Self-Assembly of amphiphilic BODIPY derivative and its nanoparticles as a photosensitizer for photodynamic therapy in corneal neovascularization

Colloids and Surfaces A 579 (2019) 123706

Contents lists available at ScienceDirect

Colloids and Surfaces A journal homepage: www.elsevier.com/locate/colsurfa

Self-Assembly of amphiphilic BODIPY derivative and its nanoparticles as a photosensitizer for photodynamic therapy in corneal neovascularization

T

Wenmin Jianga, Yao Tana, Jia-Fu Yinb, Hang Lib, Jie Wuc, Yongquan Wuc, De-Gao Wangb, ⁎⁎ ⁎ Ling Gaoa, , Gui-Chao Kuangb, a

Department of Ophthalmology, the Second Xiangya Hospital, Central South University, Changsha, Hunan, 410011, PR China State Key laboratory of Power metallurgy, Central South University, Lushan South Road 932, Yuelu District, Changsha, Hunan, 410083, PR China c School of Chemistry and Chemical Engineering, Key Laboratory of Organopharmaceutical Chemistry, Gannan Normal University, Ganzhou, Jiangxi 341000, PR China b

G R A P H I C A L A B S T R A C T

A R T I C LE I N FO

A B S T R A C T

Keywords: BODIPY Photodynamic dynamic therapy Corneal neovascularization Nanoaggregates Singlet oxygen

High efficiency photosensitizers for corneal neovascularization therapy are of importance because of their great advantages such as little adverse side effect and selective treatment. However, to develop high performance photosensitizer to cure the corneal disease remain challenging. In this work, a novel amphiphilic boron dipyrromethene (BODIPY) derivative (BDPY) was synthesized and it could self-assembly into nanoparticles in aqueous solution. These BDPY nanoparticles exhibited good photodynamic therapy effect on the corneal angiogenesis. The extended conjugation structure of BDPY lead to red-shift absorption and generated singlet oxygen upon red light irradiation. Our work might provide an interesting and valuable platform to design novel medicines for the new vessels of corneal therapy application.

1. Introduction Singlet oxygen (1O2) is believed to be the major species generated during Type II photochemical reaction of photodynamic therapy (PDT) [1–6]. PDT has shown its great advantages in wide range of therapeutic strategies due to its minimal invasion and toxicity [7–19]. When ⁎

specific photosensitizers was under the long wavelength light irradiation, they could generated 1O2, which could be used to kill microbial cells with little adverse effects [20]. Therefore, to select suitable photosensitizers for PDT is a critical issue. Several organic dyes such as porphyrin, boron dipyromethene (BDP), phthalocyanine have been reported as PDT sensitizers for tumor therapy [21–24]. However, rare

Corresponding author. Corresponding author. E-mail addresses: [email protected] (L. Gao), [email protected] (G.-C. Kuang).

⁎⁎

https://doi.org/10.1016/j.colsurfa.2019.123706 Received 10 June 2019; Received in revised form 20 July 2019; Accepted 20 July 2019 Available online 22 July 2019 0927-7757/ © 2019 Published by Elsevier B.V.

Colloids and Surfaces A 579 (2019) 123706

W. Jiang, et al.

Analytical thin-layer chromatography (TLC) was performed using TLC plates pre-coated with silica gel (TLC: 10–40 μm, 0.2-0.03 mm). Flash column chromatography was performed using 40–63 M (230–400 mesh) silica gel as the stationary phase.

attention has been paid on their function on the corneal new vessels. Zinc phthalocyanine tetrasulfonate has shown excellent effect on the retina tissues with minimal damage [25]. The challenge might be attributed to combined factors such as light penetration depth at long wavelength region (> 650 nm), inadequate new vessels damage and insufficient drug translocation. Hence, to develop new efficient photosensitizers for new vessel PDT are highly desirable. Amphiphilic molecules could form various nanoarchitectures such as vesicles and micelles [26]. These nanoparticles show great application in drug delivery, anticancer and even new vessels treatment on the cornea [27–31]. Angiogenensis plays a fundamental role in tissue development, regeneration, repairment, and pathological responses in the eye. The new generated vessels would not only impair the light transmission through cornea, but also lead to new inflammatory factors such as antigen-antibody complex [32]. Therefore, to develop nanoparticles PDT reagents as an economical and efficient medicine to cure new vessels on the cornea might be practicable [25]. Our group have been interested in amphiphilic BDP derivatives since 2014 [33–35]. The water solubility of these molecules could be elaborately tunable by changing the terminal units, functional groups or the dendritic oligo(ethylene glycol) generation. On one hand, some of our BDP molecules based aggregates could be transferred to tumor cells free of polymer carriers [36]. The absorption wavelength of these BDP derivatives could be easily shifted to red or near infrared region by extending the conjugation extent [37]. On the other hand, these BDP units incorporated porous polymers generated 1O2 under long wavelength light irradiation, which might be applicable for new vessels therapy [38,39]. In this work, we develop a novel BDP based molecule BDPY with extended conjugation structure by Knoevenagel condensation. This amphiphilic BDPY could form nanoaggregates with spherical morphology in aqueous solution. These aggregates show little cell toxicity and good PDT effect on the new vessels of the cornea (Fig. 1).

