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Heyong Huang1, Yan Ding1, Jiahong Zhou1, Qiu Jiang2* and Yuying Feng1 *
1  Analysis and Testing Center, Nanjing Normal University,
   Key Lab of Biofunctional Materials of Jiangsu Province, Nanjing 210097, PRC
2  Department of Management Consultancy, Productivity Centre of Jiangsu Province,  
   Nanjing 210016, PRC
Corresponding author: Yuying Feng, Qiu Jiang
Tel. and Fax: +86-25-85898170
E-mail address:  HYPERLINK "mailto:yyfeng3@163.com," yyfeng3@163.com, jq200505@163.com
Abstract
This article presents the development and characterization of SiO2 nannoparticles loaded with methylene blue(SiO2-MB), which are designed to administered for photodynamic therapy(PDT). Induced by light irradiation, the entrapped MB generated 1O2, and the produced 1O2 was measured with anthracene-9,10-dipropionic acid. In comparison to the unmodified MB, the MB nanoparticles display lower singlet oxygen production but higher DNA photocleavage capability. Furthermore, in vitro experiments illustrated that SiO2-MB was efficiently taken up by tumor cells, and that light irradiation of such impregnated cells resulted in significant cell death. Thus, these properties of SiO2-MB could possibly make it especially promising foruse in clinical photodynamic therapy.

Keywords
Nanomaterials, Methylene blue, Silica dioxide, Photodynamic therapy

Introduction
    Photodynamic therapy (PDT) has emerged as a promising method for overcoming some of the inherent problems in classical cancer therapies [1 5]. It involves the selective delivery of photosensitizers (PS), such as Photofrin, to tumors. When excited with an appropriate wavelength of visible or near-infrared light, the PS produces singlet oxygen (1O2) and other reactive oxygen species, resulting in irreversible damage to tumor cells, with minimal systemic toxicity.
    An ideal photosensitizer should satisfy several criteria: chemical purity, tumor selectivity, minimal dark toxicity, rapid systemic clearance, high photochemical reactivity and activation at longer wavelengths[4]. Currently available photosensitizers only partially fulfill these criteria. Many new PDT agents have been investigated including chlorins and phthalocyanines, with favorable PDT properties. Methylene blue, a water-soluble phenothiazine derivative, has been used for a variety of clinical applications, including PDT[4,6]. Methylene blue is approved by the FDA for use in methemoglobinemia. The high quantum yield of 1O2 generation (�� <" 0.5)[7], coupled with relatively low dark toxicity, makes methylene blue an attractive candidate for PDT. However, clinical use of methylene blue for PDT has been limited because of lack of significant therapeutic efficacy following systemic administration. Methylene blue accumulates extensively in erythrocytes[8] and endothelial cells[9,10], where it is reduced to leucomethylene blue, resulting in the loss of photodynamic activity[11].Unfortunately, little investigation has been conducted using drug delivery carriers with MB (Chart 1), although there has been much effort focused on the synthesis or modification of MB [12-14].
    In recent years, nanoparticles have received increasing attention as a possible means of delivering PDT agents [15,16].The porous hollow silica nanoparticle (SN), a new drug carrier for photosensitive drugs, has been receiving quickly increased research attentions because of its water-solubility, high stability, immunity to microbial attack and compatibility with biological systems, which is obviously superior to conventional drug delivery systems. In addition, a pronounced advantage of this new type of carrier is that it will never release PS but allow active oxygen species to diffuse out through the micro-holes within the shell part of SNs. Therefore, this kind of carrier seems to meet the request for PDT very well.
    In this paper, MB encapsulated in silica nanoparticles have been successfully prepared through the sol-gel method. The photocleavage capability to DNA improved effectively. In addition, the singlet oxygen pruduction and PDT efficacy to cancer cell in vitor was discussed. 

Chart 1. Structures of methylene blue(MB).

