except in the second stirrup region, whose surface is negatively charged because of the acidic residues (e.g. E280 and E282 in Homo sapiens (HsTBP)) (arrowheads in the upper panel of Fig. 1D and Supporting Information Fig. S3). The surfaces of archaeal-I TBP are biphasic. Most of the area is positively charged as in eukaryotic TBP, but the first and second stirrup regions are negatively charged because of D43 and D45 in the first stirrup region, and E134 and E136 in the second stirrup region in SaTBP (arrowheads in the lower panel of Fig. 1D and Supporting Information Fig. S3).

However, the surface of archaeal-II TBP is negatively charged (Fig. 3A), because of the large number and wide distribution of the acidic residues (shown by red in Fig. 3B). These increased acidic residues rarely overlapped with the DNA- and TFIIB/TFB-binding residues (the DNA- and TFIIB-binding residues are surrounded by blue and green lines in Fig. 3B, respectively). It is known that most of archaea, including Mj, live under the condition of the high ionic concentrations. This negative charge may serve as an adaptation to the presence of high intracellular ionic concentrations in archaea (Eisenberg 1995). MjTBP also has positively charged and non-charged areas on the concave surface (see the bottom view in Fig. 3A). These two areas of MjTBP, which consist of the conserved residues among the three groups, are likely to interact with the phosphate groups and base pairs of the TATA box, respectively.


Figure 3
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  		Figure 3  Surface properties of TATA box-binding protein (TBP) from Methanococcus jannaschii (Mj) and other species. (A) Electrostatic potential of MjTBP. The orientations of the MjTBP molecule are labeled in each panel. (B) The distribution of the acidic residues in Mj, Sa, and Homo sapiens (HsTBPs). The acidic residues are colored in red. DNA- and TFIIB/TFB-binding residues are enclosed by the blue and green lines, respectively.

 
Evolutionarily conserved and diversified surfaces

Next, we mapped the evolutionarily conserved and diversified amino acid residues of all TBP groups on the structure of MjTBP to compare the functional roles of the different TBP surfaces (Fig. 4). It is known that TBP includes family proteins such as TBP-related factors (TRF) or TBP-like proteins (TLP). However, as the structures of TRF/TLP have not been determined, we focused on TBP in this work. The tertiary structure of TRF/TLP should clear the way for a detailed comparative functional study of TBP and TRF/TLP.


Figure 4
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  		Figure 4  Analysis of the conserved and diversified surfaces of TATA box-binding protein (TBP). (A) Conserved surfaces of TBP. The row labeled "all" shows the conserved residues of TBP in all species (green). The rows labeled eukaryotes, archaea-I, and archaea-II show the conserved residues in eukaryotes (blue), archaea-I (yellow), and archaea-II (red). The upper and lower panels show the "front" and "back" views, respectively. (B) Functional surfaces of TBP. The rows labeled DNA, TFIIB/TFB, TFIIA, and TAF/Ptr2 show the residues important for interacting with DNA (magenta), TFIIB/TFB (orange), and TFIIA (cyan). Predicted TAF-interacting residues (green and yellow) and Ptr2-dependent transcriptional activation residues (yellow) are also shown. The views provided by the different panels are the same as in Fig. 4A. (C) The average values of the sequence identity ratios that are calculated by the pairwise sequence comparisons for each functional surface (see Fig. 4B). The calculation method is the same as that used in Fig. 1A. Bars in green, magenta, orange, cyan, light green and yellow represent the values for all, DNA-binding, TFIIB/TFB-binding, TFIIA-binding, predicted TAF-binding, and Ptr2-dependent transcriptional activation residues, respectively.

 
The residues that were conserved among all three groups (eukaryotic, archaeal-I and archaeal-II TBPs) were distributed mostly on the concave surface and the second stirrup region (green in Fig. 4A). The residues conserved within each TBP group are also distributed on the convex surface in addition to the concave surface and the second stirrup region (blue, yellow and red in Fig. 4A). The conserved area for each group is larger than the conserved area of all TBPs. The residues that are specifically conserved within each group but not conserved in the other groups seem to represent specific characteristics of each TBP group. They are distributed mainly on the convex surface, suggesting that the convex surface plays a role in the group-specific reaction, while the concave surface plays a role in the group-independent reaction. As described in above, we defined the word of "group" to show the three groups of TBPs: eukaryotes, archaea-I, and archaeal-II. One example of group-specific TBP interacting factors is a TBP-associated factor (TAF), which exists only in eukaryotes. Thus, the reaction using the TBP–TAF interaction is a "group-specific reaction." In contrast, the reaction using the TBP–TATA box interaction is a "group-independent reaction," because the TBP–TATA box complex exists in all three groups.

