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Stimuli-Responsive Nanomaterials for Application in Antitumor Therapy and Drug Delivery

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Stimuli-Responsive Nanomaterials for Application in Antitumor Therapy and Drug Delivery pharmaceutics Review Stimuli-Responsive Nanomaterials for Application in Antitumor Therapy and Drug Delivery Son H. Pham y, Yonghyun Choi y and Jonghoon Choi * School of Integrative Engineering, Chung-Ang University, Seoul 06974, Korea; [email protected] (S.H.P.); [email protected] (Y.C.) * Correspondence: [email protected]; Tel.: +82-2-820-5258 Authors contributed equally. y Received: 4 April 2020; Accepted: 4 July 2020; Published: 4 July 2020 Abstract: The new era of nanotechnology has produced advanced nanomaterials applicable to various fields of medicine, including diagnostic bio-imaging, chemotherapy, targeted drug delivery, and biosensors. Various materials are formed into nanoparticles, such as gold nanomaterials, carbon quantum dots, and liposomes. The nanomaterials have been functionalized and widely used because they are biocompatible and easy to design and prepare. This review mainly focuses on nanomaterials responsive to the external stimuli used in drug-delivery systems. To overcome the drawbacks of conventional therapeutics to a tumor, the dual- and multi-responsive behaviors of nanoparticles have been harnessed to improve efficiency from a drug delivery point of view. Issues and future research related to these nanomaterial-based stimuli sensitivities and the scope of stimuli-responsive systems for nanomedicine applications are discussed. Keywords: nanoparticles; stimuli-responsive; drug delivery; nanomedicine 1. Introduction Nanotechnology research has had a significant impact on the field of medicine. Particularly, nanomaterials, such as liposomes, dendrimers, polymers, metallic nanoparticles (NPs), and nanogels, are currently being developed and used in various biomedical applications. These nanomaterial systems play an important role not only in sensing, biomedical imaging, and diagnosis but also in drug delivery. These smart carrier systems have been widely developed because they are responsive to various exogenous (e.g., pH, temperature, light, and ultrasound) and endogenous (e.g., redox potential and enzyme presence) stimuli. A variety of nanoparticles are suitable for drug delivery; thus, the development of nanoparticle drug-delivery systems with stimuli-responsive properties has gained considerable attention [1–4]. There are two approaches for designing stimuli-responsive drug-delivery nanoparticles that efficiently accumulate at the tumor site, respond to intratumoral or external stimuli, and penetrate tumor cells. One of these approaches involves endogenous stimuli (i.e., enzymes, ions, and redox potential), which are mainly unique among tumor regions and can effectively enhance drug release [5,6]. This approach requires the careful selection of materials that can form effective nanocarriers, respond to specific endogenous stimuli, and release enclosed drugs. In the second approach, exogenous physical stimuli (i.e., temperature, light, electricity, magnetic fields, and ultrasound) are applied to the target tissue [7]. These exogenous stimuli can disrupt the structure of specifically designed nanocarriers and cause them to release a drug in the desired tissue. One benefit of a stimuli-responsive drug-delivery system is that it can prevent premature drug release, which is a common problem with traditional drug-delivery systems [8,9]. Therefore, research trends have moved toward stimuli-responsive drug-delivery systems that rely on a combination of two or more stimuli-responsive systems to increase Pharmaceutics 2020, 12, 630; doi:10.3390/pharmaceutics12070630 www.mdpi.com/journal/pharmaceutics Pharmaceutics 2020, 12, 630 2 of 19 Pharmaceutics 2020, 12, 630 2 of 18 responsive systems to increase targeting efficiency [7],[10,11]. However, exogenous stimuli- targetingresponsive efficiency materials [7,10 ,11have]. However, a few limitations. exogenous It stimuli-responsive is challenging to materialsfind exogenous have a few stimuli limitations. that can It ispenetrate challenging the human to find exogenoustissue and precisely stimuli that reach can the penetrate tumor thesite. human Additionally, tissue and endogenous precisely reachstimuli the that tumorwill site.contr Additionally,ol the release endogenous specifically stimuliat the tumor that will site control in an theappropriate release specifically time and dosage at the tumor are hard site to in anfind. appropriate time and dosage are hard to find. InIn this this review, review, endogenous endogenous and exogenous and exogenous stimuli, alongstimuli, with along dual- with and multi-stimuli-responsivedual- and multi-stimuli- drugresponsive delivery, drug are discussed delivery, (Figureare discussed1). This (Figure review 1). would