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Orderly Microaggregates of G-/C-Rich Oligonucleotides Associated with Spermine Yan Fu,† Xian Wang,† Jinli Zhang,† Ying Xiao,‡ Wei Li,*,‡ and Jingkang Wang§ ‡
Key Laboratory for Green Chemical Technology MOE, † Key Laboratory of Systems Bioengineering MOE, § School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, People’s Republic of China
bS Supporting Information ABSTRACT: Spermine-induced orderly assembling properties of G-/C-rich oligonucleotides are investigated in dilute and crowding conditions. The first time we report that the parallel G-quadruplexes is preferential to condense into anisotropic microaggregates in the presence of spermine, whereas the hybrid-type and the antiparallel G-quadruplexes have no significant interactions with spermine; and spermine can induce the condensation of i-motif C-rich oligonucleotides other than the random coiled C-rich strands. Moreover, the condensation of C-rich oligonucleotides can be reversibly regulated by pH and temperature. G-/C-rich oligonucleotides exhibit the cholesteric liquid crystalline phase at low strand concentration in the presence of spermine under crowding conditions. The results illuminate that the parallel G-quadruplex and i-motifs are probably necessity conformations for G-/C-rich oligonucleotides that involved in the regulation of chromosome organization in living cells.
’ INTRODUCTION DNA in viruses and cells exists in a highly condensed and tightly packed state, which is sensitive to stimuli of chemical agents, including multivalent cations, alcohol, drug, basic proteins, neutral crowding polymers, and so on.1 The natural polyamines involving spermine, spermidine, and putrescine, ubiquitous aliphatic multivalent cations with low molecular weights, can interact with backbone phosphate groups via electrostatic interactions to modulate DNA/RNA structures and condensate DNA molecules to liquid crystalline phase.2-5 Polyamines participate in cell proliferation and differentiation, as well as protect DNA molecules from common damaging agents, such as ionizing radiation and reactive oxygen species.6-9 For DNA secondary structures beyond the Watson-Crick duplex, Thomas and coworkers reported that aggregation of triple-stranded motifs promoted by polyamines was easier than double- and singlestranded DNAs, suggesting that triplex DNA may participate in the regulation of chromosome organization in living cells.10 Kenir et al. reported that large disparities of intramolecular NOEs (overhauser effects) formed due to the complex between spermine and antiparallel quadruplex (G4T4G4, G2T2G2TGTG 2 T 2 G 2 ) and linear four-stranded parallel quadruplex (TG4T), suggesting that spermine interacts discriminately with DNA, and the binding is sensitive to DNA conformation.11 Kumar and co-workers reported that polyamines can drive the c-MYC gene expression by inducing structural transition of c-MYC quadruplex to a transcriptionally active motif and regulating G-quadruplex and Watson-Crick duplex competition.12 So far, most of the reports on the interactions of polyamines and r 2011 American Chemical Society
DNA secondary structures were performed in dilution solution but not under cell-mimicking crowded conditions. Neutral crowding polymers, being utilized to mimic the intracellular crowded environment in vitro, are reported to dramatically modulate DNA polymorphic structures and induce DNA collapse owing to volume exclusion effect.13-15 Especially for the guanine-rich DNA, crowding conditions are reported to induce complete conversion into parallel G-quadruplexes of the Oxytricha nova telomeric DNA G4T4G4 and Tetrahymena telomeric DNA T2G(G3T2G) 3G in Naþ solution, as well as the human G3(T2AG3)3 telomeric DNA in Kþ solution.16-18 Rajendran et al. reported that triplet repeat CGG(CCT)nCGG (n = 4, 6, 8, 10) adopts the i-motif structure at neutral pH under molecular crowding conditions because the pKa of N3 