Interface with DNA: Surfaces conserved throughout all species

To discuss the functional roles of the MjTBP surface, we structurally analyzed amino acid substitutions during evolution. The completely evolutionarily conserved residues among all species of TBP are mainly the DNA-binding residues (green and magenta in Fig. 4A,B, respectively). The crystal structures of the TBP-TATA box complex indicate that 31 residues are important for TATA box-binding (Kim et al. 1993a,b). Among them, 18 residues are completely conserved in all species. The pairwise comparison of the 31 residues in the DNA-binding surface indicates that the residues are conserved by nearly 80% in any pair of TBPs (magenta in Fig. 4C). Although the RMSDs of the 31 C{alpha} atoms of the DNA-binding residues are relatively large (RMSD = 0.91–1.96 Å for 31 C{alpha} atoms) (Table 2B-1), structural comparisons of the DNA-binding residues in the first direct repeat, central, and second direct repeat regions show that the local structures of the DNA-binding residues are conserved among species (RMSD = 0.33–1.00, 0.30–0.80, 0.24–0.75 Å for 9, 12, and 10 C{alpha} atoms, respectively) (Table 2B-2, B-3, and B-4, respectively). The large RMSD values, therefore, arise from the relative disposition differences of the three regions. Despite the local structural similarity of the DNA-binding residues, the DNA-binding affinity of TBP is reported to be different among various species (Hahn et al. 1989; O’Brien et al. 1998; Ouhammouch et al. 2003).

The biochemical analyses suggested that the binding to the TATA box of MjTBP is weaker than those of TBPs from other species. The isothermal titration calorimetry (ITC) experiment showed that the MjTBP has a TATA box-binding activity and the observed dissociation constant (Kd) of MjTBP–TATA box complex is approximately 0.94 µM in 1.3 M potassium phosphate (pH7.0) at 25 °C (data not shown). The observed Kd of the PwTBP-TATA box complex was 0.54 µM in 10 mM MOPS, 1.3 M potassium phosphate (pH 7.0) at 25 °C (O’Brien et al. 1998), and that of the ScTBP–TATA box complex was 2.4 nM in 4 mM Tris (pH 8), 60 mM KCl, 5 mM MgCl2 at room temperature (Hahn et al. 1989). Although the conditions for binding assays are different, these results suggest that the DNA-binding activity of MjTBP is weaker than that of eukaryotic/archaeal-I TBP. This fact may arise from the difference of the relative position of the three regions of the DNA-binding site (Table 2B-1) and/or the difference of the total negative charge of TBP (Fig. 3A), which might affect the electrostatic interaction of TBP with the TATA box.

Interface with general transcription factors: Surfaces conserved dependent on factors

Next, the interaction surface of TBP for TFIIB/TFB was examined on the basis of the crystal structure of the MjTBP and TBP-TFIIB-DNA complex (Nikolov et al. 1995). In archaea, TBP and TFIIB/TFB function as transcription initiation factors, as observed in eukaryotes. The sequence comparison of TBP showed that the TFIIB/TFB-binding residues are well-conserved in TBP (green and orange in Fig. 4A and 4B, respectively). The pairwise comparison of the 11 residues in the TFIIB-binding site revealed that the residues in the TFIIB/TFB-binding surface are highly conserved in each group (approximately 80%), but the conservation ratios in the intergroup comparison were approximately 50% (orange in Fig. 4C). This fact suggests that the interaction between TBP and TFIIB/TFB is group-specific. The structure comparisons of the TFIIB-binding site of TBP also seem to support this group-specific characteristic. The RMSDs within each group (0.45–0.61 Å for 11 C{alpha} atoms) were smaller than those from the intergroup structural comparisons (1.05–1.35 Å for 11 C{alpha} atoms), except for the comparison among archaeal-I TBP and MjTBP (0.43–0.51 Å for 11 C{alpha} atoms) (Table 2C). This result suggests that the structural features of the functional interaction surface of TBP for TFIIB/TFB is conserved in each group throughout evolution. As the residues in this region are involved in the dimerization of TBP, this interaction may also contribute to the structural conservation of the residues.

