Photo-thermal effects in gold nanorods/DNA complexes
© De Sio et al. 2015
Received: 21 July 2015
Accepted: 29 September 2015
Published: 12 October 2015
An ingenious combination of plasmonic nanomaterials and one of the most relevant biological systems, deoxyribonucleic acid (DNA) is achieved by bioconjugating gold nanorods (GNRs) with DNA via electrostatic interaction between positively charged GNRs and negatively charged short DNA. The obtained system is investigated as a function of DNA concentration by means of gel electrophoresis, zeta-potential, DNA melting and morphological analysis. It turns out that the obtained bioconjugated systems present both effective electric charge and aggregate size that are particularly amenable for gene therapy and nanomedicine applications. Finally, the effect of the localized (photo-thermal heating) and delocalized temperature variation on the DNA melting by performing both light induced bio-transparent optical heating experiments and a thermographic analysis is investigated, demonstrating that the developed system can be exploited for monitoring nanoscale temperature variation under optical illumination with very high sensitivity.
Gene therapy (GT) has the potential to treat serious human diseases by providing patients with functioning replacements for defective genes or with oligonucleotides that deactivate destructive gene products . GT holds promise for treating a wide range of diseases including cancer, cystic fibrosis, heart disease, diabetes, hemophilia and AIDS. The future use of this type of therapy for clinical applications deals with the manufacturing of appropriate gene delivery vehicles (vectors) with the following capabilities: (1) selective transport of appropriate genes (oligonucleotides) to the diseased tissues; (2) protection of oligonucleotides from physiological degradation (e.g., pH change) while en route; presence of an external trigger mechanisms for gene release after the target site is reached. To date the most effective means of GT is based on viral vectors; a tool commonly used by molecular biologists to deliver genetic material into cells . However, viral vectors exhibit some intrinsic drawbacks such as: (1) they can carry only a limited amount of genetic material; (2) they can cause immune responses in patients; (3) the immune system may block the virus from delivering the gene to the patient’s cells. Biocompatible gold nanoparticles (GNPs) have gained considerable attention in recent years for potential applications in medicine due to their size dependent electronic, optical and chemical properties . GNPs possess the capability to localize light down to the nanoscale: visible electromagnetic radiation induces an oscillation of the free electrons localized at the metal (NPs)/dielectric (surrounding medium) interface. This phenomenon, called localized plasmon resonance (LPR), can be controlled in frequency by varying both the size and the shape of the nanoparticles and the dielectric constant of the surrounding medium . Plasmonic NPs have also the extraordinary capability to convert external light to heat, as the strong electric field generated around the NPs due to the LPR effect is transformed resulting in nanosized sources of heat . The ability of GNPs to interact with and enter cells has encouraged researchers to attach them various compounds and biological macromolecules [6–8] to gold in an effort to combine functionality with transport. In particular, GNPs possess a relevant potential as vehicles for gene delivery due to their low cytotoxicity when prepared in suitable size and coated with appropriate ligands. Several strategies have been proposed to bind biological molecules to GNPs . Among the various approaches, use of electrostatic interactions between GNPs and biological molecules offers one of the most viable functionalization route to obtain stable GNP bioconjugates. The convenient assembly of GNPs with suitable biosystems requires that the NP optical activity falls in the first (700–900 nm) or the second (1000–1400 nm) optical window of the NIR region of the electromagnetic spectrum, where the light attenuation by the absorption and scattering from the main tissue constituents (water, lipid, haemoglobin, melanin) is significantly reduced, thus allowing to penetrate biological systems very deeply, down to millimetres and even centimetres scale . Gold nanorods (GNRs) represent an attractive class of GNPs as due to their plasmon absorption sensitivity to the refractive index of the surrounding material, allow for an extremely accurate sensing and make them excellent candidates for biological sensing applications . In addition, GNRs present two distinct LPR, namely transversal and longitudinal ones, which can be tuned up to near-infrared (NIR), thus ensuring their activity in the biological window. Such NIR absorption peaks can be excited by a laser at specific absorption wavelength to induce a local heating, potentially able to selective destroy, via an hyperthermal process, cancerous tissues [12, 13]. Remarkably, the photoinduced thermal effect can be extremely effective in GT procedures, enabling the controlled release of therapeutic oligonucleotides from GNPs . In this paper, a comprehensive study of the electrostatic interaction between an aqueous solution of positively charged GNRs dispersed in a negatively charged short chain DNA solution is reported. A detailed investigation of the characteristics of the obtained bioconjugated has been performed as a function of GNRs concentration based on zeta-potential, gel electrophoresis, dynamic light scattering and morphological analysis. Remarkably, the effect of the localized photo-thermal heating and delocalized temperature variation on the DNA melting in the prepared bioconjugated has been demonstrated. Compared to previously employed techniques [15–17], the proposed non-invasive methodology enables to continuously monitoring photoinduced temperature variations around GNRs with high sensitivity.
