Hong, Sung Hwa, Larocque, Kevin, Jaunky, Dilan B., Piekny, Alisa J and Kwon Oh, Jung 
ORCID: https://orcid.org/0000-0002-4220-308X
(2018)
Dual disassembly and biological evaluation of enzyme/oxidation-responsive polyester-based nanoparticulates for tumor-targeting delivery.
Colloids and Surfaces B: Biointerfaces
.
ISSN 09277765
(In Press)
Preview |
Text (In press, accepted manuscript) (application/pdf)
1MBDual-disassembly-and-biological-evaluation-of-enzyme-ox_2018_Colloids-and-Su.pdf Available under License Spectrum Terms of Access. |
Official URL: http://dx.doi.org/10.1016/j.colsurfb.2018.09.013
Abstract
Polyester-based nanoparticulates (NPs) are ideal nanocarriers for intracellular delivery of anticancer drugs because of their biocompatibility. However, an on-going challenge is the controlled and enhanced release of encapsulated therapeutics in response to unique changes that occur within cancer cells. Herein, we report the versatility of dual responses to enzymatic and oxidative reactions found in cancer cells toward the development of polyester-NPs as effective tumor-targeting intracellular nanocarriers. A facile nanoprecipitation method allows for the preparation of hydrophobic cores composed of novel polyester designed with esterase-responsive ester groups and oxidation-responsive sulfide linkages on their backbones, physically stabilized with poly(ethylene glycol)-based polymeric shells. The formed core/shell-type NPs with a diameter of 120 nm exhibit excellent colloidal stability in physiological conditions and in the presence of serum proteins. When exposed to esterase and hydrogen peroxide, NP integrity is disrupted, leading to the enhanced release of encapsulated doxorubicin, confirmed by dynamic light scattering and spectroscopic analysis. Combined results from epifluorescence microscopy, confocal laser scanning microscopy, flow cytometry, and cell viability demonstrate that doxorubicin-loaded NPs reveal rapid penetration and enhanced intracellular release of doxorubicin, thus inhibiting tumor progression. Importantly, the cellular uptake of doxorubicin-loaded core/shell NPs primarily via caveolae-dependent mechanism promotes their use in targeting a broad spectrum of cancers.
| Divisions: | Concordia University > Faculty of Arts and Science > Chemistry and Biochemistry |
|---|---|
| Item Type: | Article |
| Refereed: | Yes |
| Authors: | Hong, Sung Hwa and Larocque, Kevin and Jaunky, Dilan B. and Piekny, Alisa J and Kwon Oh, Jung |
| Journal or Publication: | Colloids and Surfaces B: Biointerfaces |
| Date: | 9 September 2018 |
| Funders: |
|
| Digital Object Identifier (DOI): | 10.1016/j.colsurfb.2018.09.013 |
| Keywords: | ROS; esterase; dual stimuli-responsive degradation; polyester nanoparticles; controlled release; enhanced penetration; drug delivery |
| ID Code: | 984420 |
| Deposited By: | Monique Lane |
| Deposited On: | 20 Sep 2018 20:30 |
| Last Modified: | 09 Sep 2020 00:00 |
References:
P.G. Corrie Cytotoxic chemotherapy: clinical aspects Medicine, 36 (2008), pp. 24-28D.B. Reuben, V. Mor Nausea and vomiting in terminal cancer patients Arch. Intern. Med., 146 (1986), pp. 2021-2023
