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Part III
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Pharmaceutical Nanoscience Applications
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Chapter 15
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Stimulus-Responsive Nanoparticles
for Drug Delivery
Nikolitsa Nomikou, Hamzah Masood, and Shiv Patel
Abbreviations
BMP-2 Bone-morphogenic protein 2
CD Cyclodextrin
DA 2,3-dimethylmaleic anhydrite
DPPC Dipalmitoyl phosphatidylcholine
DSPE 1, 2-Distearoyl-sn-glycero-3-phosphoethanolamine
GOx Glucose oxidase
GSH Glutathione
GSSG Glutathione disulfide
HIFU High-intensity focused ultrasound
MRI Magnetic resonance imaging
MSNs Mesoporous silica nanoparticles
NADH Nicotinamide adenine dinucleotide
NADPH Nicotinamide adenine dinucleotide phosphate
NIR Near infrared
PBA Phenyl boroni c acid
PEG Polyethylene glycol
pHLIP pH (low) insertion peptide
PolyMTO Polymitoxantrone
ROS Reactive oxygen species
SPION Super paramagnetic iron oxide nanoparticles
UV Ultraviolet
N. Nomikou (✉) · H. Masood · S. Patel
Division of Surgery and Interventional Science, University College London, London, UK
e-mail: n.nomikou@ucl.ac.uk
© The Editor(s) (if applicable) and The Author(s), under exclusive license to
Springer Nature Switzerland AG 2024
I. F. Uchegbu et al. (eds.), Fundamentals of Pharmaceutical Nanoscience,
https://doi.org/10.1007/978-3-031-59478-6_15
389
390 N. Nomikou et al.
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15.1 Introduction
Nanotechnology has undoubtedly improved the performance of many therapeutic
agents in the treatment of an array of diseases/defects, such as cancer, inflammation,
diabetes, and infection. Nanoparticles have been developed to improve cellular
uptake at the target site and subcellular localization of agents that are hydrophobic,
have poor blood solubility, or are metabolically unstable. Overall, nanotechnology
has aimed to improve the targeted and disease-specific effects of therapeutic molecules. Although incorporation of agents in nanoparticles may improve their bioavailability, targeting is still fractional, with significant off-target accumulation and
subsequent off-target effects. Disease-specific stimulation can be provoked by using
nanosystems that respond to certain endogenous factors associated with the disease,
such as overexpressed enzymes, increased glucose concentration, tissue acidity, the
production of reactive oxygen species (ROS), a reducing environment, and hypoxia.
Externally controlled nanocarrier stimulation for drug release can also be achieved
using exogenou s stimuli, such as temperature, electromagnetic radiation, a magnetic
field, or ultrasound. These approaches offer on-demand drug release and spatiotemporal control of drug disposition, both of which can significantly improve diseasespecific effects and reduce off-target toxicities of nanoencapsulated drugs. This
chapter focuses on the smart chemistry and structural functionality of nanoparticles
designed to respond to diverse types of endogenous and exogenous stimuli.
15.2 Nanoparticles That Are Responsive
to Disease-Associated/Endogenous Stimuli
15.2.1 Enzyme-Responsive Nanoparticles
Diseased tissues or defective sites are often associated with the dysreg ulation of
enzymatic activity. A characteristic example is the overexpression of proteases
(e.g. cathepsins, matrix metalloproteinases, caspase-3, and phospholipases) within
the tumour microenvironment. The therapeutic efficacy of drugs and their sitespecific availability and/or activation can be significantly improved when they are
incorporated in “smart” nanocarriers that are designed to respond to diseaseassociated enzymes and exploit the activity of the latter to release payloads in a
site-specific manner (Hu et al. 2014). Enzyme-sensitive nanoparticles can be
designed to respond to these overexpressed enzymes in a number of
different ways: (a) nanocarrier degradation/disassembly via biochemical cleavage
of the polymer backbone, (b) direct bond cleavage of nanocarrier-drug conjugate,
(c) opening of nanocarrier pores/gates, (d) nanoparticle size/morphological change,
and (e) nanoparticle surface charge changes (Mi 2020).
15 Stimulus-Responsive Nanoparticles for Drug Delivery 391
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(a) Cleaving the structural component of nanocarriers.
Nanoparticles formed using enzyme-degradable structural components can offer
site-specific drug release and/or exposure of the drug active site. One of the most
characteristic examples is the clinically applied nanoformulation paclitaxel
polyglumex that links the chemothera peutic paclitaxel with a biodegradable polymer, poly-L-glutamic acid (Chipman et al.
polymeric backbone is based on the degradation of the polymer by the protease
cathepsin B, which is upregulated in many tumours. In an analogous manner, more
recently, doxorubicin was conjugated to a cathepsin B-sensitive peptide and the
peptide-drug conjugate formed nanoparticles via self-assembly using Pluronic F68
as a stabilizing agent. The peptide sequence can be cleaved in the tumour microenvironment leaving a doxorubicin prodrug, which is metabolized further intracellularly to liberate free doxorubicin (Kim et al.
If biochemical cleavage sites are not already present, enzyme-cleavable linkages
can be introduced into the polymer backbone of polymeric nanocarriers to enable
specific enzyme-dependent degradation of nanocarriers. For example, Rao and Khan
(2013) synthesized azoreductase-sensitive micelles from the amphiphilic diblock
copolymer poly(ethylene glycol)-b-poly(styrene) that contained an azobenzene linkage as a bridge between the hydrophilic and hydrophobic chains. In the presence of
NADH, the azoreductase secreted by the colon microbial flora cleaves the linkage,
resulting in micellar disassembly. This enzyme-responsive system can be used to
deliver hydrophobic drugs, such as sulfasalazine, in its core for the treatment of
colon diseases. Instead of enzyme-responsive polymers, peptides with recognizable
sequences by enzymes such as matrix metalloproteinase-2 (MMP-2), have been
synthesized to form spherical nanoparticles through self-assembly with hydrophobic
chemotherapeutic agents (Xu et al. 2019). It has been demonstrated that, after
accumulation in a tumour mass with overexpressed MMP-2, these peptide-based
spherical nanoparticles undergo structural transformation into rod-shaped
nanoparticles with improved tumour penetration and retention capability. In addition, the poly(L-glutamic acid-L-tyrosine) co-polymer has been used to form cathepsin B-degradable nanoparticles via self-assembly with the hydrophobic agent
hematoporphyrin, to augment the efficacy of sonodynamic therapy (Hadi et al.
2021; 2023). Enzymatic digestion of these nanoparticles led to the reduction of
their size, which improved cellular uptake and their potential to be suf ficiently
distributed throughout the mass of dense, poorly perfused tumours.
2006). The release of paclitaxel from the
2021).
(b) Direct cleaving of nanocarrier-drug conjugates.
Instead of relying on intramolecular and hydrophobic interactions, enzymecleavable linkages can be used to directly anchor drugs onto different types of
nanocarriers, such as solid–lipid nanoparticles, liposomes, micelles, gold or
mesoporous nanoparticles, dendrimers, nanorods, etc. One example is the conjugation of gemcitabine onto PEGylated peptide dendrimers through the cathepsin
B-sensitive peptide linker, GFLG, which has enabled gemcitabine release upon
digestion with cathepsin B, while drug release in the absence of the enzyme was
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