Calcium Ions Affect Water Molecular Structures Surrounding

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Calcium Ions Affect Water Molecular Structures Surrounding Oligonucleotide Duplex Revealed by Sum Frequency Generation Vibrational Spectroscopy Xu Li, Liang Ma, and Xiaolin Lu Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b01763 • Publication Date (Web): 08 Aug 2018 Downloaded from http://pubs.acs.org on August 20, 2018

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Calcium Ions Affect Water Molecular Structures Surrounding Oligonucleotide Duplex Revealed by Sum Frequency Generation Vibrational Spectroscopy Xu Li#, Liang Ma#, Xiaolin Lu* State Key Laboratory of Bioelectronics, School of Biological Science & Medical Engineering, Southeast University, Nanjing, 210096, Jiangsu Province, P. R. China

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ABSTRACT

Solvation of DNA in water facilitates the formation of a hydration layer surrounding it, thus stabilizing the DNA duplex in the biological aqueous environment. In this study, via using the lipid bilayer as a soft substrate to accommodate the duplex oligonucleotide, the structure of the water layer surrounding the oligonucleotide was detected under the perturbation of the calcium ions (Ca2+) with chiral and achiral sum frequency generation (SFG) vibrational spectroscopy. With increasing the Ca2+ concentration, both the chiral and achiral water vibrational signals showed the similar concentration-dependent changes, i.e. an initial decrease phase followed by an increase phase. However, when the Ca2+ concentrations were adjusted within the range comparable to those in the human serum, the chiral water vibrational signals kept nearly unchanged, whereas the achiral water vibrational signals still changed as a function of the Ca2+ concentration. Therefore, the current experimental result supports the possible protection function of the chiral hydration layer against the Ca2+ ions, which generally exist in the cell sap and play important roles in many biological functions.


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INTRODUCTION Deoxyribonucleic acid (DNA) encodes the genetic information and facilitates the metabolism by transcribing the protein molecules with specific amino acid sequences in the biological aqueous environment under the regulation of the transcriptase.1 Understanding the structurefunction relationship of DNA at the molecular level is thus of great importance.2-5 A duplex DNA is composed of two single strands linked by the hydrogen bonding. The hydrogen bonding between DNA and the surrounding water molecules is also believed to play an important role in stabilizing the DNA duplex structure.6-8 As is reported, the water molecules surrounding the duplex DNA can be classified as two types. One is the “bulk water” constituting the major portion of the surrounding environment, and the other is the “bound water” within the solvation shell of the duplex DNA (which can also be termed as the hydration layer).6 The strong interaction with the chiral spine of the DNA makes the water molecules in the interfacial hydration layer significantly different from those in the bulk water. Consequently, the bound water molecules surrounding a duplex DNA may function as a protective layer against the external perturbations like ions, oxygen, and ultraviolet (UV) light, etc. The bound water molecules or the hydration layer can be found in both the major and minor grooves around the duplex DNA.4,5 Any interaction with the DNA from the external environment, e.g. from the ions or the free radicals, whether directly or indirectly, has to be involved in or mediated by this hydration layer, and finally needs to overcome the protective function of this hydration layer. Previous experimental investigations have shown that the water molecules inside the minor groove of a duplex DNA are inclined to form the assembled ordered superstructure surrounding the DNA’s chiral spine and the water molecules inside the major groove prefer to be in a relatively random state.9-12 Furthermore, the molecular simulation studies suggested a slower


