Fluorescein-polyethyleneimine coated gadolinium oxide nanoparticles as T1 magnetic resonance imaging (MRI) cell labeling (CL) dual agents
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1 Kyungpook National University From the SelectedWorks of Dr. Md Wasi Ahmad 2012 Fluorescein-polyethyleneimine coated gadolinium oxide nanoparticles as T1 magnetic resonance imaging (MRI) cell labeling (CL) dual agents Wenlong Xu, Kyungpook National University Ja Young Park, Kyungpook National University Krishna Kattel, Kyungpook National University Md Wasi Ahmad, Kyungpook National University Badrul Alam Bony, Kyungpook National University, et al. Available at:
2 RSC Advances View Article Online / Journal Homepage / Table of Contents for this issue Dynamic Article Links Cite this: RSC Advances, 2012, 2, PAPER Fluorescein-polyethyleneimine coated gadolinium oxide nanoparticles as T 1 magnetic resonance imaging (MRI) cell labeling (CL) dual agents{ Wenlong Xu, a Ja Young Park, a Krishna Kattel, a Md. Wasi Ahmad, a Badrul Alam Bony, a Woo Choul Heo, a Seonguk Jin, b Jang Woo Park, b Yongmin Chang,* b Tae Jeong Kim, c Ji Ae Park, d Ji Yeon Do, e Kwon Seok Chae e and Gang Ho Lee* a Received 28th May 2012, Accepted 7th September 2012 DOI: /c2ra21052e We report the synthesis, characterization and application of highly water-soluble fluoresceinpolyethyleneimine (PEI) coated gadolinium oxide (Gd 2 O 3 ) nanoparticles to magnetic resonance imaging (MRI) and cell labeling (CL). The average particle diameter and average hydrodynamic diameter were estimated to be 3.92 and 7.5 nm, respectively. Fluorescein-PEI was prepared from EDC/NHS coupling method. The surface coating was characterized by the FT-IR absorption spectrum and the surface coating amount was estimated to be wt% from a TGA analysis, corresponding to 0.65 nm 22 grafting density. The fluorescein-pei coated gadolinium oxide nanoparticles showed r 1 and r 2 of 6.76 and s 21 mm 21, respectively, and a strong fluorescence at y527 nm. A pronounced positive contrast enhancement was clearly observed in 3 tesla T 1 MR images of a rat with a liver tumor after injection of an aqueous sample solution into a rat tail vein. After treatment of DU145 cells with a sample solution, a strong fluorescence in confocal images was also observed. These two results together confirm the excellent MRI-CL dual functionality of fluorescein-pei coated gadolinium oxide nanoparticles. Introduction Highly sensitive dual molecular imaging agents will play a vital role in diagnosing diseases in the near future because they can provide complementary information in analyzing diseases. 1,2 For example, a magnetic resonance imaging (MRI) agent combined with a cell labeling (CL) agent can be used in labeling cancer cells and acquiring high resolution spatial images around them. Cancer cells can then be analyzed after sampling out from the body. In this work, a highly sensitive gadolinium oxide a Department of Chemistry, College of Natural Sciences, Kyungpook National University, Taegu, , South Korea. ghlee@mail.knu.ac.kr; Fax: ; Tel: b Department of Molecular Medicine and Medical & Biological Engineering, School of Medicine, Kyungpook National University and Hospital, Taegu, , South Korea. ychang@knu.ac.kr c Department of Applied Chemistry, College of Engineering, Kyungpook National University, Taegu, , South Korea d Laboratory of Nuclear Medicine Research, Molecular Imaging Research Center, Korea Institute of Radiological Medical Science, Nowon-gil 75, Seoul, , South Korea e Department of Biology Education, Teachers College, Kyungpook National University, Taegu, , South Korea. kschae@knu.ac.kr { Electronic supplementary information (ESI) available: XRD patterns of both as-prepared and TGA analyzed powder samples of fluorescein- PEI coated gadolinium oxide nanoparticles, a HRTEM image of the TGA analyzed powder sample, and NMR spectra. See DOI: / c2ra21052e nanoparticle as a T 1 MRI contrast agent is combined with fluorescein as a CL agent. MRI is a very useful technique in diagnosing diseases because of its high spatial resolution and good sensitivity. 