RGD-conjugated silica-coated gold nanorods on the surface of carbon nanotubes for targeted photoacoustic imaging of gastric cancer
© Wang et al.; licensee Springer. 2014
Received: 3 April 2014
Accepted: 19 May 2014
Published: 27 May 2014
Herein, we reported for the first time that RGD-conjugated silica-coated gold nanorods on the surface of multiwalled carbon nanotubes were successfully used for targeted photoacoustic imaging of in vivo gastric cancer cells. A simple strategy was used to attach covalently silica-coated gold nanorods (sGNRs) onto the surface of multiwalled carbon nanotubes (MWNTs) to fabricate a hybrid nanostructure. The cross-linked reaction occurred through the combination of carboxyl groups on the MWNTs and the amino group on the surface of sGNRs modified with a silane coupling agent. RGD peptides were conjugated with the sGNR/MWNT nanostructure; resultant RGD-conjugated sGNR/MWNT probes were investigated for their influences on viability of MGC803 and GES-1 cells. The nude mice models loaded with gastric cancer cells were prepared, the RGD-conjugated sGNR/MWNT probes were injected into gastric cancer-bearing nude mice models via the tail vein, and the nude mice were observed by an optoacoustic imaging system. Results showed that RGD-conjugated sGNR/MWNT probes showed good water solubility and low cellular toxicity, could target in vivo gastric cancer cells, and obtained strong photoacoustic imaging in the nude model. RGD-conjugated sGNR/MWNT probes will own great potential in applications such as targeted photoacoustic imaging and photothermal therapy in the near future.
KeywordsRGD peptide Gold nanorods Multiwalled carbon nanotubes Optoacoustic imaging Gastric cancer Nude mice
Gastric cancer is the second most common cancer and the third leading cause of cancer-related death in China[1–3]. It remains very difficult to cure effectively, primarily because most patients present with advanced diseases. Therefore, how to recognize and track or kill early gastric cancer cells is a great challenge for early diagnosis and therapy of patients with gastric cancer.
We have tried to establish an early gastric cancer pre-warning and diagnosis system since 2005[5, 6]. We hoped to find early gastric cancer cells in vivo by multimode targeted imaging and serum biomarker detection techniques[7–12]. Our previous studies showed that subcutaneous and in situ gastric cancer tissues with 5 mm in diameter could be recognized and treated by using multifunctional nanoprobes such as BRCAA1-conjugated fluorescent magnetic nanoparticles, her2 antibody-conjugated RNase-A-associated CdTe quantum dots, folic acid-conjugated upper conversion nanoparticles[15, 16], RGD-conjugated gold nanorods, ce6-conjugated carbon dots, and ce6-conjugated Au nanoclusters (Au NCs)[19, 20]. However, clinical translation of these prepared nanoprobes still poses a great challenge. Development of safe and highly effective nanoprobes for targeted imaging and simultaneous therapy of in vivo early gastric cancer cells has become our concern.
Carbon nanotubes (CNTs) have been intensively investigated due to their unique electrical, mechanical, optical, thermal, and chemical properties[21–26]. In the field of biomedical engineering, CNTs have shown promise as contrast agents for photoacoustic (PA) and photothermal imaging of tumors due to their strong near-infrared region (NIR) absorption and deep tissue penetration[27–29]. To date, single-walled carbon nanotubes (SWNTs) were fully investigated for photoacoustic imaging. For example, for cell imaging, Avti et al. adopted photoacoustic microscopy to detect, map, and quantify the trace amount of SWNTs in different histological tissue specimens. The results showed that noise-equivalent detection sensitivity was as low as about 7 pg. For in vivo PA imaging, Wu et al. adopted RGD-conjugated SWNTs as a PA contrast agent, and strong PA signals could be observed from the tumor in the SWNT-RGD-injected group. With the aim of enhancing the sensitivity of the PA signal of SWNTs, Kim et al. developed one kind of gold nanoparticle-coated SWNT by depositing a thin layer of gold nanoparticles around the SWNTs for photoacoustic imaging in vivo and obtained enhanced NIR PA imaging contrast (approximately 102-fold)[33–35]. However, to date, few reports are closely associated with the use of multiwalled carbon nanotubes (MWNTs) as a PA contrast agent. Therefore, it is very necessary to investigate the feasibility and effects of the use of MWNTs and gold nanorod-coated MWNTs as PA contrast agents. In addition, CNT-based in vivo applications have to consider their toxicity. How to decrease or eliminate their cytotoxicity has become a great challenge. How to develop one kind of safe and effective NIR absorption enhancer MWNT has become our concern.
