Review ArticleOpen Access

Black phosphorus: A novel nanoplatform with potential in the field of bio-photonic nanomedicine

Shenzhen Engineering Laboratory of Phosphorene and Optoelectronics, Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Optoelectronic Engineering, Shenzhen University, Shenzhen 518060, P. R. China

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Yansheng Zhou

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Meng Qiu

E-mail Address: [email protected]

Corresponding author.

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, and

Han Zhang

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https://doi.org/10.1142/S1793545818300033Cited by:76 (Source: Crossref)

Abstract

Single- or few-layer black phosphorus (FLBP) has attracted great attentions in scientific community with its excellent properties, including biodegradability, unique puckered lattice configuration, attractive electrical properties and direct and tunable band gap. In recent years, FLBP has been widely studied in bio-photonic fields such as photothermal and photodynamic therapy, drug delivery, bioimaging and biosensor, showing attractive clinical potential. Because of the marked advantages of FLBP nanomaterials in bio-photonic fields, this review article reviews the latest advances of biomaterials based on FLBP in biomedical applications, ranging from biocompatibility, medical diagnosis to treatment.

Keywords:

1. Introduction

Two-dimensional (2D) materials, such as graphene,^{1,2,3,4,5,6,7,8}⁹ transition metal dichalcogenides (TMDs, e.g., MoS₂,^{10,11,12,13,14,15,16,17,18}¹⁹ WS₂,^{20,21,22,23,24,25} TiS₂) and black phosphorus (BP), have been applied in various fields because of their distinctive physicochemical properties,^{26,27,28,29,30,31,32,33,34,35,36,37,38,39} including easy surface modification, electrical conductivity and strong light response.^{40,41,42,43,44,45,46,47,48,49,50} Especially, 2D materials own more advantages in bio-photonic applications such as biosensing,^{51,52,53,54,55,56,57,58,59,60,61} cancer imaging^{62,63,64,65,66,67,68} and drug delivery platform.^{69,70,71,72,73} However, each 2D material has its own shortcoming which hinders its clinical applications.^74,75,76,77 Graphene displays an extremely high carrier mobility, but it has no bandgap,^{78,79,80,81,82,83,84,85,86,87,88} which limits its applications in biosensing and bioimaging. In spite of possessing a finite bandgap,^{17,89,90,91,92,93,94,95,96} the low carrier mobility of TMDs prevents their practical applications.^{97,98,99,100,101,102,103,104,105,106,107} Taken together, it is important to find a new 2D material with a well-balanced performance.

BP is a novel nanoplatform with potential applications in such as energy storage,³⁵ sensor¹⁰⁸ and bio-photonic because of its excellent properties.^{109,110,111,112,113,114,115,116,117,118,119,120} The bandgap of BP is tunable in a large range (from 0.3eV to 2eV) under different thicknesses.^{121,122,123,124} As the result of the direct and tunable bandgap, few-layer black phosphorus (FLBP) processes a widely light absorption indicating a great potential in photothermal and photodynamic therapy. FLBP also shows high carrier mobility^{125,126,127,128,129,130} while preserving large ON/OFF ratio.^{131,132,133,134,135,136,137} Due to the balance of these features, BP is often occurred in biosensing and bioimaging field. FLBP, with the unique puckered lattice configuration, possesses much larger surface area-to-volume ratio than other 2D materials, which results in extremely high drug loading capacity.¹³⁸ Furthermore, FLBP displays negligible toxicity and outstanding biodegradability in the biological environment which distinguishes it from other common 2D materials. FLBP is completely degradable in vivo, and the products, such as phosphite ions, phosphate ions and other P_xO_y, are nontoxic and can be easily exhibited a desire renal filtration. In addition, FLBP possesses attractive electrical characteristics, unique band structure and natural biocompatibility, indicating that FLBP has a great potential for biomedical field.³⁷

BP has aroused more and more research interest on its biomedicine applications with its unique physical and chemical properties. However, there is still a lot of problems needs to be solved to achieve the requirements of clinical applications, such as stability,^{139,140,141,142,143,144}in vivo toxicity,¹⁴⁵ biodegradation,¹⁴⁶ excretion,¹⁴⁷ etc. In order to meet the urgent demand for the novel 2D materials used in biomedical field, it is necessary to summarize the latest achievement of BP in bio-photonic fields. In this paper, we mainly review the biomedical research of BP in biological diagnosis and therapy.

