Precise nanomedicine for intelligent therapy of cancer

Huabing Chen; Zhanjun Gu; Hongwei An; Chunying Chen; Jie Chen; Ran Cui; Siqin Chen; Weihai Chen; Xuesi Chen; Xiaoyuan Chen; Zhuo Chen; Baoquan Ding; Qian Dong; Qin Fan; Ting Fu; Dayong Hou; Qiao Jiang; Hengte Ke; Xiqun Jiang; Gang Liu; Suping Li; Tianyu Li; Zhuang Liu; Guangjun Nie; Muhammad Ovais; Daiwen Pang; Nasha Qiu; Youqing Shen; Huayu Tian; Chao Wang; Hao Wang; Ziqi Wang; Huaping Xu; Jiang-Fei Xu; Xiangliang Yang; Shuang Zhu; Xianchuang Zheng; Xianzheng Zhang; Yanbing Zhao; Weihong Tan; Xi Zhang; Yuliang Zhao

doi:10.1007/s11426-018-9397-5

SCIENCE CHINA Chemistry

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SCIENCE CHINA Chemistry, Volume 61, Issue 12: 1503-1552(2018) https://doi.org/10.1007/s11426-018-9397-5

Precise nanomedicine for intelligent therapy of cancer

Huabing Chen¹, Zhanjun Gu², Hongwei An^2,3, Chunying Chen^3,4, Jie Chen^5,6,7, Ran Cui⁸, Siqin Chen⁹, Weihai Chen¹⁰, Xuesi Chen^5,6,7, Xiaoyuan Chen¹¹, Zhuo Chen¹², Baoquan Ding³, Qian Dong¹², Qin Fan¹³, Ting Fu¹², Dayong Hou³, Qiao Jiang³, Hengte Ke¹, Xiqun Jiang¹⁴, Gang Liu¹⁵, Suping Li³, Tianyu Li¹⁶, Zhuang Liu¹³, Guangjun Nie³, Muhammad Ovais^3,4, Daiwen Pang⁸, Nasha Qiu⁹, Youqing Shen⁹, Huayu Tian^5,6,7, Chao Wang¹³, Hao Wang³, Ziqi Wang³, Huaping Xu¹⁶, Jiang-Fei Xu¹⁶, Xiangliang Yang¹⁷, Shuang Zhu², Xianchuang Zheng¹⁴, Xianzheng Zhang¹⁰, Yanbing Zhao¹⁷, Weihong Tan^12,18,*, Xi Zhang^16,*, Yuliang Zhao^3,*

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Affiliations：

1. State Key Laboratory of Radiation Medicine and Protection, Jiangsu Key Laboratory of Neuropsychiatric Diseases, College of Pharmaceutical Sciences, Soochow University, Suzhou 215123, China

2. Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China

3. CAS Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, CAS Center for Excellence in Nanoscience, National Center for Nanoscience and Technology of China, Beijing 100190, China

4. University of Chinese Academy of Sciences, Beijing 100049, China

5. Key Laboratory of Polymer Ecomaterials, Changchun Institute of Applied Chemistry, Chinese Academy of Sciences, Changchun 130022, China

6. University of Science and Technology of China, Hefei 230026, China

7. Jilin Biomedical Polymers Engineering Laboratory, Changchun 130022, China

8. Key Laboratory of Analytical Chemistry for Biology and Medicine (Ministry of Education), College of Chemistry and Molecular Sciences, State Key Laboratory of Virology, and Institute for Advanced Studies, Wuhan University, Wuhan 430072, China

9. Center for Bionanoengineering and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou 310027, China

10. Key Laboratory of Biomedical Polymers of Ministry of Education, Department of Chemistry, Wuhan University, Wuhan 430072, China

11. Laboratory of Molecular Imaging and Nanomedicine, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, MD 20892, USA

12. Molecular Science and Biomedicine Laboratory, State Key Laboratory of Chemo/Bio-Sensing and Chemometrics, College of Chemistry and Chemical Engineering, Aptamer Engineering Center of Hunan Province, Hunan University, Changsha 410082, China

13. Jiangsu Key Laboratory for Carbon-Based Functional Materials & Devices, Institute of Functional Nano & Soft Materials, Soochow University, Suzhou 215123, China

14. Department of Polymer Science and Engineering, College of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210093, China

15. State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics & Center for Molecular Imaging and Translational Medicine, School of Public Health, Xiamen University, Xiamen 361102, China