2. Materials and methods
2.1  Reagents
    9,10-Anthracendipropionic acid, ethidium bromide (EB), dimethyl sulfoxide (DMSO), Methylene Blue (MB), tetraethylorthosilicate (TEOS), and calf thymus deoxyribonucleic acid (CT-DNA) were all purchased from Sigma Aldrich Corporation. Dulbecco s minimum essential medium (DMEM) was from Gibico. 3-(4,5-dimethylthiazol-2-yl)2,5-diphenyl tetrazolium bromide (MTT) was from Amosco.

2.2  Preparation and characterization of MBNP
    The sol gel silica nanoparticles were made via a modified method [17-19]. The typical reaction solution consists of 24 mL methanol, 6 mL ammonium hydroxide (30%wt of ammonia ) and 80�L MB solution (20 mg/mL). On mixing the solution by vigorous magnetic stirring, 0.2 mL TEOS was added dropwise to initiate the hydrolysis reaction. The resulting solution was stirred at room temperature for approximately 2 h before it was transferred to the Amicon ultrafiltration cell, where it was rinsed rigorously with distilled water and ethanol to ensure removal of all unreacted reactants. The particle suspension was finally passed through the suction filtration system with a 0.02�m filter membrane and dried to yield an end product of MBNP.
2.3  Characterization of MBSN
    Transmission electron microscopy (TEM) image was obtained on a JEM-1200EX a! electron microscopy with an acceleration voltage of 200 kV. A VARIAN CARY 5000 UV visible recording spectrophotometer was used for absorption measurements. Fluorescence spectra were measured by a Perkin-Elmer LS- 50B fluorometer with an excitation wavelength of 480 nm.
2.4  Singlet oxygen detection
    Singlet oxygen detection measurements were carried out in a plastic cuvette using the disodium salt of 9,10-anthracendipropionic acid (ADPA) as a singlet oxygen sensor [20]. In a typical experiment, an aqueous solution of ADPA (150 mL, 5.5 mmol) was mixed with MBNP (3 mL). The control experiment used ADPA mixed with aqueous solution of MB, which MBs been prepared by adding small amounts of concentrated DMSO solutions of MB to phospMBte buffer. These solutions were irradiated with a 500 W high-voltage mercury lamp with 470 nm cutoff filter. The optical densities at 378 nm (characteristic absorption peak of ADPA) were recorded every 2 min using VARIAN Cary 5000 UV vis spectrophotometer.
2.5  Photodegradation of CT DNA analysis
    To study the PDT properties of MBNP, the air-saturated buffer solution of CT DNA (8 mmol/L) (10 mmol/L ammonium acetate, 100 mmol/L sodium chloride, pH =7.0 containing ethidium bromide (16 mmol/L) was used as phototherapeutic target, after adding MBSN (MB) into the above solution, the mixture was irradiated with light above 470 nm, and the fluorescence spectrum of the mixture was recorded every 5 min.
2.6  Photodynamic effects with tumor cells in vitro
    For studying in vitro photodynamic efficiency, 96-well plates were inoculated with cells at 1�105 cells mL-1 density overnight. The medium was removed, the wells were rinsed with sterile PBS, and serum-free medium (100 mL) with MB or SiO2-MB was placed into each well. After incubation overnight, the cells were irradiated by light and the percentage of dead cells was evaluated by using the MTT assay.

3. Results and discussions
3.1. TEM imaging of MBNP
    A TEM image of SiO2-MB prepared by reprecipitation method is shown in Fig. 1. The particles are nearly ball-like, having uniform size distribution, with an average diameter of 25 nm.

Fig. 1 

3.2. Optical spectroscopy
    Between 550 nm and 800 nm, free MB has two characteristic absorbance bands, located at 664 nm and 600 nm respectively (Fig. 2). After MB was converted into SiO2-MB, the intensity of the two absorbance bands decreased. This phenomenon indicated that the surroundings of MB molecules has been changed, i.e., the MB molecules on the surface of nanoparticles can prevent the inner MB molecules from water molecules, and the inner MB molecules exist in the hydrophobic surroundings [21]. Furthermore, the absorption spectrum of two aqueous solutions of MB and SiO2-MB has shown a remarkable difference after lifting to stand for three days. The absorption intensity of two characteristic absorbance bands of SiO2-MB has no obvious change but that of the MB aqueous solution decreased in intensity. Thus, comparing the changes in the absorption spectrum, it can be determined that SiO2-MB has excellent stability in the aqueous solution. This could be due to negative surface charges on SiO2-MB.

