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NIR-triggered drug delivery system based on phospholipid coated ordered mesoporous carbon for synergistic chemo-photothermal therapy of cancer cells
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Anman Zhang, Luo Hai, Tianzheng Wang, Hong Cheng, Man Li, Xiaoxiao He*, Kemin Wang*
Chinese Chemical Letters | 2020, 31(12) : 3158 - 3162
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Chinese Chemical Letters | 2020, 31(12): 3158-3162
• Communication •
NIR-triggered drug delivery system based on phospholipid coated ordered mesoporous carbon for synergistic chemo-photothermal therapy of cancer cells
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Anman Zhang, Luo Hai, Tianzheng Wang, Hong Cheng, Man Li, Xiaoxiao He*, Kemin Wang*
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  • State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Biology, College of Chemistry and Chemical Engineering, Hunan University, State Key Laboratory for Bio-Nanotechnology and Molecular Engineering of Hunan Province, Changsha 410082, China
Published: 2020-12-15 doi: 10.1016/j.cclet.2020.04.035
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Chemo-photothermal treatment is one of the most efficient strategies for cancer therapy. However, traditional drug carriers without near-infrared absorption capacity need to be loaded with materials behaving photothermal properties, as it results in complicated synthesis process, inefficient photothermal effects and hindered NIR-mediated drug release. Herein we report a facile synthesis of a polyethylene glycol (PEG) linked liposome (PEG-liposomes) coated doxorubicin (DOX)-loaded ordered mesoporous carbon (OMC) nanocomponents (PEG-LIP@OMC/DOX) by simply sonicating DOX and OMC in PEG-liposomes suspensions. The as-obtained PEG-LIP@OMC/DOX exhibits a nanoscale size (600±15 nm), a negative surface potential (-36.70 mV), high drug loading (131.590 mg/g OMC), and excellent photothermal properties. The PEG-LIP@OMC/DOX can deliver loaded DOX to human MCF-7 breast cancer cells (MCF-7) and the cell toxicity viability shows that DOX unloaded PEG-LIP@OMC has no cytotoxicity, confirming the PEG-LIP@OMC itself has excellent biocompatibility. The NIR-triggered release studies demonstrate that this NIR-responsive drug delivery system enables on-demand drug release. Furthermore, cell viability results using human MCF-7 cells demonstrated that the combination of NIR-based hyperthermal therapy and triggered chemotherapy can provide higher therapeutic efficacy than respective monotherapies. With these excellent features, we believe that this phospholipid coating based multifunctional delivery system strategy should promote the application of OMC in nanomedical applications.

Ordered mesoporous carbon  /  Polyethylene glycol linked liposomes  /  Stimuli-responsive drug delivery system  /  NIR-triggered drug delivery  /  Chemo-photothermal therapy
Anman Zhang, Luo Hai, Tianzheng Wang, Hong Cheng, Man Li, Xiaoxiao He, Kemin Wang. NIR-triggered drug delivery system based on phospholipid coated ordered mesoporous carbon for synergistic chemo-photothermal therapy of cancer cells[J]. Chinese Chemical Letters, 2020 , 31 (12) : 3158 -3162 . DOI: 10.1016/j.cclet.2020.04.035
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Mesoporous materials, which refer to a class of porous materials with a pore size between 2-50 nm, are widely used in the fields of catalysis, adsorption, separation, sensing, medical, ecology, biology and nanotechnology [1], because of their advantageous properties, such as high specific surface area, regular and ordered pore structure, narrow pore size distribution, and a continuously adjustable pore size [2]. In recent years, various novel mesoporous materials, including mesoporous silica nanoparticles (MSN), mesoporous carbon nanoparticles, mesoporous titanium nanoparticles, etc., have drawn a great deal of attention for carrying anticancer drugs as drug carriers in tumor treatment. Especially, a series of stimuli-responsive drug delivery system (DDS) based on MSN have been developed and widely reported in the recent ten years. In these systems, the efficient release of guest molecules from MSN was regulated either by external stimuli, such as pH [3, 4], light [5, 6], temperature [7, 8], redox reactions [9, 10], biomolecules [11, 12]. Stimuli-responsive MSN DDS was one of the most efficient strategies for therapies because it is conducive to improving the efficacy. Generally, drug treatment is more effective in combination with other regimens in the design of MSN DDS. The combined use of chemotherapy and photothermal therapy (PTT) can not only