16. Department of Chemistry, Tsinghua University, Beijing 100084, China

17. National Engineering Research Center for Nanomedicine, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan 430074, China

18. Department of Chemistry and Department of Physiology and Functional Genomics, Center for Research at Bio/nano Interface, Health Cancer Center, UF Genetics Institute and McKnight Brain Institute, University of Florida, Gainesville, FL 32611-7200, USA

* Corresponding authors (email: tan@chem.ufl.edu; xi@tsinghua.edu.cn; zhaoyl@nanoctr.cn)

ReceivedNov 28, 2018
AcceptedNov 29, 2018
PublishedDec 7, 2018

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Abstract

Precise nanomedicine has been extensively explored for efficient cancer imaging and targeted cancer therapy, as evidenced by a few breakthroughs in their preclinical and clinical explorations. Here, we demonstrate the recent advances of intelligent cancer nanomedicine, and discuss the comprehensive understanding of their structure-function relationship for smart and efficient cancer nanomedicine including various imaging and therapeutic applications, as well as nanotoxicity. In particular, a few emerging strategies that have advanced cancer nanomedicine are also highlighted as the emerging focus such as tumor imprisonment, supramolecular chemotherapy, and DNA nanorobot. The challenge and outlook of some scientific and engineering issues are also discussed in future development. We wish to highlight these new progress of precise nanomedicine with the ultimate goal to inspire more successful explorations of intelligent nanoparticles for future clinical translations.

Funded by

the National Natural Science Foundation of China(11621505,11435002,31671016)

Acknowledgment

This work was supported by the National Natural Science Foundation of China (11621505, 11435002, 31671016).

Interest statement

The authors declare that they have no conflict of interest.

Contributions statement

These authors contributed equally to this work.