2.1. Animals and anesthesia 6-8 weeks old BALB/c mice were purchased from the Laboratory Animal Center of the Second Xiangya Hospital, Central South University, Changsha, China. Animals were maintained in temperaturecontrolled rooms with 12 h light/12 h dark cycle and given ad libitum access to food and water. The study was approved by the Institutional Animal Care and Use Committee at Central South University and all the procedures were conducted in accordance with the principles described in the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research. Anesthesia was induced by intraperitoneal administration of ketamine and xylazine (120 and 20 mg/kg, respectively). All the animals were randomly assigned to control group, sutured group and BDPY group. 2.2. Establishment of corneal neovascularization model Three 10.0 nylon sutures intrastromally 120˚ apart with knots left unburied were used to induce corneal neovascularization models (10.0 nylon; Alcon laboratories, USA). 2.3. Immunofluorescence of corneal neovascularization Corneal flat mounts were incubated with anti-mouse CD31(1:200; ab24590, Santa Cruz Biotechnology, Santa Cruz, CA, USA) at 4 °C overnight. After washing three times with PBS, the cornea were then incubated with donkey anti-mouse FITC (1:500; 715-095-151, Jackson Immunoresearch laboratories) at room temperature for 2 h.

2. Materials

2.4. Immunofluorescence of mitochondrial and lysosome

Unless otherwise stated, reagents were purchased from commercial sources and used without further purification. Solvents were dried by fluxing under nitrogen with calcium hydroxide. All reactions were carried out in oven dried glassware in an inert atmosphere of nitrogen.

To label mitochondria, cells were incubated with MitoTracker Green FM probes (M7514, Thermo, USA); To label lysosome, cells were

Fig. 1. (a) Molecular structure of BDPY studied in this work; (b) photoconversion pathway for BDPY based nanoparticles; (c) PDT of BDPY based nanoaggregates against corneal angiogenesis. Schematic diagram of BDPY aqueous solution was given by subconjunctival injection. 2

Colloids and Surfaces A 579 (2019) 123706

W. Jiang, et al.

4.2. Live cell imaging

incubated with LysoTracker Green DND-189 (L7535, Thermo, USA).

MCF-6 cells were placed on 14 mm glass coverslips and allowed to adhere for 12 h. The cells were washed with PBS and then incubated solely with BDPY in PBS (pH 7.4) at 25° C for 1 h. Cell imaging was then carried out after washing the cells with PBS. The excitation wavelength was 488 nm for green emission image and the collected emission wavelength was from 500 to 600 nm. While the excitation wavelength would shift to 532 nm for red emission image and the collected emission wavelength was from 620 to 700 nm.

2.5. Blocking buffer Blocking buffer include Albumin bovine (BSA), Triton X-100, 0.01 MPBS (sigma, USA).

3. Instruments 1 H and 13C NMR spectra were collected on Brüker AV-500 spectrometer with 500 MHz and 125 MHz, respectively. Chemical shift is ported as δ values in [ppm] relative to internal tetramethylsilane (Me4Si). High-resolution mass spectrometry experiments were performed with a Bruker Daltonics Apex IV spectrometer. UV–vis absorption spectra were recorded using a Hitachi U-5100 instrument. Fluorescence measurements were carried out using a Hitachi F-2700 instrument. TEM images were collected on a JEOL JEM-2100 F microscopy with an accelerating voltage of 200 kV. Prior to TEM measurements, samples were ultrasonically dispersed in ethanol and dropped to a copper grid with a diameter of 3 mm and coated with carbon film. Dynamic light scattering (DLS) were measured on MALV RN, ZETA SIZER, model ZEN3600, 25 °C. In vitro cytotoxicity was tested by means of a Tecan Infinite M200 monochromator-based multifunction microplate reader. Confocal fluorescence imaging was performed on an inverted microscope (IX81, Olympus) equipped with a confocal scanning unit (FV1000, Olympus). Light irradiation was carried out on a SR650NL having a strength of 100 mw/cm2 in a quartz cell of 1 × 1 cm. The distance between the lamp and the sample cell was 15 cm. (Scheme 1)

