Scalable fabrication of metal-phenolic nanoparticles by coordination-driven flash nanocomplexation for cancer theranostics.

Although various nanomaterials have been developed for cancer theranostics, there remains a key challenge for effective integration of therapeutic drugs and diagnostic agents into a single multicomponent nanoparticle via a simple and scalable approach. Moreover, the bottlenecks of nanoformulation in composition controllability, colloidal stability, drug loading capability and batch-to-batch repeatability currently still hinder the clinical translation of nanomedicine. Herein, we report a coordination-driven flash nanocomplexation (cFNC) process to achieve scalable fabrication of doxorubicin-based metal-phenolic nanoparticles (DITH) with a hyaluronic acid surface layer through efficient control of coordination reaction kinetics in a rapid turbulent mixing. The optimized DITH exhibited a small hydrodynamic diameter (84 nm), narrow size distribution, high drug loading capacity (26.6%), high reproducibility and pH-triggered drug release behaviors. The studies indicated that DITH significantly increased cellular endocytosis mediated by CD44+ receptor targeting and accelerated intracellular drug release owing to the sensitivity of DITH to environmental pH stimuli. Furthermore, guided by T1-weighted magnetic resonance (MR) imaging function endowed by ferric ions, DITH exhibited prolonged blood circulation, enhanced tumor accumulation, improved therapeutic performance and decreased toxic side effects after intravenous injection in a MCF-7 tumor-bearing mice model. These results confirmed that the developed DITH is a promising vehicle for cancer theranostic applications, and our work provided a new strategy to promote the development of translational nanomedicine.

[1]  K. Leong,et al.  Scalable Manufacturing of Enteric Encapsulation Systems for Site-Specific Oral Insulin Delivery. , 2018, Biomacromolecules.

[2]  Hai-Quan Mao,et al.  Hydrogen-Bonded Tannic Acid-Based Anticancer Nanoparticle for Enhancement of Oral Chemotherapy. , 2018, ACS applied materials & interfaces.

[3]  Yiyun Cheng,et al.  Foe to Friend: Supramolecular Nanomedicines Consisting of Natural Polyphenols and Bortezomib. , 2018, Nano letters.

[4]  Shengke Li,et al.  Polymeric Nanomedicine with "Lego" Surface Allowing Modular Functionalization and Drug Encapsulation. , 2018, ACS applied materials & interfaces.

[5]  Kam W Leong,et al.  Uniform Core–Shell Nanoparticles with Thiolated Hyaluronic Acid Coating to Enhance Oral Delivery of Insulin , 2018, Advanced healthcare materials.

[6]  Xuesi Chen,et al.  Tailoring Platinum(IV) Amphiphiles for Self-Targeting All-in-One Assemblies as Precise Multimodal Theranostic Nanomedicine. , 2018, ACS nano.

[7]  Xiaoquan Yang,et al.  Metal Ion/Tannic Acid Assembly as a Versatile Photothermal Platform in Engineering Multimodal Nanotheranostics for Advanced Applications. , 2018, ACS nano.

[8]  Xuesi Chen,et al.  Self‐Stabilized Hyaluronate Nanogel for Intracellular Codelivery of Doxorubicin and Cisplatin to Osteosarcoma , 2018, Advanced science.

[9]  K. Leong,et al.  Scalable production of core-shell nanoparticles by flash nanocomplexation to enhance mucosal transport for oral delivery of insulin. , 2018, Nanoscale.

[10]  Jianqing Gao,et al.  Mitochondrial Targeted Doxorubicin-Triphenylphosphonium Delivered by Hyaluronic Acid Modified and pH Responsive Nanocarriers to Breast Tumor: in Vitro and in Vivo Studies. , 2018, Molecular pharmaceutics.

[11]  Jean-Christophe Leroux,et al.  Editorial: Drug Delivery: Too Much Complexity, Not Enough Reproducibility? , 2017, Angewandte Chemie.

[12]  Zhijia Liu,et al.  Shear-responsive injectable supramolecular hydrogel releasing doxorubicin loaded micelles with pH-sensitivity for local tumor chemotherapy. , 2017, International journal of pharmaceutics.

[13]  Ruibing Wang,et al.  pH-Responsive prodrug nanoparticles based on a sodium alginate derivative for selective co-release of doxorubicin and curcumin into tumor cells. , 2017, Nanoscale.

[14]  Hongbo Zhang,et al.  Current developments and applications of microfluidic technology toward clinical translation of nanomedicines☆ , 2017, Advanced drug delivery reviews.

[15]  Xiaoyuan Chen,et al.  Rethinking cancer nanotheranostics. , 2017, Nature reviews. Materials.

[16]  Zhiyuan Zhong,et al.  Robust, tumor-homing and redox-sensitive polymersomal doxorubicin: A superior alternative to Doxil and Caelyx? , 2016, Journal of controlled release : official journal of the Controlled Release Society.

[17]  D. Sohn,et al.  Phase Controllable Hyaluronic Acid Hydrogel with Iron(III) Ion–Catechol Induced Dual Cross-Linking by Utilizing the Gap of Gelation Kinetics , 2016 .

