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1902776 (1 of 10) ©
2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.small-journal.com
Anti-VEGF-Aptamer Modified C-Dots—A Hybrid
Nanocomposite for Topical Treatment of Ocular
Vascular Disorders
Asaf Shoval, Amos Markus, Zhixin Zhou, Xia Liu, Rémi Cazelles, Itamar Willner,*
and Yossi Mandel*
Dr. A. Shoval, Dr. A. Markus, Prof. Y. Mandel
School of Optometry and Vision Science
Faculty of Life Sciences
Bar-Ilan University
Ramat-Gan 5290009, Israel
E-mail: yossi.mandel@biu.ac.il
Dr. A. Shoval, Dr. A. Markus, Prof. Y. Mandel
Bar Ilan’s Institute for Nanotechnology and Advanced Materials (BINA)
Bar Ilan University
Ramat-Gan 5290009, Israel
Dr. Z. Zhou, Dr. X. Liu, Dr. R. Cazelles, Prof. I. Willner
Institute of Chemistry
The Minerva Center for Biohybrid Complex Systems
The Hebrew University of Jerusalem
Jerusalem 91904, Israel
E-mail: Itamar.willner@mail.huji.ac.il
The ORCID identification number(s) for the author(s) of this article
can be found under https://doi.org/10.1002/smll.201902776.
DOI: 10.1002/smll.201902776
1. Introduction
Nanomedicine
[1,2]
represents a rapidly developing research
area aiming to apply nanoparticles, such as metallic nanopar-
ticles,
[3,4]
semi-conductive quantum dots
[5–7]
or carbonous mate-
rials,
[8,9]
such as graphene oxide or nanotubes for sensing,
[10–12]
imaging,
[13,14]
stimuli responsive carriers
[15]
or therapeutic
agents.
[16,17]
Carbon dots (C-dots) have attracted growing interest
as a functional nanomaterial due to their unique optical,
[18–20]
The vascular endothelial growth factor (VEGF) induces pathological angio-
genetic ocular diseases. It is a scientific challenge to develop carriers for the
controlled release of inhibitors for VEGF present in the back of the eye domain.
Carbon dots (C-dots) functionalized with the VEGF aptamer are introduced
and the hybrid nanoparticles are used for ocular nanomedicine. The C-dots are
applied as effective carriers of the anti-VEGF aptamer across the cornea, yielding
therapeutic levels upon topical administration. The hybrids show no toxicity for
both in vitro and in vivo murine animal model, and further enable noninvasive
intraocular concentration monitoring through the C-dots inherent fluorescence.
In addition, the hybrid C-dots effectively inhibit VEGF-stimulated angiogenesis
in choroidal blood vessels. This inhibition is comparable to two commercially
available anti-VEGF drugs, bevacizumab and aflibercept. The hybrid aptamer-
modified C-dots provide a versatile nanomaterial to treat age-related macular
degeneration and diabetic retinopathy.
Inhibiting Macular Degeneration
electronic,
[21]
and catalytic
[22]
properties,
making them suitable for various appli-
cations
[23,24]
such as sensing,
[25–27]
bio-
sensing,
[28,29]
imaging,
[18,30,31]
drug and
gene delivery,
[32,33]
catalysis,
[34]
electroca-
talysis,
[35]
and photo-electrochemistry.
[36]
Various methods for synthesizing C-dots
have been reported (including hydro-
thermal,
[37]
microwave,
[38]
or chemical
[39]
treatment of organic substrates), and spe-
cifically the synthesis of different sized
C-dots, which revealed tunable lumines-
cence features and programmable surface
functionalities (e.g., amino, carboxylic
acid, aldehyde, or hydroxyl groups) ena-
bling further surface modification with
molecular or biomolecular ligands.
[40,41]
Aptamers are sequence-specific nucleic
acids that selectively bind low molecular
weight ligands or macromolecules.
[42,43]
Aptamers have been
widely applied as functional materials for sensing,
[44,45]
selective
drug delivery
[46,47]
and the design of DNA nanomachines.
[48,49]
Specifically, the association of aptamers to proteins is known to
inhibit the binding and catalytic properties of proteins,
[50]
and
aptamer-based therapies were recognized.
[51,52]
One of the interesting potential applications of aptamer may
include the inhibitory effect of the anti-vascular endothelial
growth factor (VEGF) aptamer on the VEGF induced angiogenetic
driven ocular diseases.
[53]
Indeed, the VEGF aptamer has been
recently introduced
[54]
for treatment by ocular injections in cases
of age-related macular degeneration (AMD) and diabetic retin-
opathy (DR), leading causes of blindness. Treatment availability
for these diseases, however, is limited by the need for repeated
intraocular injections
[55–70]
of anti-VEGF performed by highly
qualified personnel, and is accomplished by significant systemic
and ocular adverse reactions.
[54,60,71–74]
Nevertheless, intraocular
injections remain the treatment of choice due to the limited pen-
etration capability of topically applied drugs.
[75–77]
Different nano-
structures have already been suggested as carriers for the VEGF
aptamer and such systems have been used for sensing,
[78–80]
imaging,
[81]
and stimulus-responsive drug carriers.
[52]
In the present study we report on the preparation of sur-
face modified anti-VEGF aptamer C-dots, their application as
hybrid systems for carrying the aptamer across the corneal
structure into the eye cavity and stimulating the release of
the aptamer in the presence of VEGF, thereby inhibiting the
angiogenesis functions of VEGF in the posterior eye chamber.
Small 2019, 1902776