The structural characteristics of the TFIIA-binding site are different from those of the TFIIB/TFB-binding site. The 15 residues in the TFIIA-binding site are conserved in eukaryotes but not conserved well in archaea (cyan in Fig. 4C). In addition, the RMSD values derived from least-squares fitting of the 15 C{alpha} atoms in the TFIIA-binding site are larger than those of the TFIIB/TFB-binding sites; the former are in the range of 0.85–2.78 Å (Table 2D). These findings are in good agreement with the fact that the TATA box and TFIIB/TFB are present in archaea, but TFIIA is not.

The TBP surface for binding to TAFs was also examined. The intensive pairwise sequence comparison of the 23 predicted TAF-interacting residues (green and yellow in Fig. 4B) showed that only eukaryotes have a highly conserved ratio in this surface (approximately 70%). Archaea-I and archaea-II TBPs show conserved ratios of < 30% in this region (light green in Fig. 4C). An intergroup comparison also showed low conservation ratios, suggesting that there is no evolutionary constraint in this surface except in the case of eukaryotes. A structural comparison also showed that the RMSDs of predicted TAF-binding residues were relatively large (1.03–2.54 Å for 23 C{alpha} atoms) (Table 2E). Eukaryotic TFIID has 14 TAFs, some of which are specific interaction partners for the convex surface of TBP (Leurent et al. 2004). However, archaea do not have TAFs. The structural differences among the convex surfaces of TBP, particularly the above-described difference in the conformation of helix H2 and H2' (Fig. 2C), may affect the binding between TBP and the interacting factors such as TAFs.

Interface with regulatory transcription factors: Diversified surfaces

We next examined the TBP surface involved in the regulatory transcription factor binding. In archaea, Ptr2 is the only regulatory transcription factor whose transcriptional activation activity through TBP has been investigated (Ouhammouch et al. 2003). In the analyses of the transcriptional activation mechanism by Ptr2 with TBP using closely related species of M. jannaschii (Methanothermococcus thermolithotrophicus (Mt) and Methanococcus. maripaludis (Mm)), Ouhammouch and Geiduschek revealed that the surfaces for transcriptional activation are located within the effector domain of Ptr2 by comparing the sequence and trans-activation activity of Mj, Mt and MmPtr2 based on the tertiary structure of the Ptr2 homolog (Ouhammouch & Geiduschek 2005). In this study, we interpreted the differences in the trans-activation activity among Mj, Mt and MmTBP based on the tertiary structure of MjTBP.

When Mj, Mt or MmTBP is used for MjPtr2-dependent activation, MjTBP and MtTBP exhibit the highest and lowest transcriptional activation activity through MjPtr2, respectively (Ouhammouch & Geiduschek 2005). This suggests that MtTBP-specific residues of the three TBPs are involved. The residues indicated by open circles in Supporting Information Fig. S1 seem to be involved in the lowest activity in MtPtr2-dependent transcriptional activation. These residues, namely Ser159, Glu160 and Asp172 in MjTBP, are on the helix H2' (yellow in Fig. 4B). The pairwise sequence comparison analysis showed that the Ptr2-dependent transcriptional activation residues and their surrounding residues (nine residues) are less conserved in each archaeal group as well as between archaea-I and archaea-II TBPs (Fig. 4C), although the structural comparison showed that the RMSD values of these residues are relatively small (0.44–1.35 Å for 9 C{alpha} atoms) (Table 2F). The small RMSDs can be explained by the fact that seven among nine residues of the Ptr2-dependent transcriptional activation surface are located on the helix H2'. This result suggests that this regulatory transcription factor has species-specific characteristics.

Eukaryotic regulatory transcription factors also target the convex surface of TBP. The helix H2 in the convex surface of eukaryotic TBP has been implicated in binding to the activation domains of eukaryotic transcription factors such as p53 (Liu et al. 1993). The amino acid sequence of the convex surface of the eukaryotic and archaeal TBPs is highly diversified, suggesting that the structural characteristics of TBP-interacting regulatory transcription factors differ between eukaryotes and archaea. Indeed, p53 and Ptr2 adopt completely different folds; p53 in eukaryotes is an immunoglobulin-type regulatory transcription factor, and Ptr2 in archaea is a bacterial HTH-type regulatory transcription factor.


