Investigation and improvement of DNA cleavage models of polyamide + Cu(II) nuclease + OOH- ligands bound to DNA
© Yue et al; licensee BioMed Central Ltd. 2010
Received: 21 June 2010
Accepted: 17 October 2010
Published: 17 October 2010
Copper nucleases as a famous class of artificial metallonucleases have attracted considerable interest in relation to their diverse potentials not only as therapeutic agents but also in genomic researches. Copper nucleases present high efficient oxidative cleavage of DNA, in which DNA strand scission occurs generally after hydrogen atom abstracted from a sugar moiety. In order to achieve the selective cleavage of DNA sequences by copper nucleases, the DNA specific recognition agents of the Dervan-type hairpin and cyclic polyamides can be considered as proper carriers of copper nucleases. Investigation of the DNA cleavage selectivity of copper nucleases assisted by the hairpin and cyclic polyamides at the molecular level has not yet been elucidated.
We carried out a series of molecular dynamics simulations for the nuclease [Cu(BPA)]2+ or [Cu(IDB)]2+ bound to the hairpin/cyclic polyamide and associated with DNA to investigate the selective DNA cleavage properties of Cu(II)-based artificial nucleases. The simulated results demonstrate that the DNA cleavage selectivity of the two nucleases assisted by the hairpin polyamide is improved efficiently. The [Cu(BPA)]2+ or [Cu(IDB)]2+ nuclease with a substrate OOH- bound to the hairpin polyamide can be stably located at the minor groove of DNA, and possibly abstracts H atom from the sugar of DNA. However, the DNA cleavage properties of the two nucleases assisted by the cyclic polyamide are significantly poor due to the rigidity of linking region between the cyclic polyamide and nuclease. With introduction of the flexible linker -CH2CH2CH2NH2, the modified cyclic polyamide can assist the two copper nucleases to improve the selective DNA cleavage properties efficiently.
A flexible linker and a proper binding site of the polyamide-type recognition agents play an important role in improving the DNA cleavage selectivity of copper nucleases. Current investigations provide an insight into the DNA cleavage specificities of chemical nucleases assisted by an appropriate nucleic acid recognition agent.
Artificial nucleases have attracted considerable attention for their diverse applications not only as therapeutic agents but also in biochemical research [1–4]. Among them, transition metal complexes have been studied extensively due to their diversity in structure and reactivity [5–8]. Copper complexes with the biological and accessible oxidative/reductive potentials have become a class of the most frequently studied artificial metallonucleases [9–16]. The first copper nuclease, [Cu(OP)2]2+ (OP = 1,10-phenanthroline) [17, 18], with high efficiency DNA cleavage property, motivated decade-long studies on mononuclear copper nucleases [3, 5, 19–22]. Especially, a great number of mononuclear copper nucleases[23–26] with BPA (BPA = bis(2-pyridylmethyl) amine) and IDB (IDB = N,N-bis(2-benzimidazolylmethyl) amine) ligands have attracted much attention due to their synthetic accessibility, low molecular weight and efficient DNA cleavage ability. Moreover, some experiments and theoretical calculations have predicted that the mononuclear copper nucleases present high efficient oxidative cleavage of DNA [7, 23, 29–33], in which DNA strand scission occurs generally after hydrogen atom abstractions of deoxyribose sugar moiety [2, 27, 34]. However, the oxidative DNA cleavage process only involves the hydrogen atom abstraction from any sugar in DNA, which makes most copper nucleases do not selectively recognize and cleave DNA sequences [35–37].
