Polydopamine-Based Tumor-Targeted ... - ACS Publications

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Cite This: ACS Appl. Bio Mater. XXXX, XXX, XXX−XXX

Polydopamine-Based Tumor-Targeted Multifunctional Reagents for Computer Tomography/Fluorescence Dual-Mode BioimagingGuided Photothermal Therapy Mojue Zhang,†,⊥ Yibiao Zou,†,⊥ Yaping Zhong,‡ Guangfu Liao,*,§ Chunhan Yu,† and Zushun Xu*,†

ACS Appl. Bio Mater. Downloaded from pubs.acs.org by IOWA STATE UNIV on 01/14/19. For personal use only.

†

Hubei Collaborative Innovation Center for Advanced Organic Chemical Materials; Ministry of Education Key Laboratory for The Green Preparation and Application of Functional Material, Hubei University, Wuhan, Hubei 430062, China ‡ Department of Chemistry and Collaborative Innovation Center of Chemistry for Energy Materials, Fudan University, 2005 Songhu Road, Shanghai 200438, China § School of Materials Science and Engineering, PCFM Lab, Sun Yat-sen University, Guangzhou 510275, China S Supporting Information *

ABSTRACT: Development of multifunctional diagnosis and treatment reagents is very meaningful in clinical application. Herein, we developed a polydopamine-based (PDA-based) tumor targeted multifunctional reagent by surface-initiated atom transfer radical polymerization (ATRP) strategy. First, the targeted PDA nanoparticles were prepared via combining with folic acid (FA) and dopamine. Then ATRP technology was used to graft the europium(III) complexes onto PDA surface (defined as FEDA). A series of detections revealed that the FEDA nanoparticles had been successfully prepared and exhibited a bright X-ray computer tomography (CT) and photoluminescence (PL) dual-mode imaging efficiency and an excellent photothermal therapy (PTT) effect in vivo/in vitro. KEYWORDS: folic acid targeted, polydopamine, europium(III) complexes, atom transfer radical polymerization, dual-mode imaging-guided photothermal therapy

1. INTRODUCTION

Polydopamine (PDA), an organic micromolecule monomer, has been found be applied promisingly to tumor therapy,12,13 marine antifouling,14 and hydrogel modification.15 The mechanism was that the protons of dopamine (DA) generated from the oxidation process would be consumed under alkaline conditions (pH 8.5), and the equilibrium would transfer to product.16 Especially, PDA has been widely used in cancer treatment because of its strong near-infrared (NIR) absorption and excellent photothermal conversion property.17−19 Nevertheless, PDA with single therapy function could not confirm whether the nanoagents arrive at tumor site; thus, the tumor could not be effectively treated. Therefore, the image-guided PTT multifunctional reagents combined with PDA and imaging agent are highly worth considering, which not only could effectively kill the cancer cell, but also provide more comprehensive information on tumor.20 Hu et al.21 fabricated a multifunctional nanoagent on the basis of indocyanine greenloaded PDA-iron ions coordination nanoparticles, which could increase the NIR optical absorption and decrease their fluorescence emission. Ding et al.22 developed a core−shell−

The diagnosis and treatment of cancer are still immense challenges in the field of modern medicine. Recently, a growing number of nanoagents have been extensively used for cancer diagnose and treatment,1−4 for example, carbon nanotubes (CNTs), an inorganic nonmetallic material, have been used as photothermal material in the matter of tumor therapy because of their typical structures and remarkable physical performances.5 However, the relatively low photoluminescent (PL) imaging efficiency severely limited CNTs as an outstanding imaging agent in vivo. Tian et al.6 prepared a novel hydrophilic plate-like Cu9S5 nanocrystals photothermal agent via thermal decomposition and ligand exchange method, but it suffered from low biocompatibility and high toxicity. The multimodal imaging-guided photothermal treatment (PTT) of PPy/ Fe3O4/Au nanocomposites was highly promising for cancer treatment.7 However, a short imaging time and poor imaging effect vastly diminished the potential of PPy/Fe3O4/Au nanocomposites clinically. Differently, most of organic micromolecule monomer possessed a series of advantages such as excellent biocompatibility,8 regulable particle size,9 and the further activation for surface groups,10,11 which are highly worth considering. © XXXX American Chemical Society

Received: December 11, 2018 Accepted: January 9, 2019 Published: January 9, 2019 A

