Hyaluronic Acid-Coated Silver Nanoparticles As a Nanoplatform for in

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Hyaluronic acid-coated silver nanoparticles as a nanoplatform for in vivo imaging applications Xin Zhang, Meinan Yao, Muhua Chen, Liqiang Li, Chengyan Dong, Yi Hou, Huiyun Zhao, Bing Jia, and Fan Wang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • Publication Date (Web): 20 Sep 2016 Downloaded from http://pubs.acs.org on September 20, 2016

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ACS Applied Materials & Interfaces

Hyaluronic acid-coated silver nanoparticles as a nanoplatform for in vivo imaging applications ‡

§

Xin Zhang, † Meinan Yao, †Muhua Chen, † Liqiang Li, † Chengyan Dong, Yi Hou, Huiyun Zhao, †,⊥ Bing Jia, *, †,⊥ and Fan Wang,*,†,‡

†

Medical Isotopes Research Center and Department of Radiation Medicine, School of Basic

Medical Sciences, Peking University Health Science Center, Beijing 100191, China

‡

Key Laboratory of Protein and Peptide Pharmaceuticals, CAS Center for Excellence in

Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China

§

Institute of Chemistry, Chinese Academy of Sciences, Beijing 100190, China

⊥

Medical and Healthy Analytical Center, Peking University, Beijing 100191, China

KEYWORDS. HA-Ag NPs, long-term stability, low cytotoxicity, nanoplatform, X-ray computed tomography (CT), SPECT imaging ABSTRACT. An efficient chemical reduction protocol has been developed for the synthesis of hyaluronic acid-coated silver nanoparticles (HA-Ag NPs) that are spherical, ultrasmall and monodisperse. The as-synthesized HA-Ag NPs not only exhibited excellent long-term stability

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and low cytotoxicity but also could be used as a nanoplatform for X-ray computed tomography (CT) and single-photon emission computed tomography (SPECT) imaging after being radiolabeled with 99mTc.

Noble-metal nanoparticles (NPs) have been extensively used in a wide variety of fields, including catalysis, photochemistry and medicine.1-3 In particular, silver nanoparticles (Ag NPs) have attracted great attention due to their novel physicochemical, optical, conductive and antimicrobial properties.4-6 Despite the wide use of Ag NPs, few studies have examined their biological activities because the development of silver-based nanomaterials has been limited by their toxicity and undesirable chemical stability which was caused by their susceptibility to oxidation.7, 8 Over recent decades, various synthetic efforts have been made and a number of studies have focused on the mechanisms of Ag NP-induced toxicity.9-11 However, achieving long-term stability and minimizing the cytotoxicity of Ag NPs remain major challenges.

Previous studies have demonstrated the synthesis of Ag NPs with various ligand coatings, such as citrate, poly(N-vinylpyrrolidon), poly(acrylic acid) and collagen.12-14 Surface chemistry has been shown to strongly influence both the toxicity of Ag NPs and the interactions of Ag NPs with biological systems.15, 16 Thus, employing various ligand coatings to chemically alter surface properties is a promising method for minimizing the toxicity and improving the stability of Ag NPs. Significant eﬀorts have been made to achieve this goal, including the design of thiolated Ag


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NPs and Ag NPs encapsulated with non-toxic amorphous silica.16-19 However, these modifications could have a detrimental impact on the interactions of Ag NPs with biological systems.16 Therefore, biological ligands such as biomacromolecules9, 20 that bind strongly and have little biological impact are actively being explored.