2. Biocompatibility of BP

Latiff et al.¹⁴⁵ established human lung carcinoma cancer epithelial cells (A549) model to study the toxicity of FLBP. To ensure the credibility of the results, graphene and MoS₂ are used as comparison and two similar methods based on similar principles were used to assess cell viabilities. In this work, the toxicity of FLBP increases with increasing concentration, when the concentration of FLBP is below 50ppm. They found that toxicity of FLBP is lower than that of graphene but higher than that of MoS₂. Due to the limitations of the test method and the size of FLBP used in the paper, there are still a lot of toxicity assessments to do before the clinical applications of FLBP. Zhang et al.¹⁴⁸ studied the dependence of FLBP toxicity on size, concentration, exposure time and cell type, as presented in Fig. 1. FLBP was fabricated in oxygen-free Millipore water, and centrifugation at different speeds was used to obtain FLBP with three different sizes, named BP-1, BP-2 and BP-3, from large to small. The results of this paper indicate that FLBP with the BP-3 dimensions is appropriate for biomedical applications. They proposed and verified two possible mechanisms of the cytotoxicity of FLBP: (1) FLBP produces reactive oxygen species (ROS) to kill cells and (2) FLBP destroys cell membrane integrity. The cytotoxicity of BP-1 is much higher than that of BP-3. Fortunately, the size of BP-3 happens to be the most widely used size of FLBP nanosheets in the biomedical field. The results of this paper indicate that FLBP is appropriate for biomedical applications. Mu et al.¹⁴⁹ explored toxicological studies on BP quantum dots (BPQDs), which underwent faster renal filtration than BP nanosheets, systemically with cell and animal model. Comparing the cells viability and the endocellular ROS levels in experimental group with different concentrations of BPQDs and the control group, they found that the cytotoxicity of BPQDs is mainly derived from ROS produced by itself. The results of in vivo assays indicated that catalase activity in liver will reduce 24h after injection, but there was no obvious adverse effect after a week without recurrence after a month. Song et al.¹⁵⁰ studied the dependence of FLBP cytotoxicity on dose and time. When the concentration exceeded 4ppm, FLBP showed significant cytotoxicity, which conflicts with other works probably for the reason of the difference in the size of FLBP. The percentage of live cells was detected within 12h at a dose of 10ppm and was significantly reduced after 6h, indicating the need for effective modification before BP achieves clinical applications.

Fig. 1. The dependence of cell viability on size, concentration of BP, exposure time and cell lines. Cell lines: NIH 3T3 (a–c), HCoEpiC (d–f) and 293T cells (g–i). Exposure time: 12h (a, d, g), 24h (b, e, h) and 48h (c, f, i).