of cytosine is raised in such a microenvironment.19 Therefore, cellular crowding conditions play a critical role in modulation of DNA polymorphism. Intriguingly, the cooperative effect of polyamine and crowding agent was found to induce the self-assembling of triple-stranded DNA motifs into liquid crystal microaggregates.20 G-rich DNAs, enriched in eukaryotic telomeres and proto-oncogene promoters and potentially involved in inhibition of telomere extension and modulation of gene transcription,21,22 can fold into polymorphic G-quadruplexes with cyclic Hoogsteen base pairs of four guanine bases, of which the conformational structures are influenced not Received: November 17, 2010 Revised: December 20, 2010 Published: January 14, 2011 747
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Table 1. G-/C-Oligonucleotides Used in This Study name
sequence
source
AG22
50 -AGGGTTAGGGTTAGGGTTAGGG-30
human telomeric DNA
GT12
50 -GGGGTTTTGGGG-30
Oxytricha nova telomeric DNA
TBA
50 -GGTTGGTGTGGTTGG-30
thrombin binding aptamer
bcl23
50 -GGGCGCGGGAGGAAGGGGGCGGG-30
BCL-2 promoter
c-kit1
50 -AGGGAGGGCGCTGGGAGGAGGG-30
c-kit promoter
c-kit2
50 -CGGGCGGGCGCGAGGGAGGGG-30
c-kit promoter
RET1
50 -AGGGGCGGGGCGGGGCGGGGGC-30
RET promoter
C-MYC27 CT22
50 -TGGGGAGGGTGGGGAGGGTGGGGAAGG-30 50 -CCCTAACCCTAACCCTAACCCT-30
C-MYC promoter human telomeric DNA
RET2
50 -GCCCCCGCCCCGCCCCGCCCCT-30
RET promoter
CA12
50 -CCCCAAAACCCC-30
Oxytricha nova telomeric DNA
dropped onto the clean plane (110) of the silicon wafer substrate (1 1 cm). The RAIR measurement was obtained by averaging 128 scans at a 2 cm-1 resolution and an incidence angle of 45°. The polarizer was positioned at 0, 45, and 90°, respectively. Dynamic Light Scattering (DLS). DLS measurements were performed on the Zetasizer Nano equipment (Malvern instruments) at 25.0 °C. The DNA samples (10 μM) were annealed in the absence or presence of 0.5 mM spermine in dilute solutions. Atomic Force Microscope (AFM). About 20 μL of DNA samples (10 μM) were dropped onto freshly cleaved mica substrate. After a 10 min adsorption, the mica surface was rinsed with distilled water and dried by nitrogen gas. AFM imaging was carried out using a Nanoscope IIIa AFM (Veeco Instrument) with tapping mode. All samples were imaged in air. Transmission Electron Microscope (TEM). Electron microscope was performed on JEM-2010FEF equipment (JEOL, Japan). Electron microscopy samples were prepared by applying 10 μL of DNA solutions on a carbon-coated grid for 5 min, and then excess liquid was removed with filter paper. Polarized Light Microscopy (PLM). About 20 μL of DNA samples (40 μM) were deposited between a slide and a coverslip. The DNA condensates were imaged on an Olympus microscope (Olympus). Specimens were observed through cross polarizers with the use of a quartz retardation plate positioned at an angle of 35° relative to the samples.
only by their sequence, but also by their surroundings, involving cations, temperature, drug, and molecular crowding agents.23-26 Complementary C-rich DNAs can fold into the i-motif structure at acidic pH value, a tetrameric structure formed of two parallel duplexes through the intercalation of hemiprotonated cytosinecytosine base pairs.27,28 Whether or not there exists the cooperative effect of polyamine and crowding agent on the structural transition of G-/C-rich DNAs is important to reveal the regulation of chromosome organization in living cells. In this article, under cellular environments we studied the influence of spermine on the condensation of G-quadruplex and i-motif forming sequences, that is, a series of G-rich and C-rich oligonucleotides from eukaryotic genome, involving telomeric regions and promoters of proto-oncogenes. It is intriguing to find out that very short G-rich strands display condensed states in the presence of spermine with high sequence specificity, and the condensation of C-rich oligonucleotides can be reversibly regulated by pH and temperature.