In order to improve the selective cleavage of copper nucleases to DNA molecules, specific DNA sequence recognition agents were introduced as carriers of copper nucleases [23, 38]. In the case of DNA recognition agents, polyamides have presented promising characteristics due to its simple structure, synthetic accessibility and sequence specific affinity to base pairs in the DNA minor groove [39–42]. Recently, the experimental observations reported by Aldrich-Wright and co-workers demonstrated that the complexes of the Dervan-type polyamides combined with platinum compounds can successfully recognize the relevant sequences of DNA [43, 44]. Moreover, among the Dervan-type polyamides, the hairpin and cyclic polyamides have presented higher affinities and specificities to DNA sequences than those of single-chain and antiparallel-double polyamides [1, 40, 45, 46]. Specifically, eight-ring hairpin polyamide with the flexible β-alanine (β) residue that binds to DNA as a "turn-to-tail" model possesses excellent affinity and sequence specificity of DNA molecule [6, 47]. The cyclic polyamides with γ-butyric acid (γ) can also efficiently recognize DNA sequences by a "turn-to-turn" model [48–50]. In the present work, we have performed a molecular dynamics (MD) study on the interactions of DNA with the ligands formed by each of the high efficient DNA-cleavage[22, 51] copper nucleases, [Cu(BPA)]2+ and [Cu(IDB)]2+, and by either the hairpin Dervan-type polyamide, ImImPyPy-γ-PyPyPyPy-β-Dp, or the cyclic Dervan-type polyamide, . Namely, six independent simulations were carried out, of which first four simulations were performed on hairpin-polyamide + [Cu(BPA)]2+- DNA, cyclic-polyamide + [Cu(BPA)]2+- DNA, hairpin-polyamide + [Cu(IDB)]2+- DNA and cyclic-polyamide + [Cu(IDB)]2+- DNA, to study the influences of different recognition agents and nuclease cleavage agents on the hydrogen abstractions from the sugar moiety of DNA; and the last two MD simulations were performed on modified-cyclic-polyamide and modified-cyclic-polyamide to investigate an improvement of the DNA cleavage selectivity of metal nucleases assisted by the modified cyclic polyamide with a flexible linker -CH2CH2CH2NH2.
The two polyamide-DNA systems are taken from the X-ray crystal structures of polyamide-DNA complexes. One is hairpin polyamide-DNA complex, ImImPyPy-γ-PyPyPyPy-β-Dp-d(AATATCCACCTGCA)2 (PDB code: 1M1A) ; and the other is cyclic polyamide-DNA complex, - d(CGCTAACAGGC)2 (PDB code: 1PQQ) , assigned as HPD and CPD, respectively. The branch C atom of [Cu(BPA)]2+ or [Cu(IDB)]2+ nuclease was bound manually to the tail N atom (sp3 hybridization) of each polyamide chain in HPD and CPD, which employed the protocols studied by Aldrich-Wright and co-workers for the polyamide - platinum(II) complexes [43, 44]. Then the substrate OOH- was introduced to the [Cu(BPA)]2+ or [Cu(IDB)]2+ nuclease to form an oxygen bridge for addressing the cleavage possibility. Finally, each whole system was explored to AutoDock 3.0 program for selecting the initial structure for the MD simulation. However, the position of N-tail in CPD lies in the distal Py residue of cyclic polyamide, which makes the orientation of the linking site point away from the DNA. For selecting an appropriate linking site, the group of -NH2 (as a linker) on the C atom (sp3 hybridization) of γ region was introduced to form the cyclic polyamide of associated with DNA, assigned as CPD γ , which was suggested by the previous experimental observations [55, 56]. Moreover, to improve the flexibility of liking region between the cyclic polyamide and nuclease, and to increase better the possibility of sugar hydrogen abstraction, the flexible linker of -CH2CH2CH2NH2 on the C atom (sp3 hybridization) of γ region was introduced to form the modified cyclic polyamide of associated with DNA, assigned as CPD γ Tail. The component sketches of six polyamide+copper nuclease+OOH- ligands are shown in the additional files 1A, B, C, D, E and 1F. Therefore, HPD + [Cu(BPA)OOH]+, CPD γ + [Cu(BPA)OOH]+ and CPD γ Tail + [Cu(BPA)OOH]+ were assigned as HPD-BPA, CPD γ -BPA and CPD γ Tail-BPA, respectively. Similarly, HPD + [Cu(IDB)OOH]+, CPD γ + [Cu(IDB)OOH]+ and CPD γ Tail + [Cu(IDB)OOH]+ were assigned as HPD-IDB, CPD γ -IDB and CPD γ Tail-IDB, respectively. Given that each strand of DNA has some phosphate groups, sodium ion counterions were separately added to each system to achieve electroneutrality. The systems were solvated explicitly by using the TIP3P water potential inside a central simulation box. The box dimensions ensure the solvent shell extended to10 Å in all directions of each system studied.