   Discussion
Top
 Abstract
 Introduction
 Results
 Discussion
Experimental procedures
 References
 
In the present study, we solved the crystal structure of MjTBP, which belongs to archaeal-II TBP. The crystal structure revealed that MjTBP adopts a similar structure to those of eukaryotic and archaeal-I TBPs (Fig. 2B). However, the molecular surface of MjTBP, which is negatively charged, is different from those of eukaryotic and archaeal-I TBPs, which are charged biphasically and positively, respectively (Fig. 1D and Supporting Information Fig. S3). The ITC experiment by our group and the previous experiment by other groups showed that the TATA box-binding activity of MjTBP is weaker than those of TBPs from other species. The negative charge of the MjTBP would be one of the main reasons for the weak interaction between MjTBP and the TATA box.

The present analyses of the crystal structure of MjTBP and the evolutionary relationships of various TBPs also revealed that the TBP surface can be classified into three distinct regions: a surface highly conserved among all TBPs, a group-specific conserved surface, and a highly diversified surface. The highly conserved surface is the DNA-binding surface. The highly conserved nature of this surface seems to reflect the fact that the tertiary structure and the nucleotide sequence of the TATA box are essentially the same from archaea to eukaryotes. The group-specific conserved surface consists of the TFIIB/TFB surface. The group-specific characteristics of this surface suggest that the interaction nature and interacting factors should have a group-specific characteristics and TFIIB/TFB may have evolved in a coupled manner with TBP.

"Coupled evolution" of TBP and its auxiliary factors, TFIIB/TFB and Rpb11

To confirm the evolutionary relationship between TBP and its auxiliary factors, the phylogenetic trees of them were compared. To compare the molecular phylogeny of TBP and the various factors, the phylogenetic trees generated from the sequences of the whole molecules are analyzed. In the phylogenetic trees prepared by the neighbor-joining method, a single node connects closely related species. The phylogenetic tree of TBP showed that TBP in archaea-I and archaea-II evolved from different nodes, indicating that the archaea-I and archaea-II TBPs have evolved as distinct groups (Adachi et al. 2004) (Fig. 5A). The phylogenetic tree of TFIIB/TFB shares this characteristic, although there are slight topological differences between the trees (Fig. 5A). Archaeal TFIIB/TFB can also, therefore, be classified into two groups: archaea-I and archaea-II. The observed evolutionary relationship between TBP and TFIIB/TFB is probably an example of "coupled evolution," which is also observed in the relationship between growth factors and their cognate receptors (Murphy 1993; Mitsui & Senda 1997). Indeed, TBP and TFIIB/TFB have a tight functional relationship. For example, the physical interaction between TBP and TFIIB/TFB is required to define the productive orientation of assembly of the transcription apparatus on a promoter in archaea-I (Li et al. 1994; Littlefield et al. 1999). The functional role of this interaction also seems to be conserved in other groups because of the conservation of the structure of the functional complex of TBP-DNA-TFIIB/TFB from Hs and Pw (Nikolov et al. 1995; Kosa et al. 1997; Littlefield et al. 1999).


Figure 5
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  		Figure 5  Evolutionary relationship among TATA box-binding protein (TBP), TFIIB/TFB, and Rpb11/RpoL. (A) Phylogenetic trees of TBP, TFIIB/TFB, and Rpb11/RpoL are shown. Red branches are closely related species in archaea-II groups. Branches for archaea-I are black. The human TBP sequence was included as a marker. These three phylogenetic trees show that the archaea-I and archaea-II are clearly divided into the TBP, TFIIB/TFB and Rpb11/RpoL. It is of note that the trees of other subunits of RNA polymerase do not show a clear separation between archaea-I and archaea-II as observed in the TBP, TFIIB/TFB, and Rpb11/RpoL (Supporting Information Fig. S4). (B) The putative location of the TBP (cyan) and TFIIBc (C-terminal domain of TFIIB; green) on RNA polymerase II. The Rpb11 subunit of RNA polymerase II and the N-terminal domain of TFIIB are shown in red and blue, respectively.