Fig.2

3.3. Detection of singlet oxygen
    Singlet oxygen is believed to be one of the reactive intermediates in PDT. Consequently, the quantum yield of 1O2 is an important parameter to evaluate the application potential of the photosensitizer in PDT. Thus, the ADPA bleaching experiment was carried out to detect the 1O2 generation quantum yield of SiO2-MB and MB. If the absorption intensity of ADPA continuously decreased as the irradiated time increase, the generation of singlet oxygen is confirmed (Fig. 3 inset panel). Because 1O2 can react irreversibly with ADPA to produce the endoperoxide derivative of ADPA (Scheme 1), and the 1O2 generation quantum yield can be calculated through comparing the decrease of the absorption intensity of ADPA [22].
    ADPA bleaching experiments showed that the 1O2 generation efficiency of SiO2-MB is 0.58 (taking free MB as a reference) (Fig. 3). The result indicated that the singlet oxygen delivery is hindered by the embedding in this case. This difference in activity may be partially attributed to the microenvironments in the nanoparticles, in particular, the local sequestration of produced 1O2 by the matrice. Moreover, as mentioned in the previous section, MB forms dimers in nanoparticles, which do not absorb light at 650 nm to produce 1O2.

Fig. 3 

3.4. Photodegradation of CT-DNA analysis
    MB were investigated as a potential DNA cleavage agent. According to previous references, MB can abstract one electron from DNA upon irradiation, and thus induce damage and cleavage of DNA. One electron transfer from DNA to triplet MB will result in the formation of two reduced forms of MB, MB�� and MBH2, which are the precursors of superoxide anion radical (O2��) and hydroxyl radical (�OH). On the other hand, singlet oxygen (1O2) is formed via the energy transfer from triplet MB to molecular oxygen. These reactive oxygen species promote the cleavage of DNA [23].
When irradiation was carried out in the SiO2-MB EB CTDNA buffer aerobic solution with light above 470 nm, 47.2% binding sites can be destroyed during 25 min, while only 7.6% binding sites were damaged when free MB was used as the photosensitizer. These results suggest that the photocleavage ability of SiO2-MB is superior to free MB (Fig. 4).

Fig. 4
3.5  Photodynamic effects in vitro
    The in vitro results indicate a direct relationship between the dose of drug or light and the photosensitizing efficiency. The results showed that after irradiation, both SiO2-MB and MB can cause significant cell death, and such photodynamic activity is dependent on both drug dose (Fig.5 A) and light dose (Fig.5 B). Comparative studies with SiO2-MB and MB demonstrated that the photodynamic activity of SiO2-MB was higher than that of the MB under the same experimental conditions, which is possibly because of the difference in their 1O2 generation ability. The above results  indicated that encapsulation of MB in nanoparticles enhanced the tumor cell kill over the dose range studied.
Fig. 5A
Fig. 5B 
4. Conclusions
    In conclusion, SiO2-MB can be prepared through a simple method greatly improving the water solubility, stability and ability of singlet oxygen generation. Furthermore, the high 1O2 generation quantum yield of SiO2-MB results in a higher capability to photocleave DNA than free MB, and the in vitro photodynamic activity of SiO2-MB were much higher than those of MB under the same experimental conditions. The properties of SiO2-MB make it a likely prospect for application in the clinical therapy of PDT.

Acknowledgments
  This work was supported by the Natural Science Foundation of China (Grant
No.20603018) and Science Foundation of Jiangsu (Grant No. BM2007132), China. We gratefully acknowledge the anonymous reviewers whose comments helped to improve the manuscript.

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