directly burn cancer cells, but also is helpful to sensitize the cancerous tissues to the effects of cytotoxic drugs to achieve a synergistic killing effect on tumors, which have been widely used in recent years. For example, Zhu et al. prepared PEGylated mesoporous silica coated copper sulfide (CuS@mSiO2-PEG) nanocomposites with DOX for synergistic photothermal and chemotherapy treatment of tumors [13]. Yang et al. reported a combination of MSN, CuS nanoparticles, and folic acid (FA), for synergistic therapies for chemotherapy and photothermal therapy [14]. Hu et al. designed FA and CuS-decorated MSN for synergistic treatment with photothermal and chemotherapy [15]. Huang et al. developed HB5 aptamer-functionalized MSN-carbon loaded doxorubicin (MSCN-PEG-HB5/DOX) for synergistic photothermal and chemotherapy cancer treatment [16]. Despite these burgeoning achievements, the DDS based on MSN still needs to introduce other materials with photothermal properties that have presented several disadvantages: (1) Surfactants are used in complex synthesis processes. Preparation ofmonodisperse residual surfactants in the silica microsphere process is harmful to biomedical applications even after an uneconomical and timeconsuming removal process [17, 18]. (2) The core-shell structure may inhibit photothermal effects and NIR-mediated drug release [19]. Hence, the design of mesoporousmaterials based nanocarriers for tumor synergistic chemo-photothermal therapy remains a complex and exciting challenge.
Ordered mesoporous carbon (OMC) not only has high specific surface areas, large pore volumes, chemical inertness, and excellent mechanical stability, but also has superior photothermal conversion ability within the NIR region, which can be used as a candidate for exploring the synergistic effect of chemotherapy and photothermal therapy. By taking advantage of such properties, many nanocomponents for photothermal therapy with OMC as carrier material were reported. For example, Chen et al. prepared thermo-sensitively and magnetically ordered mesoporous carbon nanospheres (TMOMCNs) with DOX for synergistic photothermal and chemotherapy treatment of tumors [20]. Wang et al. fabricated a "four-in-one" theranostic system and developed for photoacoustic (PA) imaging-guided synergistic targeting chemo-gene-thermo trimodal therapy of breast cancer. In this system, OMC is irradiated with NIR laser, which led to temperature rise and drug release for PA-imaging and chemo-gene-thermo trimodal therapy [21]. Despite these burgeoning achievements, the use of OMC for designing a drug release system is still an incipient area of research.
In the study, as shown in Fig. 1, we selected OMC nanoparticles as a carrier for drug delivery and photothermal therapy. The OMC based nanocomponents were used as DOX vectors for the synergistic treatment of cancer under NIR laser. This nanocomponent could be easily obtained by mixing PEG-linked liposomes (PEG-liposomes) with DOX and OMC under sonication (PEG-LIP@OMC), by the way, the application of PEG in drug delivery systems has also attracted widespread attention in recent years [22-24]. Due to the hydrophilic-hydrophobic effect, PEG-liposomes will self-assemble in this structure: The hydrophilic phosphate ester heads point outward to the aqueous environment on both sides, while the hydrophobic tail points inward to another layer of hydrophobic tails. By using various commercially available phospholipid derivatives, the composition of the coated phospholipid could be easily designed and controlled. In this design, the coated liposome complex consists of the essential phospholipids 1, 2-dimyristoyl-sn-glycero-3-phospho-(1-rac-glycerol) (DMPG) and phospholipids 1, 2-distearoyl-sn-glycero-3-phosphoethanolamine-N-[methoxy(polyethylene glycol)2000] (DSPE-PEG2000). Once the nanocomponents reached cancer cells, the photothermal effect of PEG-LIP@OMC/DOX through exogenous and non-invasive NIR exposure not only induced endosome destruction, but also promoted the rapid release of DOX from PEG-LIP@OMC/DOX. Subsequently, cytosolic DOX released from PEG-LIP@OMC/DOX could enter the nucleus and caused apoptosis [25, 26]. At the same time, NIR laser-induced high temperature of PEG-LIP@OMC could also induce apoptosis. Therefore, chemo-photothermal synergistic treatment was realized. In addition, loading DOX into PEG-LIP@OMC solved the problems of high metabolism of DOX and premature drug leakage and cumbersome drug carrier synthesis process. Combined with these functions, we believed that this developed multifunctional nanocomponent would greatly promote the application of OMC in chemical photothermal treatment of cancer cells in the near future.