3 Detection of diseases can be further improved by using MRI contrast agents through contrast enhancement MRI can be also combined with a variety of other molecular imaging techniques such as X-ray computed tomography (CT), positron emission tomography (PET) and fluorescent imaging (FI). Therefore, development of dual imaging agents is very important. This work deals with fluorescein coated gadolinium oxide nanoparticles. They are promising candidates as either T 1 MRI- CL or MRI-FI dual agents because gadolinium oxide nanoparticles show a longitudinal relaxivity (r 1 ) which is much larger than those of Gd(III)-chelates while dyes generally provide a very strong fluorescent intensity. 27 The enhanced r 1 of gadolinium oxide nanoparticles with respect to those of Gd(III)- chelates is due to a high density of probing Gd(III) ions in nanoparticles. Various dyes had been combined with MRI contrast agents so far. For instance, Cy5.5-cross linked iron oxide (CLIO) nanoparticles in which Cy5.5 is a near-infrared emitter, has been applied to pre-operative MRI and intra-operative optical brain tumor delineation to determine tumor margins for surgery. 28 Fluorescent hydrid paramagnetic Gd 2 O 3 nanoparticles conjugated with FITC, RBITC and Cy5 have been also applied to in vivo MRI-FI dual imaging. 20 Fluorescein-loaded This journal is ß The Royal Society of Chemistry 2012 RSC Adv., 2012, 2,
3 PLGA nanoparticles with surface modification with monoclonal antibody have been applied to targeting and labeling cancer cells. 29 Note that for clinical applications, gadolinium oxide nanoparticles must be biocompatible and completely excreted from the body through the renal system to avoid any danger such as nephrogenic systemic fibrosis. 30 Therefore, nanoparticles should be well-coated with water-soluble and biocompatible ligands. In this work, fluorescein is conjugated to hydrophilic and biocompatible polyethyleneimine (PEI) (M n = y1200 amu) to improve both water-solubility and biocompatibility of fluorescein through the EDC/NHS coupling method. 31 Finally, fluorescein-pei was conjugated to gadolinium oxide nanoparticles. In this work, we demonstrated MRI-CL dual functionality of fluorescein-pei coated gadolinium oxide nanoparticles both in vivo and in vitro. We measured relaxivities and 3 tesla T 1 MR images of a rat with a liver tumor after injection of a sample solution into a rat tail vein. We took fluorescent confocal images of DU145 cells after incubating them with a sample solution. Experimental Synthesis GdCl 3?xH 2 O (99.9%), NaOH (.99.9%), H 2 O 2 (50% in water), triethylene glycol (99%), polyethylenimine (PEI) (50% in water, M n = y1200 amu), phosphate buffer solution (PBS) (ph = 7.2), HCl (.99%), N-hydroxysuccinimide (NHS) (98%), 1-ethyl-3 (3- dimethylaminopropyl) carbodiimide (EDC) (.97%), fluorescein (95%), D 2 O (100%) and dimethyl sulfoxide (DMSO-d 6 ) (99.96%) were used. These chemicals were purchased from Sigma-Aldrich and used as received. Sterile phosphate buffer saline solution, DMEM and RPMI1640 culture media were purchased from GIBCO BRL, USA. Triply distilled water was used throughout the experiments. A reaction scheme is presented in Fig. 1a. 2 mmol of GdCl 3?xH 2 O was added to 20 ml of triethylene glycol in a three-necked flask and magnetically stirred at 80 uc and under atmospheric condition until the precursor was completely dissolved in triethylene glycol. Then, 6 mmol of NaOH was added to the precursor solution and magnetic stirring continued for 2 h. Then, 3.5 ml of H 2 O 2 solution was added to the reaction solution which was then magnetically stirred for an additional 2 h. The product solution was cooled to room temperature and then transferred into a 1 L beaker containing 500 ml of triply distilled water. It was magnetically stirred for 30 min and stored for a week or so until nanoparticles settled down to the beaker bottom. The top transparent solution was decanted and the remaining product solution was again washed with triply distilled water. This procedure was repeated three times. Fluorescein-PEI was synthesized by using the EDC/NHS coupling method. 