The application of titanium dioxide (TiO2) nanoparticles in the photo-thermal therapy of melanoma cancer model

Document Type: Original Article

Authors

1 Nano Opto-Electronic Research Center, Electrical and Electronics Engineering Department, Shiraz University of Technology, Shiraz, Iran

2 Quality Control Department, Faculty of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran

3 Pharmaceutical Sciences Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

4 Pathology Department, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract

Objective(s): Photo-thermal therapy (PTT) is a therapeutic method in which photon energy is converted into heat to induce hyperthermia in malignant tumor cells. In this method, energy conversion is performed by nanoparticles (NPs) to enhance induced heat efficacy. The low-cytotoxicity and high optical absorbance of NPs used in this technique are very important. In the present study, titanium dioxide (TiO2) NPs were used as agents for PTT. For increasing water dispersibility and biocompatibility, polyethylene glycol (PEG)-TiO2 NPs (PEGylated TiO2 NPs) were synthesized and the effect of these NPs on reducing melanoma tumor size after PTT was experimentally assessed.
Materials and Methods: To improve the dispersibility of TiO2 NPs in water, PEG was used for wrapping the surface of TiO2 NPs. The formation of a thin layer of PEG around the TiO2 NPs was confirmed through thermo-gravimetric analysis and transmission electron microscopy techniques. Forty female cancerous mice were divided into four equal groups and received treatment with NPs and a laser diode (λ = 808 nm, P = 2 W & I = 2 W/cm2) for seven min once in the period of the treatment.
Results: Compared to the mice receiving only the laser therapy, the average tumor size in the mice receiving TiO2-PEG NPs with laser excitation treatment sharply decreased.
Conclusion: The results of animal studies showed that PEGylated TiO2 NPs were exceptionally potent in destroying solid tumors in the PTT technique.