 
As the RNA polymerase in eukaryotes interacts with TBP, the phylogenetic trees of RNA polymerase's subunits were also compared with those of TBPs. This comparison showed that only Rpb2N/RpoB’, Rpb2C/RpoB’, and Rpb11/RpoL had phylogenetic trees topologically similar to those of TBPs. They can also be classified into the archaea-I and archaea-II groups (Fig. 5A and Supporting Information Fig. S4), suggesting a functional relationship among TBP, TFIIB/TFB, Rpb2/RpoB, and Rpb11/RpoL. And in fact, these factors have been shown to be necessary for transcription initiation (Roeder 1996; Thomm 1996; Ouhammouch et al. 2003). In addition, the proposed locations of TBP, TFIIB/TFB, and Rpb11/RpoL on RNA polymerase (Bushnell et al. 2004) are close to one another, suggesting intimate relationships in their function (Fig. 5B). Evolutionary coupling of TBP and Rpb2/RpoB suggests the functional relationship between TBP and Rpb2/RpoB, although the functional implication of their possible interaction(s) remains elusive.

"Coupled evolution" of TBP and other factors remains elusive

The diversified surface includes the TAF-binding site and Ptr2-binding site (or regulatory transcription factor-binding site). Although Ptr2 is an auxiliary factor of TBP, the phylogenetic tree of Ptr2 does not correlate with that of TBP (Supporting Information Fig. S4), probably because the functional overlap of TBP and Ptr2 is looser than those among TBP, TFIIB/TFB, and Rpb11/RpoL. For instance, TBP, TFIIB/TFB, and Rpb11/RpoL function around the TATA box nearly simultaneously to initiate the transcription, but Ptr2 functions not only around the TATA box but also on the sequence upstream of the TATA box, suggesting that Ptr2 is involved in the interaction with factors other than TBP, TFIIB, and Rpb11/RpoL. This possible interaction of Ptr2 would not be a general process in transcription, but rather a species-specific reaction. The relationship between Ptr2 and TBP might be elucidated when phylogenetic trees are prepared using only interaction domains/sequences between TBP and Ptr2. To elucidate the domains/sequences important for the interactions between these factors, and to understand the evolutionary relationship and gain molecular insights into the interactions among these factors, tertiary structure analyses of both the TBP-RNA polymerase complex and the TBP-Ptr2 complex are required.

The present structural and evolutionary analyses of MjTBP in comparison with other known TBPs showed that TBP surfaces can be classified into three categories depending on the functional interactions between TBP and its interacting factors. TBP seems to be evolved through changes between the interacting factors and the interacting surfaces. The coupled evolution found among transcription initiation factors and a subunit of RNA polymerase may suggest their essential roles and tight functional relationships in the transcription initiation reaction. The complex structures of RNA polymerase and transcription initiation factors will provide information on the residues involved in the interaction between them, and lead to further analyses of the coupled evolution of transcription apparatus.


   Experimental procedures
Top
 Abstract
 Introduction
 Results
 Discussion
 Experimental procedures
References
 
Protein expression, purification and crystallization

Methanococcus jannaschii TBP was expressed in Escherichia coli, purified, and crystallized as described earlier (Adachi et al. 2004).

Structure determination

Diffraction data were collected on beamline BL-5A at the Photon Factory, Tsukuba, Japan (Adachi et al. 2004). The diffraction data were processed and scaled with MOSFLM and SCALA (CCP4 package) (CCP4 1994), respectively (Table 1). The crystal structure was determined by molecular replacement with MOLREP (Vagin & Teplyakov 2000) using the Sulfolobus acidocaldarius TBP structure (PDB code 1MP9) (Koike et al. 2004) as the search model. The model building of M. jannaschii TBP was performed with Xtalview software (McRee 1993) and refined with CNS (Brünger et al. 1998) and REFMAC (Murshudov et al. 1997) software. Refinement statistics are given in Table 1.

The complete amino acid chain is well defined in the electron-density map, except for a region between Tyr34 and Pro40 for molecule A in the asymmetric unit. The current model comprises amino acid residues 3-177. The final model has 8.2% residues in allowed regions of the Ramachandran plot and 91.8% in the most favored regions according to the program PROCHECK (Laskowski et al. 1993). All molecular graphics in the manuscript were prepared with PyMOL (DeLano 2002). Electrostatic potential surfaces were calculated and visualized with PyMOL using the absolute electrostatic potential in a vacuum. The darkest blue denotes a potential of 100 kT/e, and the darkest red denotes a potential of –100 kT/e.