DOI: 10.1021/acsabm.8b00797 ACS Appl. Bio Mater. XXXX, XXX, XXX−XXX

Letter

ACS Applied Bio Materials

Figure 1. (A) Design and synthesize schematic illustration of FEDA nanoparticles for multifunctional photothermal agent. (B) XPS spectrum analysis of FEDA nanoparticles. (C) FT-IR spectra analysis of PDA-CPA and FEDA nanoparticles. (D) UV−vis/NIR spectroscopy analysis.

shell diagnosis reagent, which structured Nd3+-sensitized upconversion nanoparticles, and decorated them onto PDA surface to fabricate a nanotheranostic for imaging guidance PTT. However, all of these nanoagents suffered from poor tumor gathering and lesser blood half-life, which led to inferior imaging effect and short imaging time. Thus, the preparation of conditional controllable targeted multifunctional imagingguided PTT reagent is also of great significance.23,24 As an efficient and controllable synthetic method, surfaceinitiated atom transfer radical polymerization (ATRP) played significant role for nanoagent surface functionalization. This method provided a lot of active sites for grafting a series of polymers with terminal functional group onto NPs surfaces and offered further multibiofunctionalization for specific targeting.25,26 In particular, the initiator group (e.g., C−Cl, C−Br, and C−I) could cut C=C into C−C and subsequently graft onto the nanoagent surface.27 Thus, ATRP is an effective tool to combine PDA with other multifunctional nanoparticles. The surface of PDA contained a great amount of active amino group, which possessed many advantages such as improving biocompatibility and commanding molecular weight. These features inspired us to design and develop a high-performance X-ray computer tomography (CT) and photoluminescence (PL) dual-mode bioimaging-guided photothermal nanotheranostic agent on the basis of PDA by using surface-initiated ATRP strategy. Herein, we developed a PDA-based tumor targeted multifunctional reagent combined with folic acid (FA), europium(III) complexes, and PDA (namely FEDA) by using surfaceinitiated ATRP strategy, which showed excellent target,

photothermal, CT, and PL imaging performances. This multifunctional reagent showed a high grafting rate, which led to intense X-ray attenuation and remarkable PL imaging property, as well as strong NIR absorption and high photothermal conversion efficiency. Compared with commonly used agents in clinical, FEDA nanoparticles exhibited more outstanding imaging effect and longer imaging time. Moreover, the FEDA could be effectively concentrated on tumor by sustained targeted effect. In addition, the favorable biocompatibility and low toxicity of FEDA nanoparticles made it possible for potential biomedical applications.

2. RESULTS AND DISCUSSION 2.1. Synthesis Process of FEDA Nanoparticles. A facile ATRP strategy was presented for the preparation of FEDA nanoparticles (Figure 1A). Specifically, PDA was produced by the 3-hydroxytyramine (DA) hydrochloride self-assembly at alkaline water environment for 6 h at room temperature. To endow PDA surface with initiative and target ability, the surface of PDA was modified with 3-chloropropionic acid (CPA) and folic acid (FA) by dehydration condensation at room temperature for 12 h to form PDA-CPA. In addition, according to the previous method, we prepared Eu(AA)2(DTA)Phen for further experiment.28 Because the surface C−Cl bond of PDA-CPA can cut the C=C double bond of organic matter into C−C single bond, Eu(AA)2(DTA)Phen was mixed with PDA-CPA and magnetic stir under N2 atmosphere in a 30 °C water bath. After 15 min, CuCl and Bpy were added in the flask stir for 12 h and B


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Figure 2. (A) Cell viability of 4T1 cells. (B) Cell viability of 4T1 cells after an 808 nm NIR laser irradiate. (C) Photothermal effect of 4T1 cells after an 808 nm NIR laser irradiate (calcein-AM and PI staining).