Following the design above, we first investigated the coating of OMC by PEG-liposomes. Briefly, the appropriate size of OMC was obtained readily by sonicating the purchased OMC according to the reported method [27]. TEM image showed that the obtained OMC had visible stick structure and uniform size around 500 nm (Fig. 2A). Subsequently, PEG-liposomes was coated on OMC to form PEG-LIP@OMC by ultrasound at room temperature. In this process, the liposome was disrupted to reconstitute the vesicles and encapsulate OMC. TEM image (Fig. 2B) directly showed the structure of PEG-LIP@OMC with a bigger size of around 600 nm due to modified liposomes, and the channels become a little vague, which is caused by the coverage of liposomes on the surface. The elemental composition of C of OMC was characterized by X-ray energy dispersive spectroscopy (EDS) (Fig. 2C). The elemental composition of PEG-LIP@OMC by EDS had changed into C, N and P (Fig. 2D), which belong to the PEG-liposomes. The change in elemental composition proved the successful synthesis of PEG-LIP@OMC.
Dynamic light scattering (DLS) and zeta potential were subsequently used to confirm the successful preparation of PEG-LIP@OMC. As indicated in Table S1 (Supporting information), the hydrodynamic diameter of the naked OMC was 500 ± 20 nm with a poly-dispersity index (PDI) of 0.475. However, the hydrodynamic size of the PEG-LIP@OMC nanoparticles was increased to 600 ± 15 nm (PDI: 0.298) after PEG-LIP coating. At the same time, the change in zeta potential of PEG-liposomes, OMC and PEG-LIP@OMC also confirmed this coating process (Fig. 3A). The surface zeta potential of naked OMC and PEG-liposomes were 20.4 mV and -36.7 mV, respectively, while PEG-LIP@OMC showed the zeta potential of -8.4 mV because of the highly anionic PEG-liposomes coating.
The above results demonstrated that the PEG-liposomes could be easily coated on the OMC. Thus, the DOX loaded PEG-LIP@OMC was further prepared by incubation of the OMC with DOX before PEG-liposomes coating. The as-synthesized PEG-LIP@OMC/DOX was measured by the fluorescence spectrometer. Compared with free DOX, the fluorescence of DOX could be quenched after loaded into the OMC (Fig. S1 in Supporting information). By calculating with a standard curve (Fig. S2 in Supporting information), the loading amount of DOX from PEG-LIP@OMC/DOX was determined to be approximately 131.592 mg/g OMC. As illustrated in Fig. S3A (Supporting information), the significant small-angle XRD peaks of OMC exhibited well resolved peaks which were typical of highly ordered 2D hexagonal mesoporous structures [28, 29]. An intense reflection representing (100) crystal plane of the 2D-hexagonal structure was observed for OMC as well as the PEG-LIP@OMC/DOX indicating the 2D hexagonal porous structures stability of OMC. The appearances of well-defined reflections in the diffraction patterns suggest the formation of long-range ordered porous materials. The wide-angle XRD spectra of OMC and PEG-LIP@OMC exhibited two broad peaks (2θ = 24°–43°) (Fig. S3B in Supporting information), attributed to the amorphous carbon networks [30, 31]. The N2 adsorption desorption isotherm could be classified as a type-Ⅳ isotherm (Fig. 3B), indicating the mesoporous channels. Meanwhile, the OMC and PEG-LIP@OMC/DOX were also characterized by the surface area, pore volume and pore diameter. The results were shown in Table S2 (Supporting information) and Fig. 3B inset. The Brunauer–Emmett–Teller (BET) surface area and total pore volume of PEG-LIP@OMC/DOX were 440.080 m2/g and 0.671 cm3/g, respectively, slightly lower than those the specific surface area (765.735 m2/g) and pore volume (0.671 cm3/g) of OMC. Calculated by the Barrett-Joyner-Halenda (BJH) method, the pore-size distributions of PEG-LIP@OMC/DOX were concentrated at ca. 3.400 nm which is smaller than those of OMC (3.798 nm). The decrease of the pore size and pore volume of PEG-LIP@OMC/DOX was attributed to the loading of DOX and PEG-liposomes on OMC. These results strongly proved that the mesopores structures of OMC had not been destroyed by the related modification, and DOX was indeed embedded into PEG-LIP@OMC core.