Gold nanorods (GNRs), because of their small size, strong light-enhanced absorption in the NIR, and plasmon resonance-enhanced properties, have become attractive noble nanomaterials for their potential in applications such as photothermal therapy, biosensing, PA imaging, and gene delivery for cancer treatment. However, the toxicity derived from a large amount of the surfactant cetyltrimethylammonium bromide (CTAB) during GNR synthesis severely limits their biomedical applications. Therefore, removal of CTAB molecules on the surface of GNRs is an important step to avoid irreversible aggregation of GNRs and enhance their biocompatibility. In our previous work, we used a dendrimer to replace the CTAB on the surface of GNRs, markedly decreasing the toxicity of GNRs, and realized the targeted imaging and photothermal therapy. We also used folic acid-conjugated silica-modified GNRs to realize X-ray/CT imaging-guided dual-mode radiation and photothermal therapy. Silica-modified GNRs can markedly enhance the biocompatibility of GNRs[42–44].
In recent years, molecular imaging has made great advancement. Especially, the system molecular imaging concept has emerged, which can exhibit the complexity, diversity, and in vivo biological behavior and the development and progress of disease in an organism qualitatively and quantitatively at a system level. Finally, system molecular imaging can enable the physicians to not only diagnose tumors accurately but also provide ‘on-the-spot’ treatment efficiently. In recent years, photoacoustic imaging, as an emerging imaging mode, has become a hotspot. We also synthesized gold nanoprisms and observed that gold nanoprisms could amplify the PA signal for in vivo bioimaging of gastrointestinal cancers. However, how to obtain clear PA imaging of in vivo tumors and PA imaging-directed therapy to service clinical theranostics has become a great challenge.
All animal experiments (no. SYXK2007-0025) were approved by the Institutional Animal Care and Use Committee of Shanghai Jiao Tong University.
Multiwalled carbon nanotubes (MWNTs) were purchased from the Shenzhen Nanoport Company (Shenzhen, China), and their diameters were around 20 ~ 30 nm. Chloroauric acid (HAuCl4 · 3H2O), cetyltrimethylammonium bromide (CTAB), sodium borohydride (NaBH4), tetraethylorthosilicate (TEOS), 3-aminopropyltrimethoxysilane (APTS), 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide (EDC), N-hydroxysuccinimide (NHS), and ascorbic acid were obtained from Aldrich Company (Wyoming, IL, USA). Anhydrous ethanol and ammonium hydroxide were obtained from Sinopharm Co. (Beijing, China). RGD peptides were from Aldrich Company.
Preparation of MWNT-COOH from MWNT
Crude MWNTs (0.523 g) were added to aqueous HNO3 (20.0 mL, 60%) (Figure 1). The mixture was placed in an ultrasonic bath (40 kHz) for 40 min and then stirred for 48 h while being boiled under reflux. The mixture was then vacuum-filtered through a 0.22-mm Millipore polycarbonate membrane (Millipore Co., Billerica, MA, USA) and subsequently washed with distilled water until the pH of the filtrate was ca. 7. The filtered solid was dried under vacuum for 24 h at 70°C, yielding MWNT-COOH (0.524 g)[46, 47].
Synthesis of silica-modified gold nanorods
In a typical experiment, GNRs were synthesized according to the seed-mediated template-assisted protocol[11, 48]. Twenty milliliters of the GNR solution was centrifuged at 9,600 rpm for 15 min. The supernatant, containing mostly CTAB molecules, was removed and the solid (containing rods) was redispersed in 20 mL anhydrous ethanol adjusted to pH 10 with ammonia. After the system was sonicated for 30 min, TEOS of 4 mL (10 mM) was added to the above system and the entire system was stirred for 20 h. Next, 10 mL APTS was added to form a mixed solution and allowed to react at 80°C for 3 h. The resultant product was treated by high-speed centrifugal separation and washed with deionized water for several times, and then dried at 60°C for 3 h in a vacuum oven to obtain the sGNRs.
Fabrication of sGNR/MWNT nanohybrid
Covalent attachment of sGNRs to the MWNTs was performed using a modification of the standard EDC/NHS reaction[49, 50]. Carboxyl groups on the surface of MWNTs (5 mg) were activated by an EDC/NHS solution for 30 min. Following activation, 1 mg of sGNRs were added to form a mixed solution and allowed to react at room temperature for 6 h, and then RGD peptides were added into the mixed solution and continued to react at room temperature for 6 h. The resultant products were treated by high-speed centrifugal separation and washed with deionized water for three times, and then kept at 4°C for use.
Characterization of sGNR/MWNT nanohybrid
A JEOL JEM-2010 transmission electron microscope and a JEOL JEM-2100 F high-resolution transmission electron microscope (JEOL Ltd., Akishima, Tokyo, Japan) were used to confirm particle size and observe the interface and the binding site of sGNRs and MWNTs. UV-vis spectra were measured at 20°C with a Shimadzu UV-2450 UV-visible spectrophotometer (Shimadzu Corporation, Kyoto, Japan) equipped with a 10-mm quartz cell, where the light path length was 1 cm. The 200- to 1,000-nm wavelength region was scanned, since it includes the absorbance of the GNRs. The Fourier transform infrared (FTIR) spectra were recorded on a PerkinElmer Paragon-1000 FTIR spectrometer (PerkinElmer, Waltham, MA, USA). Zeta potential was measured with a Nicomp 380ZLS Zeta Potential/Particle Sizer (Nicomp, Santa Barbara, CA, USA).