General protocol for seed-mediated synthesis of GNRs and their characterization
Cetyltrimethylammonium bromide (CTAB) capped, water dispersible GNRs were synthesized by slight modifying the “seed-mediated growth method” . All glassware used in the following procedures were cleaned in a bath of freshly prepared 3:1 HCl/HNO3 and rinsed thoroughly in H2O prior to use. The synthesis was based on a two steps procedure. Firstly, 10 mL of “seed” solution was prepared by mixing CTAB (1 mmol) and HAuCl4∙3H2O (2.5 × 10−3 mmol) at room temperature. Then, 0.6 mL of ice–cold aqueous solution of NaBH4 (0.01 M) were added under vigorous stirring. Upon solution colour turned from greenish-yellow to brown, the mixture was further vigorously stirred for 2 h before utilizing it. In second step, 500 mL of water dispersed CTAB-stabilized GNRs (5.6 × 10−10 M) were grown by dissolving AgNO3, 18.22 g of CTAB and 100 mg of HAuCl4∙3H2O. Such mixture was kept at room temperature under continuous stirring. After 3 min, aqueous solution of ascorbic acid (AA) was drop-wise added to the above described mixture in [AA]/[Au] = 2 molar ratio. The resulting solution was kept under stirring until it became colourless [indicative for reduction of Au(III) to Au(I)] [19, 20]. At this point, 0.8 mL of seed solution were added to the growth solution and the resulting mixture was stirred. A brown colour developed in about 30 min. After preparation, GNRs solution was purified from uncoordinated CTAB by means of repeated centrifugation cycles.
Macro and micro-electrophoresis experiments
Figure 2a (second well on the right) shows that the GNRs dispersion was not affected by the electrophoretic run since GNRs are positively charged due to the presence of the CTAB bilayer. Indeed, GNRs do not exhibit any visible fluorescence band in the well, even in presence of the fluorescent tag (EtBr). The intense fluorescence of EtBr after binding with DNA is probably due to the hydrophobic environment found between the base pairs. By moving into such a hydrophobic environment and away from the solvent (water in our case), the ethidium cation is forced to shed any water molecules that was associated with it. As water is a highly efficient fluorescent quencher, only the removal of water molecules allows the ethidium to fluoresce. On the contrary, no binding event can be thought to occur between GNRs and EtBr and therefore the water based GNRs dispersion represent an effective hydrophobic environment able to induce a strong quenching of the ethidium fluorescence. By increasing the DNA concentration (W2 ≤ W ≤ W4) the solution shows a remarkable fluorescence very close to the well, pointing out an inhibited migration toward the positive electrode. Such an evidence can be accounted for by the presence of the CTAB bilayer, which makes GNRs positively charged, and thus able to electrostatically interact with the DNA molecules, without affecting their average length, however changing the effective charge of the whole system. A further increasing in the DNA concentration (W5 ≤ W ≤ W8) results in fluorescent bands broader. This evidence can be reasonably explained by thinking that, under these conditions, electrostatic interaction between GNRs and DNA exhibits a saturation and therefore all the non-conjugated DNA molecules or even the over conjugated DNA/GNRs complexes (means complexes with an effective negative electric charge) are free to run towards the positive electrode. Therefore the detected broad are likely due to at the presence of GNRs/DNA complexes with different size and charge (ranging from non-conjugated DNA to over conjugated GNRs/DNA complexes). It is worth mentioning that we have focused our study on the electrostatic interaction between GNRs and DNA (ranging from 500 to 1000 bp). As a matter of fact, it has been reported that the physical–chemical properties of cationic surfactant/DNA complexes are slightly affected by DNA size, while their ability to deliver DNA does [26, 27]. Recent results  have demonstrated that delivered DNA facilitated by cationic nanocarriers aggregates to a large extent within the cell, and aggregation is influenced by a number of factors including the location, the environmental conditions, and the DNA size itself. In particular, the smaller DNA sizes exhibited greater aggregation than the larger. Thus, we suggest that DNA size could have a minor effect, if any, on the physical–chemical characterization herein reported, while it could affect intracellular DNA photothermal release and aggregation. This is a key issue that will be addressed in future investigations.