Keywords

Main Subjects


1. Ortiz R, Melguizo C, Prados J, Alvarez PJ, Caba O, Rodriguez-Serrano F, et al. New gene therapy strategies for cancer treatment: a review of recent patents. Recent Pat Anticancer Drug Discov 2012; 7:297–312.
2. Bertrand N, Leroux J-CC. The journey of a drug-carrier in the body: an anatomo-physiological perspective. J Control Release 2012; 161:152–163.
3. Behnam MA, Emami F, Sobhani Z, Koohi-Hosseinabadi O, Dehghanian AR, Zebarjad SM, et al. Novel combination of silver nanoparticles and carbon nanotubes for plasmonic photo thermal therapy in melanoma cancer model. Adv Pharm Bull 2018; 8:49-55.
4. Moosavi Nejad S, Takahashi H, Hosseini H, Watanabe A, Endo H, Narihira K, et al. Acute effects of sono-activated photocatalytic titanium dioxide nanoparticles on oral squamous cell carcinoma. Ultrason Sonochem 2016; 32:95–101.
5. Yin ZF, Wu L, Yang HG, Su YH. Recent progress in biomedical applications of titanium dioxide. Phys Chem Chem Phys 2013; 15:4844–4858.
6. Bibin AB, Kume K, Tsutumi K, Fukunaga Y, Ito S, Imamura Y, et al. Observation the distribution of titanium dioxide nano-particles in an experimental tumor tissue by a raman microscope. AIP Conf Proc 2011; 55–58.
7. Uehara M, Ikeda H, Nonaka M, Sumita Y, Nanashima A, Nonaka T, et al. Predictive factor for photodynamic therapy effects on oral squamous cell carcinoma and oral epithelial dysplasia. Arch Oral Biol 2011; 56:1366–1372.
8. Yakunin AN, Avetisyan Y, Tuchin VV. Quantification of laser local hyperthermia induced by gold plasmonic nanoparticles. J Biomed Opt 2015; 20:51030–51030.
9. Thompson EA, Graham E, Macneill CM, Young M, Donati G, Wailes EM, et al. Differential response of MCF7, MDA-MB-231, and MCF 10A cells to hyperthermia, silver nanoparticles and silver nanoparticle-induced photothermal therapy. Int J Hyperthermia 2014; 30:312–323.
10.     Sobhani Z, Behnam MA, Emami F, Dehghanian A, Jamhiri I. Photothermal therapy of melanoma tumor using multiwalled carbon nanotubes. Int J Nanomedicine 2017; 12:4509–4517.
11.     Jhuang YY, Cheng WT. Fabrication and characterization of silver/titanium dioxide composite nanoparticles in ethylene glycol with alkaline solution through sonochemical process. Ultrason Sonochem 2016; 28:327–333.
12.     Eskandarloo H, Badiei A, Behnajady MA, Ziarani GM. Ultrasonic-assisted sol-gel synthesis of samarium, cerium co-doped TiO2 nanoparticles with enhanced sonocatalytic efficiency. Ultrason Sonochem 2015; 26:281–292.
13.     Jugan ML, Barillet S, Simon-Deckers A, Sauvaigo S, Douki T, Herlin N, et al. Cytotoxic and genotoxic impact of TiO2 nanoparticles on A549 cells. J Biomed Nanotechnol 2011; 7:22–23.
14.     Carp O, Huisman CL, Reller  A. Photoinduced reactivity of titanium dioxide. Prog Solid State Chem 2004; 32:33–177.
15.     Haseeb A, Hasan MM, Masjuki HH. Structural and mechanical properties of nanostructured TiO2 thin films deposited by RF sputtering. Surf Coat Technol 2010; 205:338–344.
16.     He Q, Wen X, Ma P, Deng X. Alkali induced morphology and property improvements of TiO2 by hydrothermal treatment. J Wuhan University Tech-Mater. Sci. Ed 2008; 23:503–506.
17.     Tanner K E. Titanium in medicine. Proc Inst Mech Eng H 2016; 216:215-215.
18.     Devanand Venkatasubbu G, Ramasamy S, Ramakrishnan V, Kumar J. Folate targeted PEGylated titanium dioxide nanoparticles as a nanocarrier for targeted paclitaxel drug delivery. Adv Powder Technol 2013; 24:947–954.
19.     Yamaguchi S, Kobayashi H, Narita T, Kanehira K, Sonezaki S, Kudo N, et al. Sonodynamic therapy using water-dispersed TiO2-polyethylene glycol compound on glioma cells: comparison of cytotoxic mechanism with photodynamic therapy. Ultrason Sonochem 2011; 18:1197–1204.
20.     Wang R, Hashimoto K, Fujishima A, Chikuni M, Kojima E, Kitamura A, et al. Light-induced amphiphilic surfaces. Nature 1997; 388:431–432.
21.     Xu P, Wang R, Ouyang J, Chen B. A new strategy for TiO2 whiskers mediated multi-mode cancer treatment. Nanoscale Res Lett 2015; 10:94–104.
22.     Ren W, Zeng L, Shen Z, Xiang L, Gong A, Zhang J, et al. Enhanced doxorubicin transport to multidrug resistant breast cancer cells via TiO2 nanocarriers. RSC Adv 2013; 3:20855–20855.
