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Protein Science (2002), 11:1978-1983.
Copyright © 2002 The Protein Society

Protein stability indicates divergent evolution of PD-(D/E)XK type II restriction endonucleases

Monika Fuxreiter and István Simon

Institute of Enzymology, Hungarian Academy of Sciences, H-1518 Budapest, Pf. 7., Hungary

Reprint requests to: Monika Fuxreiter, Institute of Enzymology, Hungarian Academy of Sciences, H-1518 Budapest, Pf. 7., Hungary; e-mail: monika{at}enzim.hu; fax: (36-1)-466-5465.

(RECEIVED December 19, 2001; FINAL REVISION May 8, 2002; ACCEPTED May 18, 2002)

Article and publication are at http://www.proteinscience.org/cgi/doi/10.1110/ps.4980102.


   Abstract
TOP
 Abstract
Introduction
 Results
 Discussion
 Materials and methods
 References
 
Type II restriction endonucleases recognize 4–8 base-pair-long DNA sequences and catalyze their cleavage with remarkable specificity. Crystal structures of the PD-(DE)XK superfamily revealed a common {alpha}/ß core motif and similar active site. In contrast, these enzymes show little sequence similarity and use different strategies to interact with their substrate DNA. The intriguing question is whether this enzyme family could have evolved from a common origin. In our present work, protein structure stability elements were analyzed and compared in three parts of PD-(DE)XK type II restriction endonucleases: (1) core motif, (2) active-site residues, and (3) residues playing role in DNA recognition. High correlation was found between the active-site residues and those stabilization factors that contribute to preventing structural decay. DNA recognition sites were also observed to participate in stabilization centers. It indicates that recognition motifs and active sites in PD-(DE)XK type II restriction endonucleases should have been evolutionary more conserved than other parts of the structure. Based on this observation it is proposed that PD-(DE)XK type II restriction endonucleases have developed from a common ancestor with divergent evolution.

Keywords: Stabilization centers; DNA recognition; phosphodiester hydrolysis; structural similarity; divergent evolution

Abbreviations: SC, stabilization center • PDB, Protein Data Bank


   Introduction
TOP
 Abstract
 Introduction
Results
 Discussion
 Materials and methods
 References
 
Type II restriction endonucleases catalyze phosphodiester bond hydrolysis in 4–8 base-pair-long DNA sequences (Roberts and Halford 1993). These enzymes serve as excellent model systems to study DNA recognition due to their remarkable selectivity. Type II restriction endonucleases consist of four superfamilies with distinct folds: PD-(D/E)XK, Nuc, GIY-YIG, and HNH nucleases (Aravind et al. 2000; Sapranauskas et al. 2000; Bujnicki et al. 2001). The presently solved crystal structures correspond to only one, the PD-(D/E)XK superfamily. These structures show high analogy among their active sites, which include two acidic residues and usually a Lys. In BamHI and BglII, however, Lys is replaced by Glu. Also each structure contains a similar {alpha}/ß core motif, which is built up by 5–6 ß strands surrounded by several flanking {alpha} helices. Despite these similarities, PD-(D/E)XK endonucleases lack substantial sequence similarity. No uniform catalytic mechanism could have been established yet for type II restriction endonucleases, mostly due to the ambiguity of the metal ions involved in catalysis (Pingoud and Jeltsch 1997; Pingoud and Jeltsch 2001; Horton et al. 1998b; Viadiu and Aggarwal 1998; Horton and Cheng 2000; Fuxreiter and Osman 2001). There are several strategies described for DNA recognition by these enzymes (McClarin et al. 1986; Winkler et al. 1993; Newman et al. 1995, HREF="#NEWMAN-ETAL-1998">1998; Horton and Cheng 2000; Lukacs et al. 2000). For example BamHI and EcoRI, approach the DNA from the major groove, whereas EcoRV and PvuII access DNA from the minor groove. The intriguing question is how these enzymes have evolved, whether they have a common ancestor from which they have developed. Exploring the evolutionary relationship between type II restriction endonucleases can also reveal basic principles of DNA recognition.

In this work we analyzed those factors that contribute to the structural stability of the PD-(D/E)XK superfamily of type II restriction endonucleases. These residues form cooperative sets of long-range interactions, which prevent unfolding of the structure. They are identified as stabilization centers (SCs), which have been defined and described previously (Dosztanyi et al. 1997; see also Materials and Methods).

Because mutation of SC-forming residues affects stability of the intact structure, these residues have been observed to be evolutionarily more conserved than average residues. Therefore, analyzing SCs in restriction endonucleases can identify those parts of the structure that are evolutionarily most conserved. In this study we focused on three structural–functional parts of PD-(D/E)XK endonucleases: (1) core motif, (2) active-site residues, and (3) residues playing a role in DNA recognition. Exploring common stability motifs can help to understand the evolutionary relationship between PD-(D/E)XK type II restriction endonucleases.