4.3. Suture-induced corneal neovascularization model The models of suture-induced corneal neovascularization were used as Ferrari et al [40]. Briefly, use a corneal trephine on the corneal and centered on the pupil, place three 10.0 nylon sutures intrastromally 120° apart with knots left unburied. After 14 days, vessels started to grow from the limbal arcade to sutures, finally the center of the corneal changed to be neovascularization. 4.4. BDPY treat corneal neovascularization as photodynamic therapy As a new method to treat corneal neovascularization, we assigned two groups treated by BDPY before or after suturing. BDPY was injected under conjunctival in the inferotemporal region of the mice. 4.5. Immunofluorescence and morphometric evaluation of corneal neovascularization Eyes were harvested from euthanized BALB/c mice, cut the cornea below the limbus, remove the suture thread, fix the cornea with acetone for 15 min, wash the cornea with PBS per 30 min 3 times. First, incubate the cornea in 50% Methanol for 10 min at room temperature, then change to 100% methanol for 10 min; Wash the corneas with PBST for per 15 min 3 times. Second, after blocking (blocking buffer: 1% BSA, 0.5% Triton X-100, 0.01 M PBS) the corneas for 60 min, incubate the corneas with CD31 antibody 4 °C overnight. Third, wash the corneas with PBST for 15 min per time for 3 times at room temperature, then corneas were incubated with donkey anti-mouse FITC at room temperature for 2 h. The corneas were flattened on microscope slides and cut into four parts. The slides were mounted using an anti-fade kit and covers lipped. Corneal blood vessels were analyzed using Image J software, Vascular structures stained as CD31-FITC(+) antibody were identified as blood vessels. The blood vessels were evaluated using the parameter of vessel area percentage to cornea by image J software [41], and do stastics by SPSS 21.

4. Methods 4.1. Cell viability assay The cytotoxicity was measured by performing methyl thiazolyl tetrazolium (MTT) assays on the MCF-6 cells lines, which were provided by the Institute of Biochemistry and Cell Biology (Chinese Academy of Sciences). The MCF-6 cells were grown in RPMI 1640 (Roswell Park Memorial Institute’s Medium) supplemented with 10% FBS (fetal bovine serum) at 37 °C under 5% CO2. The BDPY derivatives at 0, 1, 5, 10, and 15 μm concentration were added to the wells of the treatment group. The cells were incubated for 24 h at 37 °C under 5% CO2 and then MTT was added to the wells for test.

5. Synthesis and characterization of new compounds Synthesis of BDPY: BDP-1 was synthesized according to the literature [37]. BDP-1 (100 mg, 0.11 mmol), 4-pyridinecarboxaldehyde (47 mg, 0.44 mmol) and p-toluenesulfonic acid (p-TsOH, 10 mg) were dissolved in the mixture solvent of toluene and piperidine (25:1, v/v, 26 mL). Stirring was kept at 120 °C for 2 h under the protection of N2. After that, the reaction mixture was heated to 150 °C and the solvent was evaporated into the dean stark apparatus. After cooling down, 25 ml toluene and 1 mL piperidine were added to the system and the above-mentioned drying process was repeated for 6 times until the reagent was completely consumed from the TLC results. The crude product was washed with water, dried over MgSO4, filtered and evaporated. Then the residue was subjected to column chromatography with DCM/CH3OH (10:1, v/v) as eluents to afford a dark-green solid (30 mg, 25%). 1H NMR (400 MHz, CDCl3): δ = 8.86 (d, J =6.0 Hz, 4 H), 7.92 (d, J =6.2 Hz, 2 H), 7.50 (d, J =6.0 Hz, 4 H), 7.27 (t, 16.2 Hz, 2 H), 6.98 (q, J =4.5 Hz, 4 H), 6.80 (s, 2 H), 4.27 (t, J =5.0 Hz, 2 H),

Scheme 1. Synthetic route for BDPY. Reaction condition and reagents: (a) piperidine, p-toluenesulfonic acid, 4-pyridinecarboxaldehyde, toluene, reflux, 2 h. 3

Colloids and Surfaces A 579 (2019) 123706

W. Jiang, et al.

Fig. 2. (a) UV–vis spectra and (b) fluorescent spectra of BDPY (5.0 μM) in DMSO/water mixture solvents, excitation wavelength 610 nm.

