Human sodium iodide transporter gene-mediated imaging and therapy of mouse glioma, comparison between 188Re and 131I

  • Authors:
    • Rui Guo
    • Yun Xi
    • Min Zhang
    • Ying Miao
    • Miao Zhang
    • Biao Li
  • View Affiliations

  • Published online on: January 8, 2018     https://doi.org/10.3892/ol.2018.7752
  • Pages: 3911-3917
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Abstract

Novel treatment options are urgently required for patients with glioma who are not effectively treated through standard therapy. Human sodium iodide symporter (hNIS) is a molecular target of certain tumors types. Compared with 131I, 188Re possesses a higher energy and shorter half‑life; therefore, the effects of 188Re and 131I were compared in hNIS‑mediated gene imaging and therapy in the present study. Recombinant human brain glioma cell line U87 was transfected with a recombinant lentiviral vector containing hNIS (U87‑hNIS). U87‑0 cell line transfected with blank lentivirus was prepared as a control. In vitro, the 188Re and 131I uptake of U87‑hNIS cells were 21.3‑times and 25.9‑times that of the control groups, however the excretion rate of the two nuclides was very rapid, and the half‑life was only ~4 min. Sodium perchlorate inhibited hNIS‑mediated 188Re and 131I uptake to levels observed in the control groups. 188Re and 131I were able to kill U87‑hNIS cells selectively, with a survival of only 21.6 and 36.2%, respectively. U87‑hNIS nude mice appeared to accumulate 188Re, with a ratio of radioactivity counts between tumor and non‑tumor sites of ~13.5 compared with 10.3 of 131I 1 h after radionuclide injection. In contrast with in vitro studies, U87‑hNIS cells demonstrated a notable increase in 188Re retention in vivo, even 24 h after 188Re injection. U87‑hNIS cells also exhibited increased 131I retention in vivo; however, as the time increased, 131I was rapidly released with the tumor no longer able to be imaged 24 h after 131I injection. Following treatment, U87‑hNIS tumors experienced a volume reduction of 24.1%, whereas U87‑0 cells demonstrated an increase of 28.8%. 188Re and 131I were revealed to be effective at decreasing tumor volume compared with the control. However, 188Re was significantly more potent compared with 131I (P<0.01). The present study indicated that the U87‑hNIS cell line is sufficient to induce specific 188Re and 131I uptake, which may kill cells in vitro and in vivo. 188Re exhibited an increased retention time in vivo compared with 131I, which facilitates the imaging and therapy of U87-hNIS tumors.

Introduction

Glioma is one of the most common malignant tumor types globally with high morbidity and mortality. To date, surgical resection and radiotherapy remain the primary methods used for the treatment of glioma (1,2). Radiotherapy requires at least 55 Gy of external radiation to control the tumor, however, a radiation dose of >60 Gy often results in normal brain tissue necrosis (35). Therefore, novel therapeutic strategies are required.

Sodium iodide symporter (NIS) is a type of cell membrane glycoprotein that mediates the active uptake of iodine in the thyroid and other types of tissues (6). Gene therapy is an important alternative for the treatment of tumors; for example, radioiodine treatment of extra-thyroidal cancer via the ectopic transfer of the NIS gene into otherwise non-NIS-expressing cancer. A number of studies have successfully obtained ectopic expression of NIS in different tumors through gene transfer (710). The dual function of NIS as a diagnostic and therapeutic gene thereby allows easy monitoring of functional NIS expression using γ camera imaging techniques prior to the application of a therapeutic radionuclide dose (11). Our previous studies (1215) demonstrated that baculovirus-mediated human NIS (hNIS) expression may mediate multiple tumor uptake of 131I, providing a promising target for gene therapy. In previous studies, extra-thyroidal tissues have generally not been able to mediate iodide organification following NIS gene transfer, therefore rapid outflow of 131I resulted in a decreased radiation dose able to affect the activity of tumor cells, thus decreasing the curative effect (16). The use of alternative NIS-transported radioisotopes with a higher energy than 131I may improve the efficacy of NIS-mediated radionuclide targeted therapy (17,18). 188Re is a type of short physical half-life radionuclide (0.71 days), which has been applied to treat various diseases, including prostate carcinoma, hepatoma carcinoma, breast carcinoma, bladder carcinoma, refractory arthritis and coronary beta-brachytherapy (1922). Compared with 131I (0.192 MeV), due to its high energy, 188Re (23) is an ideal therapeutic alternative (0.778 MeV). Our previous study (24) suggested that lentiviruses mediate hNIS expression that results in 188Re uptake in glioma and provides a promising gene therapy strategy. However, the physical half-life of 188Re is shorter (0.71 days) compared with that of 131I (8.02 days). Therefore, the purpose of the present study was to compare the therapeutic effects of 188Re- and 131I-mediated gene therapy in vitro and in vivo.