31 A reaction scheme for this process is shown in Fig. 1b. Briefly, 2 mmol of EDC and 2 mmol of NHS were added to 20 ml of PBS (ph = 6) at room temperature and under atmospheric condition. Here, a ph = 6 of PBS was obtained by slowly adding 1 mm HCl dropwise to the original PBS with ph = 7.2. After magnetic stirring for 15 min, 0.1 mmol of fluorescein was added to the solution and then the solution was magnetically stirred for 2 h. Then, 1.2 ml of PEI solution was added to the above solution with magnetic stirring for an additional 2 h to obtain fluorescein-pei. Here, the fluorescein-pei structure given in Fig. 1b is arbitrary (i.e., one of a possible number of structures) because fluorescein can form amide bonds with any of the amine groups in PEI. As shown in Fig. 1b, gadolinium oxide nanoparticles were added to the above fluorescein-pei solution. Here, it is known that the amine group can tightly bind to a nanoparticle This can occur through donation of a pair of non-bonding electrons of a nitrogen atom to an empty orbital of a metal ion on a nanoparticle surface. Since there are many amine groups in a PEI, any of them can contribute to the bonding; the bonding structure shown in Fig. 1b is just one of possible ones. The Fig. 1 Reaction schemes for the syntheses of (a) gadolinium oxide nanoparticles and (b) fluorescein-pei and fluorescein-pei coated gadolinium oxide nanoparticles. Here, the above fluorescein-pei structure is only one of the possible structures because fluorescein can form amide bonds with any of the amine groups in PEI RSC Adv., 2012, 2, This journal is ß The Royal Society of Chemistry 2012
4 reaction mixture was magnetically stirred for 16 h, the product solution was transferred into a 1 L beaker containing 500 ml of triply distilled water, and then washed with triply distilled water three times by using the same procedure used in washing the gadolinium oxide nanoparticles. Half the volume of the sample was converted to a powder by drying it in air and the remaining half was diluted with triply distilled water to prepare sample solutions for both MRI and CL experiments. Characterization A nuclear magnetic resonance (NMR) spectrometer (Bruker, AVANCE digital 400) was used to confirm the synthesis of fluorescein-pei. After the reaction was complete, the solvent was removed under vacuum to dryness. The residue was washed by ethanol and then dissolved in D 2 O for measurement. A high resolution transmission electron microscope (HRTEM) (JEOL, JEM 2100F, 200 kv acceleration voltage) was used to measure the particle diameter (d) of fluorescein-pei coated gadolinium oxide nanoparticles. A copper grid (PELCO No. 160, TED PELLA, INC.) covered with an amorphous carbon membrane was placed onto a filter paper and then, a surface coated nanoparticle solution diluted in triply distilled water was dropped over the copper grid by using a micropipette (Eppendorf, 2 20 ml). A dynamic light scattering (DLS) particle size analyzer (UPA-150, Microtrac) was used to measure the hydrodynamic diameter (a) of the surface coated nanoparticles dispersed in triply distilled water. To measure this, an aqueous mm Gd sample solution was used. An X-ray diffraction (XRD) spectrometer (Philips, X PERT PRO MRD) with unfiltered Cu-Ka radiation (l = Å) was used to measure the crystal structure of fluorescein-pei coated gadolinium oxide nanoparticles. The scanning step and the scan range in 2h were 0.033u and u, respectively. An inductively coupled plasma atomic emission spectrometer (ICPAES) (Thermo Jarrell Ash Co., IRIS/AP) was used to measure the Gd concentration in a sample solution. A Fourier transform-infrared (FT-IR) absorption spectrometer (Mattson Instruments, Inc., Galaxy 7020A) was used to verify the surface coating of the nanoparticles. Before measuring a FT-IR absorption spectrum, a powder sample was dried on a hot plate at 50 uc in a hood for a week or so to minimize the water content. To record a FT-IR absorption