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SCIENCE CHINA Chemistry, Volume 61, Issue 10: 1243-1260(2018) https://doi.org/10.1007/s11426-018-9297-5

Theranostic nanomedicine by surface nanopore engineering

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  • ReceivedApr 24, 2018
  • AcceptedMay 27, 2018
  • PublishedAug 8, 2018

Abstract

Theranostic nanomedicine that integrates diagnostic and therapeutic agents into one nanosystem has gained considerable momentum in the field of cancer treatment. Among diverse strategies for achieving theranostic capabilities, surface-nanopore engineering based on mesoporous silica coating has attracted great interest because of their negligible cytotoxicity and chemically active surface that can be easily modified to introduce various functional groups (e.g., −COOH, −NH2, −SH, etc.) via silanization, which can satisfy various requirements of conjugating biological molecules or functional nanoparticles. In addition, the nanopore-engineered biomaterials possess large surface area and high pore volume, ensuring desirable loading of therapeutic guest molecules. In this review, we comprehensively summarize the synthetic procedure/paradigm of nanopore engineering and further broad theranostic applications. Such nanopore-engineering strategy endows the biocompatible nanocomposites (e.g., Au, Ag, graphene, upconversion nanoparticles, Fe3O4, MXene, etc.) with versatile functional moieties, which enables the development of multifunctional nanoplatforms for multimodal diagnostic bio-imaging, photothermal therapy, photodynamic therapy, targeted drug delivery, synergetic therapy and imaging-guided therapies. Therefore, mesoporous silica-based surface-nanopore engineering integrates intriguing unique features for broadening the biomedical applications of the single mono-functional nanosystem, facilitating the development and further clinical translation of theranostic nanomedicine.


Funded by

the National Key R&D Program of China(2016YFA0203700)

the National Natural Science Foundation of China(51722211,51672303,81472284,81672699)

the Program of Shanghai Academic Research Leader(18XD1404300)

Young Elite Scientist Sponsorship Program by CAST(2015QNRC001)


Acknowledgment

This work was supported by the National Key R&D Program of China (2016YFA0203700), the National Natural Science Foundation of China (51722211, 51672303, 81472284, 81672699), the Program of Shanghai Academic Research Leader (18XD1404300) and Young Elite Scientist Sponsorship Program by CAST (2015QNRC001).


Interest statement

The authors declare that they have no conflict of interest.


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  • Scheme 1

    Schematic illustration of surface nanopore engineering onto different functional nanosystems, including UCNPs, AgNPs, Fe3O4, 2D MXenes, 2D MoS2, 2D graphene, AuNPs, CuxS, etc, and the theranostic applications of these multifunctional nanoplatforms following surface nanopore engineering, including targeted drug therapy, multimodal imaging, photo-therapy, radiation, multi-therapies and theranostic nanomedicine (color online).

  • Figure 1

    One-pot strategy of surface nanopore engineering onto the surface of AuNRs. (a) TEM image and (b) SEM image of mesoporous silica-coated AuNRs. TEM images of mesoporous silica-coated AuNRs after (c) 1 h, (d) 10 h, and (e) 500 h reaction durations [70].

  • Scheme 2

    Schematic illustration of facile one-pot strategy of surface nanopore engineering. (a) Mesopore coating onto the surface of hydrophobic Fe3O4 NPs, and (b) hydrophilic Ti3C2 nanosheets [89,90].

  • Figure 2

    Surface nanopore engineering of Fe3O4 and CuS. (a) Schematic route of the synthesis of Fe3O4@mSiO2-TPP/CDs nanoplatform. (b) TEM image of the Fe3O4 NPs. The inset shows the corresponding SAED pattern. (c) TEM image of Fe3O4@mSiO2 NPs. (d) Schematic illustration for the synthetic procedure of CuS@mSiO2-TD/ICG. (e) TEM image of CuS NPs. (f) TEM images of CuS@mSiO2 NPs. (g) Energy dispersive X-ray (EDX) elemental mapping analysis of core-shell CuS@mSiO2 NPs and corresponding elemental mappings of Si, S and Cu, respectively [91,92] (color online).

  • Figure 3

    Synthesis and characterization of GO-PMS. (a) Schematic representations of a CTAC head group (left) and an admicelle (right) on a GO surface and (b) proposed mode of the formation of GO-PMS. (c) SEM images of GO-PMS (0.27) prepared at pH 11.7, and the hexagonal array with interpore distance (5.4 nm). (d) STEM pictures of GO-PMS prepared at pH 11.7, clearly showing GO sheets sandwiched by arrays of vertically aligned mesopores with the height of 20–30 nm [93] (color online).