Eu(AA)2(DTA)Phen grafted onto PDA-CPA surface by ATRP to form FEDA nanoparticles. 2.2. Characterization. TEM and SEM indicated that the diameters of CPA-PDA and FEDA were about 174 and 200 nm, separately (Figure S1A−D). The hydrodynamic diameters (Dh) of CPA-PDA and FEDA nanoparticles were about 176 and 203 nm, separately (Figure S2A−D). Energy dispersive Xray spectroscopy (EDS) and mapping EDS reflected the C, N, O, Cl, I, and Eu ions were distributed on the surface of FEDA nanoparticles (Figure S3). XPS was used to detect the chemical information on PDA-CPA and FEDA (Figure 1B and Figure S4A−C), and the distinct I 3d and Eu 3d signal peaks were showed at 620.6 and 1135.1 eV. The core level binding energies were almost as the same as those reported previously.27 In FT-IR spectra, the stretching vibrations peak located at 3434 cm−1 were ascribed to O−H. The absorption peaks located at 1609 and 1397 cm−1 were ascribed to the antisymmetric and symmetric stretching vibrations of COO−.29,30 The absorption peaks were observed at 1330 and 859 cm−1, corresponding to the symmetric stretching vibrations of −NC=O and C−Cl, separately, which demonstrated that FA and CPA were efficiently grafted on PDA surface. The stretching vibrations peak at 858 and 414 cm−1 were ascribed to C=N and Eu−O (Figure 1C). In addition, UV−vis/NIR revealed the PDA-CPA and FEDA nanoparticles exhibited favorable NIR absorption at 808 nm (Figure 1D). All of these results confirmed that the FEDA nanoparticles had been successfully prepared. 2.3. Cytotoxicity Analysis. As we know, it is essential to prepare the low toxicity or nontoxic photothermal agent for biological application. Two groups of 4T1 cells with FEDA nanoparticles were incubated for 24 and 48 h at different concentrations, separately. Figure 2A displayed that the percentages of living cells were clearly exceeded 80% after 24 h incubated even though the concentration of europium element reached 640 μg/mL. Furthermore, the FEDA was still kept a lower toxicity when the concentration of europium element reached to 160 μg/mL, indicating that FEDA

nanoparticles could be used as an excellent biological reagent application in vivo. 2.4. In Vitro PTT. The cell photothermal effect of FEDA nanoparticles in vitro was detected by standard CCK-8 assay. The 4T1 cells were added in two groups of 96-well plates and then incubated with FEDA nanoparticles at different concentrations (0−640 μg/mL). After 24 h, an 808 nm NIR light (1.5 W/cm2) was used to irradiate the samples for 10 min. The results showed that the 4T1 cells could be effectively killed due to the higher temperature produced by FEDA nanoparticles (Figure 2B). Furthermore, 4T1 cells and FEDA nanoparticles were injected to four groups 96-well plates, and then the samples were irradiated for another 10 min by an 808 nm NIR light (1.5 W/cm2). After another 2 h incubated, the calcein-AM and PI staining were added in 96-well plates, which were used to differentiate the live and dead cells (Figure 2C). It was found that the groups of PBS, PBS + Laser, and FEDA had no detectable death cell. In contrast, the majority of cells in FEDA + Laser group were killed. For the photothermal effect of FEDA nanoparticles, the temperature of control group (deionized water) had no obvious change, while the experimental group (FEDA nanoparticles) revealed significant concentration dependence with the growing of irradiation time (Figure 3A). Furthermore, the FEDA solution (320 μg/mL) rapidly reached 45.2 °C from room temperature, which was higher than the critical value of cancer cells death (43.0 °C). In the same way, another important factor for evaluating photothermal was the conversion stability. After repeated irradiation, the temperature maintained a good upward trend and the photothermal conversion efficiency reached about 32.3% (Figure 3B, Figure S5A−D, and Table S1) because of the robust chemical bonds and reduplicative charge transfer. At the same time, FEDA nanoparticles possessed an excellent IR thermal imaging contrast. The intensity of image increased with the increasing of mass concentrations and irradiation time (Figure 3C). Therefore, FEDA nanoparticles could be as an effective C