spectrum ( cm 21 ) a pellet of a powder sample in KBr was prepared. A thermogravimetric analyzer (TGA) (TA Instruments, SDT-Q 600) was used to estimate the amount of surface coated fluorescein-pei from the mass loss in the TGA curve. TGA curves of powder samples were recorded between room temperature and 900 uc under an air flow. A superconducting quantum interference device (SQUID) magnetometer (Quantum Design, MPMS-7) was used to measure the magnetic properties of fluorescein-pei coated gadolinium oxide nanoparticles. Both magnetization (M) vs. applied field (H) (i.e., M H) curves (25 H 5 tesla) at temperatures (T) = 5 and 300 K and zero-field-cooled (ZFC) M T curves (3 T 330 K) at H = 100 oersted (Oe) were recorded. In order to measure both M H and M T curves, a weighed powder sample was loaded into a non-magnetic gelatin capsule. A very small diamagnetic contribution from the capsule has a negligible contribution to the overall M, which is dominated by the sample. The observed M was mass-corrected by using both sample mass and weight percent of gadolinium oxide nanoparticles in the sample which was estimated from a TGA curve. A photoluminescence (PL) spectrometer (JASCO, FP-6500) was used to record PL spectra of both fluorescein-pei coated gadolinium oxide nanoparticles and pure fluorescein dispersed in triply distilled water at a high resolution mode. The excitation wavelength (l ex ) was 470 nm. A quartz cuvette with four optically clear sides (Sigma-Aldrich, 3 ml) was filled with a sample solution for measurement. Relaxivity measurement A 1.5 tesla MRI instrument (GE 1.5 T Signa Advantage, GE medical system) equipped with the knee coil (EXTREM) was used to measure both longitudinal (T 1 ) and transverse (T 2 ) relaxation times. A series of aqueous sample solutions with different concentrations (0.25, 0.125, and 0 mm Gd) were prepared by diluting an original sample solution with triply distilled water. The longitudinal (r 1 ) and transverse (r 2 ) water proton relaxivities were then estimated from the slopes in the plots of 1/T 1 (= R 1 ) and 1/T 2 (= R 2 ) vs. Gd concentration, respectively. The typical measurement parameters are as follows: external MR field (H) = 1.5 tesla, temperature (T) = 22 uc, number of acquisitions (NEX) = 1, field of view (FOV) = 16 cm, phase FOV = 1, matrix size = , slice thickness = 5 mm, spacing gap = 0, pixel bandwidth = , repetition time (TR) = 2009 ms, and time to echo (TE) = 9 ms. In vitro cytotoxicity test A CellTiter-Glo Luminescent Cell Viability Assay (Promega, WI, USA) was used to measure the cellular toxicity of an aqueous sample solution. In this assay, a luminometer (Victor 3, Perkin-Elmer) was used to quantify the intracellular ATP. Both human prostate cancer (DU145) and normal mouse hepatocyte (NCTC1469) cell lines were used as test cells. DMEM and RPMI1640 culture media were used for NCTC1469 and DU145 cells, respectively. Cells were seeded on a 24-well cell culture plate and incubated for 24 h ( cell density, 500 ml cells per well, 5% CO 2,37uC). A series of test sample solutions (0, 5, 10, 25 and 50 mm) were prepared by diluting an original sample solution with a sterile phosphate buffer saline solution; y2 mlof each test sample solution was treated into the cell culture media. The treated cell culture media were then incubated for 48 h. Each cell viability was measured and normalized with respect to that of the control cell line with 0.0 M Gd concentration. The measurement was repeated twice for each test solution to obtain the average cell viabilities. In vivo T 1 MR image measurement A 3 tesla MRI instrument (SIEMENS 3.0 T MAGNETOM Trio a Tim) was used to take in vivo T 1 MR images of a rat with a N1S1 liver tumor and with weight of y300 g. The rat was anesthetized by 1.5% isoflurane in oxygen. Measurements were made before and after injection of a sample solution into a rat tail vein. The injection dose was 0.1 mmol Gd kg 21. After measurement, the rat was revived from anesthesia and placed in a cage with a free access to both food and water. During measurement, the rat was maintained at y37 uc by using a This journal is ß The Royal Society of Chemistry 2012 RSC Adv., 2012, 2,