Materials and methods

Plasmid construction, lentivirus preparation and U87 cell transfection with lentivirus

Human NIS gene was obtained in the form of a pcDNA3.1-hNIS plasmid (provided by Dr Sissy Jhiang from Ohio University, OH, USA). U87 glioma cell line [American Type Culture Collection (ATCC), Manassas, VA, USA] was maintained in Dulbecco's modified Eagle's medium (DMEM; Gibco; Thermo Fisher Scientific, Inc., Waltham, MA, USA) containing 10% fetal bovine serum (Gibco; Thermo Fisher Scientific, Inc.), 100 U/ml penicillin and 100 µg/ml streptomycin (Gibco; Thermo Fisher Scientific, Inc.; 5% CO2, 37°C). The plasmid containing hNIS was packaged into lentivirus vector (Thermo Fisher Scientific, Inc.) and named as Lenti-CMV-hNIS. To generate cell line expressing hNIS controlled by cytomegalovirus-enhancer/promoter, Lenti-CMV-hNIS was added to U87 cells at a multiplicity of infection of 2.0, then were selected for further study after 3 weeks. The transfected cell line stably expressing hNIS was named U87-hNIS. U87-hNIS was validated by radionuclide uptake experiments. Cells were inoculated with DMEM containing 10% fetal bovine serum, 100 U/ml penicillin and 100 µg/ml streptomycin in 24-well plates 24 h prior to the experiment to achieve a density of 105 cells per well at the day of experiment.

In vitro radioisotope uptake experiments

188Re was eluted from a 188W/188Re generator (Jiangsu ReTai Pharmaceutical Biotechnology Co., Ltd., Changzhou, China) using 0.9% saline. 131I was supplied by Shanghai Kexin Biotech Co., Ltd. (Shanghai, China). In vitro 188Re/131I uptake experiments of U87-hNIS cells expressing hNIS were performed as Weiss and Grollman (25) described previously, with minor modifications. All data were corrected for attenuation. U87-hNIS cells were washed with 0.5 ml buffered Hanks' balanced salt solution (bHBSS; containing 10 µM HBSS and buffered with 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid, pH 7.3), incubated in 0.5 ml bHBSS (containing 3.7 kBq 188Re/131I) liquid for 1, 2, 5, 10, 20, 30, 60 and 120 min respectively, then washed two times with ice-cold bHBSS, incubated with 1 ml of 100% dehydrated ethanol for 20 min, followed by cell lysis (using trypsin and 0.25% EDTA; Gibco; Thermo Fisher Scientific, Inc.). Finally, the radioactivity (count per min) was detected using a well gamma-counter (Shanghai Institute of Nuclear Research Rihuan Instrument Co., Shanghai, China) and compared with background, in order to achieve a ratio. All the following experiments were conducted in triplicate.

Sodium perchlorate inhibition study

The specificity of 188Re/131I uptake was investigated in the present study. U87-hNIS cells (at a density of 105) were incubated with sodium perchlorate (Sigma-Aldrich; Merck KGaA, Darmstadt, Germany) and 3.7 kBq 188Re/131I in DMEM containing 10% fetal bovine serum, 100 U/ml penicillin and 100 µg/ml streptomycin (5% CO2, 37°C) for 30 min, in which the concentration of sodium perchlorate was 0, 1, 2, 5, 10, 20, 50 and 100 µM, respectively. Thereafter, the cells were washed with bHBSS twice, lysed (using trypsin and 0.25% EDTA; Gibco; Thermo Fisher Scientific, Inc.) at room temperature for three min, and their radioactivity measured, according to the methods aforementioned.

Radioisotope efflux study in vitro

The 188Re/131I efflux kinetics of U87-hNIS cells were investigated as previously described (25). U87-hNIS cells (at a density of 105) were incubated with 188Re/131I (3.7 kBq/well) at 37°C for ~30 min. The culture medium (DMEM containing 10% fetal bovine serum) was then replaced with nonradioactive bHBSS. Cells were incubated for 2, 4, 6, 8, 10, 12, 14, 16, 18 or 20 min and immediately lysed using trypsin and 0.25% EDTA (Gibco; Thermo Fisher Scientific, Inc.). Subsequently, cells were extracted with 1 ml dehydrated alcohol and the radioactivity in the cells was measured as aforementioned.