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water molecular dynamics inside the minor groove in comparison to that inside the major groove. The entropy of the water molecules for the hydration layer in the minor groove is thus less than that of the water molecules in the major groove.13-15 Recently, Petersen et al. probed the interfacial water molecular structures around a 24-base pair double-stranded DNA sequence using the chiral sum frequency generation (SFG) vibrational spectroscopy.16 The existence of the DNA’s chiral spine of hydration was confirmed, showing consistence with the previous experimental results from the X-ray crystallography.9-12 However, there still remain scientific issues deserved to be discussed. As mentioned above, the water molecules inside the DNA’s minor groove can forge a chiral water superstructure. Regarding to this, can we prove this chiral hydration layer’s protection function against the external perturbations, for example the ionic interaction? In this study, a 15-base pair double-stranded oligonucleotide sequence was used as a model DNA. We focus on probing the perturbation of the calcium ions (Ca2+) on the interfacial water structure surrounding the double-stranded oligonucleotide using the chiral and achiral SFG vibrational spectroscopy, since the Ca2+ ions are one of the most abundant metal ions in the human body. Over a broad range of the Ca2+ concentrations, the interfacial water chiral and achiral vibrational signals were detected, which reflect the water molecular structures sticking to the double-stranded oligonucleotide and outside the double-stranded oligonucleotide. We prove that, in the normal biological conditions, the chiral and achiral water layers respond differently to the external interaction from the Ca2+ ions. EXPERIMENTAL SECTION Materials. 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) and deuterated DPPC (dDPPC) samples were purchased from Avanti Polar Lipids, Inc. The single strand oligonucleotide


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sample

with

3′-end

modified

by

cholesterol-triethylene

glycol(Chol-TEG)

(5′-

GCTTCCGAAGGTCGA-3′) and the complementary one were ordered from Nanjing Genscript Biotechnology Co. Ltd. First, a lipid monolayer (DPPC and d-DPPC in a molar ratio of 1:1) deposited onto the calcium fluoride (CaF2) right-angle prism was prepared using a LangmuirBlodgett (LB) trough (KN 2003, KSV NIMA Co., Ltd.). Briefly speaking, the prism was attached to a homemade sample holder with one prism face perpendicularly dipped into the aqueous environment of the LB trough. Afterwards, the mixed lipid solution was injected onto the water surface until the surface pressure reached a certain value below 34 mN⋅m-1. After the surface pressure leveled off, two Teflon barriers were used to compress the lipid monolayer at a ratio of 5 mm/min till the surface pressure of 34 mN⋅m-1 was reached. Finally, the prism with a lipid monolayer was vertically lifted out of the water at a rate of 1 mm/min. To prepare the other lipid monolayer, the duplex oligonucleotide solution was mixed with the lipid solution in a molar ratio of 1:100 (oligonucleotide to lipid) to facilitate the assembly of the oligonucleotide and the lipid via the hydrophobic interaction (cholesterol and lipid alkyl chain). In this case, the mixed DPPC and d-DPPC bilayer with inserted duplex oligonucleotide at the bottom was prepared onto the CaF2 prism and suitable for the SFG measurement, as shown in Figure 1. SFG experimental. The SFG experiment was performed using a commercial SFG system (EKSPLA, Lithuania), which has been described elsewhere.17 In short, based on a Nd:YAG laser, a 1064-nm beam with a pulse width of ~20 ps and a frequency of 20 Hz was generated first. Through the second and third harmonic units, the 1064-nm beam was converted into a 532nm beam and a 355-nm beam. The 532-nm beam was directly used as the visible input. Via the optical parametric generation (OPG)/optical parametric amplification (OPA) and the difference frequency generation (DFG) processes, the 355-nm beam was converted into the incident


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infrared (IR) beam covering the mid-IR frequency range. The incident angles of the IR and visible beams were set to be 53° and 64°, versus the surface normal, respectively. The ssp and spp polarization combinations were used in this study. The principles of the chiral SFG have been reviewed by Simpson and Yan, et al.18-22 In general, there are three polarization combinations which can be used for detecting the chiral interface, namely, spp, psp, and pps. In this study, the spp polarization combination was chosen to detect the χzyx term (electronically nonresonant). And the ssp polarization combination was chosen to detect the χyyz term. Our SFG system was checked for the leakage problem and we found the leakage didn’t affect our experimental results. And all the SFG spectra were normalized from zero to one for the ease of comparison (see the Supporting Information for the original spectra).