5 warm water blanket. The typical imaging parameters for T 1 3D fast SPGR (spoiled GRASS) images are as follows: H = 3 tesla, T =37uC, NEX = 3 4, FOV = 100 mm, phase FOV = 0.5, matrix size = , slice thickness = 1 2 mm, spacing gap = mm, pixel bandwidth = 15.63, TR = 11 ms, and TE = 3.2 ms. In vivo TEM analysis of accumulation of nanoparticles in a normal liver For in vivo TEM analysis of nanoparticles accumulated in a normal liver, an aqueous sample solution was injected into a rat tail vein and then the liver was taken out from the rat 36 h after injection by anesthetizing and killing the rat by means of exsanguination from the vena cava. Ultra-thin sections of liver cells were obtained by using a LKB ultramicrotome (RMC, MT- X) and these were then doubly stained with both uranyl acetate and lead citrate solution. After these, the sections were imaged with a TEM (Hitachi, H-7600) at an acceleration voltage of 100 kv. Fluorescent confocal cell image measurement A confocal laser scanning microscope (Carl Zeiss, LSM 700) equipped with a solid-state laser was used to record fluorescent confocal images of DU145 cells treated with a sample solution. The l ex and the laser power were 488 nm and y8 watts, respectively. The DU145 cells were seeded onto two 35 mm cell culture dishes at a density of with 2 ml volume per dish (5% CO 2,37uC). After 24 h, one of the above two cell dishes was treated with y50 ml of an aqueous sample solution and incubated for 4 h. The treated cells were washed twice with sterile phosphate buffer saline solution. The untreated cells in the other dish served as control cells. The cells in both dishes were fixed with 4% PFA (paraformaldehyde) in sterile phosphate buffer saline solution for 10 min at room temperature. After this, the cells in both dishes were washed three times with a sterile phosphate buffer saline solution. The cell nuclei in both dishes were then stained with DAPI (49,6-diamidino-2-phenylindole) for counterstaining and then, washed again three times with a sterile phosphate buffer saline solution. The cells were mounted by using Prolong Gold (Invitrogen, Carlsbad, CA, USA) for imaging. Results and discussion Particle diameter (d) and hydrodynamic diameter (a) of gadolinium oxide nanoparticles HRTEM images of fluorescein-pei coated gadolinium oxide nanoparticles are shown in Fig. 2a and b. The nanoparticles range from 2 to 6 nm. A log normal function fit to the observed particle diameter distribution provides an d avg of 3.92 nm (Fig. 2c). An average hydrodynamic diameter (a avg ) was estimated to be 7.5 nm from a DLS pattern of fluorescein-pei coated gadolinium oxide nanoparticles dispersed in triply distilled water (0.125 mm Gd) (Fig. 2d). We also measured XRD patterns of powder samples of both as-prepared and TGA analyzed fluorescein-pei coated gadolinium oxide nanoparticles (ESI{). The lattice constant estimated from the (222) peak of a TGA analyzed powder sample is consistent with that reported in PCPDFWIN. 35 Fig. 2 (a) and (b) HRTEM images, (c) a log normal function fit to the observed particle diameters, and (d) a DLS pattern of an aqueous solution of fluorescein-pei coated gadolinium oxide nanoparticles. Surface coating with fluorescein-pei Gadolinium oxide nanoparticles were coated with fluorescein- PEI to make them water-soluble and biocompatible as well as to label them with fluorescein. In order to prove the successful synthesis of fluorescein-pei, a 400 MHz NMR spectrum of fluorescein-pei was taken. In addition to this, NMR spectra of fluorescein, PEI, and a physical mixture of all reactants (i.e., PEI, fluorescein, EDC, NHS and PBS solution) were also taken for comparison. These NMR spectra clearly confirmed the successful synthesis of fluorescein-pei (ESI{). As mentioned before, any amine groups in a PEI can be conjugated to a nanoparticle In order to confirm the presence of a surface coating, the FT-IR absorption spectrum of a powder