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Front. Optoelectron.    2020, Vol. 13 Issue (4) : 327-351    https://doi.org/10.1007/s12200-020-1084-1
REVIEW ARTICLE
Multifunctional layered black phosphorene-based nanoplatform for disease diagnosis and treatment: a review
Xiazi HUANG1,2, Yingying ZHOU1,2, Chi Man WOO1,2, Yue PAN3, Liming NIE4, Puxiang LAI1,2()
1. Department of Biomedical Engineering, Hong Kong Polytechnic University, Hong Kong, China
2. Hong Kong Polytechnic University Shenzhen Research Institute, Shenzhen 518057, China
3. Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Medical Research Center, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China
4. State Key Laboratory of Molecular Vaccinology and Molecular Diagnosis & Center for Molecular Imaging and Translational Medicine, School of Public Health, Xiamen University, Xiamen 361102, China
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Abstract

As an outstanding two-dimensional material, black phosphorene, has attracted significant attention in the biomedicine field due to its large surface area, strong optical absorption, distinct bioactivity, excellent biocompatibility, and high biodegradability. In this review, the preparation and properties of black phosphorene are summarized first. Thereafter, black phosphorene-based multifunctional platforms employed for the diagnosis and treatment of diseases, including cancer, bone injuries, brain diseases, progressive oxidative diseases, and kidney injury, are reviewed in detail. This review provides a better understanding of the exciting properties of black phosphorene, such as its high drug-loading efficiency, photothermal conversion capability, high 1O2 generation efficiency, and high electrical conductivity, as well as how these properties can be exploited in biomedicine. Finally, the research perspectives of black phosphorene are discussed.
Keywords black phosphorus (BP)      delivery nanoplatform      bioimaging      cancer therapy      bone regeneration     
Corresponding Author(s): Puxiang LAI   
Just Accepted Date: 29 October 2020   Online First Date: 25 November 2020    Issue Date: 31 December 2020
 Cite this article:   
Xiazi HUANG,Yingying ZHOU,Chi Man WOO, et al. Multifunctional layered black phosphorene-based nanoplatform for disease diagnosis and treatment: a review[J]. Front. Optoelectron., 2020, 13(4): 327-351.
 URL:  
https://academic.hep.com.cn/foe/EN/10.1007/s12200-020-1084-1
https://academic.hep.com.cn/foe/EN/Y2020/V13/I4/327
Fig.1  Schematic illustration of the atomic structure of 2D BP. (a) Top view. (b) 3D view. Reproduced from Ref. [17]. (c) Schematic illustration of the 2D layered-BP preparation methods. (d) Schematic illustration of mechanical exfoliation. (e) Schematic illustration of liquid-phase exfoliation. (f) Schematic illustration of the CVD method
synthesis method description advantages disadvantages
top-down mechanical exfoliation making BP layers flake off and thin from BP bulk crystal by repeatedly bonding/separating with the help of adhesive tapes or plasma etching • high quality BPNSs • not suitable for large-scale production of BPNSs
• hard to control the thickness and size of BPNSs
liquid exfoliation BP bulk crystal is immersed into solvents and the ions weaken and break the interlayer attractions between BP layers under sonication • large-scale production
• diverse BP nanostructures (e.g., BPQDs and BPNSs)
• controllable size and thickness of final product
• low cost		 • hard to produce large area phosphorene
• lower purity
bottom-up chemical vapor deposition (CVD) forming BP thin films by doping phosphorus atoms in the vacuum • suitable for large area BPNSs production • high cost
• produce by-products
Tab.1  Summary of the popular synthesis methods
material application disease highlight of the research Ref.