Isothermal titration calorimetry (ITC)

The His-tagged MjTBP protein was dialyzed against two changes of 1.3 M potassium phosphate buffer (pH 7.0) at 25 °C using dialysis cassette with the molecular weight cut-off at 3500 (Thermo Scientific Inc.). The DNA (sequence with binding site underlined; AAGCTATTAATAGTAA-CCTCC-TTACTATTAATAGCTT) was designed to form a hairpin loop. The oligonucleotide was prepared by dissolving in 1.3 M potassium phosphate buffer (pH 7.0) at 25 °C. Before use, the oligonucleotide was heated to approximately 90 °C and rapidly cooled in ice to ensure hairpin formation.

The ITC experiments were conducted using a VP-ITC (MicroCal Inc.). In the experiments, the injections of DNA (100 µM) were made into His-tagged MjTBP (10 µM) in the ITC cell at 25 °C, and the following instrument settings were used: 8 µL per injection (5 µL for first injection only); 210 s per injection; 30 injections; 2 s filter; 16 s injection duration; 300 r.p.m. stirring speed. The heats of dilution of DNA into buffer (1.3 M potassium phosphate buffer (pH 7.0) at 25 °C) were determined in separate experiments and subtracted from the titration prior to data analysis. The data were analyzed using the ORIGIN software (MicroCal Inc.) supplied with the calorimeter. In this experiment, the experimental data were analyzed using "One Sites" model, resulting in the stoichiometry (N) = 0.671 ± 0.022, the association constant (Ka) = 1.06 x 106 ± 0.18 x 106/M, enthalpy ({Delta}H) = 1.64 x 104 ± 0.08 x 104 cal/mol, and entropy ({Delta}S) = 82.4 cal/mol/K.

Sequence comparison

The pairwise sequence comparisons were performed using a self-made program written in Perl. All sequence information was derived from the NCBI database <http://www.ncbi.nlm.nih.gov/>. The program compares every pair of sequences in the aligned sequence data, calculates the ratio of the sequence identity (identity ratio) and calculates the average and standard deviation of the identity ratios of each category. The results of the sequence comparisons were classified into six categories: the comparisons within each group, namely eukaryotes, archaea-I, and archaea-II, and the inter-group comparisons, namely eukaryotes vs. archaea-I, eukaryotes vs. archaea-II, and archaea-I vs. archaea-II. The gene IDs of sequence used in these calculations are shown in Supporting Information Table S2.

Structural comparison

RMSDs were obtained from the least-squares fittings calculated by the program lsqkab in the CCP4 program suit (CCP4 1994). The PDB codes used in the structural comparison are chain A of 1VOK (At), 1TBP (Sc), 1MP9 (Sa), and 1PCZ (Pw), and chain P of 2Z8U (Mj). The RMSD values comparing chain P and chains Q, A, and B in the asymmetric unit of MjTBP are significantly smaller than those comparing MjTBP and other species of TBP.

Phylogenetic tree

Multiple alignments and Guide trees were prepared using the NJ method with the program ClustalW <http://www.ebi.ac.uk/Tools/clustalw/index.html>. Phylogenetic trees were drawn by the program Unrooted <http://pbil.univ-lyon1.fr/software/unrooted.html>.


   Acknowledgements
 
Authors thank Drs K. Hasegawa, Y. Tachibana, R. Weisburd, N. Whitby and P. Hughes for their critical comments on the manuscript. Authors also thank Drs S. Kidokoro and K. Ono for supporting the ITC experiment and data analysis. This work was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan, the New Energy and Industrial Technology Development Organization (NEDO), the Mitsubishi Foundation, and the Uehara Memorial Foundation, and by a grant for Exploratory Research for Advanced Technology (ERATO) of the Japan Science and Technology Corporation (JST). The coordinates and structure factors have been deposited in the Protein Data Bank under ID code 2Z8U.


   Footnotes
 
Communicated by: Hiroshi Handa

* Correspondence: toshiya-senda{at}aist.go.jp and horikosh{at}iam.u-tokyo.ac.jp


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Accepted: 7 August 2008





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