23.     Liu E, Zhou Y, Liu Z, Li J, Zhang D, Chen J, et al. Cisplatin loaded hyaluronic acid modified TiO2 nanoparticles for neoadjuvant chemotherapy of ovarian cancer. J Nanomater 2015; 2015:1–8.
24.     Zhang Z, Wang J, Nie X, Wen T, Ji Y, Wu X, et al. Near infrared laser-induced targeted cancer therapy using thermoresponsive polymer encapsulated gold nanorods. J Am Chem Soc 2014; 136:7317–7326.
25.     Brownell J, Wang S, Tsoukas MM. Phototherapy in cosmetic dermatology. Clin Dermatol 2016; 34:623–627.
26.     Narayanan DL, Saladi RN, Fox JL. Review: ultraviolet radiation and skin cancer. Int J Dermatol 2010; 49:978–986.
27.     Jiao Z, Chen Y, Wan Y, Zhang H. Anticancer efficacy enhancement and attenuation of side effects of doxorubicin with titanium dioxide nanoparticles. Int J Nanomedicine 2011; 6:2321–2326.
28.     Li Q, Wang X, Lu X, Tian H, Jiang H, Lv G, et al. The incorporation of daunorubicin in cancer cells through the use of titanium dioxide whiskers. Biomaterials 2009; 30:4708–4715.
29.     López T, Sotelo J, Navarrete J, Ascencio JA. Synthesis of TiO2 nanostructured reservoir with temozolomide: structural evolution of the occluded drug. Opt Mater 2006; 29:88–94.
30.     Kim C, Kim S, Oh WK, Choi M, Jang J. Efficient intracellular delivery of camptothecin by silica/titania hollow nanoparticles. Chemistry 2012; 18:4902–4908.
31.     Mano SS, Kanehira K, Sonezaki S, Taniguchi A. Effect of polyethylene glycol modification of TiO2 nanoparticles on cytotoxicity and gene expressions in human cell lines. Int J Mol Sci 2012; 13:3703–3717.
32.     Naghibi S, Madaah Hosseini HR, Faghihi Sani MA, Shokrgozar MA, Mehrjoo M. Mortality response of folate receptor-activated, PEG-functionalized TiO2 nanoparticles for doxorubicin loading with and without ultraviolet irradiation. Ceram Int 2014; 40:5481–5488.
33.     Du Y, Ren W, Li Y, Zhang Q, Zeng L, Chi C, et al. The enhanced chemotherapeutic effects of doxorubicin loaded PEG coated TiO2 nanocarriers in an orthotopic breast tumor bearing mouse model. J Mater Chem B 2015; 3:1518–1528.
34.     Sowa P, Rutkowska-Talipska J, Sulkowska U, Rutkowski K, Rutkowski R. Electromagnetic radiation in modern medicine: physical and biophysical properties. Ann Med 2012; 19:139–142.
35.     Sowa P, Rutkowska-Talipska J, Rutkowski K, Kosztyła-Hojna B, Rutkowski R. Optical radiation in modern medicine. Postepy Dermatol Alergol 2013; 30:246–251.
36.     Penjweini R, Mokmeli S, Becker K, Dodt H-U, Saghafi S. Effects of UV-, visible-, near-infrared beams in three therapy resistance case studies of fungal skin infections. Optics Photonics J 2013; 3:1–10.
37.     Bashkatov AN, Genina EA, Tuchin V V. Optical properties of skin, subcutaneous, and muscle tissues: a review. J Innov Opt Health Sci 2011; 4:9–38.
38.     Juzeniene A, Brekke P, Dahlback A, Andersson-Engels S, Reichrath J, Moan K, et al. Solar radiation and human health. Rep Prog Phys 2011; 74:66701–66757.
39.     Polefka TG, Meyer T a, Agin PP, Bianchini RJ. Effects of solar radiation on the skin. J Cosmet Dermatol 2012; 11:134–143.
40.     Huang X, El-Sayed M a. Plasmonic photo-thermal therapy (PPTT). Alexandria J Med 2011; 47:1–9.
41.     Huang X, El-Sayed M a. Gold nanoparticles: optical properties and implementations in cancer diagnosis and photothermal therapy. J Adv Res 2010; 1:13–28.
42.     Vinardell M, Mitjans M. Antitumor activities of metal oxide nanoparticles. Nanomaterials 2015; 5:1004–1021.
43.     Kwatra D, Venugopal A, Anant S. Nanoparticles in radiation therapy: a summary of various approaches to enhance radiosensitization in cancer. Transl Cancer Res 2013; 2:330–342.
44.     Filonov GS, Piatkevich KD, Ting L-MM, Zhang J, Kim K, Verkhusha VV. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat Biotechnol 2011; 29:757–761.
45.     Shcherbakova DM, Verkhusha VV. Near-infrared fluorescent proteins for multicolor in vivo imaging. Nat Methods 2013; 10:751–754.
46.     Ni W, Li M, Cui J, Xing Z, Li Z, Wu X, et al. 808 nm light triggered black TiO2 nanoparticles for killing of bladder cancer cells. Mater Sci Eng C Mater Biol Appl 2017; 81:252–260.
47.     Petković J, Küzma T, Rade K, Novak S, Filipič M. Pre-irradiation of anatase TiO2 particles with UV enhances their cytotoxic and genotoxic potential in human hepatoma HepG2 cells. J Hazard Mater 2011; 196:145–152.