Hyaluronic acid (HA) is a high-molecular-weight glycosaminoglycan with excellent biocompatibility present in almost all biological fluids and tissues;21 HA is regarded as an extracellular matrix component that facilitates cell locomotion and proliferation.22 HA possesses a large number of negatively charged carboxyl groups, which strongly interact with Ag+ ions, thereby enabling the formation of stable Ag NP complexes.1 These features make HA a promising ligand for coating Ag NPs to achieve low cytotoxicity and prolonged stability. In addition, the abundant carboxyl groups can be functionalized with specific moieties easily and covalently; in this way, Ag NPs could serve as a nanoplatform for various biological applications. There have been several reports of hyaluronan fibers1 or HA-based nanofibrous membranes23 synthesized as Ag NP scaffolds specifically for antibacterial applications. However, very few studies have attempted to synthesize HA-coated Ag NPs, and little is known about the potential in vivo applications of this material. Cui et al. fabricated Ag nanostructures by using HA as a stabilizing agent via photoreduction.24 The size and morphology of these silver nanostructures changed with different irradiation times, and sedimentation was observed after extensive


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irradiation. These results demonstrate the difficulty of controlling irradiation conditions to obtain monodisperse Ag NPs of uniform morphology.

In this study, we used the borane-based reducing agent sodium borohydride (NaBH4) to rapidly reduce Ag+ complexes into spherical, monodisperse and ultrasmall Ag NPs. The assynthesized HA-Ag NPs exhibited excellent long-term stability and very low cytotoxicity, even at high concentrations. As illustrated in Graphic for manuscript, X-ray attenuation could be measured via computed tomography (CT) imaging, which indicated that HA-Ag NPs held great promise as a CT contrast agent. After being functionalized with the chelator 6hydrazinonicotinyl and radiolabeled with

99m

Tc, the HA-Ag NPs could be used as a radiotracer

for both tumor single-photon emission computed tomography (SPECT) imaging and evaluating their distribution in vivo, since the hydrodynamic diameter (HD) of the 99mTc-HA-Ag NPs would permit their passive accumulation in tumors via the enhanced permeability and retention (EPR) effect.25, 26

To synthesize the HA-stabilized Ag NPs, HA was incubated with AgNO3 to allow Ag+ to bind to the carboxyl groups on the HA backbones. Then, aqueous NaBH4 was added dropwise into the AgNO3/HA solution with vigorous stirring, which resulted in the solution immediately changing from colorless to yellowish brown. The UV-vis spectra of the solution showed an absorption band centered at 395 nm, which indicated the formation of HA-Ag NPs (Fig. S1). Cryo-transmission electron microscopy (cryo-TEM) was used to verify the successful synthesis


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of monodisperse HA-Ag NPs with a uniform size distribution. The HD measured using dynamic light scattering (DLS) was 13.5 nm, which was consistent with the cryo-TEM results (Fig. 1a). The zeta potential of the HA-Ag NPs was -35.5 mV due to the carboxylic acid groups on the NP surface (Fig. S2). The long-term stability of the HA-Ag NPs was assessed using continuous DLS measurements; little change was observed over a period of 15 days (Fig. 1b), and the samples remained suspended for at least 30 days when stored at 4 °C (Fig. S3).

RAW264.7 macrophages were used to assess HA-Ag NP cytotoxicity. The cells were incubated with increasing concentrations of HA-Ag NPs for 24 and 48 h, and the number of viable cells was measured using a colorimetric cell-counting kit 8 (CCK-8) assay. The cell survival results are expressed as treatment over control (T/C) values. Equal concentrations of citrate-coated Ag NPs (citrate-Ag NPs) were used for contrast. The cells incubated with HA-Ag NPs for 24 h showed increased viability up to 800 µM, and slight toxicity was observed at 1,000 µM, the highest concentration tested. The citrate-Ag NPs were strongly cytotoxic, resulting in 25.5% cell viability at 400 µM, and viability continued to decrease with increasing NP concentrations (Fig. 2a). The cells incubated with HA-Ag NPs for 48 h showed increased viability up to 600 µM, and significant toxicity was observed at 1,000 µM, which resulted in a cell viability of 28.1%. The citrate-Ag NPs were strongly cytotoxic after 48 h, resulting in a cell viability of 57.3% at 200 µM; furthermore, viability remained below 10% at higher


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concentrations (Fig. 2b). Taken together, these results indicate that the biological HA coating plays a prominent role in the decreased cytotoxicity of the HA-Ag NPs.

