Strategies to assemble therapeutic and imaging molecules into inorganic nanocarriers
Sheikh Tanzina HAQUE1, Mark M. BANASZAK HOLL2, Ezharul Hoque CHOWDHURY1,3()
1. Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway, 47500 Subang Jaya, Selangor, Malaysia 2. Department of Chemical and Biological Engineering, Monash University, Clayton, Victoria 3800, Australia 3. Health and Wellbeing Cluster, Global Asia in the 21st Century (GA21) Platform, Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway, 47500 Subang Jaya, Selangor, Malaysia
Inorganic nanocarriers are potent candidates for delivering conventional anticancer drugs, nucleic acid-based therapeutics, and imaging agents, influencing their blood half-lives, tumor targetability, and bioactivity. In addition to the high surface area-to-volume ratio, they exhibit excellent scalability in synthesis, controllable shape and size, facile surface modification, inertness, stability, and unique optical and magnetic properties. However, only a limited number of inorganic nanocarriers have been so far approved for clinical applications due to burst drug release, poor target specificity, and toxicity. To overcome these barriers, understanding the principles involved in loading therapeutic and imaging molecules into these nanoparticles (NPs) and the strategies employed in enhancing sustainability and targetability of the resultant complexes and ensuring the release of the payloads in extracellular and intracellular compartments of the target site is of paramount importance. Therefore, we will shed light on various loading mechanisms harnessed for different inorganic NPs, particularly involving physical entrapment into porous/hollow nanostructures, ionic interactions with native and surface-modified NPs, covalent bonding to surface-functionalized nanomaterials, hydrophobic binding, affinity-based interactions, and intercalation through co-precipitation or anion exchange reaction.
Results with drug loaded nanocarriers vs. free drugs
Refs.
PEI/PEG/MSNs
Trastuzumab
In trastuzumab-resistant HCC1954 xenografts, single dosage of siHER2–NPs significantly decreased (60%) HER2 protein levels. Treatment with multiple intravenous doses over three weeks resulted in a marked reduction in tumor growth. Trastuzumab (10 mg·kg?1) administered intraperitonially, trastuzumab (5 mg·kg?1) injected via tail vein, and trastuzumab (5 mg·kg?1) and paclitaxel (3.1 mg·kg?1) injected via tail vein showed a reduced efficacy in suppressing tumor progression in HCC1954 tumor-bearing mice.
[54]
C60@Au-PEG
DOX
1. In contrast to the DOX group, C60@Au-PEG/DOX (amide bond), and C60@Au-PEG/DOX (hydrazone bond) exhibited significant levels of DOX in the blood after injection, suggesting that C60@Au-PEG/DOX (amide bond) and C60@Au-PEG/DOX (hydrazone bond) prolonged DOX circulation time in the blood in S180 tumor-induced female BALB/c mice.2. In comparison to DOX, C60@Au-PEG/DOX (amide bond) and C60@Au-PEG/DOX (hydrazone bond) markedly lowered the accumulation of DOX in the heart and spleen, decreasing the adverse effects of DOX on heart and spleen.3. The relative tumor volume (V/V0) of DOX was 2.7±0.26 compared to 1.9±0.21 for C60@Au-PEG/DOX, indicating that more DOX could potentially enter the tumor site with C60@Au-PEG.
[69]
PEI-PEG-MSNs
DOX
Dox and P-gp siRNA loaded PEI-PEG-MSNs complex in MCF-7/MDR tumor-bearing xenograft model demonstrated greater accumulation in the tumor as a result of prolonged blood circulation, leading to 80% of tumor growth suppression in comparison to free DOX (17%), MSN-DOX (62%) and P-gp siRNA (0%).
[60]
CPNPs
Cer10
MTS cytotoxicity assay demonstrating dosage responsive cytotoxic actions of Cer10-CPNPs compared to control CPNPs which exhibit modest cytotoxicity at the highest particle number concentration and Cer10 in UACC 903 melanoma cells.
[67]
MSN@Gelatin
DOX
For DOX/MSN@Gelatin, a dose-dependent cytotoxicity was recorded (IC50 = (17.27±0.63) μg·mL?1) in Hep-G2 cells, which was higher than that of free DOX. On the contrary, minimal toxicity (IC50 > 100 μg·mL ?1) was observed for MSN@Gelatin.