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Scheme 1
Schematic illustration of precise nanomedicine for intelligent therapy of cancer (color online).
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Figure 1
Illustration of novel approach to confine tumor using Gd@C₈₂(OH)₂₂ nanoparticles as emerging tumor caging agent for tumor imprisonment (color online).
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Figure 2
Schematic representation of the characteristics of supramolecular chemotherapy (color online).
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Scheme 2
Various nanoparticles for intelligent therapy of cancer discussed in this review (color online).
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Figure 3
Schematic representation of the therapeutic mechanism of nanorobot-Th within tumor vessels. (a) DNA origami sheet is prepared by annealing the mixture of M13 DNA scaffold and staples strands. Thrombin molecules are arranged at four designated locations on the origami sheet. Addition of the fasteners and targeting strands results in the formation of thrombin-loaded, tubular DNA nanorobots with additional targeting aptamers at both ends. Closed nanorobot binds to tumor endothelial cells by recognizing the cell surface targeting protein, nucleolin, and the tube subsequently opens to expose the encapsulated thrombin. Thrombin induces a localized thrombosis by activating platelets and inducing fibrin generation. (b) DNA nanorobot-Thrombin was administrated to tumor xenografted mice by tail vein injection and targeted tumor-associated vessels to deliver thrombin. The nanorobot-Th binds to the vascular endothelium by recognizing nucleolin and opens to expose the encapsulated thrombin, which induces localized thromboses, tumor infarction and cell necrosis [6] (color online).
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Figure 4
Schematic illustration of assembly and release of GroEL-DOX and their mechanism of action in tumor cells. (a) DOX is loaded into GroEL and ATP triggers its release from cis and trans-ring of GroEL by causing a conformational change. (b) When GroEL-DOX gets to the tumor vasculature, it enters tumor microenvironment. It can attach to plectin, which is highly expressed on the tumor cells and since there is an augmented level of ATP, a conformational change occurs to GroEL and as a final step DOX is released. It can pass through the lipophilic cell membrane and penetrate into the cell nucleus and commence apoptosis [39] (color online).
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Figure 5
Diselenide-containing polymeric micelles loaded with Dox responded to γ-radiation as low as 5?Gy. (a) Schematic illustration of γ-radiation responsive release of Dox; (b) release profile of polymeric micelles under different doses of γ-radiation; (c) TEM figures showed morphology of polymeric micelles after different doses of γ-radiation [54] (color online).
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Figure 6
Tellurium-containing polymeric micelles respond to low concentration of ROS or low dose of γ-radiation [55] (color online).
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Figure 7
Schematic illustration of the design of in vivo self-assembled nanostructures in physiological environment, in which the building blocks and triggering factors are two important components (color online).
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Figure 8
The schematic illustration of the AIR effect of compound 1 in tumor site compared with compound 2, which was quickly excreted from the tumor [76] (color online).
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Figure 9
Schematic illustration of theranostic Ag₂S nanodots generated via albumin-templated nanoreactor method [126] (color online).
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Figure 10
Ferritin caging CuS nanoparticles for efficient cancer theranostics. (a) Synthetic process of Ferritin caging CuS nanoparticles (CuS-Fn NCs) via nanoreactor method; (b) TEM images of CuS-Fn NCs with negative staining; (c) UV-Vis absorbance spectra of Fn without iron, Fn and CuS-Fn NCs; (d) PET images of tumor bearing mice at 2, 4, 8, 20, and 24?h post-injection of CuS-Fn NCs; (e) tumor growth profiles of the mice suffering from different treatments [149] (color online).
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Figure 11
Schematic illustration of Prussian blue nanoparticles inside CCMV capsid [157] (color online).
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Figure 12
Schematic illustration of various nucleic acid-based nanostructures (color online).
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Figure 13
Assembly of the ET module (a) and the FT module (b); (c) mechanism of EDTD for catalytic signal enhancement of specific mRNA expression in living cells [170] (color online).
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Figure 14
Working principle of DNA engineered nanomachine. (a) Structural diagram of DNA-logic gate TP nanomachine, which contains reporter toe, recognition toe 1, recognition toe 2 and DNA TP scaffold. Strand cS is completely complementary to strand S and a piece of sgc8c, whereas strand cF is completely complementary to strand F and a piece of sgc4f. (b) Scheme of aptamer-based 3D DNA nanomachine for targeted cell surface computing. Two aptamers recognize and bind to their membrane biomarkers, thus releasing cS and cF from respective recognition toes. Driven by DNA strand displacement reactions, the fluorescence signal in reporter toe switches to “ON” from its original quenched (OFF) state [171] (color online).
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Figure 15
(a) Chemical structure of COX-2 probe and the different probe response at low or high COX-2 concentrations [198]. (b) Chemical structure of β-gal activatable probe and its turn-on mechanism [200]. (c) Structure of cetuximab-conjugated AIE nanoprobe [203]. (d) Structure of the activatable aptamer probe. Its fluorescence will be turned on upon binding to target cancer cells via a conformational alteration [207] (color online).