S1). The nanoparticles are stable for at least for three months. It is very important to promote BDPY to generate more 1O2 for the following PDT. Therefore, 1,3-diphenylisobenzofuran (DPBF) was used as monitor to determine the efficiency of 1O2 generation ability of BDPY in mixture solution (DMSO/H2O, 5/95) [43]. The absorption of DBPF decreased gradually under red lamp irradiation (λ = 650 nm) and reached balance after 3 min (Fig. S2a). BDPY was photostable from NMR test results (Fig. S2). In contrast, little absorption intensity change was observed without this lamp irradiation (Fig. S3b). These results revealed that the long wavelength irradiation plays a critical role for BDPY to generate 1O2 for DPBF decomposition. In order to investigate the application in corneal application, vitro test in living cells was tested. First, the toxicity of BDPY was investigated by direct cell viability and methyl thiazolyl tetrazolium (MTT) measurements (Fig. S4c). Toxicity test results demonstrated that cell viability showed little change even when the concentration of BDPY reached 15 μM. However, under 650 nm red light irradiation, the phototoxicity of BDPY toward cancer cells were dramatically increased. Control experiment with MCF-7 cells only stained by JC-1 showed normal red emission (Fig. S5). When co-stained by JC-1 and BDPY, the cells showed apparently emission change from red to green upon 650 nm light irradiation, which indicated that the MCF-7 cells were dead or withered (Fig. S6). The withered cells were dependent on the irradiation time and BDPY concentration. A MTT assay diagram determined after 5 min irradiation time was collected (Fig. S7). The results showed that most of cell were dead when the BDPY concentration reached 5 μM after 15 min irradiation (Fig. 4). Living cell imaging tests were performed by Confocal Laser

4.19 (t, J =4.9 Hz, 4 H), 3.50–3.92 (m, 42 H), 3.37 (d, J =10.0 Hz, 9 H). 13C NMR (100 MHz, CDCl3): δ = 153.90, 152.65, 150.53, 143.49, 141.58, 140.52, 136.66, 133.85, 130.55, 123.36, 121.45, 117.22, 110.71, 72.72, 72.00, 70.95, 70.68, 70.59, 69.83, 69.31. Mass. [M +H]+ Cal. 1093.5368; Found [M+H]+ 1093.5334.

6. Results and discussion The photophysical properties were investigated by collecting the absorption and emission spectra of BDPY in various organic solvents. Both the absorption and emission maximum peaks show small change in different polarity solvents, indicating that there is no apparent donoracceptor interaction in the ground state. Detail value about the photophysical properties were demonstrated in Table S1. UV–vis spectra of BDPY in DMSO/water mixture solvents demonstrate decreased absorption intensity when the water fraction increase, which indicates the formation of nanoaggregates in aqueous solution. Blue emission shift proved the H-aggregation [42] (Fig. 2). In order to reveal the aggregate properties of above BDPY in detail, the critical aggregation concentration (CAC) and aggregation morphology measurements were performed. The fluorescent spectra of the compounds in varying concentration range were collected to determine the CAC values (Fig. 3a). We found the CAC of BDPY in aqueous solution was roughly 3.4 × 10−6 M. The aggregation morphologies of sample were investigated by transmission electron microscopy (TEM). Spherical micelles architecture with 30 nm diameter could be observed for BDPY (Fig. 3b). DLS) result demonstrated the nanoparticles size were around 30 nm, which was consistent with the TEM results (Fig.