[58]
PEG-SWCNTs
PTX
In vitro PTX-PEG-SWCNTs showed higher efficacy in suppressing tumor growth compared to PTX alone in a murine 4T1 breast cancer model, owing to prolonged blood circulation and 10-fold higher tumor PTX uptake by SWNT delivery through enhanced permeability and retention (EPR).
[123]
MSNs-capped MMP9
Cisplatin, Bz
1. Cisplatin and Bz-loaded MSNs capped with MMP9 were found to cause significant cell apoptosis in human tumor cells and mouse and human lung tumors. The lowest cisplatin dose (2 μmol·L?1) had the most enhanced cytotoxicity, increasing by over 35% in the presence of Bz. It represents an increase in cytotoxic potency of 5- to 10-fold for nontoxic doses of a single drug. These findings demonstrated that cisplatin and Bz delivered together via NPs were additively cytotoxic, enabling a reduction in drug dosage.2. Kras mutant mouse 3D-LTC treated with free (nonencapsulated) drug(s) induced apoptosis with no distinction between tumorous and nontumorous tissues.
[87]
PEG-CA and biotinylated PEG-fibronectin-CA
Gemcitabine, anastrozole
1. HPLC revealed that cellular uptake of gemcitabine and anastrozole was higher in breast cancer cells for the surface-modified NPs than CA and free drugs.2. In the cytotoxicity study, surface modified NPs showed greater toxicity than unmodified CA NPs and free gemcitabine and anastrozole.3. Tumor regression study using surface-modified gemcitabine-encapsulated NPs revealed dramatic shrinkage of tumors compared to free gemcitabine.
[90]
LDH
MTX
The antitumor effects of intact MTX (30 mg·kg?1) and MTX-LDH (75 mg·kg?1 was equivalent to 30 mg·kg?1 MTX) using HOS-bearing xenograft mice models demonstrated that MTX-LDH treated tumors were considerably smaller than intact MTX.
[105]
LDH
5-Fu
The 5-fluorouracil-LDH (5-Fu–LDH) revealed sustained release, prolonged half-life, and increased distribution of 5-Fu in tumors in comparison to free 5-Fu.
In biodistribution experiments with xenografted mice, the tumor-to-blood ratio of BSH in the BSH-LDH (boron delivery system) treated group was shown to be 4.4 times greater than in the intact BSH treated group 2 h after drug administration.
[113]
Ferrous ions doped MgAl-LDH (Fe-LDH)
DOX
Tumor growth in 4T1 bearing mice was suppressed following treatment of PTT and chemotherapy with Fe-LDH/DOX compared to free DOX.
[114]
Pt-PEG-GNRs
Cisplatin
In comparison to free cisplatin, cytotoxicity analyses (MTT assay) revealed increased toxicity for cervical cancer HeLa cells, human lung carcinoma A549 cells and human breast adenocarcinoma MCF-7 cells, with IC50 values around 9 to 65 fold lower.
[135]
TCL-SPION
DOX
In vivo studies showed more significant tumor growth suppression with DOX@TCL-SPIONs than mice treated with 5% glucose, TCL-SPION, DOX (0.64 mg·kg?1), and DOX (5 mg·kg?1).
[138]
CaCO3
DOX
The in vitro chemosensitivity test utilizing MTT, modified neutral red/trypan blue assay, and LDH were used to demonstrate that CaCO3/DOX nanocrystals could mitigate tumor cell growth more than free DOX.
[140]
Mesoporous CaCO3
Etoposide
The MTT assay showed that etoposide-loaded mesoporous CaCO3 inhibited SGC-7901 cells more effectively and lessened the toxic effects of etoposide in HEK 293 T cells compared with free etoposide.
[142]
α-Ketoglutaric acid-modified CA
AZ628 (Raf-kinase inhibitor)
The MTT assay on MCF-7 and 4T1 cells showed that the %cytotoxicity of AZ628-loaded α-KAMCA NPs was substantially greater than that of AZ628-loaded CA NPs, and only AZ628 at similar doses. In MCF-7 and 4T1 cells, AZ628-loaded α-KAMCA NPs displayed around 9% and 12% higher cytotoxicity, respectively, than AZ628-loaded CA NPs, and a 30% greater cytotoxic efficacy compared to free drugs.