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experimental groups (PBS + Laser and FEDA+ Laser) for another 10 min. Figure 4A and B display that tumor temperature of PBS + Laser group has promoted slowly, and the FEDA + Laser group showed a quickly increasing from ∼30 °C to ∼49.5 °C. It was demonstrated that FEDA + NIR laser could induced an excellent photothermal effect and could availably destroy the tumor cells. Figure 4C showed the relative tumor growth curves after PTT. The experimental group (FEDA + Laser) can be observed an obvious tumor restrain. After PTT 10 days, the tumor volume was controlled at about 80 mm3. In contrast, the tumor volume ratios (V/V0) of control groups (PBS and PBS + Laser) and FEDA groups were increased to 6.2-, 5.4-, and 4.5times after 10 days laser irradiation (V is the tumor volume after irradiation 10 days, V0 is the origin tumor volume, which about ∼100 mm3). Thus, single FEDA and NIR light cannot inhibit the tumor growth. All of them clearly suggested that the FEDA + Laser displayed excellent photothermal ablation. 2.6. CT and PL Imaging. As we know, atomic number and electron density were vastly influenced by CT imaging efficiency with the progressively enhancement of attenuation coefficient. To prove whether the FEDA nanoparticles possessed excellent X-ray absorption, the CT imaging in vitro/in vivo was studied. For in vivo CT, after intravenous injection of FEDA nanoparticles, tumor regions showed significant enhancement in CT imaging observation, and tumor CT value reached to maximum at 24 h after injection (Figure 5A). For in vitro CT, control group (iodixanol) and FEDA were used as experimental group, and X-ray attenuation potency was detected at the same mass concentrations gradient. As the result displayed, the CT signal intensity of FEDA showed a concentration-dependent tendency (Figure 5B,C). As shown in Figure 5D, FEDA showed higher X-ray

Figure 3. (A) Temperature change of deionized water and FEDA. (B) Temperature conversion stability of FEDA (320 μg/mL). (C) Infrared thermal imaging of deionized water and FEDA solution at different concentrations.

nanotheranostic reagent for clinical diagnosis and antitumor treatment. 2.5. In Vivo PTT. For the photothermal effect in vivo, four groups 4T1 cell-bearing mice were intravenous injected with PBS and FEDA (1.6 mg/mL, 150 μL) when tumor volume increased to ∼100 mm3, respectively. Twenty-four hours later, 808 nm NIR light (1.5 W/cm2) was used irradiate two

Figure 4. (A) Infrared thermal imaging after intravenously injected PBS and FEDA. (B) Tumor temperature change curves. (C) Tumor growth curves during PTT. D


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Figure 5. (A) In vivo CT imaging. (B, C) CT imagings and values of FEDA and iodixanol solutions at different concentrations (mg mL−1). (D) Tumor CT values (corresponding to Figure 5A).

Figure 6. (A) Cellular internalization analysis. (B) In vivo PL imaging. (C) Fluorescence signal intensities at kidney region (mean ± SD, n = 4).

tested through inherent red fluorescence. Figure 6A showed that FEDA was accumulated in cytoplasm and with the incubation time prolong the fluorescence intensity was clearly increased. The cytoplasm showed a weak red fluorescence after the FEDA was incubated for 2 h with 4T1 cells. However, after incubated for 48 h, the effect of red fluorescence showed clear uptake enhancement. Furthermore, fluorescence intensity distribution was tested at different time point after intravenous

attenuation than iodoxanol, and after 48 h injected, the tumor CT value was reached maximum. Therefore, the FEDA nanoparticles possessed a strongly potential for CT imaging in clinical diagnosis. This result confirmed that FEDA nanoparticles showed an excellent CT imaging ability. Cellular internalization of FEDA in 4T1 cells was tested by confocal laser scanning microscopy (CLSM). Hoechst 33342 was used to label nuclei (blue fluorescence), and FEDA were E


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Figure 7. (A) Histology analysis. (B) Body weight change after PTT. (C) Biodistribution of elemental Eu (mean ± SD, n = 6).

europium element was evidently accumulated in kidney after injected for 48 h, the europium elements content revealed a decline trend, respectively. On the contrary, the tumor revealed an increase trend due to the overexpression of the folate receptor on the surface of the cancer cells, which allowed the nanoparticles whose surface were grafted with folic acid to bind to the folate receptor via receptor-mediated endocytosis. This allowed nanoparticles to enter cancer cells first. In addition, the heart, liver, spleen, and lung retained a handful of europium elements after injected for 48 h, a lower uptake by reticuloendothelial system (RES) tissues.