Fig. 3. Changes in fluorescence intensity with increasing the concentrations of (a) BDPY (λex =628 nm, λem =640 nm) and (b) TEM image of BDPY made from DMSO/H2O (5/95) solution (concentration is 5.0 μM). Inset is the aggregates size distribution. 4

Colloids and Surfaces A 579 (2019) 123706

W. Jiang, et al.

Fig. 4. Confocal images of MCF-7 cells (a, d, h) stained by BDPY solution (5 μM), excitation wavelength is 532 nm; (b) Bright field image; (e) Co-stained by (LTG, excitation wavelength is 488 nm; (i) Co-stained by MTG, excitation wavelength is 488 nm; (c), (f) and (j) are the merged images of (a,b), (d,e) and (h,i), respectively.

subconjunctival injection of BDPY solution and then irradiation by the 650 nm wavelength red light for 10 min, the new vessels decreased dramatically (Fig. 5f). Control experiments to corneal neovascular models by subconjunctival injection 0.1 M PBS or without light irradiation showed no changes (Fig. 5e). Therefore, the disappearance of the new vessels was attributed to the 1O2 from BDPY. In order to further demonstrate the critical role of the BDPY aggregates to diminish the new vessels in the cornea, CD31-FITC immunofluorescent staining measurement was performed. The FITC stained vessels could be clearly detected (Fig. 5g). After red light irradiation (λ =650 nm), the generated 1O2 depressed most of new vessels, suggesting that the BDPY aggregates is a good chemical candidate to treat neovascularization in the eyes by PDT (Fig. 5h). The new vessels were stained with CD31-antibody were statistically determined (Fig. S10 and S11), which shows the corneal neovascularization degraded obviously, which verified the antiangiogesis function of BDPY.

Scanning Microscopy (CLSM). The human breast cancer cells (MCF-7) showed no morphology change after incubation with BDPY solution for 24 h (Fig. S8a-b). This result is consistent with MTT test that our BDPY show no toxicity at this concentration. Red fluorescence emission could be observed under CLSM (Fig. 9a). Furthermore, considering the properties to target specific organelles exhibited in our previous amphiphilic BDP derivatives and polymer [35,36], we further trace the BDPY with lyso-tracker green (LTG) and mitochondria tracker green (MTG), respectively. After co-staining with BDPY and either of the two different organelle green trackers, the MCF-7 cells exhibited corresponding color emission. However, the merged images demonstrated that the red and green color didn’t overlap well (Fig. 10f-j). Partially overlap yellow could be observed from the merged image from BDPY and LTG. Their corresponding average overlap percentage the four marked areas was less than 50% (Fig. S8). For co-stained experiment by BDPY and MTG, the overlap percentage was as low as 20% (Fig. S9). Therefore, merged images revealed that these BDPY aggregates were mainly located in the cytoplasm, not in lysosome or mitochondria. Considering the BDPY based nanoaggregates are cell membrane permeable and low toxicity, we injected BDPY solution under the conjunctiva for vivo bioimaging tests. The aim is to investigate the BDPY function for antiangiogenic under long wavelength light irradiation. We built up corneal neovasculation animal models by suturing 10.0 nylon threads on the cornea. After 2 weeks, corneas were neovascularized around the knots and even extended to the center of the corneas (Fig. 5b). Corneal slices of normal eye (Fig. 5c) and neovascularized eye (Fig. 5d) clearly demonstrate the morphology changes. The effects of photodynamic therapy with BDPY aggregates was tested. Stimulated by the knots, new vessels grew gradually and became apparent after 14 days (Fig. 5b). The mice were treated by

7. Conclusion A novel amphiphilic BDPY with red emission was synthesized and its nanoaggregates properties were investigated. Beneficial from their long wavelength red emission and little toxicity, these aggregates were used for bioimaging in living cells and photodynamic dynamic therapy on the neovascularized cornea. Upon the red light irradiation (650 nm), the BDPY generated 1O2, which could depress the new vessels greatly. This work might pave a new way to extend the PDT application of BDP derivatives.

5

Colloids and Surfaces A 579 (2019) 123706

W. Jiang, et al.

Fig. 5. Schemetic diagrams of neovascularized corneal model and PDT effect. (a) the sham group, (b) neovascularized cornea induced by 10.0 nylon thread knots; (c) immunohistochemical staining in the normal cornea with CD31-antibody; (d) CD31- positive-stained neovascularized corneas. (e) After 14 days suturing, photograph of mouse eyeball which was treated with subconjunctival injection 0.1 M PBS or without light irradiation. (f) Photograph of mouse eyeball which was treated with subconjunctival injection of BDPY solution and then irradiation by the 650 nm wavelength red light for 10 min. CD31-FITC immunofluorescent staining images (g) before and (h) after PDT of mouse eyes (10 ×). The red light wavelength is 650 nm. Scale Bar: (a), (b), (e), (f) 1 mm, (c), (d) 200 μm, (g), (h) 500μm (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).