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Figure 16
(a) Structure of the extracellular pH-activatable nanoprobe and (b) its response to the change of pH condition [208]; (c) chemical structure of the hypoxia-responsive probe [209]; (d) two-step response of the successively activatable probe to the acidic and hypoxic tumor microenvironment [211] (color online).
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Figure 17
Schematic overview of (a) the principles of PET, SPECT, CLI and RLI. (b) Proposed flowchart of general procedures for nanomaterial-assisted PET, SPECT and multivalent approach. (c) Common strategies for radioactive nanomaterial fabrication: (1) chelator-assisted surface radiolabeling; (2) rapid covalent attachment; (3) nanomaterial surface/core-doping via chelator-free methods; (4) isotope/cation exchange; (5) proton/neutron beam activation; (6) molecular self-assembly of radiolabeled precursors (Note: blue/yellow semispheres denote applicability of both organic and inorganic nanomaterials) (color online).
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Figure 18
Alluvial diagram quantitatively maps the extent of relations between nanostructure, radioisotope and imaging characteristics among organic and inorganic radioactive nanomaterials. The inorganic class is the most popular one for radionuclide-based imaging, in which iron oxide, gold, quantum dots and silica NPs are frequently used nanoplatforms. ⁶⁴Cu, ⁸⁹Zr, ¹⁸F and ⁶⁸Ga are mostly reported in PET and CLI/CRETI, while ^99mTc, ¹¹¹In, ¹²⁵I, ¹³¹I are commonly used in SPECT. ^99mTc is also a major radionuclide for RLI application. SWN: single-walled carbon nanotube; MSN: mesoporous silica nanoparticles; HMSN: hollow mesoporous silica nanoparticle; EC: electron capture; UCNP: upconverting nanoparticles; CD: cluster decay; FI: fluorescence imaging; NIRFI: near-infrared fluorescence imaging; MRI: magnetic resonance imaging; PAI: photoacoustic imaging. Note: Alluvial diagram was obtained using RAWGraphs [243] (color online).
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Figure 19
Molecular subtyping of breast cancers with different 5-year prognosis using QDs [290]. (a) Tissue microarrays of breast cancer specimens; (b) imaging of 3 key molecules of BC based on QD-IHC; (c) multi-spectral image analysis to acquire spectral information for each molecule of breast cancer specimens; (d) quantitative information of 3 key molecules for each breast cancer case related to 5-year disease free survival (color online).
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Figure 20
In vivo noninvasive fluorescence imaging of the tumor in the NIR-IIb window [320]. (a) Schematic drawing illustrating in-vivo confocal imaging of a mouse through the skin. (b) High-magnification (10× objective), wide-field fluorescence imaging (～1600?nm emission, 808?nm excitation) of a xenograft MC38 tumor on a mouse after tail vein i.v. injection of PEG-CSQDs (Scale bar: 1?mm). (c) In vivo layer-by-layer fluorescence confocal imaging of tumor vessels over an area (2500 μm×2500?μm) after an i.v. injection of PEG-CSQDs; z=0 is defined as the position when NIR-IIb signal started to show up in the tumor (Scale bar: 500?μm). (d, e) High-resolution fluorescence confocal imaging of tumor vessels at a depth of 180?μm. (d) 800 μm×800?μm (Scale bar: 200?μm); (e) 300 μm×300?μm (Scale bar: 50?μm). (f) Cross-sectional fluorescence intensity profile of the tumor vessel marked in J with the FWHM of ～9.2 and S/B ratio of 8.8 (color online).
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Figure 21
Preparation and application of Ag₂Se@Mn QDs [325]. (a) Fabrication of Ag₂Se@Mn QDs by controlling the reaction of Mn²⁺ with the Ag₂Se nanocrystals having been pretreated in 80?°C NaOH solution (0.1?M) for 10?min. (b) Ag₂Se@Mn QD labeling of cell-derived microvesicles (MVs) with the assistance of electroporation, and its applications in whole-body high-resolution dual-mode real-time tracking and in situ quantitative analysis of the dynamic bio-distribution of MVs in vivo (color online).
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Figure 22
Construction of biodegradable and highly efficient nanoparticles for gene delivery by introducing multiple interactions into polylysine [336] (color online).
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Figure 23
Illustration of ultrasensitive pH-triggered charge/size-rebound nanoparticles as gene delivery system [342] (color online).
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Figure 24
Summary of 2R2SP requirements and the 3S nanoproperty transitions in the CAPIR cascade for cancer nanomedicine [388,405] (color online).
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Figure 25
Scheme of the “cluster bomb”-like nanoassembly (a) and its 3S nanoproperty transition and traversing the CAPIR cascade (b) [388] (color online).
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Figure 26
Photoactive nanoparticles (NPs)-based phototherapy for cancer treatment. In both forms of photodynamic therapy (PDT) and photothermal therapy (PTT), photoactive NPs accumulated at tumors are used to produce reactive oxygen species (ROS) or induce temperature elevation under light exposure at a specific wavelength for triggering cancer cell death (color online).
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Figure 27
(A) Schematic illustration of Ce6-loaded gold vesicles for imaging-guided synergistic PTT/PDT; (B) In vivo NIR fluorescence imaging (a), thermal imaging (b), and photoacoustic imaging (c) of the tumor-bearing mice treated with the vesicles; (C) tumor growth profiles of tumor-bearing mice after different treatments [527] (color online).
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Figure 28