Figure 1. Schematic shows the SFG experimental setup in this study. RESULTS and DISCUSSION Regarding the duplex oligonucleotide anchoring onto the lipid bilayer,23,24 the SFG ssp and spp spectra in the frequency range from 2800 cm-1 to 3800 cm-1 were collected, corresponding to the CH and OH stretching vibrational range, as shown in Figure 2. Since the symmetric lipid bilayer (DPPC and d-DPPC in a molar ratio of 1:1) was used, no CH vibrational signals from the lipid molecules were observed and only the water OH vibrational signals were detected. Attention


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should be paid, in the case that the lipid bilayer was damaged, different SFG vibrational signals from the current ones would be observed. Perturbed by the Ca2+ ions, the interfacial water vibrational signals resulting from both the duplex oligonucleotide/water and lipid bilayer/water interfaces showed a strong dependence on the Ca2+ concentration, for both ssp and spp spectra. Previous reports indicated, even for the seemingly simple system, i.e. the water surface in air, assignment of the water OH stretching vibrational bands can be very complicated.25-30 Here for this relatively complex system, we tentatively assign the broad band located at ~3200 cm-1 to the strongly hydrogen-bonded water, while the band at ~3400 cm-1 is assigned to the mediumintensity hydrogen-bonded water.16 And the one at ~3600 cm-1 is attributed to the weakly hydrogen-bonded water.16 As shown in Panel A of Figure 2, for the pure bilayer, the achiral (ssp) water vibrational signals were very weak. Upon anchoring of the duplex oligonucleotide, the spectral intensity significantly increased since the negative charged oligonucleotide would induce the orientation of the adjacent water molecules and favor the ordered arrangement of the interfacial water molecules.31,32 With the addition of the Ca2+ ions, the overall spectrum showed a two-phase change, namely, an initial decline (from 0.006 mM to 0.6 mM) followed by an latter increase (from 0.6 mM to 60 mM), as shown in Panel C of Figure 2. As is known, the phase-sensitive SFG could resolve the sign for each individual vibrational peak. However, in this study, we are more interested in the peak area rather than the sign. So the integrated peak area was plotted as a function of the Ca2+ concentration. One may ask, why the amplitude was not used here. Actually, owing to the inhomogeneous broadening and distortion of the water OH stretching vibrational peaks, using the amplitude might lead to the nonnegligible error. So using the integrated peak area is relatively a better approach to reflect the water vibrational signal change in terms of the


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Ca2+ concentration. In Panel C of Figure 2, the decline phase can be explained by the screening effect due to the introduction of the positive Ca2+ ions.31,32 The induced order of the water molecules by the duplex oligonucleotide would gradually degenerate into a relatively random state. Furthermore, when the interfacial Ca2+ concentration reached a certain critical value, the interfacial charge effect will totally be screened and then the spectral intensity will reversely increase with the augment of the Ca2+ ions due to the accumulation of the positive charge at the interface. Here a question should be raised, why the Ca2+ ions were continuously adsorbed onto the interface after the negative charge of the duplex oligonucleotide had already been screened. In order to answer this question, the interfacial water behavior for the pure bilayer perturbed by the Ca2+ ions needs to be investigated. As shown in Panels A and B of Figure 3, the intensity of the interfacial water vibrational signals of the pure bilayer continuously increased with the augment of the Ca2+ concentration. Apparently, the pure bilayer has the capability to attract the Ca2+ ions from the bulk solution. Based on the previous reports,33-36 the carboxyl groups at the lipid hydrophilic head part can bind positive charged ions, such as Na+, K+ and Ca2+. Thereafter, besides the phosphate groups, the carboxyl groups also contribute to the interfacial accumulation of the Ca2+ ions, leading to the increase of the interfacial water vibrational signals. To summarize, the added Ca2+ ions would first be adsorbed onto the surface of the duplex oligonucleotide due to the strong electrostatic interaction. At the same time, the Ca2+ ions could be bound to the lipids. After the oligonucleotide surface charge was neutralized, the excessive Ca2+ ions would induce the order of the interfacial water molecules. Hence, the collected spectra showed a two-phase variation. Up to now, we have observed the Ca2+ concentration-dependent behavior for the interfacial achiral (ssp) water vibrational signals contributed by both the duplex oligonucleotide/water and the lipid/water interfaces. Next, the chiral (spp) SFG will be used to