[150]
Citrate-modified CA and α-ketoglutaric acid-modified CA
CYP, DOX
1. Compared with CYP alone, the antitumor efficacy of the group treated with CYP-loaded α-ketoglutaric acid-modified CA NPs showed a five-fold reduction in tumor growth in murine breast cancer models. In addition, the CYP-loaded NPs accumulated more in the tumor than free CYP.2. Biodistribution studies showed less accumulation of DOX-loaded NPs in the heart than free DOX, suggesting their effectiveness in attenuating cardiotoxicity in mice. These findings indicated that both citrate-modified CA and α-ketoglutaric acid-modified CA carriers could prolong the circulation time, increase the antitumor effect, and abate the toxicity of the chemotherapeutic drugs in healthy tissues.
[148]
Citrate-modified CA
DOX
In MCF-7 cells, citrate-modified CA enhanced the cellular uptake and had a half-maximal inhibitory concentration 1000 times lower than free DOX.
[151]
Fe-PEI NPs
Cisplatin
Fe-PEI NPs loaded cisplatin could more effectively suppress cancer cell growth (in vitro and in vivo) than free cisplatin.
[163]
Anti-EGFR-TCS-GNSs
PTX
In MDA-MB-231 cells, the anti-EGFR-PTX-TCS-GNSs + laser irradiation group induced 81.9% apoptosis. In comparison, the photothermal therapeutic potencies of free PTX, PTX-TCSGNSs, and anti-EGFR-PTX-TCS-GNSs were 25.45%, 17.15%, and 13.27%, respectively. The anti-EGFR-PTX-TCS-GNSs + laser irradiation group demonstrated a 100% survival rate over a period of 34 d, compared to all other groups. In addition, antibody-decorated conjugates uptake was four times than that of non-targeted samples after 5 h of treatment, demonstrating the receptor-mediated internalization of anti-EGFR-PTX-TCS-GNS.
[181]
Lysine/SWCNTs
DOX
The inhibition of tumor growth on SMMC-7721 cells and the sarcoma 180-bearing mice was significantly enhanced after treatment with DOX-lysine/SWCNTs in near-infrared laser light at 808 nm. A dramatic rise in body weight, food and water intake, and mental state was noticed in sarcoma 180 tumor-induced mice on DOX-lysine/SWCNTs treatment compared to free DOX.
[208]
Mn@CaCO3-loaded PD-L1-targeting siRNA
ICG
In Lewis lung cancer cells, Mn@CaCO3/ICG-loaded PD-L1-targeting siRNA increased the PDT effect in vitro. Furthermore, in vivo tests revealed that this nanoplatform was capable of transporting the cargos to the tumor and inhibit tumor growth more efficiently than free ICG.
[218]
PEI/PEG/MSNs
DOX
Using near-infrared fluorescence imaging and elemental Si analysis, the human squamous carcinoma xenografts in nude mice after intravenous injection revealed passive accumulation of 12% of the tail vein-injected PEI/PEG/MSNs at the tumour site, indicating successful cellular internalization and DOX delivery to KB-31 cells. The resultant NPs showed apoptosis and tumor shrinkage that was greater than that of free DOX.
[219]
F-FMSNs
CPT
In tumor regression study using nude mice induced with MCF-7 cells, administration of CPT suppressed tumor growth by 14% at the end of the study (the 68th day) compared to control, indicating that it is an efficient tumor-suppressing agent when dissolved in DMSO. In contrast, from day 48 on, the average tumor volumes in groups treated with CPT-loaded FMSN or CPT-loaded F-FMSN continued to decrease at a faster rate.
[220]
ZnO-Au-PLA-GPPS-FA-1 and ZnO-Au-PLA-GPPS-FA-2
CPT
The CPT-loaded nanocarriers were more cytotoxic to Hela cells at the same concentration of up to 75 μg·mL?1 for ZnO-Au-PLA-GPPS-FA-1 and ZnO-Au-PLA-GPPS-FA-2 nanocarriers, containing about 4.7 and 6.5 μg·mL?1 free CPT in both systems, respectively. Despite the same levels of CPT, the inhibition rates of the CPT-loaded nanocarriers were greater than those of the free CPT.
[221]
ZnO
DOX
The cytotoxicity study showed that DOX-loaded ZnO NPs had a greater anticancer effect than either blank ZnO NPs or DOX alone.