   Results
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 Abstract
 Introduction
 Results
Discussion
 Materials and methods
 References
 
The distribution of stabilization centers in the {alpha}/ß core of BamHI, EcoRI, FokI, BglII, EcoRV, PvuII, Cfr01, and BglI compared to the whole enzyme is displayed in Table 1Go. The core is structurally most conserved, and hence it is expected to be most stable in PD-(D/E)XK endonucleases. This motif, however, does not contain the majority of stabilization centers in each enzyme. Ratio of SCs belonging to the core covers a wide range: SCs are dominant in the core of EcoRV (~60%); this ratio varies between 30% and 40% in BglI and EcoRI, whereas in other enzymes it decreases to 10%–30%. Interestingly, PvuII, which is believed to be most closely related to EcoRV has the lowest ratio of core SCs. In most cases the ratio of SCs in the core motif is comparable with the relative size of the core. This observation indicates that contribution of the core to structural stability of the whole enzyme is approximately proportional to the size of the core. EcoRV and PvuII are exceptions in which the ratio of core SCs is significantly higher or lower than the ratio of the core, respectively. In PvuII only 5 SCs are sufficient to keep the core intact.


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  		Table 1. Stabilization centers, in the core motif of type II restriction endonucleases
 
The core motifs also form only a few SCs with the rest of the structure. Other structural parts are involved in more SCs, thus providing a greater contribution to preventing proteins from degradation. These results suggest that the core is important but not dominant for the structural stability of PD-(D/E)XK type II restriction endonucleases. Consequently, despite the structural similarity of the core motifs, it is unlikely that the core represents the evolutionary relationship between these enzymes.

Because the binding of DNA affects protein conformation in many enzymes, SCs in the free enzymes have been compared to complex structures. Protein–DNA complexes in general are more compact than free enzyme structures, which can increase the number of SCs. Interestingly, in EcoRV, EcoRI, and BglII, in which DNA undergoes major distortion upon interacting with the protein, the number of SCs increases in the catalytically competent complexes compared to the free enzymes. In BamHI and PvuII, in which DNA retains B-DNA conformation, the number of SCs in the protein remains fairly stable.

The catalytic machinery of restriction endonucleases requires the presence of several negatively charged side chains in the active site. The primary role of these residues is to ligate the catalytically essential metal ion cofactor. Correlation between SCs and active-site residues are displayed in Table 2Go. In all studied enzymes, at least one active-site residue is involved in an SC. The only exception is the complex of EcoRI with DNA, in which no active-site residue forms SC. In the free enzyme and in a catalytically active complex with a metal ion, however, two active-site residues contribute to stabilization of the structure. Involvement of two or more active-site residues in SC elements is quite frequent. Interestingly, in several cases, like EcoRI, EcoRV, Cfr10I, BglII, MunI, and BsoBI two active-site residues form an SC with each other. In BamHI complexes and in FokI a residue next to an active-site residue makes SC link with another active-site residue. It suggests that the active-site residues provide an important contribution to the stabilization of the whole enzyme structure. In other words, although the active-site residues belong to different secondary structure elements, they form a structurally stable unit, which should have been conserved during evolution. The fact that not all active-site residues are involved in SC formation can explain the small variability of the active sites in PD-(D/E)XK type II restriction endonucleases.


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  		Table 2. Active site residues participating in stabilization centers of type II restriction endonucleases
 
Type II restriction endonucleases use diverse strategies to interact with their substrate DNA (Aggarwal 1995). Several attempts have been made to establish a correlation between the specific base-pair sequences and the recognition motifs. Besides understanding this fascinating phenomena, there is a practical goal behind these works, namely to alter the specificity of restriction endonucleases. During the SC analysis of restriction endonucleases, a correlation has been found between some of the recognition residues and the stabilization elements. Those residues, which play a role in DNA recognition and are also involved in SCs, are shown in Table 3Go. For all studied type II endonucleases, with the exception of NgoMIV, at least one residue binding to the cognate DNA sequence also plays a role in SC formation. In the case of NgoMIV Ser 40, which orients a recognition residue, Arg 227, participates in SC formation. The presence of SCs indicates an extensive set of interactions between two parts of the structure, which are responsible for making specific contacts with DNA. It is also reflected by the fact that in several cases the neighboring side chains of a recognition residue are involved in SC formation. At first, the contribution of recognition residues to protein stability is surprising. Because restriction endonucleases work on more than 200 sequences (Roberts and Macelis 2001), the recognition motifs are expected to be highly variable during evolution. On the other hand, our observation means that bringing together those residues, which are responsible for specific DNA binding, also contributes to stabilization of the structure. Thus, it makes the recognition motif evolutionarily more conserved. It means, that PD-(D/E)XK endonucleases contain a stable motif with appropriate geometry to contact with either or both DNA grooves. This structural element is held together with an extensive set of long-range interactions around the central residue, which is important for the stability of the protein structure. The structural stability has been proposed to contribute to preserving this motif and hence its DNA recognition function during evolution. As there is only one conserved pair in the interaction of the recognition residues, the rest is highly variable, providing diversity in the cognate sequences.