In vitro assessment of radioisotope toxicity by clonogenic assay

Prior to the experiment, U87-hNIS cells were cultured in 24-well plates, in order to achieve a density of 105 cells/well at the day of study. As presented in Table I, cells were divided into five groups. Group 1 comprised U87-hNIS cells washed with bHBSS with 740 kBq 188Re, then cultured (5% CO2, 37°C) for 7 h. Group 2 was processed much the same as group 1, with the exception that 188Re was replaced with 131I. Groups 3 and 4 were non-transfected U87 cells with 188Re and 131I, respectively. Group 5 comprised non-transfected U87 cells without the addition of any radionuclide. Groups 3, 4 and 5 all served as controls. The 5 groups of cells were then washed and lysed as described above, and seeded in 6-well plates at a density of 200 cells/well. The cells were cultured for 7 days (5% CO2 at 37°C). Following removal of the culture medium as aforementioned, cells were stained with crystal violet solution (0.1%) at room temperature for 10 min and the colonies >30 cells were counted using an optical microscope (×100 magnification; CKX41; Olympus Corporation, Tokyo, Japan). Results were expressed as the percentage of surviving cells compared with untreated U87 cells (Group 5).

Table I.

Subgroup of in vitro 188Re and 131I clonogenic assay.

Table I.

Subgroup of in vitro 188Re and 131I clonogenic assay.

CharacteristicGroup 1Group 2Group 3Group 4Group 5
U87-human
sodium iodide
symporter++
U87 +++
188Re+ +
131I + +
Animal models

A total of 18 female 5-week-old athymic Balb/c nude mice (18–20 g in weight) were used (Shanghai Laboratory Animal Centre Chinese Academy of Sciences, Shanghai, China). A full light-dark cycle with 10 h of light and 14 h of darkness each day was applied, with conditions including a temperature of 26–28°C, a humidity of 40–60%, and general feed and drinking water provided. Mice were sacrificed 4 weeks after the first intravenous injections of 188Re or 131I. Animal experiments were approved by the Ethics Committee and Animal Care Committee of Shanghai JiaoTong University, School of Medicine (Shanghai, China). A xenograft model was generated by subcutaneous injection of U87-hNIS cells (5×106 cells, suspended in 150 µl PBS) into the right armpit of the mice. Subsequently, ~6 weeks following inoculation, the tumor diameters reached 0.8–1.0 cm, which could be used for imaging and therapies.

Tumor imaging and therapy study in a xenograft model

Tumor imaging studies were performed in six U87-hNIS nude mice. 188Re (55.5 MBq) or 131I (55.5 MBq) was injected through the caudal vein. Tumor images were performed 15 min, 1, 2, 4 and 24 h after injection using a high-resolution gamma camera equipped with a pinhole collimator (GE Healthcare Life Sciences, Little Chalfont, UK) immediately following 188Re or 131I injection. Each image lasted for 3 min. The matrix size was 256×256. Region of interest was placed on the area of tumor and the contralateral axillary, and the ratio of radioactivity counts between tumor and non-tumor sites (T/NT) at each time point was measured.

Tumor therapy studies were performed in U87-hNIS nude mice at the same time. In the present study, no animal presented with multiple tumors, and when the tumor diameter of nude mice grew to 0.8–1.0 cm in diameter (the minimum and maximum diameter exhibited by a single tumor in the present study were 0.82 and 0.96 cm, respectively), they were randomly divided into three groups (n=6). Group 1 was given two intravenous injections of 55.5 MBq 188Re with an interval of 1 week. Group 2 was treated intravenously with 2 injections of 55.5 MBq 131I with a 1 week interval. Group 3 was left untreated. In order to evaluate the therapeutic effect of hNIS mediated radionuclides, tumor size was measured with calipers prior to and following the administration of 188Re or 131I every week, in three dimensions. Tumor volume was estimated by the following formula: Length × width2x0.52.

Statistical methods

Origin 7.5 (OriginLab, Northampton, UK) and SPSS 16.0 (SPSS, Inc., Chicago, IL, USA) software were used in the present study. All experiments were performed in triplicates unless otherwise indicated. Numeric data are expressed as mean ± standard deviation. One-way analysis of variance was performed to evaluate the difference amongst groups followed by Tukeys post hoc test. P<0.05 was considered to indicate a statistically significant difference.