Molecular dynamics simulations
To take advantage of previous extensive simulations [44, 54, 57–60], the protocols employed therein were directly adapted in this study. The six MD simulations were carried out using the AMBER9 package with the AMBER force fields of parm99[61, 62] and gaff . The atomic types for the studied polyamides, OOH-, [Cu(BPA)]2+ and [Cu(IDB)]2+, except for copper atoms surrounding of [Cu(BPA)]2+ and [Cu(IDB)]2+ nucleases, were generated by using the ANTECHAMBER module included in AMBER9 program package. The force field parameters of copper center of [Cu(BPA)OOH]+ and [Cu(IDB)OOH]+ were evaluated based on the quantum chemical calculations in our previous work reported elsewhere [30, 33, 57]. The electrostatic potentials for RESP calculations have been calculated at the HF/6-31G** level of theory[64–66] using Gaussian03 program . The RESP charges of the polyamides, OOH-, [Cu(BPA)]2+ and [Cu(IDB)]2+ were derived by the RESP program based on the calculated electrostatic potentials.
The protocol for all MD simulations was described herein as follows: (1) The systems were energetically minimized to remove unfavorable contacts. Four cycles of minimizations were performed as follows, i.e. 5000 steps of each minimization with harmonic restraints from 100, 75, 50 to 25 kcal·mol-1·Å-2, which means that the restraints were relaxed stepwise by 25 kcal·mol-1·Å-2 per cycle, on DNA, polyamide and nuclease positions. The fifth cycle consists of 10000 steps of unrestrained minimization before heating process. The cutoff distance used for the nonbonded interactions was 10 Å. The SHAKE algorithm  was used to restrain the bonds containing hydrogen atoms. (2) Each energy-minimized structure was heated over 120 ps from 0 to 300 K (with a temperature coupling of 0.2 ps), while the positions of DNA, polyamide and nuclease were restrained with a small value of 25 kcal·mol-1·Å -2. The constant volume was maintained during the processes. (3) The unrestrained equilibration of 200 ps with constant pressure and temperature conditions was carried out for each system. The temperature and pressure were allowed to fluctuate around 300 K and 1 bar with the corresponding coupling of 0.2 ps, respectively. For each simulation, the integration step of 2 fs was used. (4) Finally, production runs of 30 ns were carried out by following the same protocol. A time of 200 ps after thermal warm-up in each simulation was selected as a starting point for data collections. During the production run, 15000 structures for each simulation were saved for post-processing by uniformly sampling the trajectory.
Results and Discussion
With the help of thirty nanosecond-long MD simulations, it was noted that these systems in water environment can be successfully simulated by using the protocol described above. The energies and root-mean-square deviations (RMSDs) for each simulation have been examined to clarify if each system had attained equilibrium. The RMSDs of each studied system with respect to its starting structure have attained equilibrium after 5 ns. The energies were found to be stable during the course of each remainder simulation. Hence, a time of 5 ns after thermal warm-up in each simulation was selected as a starting point for data collection and further analysis. The trajectory analysis for each system involves extracting the equilibrated conformations between 5 ns and 30 ns of simulation time, recording 12500 snapshots at every 2 ps time-interval of each trajectory. For the analyses of trajectories, the PTRAJ module of the AMBER9 program was used to extract production conformations.
Simulations of polyamide + [Cu(BPA)OOH]+-DNA complexes (HPD-BPA and CPD γ -BPA)
Simulations of polyamide + [Cu(IDB)OOH] +- DNA complexes (HPD-IDB and CPD γ -IDB)
Based on the discussion above, the two systems of HPD-BPA and HPD-IDB with different nuclease cleavage agents present similar cleavage properties to DNA. Namely, the [Cu(BPA)OOH]+ and [Cu(IDB)OOH]+ nucleases can be stably located at the minor groove of DNA, though the orientation of each cleavage agent in the minor groove of DNA is different. The [Cu(BPA)OOH]+ nuclease is parallel to the wall of the minor groove of DNA, and the [Cu(IDB)OOH]+ nuclease is located perpendicularly at the minor groove of DNA. On the other hand, for hairpin-polyamide recognition, the probability of hydrogen abstraction of the copper nuclease ligand [Cu(BPA) OOH]+ from DNA is similar to that of the [Cu(IDB)OOH]+ ligand, i.e., the C4'H abstraction from the sugar of DNA is favorable. However, for the two systems of CPD γ -BPA and CPD γ -IDB, both nuclease ligands cannot cause DNA strand scissions due to the inaccessibility of any hydrogen of the sugar moiety of DNA, which suggests that the DNA cleavage properties of [Cu(BPA)]2+ and [Cu(IDB)]2+ nucleases assisted by the cyclic polyamide are poor. In addition, though the recognition property of the cyclic polyamide with DNA is better than that of the hairpin polyamide,[48, 53, 56] the [Cu(BPA)]2+ or [Cu(IDB)]2+ nuclease assisted by the cyclic polyamide cannot achieve the specific DNA strand scission.