3. Medical Diagnosis

3.1. Biomolecular biosensors

With a high carrier mobility and large switching ratios, FLBP has great applications potential on highly sensitive and selective biosensors.^{151,152,153,154,155,156,157,158,159,160} Chen et al.¹⁶¹ investigated FLBP for human immunoglobulin G (IgG) detection. FLBP was fabricated by a mechanical exfoliation method and passivated with Al₂O₃. The FLBP-based device showed rapid response performances and excellent sensitivity ( $\sim$ 10ngmL $^{- 1}$ ) to human IgG. Furthermore, the FLBP-based device exhibited good stability without obvious changes in performance. Mayorga-Martinez et al.¹⁶² obtained FLBP with the size of $40 \sim 200$ nm by electrochemical exfoliation. The as-fabricated FLBP showed active electrocatalytic performances for the hydrogen evolution reaction and IgG detection. In addition, FLBP with poly-L-lysine (PLL) displays a great potential in label-free detection of myoglobin (Mb), which is an important signal of cardiovascular events.¹⁶³ FLBP was created by liquid-phase exfoliation (LPE) with an aqueous surfactant solution in argon atmosphere, and PLL was used to functionalize FLBP in order to accelerate binding with anti-Mb DNA aptamers. The PLL-BP dispersed stability in aqueous medium and showed a stable detection performance in phosphate-buffered saline (PBS) and serum samples, indicating successful surface modification. The FLBP-based device possesses a high sensitivity (36 $μ$ Apg $^{- 1}$ mLcm $^{- 2}$ ) and a low detection limit (0.524pgmL $^{- 1}$ ), with a widely dynamic response range (1pgmL $^{- 1}$ to 16 $μ$ gmL $^{- 1}$ ).

In addition to excellent electrical properties, the unique fluorescence properties of FLBP were also applied to biological detection. Gu et al.¹⁶⁴ investigated BPQDs with a sonication-assisted solvothermal method for the applications of acetylcholinesterase activity sensing probes. The BPQDs showed strong green fluorescence at 497nm and an extremely high quantum yield (8.4%). Furthermore, pH relevant fluorescence property with reliable photostability had been observed in this work. Lee et al.¹⁶⁵ prepared BPQDs with a strong visible blue-emitting performance by LPE in various organic solvents. They used catechol-grafted poly(ethylene glycol) (CA-PEG) to functionalize BPQDs in basic buffer to achieve a stable dispersible in water and an extremely low cytotoxicity. The photoluminescence emission centered of PEG-BPQDs is 428nm and the photoluminescence quantum yield is $\approx$ 5% when the excitation wavelength is 365nm. Yew et al.¹⁶⁶ demonstrated FLBP as a platform in fluorescence-based DNA biosensors. BP crystals transformed from red phosphorus allotrope in the high pressure, and FLBP was synthesized by share force milling at 17,000rpm. FLBP showed an obvious photoluminescence emission centered at 527nm with an excitation wavelength of 200 nm, indicating potential applications as fluorescent sensing platform. This biosensor shows a low detection limit (5.9pM) and quantification limit (19.7pM). In addition, an excellent linearity ( $r = 0.91$ ) and a widely dynamic response range (4–4000pM) were observed in this work.

3.2. Tumor imaging

Cancer is a malignant disease that kills millions of people every year.^{38,167,168,169,170,171,172,173,174,175,176,177} With the enhanced permeability and retention (EPR) effect,^{178,179,180,181,182,183,184,185,186,187,188} FLBP can be passively enriched to the tumor site, so the tumor imaging based on FLBP has received extensive attention. Shao et al.¹⁴⁷ investigated that BPQDs, which manufactured by the simple liquid exfoliation method, with poly lactic-co-glycolic acid (PLGA) were used to modify BPQDs in order to enhance the stability and solubility of BPQDs in water. As-fabricated BP-PLGA can effectively passively accumulate to the tumor region with tail vein injection because of the EPR effect. Figure 2(a) demonstrates the infrared thermographic images of the mice irradiated by near-infrared (NIR) laser 24h after injection. Drawing a comparison between the tumor temperature of the test groups and of the control groups under the same power irradiation, it is obvious that the tumor temperature of the test groups (26.3^∘C of BP-PLGA) increased much more than that of the control groups (6.2^∘C, 7.8^∘C and 10.8^∘C of PBS, PLGA and bare BPQDs, respectively), indicating the excellent photothermal performance of BP-PLGA. In addition, many other researchers also have achieved extremely good photothermal imaging by different modifications of FLBP.^189,190