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  		Table 3. Recognition sites participating in stabilization centers of type II restriction endonucleases
 
Type II restriction endonucleases can be divided into {alpha} and ß subfamilies (Huai et al. 2000; Bujnicki 2001), which have different dimerization schemes and DNA recognition patterns. Enzymes belonging to the {alpha} family (e.g., EcoRI, BamHI, MunI, FokI, and Cfr10I) use an {alpha} helix and a loop for DNA recognition and usually produce 5` overhanging ends, whereas members of the ß family (e.g., EcoRV, PvuII, BglI, and NaeI) use a ß strand to interact with the cognate DNA sequence and give blunt-ended products. It is interesting to analyze whether SCs indicate any difference between these two endonuclease subfamilies. Residues involved in dimerization were observed to form very few SC links; hence they cannot be used as a distinction criteria. Those SC-forming residues that participate in DNA recognition, however, interact with different base pairs in the two subfamilies. In enzymes of the {alpha} family almost all SC-forming recognition residues make contact with either or both of the outer two guanines, whereas in the ß family, they interact with the second thymine. The present definition of SCs, however, is not suitable for quantitative characterization of evolutionary distances of enzymes. Hence, based on SC similarities, we cannot derive a structure-based phylogenetic tree of restriction endonucleases (Bujnicki 2000).

The SC analysis was also extended to two related DNA repair nucleases: the mismatch repair MutH (Ban and Yang 1998) and the very short patch repair Vsr endonuclease (Tsutakawa et al. 1999), which exhibit the same fold as PD-(D/E)XK endonucleases. In MutH two active-site residues (Glu 77 and Lys 79) and one recognition residue (Phe 94) participate in SC formation. In Vsr Asp 51 of the active site and Gly 65, as well as Glu 116 of the recognition motif, are involved in SCs. These results indicate that some of the active-site and recognition residues contribute to overall structural stability in all nucleases with PD-(D/E)XK fold.


   Discussion
TOP
 Abstract
 Introduction
 Results
 Discussion
Materials and methods
 References
 
Stabilization centers have been analyzed to test the possible evolutionary relationships between structures of PD-(D/E)XK type II endonucleases. In general, the common {alpha}/ß core motif was not found to provide a major contribution to structure stabilization in these enzymes. The active-site residues, as well as some residues in the recognition sites, are, however, persistently involved in SC formation. Hence, these parts of the enzyme—the active site and the recognition site–can be concluded to be evolutionarily most conserved in PD-(D/E)XK endonucleases. Conserving a stabilization center in these sites, however, does not prohibit the variability of these sites. In most cases two residues of the active site or recognition site are involved in SC formation. The conservation of other residues is not required to provide sufficient stability for these structural motifs via an extensive set of long range interactions. It can explain the diversity of the DNA sequences, which can be recognized by these enzymes. Our results support the hypothesis that PD-(D/E)XK type II restriction endonucleases have been developed from a common ancestor with divergent evolution.


   Materials and methods
TOP
 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
References
 
Crystal structures of 14 enzymes: BamHI, EcoRI, EcoRV, PvuII, BglI, BglII, FokI, Cfr10I, MunI, NaeI, NgoMIV, BsoBI, Bse634I, and HincII were analyzed in free forms, in complexes with substrate DNA, and in catalytically active form with DNA and metal ions. The Protein Data Bank (PDB) codes are displayed in Tables 1–3GoGoGo; the references are given in Table 2Go. BamHI and EcoRV complexes with nonspecific DNA were also included. The crystal structures were not optimized. The core motifs in Table 1Go were defined to include five ß strands and two {alpha} helices involved in dimerization, which are as follows: BamHI (ß3, ß4, ß5, ß6, ß7, {alpha}4, and {alpha}6); EcoRI (ß1, ß2, ß3, ß4, ß5, {alpha}4, and {alpha}5); EcoRV (ßc, ßd, ße, ßg, ßh, {alpha}A, and {alpha}B); PvuII (ßa, ßb, ßc, ße, ßf, {alpha}A, and {alpha}B); BglI (ß1, ß2, ß3, ß8, ß9, {alpha}2, and {alpha}4); BglII (ß3, ß4, ß5, ß6, ß7, {alpha}4, and {alpha}5); FokI (ß1, ß2, ß3, ß4, ß5, {alpha}4, and {alpha}5); and Cfr10I (ß3, ß4, ß5, ß6, ß7, {alpha}7, and {alpha}8).

The stabilization centers were calculated using the original definition (Dosztanyi et al. 1997). Two residues form an SC element if (1) they are involved in long-range interaction, that is, they are separated by at least 10 residues in sequence and the contact distance of their two closest atoms is less than the sum of their van der Waals radii plus 1 Å, and (2) two supporting residues can be selected from both of their flanking tetrapeptides, which together with the central residues form at least seven out of the possible nine contacts.


   Acknowledgments
 
We thank Prof. Roman Osman for stimulating discussions. The research has been sponsored by OTKA grants T30566, T34131, U.S.-Hungarian Mobility grant 99/MO/01, as well as Bolyai and OTKA D34572 fellowships.

The publication costs of this article were defrayed in part by payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 USC section 1734 solely to indicate this fact.


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