T. Sun, Y.S. Zhang, B. Pang, D.C. Hyun, M. Yang, Y. Xia Engineered nanoparticles for drug delivery in cancer therapy Angew. Chem. Int. Ed., 53 (2014), pp. 12320-12364
Y. Matsumura, K. Kataoka Preclinical and clinical studies of anticancer agent-incorporating polymer micelles Cancer Sci., 100 (2009), pp. 572-579
A.S. Mikhail, C. Allen Block copolymer micelles for delivery of cancer therapy: Transport at the whole body, tissue and cellular levels J. Controlled Release, 138 (2009), pp. 214-223
Y.H. Bae, K. Park Targeted drug delivery to tumors: Myths, reality and possibility
J. Controlled Release, 153 (2011), pp. 198-205
F. Danhier, O. Feron, V. Préat To exploit the tumor microenvironment: Passive and active tumor targeting of nanocarriers for anti-cancer drug delivery J. Controlled Release, 148 (2010), pp. 135-146
A.E.v.d. Ende, E.J. Kravitz, E. Harth Approach to formation of multifunctional polyester particles in controlled nanoscopic dimensions J. Am. Chem. Soc., 130 (2008), pp. 8706-8713
G.B. Jacobson, R. Shinde, C.H. Contag, R.N. Zare Sustained release of drugs dispersed in polymer nanoparticles Angew. Chem. Int. Ed., 47 (2008), pp. 7880-7882
D. Brambilla, J. Nicolas, B. Le Droumaguet, K. Andrieux, V. Marsaud, P.-O. Couraud, P. Couvreur Design of fluorescently tagged poly(alkyl cyanoacrylate) nanoparticles for human brain endothelial cell imaging Chem. Commun., 46 (2010), pp. 2602-2604
S. Taurin, H. Nehoff, K. Greish Anticancer nanomedicine and tumor vascular permeability; Where is the missing link? J. Controlled Release, 164 (2012), pp. 265-275
L. Zhang, Y. Li, J.C. Yu Chemical modification of inorganic nanostructures for targeted and controlled drug delivery in cancer treatment J. Mater. Chem. B, 2 (2014), pp. 452-470 J.W. Nichols, Y.H. Bae Odyssey of a cancer nanoparticle: From injection site to site of action Nano Today, 7 (2012), pp. 606-618
C.J.F. Rijcken, O. Soga, W.E. Hennink, C.F. van Nostrum Triggered destabilization of polymeric micelles and vesicles by changing polymers polarity: An attractive tool for drug delivery J. Controlled Release, 120 (2007), pp. 131-148
Q. Zhang, N.R. Ko, J.K. Oh Recent advances in stimuli-responsive degradable block copolymer micelles: synthesis and controlled drug delivery applications Chem. Commun., 48 (2012), pp. 7542-7552
H. Wei, R.-X. Zhuo, X.-Z. Zhang Design and development of polymeric micelles with cleavable links for intracellular drug delivery Prog. Polym. Sci., 38 (2013), pp. 503-535
S. Mura, J. Nicolas, P. Couvreur Stimuli-responsive nanocarriers for drug delivery
Nat. Mater., 12 (2013), pp. 991-1003
C. Alvarez-Lorenzo, A. Concheiro Smart drug delivery systems: from fundamentals to the clinic Chem. Commun., 50 (2014), pp. 7743-7765
R.V. Ulijn Enzyme-responsive materials: a new class of smart biomaterials J. Mater. Chem., 16 (2006), pp. 2217-2225
M.H. Lee, Z. Yang, C.W. Lim, Y.H. Lee, D. Sun, C. Kang, J.S. Kim Disulfide-Cleavage-Triggered Chemosensors and Their Biological Applications Chem. Rev., 113 (2013), pp. 5071-5109
B.S. Bolu, B. Golba, N. Boke, A. Sanyal, R. Sanyal Designing Dendron-Polymer Conjugate Based Targeted Drug Delivery Platforms with a "Mix-and-Match" Modularity Bioconjugate Chemistry, 28 (2017), pp. 2962-2975
