In Vivo and Cellular Trafficking of Acetalated Dextran Microparticles for Delivery of a Host-Directed Therapy for Salmonella enterica Serovar Typhi Infection.

Previously we have encapsulated host-directed therapy AR-12 into acetalated dextran (Ace-DEX) microparticles (MPs) to mitigate drug toxicity and passively target phagocytic host cells. Herein, we have improved upon our initial emulsion-based formulation of Ace-DEX MPs encapsulating AR-12 (AR-12/MPs) by improving the drug encapsulation efficiency, evaluating sterilization processes for manufacturing, and understanding cellular and in vivo trafficking of the MPs. By using an alternative solvent system, ethyl acetate, we report an increased encapsulation efficiency of AR-12 while maintaining the pH-responsive degradation kinetics of Ace-DEX MPs. To better manufacture this novel antimicrobial formulation, we sterilized AR-12/MPs by gamma irradiation or ethylene oxide and evaluated their efficacy against intracellular Salmonella enterica serovar Typhi. Sterilized AR-12/MPs resulted in a significant reduction in intracellular bacterial burden compared to Blank/MPs. We also characterized intracellular trafficking of Ace-DEX MPs encapsulating fluorophores, which demonstrated internalization of MPs in endo/lysosomal compartments and time and degradation-rate dependent lysosomal escape into cytosolic compartments. Additionally, in vivo toxicity was mitigated following encapsulation of AR-12, where the maximum tolerated dose of AR-12 was increased compared to soluble treatment via intranasal, intravenous, and intraperitoneal administration routes. Following in vivo trafficking of Ace-DEX MPs via the same routes, intranasal administration demonstrated the highest accumulation in the lungs, liver, and kidneys, which persisted out to 240 h. Overall, we have advanced the formulation of this host-directed therapy and broadened the understanding of Ace-DEX MP delivery.

[1]  W. Hennink,et al.  The microclimate pH in poly(D,L-lactide-co-hydroxymethyl glycolide) microspheres during biodegradation. , 2012, Biomaterials.

[2]  K. Ainslie,et al.  Host-mediated Leishmania donovani treatment using AR-12 encapsulated in acetalated dextran microparticles. , 2016, International journal of pharmaceutics.

[3]  Mauro Ferrari,et al.  Principles of nanoparticle design for overcoming biological barriers to drug delivery , 2015, Nature Biotechnology.

[4]  A. Scala,et al.  Intracellular trafficking and therapeutic outcome of multiwalled carbon nanotubes modified with cyclodextrins and polyethylenimine. , 2018, Colloids and surfaces. B, Biointerfaces.

[5]  Diane J Burgess,et al.  Effect of acidic pH on PLGA microsphere degradation and release. , 2007, Journal of controlled release : official journal of the Controlled Release Society.

[6]  Samantha A. Meenach,et al.  Enhanced stability of horseradish peroxidase encapsulated in acetalated dextran microparticles stored outside cold chain conditions. , 2012, International journal of pharmaceutics.

[7]  J. Lee,et al.  Dose Escalation Methods in Phase I Cancer Clinical Trials , 2009, Journal of the National Cancer Institute.

[8]  Marcel Leist,et al.  Cathepsin B Acts as a Dominant Execution Protease in Tumor Cell Apoptosis Induced by Tumor Necrosis Factor , 2001, The Journal of cell biology.

[9]  S. Kulp,et al.  Eradication of intracellular Francisella tularensis in THP-1 human macrophages with a novel autophagy inducing agent , 2009, Journal of Biomedical Science.

[10]  Tao Jiang,et al.  A Comparison of Intravenous plus Intraperitoneal Chemotherapy with Intravenous Chemotherapy Alone for the Treatment of Gastric Cancer: A Meta-Analysis , 2015, Scientific Reports.

[11]  F. Cordelières,et al.  A guided tour into subcellular colocalization analysis in light microscopy , 2006, Journal of microscopy.

[12]  P. Dent,et al.  AR‐12 Inhibits Multiple Chaperones Concomitant With Stimulating Autophagosome Formation Collectively Preventing Virus Replication , 2016, Journal of cellular physiology.

[13]  Graham C. Collins,et al.  Degradation of acetalated dextran can be broadly tuned based on cyclic acetal coverage and molecular weight. , 2016, International journal of pharmaceutics.

[14]  Benu Sethi,et al.  Sterilization techniques for biodegradable scaffolds in tissue engineering applications , 2016, Journal of tissue engineering.

[15]  H. Takeuchi,et al.  Real-time in vivo imaging of surface-modified liposomes to evaluate their behavior after pulmonary administration. , 2014, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[16]  O. Farokhzad,et al.  Challenges in DNA Delivery and Recent Advances in Multifunctional Polymeric DNA Delivery Systems. , 2017, Biomacromolecules.

[17]  K. Ainslie,et al.  Tunable degradation of acetalated dextran microparticles enables controlled vaccine adjuvant and antigen delivery to modulate adaptive immune responses , 2018, Journal of controlled release : official journal of the Controlled Release Society.