TiL4@BPQDs photoacoustic imaging (PAI) MCF-7 tumor It demonstrates that BP-based PA agents are stable and can be used for efficient bioimaging of cancer; the performance is superior to that of gold nanoparticles (AuNPs). [30]
BP-DEX/PEI-FA PAI and photothermal therapy (PTT) BP-DEX/PEI-FA The biocompatible and water-soluble BP nanoparticles exhibit high photothermal conversion efficacy for PAI and photothermal therapy of cancer. [79]
BP@lipid-PEG PAI/NIR-II optical imaging It first reports that the BPNSs modified with cholesterol display strong NIR-II fluorescence and can be capsulated with the PEGylated lipid into BP@lipid-PEG nanoparticles for NIR-II optical imaging. [80]
BPNS@TA-Mn PAI/MRI/PTT HeLa tumor It applies PAI/MRI dual-mode imaging for guided PTT. [81]
MUCNPs@BPNs-Ce6 MRI/PAI/ultrasound /fluorescence/
PTT/ photodynamic (PDT)		 HeLa tumor The multi-functional layered-BP platform can simultaneously implement four imaging modalities and two treatment schemes; the agent has strong absorption of NIR light for deep tissue applications. [82]
NB@BPs PTT MCF7 breast tumor A Nile Blue (NB) diazonium tetrafluoroborate salt is covalently doped with BPs, enhancing the stability. [83]
NIR-II-CD/BP PTT 4T1 tumor NIR-II-CD/BP show remarkably enhanced photothermal conversion efficacy and antitumor efficiency in NIR-II region, the most suitable optical window for clinical use. [84]
MTP-BP-al-PEG PTT 4T1 tumor Targeting to higher potential membrane and mitochondria of cancer cells greatly boost the PTT efficiency. [85]
BPQDs/GA/PLLA-PEG-?PLLA PAI/PTT T47D tumor Gambogic acid inhibits heat shock protein expression conducing a better PTT effect. [86]
PEGylated BPQDs PDT S180 tumor It demonstrates the good stability, no cytotoxicity and PDT potential of BP. [87]
Cy5-dHeme-BPNS-FA PDT HeLa tumors The excessive intracellular H2O2 were catalyzed with passivated BP-based nanoplatform to generate O2 that is essential for PDT, leading to significant enhancement of PDT efficacy for tumor treatment. [88]
BP-DOX PDT/PTT/chemotherapy 4T1 tumor The drug loading rate of layered-BP is increased by up to 9.5 folds. [89]
BP@hydrogel chemotherapy MDA-MB-231 tumors By loading DOX in the layered-BP modified with hydrogel, laser exposure can be regulated to release drugs to treat cancer. [90]
BP-DOX@PDA-PEG-FA PTT/chemotherapy Hela tumor BP-DOX@PDA-PEG-FA combined with laser irradiation yields dramatic synergistic antitumor effects, inducing no acute side effects. [91]
BP-R-D@PDA-PEG-Apt genetherapy/ chemotherapy/PTT MCF-7 tumor BP can be used in targeted chemo, PTT, and gene against multidrug-resistant cancer. [92]
BSPTD chemotherapy/PTT/ fluorescence 4T1 tumor It can specifically target the tumor site, and inhibit metastasis during the targeting chemo-photothermal therapy, benefiting from the secondary drug delivery facilitated by photothermal degradation. [93]
RV/CAT-BP@MFL fluorescence/PTT/
PDT/chemotherapy		 MCF-7 tumor It displays folate receptor-targeted delivery, tumor hypoxia relief, and synergistic suppression of tumorous cell propagation. [94]
BPNVs-CpG PDT/immunotherapy/PAI 4T1-tumor It enhances deeper tumor penetration synergized immunotherapy induced by CpG, yielding an excellent cancer therapy effect. [95]
R-MnO2-FBP MRI/fluorescence/PDT HeLa tumor It demonstrates a dual-mode of fluorescence imaging and MR imaging for guided PDT. [96]
NE hydrogel osteanagenesis calvarial defect It demonstrates BP nanosheets-based nanoengineered hydrogels can increase biological mineralization and promote bone osteogenic cell differentiation and bone regeneration. [97]
BPNs/chitosan/PRP osteanagenesis/PTT/PDT rheumatoid arthritis Platelet-rich plasma-chitosan was combined with BP which induced calcium-extracted biomineralization and phototherapy, getting a better curative effect of rheumatoid arthritis. [98]
BP@PDA-incorporated ?GelMA scaffold MSC differentiation It can significantly promote the differentiation of mesenchymal stem cells (MSC) into neural-like cells under the synergistic electrical stimulation. [99]
BP nanosheets Cu2+ regulation neurodegenerative disorder BP nanosheets are promising neuroprotective nanodrug for NDs because they process preeminent photothermal effect, increasing its blood–brain barrier permeability and subsequently act as a chelator to regulate Cu2+ concentration. [100]
PEG-LK7@BP Cu2+ regulation /chemotherapy Alzheimer’s disease BP can efficiently bind with the peptide inhibitor LK7 to inhibit amyloid formation. [101]
BP nanosheets antioxidative therapy acute kidney injury BP nanosheets are easily to be oxidized into phosphorus oxides which can act as promising antioxidative agents for consuming excess cytotoxic reactive oxygen species. [102]
Tab.2  Biomedical applications of layered black phosphorus-based platforms in disease diagnosis and treatment
Fig.2  (a) Preparation of the PEGylated BP theranostic delivery platform. 1: PEG–NH2 (surface modification), 2: DOX (therapeutic agents), 3: Cy7–NH2 (NIR imaging agents), 4: FA–PEG–NH2 (targeting agents), 5: FITC–PEG–NH2 (fluorescent imaging agents). (b) Screening and summary of the endocytosis pathways and the biological activities of PEGylated BPNSs in cancer cells. Reproduced from Ref. [32]