Simulations of modified-cyclic-polyamide + [Cu(BPA)OOH]+/[Cu(IDB)OOH]+-DNA complexes (CPD γ Tail-BPA and CPD γ Tail -IDB)
In summary, the simulated results of CPD γ Tail-BPA and CPD γ Tail-IDB present the stable conformations of the [Cu(BPA)OOH]+ and [Cu(IDB)OOH]+ ligands respectively bound to the N-tail of the modified cyclic polyamide associated with DNA. With the -CH2CH2CH2NH2 linker introduced, the [Cu(BPA)OOH]+ or[Cu(IDB)OOH]+ ligand can stably lie in the minor groove of DNA. There are some contacts between the linker and the minor groove of DNA, which leads to the increase of binding affinity, resulting in enhancing the probability of DNA strand scission. These observations suggest that a flexibility linker between the recognition and cleavage agent can provide crucial contributions to specific DNA cleavage of metal nucleases. In addition, it can be seen from the comparison of the HPD-BPA(IDB) and CPD γ Tail-BPA(IDB) systems, the two nucleases assisted by both hairpin polyamide and modified cyclic polyamide with a linker -CH2CH2CH2NH2 all can achieve selective DNA cleavage via the hydrogen abstraction from the sugar moiety of DNA, although the abstracted hydrogen type is different, i.e., the nucleases bound to the hairpin polyamide can efficiently abstract the C4'H atom of sugar; however, the nucleases bound to the modified cyclic polyamide with a linker -CH2CH2CH2NH2 can efficiently abstract the C1'H atom of sugar. That is to say the chemical nucleases bound to an appropriate polyamide-type recognition agent can improve efficiently the DNA cleavage selectivity.
A series of molecular dynamics simulations was performed to investigate the DNA cleavage specificities of the nucleases [Cu(BPA)]2+ and [Cu(IDB)]2+ assisted by the DNA recognition agents, hairpin and cyclic polyamides, via the analysis of hydrogen atom abstractions from the sugar rings in DNA. The simulated results indicate that the studied polyamide bound by the nuclease [Cu(BPA)]2+ or [Cu(IDB)]2+, presents a stable conformation located in the minor groove of DNA, which is consistent with the conformation of the corresponding polyamide bound to DNA presented in X-ray structure. For the different nucleases assisted by hairpin polyamide in the two systems of hairpin-polyamide + [Cu(BPA)OOH] + - DNA and hairpin-polyamide + [Cu(IDB)OOH] + - DNA, the nucleases present the similar DNA cleavage properties. That is to say, the [Cu(BPA) ]2+ or [Cu(IDB) ]2+ nuclease with a substrate OOH- bound to the hairpin polyamide can be stably located at the minor groove of DNA, and possibly abstracts the C4'H atom from the sugar moiety of DNA. However, for the [Cu(BPA)]2+ or [Cu(BPA)]2+ nuclease assisted with the cyclic polyamide in the systems of cyclic-polyamide + [Cu(BPA)OOH] + - DNA and cyclic-polyamide + [Cu(IDB)OOH] + - DNA, the probabilities of any hydrogen abstraction of the two nucleases from the sugar moiety of DNA are very small, which suggests that the nucleases cannot achieve DNA strand scission, due to the short and rigid linker between the branch C atom of nucleases and backbone of the cyclic polyamide. Therefore, the flexible linker of -CH2CH2CH2NH2 of γ region was introduced to the cyclic polyamide to improve DNA cleavage selectivity of the nucleases. It is of note that with the flexible linker introduction, the simulated results for the systems of modified-cyclic-polyamide + [Cu(BPA)OOH] + - DNA and modified-cyclic-polyamide + [Cu(IDB)OOH] + - DNA exhibit the high possibility of DNA cleavage by the [Cu(BPA)]2+ or [Cu(IDB)]2+ nuclease bound at the tail of the linker of the modified cyclic polyamide via C1'H atom abstraction from the sugar ring in DNA. Current observations suggest that the polyamide-type recognition agents with a flexible linker (γ-amino butyric acid) can efficiently improve the DNA cleavage properties of copper nucleases.
The authors acknowledge research support from the National Science Foundation of China (No. 20631020, 20771017, 20973024 and 21073015), the Major State Basic Research Development Programs (grant No. 2011CB808500). We also thank the HPSC of Beijing Normal University for providing computer resources.
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