Acknowledgements

[12] J. Mosafer, K. Abnous, M. Tafaghodi, H. Jafarzadeh, M. Ramezani, Preparation and characterization of uniform-sized PLGA nanospheres encapsulated with oleic acidcoated magnetic-Fe3O4 nanoparticles for simultaneous diagnostic and therapeutic applications, Colloids Surf. A Physicochem. Eng. Asp. 514 (2017) 146–154. [13] H. Sun, S. Li, W. Qi, R. Xing, Q. Zou, X. Yan, Stimuli-responsive nanoparticles based on co-assembly of naturally-occurring biomacromolecules for in vitro photodynamic therapy, Colloids Surf. A Physicochem. Eng. Asp. 538 (2018) 795–801. [14] P. Azcona, I. López-Corral, V. Lassalle, Fabrication of folic acid magnetic nanotheranostics: an insight on the formation mechanism, physicochemical properties and stability in simulated physiological media, Colloids Surf. A Physicochem. Eng. Asp. 537 (2018) 185–196. [15] J. Yan, H. Sun, J. Li, W. Qi, H. Wang, A theranostic plaster combining photothermal therapy and photodynamic therapy based on chlorin e6/gold nanorods (Ce6/Au nrs) composite, Colloids Surf. A Physicochem. Eng. Asp. 537 (2018) 460–466. [16] H. Ma, S. Li, H. Zhang, Y. Wei, L. Jiang, Fabrication of polydopamine-based layerby-layer nanocomposites for combined pH-sensitive chemotherapy and photothermal therapy, Colloids Surf. A Physicochem. Eng. Asp. 561 (2019) 332–340. [17] S. Li, Q. Zou, Y. Li, C. Yuan, R. Xing, X. Yan, Smart peptide-based supramolecular photodynamic metallo-nanodrugs designed by multicomponent coordination selfassembly, J. Am. Chem. Soc. 140 (2018) 10794–10802. [18] H. Zhang, K. Liu, S. Li, X. Xin, S. Yuan, G. Ma, X. Yan, Self-assembled minimalist multifunctional theranostic nanoplatform for magnetic resonance imaging-guided tumor photodynamic therapy, ACS Nano 12 (8) (2018) 8266–8276. [19] M. Abbas, Q. Zou, S. Li, X. Yan, Self-assembled peptide- and protein-based nanomaterials for antitumor photodynamic and photothermal therapy, Adv. Mater. 29 (12) (2017) 1605021. [20] L. Cheng, C. Wang, L. Feng, K. Yang, Z. Liu, Functional nanomaterials for phototherapies of Cancer, Chem. Rev. 114 (21) (2014) 10869–10939. [21] E. Secret, M. Maynadier, A. Gallud, A. Chaix, E. Bouffard, M. Gary-Bobo, N. Marcotte, O. Mongin, K.E. Cheikh, V. Hugues, M. Auffan, C. Frochot, A. Morere, P. Maillard, M. Blandhard-Desce, M.J. Sailor, M. Garcia, J.O. Durand, F. Cunin, Two-photon excitation of porphyrin-functionalized porous silicon nanoparticles for photodynamic therapy, Adv. Mater. 26 (2014) 7643–7648. [22] R. Bonnett, Photosensitizers of the porphyrin and phthalocyanine series for photodynamic therapy, Chem. Soc. Rev. 24 (1) (1995) 19–33. [23] C.S. Kue, S.Y. Ng, S.H. Voon, A. Kamkaew, L.Y. Chung, L.V. Kiew, H.B. Lee, Recent strategies to improve boron dipyrromethene (BODIPY) for photodynamic cancer therapy: an updated review, Photochem. Photobiol. Sci. 17 (11) (2018) 1691–1708. [24] S. Ye, J. Rao, S. Qiu, J. Zhao, H. He, Z. Yan, T. Yang, Y. Deng, H. Ke, H. Yang, Y. Zhao, Z. Guo, H. Chen, Rational design of conjugated photosensitizers with controllable photoconversion for dually cooperative phototherapy, Adv. Mater. 30 (2018) 1801216. [25] Y. Huang, G. Xu, Y. Peng, H. Lin, X. Zheng, M. Xie, Zinc Phthalocyanine Tetrasulfonate (ZnPcS4): a new photosensitizer for photodynamic therapy in choroidal neovascularization, J. Ocul. Pharmacol. Ther. 23 (4) (2007) 377–386. [26] X. Zhang, C. Wang, Supramolecular amphiphiles, Chem. Soc. Rev. 40 (1) (2011) 94–101. [27] N. Song, L. Fu, Y. Liu, Y. Li, L. Chen, X. Wang, S. Liu, Z. Xie, Rational design of BODIPY organic nanoparticles for enhanced photodynamic/photothermal therapy, Dye. Pigment. 162 (2019) 295–302. [28] X. Wang, W. Lin, W. Zhang, C. Li, T. Sun, G. Chen, Z. Xie, Amphiphilic redoxsensitive NIR BODIPY nanoparticles for dual-mode imaging and photothermal therapy, J. Colloid Interface Sci. 536 (2019) 208–214. [29] A. Turksoy, D. Yildiz, E.U. Akkaya, Photosensitization and controlled photosensitization with BODIPY dyes, Coord. Chem. Rev. 379 (2019) 47–64.