In addition, in order to achieve the ability of NIR fluorescence tracing of PEG-LIP@OMC/DOX, the NIR fluorescent dye atto647N was conjugated onto PEG-LIP@OMC/DOX to get atto647N labeled PEG-LIP@OMC/DOX (atto647N-PEG-LIP@OMC/DOX) using a streptavidinbiotin crosslinking method. PEG was used in the molecule as a spacer to prevent quenching of the fluorescent probe by OMC through fluorescence resonance energy transfer. The formation of atto647N-PEG-LIP@OMC/DOX was characterized using the ultraviolet visible (UV–vis) spectroscopic method. As shown in Fig. S4 (Supporting information), the absorbance spectrum of atto647N-PEG-LIP@OMC/DOX showed an apparent clear peak (λmax = 644 nm), which was the characteristic peak of atto647N, whileno signal was detected for DOX, OMC and PEG-LIP@OMC. It indicated that the atto647N was successful conjugated to PEG-LIP@OMC/DOX. Moreover, atto647N labeling was also confirmed by using the fluorescence method. Comparing with atto647N-PEG-LIP, the fluorescence spectrum showed that atto647N-PEG-LIP@OMC still had an emission wavelength of 669 nm, which was the characteristic fluorescence emission spectrum of atto647N (Fig. S5 in Supporting information). Collectively, these results described above provided direct evidence for the successful preparation of the PEG-LIP@OMC/DOX nanocomponent. Such perfect phospholipid-based biocompatible coating favorably supported the potential of PEG-LIP@OMC/DOX for biomedical applications.
As a drug carrier in the DDS synthesized above, it was essential to study the photothermal conversion ability of the PEG-LIP@OMC as a drug carrier. Therefore, to study the efficiency of PEG-LIP@OMC for PTT, different concentrations of naked OMC and PEG-LIP@OMC solutions were exposed to a 780 nm NIR laser (1.1 W/cm2), respectively. It was demonstrated that the temperature of the naked OMC solution could reach 43.9, 49.7, 54.8, 59.0 ℃ at different concentrations of 31.25, 62.50, 125.00 and 250.00 μg/mL, respectively (Fig. S6 in Supporting information).We could also observe that the temperature of PEG-LIP@OMC/DOX solutions could still reach 43.5, 49.8, 54.3, 58.8 ℃ at different concentrations of 31.25, 62.50, 125.00 and 250.00 μg/mL, respectively, displayed in Fig. 3C. On the contrary, the solution temperature of pure water changed slightly under the same power of NIR laser irradiation (from 28.7 ℃ to 31.5 ℃). The thermal imaging photographs also reveal a clear visual observation for the temperature change. As displayed in Fig. 3E, the temperaturesobtainedfrom the thermalinfrared camera atdifferent concentrations and irradiation times were similar to the temperature which was monitored by the on-line temperature acquisition device. These results strongly proved that the PEG-LIP@OMC could efficiently convert the NIR laser into heat without being affected by liposome coating and exhibited an obvious concentration- and time-dependent temperature elevation. Besides, after continuous 780 nm laser irradiation for five cycles, the process of temperature changes did not show obvious difference, showing good photothermal stability (Fig. S7 in Supporting information).