injection. The kidney and liver showed a significant increase in fluorescence intensity after injected at 8 h, which was related to the high luminous character of europium (Figure 6B,C). Otherwise, the fluorescence intensity of mice began to decrease after injected FEDA at 12 h. Furthermore, 48 h after intravenous injection, the kidneys and liver were dominated metabolism organs for the FEDA nanoparticles. These results indicated that FEDA have an excellent PL imaging potential, which was attributed to the higher grafting rate. In summary, the prepared FEDA could be used as an outstanding CT/PL bioimaging-guided PTT nanoagent. 2.7. In Vivo Safety Evaluation. In this study, the FEDA safety was assessed by the change of body weight and HEstained histology analysis before being used as diagnosis and treatment reagent. After intravenous injection of PBS and FEDA nanoparticles 10 days, heart, liver, spleen, lung, and kidney (PBS, PBS + Laser, and FEDA) were detected and had no noticeable lesion (Figure 7A). However, the tumor in the experimental group was severely damaged. The tumor tissue structures of the FEDA + Laser groups were completely destroyed after irradiation. Another major indicator of body poisoning is weight analysis. The mice have no significant weight loss or death after treatment during the whole experiment (Figure 7B). All of these results indicated that FEDA nanoparticles possessed a promising prospect in clinical application as a cancer diagnostic and therapeutic agent. 2.8. Biodistribution in Vivo. For biodistribution in vivo, ICP-AES was used to detect metal ion concentration of europium in organs and tumors. As shown in Figure 7C, the

3. CONCLUSION This paper provided a facile way to construct a PDA-based FA targeted multifunctional reagent (FEDA) for dual-mode bioimaging-guided PTT via utilizing ATRP strategy. FEDA nanoparticles showed a high grafting rate, which led to strong X-ray attenuation and outstanding PL imaging property. Compared with the commonly used agents in clinical application, FEDA nanoparticles exhibited more outstanding imaging effect. Under the specific NIR irradiation for 10 min, the FEDA achieved an effective PTT in vitro, and the photothermal conversion efficiency ran up to 32.3%. In addition, the FEDA nanoparticles could be efficiently concentrated on the tumor region by sostenuto targeted effect as well as provided an outstanding CT/PL imaging and effective antitumor treatment. Furthermore, the favorable F