In order to study the effective electric charge of the system, electrophoretic mobility experiments were carried out by means of a laser Doppler electrophoresis technique (Malvern-NanoZetaSizer) . The mobility u was converted into the zeta-potential using the Smoluchowski relation: zeta-potential = uη/ε, where ε is the permittivity of the solvent phase while η is the solvent viscosity. Zeta-potential measurements were performed in triplicate and results are reported as average value ± standard deviation in Fig. 2b. This experiment, realized by measuring the effective electric charge of the system (zeta potential) without adding the EtBr, shows that by increasing the DNA concentration (decreasing W, Fig. 2b) the zeta potential decreases. In particular for W = 2 × 10−7, GNRs/DNA complexes also undergo through a charge inversion effect differentiating negatively and positively charged aggregates. Indeed, this behavior, very similar to the one reported in Fig. 2a (electrophoresis analysis), highlights that the low concentration of EtBr does not affect the overall electric charge of the GNRs/DNA mixtures. As described in details in the Additional file 1 and confirmed by the environmental scanning electron microscope (ESEM) analysis reported in the inset of Fig. 2b for W < 10−6 the GNRs/DNA complexes are quasi-spherical clusters (region I), while for W > 10−6 their shape is elliptical like (region II). As a result, the GNRs/DNA complexes in region II are simultaneously positively charged and small in size (see Additional file 1). These relevant features make the system a good candidate for drug delivery and GT applications. To this end, it is important to say that the electrostatic interactions are modified in a physiological environment, where ionic strength acts to modify the complex overcharging. Physiological saline solutions have a destabilizing effect on the structure of GNRs/DNA complexes, either when they are prepared in these solutions or added to them after being prepared in low ionic strength solutions [30, 31]. The presence of salt during complex formation induces a smaller complexation efficiency for each given charge ratio. High salt concentration weakens the association between GNRs and DNA in preformed complexes, with the occurrence of some dissociation.
UV spectroscopy characterization
The effect of the GNRs/DNA conjugation on the overall DNA stability was investigated by performing a thorough spectral characterization of the system and by monitoring the absorption spectrum of the DNA solution, GNRs dispersion and GNRs/DNA complexes as a function of temperature. Absorbance versus temperature profiles were obtained (by means of a computer-interfaced Jasco V-630 spectrophotometer equipped with a thermoelectrically controlled cell holder) by monitoring (at λ = 260 nm) the intensity of the absorption while heating up (3 °C/min) the samples (DNA solution, GNRs dispersion and GNRs/DNA complexes). The melting temperature (T m ) for each transition was obtained from the optical melting curves by using a previously described procedure . One of the most commonly used and simplest techniques for the DNA melting point determination is spectroscopic analysis by UV absorption. The absorption spectrum is recorded against the dependence of the temperature where the turning point of the graph describes the exact temperature (T m ) at which half of helix structure is lost. In the actual case, the intensity absorption was monitored at λ = 260 nm since the DNA solution exhibits a well-known sharp maximum at 260 nm due to the absorption of the subunits of nucleic acids (purines and pyrimidines)  while the GNRs dispersion does not show any absorbance peak at 260 nm and moreover their overall absorbance does not change with temperature (data not reported). Indeed, high temperature causes DNA to melt due to breaking of hydrogen bonds connecting the bases and, consequently, the absorbance at 260 nm rises (this effect being known as a hyperchromic effect).