Results

Preparation of the lentiviruses

The lentiviral vector Lenti-cytomegalovirus (CMV)-hNIS containing CMV promoter and hNIS gene was packed successfully, and the Lenti-CMV-0 vector was packed as control. Stable cell lines U87-hNIS and U87-0 were established 3 weeks after infection with recombinant lentivirus. For the purpose of comparing hNIS mediated uptake of radioisotope in the cell line, 188Re and 131I uptake experiments were performed and compared in the following studies.

hNIS mediated in vitro radioisotope uptake

In U87-hNIS cells, uptake of 188Re/131I in relation to incubation time is presented in Fig. 1. The results reveal the initial 188Re/131I uptake dependent on incubation time. The results demonstrated that 188Re/131I influx rapidly into U87-hNIS cells, reaching a peak at 30 min. The 188Re/131I uptake of U87-hNIS cells was measured to be 21.3 and 25.9-fold higher compared with that of U87-0 cells. The radioactivity measured 2 h after 188Re/131I incubation was 84.7 and 88.5% of the maximal uptake. 131I experienced an increased uptake compared with 188Re in U87-hNIS cells. In a similar study performed by Zuckier et al (26), 188Re and 131I were reported to demonstrate a high uptake.

Sodium perchlorate inhibition study

In order to verify the specificity of hNIS mediated 188Re/131I uptake, 188Re/131I inhibition test was performed in U87-hNIS cells in the presence of varying concentrations of sodium perchlorate, an already confirmed competitive inhibitor. Fig. 2 presents the effect of distinct concentrations of sodium perchlorate on 188Re/131I uptake in U87-hNIS cells. When cells were treated with sodium perchlorate (1–100 µM), 188Re/131I uptake in U87-hNIS cells was inhibited in a dose-dependent manner. At 5 µM, sodium perchlorate decreased 188Re/131I uptake to 15.3 and 18.1% of original levels, respectively, compared with and an inhibition rate of 96 and 95.3% at 50 µM. These results demonstrate that sodium perchlorate may specifically block 188Re/131I uptake in U87-hNIS cells, suggesting that 188Re/131I uptake in U87-hNIS cells is mediated by functional hNIS expression.

Radionuclide efflux assay

188Re/131I efflux assays were performed 30 min after the addition of 188Re/131I into the cultured cells (the aforementioned cell uptake experiment identified that the highest intracellular uptake was obtained at 30 min). The culture medium containing 188Re/131I was replaced by nonradioactive DMEM, the remaining 188Re/131I activity in U87-hNIS cell lysate was determined. As presented in Fig. 3, the intracellular radionuclides were released rapidly into the medium, with >50% of radionuclides excreted out of the cells within the first 4 min, whereas a limited amount of residual radionuclide was observed 20 min after 188Re/131I was replaced by nonradioactive DMEM. These results suggested that radioactivity is rarely retained in U87-hNIS cells without reuptaking.

Radio toxicity assessed by colony-forming assay

Following treatment with 188Re/131I, a colony-forming experiment was performed to calculate the survival rate of the cells. The results are presented in Fig. 4. The data are expressed as the percentage of surviving cells. In Groups 3 and 4, U87-0 cells were treated with 188Re/131I, with the number of colonies representing 76.3 and 85.7% of the blank control group (Group 5), indicating that the two radionuclides exhibit nonspecific killing effects on U87-0 cells. Following treatment with 188Re/131I, survival of Groups 1 and 2 were markedly decreased compared with that of the other 3 groups, with survival rates of only 21.6 and 36.2%, respectively. These results suggest that 188Re/131I exhibits a selective killing effect on U87-hNIS cells, with an increased killing capacity of 188Re compared with that of 131I.