’ MATERIALS AND METHODS Chemicals and Reagents. Oligonucleotides listed in Table 1 were purchased from Japanese Takara Bio. (Dalian), with the purity higher than 98% measured by HPLC. Spermine was purchased from Sigma with the purity higher than 97%. Polyethylene glycol 200 (PEG200) was purchased from Tianjin Chemical Reagent Co. with A. R grade. In this study, single tetravalent spermine was dissolved in Trisborate or MES buffers, and no nuclear aggregates were detected. Circular Dichroism (CD). CD experiments were carried out with a Jasco J-810 spectropolarimeter equipped with a Julabo temperature controller. All the CD spectra were measured in a 1 mm cell from the wavelength of 220-350 nm with a scan speed of 100 nm/min. CD samples were annealed by heating to 95 °C for 5 min and then cooling to room temperature in 90 mM Tris-Borate buffer (pH 7.0) for G-rich strands and 20 mM MES (pH 5.0) for C-rich strands. UV Spectroscopy (UV). UV spectra were performed on a Cary Varian UV/vis spectrophotometer equipped with a digital circulating water bath. UV spectra were measured in a 1 mm cell at 5 min later since the titration of spermine into DNA containing buffer solutions. Each sample was scanned from the wavelength of 220-500 nm with a scan speed of 200 nm/min. UV melting profiles were monitored at 260 or 295 nm in a cuvette of 1 mm path length with a heating rate of 0.5 °C/min. UV samples were prepared as those used in CD spectra. Infrared reflection-absorption spectroscopy (IR-RAS). A Nicolet iS10 FT spectrometer equipped with the Model 500° variable angle specular reflectance accessory and the MCT detector was used to obtain the polarized IR-RAS spectra. About 20 μL of DNA samples were
’ RESULTS AND DISCUSSION Sequence Specificity of Spermine-Induced Condensation of G-Rich Oligonucleotides. According to the structural char-
acteristics of the G-quadruplex, G-rich oligonucleotides from telomeric regions and promoters of proto-oncogenes, as listed in Table 1, are classified into three groups, that is, the parallel, the antiparallel, and the mixed antiparallel/parallel G-quadruplexes. The conformational structures of all these G-rich oligonucleotides in dilute solutions are consistent with previous references through characterization of the CD spectra (Figure S1 in the Supporting Information). As the representative of the parallel G-quadruplexes, CD spectra of the c-kit2 solution titrated by spermine in the presence of Kþ at 20 °C are shown in Figure 1a, which indicates that the typical band of parallel G-quadruplex around 262 nm gradually decreases with a red-shift as the concentration of spermine increases to 1 mM, while the CD intensity near 290 nm apparently enhances. Figure 1b displays the UV spectra of the spermine-titrated c-kit2 solution; the peak at 255 nm gradually decreases, whereas the peak near 320 nm increases with the 748
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Figure 1. CD (a) and UV (b) spectra of the parallel G-quadruplex c-kit2 (20 μM) in 100 mM Kþ (90 mM TB, pH 7.0) titrated with spermine from 0.1 to 1 mM at 20 °C; (c) Plot of normalized A320 nm of four G-rich oligonucleotides forming the parallel quadruplexes as a function of spermine concentration; (d) UV melting curves of 20 μM c-kit2 in the absence and the presence of 0.05, 0.1, 0.2, and 0.5 mM spermine, respectively.
spermine concentration. In addition, there exist isosbestic points around 270 nm at the spermine concentration of 0-0.5 mM, which gradually shift to 288 nm as the spermine concentration increases to 0.6-1.0 mM, suggesting the occurrence of a multistate conformational transition of G-quadruplex associated with spermine. It is known that UV absorbance of DNA solutions at the long wavelengths such as 320 nm (A320 nm) is a clear manifestation of Tyndall scattering, indicating the existence of nanometer DNA aggregates.29,30 Interestingly, for other parallel G-quadruplexes including RET1, C-MYC27, and c-kit1 in the presence of 100 mM Kþ, UV spectra also show that the A320 nm value increases with the spermine concentration just like c-kit2, which illustrates that spermine can induce the type of parallel G-quadruplexes to condense into microaggregates (Figure 1c). We performed UV melting experiments to investigate the thermodynamic effects of spermine on the structural transition of c-kit2 in Kþ solution. As shown in Figure 1d, the transition temperature (Tm) increases by 3.0 °C in the presence of 0.1 mM spermine. As the spermine concentration increases from 0.2 to 0.5 mM, the Tm value is enhanced and the UV melting profiles turn to be nonsingle stages with two transition temperatures. The low and high Tm values are determined, respectively, as 25.0 and 78.0 °C at 0.2 mM spermine and 34.0 and 82.0 °C at 0.5 mM
spermine. These results are consistent with the shift of multiisosbestic points in UV spectra (Figure 1b). DLS measurements (Figure 2a) indicate that titration of 0.5 mM spermine into the c-kit2 solution makes the average hydrodynamic diameter increase from 0.7 nm to 1 μm, and the hydrodynamic diameter turns to be 1.5 μm when the final mixing solution was annealled. AFM images (Figure 2b and Figure S2) display that c-kit2 can assemble into the network-like structure in the presence of spermine with an average height of 4.5 nm. TEM images as shown in Figure 2c exhibit the network-like microaggregates with a size distribution of >1 μm. We also study the influence of spermine on other types of G-quadruplexes involving the hybrid-type and the antiparallel. As shown in Figure 3a, titration of spermine has little effect on the CD spectra of the hybrid conformation of AG22, and the UV spectra only show a fraction of intensity decrease at 255 nm without the appearance of a band around 320 nm (Figure S3a). UV melting curves of AG22 in the presence of different concentrations of spermine exhibit a single transition temperature, and the Tm value increases about 3.0 °C at high spermine concentration of 1 mM (Figure 3b). DLS measurement shows that small nanoparticles with a size distribution of 0.6-3.5 nm are observed in the presence of 0.5 mM spermine after annealing, and no large aggregates are detected for this hybrid-type 749
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Figure 2. (a) DLS measurements of the parallel G-quadruplex c-kit2 (10 μM) in 100 mM Kþ solution (90 mM TB, pH 7.0) in the absence and presence of 0.5 mM spermine; (b) AFM images of 10 μM c-kit2 in 100 mM Kþ solution (90 mM TB, pH 7.0) with 0.5 mM spermine, the scan scale is 5 5 μm; (c) TEM images of 10 μM c-kit2 in 100 mM Kþ solution (90 mM TB, pH 7.0) with 1 mM spermine, the scale bar is 0.2 μm.
