Elsevier

Biomaterials

Volume 35, Issue 13, April 2014, Pages 4058-4065
Biomaterials

Structure-dependent photothermal anticancer effects of carbon-based photoresponsive nanomaterials

https://doi.org/10.1016/j.biomaterials.2014.01.043Get rights and content

Abstract

Here, we report the effect of structure on the biological properties of photoresponsive carbon nanomaterials. Poloxamer 407-functionalized single-walled carbon nanotubes (PSWCNT) and poloxamer 407-functionalized graphene nanosheets (PGNS) exhibited similar physical stability and heating capacities after irradiation with an 808 nm near-infrared (NIR) laser. Despite sharing common physical properties, the cellular uptake of the PSWCNT and PGNS differed significantly. Cancer cells treated with PGNS took up a higher quantity of the nanosheets than of the PSWCNT and displayed a higher rate of cancer cell killing upon laser irradiation. Structure of carbon nanomaterials also affected the in vivo behaviors. PGNS could circulate in the blood 2.2 times longer than that of the PSWCNT. PGNS accumulated in the SCC tumor tissues to a greater degree than did PSWCNT over 7 days. NIR irradiation resulted in the complete ablation of tumor tissues in the PGNS-treated group but not in the other groups. After NIR irradiation, 100% of the PGNS-treated and NIR-irradiated mice survived until day 70. These results suggest the importance of structure in controlling the in vivo behaviors of carbon nanomaterials. Moreover, the results indicate the structural advantages of nanosheets over nanotubes in the enhancement of photothermal anticancer effects.

Introduction

Although remarkable progress has been made in cancer treatment, conventional strategies, such as surgical resection, chemotherapy, radiotherapy, and their combinations have shown limited success toward cancer eradication over the past few decades. Photothermal therapy (PTT) for the treatment of solid tumors recently emerged as an attractive alternative approach to converting absorbed light into local heating through nonradiative mechanisms [1]. Anticancer PTT is advantageous over surgical methods and chemotherapy because it permits spatial and temporal control, is minimally invasive, and results in few complications [2], [3], [4].

Near-infrared (NIR) light (700–1100 nm) is used in PTT because it penetrates deeply into the tissue and is absorbed only to a small degree by normal tissue [5], [6]. Light-absorbing agents that display a high degree of absorption in the NIR are generally involved in PTT processes to facilitate energy conversion from light to heat in localized tumor tissues. Experimentally tested photoresponsive light absorbers include gold [2], [7], and carbon nanomaterials such as carbon nanotubes [8] and graphene [9], [10].

Single-walled carbon nanotubes (SWCNT) and graphene nanosheets have been studied for their utility in photothermal cancer treatment. Intratumoral injection of phospholipid-polyethylene glycol-coated SWCNT [8] or polyethylene glycol-conjugated SWCNT [11] has been reported to destroy tumors upon irradiation with NIR laser. Intravenous injection of polyethylene glycol-conjugated graphene nanosheets [9] has been shown to provide NIR laser-induced antitumor photothermal effects. Polyvinylpyrrolidone-coated graphene nanosheets were reported to induce photothermal death of human glioma cells [12].

Although previous studies described the potential utility of SWCNTs and graphene-based nanosheets in PTT, it is little studied whether the different geometry of these carbon-based nanomaterials could influence the biological and pharmacological effects. In this study, using amphiphilic triblock copolymer-functionalized SWCNT and graphene nanosheets, we tested whether the structure of carbon-based nanomaterials could affect their physical properties, in vivo fates, and photothermal anticancer effects.

Section snippets

Preparation of carbon nanomaterials functionalized with poloxamer 407

Graphene nanosheets functionalized with poloxamer 407 (PGNS) were prepared by the aqueous-phase exfoliation of graphite in the presence of poloxamer 407 (Sigma–Aldrich, St. Louis, MO, USA), as described previously [13]. In brief, 50 mg graphite powder (Sigma–Aldrich) was suspended in 50 mL of a 1% w/v poloxamer 407 solution. The dispersions were sonicated over ice for 2 h using a horn ultrasonicator equipped with a 13 mm diameter probe (VCX 500, Sonics & materials, Inc., Newtown, CT, USA). The

Characterization and thermal conductivity of carbon-based nanomaterials

PSWCNT and PGNS provided similar dispersions, UV spectra, and photothermal conductivity values (Fig. 1A). Both PSWCNT and PGNS were freely dispersed in fetal bovine serum (Fig. 1B). The absorption patterns of the UV–vis spectra of the two carbon-based nanomaterials showed peaks at 260–270 nm and tapered down at longer wavelengths (Fig. 1C). TEM measurements revealed the unique nanotube and nanosheet structures for PSWCNT (Fig. 1D) and PGNS (Fig. 1E), respectively. The photothermal properties of

Discussion

This study demonstrated that the in vitro and in vivo behaviors of photoresponsive carbon nanomaterials differed significantly depending on their structures. The structure of carbon-based nanomateris affected the in vitro cellular uptake and photo-induced antitumor effects. Moreover, the structure of carbon nanomaterials affected the pharmacokinetics, tumor accumulation, and photothermal tumor ablation capacity. The structure comparison study showed that PGNS was greater than the corresponding

Conclusions

Our study showed that the geometry of the carbon nanomaterials affected the cellular uptake, in vivo fate, and the efficacy of photothermal anticancer therapy. Compared to PSWCNT, PGNS provided a higher cellular uptake, longer blood circulation time, preferential distribution in the tumor tissue, higher photothermal effect. Unlike PSWCNT, PGNS were effective in providing photothermal anticancer effects and in prolonging the complete survival of the mice over 70 days. The results indicate that

Acknowledgments

This work was supported by research grants from the Ministry of Science, ICT and Future Planning (2013K000264; 2013035166), from the Bio & Medical Technology Development Program of the National Research Foundation funded by the Korean government (MSIP) (2013036131), and from the Korean Health Technology R&D project, Ministry of Health and Welfare (A092010).

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