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Glucose-Responsive Gene Delivery at Physiological Ph Through Tertiary-Amine Stabilized Boronate-PVA Particles Synthesized by One-Pot Reaction

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Glucose-Responsive Gene Delivery at Physiological Ph Through Tertiary-Amine Stabilized Boronate-PVA Particles Synthesized by One-Pot Reaction pharmaceutics Article Glucose-Responsive Gene Delivery at Physiological pH through Tertiary-Amine Stabilized Boronate-PVA Particles Synthesized by One-Pot Reaction Mangesh Morey, Akshay Srivastava † and Abhay Pandit * CÚRAM, SFI Research Centre for Medical Devices, National University of Ireland, H91 W2TY Galway, Ireland; [email protected] (M.M.); [email protected] (A.S.) * Correspondence: [email protected]; Tel.: +353-91-495833 † Current Address: Akshay Srivastava is currently working at Department of Medical Devices, National Institute of Pharmaceutical Education and Research, Ahmedabad, Gujarat 382355, India. Abstract: We report a physiologically stable and cytocompatible glucose-responsive nonviral gene delivery system made up of boronate functionalized polymeric material. Herein, we utilize boronate cis-diol interactions to develop a glucose-responsive submicron particle (SMP) system. The stability of the boronate interaction at a physiological pH was achieved by copolymerization of dimethyl aminoethyl methacrylate (DMAEMA) with acrylamidophenylboronic acid (AAPBA) and the forma- tion of a complex with polyvinylalcohol (PVA) which is governed by cis-diol interactions. The shift in hydrodynamic diameter of SMPs was observed and correlated with increasing glucose concentrations at a physiological pH. Optimal transfection was observed for a 5 µg dose of the gaussia luciferase reporter gene in NIH3T3 cells without any adverse effect on cellular viability. The destabilization of the AAPBA–PVA complex by interacting with glucose allowed the release of encapsulated bovine serum albumin (BSA) in a glucose-responsive manner. In total, 95% of BSA was released from SMPs at a 50 mM glucose concentration after 72 h. A two-fold increase in transfection was observed in Citation: Morey, M.; Srivastava, A.; 50 mM glucose compared to that of 10 mM glucose. Pandit, A. Glucose-Responsive Gene Delivery at Physiological pH through Keywords: glucose-responsive gene delivery; boronic acid; free radical polymerization; drug delivery Tertiary-Amine Stabilized Boronate-PVA Particles Synthesized by One-Pot Reaction. Pharmaceutics 2021, 13, 62. https://doi.org/ 1. Introduction 10.3390/pharmaceutics13010062 Nonviral gene therapy is a promising therapeutic choice for many diseases [1,2]. However, low transfection is one of the main barriers associated with nonviral gene car- Received: 30 October 2020 riers [1–3]. This challenge can be solved by the use of a stimulus-responsive delivery Accepted: 2 January 2021 system [4]. Glucose-responsive drug delivery systems represent up-and-coming appli- Published: 6 January 2021 cations in diabetes therapy and have attracted much more interest in recent years [5,6]. Glucose-responsive delivery systems are widely preferred stimulus-responsive delivery Publisher’s Note: MDPI stays neu- tral with regard to jurisdictional clai- systems based on Glucose oxidase enzyme (GOx), glucose binding proteins (GBPs), and ms in published maps and institutio- phenylboronic acid (PBA) [6]. The use of these glucose oxidase-based systems is minimal, nal affiliations. as enzyme activity can be reduced over time [7]. Concanavalin A is a natural GBP class that is one of the most widely used lectins for glucose-responsive insulin delivery. The problem with concanavalin-based systems is that they are inflammatory [8]. PBA is a synthetic molecule that reversibly binds to 1,2- or 1,3-cis-diols, including many kinds of sugars, to Copyright: © 2021 by the authors. Li- form cyclic esters. censee MDPI, Basel, Switzerland. Recently, boronate-based systems have been reported for their potential applications This article is an open access article as saccharide [9], optical [10], and conductivity sensors [11,12], and also in drug release distributed under the terms and con- systems [13–15]. Boronate-based systems have been widely preferred because of their ditions of the Creative Commons At- stability, efficiency, and ease of use. In aqueous media, phenylboronic acid forms a pH- tribution (CC BY) license (https:// dependent equilibrium between the nonionic trigonal boronic acid and anionic tetrahedral creativecommons.org/licenses/by/ boronate. Boronate provides a reversible interaction with cis-diol-containing carbohydrates, 4.0/). Pharmaceutics 2021, 13, 62. https://doi.org/10.3390/pharmaceutics13010062 https://www.mdpi.com/journal/pharmaceutics Pharmaceutics 2021, 13, 62 Pharmaceutics 2021, 13, x FOR PEER REVIEW 2 of 10 2 of 10 nucleotides, nucleoside,bility, efficiency, and glycoproteins and ease of use. [16 In]. aqueous It has beenmedia, used phenylboronic