Tumor imaging and therapy study

The results of in vivo uptake and efflux of 188Re/131I were different from those observed in vitro. U87-hNIS tumor demonstrated an efficient 188Re/131I uptake in vivo, which accumulated 188Re/131I rapidly and significantly as indicated by the arrows in imaging results of the right armpit in Fig. 5. Organs naturally expressing hNIS (such as the thyroid and stomach) and organs participating in 188Re/131I excretion (such as the kidneys and bladder) were able to be visualized. Quantified results are presented in Fig. 6. The accumulation of 188Re/131I reached a peak 1 h after administration (T/NT, 13.5±3.2 and 10.3±2.1, respectively). 188Re remained at a steady level until 24 h (T/NT, 11.6±2.1), whereas 131I experienced limited retention at 24 h (T/NT, 3.9±0.7). Thyroid naturally expressing NIS markedly accumulated 131I 24 h after injection, whereas 188Re demonstrated limited accumulation (Fig. 5). As a result of lacking organification, 188Re cannot be retained in the thyroid for a prolonged period of time, therefore its half-life is relatively short in the thyroid and may protect the thyroid from hypothyroidism. In contrast, 131I can be organified by the thyroid, which alongside a long half-life may increase the risk of hypothyroidism.

A total of 3 weeks following treatment, a difference in tumor volume was demonstrated among mice treated with 188Re (409.6±113.4 mm3), 131I (468.4±148.9 mm3) and non-treated animals (582.1±178.8 mm3) (P<0.05). No difference was observed between the 188Re and 131I treatment group at 3 weeks. The association between treatment group and tumor volume was more significant at 4 weeks post treatment. The tumor volume was significantly different between mice treated with 188Re (317.2±72.1 mm3), 131I (560.8±97.4 mm3) and non-treated (861.1±153.8 mm3) (P<0.01; Fig. 7). Following therapy, 188Re treated U87-hNIS tumors experienced a volume reduction of 24.1%, whereas 131I treated U87-hNIS tumors demonstrated a volume increase of 28.8%. 188Re and 131I were demonstrated to be effective at decreasing the tumor volume compared with the untreated control, with 188Re revealed to exhibit an increased effect compared with 131I (P<0.01).

Discussion

NIS-mediated radionuclide therapy possesses several advantages (27), making it an attractive approach for glioma imaging and therapies. It does not require complex radiolabeling procedures, it also is small-sized allowing it to penetrate the blood brain barrier and diffuse into the tumor (28). Radioisotopes exhibit the potential of a bystander effect, which may destroy tumor cells without hNIS expression by radionuclides emitted from surrounding hNIS expression tumor cells (29). The hNIS gene is not expressed in normal cells however is in glioma cells (30), this indicates that it may assist in improving the specificity of tumor therapy and decreasing the damage to normal brain tissue.

131I is an isotope commonly used in NIS-associated radionuclide therapy studies (31). However, as the radiation energy is not high enough, therapeutic efficacy of 131I is limited (3). The use of a high-energy radionuclide also transported by NIS including 188Re, may be an effective strategy to improve therapeutic effect. A previous study demonstrated that 188Re and 125I share similar biodistribution patterns in mice, with the exception of the thyroid gland, as the thyroid gland has an organic function of iodine, which can retain 125I (26). With lower γ-photons energy, 188Re (155 keV) (32) is suitable for imaging, unlike 131I (364 keV). 188Re can be easily generated using a 188W/188Re generator (33). These attractive physical properties make 188Re a promising candidate for tumor imaging and therapy (19). 188Re possesses a higher β energy, but relatively shorter physical half-life compared with 131I (34). Therefore, in the current study, the effects of 188Re and 131I in the treatment of glioma were compared in vivo and in vitro.

In the present study, it was demonstrated that a lentivirus containing CMV-hNIS expression cassette is able to transfect U87 cells, as revealed by efficient 188Re/131I uptake in U87-hNIS cells. 188Re/131I exhibit rapid uptake in U87-hNIS cells, and the dynamic uptake pattern of 188Re/131I was similar to that of previous studies (30,31). 188Re uptake of U87-hNIS was up to 21.3-times that of the U87-0 control group, whereas 131I uptake was up to 25.9-fold of that of the control group. The two isotopes experienced a plateau phase akin to previous studies (35,36), when the uptake and efflux of the isotopes reached a state of equilibrium (25). As with previous NIS studies, radionuclide retention time was short, and rapid outflow remained a problem in the in vitro studies, in the present study. Neither 188Re nor 131I experienced a long retention time in vitro.

In the in vitro experiments, isotope flow was rapid, with the outflow kinetics of the two radionuclides being similar. In addition, the colony formation assay demonstrated that U87-hNIS cells could be killed effectively by 188Re and 131I. The absorbed dose of 188Re was sufficiently high to selectively kill 78.4% of the cells, whereas 131I was able to kill up to 63.8% of the cells. These data are sufficient to suggest that even with a lower uptake than that of 131I, 188Re may also be able to deliver a greater radiation dose to tumor cells, which is similar to the results reported by Kang et al (37) who identified that 188Re uptake increased 87-times, whereas 125I uptake increased 150-times in NIS transfected hepatocellular carcinoma cells, compared with untransfected cells. Following treatment with 188Re or 131I, the survival rate of cells was 28.9 and 46.3% respectively. Therefore, a superior therapeutic effect of 188Re was demonstrated.