C. Deng, Y. Jiang, R. Cheng, F. Meng, Z. Zhong Biodegradable polymeric micelles for targeted and controlled anticancer drug delivery: Promises, progress and prospects
Nano Today, 7 (2012), pp. 467-480
M. Huo, J. Yuan, L. Tao, Y. Wei Redox-responsive polymers for drug delivery: from molecular design to applications Polym. Chem., 5 (2014), pp. 1519-1528
S. Binauld, M.H. Stenzel Acid-degradable polymers for drug delivery: a decade of innovation Chem. Commun., 49 (2013), pp. 2082-2102
I.R. Fernando, D.P. Ferris, M. Frasconi, D. Malin, E. Strekalova, M.D. Yilmaz, M.W. Ambrogio, M.M.Algaradah, M.P. Hong, X. Chen, M.S. Nassar, Y.Y. Botros, V.L. Cryns, J.F. Stoddart Esterase- and pH-responsive poly(β-amino ester)-capped mesoporous silica nanoparticles for drug delivery Nanoscale, 7 (2015), pp. 7178-7183
L.A. Needham, A.H. Davidson, L.J. Bawden, A. Belfield, E.A. Bone, D.H. Brotherton, S. Bryant, M.H.Charlton, V.L. Clark, S.J. Davies Drug targeting to monocytes and macrophages using esterase-sensitive chemical motifs J. Pharmacol. Exp. Ther., 339 (2011), pp. 132-142
L. Zhu, P. Kate, V.P. Torchilin Matrix Metalloprotease 2-Responsive Multifunctional Liposomal Nanocarrier for Enhanced Tumor Targeting ACS Nano, 6 (2012), pp. 3491-3498
R. Dorresteijn, N. Billecke, M. Schwendy, S. Puetz, M. Bonn, S.H. Parekh, M. Klapper, K. Muellen Polylactide-block-polypeptide-block-polylactide copolymer nanoparticles with tunable cleavage and controlled drug release Adv. Funct. Mater., 24 (2014), pp. 4026-4033
L. Gao, B. Zheng, W. Chen, C.A. Schalley Enzyme-responsive pillar[5]arene-based polymer-substituted amphiphiles: synthesis, self-assembly in water, and application in controlled drug release Chem. Commun., 51 (2015), pp. 14901-14904
N. Li, H. Cai, L. Jiang, J. Hu, A. Bains, J. Hu, Q. Gong, K. Luo, Z. Gu Enzyme-Sensitive and Amphiphilic PEGylated Dendrimer-Paclitaxel Prodrug-Based Nanoparticles for Enhanced Stability and Anticancer Efficacy, ACS Appl. Mater. Interfaces, 9 (2017), pp. 6865-6877
W. Yin, J. Li, W. Ke, Z. Zha, Z. Ge Integrated Nanoparticles To Synergistically Elevate Tumor Oxidative Stress and Suppress Antioxidative Capability for Amplified Oxidation Therapy,
ACS Appl. Mater. Interfaces, 9 (2017), pp. 29538-29546
S.G. Levesque, M.S. Shoichet Synthesis of Enzyme-Degradable, Peptide-Cross-Linked Dextran Hydrogels Bioconjugate Chemistry, 18 (2007), pp. 874-885
M. Segal, R. Avinery, M. Buzhor, R. Shaharabani, A.J. Harnoy, E. Tirosh, R. Beck, R.J. Amir Molecular Precision and Enzymatic Degradation: From Readily to Undegradable Polymeric Micelles by Minor Structural Changes J. Am. Chem. Soc., 139 (2017), pp. 803-810
I. Rosenbaum, A.J. Harnoy, E. Tirosh, M. Buzhor, M. Segal, L. Frid, R. Shaharabani, R. Avinery, R. Beck, R.J. Amir Encapsulation and Covalent Binding of Molecular Payload in Enzymatically Activated Micellar Nanocarriers J. Am. Chem. Soc., 137 (2015), pp. 2276-2284
J. Guo, J. Zhuang, F. Wang, K.R. Raghupathi, S. Thayumanavan Protein AND Enzyme Gated Supramolecular Disassembly J. Am. Chem. Soc., 136 (2014), pp. 2220-2223
M.-H. Xiong, Y. Bao, X.-J. Du, Z.-B. Tan, Q. Jiang, H.-X. Wang, Y.-H. Zhu, J. Wang Differential Anticancer Drug Delivery with a Nanogel Sensitive to Bacteria-Accumulated Tumor Artificial Environment ACS Nano, 7 (2013), pp. 10636-10645