to develop acid glucose-forms a pH-de- pendent equilibrium between the nonionic trigonal boronic acid and anionic tetrahedral responsive delivery systems for closed-loop insulin delivery [6]. However, boronate-based boronate. Boronate provides a reversible interaction with cis-diol-containing carbohy- glucose-responsivedrates, polymers nucleotides, have nucleoside, been reported and glycoprote to remainins functional[16]. It has been only used in alkalineto develop glu- media and not at physiologicalcose-responsive pH delivery [17]. Thissystems is duefor closed-loop to the high insulin pKa delivery value of [6]. the However, boronate boronate- moiety. Hence, boronate’sbased glucose-responsive optimal use in polymers biomedical have engineeringbeen reported to is remain restricted functional due to only the in alka- limitations of boronateline media groups’ and inactivity not at physiological at physiological pH [17]. pHThis (7.4) is due [17 to– the20]. high Several pKa value methods of the boro- have been developednate tomoiety. reduce Hence, the pKaboronate’s of the optimal boronate use in group biomedical to enhance engineering its functionalis restricted due to sensitivity at physiologicalthe limitations pH. Oneof boronate such approach groups’ inactivity involves at introducingphysiological anpH amino(7.4) [17–20]. group Several methods have been developed to reduce the pKa of the boronate group to enhance its in the vicinity of boronicfunctional acid sensitivity to decrease at physiological the boronate pH. One group’s such pKaapproach value involves by forming introducing a an coordination bond betweenamino group nitrogen in the vicinity and boron of boronic (Figure acid1 ).to Thedecrease effect the could boronate be increasedgroup’s pKa by value by introducing a tertiaryforming amine a coordination into the boronate bond between system nitrogen [21]. Boronate-containing and boron (Figure 1). The polymeric effect could be systems also showedincreased adverse by introducing effects on a cell tertiary metabolic amine into activity the boronate [22]. Thesesystem problems[21]. Boronate-contain- still need to be resolveding before polymeric their systems potentially also showed significant adverse contribution effects on cell to clinicalmetabolic applications activity [22]. These can be recognized. problems still need to be resolved before their potentially significant contribution to clin- ical applications can be recognized. DMAEMA-Boronate DMAEMA-Boronate Figure 1. Schematic representation of stabilization of boronate by tertiary amine of dimethyl aminoethyl methacrylate Figure 1. Schematic representation of stabilization of boronate by tertiary amine of dimethyl (DMAEMA) in a submicron particle (SMP) system. The pKa of boronate was reduced by the addition of amino group in theaminoethyl vicinity of boronic methacrylate acid by the (DMAEMA) formation of a incoordination a submicron bond particle between (SMP)nitrogen system. and boron. The pKa of boronate was reduced by the addition of amino group in the vicinity of boronic acid by the formation of a coordination bond betweenThe nitrogen goal of the and study boron. is to develop a boronate-based glucose sensitive gene delivery system. As per our knowledge, this is the first of its kind research to report the glucose- The goal of theresponsive study is gene to developdelivery system. a boronate-based Additionally, we glucose have made sensitive boronate gene active deliv- at physio- ery system. As perlogical our pH knowledge, and made this this synthesis is the very first simple of its by kind using research a single-pot to reaction. report To the achieve this, we hypothesized that copolymerization of the boronate-containing monomer with glucose-responsivedimethyl gene delivery aminoethyl system. methacrylate Additionally, (DMAEMA) we haveand the made complexation boronate of activea boronate at moi- physiological pH andety with made polyvinyl this synthesis alcohol (PVA) very simplein a single by reaction using amixture single-pot could reaction.provide an To efficient achieve this, we hypothesizedmethod for the that fabrication copolymerization of boronate-containing of the boronate-containing particles for delivery monomer in physiological with dimethyl aminoethyl methacrylate (DMAEMA) and the complexation of a boronate moiety with polyvinyl alcohol (PVA) in a single reaction mixture could provide an efficient method for the fabrication of boronate-containing particles for delivery in physiological conditions. Herein, we fabricate boronate-PVA submicron particles (SMPs) and charac- terize the release of bovine serum albumin (BSA) as a standard biomolecule at different glucose concentrations. The SMPs were validated for glucose-responsive delivery of gaus- sia luciferase (GLuc) polyplexes which transfected an NIH3T3 fibroblast cell line without adversely affecting cellular viability. Pharmaceutics 2021, 13, x FOR PEER
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