After proved that the PEG-LIP@OMC had excellent light-to-heat conversion performance, we subsequently investigated whether the PEG-LIP@OMC/DOX could release cargoes in a controlled manner upon exposure to NIR laser. The drug release studies in buffer were performed with or without NIR laser stimulation. As shown in Fig. 3D, the DOX release from PEG-LIP@OMC/DOX was minimal when NIR irradiation was not used (less than 42.38% in 60 min). For OMC/DOX, the DOX release reached 91.93% in 60 min. The results supported that PEG-LIP@OMC/DOX was robust and premature drug release was effectively inhibited due to the blocking effect of coating PEG-liposomes. Notably, interesting burst-like release from PEG-LIP@OMC/DOX was markedly boosted under laser irradiation, e.g., from 39.43% to 68.49% at 30 min. The drug release was practically switched off following retreating NIR irradiation. Similar results were observed when the same laser treatment was repeated, in which drug release was augmented from 75.67% to 79.82% at 60 min. It was evident that the DOX release from PEG-LIP@OMC/DOX could be repeatedly triggered by NIR laser.
Before investigating the NIR laser-responsive performance of PEG-LIP@OMC/DOX in cells, the cellular uptake of PEG-LIP@OMC/DOX was first monitored by screening the fluorescence of atto647N molecules modified at the nanocomponents. Using human MCF-7 breast carcinoma cells (MCF-7 cells) as demonstration, the cellular uptake of atto647N-PEG-LIP@OMC was observed by confocal laser scanning microscopy (CLSM). It was displayed that the fluorescence signals from atto647N-PEG-LIP@OMC (red) were gradually increased with the rising incubation time of MCF-7 cells and atto647N-PEG-LIP@OMC (Fig. S8 in Supporting information), indicating successful cellular uptake of the atto647N-PEG-LIP@OMC. Subsequently, the release behavior of DOX from PEG-LIP@OMC/DOX in the living cells was detected by using the CLSM. As described above, the fluorescence of the loaded DOX was quenched by OMC. Therefore, we could not detect the fluorescence of the DOX if it was not released from the PEG-LIP@OMC/DOX. The results were indeed in line with our expectations. As shown in Fig. 4A, without the application of a NIR laser stimulus, the fluorescence of DOX molecules was quenched by OMC, no obvious red fluorescence of DOX was observed in the cells during the 60 min of incubation. However, the red fluorescence of DOX, belonging to the released DOX of internalized PEG-LIP@OMC/DOX, was clearly visible in the cytoplasm of MCF-7 cells under laser. Therefore, the PEG-LIP@OMC/DOX, as an intracellular DDS, could effectively hold DOX before NIR laser exposure. The photothermal heating of PEG-LIP@OMC/DOX induced the PEG liposomes coating disruption, leading to the release of DOX into the cells. These results described above have demonstrated that the controlled release behavior of PEG-LIP@OMC/DOX was NIR laser-dependent.
After confirming the cellular uptake and DOX release behavior under NIR laser illumination, we moved on to further study the intrinsic toxicity of PEG-LIP@OMC to MCF-7 cells because that biocompatibility was the key concern for the biomedical applications of drug carriers. The MCF-7 cells were incubated with different concentrations of PEG-LIP@OMC. As shown in Fig. 4B, it was illustrated that the PEG-LIP@OMC showed low cytotoxicity to cells in a concentration rang of 0–80 μg/mL. Nearly 78.8% of the cells were alive at the highest concentration of PEG-LIP@OMC (80 μg/mL). The concentrations of PEG-LIP@OMC/DOX used in the following experiments were lower than 80 μg/mL, so we might consider that the drug carrier itself had no obvious short-term toxicity to MCF-7 cells. In addition, no hemolysis appeared under different concentrations of PEG-LIP@OMC, indicating good biocompatibility of PEG-LIP@OMC (Fig. S9 in Supporting information).