H. Sun, R. Cheng, C. Deng, F. Meng, A.A. Dias, M. Hendriks, J. Feijen, Z. Zhong Enzymatically and Reductively Degradable α-Amino Acid-Based Poly(ester amide)s: Synthesis, Cell Compatibility, and Intracellular Anticancer Drug Delivery Biomacromolecules, 16 (2015), pp. 597-605
D. Trachootham, J. Alexandre, P. Huang Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Dis., 8 (2009), pp. 579-591
S. Kawanishi, Y. Hiraku, S. Pinlaor, N. Ma Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis Biological Chem. (2006), p. 387
B.L. Allen, J.D. Johnson, J.P. Walker Encapsulation and Enzyme-Mediated Release of Molecular Cargo in Polysulfide Nanoparticles ACS Nano, 5 (2011), pp. 5263-5272
K. Kim, C.-S. Lee, K. Na Light-controlled reactive oxygen species (ROS)-producible polymeric micelles with simultaneous drug-release triggering and endo/lysosomal escape
Chem. Commun., 52 (2016), pp. 2839-2842
F.H. Sobotta, F. Hausig, D.O. Harz, S. Hoeppener, U.S. Schubert, J.C. Brendel Oxidation-responsive micelles by a one-pot polymerization-induced self-assembly approach
Polym. Chem., 9 (2018), pp. 1593-1602
C. de Gracia Lux, S. Joshi-Barr, T. Nguyen, E. Mahmoud, E. Schopf, N. Fomina, A. Almutairi Biocompatible Polymeric Nanoparticles Degrade and Release Cargo in Response to Biologically Relevant Levels of Hydrogen Peroxide J. Am. Chem. Soc., 134 (2012), pp. 15758-15764
M. Zhang, C.-C. Song, F.-S. Du, Z.-C. Li Supersensitive Oxidation-Responsive Biodegradable PEG Hydrogels for Glucose-Triggered Insulin Delivery ACS Appl. Mater. Interfaces, 9 (2017), pp. 25905-25914
L. Brannon-Peppas Poly(ethylene glycol): Chemistry and biological ap Plications J.M. Harris, S. Zalipsky (Eds.), J. Control. Release, 66 (2000), p. 321
K. Knop, R. Hoogenboom, D. Fischer, U.S. Schubert Poly(ethylene glycol) in Drug Delivery: Pros and Cons as Well as Potential Alternatives Angew. Chem., Int. Ed., 49 (2010), pp. 6288-6308
M.W. Kim Surface activity and property of polyethyleneoxide (PEO) in water,
Colloids Surf., A, 128 (1997), pp. 145-154
B.H. Cao, M.W. Kim Molecular weight dependence of the surface tension of aqueous poly(ethylene oxide) solutions Faraday Discuss., 98 (1995), pp. 245-252
A. Bera, K. Ojha, A. Mandal Synergistic Effect of Mixed Surfactant Systems on Foam Behavior and Surface Tension J. Surf. Deter., 16 (2013), pp. 621-630
M. Yao, Y. Ma, H. Liu, M.I. Khan, S. Shen, S. Li, Y. Zhao, Y. Liu, G. Zhang, X. Li, F. Zhong, W. Jiang, Y.Wang Enzyme degradable hyperbranched polyphosphoester micellar nanomedicines for NIR imaging-guided chemo-photothermal therapy of drug-resistant cancers Biomacromolecules, 19 (2018), pp. 1130-1141
W. Wang, J. Ding, C. Xiao, Z. Tang, D. Li, J. Chen, X. Zhuang, X. Chen Synthesis of Amphiphilic Alternating Polyesters with Oligo(ethylene glycol) Side Chains and Potential Use for Sustained Release Drug Delivery Biomacromolecules, 12 (2011), pp. 2466-2474
M.K. Gupta, T.A. Meyer, C.E. Nelson, C.L. Duvall Poly(PS-b-DMA) micelles for reactive oxygen species triggered drug release J. Controlled Release, 162 (2012), pp. 591-598
J.M. Sarapas, G.N. Tew Poly(ether-thioethers) by Thiol-Ene Click and Their Oxidized Analogues as Lithium Polymer Electrolytes Macromolecules, 49 (2016), pp. 1154-1162