  • Figure 4

    Surface nanopore engineering of 2D nanosheets including graphene and MoS2. (a) Schematic illustration of the synthesis of mesoporous silica-coated graphene (GS) nanosheets. (b) Small-angle XRD pattern and (c–e) HRTEM and TEM images of GS. (f) Synthesis procedure of MoS2@SiO2 (PSMS). (g) AFM image of PSMS-NH2 (scale bar=300 nm) (h) TEM image and (i) corresponding elemental maps of PSMS-NH2 (scale bar=100 nm) [69,96] (color online).

  • Figure 5

    Surface nanopore engineering of UCNPs for multimodal imaging. (a) Schematic illustration for the synthesis of UCS-Balls. (b, c) Trimodal images of mice bearing a Walker 256 tumor using UCS-Balls: pre-injection (left), post-injection (right). At the top: pre- and post-injection fluorescence imaging; in the middle: pre- and post-injection MR imaging; At the bottom: pre- and post-injection CT imaging. In MRI, area-1 and area-2 are for the background and tumor site, respectively. In CT imaging, area-1 and area-2 are for the tumor and soft tissue sites, respectively [99] (color online).

  • Figure 6

    Multifunctional nanoprobes (PEGylated UCNPs@TEMPO@SiO2 nanocomposites) for upconversion luminescence and magnetic resonance dual-modality imaging. (a) Schematic illustration for the synthesis of PEGylated UCNP@TEMPO@SiO2 nanocomposite. (b) T1-weighted MR images (upper) of PEGylated UCNP@TEMPO@SiO2 nanocomposites as a function of TEMPO radical concentration (mM) in aqueous solution (9.4 T, 25 °C) and T1-weighted MR images (lower) of HeLa cells treated with PEGylated UCNP@TEMPO@SiO2 nanocomposites at different concentrations (0, 40, 80, 120, 160 and 200 mg/mL) for 6 h at 37 °C. (c) In vivo T1-weighted coronal MR images of the whole body (c1, c2) and the transversal cross-sectional images of the liver (c3, c4) of mice at pre-injection and at 30 min post-injection of PEGylated UCNP@TEMPO@SiO2 nanocomposites [101] (color online).

  • Figure 7

    Surface nanopore engineering of magnetic Fe3O4 for multimodal imaging. (a) A schematic illustration of the synthesis of WS2-IO/S@MO-PEG. (b) T1 and T2-weighted MR images of WS2-IO/S@MO-PEG solutions at different pH as recorded on a 3T MR scanner, and the T1/T2 signal intensity ratios of WS2-IO/S@MO-PEG measured under different pH. (c) In vivo T1 and T2 MR images of a mouse before and 24 h post i.v. injection of WS2-IO/S@MO-PEG. (d) T1 and T2 MR images of a mouse before and after local injection of WS2-IO/S@ MO-PEG within its muscle (left) or tumor (right). (e) Quantification analysis of T1/T2 signals in muscle and tumor before and after injection of WS2-IO/S@MO-PEG based on images in (d) [102] (color online).

  • Figure 8

    Surface nanopore engineering of Fe3O4 for MRI-guided synergistic targeted therapy. (a) Schematic representation of multifunctional Fe3O4@mSiO2-FA-CuS-PEG core-shell nanocomposites. (b1, b2) Low- and high-magnification TEM images of Fe3O4@mSiO2 NPs. (b3, b4) Low- and high-magnification TEM images of Fe3O4@mSiO2-FA-CuS-PEG nanocomposites. (c) T2-weighted MRI photographs of Fe3O4@mSiO2-FA-CuS-PEG nanocomposites at different Fe concentrations. (d) T2 relaxation rate of Fe3O4@mSiO2-FA-CuS-PEG nanocomposites as a function of Fe concentration. The insets are the photographs illustrating that the synthesized Fe3O4@mSiO2-FA-CuS-PEG nanocomposites could be collected from the dispersion by an external magnet in 30 s [103] (color online).

  • Figure 9

    Surface nanopore-based targeted delivery nanosystems of graphene. (a) Design of GSPID as a multifunctional drug delivery system for combined chemo-photothermal targeted therapy. (b–e) Confocal microscopy of glioma cells via live-dead staining. BF: bright field images. Green: live cells. Red: dead cells. Scale bar=75 μm. Confocal microscopy images of GSPD (f) and GSPID (g) incubated with U251 cells and 1800 cells for 30 min. Red: DOX. Scale bar=75 μm. (h) Cytotoxicity of GSPD and GSPID incubated with U251 cells and 1800 cells for 6 h [69] (color online).