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(9) Liang, X.; Fang, L.; Li, X.; Zhang, X.; Wang, F. Activatable Near Infrared Dye Conjugated Hyaluronic Acid Based Nanoparticles as a Targeted Theranostic Agent for Enhanced Fluorescence/CT/Photoacoustic Imaging Guided Photothermal Therapy. Biomaterials 2017, 132, 72−84. (10) Zhong, Y.; Xue, F.; Wei, P.; Li, R.; Cao, C.; Yi, T. WaterSoluble Mos2 Quantum Dots for Facile and Sensitive Fluorescence Sensing of Alkaline Phosphatase Activity in Serum and Live Cells Based on the Inner Filter Effect. Nanoscale 2018, 10, 21298−21306. (11) Xu, P.; Liao, G. A Novel Fluorescent Biosensor for Adenosine Triphosphate Detection Based on a Metal-Organic Framework Coating Polydopamine Layer. Materials 2018, 11, 1616. (12) Liu, F.; He, X.; Lei, Z.; Liu, L.; Zhang, J.; You, H.; Zhang, H.; Wang, Z. Facile Preparation of Doxorubicin-Loaded Upconversion@ Polydopamine Nanoplatforms for Simultaneous In Vivo Multimodality Imaging and Chemophotothermal Synergistic Therapy. Adv. Healthcare Mater. 2015, 4, 559−568. (13) Li, Q.; Liao, G.; Tian, J.; Xu, Z. Preparation of Novel Fluorinated Copolyimide/Amine-Functionalized Sepia Eumelanin Nanocomposites with Enhanced Mechanical, Thermal, and UVShielding Properties. Macromol. Mater. Eng. 2018, 303, 1700407. (14) Kim, S.; Gim, T.; Jeong, Y.; Ryu, J. H.; Kang, S. M. Facile Construction of Robust Multilayered PEG Films on PolydopamineCoated Solid Substrates for Marine Antifouling Applications. ACS Appl. Mater. Interfaces 2018, 10, 7626−7631. (15) Li, Q.; Barrett, D. G.; Messersmith, P. B.; Holten-Andersen, N. Controlling Hydrogel Mechanics via Bio-Inspired Polymer-Nanoparticle Bond Dynamics. ACS Nano 2016, 10, 1317−1324. (16) Bernsmann, F.; Ball, V.; Addiego, F.; Ponche, A.; Michel, M.; Gracio, J. J.; Toniazzo, V.; Ruch, D. Dopamine-Melanin Film Deposition Depends on the Used Oxidant and Buffer Solution. Langmuir 2011, 27, 2819−2825. (17) Cong, Y.; Xia, T.; Zou, M.; Li, Z.; Peng, B.; Guo, D.; Deng, Z. Mussel-Inspired Polydopamine Coating as a Versatile Platform for Synthesizing Polystyrene/Ag Nanocomposite Particles with Enhanced Antibacterial Activities. J. Mater. Chem. B 2014, 2, 34−50. (18) Wang, Y.; Shang, B.; Hu, X.; Peng, B.; Deng, Z. Temperature Control of Mussel-Inspired Chemistry toward Hierarchical Superhydrophobic Surfaces for Oil/Water Separation. Adv. Mater. Interfaces 2017, 4, 1600727. (19) Deng, Z.; Shang, B.; Peng, B. Polydopamine Based Colloidal Materials: Synthesis and Applications. Chem. Rec. 2018, 18, 410−432. (20) Zhang, M.; Zhang, L.; Chen, Y.; Li, L.; Su, Z.; Wang, C. Precise Synthesis of Unique Polydopamine/Mesoporous Calcium Phosphate Hollow Janus Nanoparticles for Imaging-Guided Chemo-Photothermal Synergistic Therapy. Chem. Sci. 2017, 8, 8067−8077. (21) Huang, P.; Bao, L.; Zhang, C.; Lin, J.; Luo, T.; Yang, D.; He, M.; Li, Z.; Gao, G.; Gao, B.; Fu, S.; Cui, D. Folic Acid-Conjugated Silica-Modified Gold Nanorods for X-Ray/CT Imaging-Guided DualMode Radiation and Photo-Thermal Therapy. Biomaterials 2011, 32, 9796−9809. (22) Liu, J.; Chen, H.; Fu, Y.; Li, X.; Chen, Y.; Zhang, H.; Wang, Z. Fabrication of Multifunctional Ferric Oxide Nanoparticles for TumorTargeted Magnetic Resonance Imaging and Precise Photothermal Therapy with Magnetic Field Enhancement. J. Mater. Chem. B 2017, 5, 8554−8562. (23) Hu, D.; Liu, C.; Song, L.; Cui, H.; Gao, G.; Liu, P.; Sheng, Z.; Cai, L. Indocyanine Green-Loaded Polydopamine-Iron Ions Coordination Nanoparticles for Photoacoustic/Magnetic Resonance DualModal Imaging-Guided Cancer Photothermal Therapy. Nanoscale 2016, 8, 17150−17158. (24) Ding, X.; Liu, J.; Liu, D.; Li, J.; Wang, F.; Li, L.; Wang, Y.; Song, S.; Zhang, H. Multifunctional Core/Satellite Polydopamine@Nd3+Sensitized Upconversion Nanocomposite: A Single 808 nm NearInfrared Light-Triggered Theranostic Platform for In Vivo ImagingGuided Photothermal Therapy. Nano Res. 2017, 10, 3434−3446. (25) Fan, Q. L.; Neoh, K. G.; Kang, E. T.; Shuter, B.; Wang, S. C. Solvent-Free Atom Transfer Radical Polymerization for the Preparation of Poly (Poly (Ethyleneglycol) Monomethacrylate)-

biocompatibility and low toxicity ensured FEDA can be potentially used in diagnosis and treatment applications.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsabm.8b00797. Materials and methods, calculation of photothermal conversion efficiency (η), TEM and SEM images, hydrodynamic diameter analysis, EDS spectrum analysis, survey XPS spectra, photothermal response, linear time data (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Guangfu Liao: 0000-0003-1299-8106 Zushun Xu: 0000-0001-7314-170X Author Contributions ⊥

These two authors contributed equally to this project.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This paper was supported by the National Natural Science Foundation of China (Grant No. 51573039). REFERENCES