and TBA in 100 mM Kþ (the so-called nontransform-group) show no conformational transition induced by the crowding condition. The CD characteristic band of the transform-group AG22 in Kþ solution is intensified with a slight blue-shift as spemine increased to 0.5 mM and then decreased as 1 mM spermine titrated, indicating conformational changes can be induced by spermine under crowding conditions but not in dilute solutions (Figure 4b and Figure 3a). It is noteworthy that as the spermine concentration increases from 0.1 to 1 mM, UV spectra of the transform-group oligonucleotides show a significant increase of the A320 nm signal and a gradual decrease of A260 nm signal with a slight red-shift, as shown in Figure 4c,d. The increased A320 nm signal indicates the formation of microaggregates, and the scale of dense aggregates can reach to 1 μm, which was proved by AFM images of AG22 in 100 mM Kþ under crowding conditions (Figure S4), unlike those small nanoparticles (about 2 nm) in dilute solutions. However, for the nontransform-group oligonucleotides, no increase of UV absorbance at 320 nm is observed, and only small nanoparticles appear in AFM images of the spermine-titrated DNA solution (Figure S5). The results suggest that the condensation caused by spermine has a sequence specificity of G-rich oligonucleotides, that is, only the parallel G-quadruplexes are susceptible to assemble into
quadruplex (Figure 3c). AFM images shown in Figure 3d confirm that the AG22-spermine complex exhibits nanoparticles (about 2 nm) without further assembling to microaggregates like parallel c-kit2 (Figure 2b). Similarly, for the antiparallel quadruplex of AG22 and GT12 in the presence of 100 mM Naþ, as well as TBA and bcl23 in the presence of 100 mM Kþ, no UV absorbance of DNA solutions around 320 nm are observed during the titration of spermine, as reflected by the UV spectra in Figures S3a and S3b. Therefore, it indicates that the parallel G-quadruplexes are preferential to condense into network microaggregates in the presence of spermine, whereas the hybrid-type and the antiparallel G-quadruplexes have no significant interactions with spermine. Crowding conditions have been reported to induce the complete conversion of Oxytricha nova telomeric DNA G4T4G4 into parallel G-quadruplexes in the presence of Naþ,17 it enlightens us to investigate the influence of spermine on the hybrid-type and the antiparallel G-quadruplexes under crowding conditions. Under molecular crowding conditions created by 40% PEG200, as shown in Figure 4a, CD spectra indicate that the antiparallel quadruplex GT12 in 100 mM Naþ, the hybrid-type quadruplexes AG22 and bcl23 in 100 mM Kþ (the so-called transform-group) exhibit a structural transition into the parallel conformation, whereas the antiparallel AG22 in 100 mM Naþ 750
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Figure 3. (a) CD spectra of the hybrid-type quadruplex AG22 (20 μM) in 100 mM Kþ solution titrated with spermine (0.2, 0.5, 1 mM) at 20 °C; (b) UV melting of 20 μM AG22 in the absence and the presence of 0.2, 0.5, and 1 mM spermine, respectively; DLS measurement (c) and AFM image (d) of 10 μM AG22 in 100 mM Kþ solution (90 mM TB, pH 7.0) in the presence of 0.5 mM spermine after annealing; the scan scale is 2 2 μm.