This work was supported by the State Key Laboratory of Powder Metallurgy, Central South University, the National Natural Science Foundation of China (21204047, 21501031, 81700838 and 81072221), the Natural Science Foundation of Hunan, China (2018JJ2487), Hunan Provincial Key Research & Development Projects (2017SK2020), Beijing National Laboratory for Molecular Sciences (BNLMS201829). Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.colsurfa.2019.123706. References [1] R. Vankayala, K.C. Hwang, NIR light activatable nanomaterials-mediated phototheranostic nanomedicines: an emerging paradigm for Cancer treatment, Adv. Mater. 30 (23) (2018) 1706320. [2] Y.Y. Huang, Y. Tian, X.Q. Liu, Z. Niu, Q.Z. Yang, V. Ramamurthy, C.H. Tung, Y.Z. Chen, L.Z. Wu, Luminescent supramolecular polymer nanoparticles for ratiometric hypoxia sensing, imaging and therapy, Mater. Chem. Front. 2 (10) (2018) 1893–1899. [3] K.V. Sudheesh, P.S. Jayaram, A. Samanta, K.S. Bejoymohandas, R.S. Jayasree, A. Ajayaghosh, A cyclometalated IrIII complex as a lysosome-targeted photodynamic therapeutic agent for integrated imaging and therapy in cancer cells, Chem. Eur. J. 24 (43) (2018) 10999–11007. [4] S.S. Lucky, K.C. Soo, Y. Zhang, Nanoparticles in photodynamic therapy, Chem. Rev. 115 (4) (2015) 1990–2042. [5] S. Yano, S. Hirohara, M. Obata, Y. Hagiya, S. Ogura, A. Ikeda, H. Kataoka, M. Tanaka, T. Joh, Current states and future views in photodynamic therapy, J. Photochem. Photobiol. C Photochem. Rev. 12 (1) (2011) 46–47. [6] N.F. Gamaleia, I.O. Shton, Gold mining for PDT: great expectations from tiny nanoparticles, Photodiagn. Photodyn. Ther. 12 (2) (2015) 221–231. [7] C. Conte, S. Maiolino, D.S. Pellosi, A. Miro, F. Ungaro, F. Quaglia, Polymeric nanoparticles for Cancer Photodynamic therapy, Top. Curr. Chem. 370 (2016) 61–112. [8] Z. Guo, Y. Zou, H. He, J. Rao, S. Ji, X. Cui, H. Ke, Y. Deng, H. Yang, C. Chen, Y. Zhao, H. Chen, Bifunctional platinated nanoparticles for photoinduced tumor ablation, Adv. Mater. 28 (46) (2016) 10155–10164. [9] X. Ai, C.J.H. Ho, J. Aw, A.B. Attia, J. Mu, Y. Wang, X. Wang, Y. Wang, X. Liu, H. Chen, M. Gao, X. Chen, E.K. Yeow, G. Liu, M. Olivo, B. Xing, In vivo covalent cross-linking of photon-converted rare-earth nanostructures for tumour localization and theranostics, Nat. Cummun. 7 (2016) 10432. [10] C. Li, A targeted approach to cancer imaging and therapy, Nat. Mater. 13 (2) (2014) 110–115. [11] J. Sun, Y. Guo, R. Xing, T. Jiao, Q. Zou, X. Yan, Synergistic in vivo photodynamic and photothermal antitumor therapy based on collagen-gold hybrid hydrogels with inclusion of photosensitive drugs, Colloids Surf, A Physicochem. Eng. Asp. 514 (2017) 155–160.