[222]
LDH
RH
The MTT assay reveals that RH-LDHs delivered drugs more effectively to cancer cells cancer cells compared to pure RH due to pure RH’s poor bioavailability.
[223]
LDH
MTX
The half maximal inhibitory concentration of MTX-LDH (48 h) suggested that MTX-LDH had improved efficacy and sensitivity in human colon cancer cells HCT-116. In comparison, naked MTX took 72 h to achieve similar outcomes.
[224]
Carboxylate-modified MgAl LDH
Cisplatin
The anti-proliferative effect of cisplatin-conjugated carboxylate-modified MgAl LDH on colon cancer cell lines was stronger than that of the free drug, according to in vivo data.
[225]
NaCa-LDH
DAC
On malignant (A-375) melanoma and breast cancer (MCF-7) cell lines, the anticancer activity of DAC-NaCa-LDH is higher than that of free DAC.
[226]
PLGA-coated MgAl LDH (PLGA-LDH)
MTX
Greater therapeutic efficacy was observed with PLGA-LDH-MTX than that of the bare MTX, according to in vitro and in vivo experiments.
[227–228]
FA-modified nanocarrier based on the self-assembly of delaminated CoAl LDH and MnO2
DOX, PTX
Based on both in vitro cytotoxicity studies and a xenograft tumor model of hepatoma, this nanocarrier was more effective in fighting cancer than either the free drugs alone or the corresponding cocktail solutions.
[229]
GE11-Se NPs
Ori
GE11-Ori-Se NPs caused a larger level of ROS in KYSE-150 cells than oridonin or Chi-Se NPs, implying that the combination of Chi-Se NPs and oridonin synergistically increased intracellular ROS levels in KYSE-150 cells, increasing the anticancer activity.
[230]
FA-QD
DOX
1. Fluorescence microscopy and the MTT assay revealed that the folate-targeted DOX-QD NPs exhibit greater toxic effects than non-targeted NPs and the free DOX, demonstrating their preferential accumulation in 4T1 and MCF-7 cells in vitro.2. The in vivo tumor inhibitory impact of FA-QD-DOX NPs revealed that the targeted formulation outperformed the non-targeted formulation and free DOX in terms of therapeutic efficacy.
The platin-Au-Fe3O4-Herceptin NPs serve as nanocarriers for the targeted delivery of platin into Her2-positive breast cancer cells (Sk-Br3). The half-maximal inhibitory concentration (IC50) of platin-Au-Fe3O4-Herceptin NPs against Sk-Br3 cells is 1.76 μg of Pt/mL, which is significantly less than the 3.5 μg·mL?1 required for cisplatin.
[232]
Au NPs with a PEG spacer linked via an acid-labile linkage (DOX-Hyd@AuNPs)
DOX
When compared to free DOX, DOX-Hyd@AuNPs boosted drug accumulation and retention in multidrug-resistant MCF-7/ADR cancer cells, resulting in higher toxicity and greater apoptosis in MCF-7/ADR cancer cells.
[233]
MSA-capped gold nanoconstructs loaded with SMI#9 (Rad6 protein inhibitor)
Cisplatin
In vitro, the effective dose of cisplatin required to suppress the development of 50% of cancer cells (4.9 μmol·L?1) was about five times lower than free cisplatin (> 25 μmol·L?1).
[234]
Calcium phosphate-polymer hybrid with inhibitors for microRNA-221 and microRNA-222
pac
MTS assay was used to evaluate the cytotoxic efficacy of pac-encapsulated NPs (NP(pac)), co-delivery NPs (NP(pac/miRi) or NP(pac/miRi NC)), and free pac in MDA-MB-231 cells after 72 h. The difference between the encapsulated form (NP(pac)) and the free form of pac in terms of cell viability was small. At a high dosage of 0.67 μg·mL?1, pac reduced cell viability by 40%. At the same dosage of 0.67 μg·mL?1, the cell viability of NP(pac/miRi) decreased by 80%. The cytotoxicity evaluation at a broader range of concentrations demonstrated that the NP(pac/miRi) only needed 1% of the pac in the free form to produce the same cytotoxicity (around 80%).
[235]
PEGylated Au NP
Pc 4
The in vivo drug delivery period for PDT has been lowered to less than 2 h with the Au NP-Pc 4 conjugates, compared to 2 d with the free Pc 4 conjugates.
[236]
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