Sun et al.¹⁹¹ investigated BPQDs with excellent photostability for the applications of photoacoustic (PA) imaging, as shown in Fig. 2(b). The PEGylated BPQDs with a uniform size were fabricated by a simple high energy mechanical milling method. When the concentration of the PEGylated BPQDs is in the range of 0–250 $μ$ gmL $^{- 1}$ , the intensity of the PA signal rises linearly as the concentration increases. Furthermore, the PA signal intensity in tumor was still higher than that of liver and kidney, 24h after injection, representing a long retention time and EPR effect. Sun et al.¹⁹² reported BPQDs loaded with titanium ligand (TiL4) as PA imaging agent. Dispersibility and stability of TiL₄@BPQDs in water are much better than those of bare BPQDs. With increasing wavelength of the irradiation, the intensity of the PA signal decreased because the optical absorption of wavelength range from 680nm to 808nm reduces.

Yang et al.¹⁹³ prepared FLBP coated with Au nanoparticles for surface-enhanced Raman scattering (SERS) imaging. BP–Au NSs were fabricated with a facile reflux method, and mPEG-SH was added to improve the dispersion and stability in water. The molecular mechanism of photothermal therapy (PTT) was investigated by SERS analysis. The SERS analysis illustrates that PTT damages the membrane microstructure in tumor, and some BP–Au NSs appear in the nucleus region.

4. Medical Therapy

4.1. Phototherapy

Phototherapy, mainly including PTT^194,195 and photodynamic therapeutic (PDT),^196,197 has become a potential alternative to traditional cancer therapy with its advantages of little double consequences,^{198,199,200,201,202,203,204,205} excellent targeting^{206,207,208,209,210,211,212,213,214,215} and intelligent controllability.^{216,217,218,219,220,221,222} The principle of PTT is based on the heat energy generated by the photothermal agent under irradiation to achieve the therapeutic effect. PDT agent can generate ROS to kill cancer cells under laser irradiation. FLBP has broadband absorption characteristics because of its tunable direct band gap, indicating great potential for the applications of cancer phototherapy.

4.1.1. PTT

Sun et al.²²³ fabricated BPQDs by liquid exfoliation method as photothermal agent. BPQDs were functionalized with PEG to prevent BPQDs from aggregating in PBS. As-fabricated PEG-BPQDs possessed a large extinction coefficient (14.8Lg $^{- 1}$ cm $^{- 1}$ at 808nm), which is much more larger than that of Au nanorods. In addition, PEG-BPQDs showed a high photothermal conversion efficiency (28.4%) and favorable photostability. The aqueous solutions of PEG-BPQDs rise 31.5^∘C in 10min at the concentration of 50ppm when the power density of NIR laser irradiation is 1.0Wcm $^{- 2}$ , indicating an excellent photothermal performance. The percentage of live cells had no significant decrease even with a high incubation concentration of PEG-BPQDs (200ppm) without NIR laser. The PEG-BPQDs killed the most of the cancer cells with a low concentration after the NIR irradiation for 10min, as shown in Fig. 3. The results of this work illustrate the good biocompatibility and photothermal performance of BPQDs.

Fig. 3. The dependence of cell viability on concentration of BPQDs and cell lines. The irradiation time is 10min and power density of 808nm laser is 1.0Wcm $^{- 2}$ . (a) Fluorescence images of cancer cells incubated with BPQDs after irradiation of 808nm laser. (b) C6 cells viability after treatments with different concentrations of BPQDs. (c) MCF7 cells viability after treatments with different concentrations of BPQDs.