B. Yan, Y. Zhang, C. Wei, Y. Xu Facile synthesis of ROS-responsive biodegradable main chain poly(carbonate-thioether) copolymers Polym. Chem., 9 (2018), pp. 904-911
Z. Gao, T. Ma, E. Zhao, D. Docter, W. Yang, R.H. Stauber, M. Gao Small is Smarter: Nano MRI Contrast Agents - Advantages and Recent Achievements Small, 12 (2016), pp. 556-576
C.D. Walkey, J.B. Olsen, H. Guo, A. Emili, W.C.W. Chan Nanoparticle Size and Surface Chemistry Determine Serum Protein Adsorption and Macrophage Uptake J. Am. Chem. Soc., 134 (2012), pp. 2139-2147
S. Kashyap, N. Singh, B. Surnar, M. Jayakannan Enzyme and Thermal Dual Responsive Amphiphilic Polymer Core–Shell Nanoparticle for Doxorubicin Delivery to Cancer Cells Biomacromolecules, 17 (2015), pp. 384-398
M. Conda-Sheridan, S.S. Lee, A.T. Preslar, S.I. Stupp Esterase-activated release of naproxen from supramolecular nanofibers Chem. Commun., 50 (2014), pp. 13757-13760
S. Aleksanian, B. Khorsand, R. Schmidt, J.K. Oh Rapidly thiol-responsive degradable block copolymer nanocarriers with facile bioconjugation Polym. Chem., 3 (2012), pp. 2138-2147
N. Chan, B. Khorsand, S. Aleksanian, J.K. Oh A dual location stimuli-responsive degradation strategy of block copolymer nanocarriers for accelerated release Chem. Commun., 49 (2013), pp. 7534-7536
J. Herzberger, K. Fischer, D. Leibig, M. Bros, R. Thiermann, H. Frey Oxidation-responsive and “clickable” poly (ethylene glycol) via copolymerization of 2-(methylthio) ethyl glycidyl ether J. Am. Chem. Soc., 138 (2016), pp. 9212-9223
I.N. Kurniasih, H. Liang, P.C. Mohr, G. Khot, J.P. Rabe, A. Mohr Nile Red Dye in Aqueous Surfactant and Micellar Solution Langmuir, 31 (2015), pp. 2639-2648
J.A. Bohnert, B. Karamian, H. Nikaido Optimized Nile Red Efflux Assay of AcrAB-TolC Multidrug Efflux System Shows Competition between Substrates Antimicrob. Agents Chemother., 54 (2010), pp. 3770-3775
Y.T. Phung, D. Barbone, V.C. Broaddus, M. Ho Rapid generation of in vitro multicellular spheroids for the study of monoclonal antibody therapy J. Cancer, 2 (2011), p. 507
T.-G. Iversen, T. Skotland, K. Sandvig Endocytosis and intracellular transport of nanparticles: present knowledge and need for future studies Nano Today, 6 (2011), pp. 176-185
B. Yameen, W.I. Choi, C. Vilos, A. Swami, J. Shi, O.C. Farokhzad Insight into nanoparticle cellular uptake and intracellular targeting J. Controlled Release, 190 (2014), pp. 485-499
S.-J. Seo, M. Chen, H. Wang, M.S. Kang, K.W. Leong, H.-W. Kim Extra- and intra-cellular fate of nanocarriers under dynamic interactions with biology Nano Today, 14 (2017), pp. 84-99
J. Zhao, M.H. Stenzel Entry of nanoparticles into cells: the importance of nanoparticle properties Polym. Chem., 9 (2018), pp. 259-272
L.H. Wang, K.G. Rothberg, R.G.W. Anderson Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation J. Cell Biol., 123 (1993), pp. 1107-1118
R.G. Parton, B. Joggerst, K. Simons Regulated internalization of caveolae J. Cell Biol., 127 (1994), pp. 1199-1216
G. Sahay, D.Y. Alakhova, A.V. Kabanov Endocytosis of nanomedicines J. Controlled Release, 145 (2010), pp. 182-195
All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access.
Repository Staff Only: item control page
Download Statistics
Download Statistics