microaggregates through interactions with spermine; moreover, the crowding agent works as a structural inducer to facilitate the condensation of G-rich DNAs besides its function of producing a crowding environment between macromolecules. To assess the nature of microaggregates observed by AFM, we observed the microaggregates of AG22 in 100 mM Kþ solution under 40% PEG200 incubated at 1 mM spermine using polarized light microscopy, respectively. As shown in Figure 4e, microaggregates of AG22 exhibit highly birefringent fluid droplets, which represent the cholesteric mesophase at low strand concentration (0.27 mg/mL). Previous work on Watson-Crick duplexes reported that DNA condensation can not be observed for segments 250 mM).20 In the case of AG22 incubated with 0.5 mM spermine, the UV absorbance at 320 nm gradually decreases with the temperature increasing to 90 °C, suggesting the microaggregates partially melt at high temperature. In the cooling process, the gradually increased A320 nm value indicates the formation of microaggregates at low temperature. However, as the spermine concentration increases to 1 mM, the A320 nm value is not sensitive to the increasing temperature, suggesting that AG22 condensates are stable at high temperature under such conditions (Figure 7b). Next, the above single-inflection melting curves of i-motif CT22 enlighten us to study the reversible regulation of the condensed microaggregates by the stimuli of pH and temperature. UV spectra of i-motif CT22 illustrate that both A320 nm and A260 nm values exhibit reversible changes by adjusting repetitively the pH level between 5.0 and 7.0 (Figure 8a), indicating the possibility of reversible regulation of the condensation of CT22 in the presence of spermine. Such a kind of reversible regulation of the condensation by adjusting pH is also observed for the i-motif RET2 (Figure S8). As shown in Figure 8b, the strong signal of A320 nm value occurs at state 2, while the other three states show a low signal, which corresponds to spermine concentration and pH levels.
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Moreover, the A320 nm and A260 nm signals can also be reversibly modulated by the temperature level. For the i-motif CT22 in the presence of spermine (the Tm value of 55.5 °C, Figure 6b), the microaggregates are stable at 50 °C, with a significant A320 nm signal, while the microaggregates resolubilize at 70 °C without A320 nm signals (Figure 8c). Figure 8d shows the A320 nm value only has a strong signal at state 1, responding to pH and temperature. In the case of C-rich RET2 in the presence of spermine, the melting temperature at pH 6.3 and 5.0 is 55 and 78 °C, respectively (Figure 8e). It is shown that the A320 nm signal of RET2 at pH 6.3 titrated with spermine disappears at 70 °C, whereas this induced signal is significant at pH 5.0 and 70 °C. Figure 8f shows that only state 4 has no clear absorbance at 320 nm, which is stimulated by pH and temperature. These intriguing results illustrate that the i-motif C-rich oligonucleotides are potential candidates to explore switchable nanomolecular materials based on the reversible regulation of the condensed microaggregates responding to the change of pH and temperature. Several reports have systematically investigated the regulation of condensation process of DNA molecules. For instance, the condensed state of DNA molecules, involving Watson-Crick duplex or triplex, can be resolubilized by increasing the concentration of salts or polyamines.10,20 Condensation behavior of linear DNA molecules can be controlled by pH- or lightresponsive cationic surfactant.41,42 Polyamine-promoted nanoparticles of condensed λ-DNA show the changes in morphology and size with an increase in temperature. However, reversible regulation of polyamine-induced condensation is the first time reported here for the i-motif C-rich oligonucleotides.
’ CONCLUSIONS A series of G-rich or C-rich oligonucleotides from eukaryotic genome, involving telomeric regions and promoters of protooncogenes are chosen to study the influence of spermine on the structures of G-quadruplexes and i-motifs both in dilute and crowding solutions. The first time we report that very short G-rich strands display condensed states in the presence of spermine with high sequence specificity, that is, the parallel G-quadruplex motifs are preferable to condensate both in dilute and crowding conditions. The condensation of C-rich oligonucleotides is favorable to i-motif structures at acidic conditions rather than random coils at neutral conditions, which can be reversibly regulated by pH and temperature. G-/C-rich oligonucleotides exhibit the cholesteric liquid crystalline phase at low strand concentration in the presence of spermine under crowding conditions. Therefore, the observations strongly support the notion that polymorphic oligonucleotides, especially the parallel G-quadruplex and i-motifs, are necessity conformations that involve the regulation of chromosome organization in living cells and further participate in gene expression and DNA protection. ’ ASSOCIATED CONTENT
bS
Supporting Information. Supporting Figures S1-8. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Tel.: þ86-22-27890643. Fax: þ86-22-27890643. E-mail: liwei@ tju.edu.cn. 755
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’ ACKNOWLEDGMENT This work was supported by NSFC (20776102, 20836005), the National Basic Research Program of China (2006CB202500), the RFDP, and the NCET.
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