Invited review
Nanomaterials formulations for photothermal and photodynamic therapy of cancer

https://doi.org/10.1016/j.jphotochemrev.2012.09.004Get rights and content

Abstract

Nanomaterials with well-defined size, shape, composition, and surface functionalities offer multimodal and multifunctional platforms for various bioanalytical, bioimaging, and therapeutic applications. In this review, we focus on the different theranostic formulations of nanomaterials based on gold, silver, silica, semiconductor quantum dots, upconversion lanthanides, oxide magnets, polymers, liposomes, carbon nanotubes, graphene and carbon nanohorns, and their applications in photothermal and photodynamic therapy of cancer.

Highlights

► Organic and bioconjugation of nanomaterials formulate nanomedicine. ► Antibodies/peptide conjugation helps drug delivery. ► Photoactivation of nanomedicine formulations produces local heating or reactive oxygen intermediates. ► Photoactivation of the nanomedicine offers new dimensions for phototherapy of cancer.

Introduction

Phototherapy is a form of medical treatment in which light is used to treat diseases such as cancers and peripheral infections to normalize the body and relieve the depression. Photothermal therapy (PTT) and photodynamic therapy (PDT) are the two kinds of phototherapy used for the treatment of diseases so far. In PTT, a photothermal (PT) agent is employed for the selective local heating for healing abnormal cells or tissues; whereas, in PDT, the treatment occurs through a series of photochemical reactions triggered by photoactivated molecules or materials called photosensitizer (PS) drugs. In recent past, nanomaterials are used in different aspects of cancer management in terms of nanomedicine. On the basis of the growing applications of nanomaterials in PDT and PPT of cancer, in this review, we mainly focus on the different formulations of nanomaterials suitable for PTT and PDT.

Thermal treatment of cancerous cells by applying the local heating to 70 °C and general hyperthermia (heating to 41–47 °C) is known since 18th century [1]. During the local heating or hyperthermia, cells undergo irreversible damage due to the denaturation of proteins and the disruption of the cell membrane. But these thermal treatments damage the healthy tissues as well. More recently, incorporation of laser radiation treatment in thermal cancer therapy opened up a PT method for the selective treatment of cancers. As a result, laser radiation with fiber-optic waveguides finds growing applications in cancer therapy, which is called laser hyperthermia [2]. The main drawback of the laser treatment is the requirement of high-power lasers for the effective stimulation of the tumor cell death [3]. Meanwhile PTT was proposed, in which a PT agent helps the selective heating at the local environment [4]. Basic requirements of PTT are a biocompatible PT agent with large absorption coefficient in the NIR regions and an NIR light source. Thus, surface-modified nanomaterials of carbon, metals, and semiconductors with NIR absorption can be ideal PT agents. The percentage increase in the temperature during PTT strongly depends on the NIR absorption wavelength and the coefficient as well as the power of the excitation light [5]. Illumination of nanomaterials with NIR laser results in an increase in the temperature of the medium, which reaches a maximum value when the NIR absorption maximum coincides with the laser wavelength (Fig. 1).

The basic principle underlying PDT of cancers is a chain of photochemical reactions triggered by a photoactivated PS drug. During the irradiation of a PS drug at a suitable wavelength, it will be activated to the excited singlet (S1) and subsequently to the triplet (T1) state via intersystem crossing. The lifetime of the T1 state is longer than that of S1, which facilitates the extended interactions of the PS drug in the T1 states with the surrounding molecules [6]. Two types of mechanisms, Type I and Type II, are known for such interactions at the T1 state [7]. Type I mechanism involves either the abstraction of a hydrogen atom, or the transfer of an electron between the excited PS and the substrate, which can be a solvent/biomolecule or another PS resulting in the formation of free radicals. Type II mechanism involves the energy transfer between a photoactivated PS and molecular oxygen in the ground state, also called triplet oxygen (3O2). This energy transfer will result in the formation of a chain of reactive oxygen intermediates (ROI) such as singlet oxygen (1O2), superoxide, hydrogen peroxide, and hydroxyl radical. Such photophysical and photochemical processes involved in PDT are shown in Fig. 2. The ROI, due to their short lifetime, immediately react with vital biomolecules, causing the selective damage of tumor cells [8]. The destruction of biomolecules is limited to the size of the diffusion sphere of ROI, which is less than 0.1 μm in the case of 1O2 [9]. Hence the localization of PS is crucial for the targeted as well as efficient PDT [10].