sample of fluorescein-pei coated gadolinium oxide nanoparticles was recorded. FT-IR spectra of both fluorescein and PEI were also taken as reference spectra (Fig. 3a). Here, water was completely removed from PEI by heating a 50% PEI aqueous solution at 70 uc for a week or so. From comparison of FT-IR absorption spectrum of the powder sample with those of both fluorescein and PEI, it is clear that gadolinium oxide nanoparticles are Fig. 3 (a) FT-IR absorption spectra of PEI, fluorescein and a sample powder of fluorescein-pei coated gadolinium oxide nanoparticles and (b) a TGA curve of a sample powder of fluorescein-pei coated gadolinium oxide nanoparticles RSC Adv., 2012, 2, This journal is ß The Royal Society of Chemistry 2012
6 coated with fluorescein-pei. Characteristic IR absorption frequencies at 3440 and 1635 cm 21 are assigned as N H stretch and bend (or scissoring), respectively, that at 2920 cm 21 as C H stretch, and that at 1076 cm 21 as C N stretch The broad peak at 3440 cm 21 is due to overlap with the OH stretch. The amount of surface coating was estimated to be wt% from the TGA curve (Fig. 3b). An initial mass loss of 11.57% between room temperature and 128 uc is mainly due to water desorption while mass loss above 128 uc is mainly due to ligand combustion. Here, the boundary between water desorption and ligand burning was estimated by the crossing of the two slopes (Fig. 3b). From this, a grafting density 39 was estimated to be 0.65 nm 22 by using d avg of 3.92 nm from HRTEM images and bulk density of g ml 2140 of Gd 2 O 3. This value shows a sufficient surface coating. In addition to the FT-IR absorption spectrum and TGA data, futher evidence for a surface coating was seen. These include a pale pink colored sample solution, a Fig. 4 Mass corrected (i.e., net) (a) M H and (b) ZFC M T curves of gadolinium oxide nanoparticles in fluorescein-pei coated gadolinium oxide nanoparticles. Fig. 5 Plot of 1/T 1 and 1/T 2 as a function of Gd concentration. The slopes correspond to r 1 and r 2, respectively. fluorescent sample solution after UV irradiation, and a photoluminescence (PL) spectrum, as will be discussed later. Magnetic properties The magnetic properties of fluorescein-pei coated gadolinium oxide nanoparticles were characterized by recording both M H curves (25 H 5 tesla) at T = 5 and 300 K and ZFC M T curves (5 T 330 K) at H = 100 Oe (Fig. 4). The net magnetization of gadolinium oxide nanoparticles was estimated by using the net mass of gadolinium oxide nanoparticles estimated from a TGA analysis. Both coercivity and remanence in M H curves are zero (i.e. no hysteresis). This lack of hysteresis and no magnetic transition down to T =5KintheM T curve show that gadolinium oxide nanoparticles are paramagnetic down to 5 K, which is consistent with a previous neutron beam experiment. 41 From the M H curves, saturation magnetizations of gadolinium oxide nanoparticles were estimated to be and 6.63 emu g 21 at T = 5 and 300 K, respectively. These magnetizations are large even for inducing water proton relaxations even though gadolinium oxide nanoparticles are paramagnetic. This results from a large number of pure S-state 7 unpaired 4f-electrons of Gd(III) ion. Relaxivities The r 1 and r 2 were estimated to be 6.76 and s 21 mm 21 from the slopes in the plots of 1/T 1 and 1/T 2 as a function of Gd concentration, respectively (Fig. 5). The measured relaxivities are also provided in Table 1, together with those of other chemicals. The value of r 1 is y2 times larger than those 4,5 of commercial Gd(III)-chelates. This is due to a high density of probing Gd(III) ions in the nanoparticles. Also Gd(III) ion has the largest spin magnetic moment (S = 7/2) among the elements in the periodic table 45 and thus, can very efficiently induce the longitudinal relaxation of water protons. 4,5 On the other hand, r 2 is smaller than those of superparamagnetic iron oxide (SPIO) nanoparticles (Table 1). This is due to much smaller magnetizations of gadolinium oxide nanoparticles than those of iron oxide nanoparticles at room temperature because SPIO nanoparticles are easily saturated at relatively low applied fields at room temperature. 