(1) Roy, E.; Patra, S.; Madhuri, R.; Sharma, P. Carbon Dot/TAT Peptide Co-conjugated Bubble Nanoliposome for Multicolor Cell Imaging, Nuclear-Targeted Delivery, and Chemo/Photothermal Synergistic Therapy. Chem. Eng. J. 2017, 312, 144−157. (2) Zou, Y.; Sun, F.; Liu, C.; Yu, C.; Zhang, M.; He, Q.; Xiong, Y.; Xu, Z.; Yang, S.; Liao, G. A Novel Nanotheranostic Agent for DualMode Imaging-Guided Cancer Therapy Based on Europium Complexes-Grafted-Oxidative Dopamine. Chem. Eng. J. 2019, 357, 237−247. (3) Zhang, M.; Wang, W.; Wu, F.; Yuan, P.; Chi, C.; Zhou, N. Magnetic and Fluorescent Carbon Nanotubes for Dual Modal Imaging and Photothermal and Chemo-Therapy of Cancer Cells in Living Mice. Carbon 2017, 123, 70−83. (4) Zhang, M.; Wang, J.; Wang, W.; Zhang, J.; Zhou, N. Magnetofluorescent Photothermal Micelles Packaged with GdN@ CQDs as Photothermal and Chemical Dual-Modal Therapeutic Agents. Chem. Eng. J. 2017, 330, 442−452. (5) Bao, Y.; Hua, X.; Chen, X.; Wu, F. Platinum-Doped Carbon Nanoparticles Inhibit Cancer Cell Migration Under Mild Laser Irradiation: Multi-Organelle-Targeted Photothermal Therapy. Biomaterials 2018, 183, 30−42. (6) Tian, Q.; Jiang, F.; Zou, R.; Liu, Q.; Chen, Z.; Zhu, M.; Yang, S.; Wang, J.; Wang, J.; Hu, J. Hydrophilic Cu9S5 Nanocrystals: A Photothermal Agent with a 25.7% Heat Conversion Efficiency for Photothermal Ablation of Cancer Cells In Vivo. ACS Nano 2011, 7, 9761−9771. (7) Han, L.; Zhang, Y.; Zhang, Y.; Shu, Y.; Chen, X.; Wang, J. A Magnetic Polypyrrole/Iron Oxide Core/Gold Shell Nanocomposite for Multimodal Imaging and Photothermal Cancer Therapy. Talanta 2017, 171, 32−38. (8) Yang, K.; Xu, H.; Cheng, L.; Sun, C.; Wang, J.; Liu, Z. In Vitro and In Vivo Near-Infrared Photothermal Therapy of Cancer Using Polypyrrole Organic Nanoparticles. Adv. Mater. 2012, 24, 5586− 5592. G


Letter

ACS Applied Bio Materials Grafted Fe3O4 Nanoparticles: Synthesis, Characterization and Cellular Uptake. Biomaterials 2007, 28, 5426−5436. (26) Zhou, Y.; Wang, S.; Ding, B.; Yang, Z. Modification of Magnetite Nanoparticles via Surface-Initiated Atom Transfer Radical Polymerization (ATRP). Chem. Eng. J. 2008, 138, 578−585. (27) Zou, Y.; Jin, H.; Sun, F.; Dai, X.; Xu, Z.; Yang, S.; Liao, G. Design and Synthesis of Lead Sulfide-Based Nanotheranostic Agent for Computer Tomography/Magnetic Resonance Dual-Mode Bioimaging Guided Photothermal Therapy. ACS Appl. Nano. Mater. 2018, 1, 2294−2305. (28) Wang, X.; Tu, M.; Yan, K.; Li, P.; Pang, L.; Gong, Y.; Li, Q.; Liu, R.; Xu, Z.; Xu, H.; Chu, P. K. Trifunctional Polymeric Nanocomposites Incorporated with Fe3O4/Iodine-Containing Rare Earth Complex for Computed X-ray Tomography, Magnetic Resonance, and Optical Imaging. ACS Appl. Mater. Interfaces 2015, 7, 24523−24532. (29) Liao, G.; Chen, J.; Zeng, W.; Yu, C.; Yi, C.; Xu, Z. Facile Preparation of Uniform Nanocomposite Spheres with Loading Silver Nanoparticles on Polystyrene-methyl Acrylic Acid Spheres for Catalytic Reduction of 4-Nitrophenol. J. Phys. Chem. C 2016, 120, 25935−25944. (30) Liao, G.; Li, Q.; Zhao, W.; Pang, Q.; Gao, H.; Xu, Z. In-Situ Construction of Novel Silver Nanoparticle Decorated Polymeric Spheres as Highly Active and Stable Catalysts for Reduction of Methylene Blue Dye. Appl. Catal., A 2018, 549, 102−111.

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