Fig.3  (a) and (b) Targeted imaging of tumors with BP-DEX/PEI-FA nanoparticles. (a) In vivo PA images of the 4T1 tumor-bearing mice before and after tail vein injection of BP-DEX/PEI and BP-DEX/PEI-FA nanoparticles (2 mg/mL) at different time points. (b) PA signal intensities of the tumors from the 4T1 tumor-bearing mice collected at different time points after tail vein injection of BP-DEX/PEI and BP-DEX/PEI-FA nanoparticles. (c) In vivo NIR-II fluorescence images of a mouse collected at different time intervals using a 1400-nm optical filter after intravenous injection of BP@lipid-PEG nanosphere aqueous solutions. (d) Enlargement of the image acquired at 30 s post-injection with different optical filters (1400 and 1250 nm, respectively). Scale bar = 5 mm. Reproduced from Refs. [80,107]
Fig.4  Schematic illustration of the fabrication of BP-based nanoplatforms (MUCNPs@BPNs-Ce6). Reproduced from Ref. [109]
Fig.5  (a) Schematic illustration of the fabrication of NB@BPs. (b)–(f) Material stability examinations. Time-dependent variations in the (b) absorption ratios at the respective peak wavelength (A/A0) and (c) increase in the temperature of the bare BPs and NB@BPs in water under 808 nm and 1.0 W/cm2 laser irradiations for 10 min. (d) Time-dependent variations of the fluorescence intensity of NB@BPs in water. Optical images of micro-sized (e) bare BPs and (f) NB@BPs exposed under ambient conditions for different dispersion time lengths. Reproduced from Ref. [83]
Fig.6  (a) Schematic illustration of in vitro deep-tissue PTT. (b) and (c) Temperature change of the NIR-II-CD/BP solution irradiated by an 808- or 1064-nm laser in the presence of varied thicknesses of additional tissue. (d) Fitted temperature change exponential decay of NIR-II-CD/BP hybrids upon 808- and 1064-nm laser irradiations. Reproduced from Ref. [84]
Fig.7  (a) HSP90 expressions in tumors collected from mice 2 days after applying various treatments, as determined by immunofluorescence staining. (b) Western blot data of T47D tumor lysates collected from mice 2 days after applying various treatments. (c) Relative expression of HSP90 normalized against β-actin (control). **P < 0.01, ***P < 0.001. Reproduced from Ref. [86]
Fig.8  (a) Schematic illustration of singlet-oxygen production by BPNSs under laser irradiation. (b) Photographs of PEGylated BPQDs dispersed in various media. (RPMI refers to RPMI 1640 media) (c) Cell viability of HeLa and L02 cells after incubation with BPQDs at different concentrations at 37°C for 24 h. (d) In vivo imaging monitoring of the PDT effect on tumor-bearing mice in both the left and right flanks after the injection of Cy5-dHeme-BPNS-FA or Cy5-BPNS-FA. After 24 h post-injection, the tumor in the right flank was irradiated with laser, whereas the tumor in the left was kept away from light as the control. (e) Relative change of the averaged tumor volume after treatment with PBS, Cy5-dHeme-BPNS-FA, and Cy5-BPNS-FA with and without laser irradiation. Statistical analysis was performed using Student’s t-test (**P < 0.01 and ***P < 0.001). Reproduced from Refs. [87,88,113]
Fig.9  (a) Schematic illustration of the working principle of BP@hydrogel. BP@hydrogel releases the encapsulated chemotherapeutics under NIR-light irradiation to break the DNA chains, thereby inducing apoptosis. (b) Viability of HeLa cells cultured with DOX-loaded nanoformulations in comparison with that of free DOX at the same DOX dose after 24 h (∗∗P < 0.01). (c) Anti-tumor efficacy of saline, DOX, BP-DOX@PDA-PEG, BP-DOX@PDA-PEG-FA, and BP-DOX@PDA-PEG-FA + NIR on the nude mice bearing HeLa cell xenografts. Tumor weight of each group was obtained from the sacrificed mice at the end of the study (∗∗P < 0.01). Reproduced from Refs. [90,91]
Fig.10  (a) Schematic illustration of the procedure used to fabricate nanostructures and the combined chemo/gene/photothermal targeted therapy of tumor cells. (b) Inhibition of tumor growth after different treatments. (c) Morphology of tumors removed from the sacrificed mice in all groups at the end of the study (**P < 0.01, ***P < 0.001). Reproduced from Ref. [92]
Fig.11  Schematic illustration of the formation of RV/CAT-BP@MFL and its application for photothermally contrived drug delivery and oxygen self-enriched photodynamic multifarious cancer therapy. Reproduced from Ref. [94]
Fig.12  (a) and (b) In vivo time-dependent imaging. (a) Time-dependent in vivo fluorescence images by dual-channel of RhB and Cy5.5. (b) MR images of a mouse bearing a subcutaneous HeLa tumor after being injected with R-MnO2-FBP. Scale bar: 5.0 mm. (c)–(e) In vivo assessment of the PDT therapeutic efficacy as monitored by (c) fluorescence and (d) MRI on the tumor-bearing mice at 24, 28, and 36 h, separately, after injection of R-MnO2-FBP. The tumors were irradiated by a 660-nm laser at 150 mW/cm2 for 10 min. Scale bar: 5.0 mm. (e) Relative change of the averaged tumor volume after different treatments. Mean ± SD, n = 5 (**P < 0.01). Reproduced from Ref. [96]
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