[18]  Joseph J. Richardson,et al.  Engineered Metal-Phenolic Capsules Show Tunable Targeted Delivery to Cancer Cells. , 2016, Biomacromolecules.

[19]  Ning Zhang,et al.  Interfacial Cohesion and Assembly of Bioadhesive Molecules for Design of Long-Term Stable Hydrophobic Nanodrugs toward Effective Anticancer Therapy. , 2016, ACS nano.

[20]  R. Prud’homme,et al.  Principles of nanoparticle formation by flash nanoprecipitation , 2016 .

[21]  P. Prasad,et al.  Nanochemistry and Nanomedicine for Nanoparticle-based Diagnostics and Therapy. , 2016, Chemical reviews.

[22]  J. L. Santos,et al.  Control of polymeric nanoparticle size to improve therapeutic delivery. , 2015, Journal of controlled release : official journal of the Controlled Release Society.

[23]  Zhijia Liu,et al.  Injectable shear-thinning xanthan gum hydrogel reinforced by mussel-inspired secondary crosslinking , 2015 .

[24]  Zhijia Liu,et al.  Injectable thermo-responsive hydrogel composed of xanthan gum and methylcellulose double networks with shear-thinning property. , 2015, Carbohydrate polymers.

[25]  Huimao Zhang,et al.  Gram-scale synthesis of coordination polymer nanodots with renal clearance properties for cancer theranostic applications , 2015, Nature Communications.

[26]  Mengmeng Sun,et al.  Design of tumor-homing and pH-responsive polypeptide-doxorubicin nanoparticles with enhanced anticancer efficacy and reduced side effects. , 2015, Chemical communications.

[27]  Bum Jin Kim,et al.  Mussel-Inspired Protein Nanoparticles Containing Iron(III)-DOPA Complexes for pH-Responsive Drug Delivery. , 2015, Angewandte Chemie.

[28]  Zhiyuan Zhong,et al.  Reversibly crosslinked hyaluronic acid nanoparticles for active targeting and intelligent delivery of doxorubicin to drug resistant CD44+ human breast tumor xenografts. , 2015, Journal of controlled release : official journal of the Controlled Release Society.

[29]  Hak Soo Choi,et al.  Self-assembled micellar nanocomplexes comprising green tea catechin derivatives and protein drugs for cancer therapy , 2014, Nature nanotechnology.

[30]  Q. Ping,et al.  Kidney-specific drug delivery system for renal fibrosis based on coordination-driven assembly of catechol-derived chitosan. , 2014, Biomaterials.

[31]  Xinling Wang,et al.  Facile preparation of mussel-inspired polyurethane hydrogel and its rapid curing behavior. , 2014, ACS applied materials & interfaces.

[32]  Robert Langer,et al.  Ultra-High Throughput Synthesis of Nanoparticles with Homogeneous Size Distribution Using a Coaxial Turbulent Jet Mixer , 2014, ACS nano.

[33]  Lehui Lu,et al.  Polydopamine and its derivative materials: synthesis and promising applications in energy, environmental, and biomedical fields. , 2014, Chemical reviews.

[34]  Jiwei Cui,et al.  One-Step Assembly of Coordination Complexes for Versatile Film and Particle Engineering , 2013, Science.

[35]  S. Vinogradov,et al.  Hyaluronic acid-based nanogel-drug conjugates with enhanced anticancer activity designed for the targeting of CD44-positive and drug-resistant tumors. , 2013, Bioconjugate chemistry.

[36]  F. Busqué,et al.  Catechol‐Based Biomimetic Functional Materials , 2013, Advanced materials.

[37]  Kostas Kostarelos,et al.  Liposomes: from a clinically established drug delivery system to a nanoparticle platform for theranostic nanomedicine. , 2011, Accounts of chemical research.

[38]  Kurt E. Geckeler,et al.  Polymer nanoparticles: Preparation techniques and size-control parameters , 2011 .

[39]  S. Van Vlierberghe,et al.  Biopolymer-based hydrogels as scaffolds for tissue engineering applications: a review. , 2011, Biomacromolecules.

[40]  Henrik Birkedal,et al.  pH-induced metal-ligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli , 2011, Proceedings of the National Academy of Sciences.

[41]  Hongbo Zeng,et al.  Strong reversible Fe3+-mediated bridging between dopa-containing protein films in water , 2010, Proceedings of the National Academy of Sciences.

[42]  Peter Fratzl,et al.  Iron-Clad Fibers: A Metal-Based Biological Strategy for Hard Flexible Coatings , 2010, Science.

[43]  Robert Langer,et al.  Microfluidic platform for controlled synthesis of polymeric nanoparticles. , 2008, Nano letters.

[44]  Haeshin Lee,et al.  Mussel-Inspired Surface Chemistry for Multifunctional Coatings , 2007, Science.

[45]  N. Lu,et al.  Transferrin-inspired vehicles based on pH-responsive coordination bond to combat multidrug-resistant breast cancer. , 2017, Biomaterials.

[46]  Zhijia Liu,et al.  Versatile injectable supramolecular hydrogels containing drug loaded micelles for delivery of various drugs , 2014 .