43,44,46 Fluorescent properties The fluorescent properties of fluorescein-pei coated gadolinium oxide nanoparticles diluted in triply distilled water were characterized by recording a PL spectrum at the excitation wavelength (l ex ) of 470 nm (Fig. 6a). By comparison with a Table 1 Water proton relaxivities (r 1 and r 2 ) of various chemicals Chemical Ligand d avg /nm r 1 /s 21 mm 21 r 2 /s 21 mm 21 Applied field/tesla T/uC Ref. Gd(III) H 2 O DTPA a Gd 2 O 3 D-Glucuronic acid Gd 2 O 3 PEG-silane MnO D-Glucuronic acid Fe 3 O 4 /c-fe 2 O 3 (Resovist) Carboxydextran Fe 3 O 4 (Feridex) Dextran Gd 2 O 3 Fluorescein-PEI This work a Diethylenetriaminepentaacetic acid. This journal is ß The Royal Society of Chemistry 2012 RSC Adv., 2012, 2,
7 Fig. 6 (a) PL spectra of both aqueous solutions of fluorescein-pei coated gadolinium oxide nanoparticles and free fluorescein and pictures of (b-1) an aqueous sample solution and (b-ii) a fluorescent aqueous sample solution after irradiation with a mercury lamp with l ex of 365 nm. reference PL spectrum of a free fluorescein solution (Fig. 6a), a maximum emission of the sample solution at y527 nm can be assigned as due to fluorescein. A red shift by 15 nm from a free fluorescein was observed, which is likely due to conjugation of fluorescein to PEI. A fluorescent sample solution after irradiated with a mercury lamp with l ex of 365 nm is shown in Fig. 6b, showing a fluorescence in the green region, which is due to absorption at y527 nm. In vitro cytotoxicity Fluorescein-PEI coated gadolinium oxide nanoparticles should be non-toxic for in vivo applications. An in vitro cytotoxicity test was performed by using both NCTC1469 and DU145 cell lines with Gd concentrations up to 50 mm (Fig. 7), showing that PEIfluorescein coated Gd 2 O 3 nanoparticles are slightly toxic. PEI is known to be more or less toxic. 47,48 The cytotoxicity slightly increased with increasing sample concentration, as consistent with this expectation. Finally, the cell viability at 50 mm Gd reached y65% for both cell lines due to this toxicity of PEI. In vivo 3 tesla T 1 MR images of a rat with a N1S1 liver tumor To find out the effectiveness of fluorescein-pei coated gadolinium oxide nanoparticles as a T 1 MRI contrast agent in vivo, we took 3 tesla T 1 MR images. 0.1 mmol Gd kg 21 of an aqueous sample solution was injected into a rat tail vein and a series of T 1 Fig. 8 3 tesla T 1 spin echo MR images of a rat with a N1S1 liver tumor before and 4.5 h after injection of an aqueous sample solution of fluorescein-pei coated gadolinium oxide nanoparticles into a rat tail vein. A three-dimensional (3D) flash (i.e., volume interpolated breathhold examination) T 1 MR image also clearly indicates the location of the liver tumor through positive contrast enhancement. Fig. 7 Cytotoxicity results of an aqueous sample solution by using both NCTC1469 and DU145 cell lines with Gd concentrations up to 50 mm. Fig. 9 TEM images of fluorescein-pei coated gadolinium oxide nanoparticles in vesicles (labelled as V) of a liver RES cell. (a) and (b) Filled and likely ruptured vesicles are shown. A dotted square region in (b) is magnified in (c) in which nanoparticles (as examples, four nanoparticles are labelled with arrows) can be seen in a likely ruptured vesicle. Here, many of nanoparticles appear as aggregates RSC Adv., 2012, 2, This journal is ß The Royal Society of Chemistry 2012