This providereview would a summary provide of currenta summary research of current on variousresearch stimuli on various and responding stimuli nanoparticlesand responding as wellnanoparticles as their up-to-date as well as application. their up-to While-date thereapplication. were severalWhile reports there were on stimuli-responsive several reports on block stimuli copolymer-responsive carriers, block this copolymer review would carriers, not this limit review the scope would onlynot on limit the polymericthe scope nanocarriers. only on the The polymeric state-of-art nanocarriers. nanosized materialsThe state responding-of-art nanosized to external materials and internalresponding stimuli to would external be and discussed. internal stimuli would be discussed. Figure 1. Schematic diagram of stimuli-responsive nanomaterials used for bioimaging, therapy, Figure 1. Schematic diagram of stimuli-responsive nanomaterials used for bioimaging, therapy, and and triggered drug release. triggered drug release. 2. Endogenous Stimuli-Responsive Systems 2. Endogenous Stimuli-Responsive Systems 2.1. Redox-Responsive Systems 2.1.The Redox redox-Responsive potential Systems of tumor cells is 100- to 1000-fold higher than that of other cells [12]. Glutathione (GSH) isThe an importantredox potential antioxidant of tumor that can cells inhibit is 100 the- reactiveto 1000 oxygen-fold higher species than (ROS) that produced of other in cellularcells [12]. components.Glutathione The (GSH) redox is potentialan important difference antioxidant between that the can extracellular inhibit the (oxidative)reactive oxygen and intracellularspecies (ROS) (reductive)produced spaces in cellular is associated components. with The the extracellularredox potential and difference intracellular between GSH the concentrations extracellular [ 13(oxidative]. ) andThe intracellular development (reductive) of drug-delivery spaces is systems associated based with on GSH-responsivethe extracellular assemblies and intracellular has gained GSH increasingconcentrations attention. [13].GSH can destabilize disulfide linkages in nanoparticles in a redox-mediated manner.The Block development copolymers of contain drug- disulfidedelivery linkagessystems betweenbased on hydrophilic GSH-responsive and hydrophobic assemblies blocks has gained that areincreasing GSH-responsive. attention. This GSH enables can thedestabilize formation disulfide of micelles, linkages which in are nanoparticles also known asin ‘shell-sheddable’a redox-mediated micelles.manner. When Block these copolymers micelles contain interact disulfide with GSH, linkages they become between destabilized hydrophilic and and release hydrophobic therapeutic blocks materialsthat are [ 14GSH,15].-responsive. This enables the formation of micelles, which are also known as ‘shell- sheddable’High concentrations micelles. When of reducing these micelles materials interac in intracellulart with GSH, compartments they become help destabilized maintain polymersand release withtherapeutic disulfide materials linkages; [14,15 however,]. polymers containing hydrophobic blocks (i.e., polypropylene sulfide [High16–18 ])concentrations are sensitive to of the reducing oxidative materials environments in createdintracellular by many compartments disease states. help Pioneering maintain workspolymers by Tirelli with et disulfide al., showed linkages; polysulfides however, nanocarriers polymers that containing could respond hydrophobic to the presence blocks of(i.e., oxidantspolypropylene and their sulfide use for [16 immune–18]) are modulating sensitive to applications the oxidative [16 –environments18]. Hydrophobic created parts by in many polymers disease werestates. also Pioneering used for works the oxidation-induced by Tirelli et al., showed solubility polysulfides variations nanocarriers in a selenium that could block respond copolymer. to the Pharmaceutics 2020, 12, 630 3 of 18 Spherical micelles were generated from copolymers in an aqueous medium with hydrophobic selenium cores. The oxidation of selenium to selenoxide [19] using hydrogen peroxide led to a phase transition from hydrophobic to hydrophilic causing the micelles to disassemble [19]. By adding reducing agents, spherical micelles were reproduced, and it showed that these selenium-containing nanocapsules were responsive to oxidizing and reducing conditions. Disulfide linkages have been frequently used to design nanocarriers. For example, redox-responsive capsules were prepared by combining poly (N-vinyl pyrrolidone) (PVPON), poly (methyl methacrylate) (PMAA), and a disulfide cross-linker that could deliver plasmid DNA and doxorubicin [20]. One concern with this technology is its stability and premature drug release since cysteine and GSH are present in the extracellular compartment. This problem may be solved using manifold disulfide linkages created by adjusting the number
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