Schematic representation of the real-time monitoring of ATP-responsive drug release from polypeptide wrapped TDPA-Zn²⁺-UCNP@MSNs. Small molecule drugs were entrapped within the mesopores of the silica shell on the hybrid nanoparticles by capping the pores through multivalent interaction between oligo-aspartate side chain in polypeptide and TDPA-Zn²⁺ complex on nanoparticles surface using polypeptide. The UV-Vis emission from the multicolor UCNP under 980?nm excitation was quenched because of LRET between the loaded drugs and UCNPs. The addition of ATP led to a competitive binding of ATP to the TDPA-Zn²⁺ complex, which then displaced the surface bound compact polypeptide due to the high binding affinity of ATP to the metallic complex. The drug release was accompanied with an enhancement in the UV-Vis emission of UCNPs, thus providing real-time monitoring of drug release [578] (color online).
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Figure 29
(a) Synthetic process of UCNPs@PAA-DNA; (b) details of precise tumor targeting and specific photodynamic therapy for cancer [613] (color online).
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Figure 30
Local immunostimulatory radiation therapy based on the biomaterials together with systemic immune checkpoint blockade can induce a strong antitumor immune response to inhibit the tumor metastasis and prevent tumor recurrence. (a) Scheme of the combination of radioisotope therapy and immune therapy based on alginate hydrogel. (b) Gamma imaging of mice after i.t. injection of therapeutic agents. (c) Growth curves for tumors on mice after various treatments. Survival of mice with spontaneous metastases 4T1 tumors after various treatments to dispel their primary breast tumors. (d) Tumor growth curves of rechallenged tumors and survival curves of mice after various treatments [637] (color online).
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Figure 31
In situ activation of P-aPDL1 promoted the releases of anti-PDL1 (aPDL1) and cytokines. (a) Schematic illustration of the delivery of aPDL1 to the primary-tumor resection site by platelets; (b) fluorescence imaging of the mice 2?h after i.v. injection of P-aPDL1 or an equivalent dose of free aPDL1; (c) confocal images of the slices from residual tumors from the mice shown in (b); (d) quantified bioluminescence for the tumors from different treatment groups; (e, f) tumor growth (size) and survival curves [649] (color online).
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Figure 32
Embolization mechanisms for Ivalon (PVA microparticles), Lipiodol, and PIB-I-6150. Ivalon: collateral circulation occurs after embolization due to the large size of PVA microparticles; Lipiodol: embolization is rapidly eliminated due to blood scouring and tissue clearance in the peripheral blood vessels; PIB-I-6150: permanent and peripheral embolization is achieved by the formation of high-strength hierarchical 3D networks of nanogels through sol-gel transitions (color online).
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Figure 33
Role of serum proteins in the interaction of AuNRs with membranes. Partially exposed CTAB/AuNRs are incubated with BSA to form a hard BSA corona via Au?S coordination. The existence of the protein corona facilitates the protein receptor-mediated internalization and translocation of AuNRs to endo-/lysosomes, where the CTAB bilayer on AuNRs can probably induce lysosome-associated apoptosis. Without a protein coating, CTAB/AuNRs can directly destroy the cytoplasmic membrane, form defects, and cause the release of LDH, which eventually induces necrosis [693] (color online).
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Figure 34
Diagram of the ADME processes of NMs/NPs in vivo and summary of the current challenges for their quantitative analysis. NMs/NPs are exposed to human beings mostly through four routes, i.e., oral intake, skin contact, inhalation, and intravenous injection. Upon entering the body, NMs/NPs are quickly distributed into specific organs and then metabolized primarily by the liver. The final excretion of NMs/NPs usually occurs in the liver and kidney in the form of urine and feces. In general, the most important issues regarding the ADME processes of NMs/NPs include: (1) Where do and how much NMs/NPs get in (via absorption)? (2) Where do and how much NMs/NPs go (via distribution)? (3) How much, when do, and what form of NMs/NPs remain intact (via metabolism)? (4) Where do, how much, and what form of NMs/NPs stay in the system (via excretion)? At various stages of the ADME processes, the challenges for in vivo analysis of NMs/NPs may become largely different. Important analytical methods to resolve the analytical challenges for each ADME process are summarized [698] (color online).

Table 1 Table 1 Some classical embolic agents for clinical applications

Trade name	Material	Mechanism of embolization	Advantage	Disadvantage
Lipiodol^?	Iodized poppyseed oil	Selective deposition in hepatocellular carcinoma, and frequently use with gelatin sponges	Excellent X-ray contrast andlipiodol deposition in tumor asgold standard for TACE	Pulmonary embolism caused byexcessive dosage
Gelation sponge	Gelatin	Irregular shape, and mechanicalembolization of blood vessels	Biodegradability	Usually use in combination with contrast agent, and not suitable for drug loadingand long-term embolization
KMGmicrosphere	Sodium alginate	Mechanical embolization ofmicrospheres into blood vessels	Biodegradability and standardmicrospheres	Usually use in combination with contrast agent and not suitable for drug loading
DC Bead^?	Sulfonylated PVA	Mechanical embolization of bloodvessels, and electrostatic interaction with chemotherapeutic drug	Extensive use as drug-eluting bead, high drug loading efficiency, and slow drug release	DC Bead is not superior to C-TACEin the treatment of liver cancer inclinic

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Precise nanomedicine for intelligent therapy of cancer

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