In the in vitro study, cells in the culture dishes were arranged in a single layer, which is not a three-dimensional structure. Conclusions from the cells cannot be applied to solid glioma with a three-dimensional structure, which requires further confirmation in xenografts. In vivo, U87-hNIS glioma cells are close to each other, which allows for rapid reuptake of radionuclides in the cells and serves as a mechanism for isotope trapping by glioma. The results of the in vivo imaging investigations in the present study suggested that 188Re remained in U87-hNIS glioma cells even 24 h after administration, whereas a limited amount of 131I was retained in the cells 24 h after treatment. The results of the present study suggest that 188Re cannot be retained in the thyroid gland, as it cannot be organified. A previous study has reported a similar biodistribution pattern for 131I and 188Re (38). In fact, the thyroid will decrease the competitive uptake of 188Re, thereby decreasing thyroid injury and increasing tumor reuptake of 188Re, which is an advantage of hNIS-mediated radionuclide therapy in non-thyroid tumors. In addition, the results of the present study demonstrated that the degree of 188Re/131I uptake and retention are sufficient to achieve tumor therapeutic effects. Following treatment for 4 weeks, there was a significant difference in tumor size between 188Re treated U87-hNIS mice and 131I treated U87-hNIS mice.

The present study also possessed a number of limitations. A stable hNIS transfected cell line was used to express hNIS, which could not be used directly in clinical practice. As a result of the variation of hNIS transfection efficiency and the difference in specificity, actual clinical efficacy of 188Re and 131I requires further evaluation. It is reported that U87 MG ATCC cell line has been contaminated/misidentified, however it is most probably also a glioblastoma cell line (39). hNIS mediates uptake of iodine in thyroid and numerous types of non-thyroid cells (6), as a result, a number of previous studies have also successfully obtained ectopic expression of hNIS in different tumors by gene transfer (710). The main purpose of the present study was to compare the therapeutic effects of 188Re and 131I mediated by hNIS, rather than a study into the underlying molecular mechanisms of their effects, therefore the U87 cell line could be replaced with a variety of cell lines that express hNIS, as such the aforementioned misidentification/contamination issue is unlikely to have affected the outcomes of the present study.

In conclusion, the results of the present study demonstrated that 188Re appeared to be more efficient than 131I in the treatment of gliomas. The strategy appears to be a novel method for tumor imaging and therapy. However, improvements to decrease efflux and achieve increased radiation doses in the target tissue are still required.

Acknowledgements

The present study was supported by the National Natural Science Foundation of China (grant nos. 81101071 and 81471687) and the Medical Engineering (Science) Cross Foundation of Shanghai JiaoTong University (grant no. YG2013MS27).

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March-2018
Volume 15 Issue 3

Print ISSN: 1792-1074
Online ISSN:1792-1082

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Spandidos Publications style
Guo R, Xi Y, Zhang M, Miao Y, Zhang M and Li B: Human sodium iodide transporter gene-mediated imaging and therapy of mouse glioma, comparison between 188Re and 131I. Oncol Lett 15: 3911-3917, 2018
APA
Guo, R., Xi, Y., Zhang, M., Miao, Y., Zhang, M., & Li, B. (2018). Human sodium iodide transporter gene-mediated imaging and therapy of mouse glioma, comparison between 188Re and 131I. Oncology Letters, 15, 3911-3917. https://doi.org/10.3892/ol.2018.7752
MLA
Guo, R., Xi, Y., Zhang, M., Miao, Y., Zhang, M., Li, B."Human sodium iodide transporter gene-mediated imaging and therapy of mouse glioma, comparison between 188Re and 131I". Oncology Letters 15.3 (2018): 3911-3917.
Chicago
Guo, R., Xi, Y., Zhang, M., Miao, Y., Zhang, M., Li, B."Human sodium iodide transporter gene-mediated imaging and therapy of mouse glioma, comparison between 188Re and 131I". Oncology Letters 15, no. 3 (2018): 3911-3917. https://doi.org/10.3892/ol.2018.7752