Finally, the in vitro chemo-photothermal therapy effect of PEG-LIP@OMC/DOX on MCF-7 cells was investigated by MTT assay. As displayed in Fig. 4C, free DOX showed a certain extent of cytotoxicity to MCF-7 cells at a concentration rang of 0–10.53 μg/mL. The PEG-LIP@OMC/DOX exhibited lower antitumor activity in MCF-7 cells than that of free DOX at a dosage of 10.53 μg/mL (the viability of the cells was 72.47% and 70.06%, respectively). The reason for this lower antitumor was because of the blocking effect of liposomes, and a portion of DOX could not be released into cells. The PEG-LIP@OMC under 10 min NIR irradiation also displayed a certain extent of cytotoxicity, and cell viability of 63.54% was observed at 80 μg/mL. It declared that the PEG-LIP@OMC had the PTT effect, which could convert the NIR laser into heat and subsequently kill the cells. Remarkably, the viability of the cells was only 33.20% at a concentration of 10.53 μg/mL DOX for combination therapy, a value which was lower than that of free DOX, PEG-LIP@OMC with NIR irradiation or PEG-LIP@OMC/DOX without NIR irradiation, respectively. All of these results described above clearly suggested that the system of PEG-LIP@OMC/DOX had an effective synergistic treatment effect and this synergistic treatment could offer a better therapeutic effect at the cellular level compared to monotherapies. In addition, the combination index (CI) value of PEG-LIP@OMC/DOX was calculated according to the reported method [32]. It was calculated to be 0.112 (Fig. 4C), indicating that the theoretical data also can effectively demonstrate the strong synergistic chemo-photothermal therapy mediated by PEG-LIP@OMC/DOX.
In summary, we successfully synthesized DOX loaded OMC and then coated PEG-liposomes onto the OMC surface for inhibiting anti-cancer drug DOX release premature. The composition of the coated phospholipid could be readily designed and controlled by using various commercially available phospholipid derivatives, which allowed the display of various functional groups, signal molecules, and biological ligands on the OMC surface. In this study, the coating liposome composite consisted of essential phospholipids DMPG, and phospholipids DSPE-PEG2000. PEG-LIP@OMC is capable of loading DOX. The PEG-LIP@OMC showed high efficiency for the conversion of NIR laser into heat. Moreover, in vitro studies using MCF-7 cells demonstrated that this NIR-responsive DDS enabled on-demand drug release, presumably by heat-induced disruption of the PEG-liposomes. Most importantly, under NIR laser irradiation, chemo-photothermal synergistic therapy was realized. This phospholipid coating based multifunctional delivery system was facile, stable, biocompatible, and highly-effective, which provided an important addition to therapy tools. We believe that this developed multifunctional nanocomponent will greatly advance the application of OMC for cancer therapy in the near future.
Declaration of competing interest
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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
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This work was financially supported by the National Natural Science Foundation of China (Nos. 21735002, 21521063, 21675046, 21874035, 21806186 and 21775036), the Natural Science Foundation of Hunan Province, China (No. 2018JJ2033), and the Key Point Research and Invention Program of Hunan Province, China (No. 2017DK2011).
Appendix A. Supplementary data
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Supplementary material related to this article can befound, in the online version, at doi: https://doi.org/10.1016/j.cclet.2020.04.035.
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Year 2020 volume 31 Issue 12
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doi: 10.1016/j.cclet.2020.04.035
  • Receive Date：2020-03-04
  • Online Date：2026-01-31
  • Published：2020-12-15
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  • Received：2020-03-04
  • Revised：2020-04-20
  • Accepted：2020-04-21
Affiliations
    State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Biology, College of Chemistry and Chemical Engineering, Hunan University, State Key Laboratory for Bio-Nanotechnology and Molecular Engineering of Hunan Province, Changsha 410082, China
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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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