Plasmonic photo-thermal heating
This result shows that it is possible to measure the average temperature around GNRs at a given illumination time with a sensitivity of about 0.06 °C by simply monitoring the intensity of the absorption peak at 260 nm. Remarkably the presented method offer an original tool to monitor nanoscale temperature variation in a biocompatible environment by exploiting the DNA melting process. In order to visualize the difference between localized (confined to the illuminated area) and delocalized (uniform) temperature variation, the temperature of the GNRs/DNA solution was measured by heating up the quartz cuvette with a hot plate, the investigated area is marked with a white circle in Fig. 6. As a result (Fig. 6c–f), the heating transfer from the plate to the cuvette results in a quite uniform temperature distribution along the surface of the cuvette, clearly pointing out the difference between localized (generated by light) and delocalized (generated by a hot plate) temperature variation. This “visual comparison” based on a thermographic analysis is a proof-of-concept that in case of in vivo applications (e.g., GT or photo-thermal therapy) only the illuminated area is photo-heated (e.g., cancer cells) while the surrounding medium is not affected (e.g., healthy cells). Conversely, in case of heat generated through magnetic therapy (delocalized heat) the whole sample area is affected by the treatment (e.g., both cancer and healthy cells). Moreover, the localized heat can be used for photothermal release of DNA from GNRs for GT applications. It is worth mentioning that the reported method has been investigated in a temperature range between 72 and 85 °C (or irradiation time between 19 and 30 s) in order to study the photo-induced melting properties of the DNA solution. However, the same approach can be extended to other, lower, temperature range (e.g., 25–72 °C), by using a different calibration curve since the full melting diagram of a DNA solution exhibits a sigmoidal behavior, due to superimposition of two linear calibration curves (see Fig. 3). Above 85 °C, since all the double-stranded DNA unwinds and separates into single-stranded DNA, the melting curve exhibits a saturation region (see Fig. 3). For this reason, there is no physical meaning for studying the photo-thermal properties of the DNA/GNRs solution beyond 30 s.
A detailed study has been reported on the electrostatic interaction between a GNRs dispersion and a DNA solution. Both effective electrostatic charge and average size/shape can be easily controlled by carefully selecting the suitable GNRs/DNA molar ratio. In particular, the GNRs/DNA complexes also undergo through a charge inversion effect, finally differentiating negatively and positively charged conjugates. These distinctive features make them promising candidates for drug delivery and GT applications both in vitro and in vivo . Photo-heating experiments realized through a bio-transparent optical radiation (λ = 800 nm) demonstrated that the system represent an accurate temperature sensor able to monitor heating variation trough the DNA melting (at λ = 260 nm) with a sensitivity of about 0.06 °C. The overall results allow a deeper fundamental understanding of the interaction between charged plasmonic and biological materials  and, at the same time, open-up the venue for realizing a new generation of tools for nanomedicine.
LD, GC, RB conceived the photo-thermal strategy in GNRs/DNA complexes. LD performed the photo-heating experiments, GC and DP performed the zeta-potential and DNA melting experiments, FA and AP realized the gel electrophoresis analysis, TP realized the synthesis of GNRs, RC performed the TEM analysis, MLC and AA supplied background of GNRs synthesis and optical characterization, RB supplied background of photo-thermal heating of GNRs and DNA characterization. LD, GC wrote the paper. All authors read and approved the final manuscript.
Authors are grateful to: Dr. Giovanni Desiderio for performing the ESEM analysis. The research is supported by the Air Force Office of Scientific Research (AFOSR), Air Force Research Laboratory (AFRL), U.S. Air Force, under grant FA9550-14-1-0050 (P.I. L. De Sio, EOARD 2014/2015) and the Materials and Manufacturing Directorate, AFRL; by 2011 - prot. 2010C4R8M8 and 2012 prot. 2012T9XHH7 PRIN Projects. Fundings have been generously provided to GC by the “Futuro in Ricerca 2008” program funded by the Italian Minister for University and Research (Grant No. RBFR08TLPO) and by the Istituto Italiano di Teconologia, Center for Life Nano Science@Sapienza.
The authors declare that they have no competing interests.
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