  • Figure 10

    Surface nanopore engineering of targeted delivery nanosystems of 2D MXene. (a) Amination of Ti3C2@mMSNs. (b) PEGylation of Ti3C2@mMSNs-NH2. (c) RGD conjugation of Ti3C2@mMSNs-PEG. (d) CLSM images of SMMC-7721 cells incubated with FITC-labeled Ti3C2@mMSNs for 2, 4 and 8 h. The nucleus of SMMC-7721 cells were stained by DAPI (blue). FITC fluorescence from Ti3C2@mMSNs in cells was green, including (1): Ti3C2@mMSNs-PEG, (2): Ti3C2@mMSNs-RGD, (3): Ti3C2@mMSNs-RGD+free RGD. (All scale bars: 50 μm). (e) Bio-distribution of Si (% ID of Si per gram of tissues) in main tissues and tumor after intravenous administration of Ti3C2@mMSNs-RGD dispersed in PBS for varied time intervals (4, 8 and 24 h,m=3) [89] (color online).

  • Figure 11

    Surface nanopore engineering of MoS2 (MoS2−PMS) for synergistic chemo-PTT. (a) NIR-responsive temperature elevation of nanoplates. (b) Photo-responsive drug release of DOX from DOX-PSMS-PEG in vitro. (c) Confocal microscopic images of DOX-PSMS-PEG treated HeLa cells, which was further irradiated or not irradiated by 808 nm laser (5 W/cm2). The cell nucleus was stained by DAPI (blue) and DOX was false-imaged as red. (Scale bar=50 μm). (d) Schematic illustration of photo-thermally assisted endosomal escape for effective drug release. NIR-induced cytotoxicity of DOX-PSMS-PEG or PSMS-PEG against (e) HeLa and (f) MCF-7 cancer cells. [96] (color online).

  • Figure 12

    Surface nanopore engineering of Au (Au@mSiO2) for combating chemotherapeutic resistance of cancer cells via PTT process. (a) Mechanism of fs-pulsed laser irradiation on combating drug resistance with the aid of a multifunctional nanocarrier (Au@SiO2) and triggered photothermal effects. (b) Dose and time-dependent effects of Au@SiO2-DOX on MCF-7/ADR cell viability. (c) Thermal effects of both nanocarriers on cell viabilities 24 h post-irradiation. (d) The influence of thermal treatment on both the transcription level (mRNA) of key resistance-related genes, including HSF-1, TP53, and MDR-1, and the expression of major resistance-related proteins such as p53 and Pgp after NIR irradiation [111] (color online).

  • Figure 13

    Synergistic PDT and PTT by surface nanopore engineering of AuNRs. (a) Design of enhanced PDT by utilizing the surface plasmonic effect of AuNRs to simultaneously increase the absorption coefficient and reduce photo-degradation of the photodynamic dye ICG. Mesoporous silica provided the photo-protection for ICG by facilitating the formation of ICG aggregates. The double photo-protection would significantly enhance the stability of loaded ICG in comparison with the single photo-protection of silica shell. (b) Infrared thermal images (at the 3 min time point) of orthotopic breast tumors in nu/nu mice after irradiation with an 808 nm NIR laser 24 h after intravenous injection of Au@SiO2-ICG and various control reagents. (c) Tumor growth in nu/nu mice after various treatments [118] (color online).

  • Figure 14

    Theranostic AuNRs@mSiO2 nanoplatform. (a) Schematic illustration of mesoporous silica-coated AuNRs (AuNRs@SiO2) as a novel multifunctional theranostic platform for cancer treatment. Time- and dose-dependent effects of (b) DOX, (c) AuNRs@SiO2-DOX. (d) The effects of NIR laser irradiation on lysosomal membrane integrity as determined by acridineorange (AO) staining. AuNRs@SiO2-DOX-untreated A549 cells were used as control and irradiated by a NIR laser, and AuNRs@SiO2-DOX (containing 5 M DOX)-treated cells are irradiated by laser at two different power densities, 24 and 48 W/cm2 for 0, 3, and 8 min. (e) Differences in viability of A549 cells as irradiated by NIR laser for 8 min (AuNRs@SiO2) and for 3, 4, and 8 min (AuNRs@SiO2-DOX) [112] (color online).