6

Colloids and Surfaces A 579 (2019) 123706

W. Jiang, et al.

[30] T. Zhang, C. Ma, T. Sun, Z. Xie, Unadulterated BODIPY nanoparticles for biomedical applications, Coord. Chem. Rev. 390 (2019) 76–85. [31] A.T. Ogunjimi, S.M.G. Melo, C.G. Vargas-Rechia, F.S. Emery, R.F.V. Lopez, Hydrophilic polymeric nanoparticles prepared from Delonixgalactomannan with low cytotoxicity for ocular drug delivery, Carbohyd. Polym. 157 (2017) 1065–1075. [32] K. Halasz, S.J. Kelly, M.T. Iqbal, Y. Pathak, V. Sutariya, Utilization of apatinibloaded nanoparticles for the treatment of ocular neovascularization, Curr. Drug Deliv. 16 (2) (2019) 153–163. [33] S. Li, K. Liu, G.C. Kuang, T. Masuda, A.F. Zhang, Thermoresponsive helical poly (phenylacetylene)s, Macromolecules 47 (10) (2014) 3288–3296. [34] H. Wang, Y. Wu, P. Tao, X. Fan, G.C. Kuang, BODIPY-based oligo(ethylene glycol) Dendrons as fluorescence thermometers: when thermoresponsiveness meets intramolecular Electron/Charge transfer, Chem. Eur. J. 20 (50) (2014) 16634–16643. [35] H. Wang, Y. Wu, Y.L. Shi, P. Tao, X. Fan, X.Y. Su, G.C. Kuang, BODIPY-based fluorescent thermometer as a lysosome-targetable probe: how the oligo(ethylene glycols) compete photoinduced Electron transfer, Chem. Eur. J. 21 (8) (2015) 3219–3223. [36] L. Yang, Y.J. Ji, J.F. Yin, Y. Wu, H. Fan, Y. Zhang, G.C. Kuang, Amphiphilic BODIPY derivatives: the solvophobic effect on their photophysical properties and bioimaging in living cells, Soft Matter 12 (41) (2016) 8581–8587. [37] J.F. Yin, Y. Hu, H. Wang, Z. Jin, Y. Zhang, G.C. Kuang, Near-infrared-Emissive

[38]

[39]

[40]

[41]

[42] [43]

7

amphiphilic BODIPY assemblies manipulated by charge-transfer interaction: from nanofibers to nanorods and nanodisks, Chem. Asian J. 12 (23) (2017) 3088–3095. D.G. Wang, Q. Li, Y.L. Zhu, H. Tang, M. Song, G.C. Kuang, BODIPY-based porous organic polymers: how the monomeric methyl substituents and isomerization affect the porosity and singlet oxygen generation, Macromol. Chem. Phys. 218 (15) (2017) 1700101. D.G. Wang, F. Song, H. Tang, X.R. Jia, M. Song, G.C. Kuang, A facile route to prepare dimeric BODIPY-based porous organic polymers using FeCl3, New J. Chem. 41 (13) (2017) 5263–5266. C. Giacomini, G. Ferrari, F. Bignami, P. Rama, Alkali burn versus suture-induced corneal neovascularization in C57BL/6 mice: an overview of two common animal models of corneal neovascularization, Exp. Eye Res. 121 (2014) 1–4. D. Yuen, S. Grimaldo, R. Sessa, T. Ecoiffier, T. Truong, E. Huang, M. Bernas, S. Daley, M. Witte, L. Chen, Role of Angiopoietin-2 in corneal lymphangiogenesis, IOVS 55 (5) (2014) 3320–3327. F.C. Spano, The Spectral Signatures of Frenkel Polarons in H- and J-Aggregates, Acc. Chem. Res. 43 (3) (2010) 429–439. X. Ding, B.H. Han, Microscale crystals of cytochrome c and Calixarene on electrodes: interprotein Electron transfer between defined sites, Angew. Chem., Int. Ed. 54 (21) (2015) 6356–6359.