Section snippets

Nanomaterials in photothermal therapy

Noble metal nanostructures are promising candidates in various aspects of chemistry, physics and biology owing to their unique properties such as large optical field enhancements due to the strong scattering and absorption of light. The optical and PT enhancements of metallic NPs arise from the unique interaction of nanoparticles (NPs) with light. When illuminated, the valance electrons of the metal NPs undergo a collective coherent oscillation with respect to the lattice [11], [12], [13], [14]

Nanomaterials in photodynamic therapy

An ideal PS drug has high absorption coefficient in the 650–850 nm region, high yield of 1O2, solubility under physiological conditions, large tumor selectivity, poor damage of healthy tissues and fewer side effects such as mutagenic, carcinogenic and allergic effects. The main advantages of PDT over radiation therapy and chemotherapy are its site-specific photoactivation of targeted PS drugs with visible or NIR light and minimal damage of the normal tissues. The main two classifications of PS

Summary and perspectives

Benefitting from the recent developments in the nanomaterials field and the emergence of an interface between nanomaterials and bioconjugate chemistry, photothermal and photodynamic therapies of cancer take new dimensions in the preclinical and clinical scenario. Nanomaterials with well-defined size, shape, composition, and surface functionalities offer multimodal and multifunctional platforms for cancer management – from detection to curing both in vitro and in vivo. Strong absorption of

Acknowledgments

VB thank Japan Science and Technology Agency for Precursory Research for Embryonic Science and Technology (PRESTO) program and Japan Society for the Promotion of Science (JSPS) for Grant-in-Aid for Scientific Research. ESS thanks JSPS for a postdoctoral fellowship.

Edakkattuparambil Sidharth Shibu received his Under Graduate (2002) and Mater (2004) Degrees in Chemistry from the University of Calicut. Subsequently, he joined the Department of Chemistry at Indian Institute of Technology (IIT) Madras for his graduate studies, where he obtained a PhD degree in Chemistry (2011) under the guidance of Prof. T. Pradeep. In January 2011, he joined AIST as a Postdoctoral Fellow under the supervision of Prof. V. Biju. Since November 2011, he is a JSPS Postdoctoral

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    Edakkattuparambil Sidharth Shibu received his Under Graduate (2002) and Mater (2004) Degrees in Chemistry from the University of Calicut. Subsequently, he joined the Department of Chemistry at Indian Institute of Technology (IIT) Madras for his graduate studies, where he obtained a PhD degree in Chemistry (2011) under the guidance of Prof. T. Pradeep. In January 2011, he joined AIST as a Postdoctoral Fellow under the supervision of Prof. V. Biju. Since November 2011, he is a JSPS Postdoctoral Fellow working in AIST with Prof. Biju. His current research is focused on the synthesis of multimodal nanomaterials and investigations of their applications for bioimaging and phototherapy. He is the recipient of the best paper awards of Taiwan's RCAS-TNNA Symposium and JSPS-DST Japan-India Bilateral Seminar.

    Morihiko Hamada obtained his Undergraduate (2009) and Master (2011) degrees in Engineering from Kagawa University in Japan. Since April 2012 he is a graduate student affiliated with AIST Innovation School and Kagawa University. He is carrying out his graduate research in AIST under the guidance of Prof. V. Biju (AIST) and Prof. Shunsuke Nakanishi (Kagawa University). His graduate research is on the development of unidirectional energy donor-acceptor systems and investigation of Förster Resonance Energy Transfer in the systems. He is the recipient of the international travel award of NEC and the Nippon Electronic Corporation (NEC) and the award of the Chugoku-Shikoku Branch of the Chemical Society of Japan (2012).

    Norio Murase received his master degree in Chemistry from Tokyo University. Subsequently he entered into Hitachi Ltd. for the study of materials for high density optical memory, for which he obtained a PhD there in 1994. Immediately after that, he gave up the position in Hitachi, and joined in National Institute of Advanced Industrial Science and Technology (AIST). He is currently the group leader of Nanobioanalysis Research Group, Health Research Institute, AIST. Since 2010, he is also appointed as a Visiting Professor at Kwansei Gakuin University, Japan. His current research is focused on the development of silica encapsulated quantum dots.

    Vasudevanpillai Biju studied chemistry at the University of Kerala and obtained his PhD in 2000. After doing postdoctoral research in AIST (2000–2002) and Nanotechnology Research Institute (2002-2003; JSPS Fellow) in Japan, he moved in Pacific Northwest National Laboratory in USA as a Postdoctoral Fellow (2003–2004). Currently, he is a Chief Scientist in Health Research Institute, AIST. In parallel, he is appointed as a PRESTO Researcher of the Japan Science and Technology Agency (JST; since October 2010), a Visiting Professor at the University of Kerala (since 2007), an Adjunct Professor at Southern University (since 2012), and a Guest Professor at the University of Tokushima (since 2012). His current research includes the development of biofunctional and photofunctional nanomaterials, single-molecule spectroscopy and microscopy, optical and magnetic properties of functional nanomaterials, and bioimaging and phototherapy. He is serving as the Associate Editor of the J. Photochem. Photobiol. C, Editor of Nano Reviews, Editorial Board Member of the J. Bioengg. Biomed. Sci., and Chairman of Asian Nanoscience and Nanotechnology Association (ANNA). He has received many academic recognitions, which include the 14th Gen-nai Award by the Ozaki Foundation, Most Cited Certificate from Analytical and Bioanalytical Chemistry, Distinguished Lectureship Award by the Chemical Society of Japan (2010), Asian and Oceanian Photochemistry Award for Young Scientist (2010), Young Lectureship by the Chemical Society of Japan (2011), and the Japanese Photochemistry Association Award for Young Scientist (2011). Since 2011, he is the Fellow of the Royal Society of Chemistry (FRSC).

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