Shao et al.¹⁴⁷ demonstrated BPQDs coated with PLGA for PTT. PLGA enhanced the stability of BPQDs and adjusted the degradation rate of nanoparticles by adjusting the chemical composition. PLGA-BPQDs maintained stable photothermal properties within 8 days, and it degraded by almost 80% after 8 weeks, indicating a balance of therapeutic and biodegradable. In vitro experiments showed that PLGA-BPQDs killed the most of cancer cells at an extremely low concentration (10ppm). What’s more, the final degradation products of PLGA-BPQDs are carbon dioxide, water, phosphate and phosphonate, which normally exist both in vivo and in vitro and result in little side effects. Fu et al.²²⁴ prepared three types of FLBP with average size of $394 \pm 75$ nm, $118 \pm 22$ nm and $4.5 \pm 0.6$ nm by LPE method, named as L-BP, M-BP and S-BP. The temperature of L-BP solution with a concentration of 25ppm was able to rise by 24^∘C under NIR laser irradiation for 10min, whereas temperatures of M-BP and S-BP solutions with the equal concentration could only rise by 21.8^∘C and 19.2^∘C, indicating that L-BP has the best photothermal performance. In addition, there are some studies dedicated to improving the photothermal stability of FLBP.^225,226,227 Some researchers explored new applications for the thermal performance of BP, such as post-surgical treatment of cancer, 3D-printed scaffolds and neuroprotective nanomedicine.^189,228,229

4.1.2. PDT

FLBP for PDT was fabricated by LPE in an aqueous solvent.²³⁰ At a wavelength of 530nm, the quantum yield of FLBP producing singlet oxygen is very high (0.91). In vitro and in vivo FLBP experiments showed good PDT effects, as shown in Fig. 4. BPQDs were synthesized by LPE in $N$ -methyl pyrrolidone and coated with PEG to achieve enhanced stability in water. Guo et al.²³¹ used BP dispersion to incubate cancer cells under 670nm laser irradiation and researched the dependence of cell survival rate on BPQD concentrations, illumination time and laser intensity. The ROS generated by FLBP was able to kill the cancer cells efficiently at very low concentration (1.6ppm) and at very weak laser power (160mWcm $^{- 2}$ ). Furthermore, 65% of BPQDs was found excreted with urine within 8h, probably for the reason of the ultra-small hydrodynamic size of BPQDs, indicating that BPQDs have a good biocompatibility. Chen et al.²³² found that the bleaching signal of BPQDs is built up rapidly ( $<$ 2ns) and lasts a long time (100 $μ$ s). The triplet generation attributed to intersystem crossing was observed and may be the reason of the highly efficient singlet oxygen generation of BPQDs. Tan et al.²³³ achieved in situ disinfection with PDT based on FLBP. FLBP was modified with poly(4-pyridonemethylstyrene) endoperoxide (PPMS-EPO). PPMS not only enhances the stability of FLBP, but also stores singlet oxygen. The PPMS-EPO/BPS showed good photodynamic performance even in the absence of light, indicating a good clinical potential.

Fig. 4. *In vivo* PDT. (a) Tumor volume of different time post-injections. (b) Tumor pictures of experimental group and control group after treatments. (c) PCNA and TUNEL analysis of tumor tissues.

4.2. Therapeutic agent delivery

Chemotherapy is an effective cancer treatment,^234,235 but the high toxicity,²³⁶ low targeting^237,238 and drug resistance²³⁹ limit its therapeutic effect. In order to solve the aforementioned problems, researchers load therapeutic agents onto drug delivery systems (DDSs) to enhance chemotherapeutic effect. With large surface area-to-volume radio, unique pleated structure and excellent light response characteristics, FLBP has great potential for DDSs. Tao et al.²⁴⁰ first applied FLBP to DDSs, as shown in Fig. 5. PEG-FA/Cy7-functionalized FLBP exhibited good biocompatibility, obvious tumor targeting and strong fluorescence signal and was loaded with doxorubicin (DOX) via electrostatic adsorption. In addition, the endocytosis pathway of the FLBP nanoparticle had also been screened. Chen et al.¹³⁸ prepared a drug loading platform with a pH/photo response based on FLBP. Their results showed that FLBP has a very high DOX loading (980%) due to its puckered lattice configuration, large interlay distance 0.524nm and negative charge. They used the therapeutic system to achieve synergistic treatment of PTT/PDT/chemotherapy and achieved good anti-tumor effects. Wang et al.²⁴¹ used one-pot method to prepare HSA-modified FLBP, which can effectively load paclitaxel by hydrophobic interactions. Qiu et al.¹⁹⁰ fabricated a BP@hydrogel-based DDS. The DDSs enable intelligent light-controlled drug release and degradation, and the degradation products are completely nontoxic and easily metabolized. Yin et al.²⁴² fabricated FLBP loaded with interfering RNA as the applications of gene delivery systems. Compared with the commercial delivery reagents, the BPQDs exhibited a higher transfection efficiency and low toxicity.