[18]  Uwe Sukowski,et al.  Cyanine dyes as contrast agents for near-infrared imaging in vivo: acute tolerance, pharmacokinetics, and fluorescence imaging. , 2011, Journal of biomedical optics.

[19]  O. Shirihai,et al.  Nanoparticle tumor localization, disruption of autophagosomal trafficking, and prolonged drug delivery improve survival in peritoneal mesothelioma. , 2016, Biomaterials.

[20]  Liguo Wang,et al.  Controlled Endolysosomal Release of Agents by pH-responsive Polymer Blend Particles , 2015, Pharmaceutical Research.

[21]  S. Gilch,et al.  The celecoxib derivatives AR-12 and AR-14 induce autophagy and clear prion-infected cells from prions , 2017, Scientific Reports.

[22]  P. Flandroy,et al.  Preparation of poly (D,L) lactide microspheres by emulsion-solvent evaporation, and their clinical applications as a convenient embolic material. , 1992, Journal of biomedical materials research.

[23]  Ivo D. Shterev,et al.  A robust microparticle platform for a STING‐targeted adjuvant that enhances both humoral and cellular immunity during vaccination , 2017, Journal of controlled release : official journal of the Controlled Release Society.

[24]  T. Anchordoquy,et al.  Drug delivery trends in clinical trials and translational medicine: challenges and opportunities in the delivery of nucleic acid-based therapeutics. , 2011, Journal of pharmaceutical sciences.

[25]  T. Ebensen,et al.  New Horizons in the Development of Novel Needle-Free Immunization Strategies to Increase Vaccination Efficacy. , 2016, Current topics in microbiology and immunology.

[26]  Hong Ding,et al.  Development of PEGylated PLGA nanoparticle for controlled and sustained drug delivery in cystic fibrosis , 2010, Journal of nanobiotechnology.

[27]  Darrell J Irvine,et al.  Cytosolic delivery of membrane-impermeable molecules in dendritic cells using pH-responsive core-shell nanoparticles. , 2007, Nano letters.

[28]  Vasilis Ntziachristos,et al.  Dynamic imaging of PEGylated indocyanine green (ICG) liposomes within the tumor microenvironment using multi-spectral optoacoustic tomography (MSOT). , 2015, Biomaterials.

[29]  Stephen J. Lomnes,et al.  Tissue-like phantoms for near-infrared fluorescence imaging system assessment and the training of surgeons. , 2006, Journal of biomedical optics.

[30]  Yee‐Shin Lin,et al.  AR‐12 suppresses dengue virus replication by down‐regulation of PI3K/AKT and GRP78 , 2017, Antiviral research.

[31]  K. Christman,et al.  Tunable protein release from acetalated dextran microparticles: a platform for delivery of protein therapeutics to the heart post-MI. , 2013, Biomacromolecules.

[32]  Shutao Guo,et al.  Nanoparticles escaping RES and endosome: challenges for siRNA delivery for cancer therapy , 2011 .

[33]  Jayanth Panyam,et al.  Rapid endo‐lysosomal escape of poly(DL‐lactide‐coglycolide) nanoparticles: implications for drug and gene delivery , 2002, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[34]  T. Jämsä,et al.  Gamma Irradiation and Ethylene Oxide in the Sterilization of Native Reindeer Bone Morphogenetic Protein Extract , 2005, Scandinavian journal of surgery : SJS : official organ for the Finnish Surgical Society and the Scandinavian Surgical Society.

[35]  Akhilesh Kumar Shakya,et al.  Adjuvant properties of a biocompatible thermo-responsive polymer of N-isopropylacrylamide in autoimmunity and arthritis , 2011, Journal of The Royal Society Interface.

[36]  M. Sullivan,et al.  Journey to the Center of the Cell: Current Nanocarrier Design Strategies Targeting Biopharmaceuticals to the Cytoplasm and Nucleus. , 2016, Current pharmaceutical design.

[37]  Erica N Pino,et al.  Acetalated Dextran: A Tunable and Acid-Labile Biopolymer with Facile Synthesis and a Range of Applications. , 2017, Chemical reviews.

[38]  E. Korn Cell membranes: structure and synthesis. , 1969, Annual Review of Biochemistry.

[39]  J. Gunn,et al.  Delivery of host cell-directed therapeutics for intracellular pathogen clearance , 2013, Expert review of anti-infective therapy.

[40]  R. Langer,et al.  Biodegradable polymeric microspheres and nanospheres for drug delivery in the peritoneum. , 2006, Journal of biomedical materials research. Part A.

[41]  Kevin J. Kauffman,et al.  Synthesis and characterization of acetalated dextran polymer and microparticles with ethanol as a degradation product. , 2012, ACS applied materials & interfaces.

[42]  Murugesan V. S. Rajaram,et al.  Acetalated dextran encapsulated AR-12 as a host-directed therapy to control Salmonella infection. , 2014, International journal of pharmaceutics.

[43]  Kyle E Broaders,et al.  Acetal-derivatized dextran: an acid-responsive biodegradable material for therapeutic applications. , 2008, Journal of the American Chemical Society.

[44]  B. Coburn,et al.  Salmonella, the host and disease: a brief review , 2007, Immunology and cell biology.