X-ray CT is one of the most powerful noninvasive diagnostic imaging techniques in modern medicine.27 The unique properties of nanomaterials, including long circulating half-life, passive accumulation at tumor sites, facile surface modification, and multifunctionality, are advantages of using nanomaterials as CT contrast agents.28 The X-ray attenuation of the HA-Ag NPs was explored to assess the potential of this material for use in CT imaging. The CT image intensity clearly increased with HA-Ag NP concentration (Fig. 3a). By plotting the CT value (in Hounsfield units, HU) at different concentrations (Fig. 3b), we can see that this increase in CT value with HA-Ag NP concentration was linear. HA-Ag NPs must exhibit good X-ray attenuation to be effective contrast agents for sensitive CT imaging applications.

As the observed HD of 13.5 nm is desirable for tumor targeting via the EPR effect, SPECT imaging was performed to examine the passive tumor-targeting capability of these particles in mice. HA-Ag NPs were labeled with

99m

Tc using tricine and trisodium triphenylphosphine-

3,3’,3’’-trisulfonate (TPPTS) as coligands.29,

30

The radiolabeled HA-Ag NPs (99mTc-HA-Ag

NPs) exhibited slightly different HD and zeta potential values compared with the unlabeled particles (Fig. S2). Female C57 mice bearing Lewis lung carcinoma (LLC) tumor xenografts were injected with 20.4 MBq of

99m

Tc-HA-Ag NPs via the tail vein to evaluate the

biodistribution of this radiotracer in tumor tissues and major organs (n=3). As a control


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experiment, 37 MBq of

99m

Tc-HA were administered into LLC bearing mice via intravenous

injection (n=3). At 2, 4, 8, and 12 h post-injection (p.i.), the mice were anesthetized by inhaling 2% isoflurane and imaged using the NanoSPECT/CT system. As shown in Fig. 3c, the LLC tumor lesions were clearly visualized by the 99mTc-HA-Ag NPs with a high contrast at each time point. In addition, the maximum tumor uptake of 2.21 ID% (percent of the injected dose) occurred at 8 h p.i., which then dropped to 1.79 ID% at 12 h p.i. (Fig. 3d). SPECT imaging revealed strong

99m

Tc-HA-Ag NP signals in the abdominal area, particularly in the liver and

spleen, which indicated NP circulation via the reticuloendothelial system. The HA-Ag NPs exhibited very low kidney accumulation from 2 to 12 h. As the particles are negatively charged and very small, they can avoid renal excretion and accumulate at tumor sites after prolonged 99m

circulation. As shown in Fig. S8, compared with

Tc-HA-Ag NPs showed different biodistribution patterns

99m

Tc-HA and the background signal was very low.

quantitative analysis (Fig. S9),

According to the

99m

Tc-HA-Ag NPs performed a much lower uptake in intestine,

bone and muscle, while the uptake values in LLC tumors were much higher. The tumor-tomuscle and tumor-to-bone activity ratios of

99m

Tc-HA-Ag NPs were 8.5 and 7.88 at 8 h p.i.,

while the ratios were 2.31 and 0.94 for 99mTc-HA. These results demonstrated that 99mTc-HA-Ag NPs hold the capability for effective tumor SPECT imaging.

In summary, we have developed a rapid and simple chemical reduction approach to synthesize HA-Ag NPs that are spherical, ultrasmall and monodisperse. Furthermore, the as-


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synthesized HA-Ag NPs exhibited excellent stability and low cytotoxicity, which have been major challenges for the development of Ag NPs. To the best of our knowledge, this is the first nanoplatform based on Ag NPs specifically designed and synthesized for in vivo imaging applications. (1) The HA-Ag NPs exhibited good X-ray attenuation via CT imaging, indicating their potential to be used as a sensitive CT contrast agent. (2) Tumor SPECT imaging demonstrated the efficient accumulation of 99mTc-HA-Ag NPs at tumor sites with high tumor-tomuscle activity ratios. Further investigations should focus on developing this HA-Ag NP nanoplatform into a drug delivery system comprising function-specific components for use as an efficient tumor theranostic agent.