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differentiate the vibrational signals of the water molecules binding to the duplex oligonucleotide from those binding to the lipid bilayer.

Figure 2. Achiral (ssp, A) and chiral (spp, B) SFG spectra for the duplex oligonucleotideanchored lipid bilayer in contact with the Ca2+ solutions with different concentrations (from 0.006 mM to 60 mM). The data points were approximately fitted by using the Lorentz function. The change of the integrated area for the vibrational signals as a function of the Ca2+ concentration was also presented (ssp, C; spp, D). All the spectra have been normalized and offset for clarity. (The error bar for 10 mM in Panel D is too small to be observed.)


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Figure 3. Achiral (A) SFG spectra for the lipid bilayer in contact with the Ca2+ solutions with different concentrations (from 0.006 mM to 60 mM). The data points were approximately fitted by using the Lorentz function. The change of the integrated area for the vibrational signals as a function of the Ca2+ concentration was also presented (B). All the spectra have been normalized and offset for clarity. As shown in Panel C of Figure 2, the chiral (spp) SFG spectra were used to reveal the chiral structure of the water molecules binding to the duplex oligonucleotide under the perturbation of the Ca2+ ions. Our experiment showed that there are no chiral (spp) vibrational signals for the pure lipids, indicating no chiral water structure exists at the lipid/water interface. Upon adding the Ca2+ ions, the intensity of the chiral water vibrational signals showed an initial decrease and then an increase trend as a function of the Ca2+ concentration, as shown in Panels C and D of Figure 2. This initial decrease can easily be understood on considering the screening effect from the Ca2+. The latter increase suggests the excessive Ca2+ ions could also bind to the duplex oligonucleotide and might induce the chiral order of the interfacial water molecules. The above experimental observation is actually consistent with what people expect, i.e. the Ca2+ ions at the interface not only interact with the lipid surface but also with the duplex oligonucleotide. Within


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such a broad range of the Ca2+ concentrations (from 0.006 mM to 60 mM), it seems there is no much difference for the achiral and chiral water vibrational signals in terms of the Ca2+ concentration, namely, both the achiral and chiral water vibrational signals were strongly affected by the Ca2+ ions. As reported in literatures,4,5,9-16 the chiral water signals are mainly contributed by the water molecules in the minor groove of the duplex oligonucleotide, which forms a chiral superstructure around the duplex oligonucleotide. This chiral water layer is assumed to be strongly bound to the backbone of the duplex oligonucleotide. However, our experiment discloses that order or arrangement of this strongly binding water layer can still be affected by the Ca2+ ions.

Figure 4. Achiral (ssp, A) and chiral (spp, B) SFG spectra for the duplex oligonucleotideanchored lipid bilayer in contact with the Ca2+ solutions with different concentrations (from 0.6