  • Figure 15

    Theranostic Janus AuNR@mSiO2 nanoplatforms. (a) Schematic illustration of the application of DOX-loaded Au-mesoporous silica Janus NPs and their application for synergetic chemoradiotherapy and CT imaging in HCC theranostics. (b) TEM images of FA-GSJNs. (c) In vivo CT images of SMMC-7721 tumor-bearing nude mice at 24 h post-injection with FA-GSJNs-DOX or GSJNs-DOX. (d) Tumor-weight of different treatment groups. (e) Tumor photograph at the end of the treatments [125] (color online).

  • Figure 16

    Theranostic Fe3O4@Au@mSiO2 nanoplatforms. (a) Schematic illustration of the synthetic process of Fe3O4@Au@mSiO2-dsDNA/DOX NPs for synergistic in vivo chemotherapy and PTT in a magnetic-targeting manner. (b) The T2-weighted MR images of tumor-bearing mice after receiving Fe3O4@Au@mSiO2-dsDNA/DOX. The images were captured on pre-injection and post-injection 30 min. White arrows indicate the location of tumor. (c) Tumor growth curves of different treatment groups. Tumor sizes were normalized to their initial sizes [129] (color online).

  • Figure 17

    Double-mesoporous core-shell nanosystems (mPt@mSiO2-GdDTPA) for in vivo MRI and PTT. (a) The synthestic process of mPt@mSiO2-GdDTPA nanosystems and their applications for in vivo MR imaging and PTT. (b) TEM image of mPt-mSiO2-GdDTPA and the corresponding elemental mapping images (elemental color distribution). (c) Viabilities of HeLa cells incubated with different concentrations of mPt@mSiO2-GdDTPA under 808 nm laser irradiation for 10 min. (d) In vivo T1-weighted MR images of Kunming mice after the tail intravenous injection for varied time periods of liver. The red dashed circles represent the region of liver [136] (color online).

  • Figure 18

    Theranostic PEG-UCNPs@SiO2-SNO for X-ray-controlled NO release. (a) Construction of PEG-UCNPs@SiO2-SNO for X-ray-controlled NO release. (b) TEM and (c) SEM images of UCNPs@SiO2. (d–f) The corresponding element mapping of UCNPs@SiO2: (e) Si; (f) Y. (g) X-ray-triggered NO release from PEG-UCNPs@SiO2-SNO in zebrafish larvae, and CLSM images of NO release in living zebrafish larvae with brain ventricle microinjection of PEG-UCNPs@SiO2-SNO upon exposure to different doses of X-ray radiation: (g1) 0 Gy, (g2) 1 Gy, (g3) 3 Gy, (g4) 5 Gy and (g5) 10 Gy. (h) Relative tumor growth curve and of 4T1 tumor-bearing mice over half a month after different treatments [137] (color online).

  • Figure 19

    Multifunctional UCNP-based nanoradiosensitizer with high hypoxia-specific and radiosensitive cytotoxicity to substantially enhance the radiotherapeutic efficacy on solid tumors. (a) Schematic diagram of synthesizing UCNPs with hollow, mesoporous silica outer shells (UCHMs), through (I) the water-in-oil reverse microemulsion strategy, (II) the aqueous phase regrowth method, and (III) the hot-water selective etching method. dSiO2=dense silica. (b) Immunofluorescence assay after MAb1, which could bind to protein, peptide, and amino acid adducts of 2-nitroimidazole in hypoxic cells, was added to tumor tissue sections: red regions are hypoxic tissues at (i–iii) 100 original magnification and (iv–vi) 200 original magnification. Hypoxic cells in tumors are marked with 2-nitroimidazole prior to immunofluorescence. (c) Western blot analysis of the expressions, in HeLa cells, of the Snail transcription factor, and of the GLUT1 glucose transporter, under normoxia (pO2: 21%) or hypoxia (pO2: 2%), after treatments: i, PBS; ii, UCHMs; iii, TPZ@UCHMs+RT. Actin was used as loading control. (d) Time-dependent tumor growth curves of different groups of mice under various treatments in vivo. The data confirm the hypoxia-specific synergistic effects of RT following injection of TPZ@UCHMs [138] (color online).

  • Figure 20

    Summary of the development and current applications of surface nanopore engineering strategy in theranostic nanomedicine, and future prospect of improving the efficacy of such a strategy for further potential clinical translation (color online).

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