8 Fig. 10 Confocal images of DU145 cells: (a) and (b) control cells, (c) and (d) sample cells. Images (a) and (c) were obtained before and (b) and (d) after irradiation with a laser (l ex = 488 nm and y8 watts). No fluorescence was observed in control cells (i.e., (b)) whereas a strong fluorescence in the green region was observed in sample cells (i.e., (d)). The cells were imaged at a magnification of 400. MR images were recorded as a function of time. We observed a clear positive contrast enhancement in a N1S1 liver tumor after injection of the sample solution (Fig. 8). This clear contrast enhancement proves that fluorescein-pei coated gadolinium oxide nanoparticles are functioning as a T 1 MRI contrast agent. This liver tumor model perhaps suggests the possibility of early detection of tumors. The nanoparticles, which had no active targeting ligands on their surfaces, were not targeted to liver tumor. Instead, nanoparticles seem to be naturally more accumulated in liver tumor than in normal liver tissue. The accumulation of nanoparticles in cells can be generally accomplished by active phagocytosis action of the reticuloendothelial system (RES) cells. 49,50 Therefore, the higher contrast enhancement in liver tumor than normal liver in MR images is likely due to this. Accumulation of nanoparticles in a normal liver Since a typical biodistribution study of nanoparticles for various organs in a rat needs time and is also expensive, we simply confirmed the accumulation of nanoparticles into a normal liver by taking in vivo TEM images. This will also confirm the contrast enhancement of the normal liver tissue as well as liver tumor. It is well-known that nanoparticles are uptaken by liver RES cells after intravenous injection. 49,50 In order to see this, we took a TEM images of a normal liver 36 h after an aqueous sample solution was injected into a rat tail vein (Fig. 9). TEM images of vesicles in a liver RES cell clearly showed the internalization of nanoparticles into liver RES cells (Fig. 9). Some of vesicles are filled with nanoparticles whereas some of them are likely to be ruptured. In the latter case, some internalized nanoparticles as aggregates appeared to be released into the cytoplasm by ruptured trafficking vesicles (Fig. 9c). In vitro fluorescent confocal images In order to prove CL, fluorescent confocal images of DU145 cells were taken after incubating them with a sample solution. The violet tinted cell nuclei are due to counterstaining with DAPI. Strongly fluorescent confocal images in the green region were observed in the cells after irradiation with a solid-state laser with 488 nm and y8 watts (Fig. 10). This strong fluorescence is due to fluorescence from fluorescein-pei coated gadolinium oxide nanoparticles internalized into DU145 cells. No fluorescence was, however, observed in control cells which were not treated with a sample solution. Conclusion In summary, fluorescein-pei coated gadolinium oxide nanoparticles were synthesized and their MRI-CL dual functionality was studied both in vivo and in vitro. The core d avg and a avg of fluorescein-pei coated gadolinium oxide nanoparticles were estimated to be 3.92 and 7.5 nm, respectively. These nanoparticles showed r 1 and r 2 of 6.76 and s 21 mm 21, respectively, and fluorescence at y527 nm (green region). The MRI functionality was demonstrated through a clear positive contrast enhancement in 3 tesla T 1 MR images of a rat with a N1S1 liver tumor after intravenous injection of a sample solution into a rat tail vein while the CL functionality, through fluorescent confocal images of DU145 cells after incubation with a sample solution. These two results together clearly show the excellent T 1 MRI-CL dual functionality of fluorescein-pei coated gadolinium oxide nanoparticles. Acknowledgements This work was supported by Grant No. RTI from the Regional Technology Innovation Program of the Ministry of Commerce, Industry, and Energy funded by the Korean Government, Kyungpook National University Research Fund (2012), the Basic Science Research Program through the National Research Foundation funded by the Ministry of Education, Science, and Technology (2012R1A1B to K. S. C., to Y. C., and to G. H. L.), and the R&D program of MKE/KEIT ( , development and commercialization of molecular diagnostic technologies for lung cancer through clinical validation). We thank the Korea Basic Science Institute for allowing us to use their HRTEM and XRD spectrometer. References 1 M. Lewin, N. Carlesso, C. H. Tung, X. W. Tang, D. Cory, D. T. Scadden and R. 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