Effects of RGD-GNR-MWNT nanoprobes on cell viability
Nanoprobes for in vitro targeted imaging of gastric cancer cells
Gastric cancer cell line MGC803 used as target cells and human gastric mucous GES-1 used as control cells were cultured and collected[12–15], and then were treated with 50 μg/mL of prepared nanoprobes and cultured in a humidified 5% CO2 balanced air incubator at 37°C for 4 h. Meanwhile, the MGC803 and GES-1 cells treated with the prepared probes were used as the control group. Afterward, the cells were rinsed with phosphate buffered saline (PBS) three times and then fixed with 2.5% glutaraldehyde solution for 30 min. For nuclear counterstaining, MGC803 cells were incubated with 1 mM Hoechst 33258 in PBS for 5 min. The cells were observed and imaged using a fluorescence microscope (Nikon TS100-F, Nikon Co., Tokyo, Japan).
Preparation of gastric cancer-bearing nude mice model
Pathogen-free athymic nude (nu/nu) BALB/c mice were housed in an accredited vivarium, maintained at 22°C ± 0.5°C with a 12-h light/dark cycle and were allowed to access food and water. Male athymic nude mice (4 to 6 weeks old) were used to establish subcutaneous gastric cancer models; 2 × 106 MGC803 cells suspended in 100 μL of pure DMEM were subcutaneously injected into the right anterior flank area of each mouse. Four weeks later, tumors were observed to grow to approximately 5 mm in diameter.
RGD-conjugated sGNR/MWNT nanoprobes for photoacoustic imaging
Photoacoustic imaging of the study in vitro and in vivo was accomplished by a PA system (Endra Nexus 128, Endra Life Sciences, Ann Arbor, MI, USA). The excitation laser (Opotek, Carlsbad, CA, USA) is irradiated from the bottom of a hemispherical bowl, whose wavelength is tunable from 680 to 950 nm. PA characteristics of prepared nanoprobes in vitro were firstly investigated before in vivo imaging. PA intensity corresponding to different concentrations and wavelengths were studied by setting the probe in the tube. Subsequently, gastric cancer-bearing nude mice were treated with 500 μg of prepared nanoprobes. Animal orientation and tumor position should be kept constant in the bowl during experiments to make sure that each scan was in the same position in favor of comparison and imaging alignment. Filling the slot with distilled water provided acoustic coupling with the animal. Then, pre-injection scans and post-injection scans were both acquired when the tumor site was irradiated by the laser. The PA signals, which were received by the ultrasonic transducers, were spirally distributed on the surface of the bowl and then directed to a computer. Reconstruction of the 2D and 3D PA image was performed using Osirix imaging software (OsiriX Foundation, Geneva, Switzerland).
Results and discussion
Preparation and characterization of sGNR/MWNT hybrid
Binding sites of sGNRs and MWNTs
UV-vis spectra of gold nanorods
FTIR spectroscopy of RGD-conjugated GNR/MWNT nanoprobes
Effects of RGD-GNR-MWNT on cell viability
RGD-GNR-MWNT nanoprobes for in vitro cell targeted imaging
RGD-GNR-MWNT nanoprobes for in vivo photoacoustic imaging
In summary, we for the first time designed and prepared RGD-conjugated MWNT/sGNR nanoprobes, demonstrated that GNRs can enhance the PA signal of multiwalled carbon nanotubes and that RGD-conjugated MWNT/sGNR nanoprobes have good biocompatibility and can be used to target in vivo tumor vessels, and realized enhanced MWNTs' PA imaging of tumor vessels. Our results also confirm that MWNTs may be good PA imaging contrast agents. Although prepared RGD-conjugated MWNT/sGNR nanoprobes' distribution and metabolism are not clarified well, the novel hybrid nanostructure should open up new possibilities in nanomedicine as a multimodal photoacoustic and photothermal contrast agent, and will have great potential applications in advanced sensing, photoacoustic imaging, and photothermal therapy in the near future.
This work is supported by the National Key Basic Research Program (973 Project) (No. 2011CB933100), National Natural Scientific Fund (Nos. 81225010, 81327002, and 31100717), 863 project of China (2012AA022703), Shanghai Science and Technology Fund (Nos. 13NM1401500 and 11 nm0504200), and Shanghai Jiao Tong University Innovation Fund for Postgraduates (No. AE340011).
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