Fig. 5. (a) Schematic representation of the FLBP nanoparticle. 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) The endocytosis pathway of the FLBP nanoparticle.

5. Summary

This paper summarizes the latest progress in FLBP research from three aspects, including biocompatibility of BP, medical diagnosis and medical therapeutic based on BP. Various factors such as size, concentration and test cell line can affect the toxicity of FLBP, but overall, FLBP shows relatively low toxic at effective dosing dose. Due to its attractive electrical properties, fluorescence characteristics and large surface area-to-volume ratio, FLBP shows a great potential for biosensors and imaging. In terms of biological therapy, FLBP mainly achieves therapeutic effects through its excellent optical response characteristics and as a drug delivery platform.

Although studies on the biomedical applications of FLBP have made a lot of progress, there are still some problems that need to be solved before its clinical translation. First of all, because the size of the FLBP has a great impact on toxicity and treatment effects, it is very important to find a novel method to fabricate FLBP with uniform size and high production. Secondly, other treatments such as chemotherapy, immunotherapy, etc. could be combined with BP to achieve synergistic effect. Finally, the targeted treatments based on FLBP should be developed for specific diseases to achieve smaller side effects and better therapeutic effects. This requires multidisciplinary researchers to work together. FLBP has great potential in biomedicine. To promote the clinical applications of FLBP, we summarized the progress of FLBP in biomedical field.

Abbreviations

FLBP	few-layer black phosphorus
2D	two-dimensional
BP	black phosphorus
TMDs	transition metal dichalcogenides
ROS	reactive oxygen species
QDs	quantum dots
IgG	immunoglobulin G
PLL	poly-L-lysine
Mb	myoglobin
PBS	Phosphate-buffered saline
CA-PEG	catechol-grafted poly (ethylene glycol)
EPR	enhanced permeability and retention
PLGA	poly lactic-co-glycolic acid
NIR	near-infrared
PA	Photoacoustic
HEMM	high energy mechanical milling
TiL4	titanium ligand
SERS	surface-enhanced Raman scattering
PTT	photothermal therapy
PDT	photodynamic therapeutic
PEG	poly (ethylene glycol)
NMP	$N$ -methyl pyrrolidone
PPMS-EPO	poly(4-pyridonemethylstyrene) endoperoxide
DDSs	drug delivery systems
DOX	Doxorubicin

Acknowledgments

We acknowledge financial support from the National Natural Science Foundation of China (61435010 and 61575089, H. Z.), the Science and Technology Innovation Commission of Shenzhen (KQTD2015032416270385 and JCYJ20150625103619275, H. Z.), the China Postdoctoral Science Foundation (2017M610540, 2018T110892, M. Q.), the Natural Science Foundation of Shandong Province, China (ZR2016BB33, M. Q.) and the Natural Science Foundation of Guangdong Province, China (2018A030310500, M. Q.).

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Vol. 11, No. 06

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History

Received 4 September 2018

Accepted 21 October 2018

Published: 16 November 2018

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This is an Open Access article published by World Scientific Publishing Company. It is distributed under the terms of the Creative Commons Attribution 4.0 (CC-BY) License. Further distribution of this work is permitted, provided the original work is properly cited.

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