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mM to 6 mM). The data points were approximately fitted by using the Lorentz equation. The change of the integrated area for the water vibrational signals as a function of the Ca2+ concentration was presented (ssp, C; spp, D). All the spectra have been normalized and offset for clarity. Attention should be paid that the normal Ca2+ concentrations in the human serum are between ~0.94 mM and ~1.33 mM.37,38 We would like to know, in a Ca2+ environment similar to the human serum, whether the water layer surrounding the duplex DNA can offer the protection against the change of the external Ca2+ ions. Hence, we focused on the Ca2+ concentration range from 0.6 mM to 6 mM. As shown in Panels A and C of Figure 4, from the achiral water vibrational signals, the normal interfacial water layer (achiral, from the lipid/water and duplex oligonucleotide/water interfaces) was strongly affected by the Ca2+ ions, showing a significant dependence on the Ca2+ concentration. But from the chiral water vibrational signals, as shown in Panels B and D of Figure 4, within the limit of the experimental error, no obvious change was observed in terms of the Ca2+ concentration. The chiral spine of the water layer binding to the duplex oligonucleotide, however, only showed an intensity fluctuation within the Ca2+ concentration range from 0.6 mM to 6 mM. Hence, it can be claimed, based on the current SFG experiment, the hydration layer surrounding the model duplex oligonucleotide can resist the electrostatic interaction from the Ca2+ ions in the normal biological condition. It is very intriguing to find the resistant property against the Ca2+ ions for the chiral water layer surrounding the duplex oligonucleotide. But before the further discussion, it is necessary to know the detailed DNA molecular structure first. Previous reports have shown that, for the B-DNA, the minor groove width is ~5.7 Å and the major groove width is ~11.7 Å.9,16,39,40 The water molecules can be accommodated inside both the minor and major grooves surrounding the DNA


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chiral contour. However, the X-ray crystallography experiment showed that there exists the structural water in the minor groove rather than in the major groove.9-12 A stable layer of the structural water in the minor groove should be associated with the following two-fold reasons. First, the negative charged minor groove can attract the vicinal water molecules, which can form an ordered arrangement surrounding the DNA’s chiral spine. The other is the spatial confinement effect. The size of a water molecule is ~3.2 Å, which is well suitable for the inner space of the minor groove as an order-of-magnitude estimation. Indeed, based on the molecular dynamics simulation,13-15 the water molecules inside the minor groove show a much slower dynamic behavior in comparison to those in the major groove. Therefore, a water layer with the chiral superstructure in the minor groove should exist, which serves as a protective solvation shell against the Ca2+ ions in the normal biological conditions. CONCLUSIONS In this study, by using the lipid bilayer as a soft substrate to accommodate the duplex oligonucleotide, the achiral and chiral interfacial water spectra were collected in terms of the Ca2+ concentration. Over the concentration range from 0.006 mM to 60 mM, both achiral and chiral vibrational signals showed the concentration-dependent variations, indicating the Ca2+ ions can affect the interfacial water molecular structures at the duplex oligonucleotide/water and the lipid/water interfaces. However, when the Ca2+ concentrations were adjusted in the range similar to the biological conditions (0.6 mM to 6 mM), the chiral water vibrational signals did not show any obvious change while the achiral water vibrational signals showed an obvious concentrationdependent change. In consequence, it can be argued that the chiral water layer in the minor groove offers a protective solvation shell against the Ca2+ interaction for the duplex oligonucleotide, leading to the chiral water vibrational signals more or less inert to the change of


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the Ca2+ concentration in the normal biological conditions. In the future, metal ions other than the Ca2+ ions will be investigated and reported, including Mg2+, Na2+ and K+, etc. We hope that this chiral and achiral SFG investigation can stimulate more insightful studies on the water molecular structures surrounding DNA using nonlinear vibrational spectroscopy, which will advance our understanding on the relationship between the DNA and the water.

AUTHOR INFORMATION Corresponding Author *E-mails: [email protected] (X. L) Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. #These authors contributed equally. ACKNOWLEDGMENT This study was supported by the National State Key R&D Program of China (2017YFA0700500), the State Key Development Program for Basic Research of China (2016YFA0501600), the National Natural Science Foundation of China (Grant 21574020), the Fundamental Research Funds for the Central Universities, the project funded by the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions, and the National Demonstration Center for Experimental Biomedical Engineering Education (Southeast University). REFERENCES


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Calcium Ions Affect Water Molecular Structures Surrounding

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