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Figure 1. (a) Size distribution histogram of HA-Ag NPs based on DLS measurement. Inset image shows the Freeze Transmission Electron Microscope (Cryo-TEM) image of freshly prepared HA-Ag NPs, scale bar = 10 nm. (b) Continuous DLS measurements of HA-Ag NPs until 15 days. The hydrodynamic diameter (HD) were presented as the average of hydrodynamic diameter measurements (n>3).

Figure 2. Viability of RAW 264.7 cells treated with different concentrations of HA-Ag NPs or Citrate-Ag NPs for 24 h (a) and 48 h (b). The values represent the mean of independent experiments normalized to untreated controls.


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Figure 3. (a-b) CT imaging and quantitative CT value (in HU) of HA-Ag NPs at different concentrations. (c) Representative whole-body NanoSPECT/CT images of C57 mice with LLC tumor xenografts obtained at 2, 4, 8, and 12 h after 99mTc-HA-Ag NPs injection. Tumor, liver, spleen and bladder were marked by T, L, S and B, respectively. (d) Uptake values (ID%) in tumor site obtained from NanoSPECT images taken at different times. ASSOCIATED CONTENT

Supporting Information.

Experimental details; cell culture and animal models; synthesis of HY-HA; synthesis of HA-Ag NPs and citrate-Ag NPs;

99m

Tc radiolabeling and in vivo SPECT/CT imaging; cytotoxicity test;

additional tables and figures (PDF)

AUTHOR INFORMATION Corresponding Author


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*Fan Wang. E-mail: [email protected]

*Bing Jia. E-mail: [email protected] Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT This research was supported by National Natural Science Foundation of China (NSFC) projects (81371614, 81125011, 81321003, 81427802, 81420108019, 81630045), a grant from the Beijing Ministry of Science and Technology (Z141100000214004), and Strategic Priority Research Program of the Chinese Academy of Sciences (XDA12020216). REFERENCES (1) Abdel-Mohsen, A. M.; Hrdina, R.; Burgert, L.; Krylova, G.; Abdel-Rahman, R. M.; Krejcova, A.; Steinhart, M.; Benes, L. Green Synthesis of Hyaluronan Fibers with Silver Nanoparticles. Carbohydr. Polym. 2012, 89, 411-422. (2) Jin, R.; Cao, Y. C.; Hao, E.; Metraux, G. S.; Schatz, G. C.; Mirkin, C. A. Controlling Anisotropic Nanoparticle Growth through Plasmon Excitation. Nature 2003, 425, 487-490. (3) Noginov, M. A.; Zhu, G.; Belgrave, A. M.; Bakker, R.; Shalaev, V. M.; Narimanov, E. E.; Stout, S.; Herz, E.; Suteewong, T.; Wiesner, U. Demonstration of a Spaser-based Nanolaser. Nature 2009, 460, 1110-1112. (4) Li, W.; Camargo, P. H.; Lu, X.; Xia, Y. Dimers of Silver Nanospheres: Facile Synthesis and Their Use as Hot Spots for Surface-enhanced Raman Scattering. Nano Lett. 2009, 9, 485-490. (5) Ahamed, M.; Alsalhi, M. S.; Siddiqui, M. K. Silver Nanoparticle Applications and Human Health. Clin. Chim. Acta 2010, 411, 1841-1848. (6) Chudobova, D.; Nejdl, L.; Gumulec, J.; Krystofova, O.; Rodrigo, M. A.; Kynicky, J.; Ruttkay-Nedecky, B.; Kopel, P.; Babula, P.; Adam, V.; Kizek, R. Complexes of Silver(I) Ions and Silver Phosphate Nanoparticles with Hyaluronic Acid and/or Chitosan as Promising Antimicrobial Agents for Vascular Grafts. Int. J. Mol. Sci. 2013, 14, 13592-13614.


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Graphic for manuscript.


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Hyaluronic Acid-Coated Silver Nanoparticles As a Nanoplatform for in

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