Adaptable Hydrogels Mediate Cofactor‐Assisted Activation of Biomarker‐Responsive Drug Delivery via Positive Feedback for Enhanced Tissue Regeneration

The targeted and simultaneous delivery of diverse cargoes with vastly different properties by the same vehicle is highly appealing but challenging. Here, a bioactive nanocomposite hydrogel based on hyaluronic acid and self-assembled pamidronate-magnesium nanoparticles for the localized elution and on-demand simultaneous release of bioactive ions and small molecule drugs is described. The obtained nanocomposite hydrogels exhibit excellent injectability and efficient stress relaxation, thereby allowing easy injection and consequent adaptation of hydrogels to bone defects with irregular shapes. Magnesium ions released from the hydrogels promote osteogenic differentiation of the encapsulated human mesenchymal stem cells (hMSCs) and activation of alkaline phosphatase (ALP). The activated ALP subsequently catalyzes the dephosphorylation (activation) of Dex phosphate, a pro-drug of Dex, and expedites the release of Dex from hydrogels to further promote hMSC osteogenesis. This positive feedback circuit governing the activation and release of Dex significantly enhances bone regeneration at the hydrogel implantation sites. The findings suggest that these injectable nanocomposite hydrogels mediate optimized release of diverse therapeutic cargoes and effectively promote in situ bone regeneration via minimally invasive procedures.

[1]  Ying Liu,et al.  Local and sustained miRNA delivery from an injectable hydrogel promotes cardiomyocyte proliferation and functional regeneration after ischemic injury , 2017, Nature Biomedical Engineering.

[2]  Khusru Asadullah,et al.  Mechanisms involved in the side effects of glucocorticoids. , 2002, Pharmacology & therapeutics.

[3]  Su‐Li Cheng,et al.  Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. , 1994, Endocrinology.

[4]  J. Cowan Structural and catalytic chemistry of magnesium-dependent enzymes , 2002, Biometals.

[5]  Arti Vashist,et al.  Recent advances in hydrogel based drug delivery systems for the human body. , 2014, Journal of materials chemistry. B.

[6]  O. Lee,et al.  Dexamethasone-induced cellular tension requires a SGK1-stimulated Sec5–GEF-H1 interaction , 2015, Journal of Cell Science.

[7]  Yufeng Zheng,et al.  Implant-derived magnesium induces local neuronal production of CGRP to improve bone-fracture healing in rats , 2016, Nature Medicine.

[8]  E. Alsberg,et al.  In‐Situ Formation of Growth‐Factor‐Loaded Coacervate Microparticle‐Embedded Hydrogels for Directing Encapsulated Stem Cell Fate , 2015, Advanced materials.

[9]  C. R. Howlett,et al.  Mechanisms of magnesium-stimulated adhesion of osteoblastic cells to commonly used orthopaedic implants. , 2002, Journal of biomedical materials research.

[10]  Jason A Burdick,et al.  Progress in material design for biomedical applications , 2015, Proceedings of the National Academy of Sciences.

[11]  R. Reid,et al.  Hydrogel drug delivery system with predictable and tunable drug release and degradation rates , 2013, Proceedings of the National Academy of Sciences.

[12]  H. Tanihara,et al.  Involvement of RhoA/Rho-associated kinase signal transduction pathway in dexamethasone-induced alterations in aqueous outflow. , 2012, Investigative ophthalmology & visual science.

[13]  Yun Bai,et al.  Graphene‐Based MicroRNA Transfection Blocks Preosteoclast Fusion to Increase Bone Formation and Vascularization , 2017, Advanced science.

[14]  J. Millán Alkaline Phosphatases , 2006, Purinergic Signalling.

[15]  M. Kaplan Alkaline phosphatase. , 1972, Gastroenterology.

[16]  Kongchang Wei,et al.  Bioadhesive Polymersome for Localized and Sustained Drug Delivery at Pathological Sites with Harsh Enzymatic and Fluidic Environment via Supramolecular Host-Guest Complexation. , 2018, Small.

[17]  C. Sharma,et al.  Effect of calcium, zinc and magnesium on the attachment and spreading of osteoblast like cells onto ceramic matrices , 2007, Journal of materials science. Materials in medicine.

[18]  Hui-zhen Jia,et al.  NIR‐Activated Polydopamine‐Coated Carrier‐Free “Nanobomb” for In Situ On‐Demand Drug Release , 2018, Advanced science.

[19]  Alexis M Pietak,et al.  Magnesium and its alloys as orthopedic biomaterials: a review. , 2006, Biomaterials.

[20]  Qian Feng,et al.  Mechanically resilient, injectable, and bioadhesive supramolecular gelatin hydrogels crosslinked by weak host-guest interactions assist cell infiltration and in situ tissue regeneration. , 2016, Biomaterials.

[21]  H. Haferkamp,et al.  In vivo corrosion of four magnesium alloys and the associated bone response. , 2005, Biomaterials.

[22]  Yisheng Wang,et al.  Dexamethasone-induced adipogenesis in primary marrow stromal cell cultures: mechanism of steroid-induced osteonecrosis. , 2006, Chinese medical journal.

[23]  James C. Weaver,et al.  Hydrogels with tunable stress relaxation regulate stem cell fate and activity , 2015, Nature materials.

[24]  D. Kohane,et al.  A Supramolecular Shear‐Thinning Anti‐Inflammatory Steroid Hydrogel , 2016, Advanced materials.

[25]  P. Barnes,et al.  Anti-inflammatory actions of glucocorticoids: molecular mechanisms. , 1998, Clinical science.

[26]  J. Simon,et al.  Immune responses to implants - a review of the implications for the design of immunomodulatory biomaterials. , 2011, Biomaterials.

[27]  C. Devlin,et al.  Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. , 1992, Journal of cell science.

[28]  Ali Khademhosseini,et al.  Advances in engineering hydrogels , 2017, Science.

[29]  Won Jong Kim,et al.  Reactive‐Oxygen‐Species‐Responsive Drug Delivery Systems: Promises and Challenges , 2016, Advanced science.

[30]  S. Bruder,et al.  Osteogenic differentiation of purified, culture‐expanded human mesenchymal stem cells in vitro , 1997, Journal of cellular biochemistry.

[31]  Liming Bian,et al.  Self‐Assembled Injectable Nanocomposite Hydrogels Stabilized by Bisphosphonate‐Magnesium (Mg2+) Coordination Regulates the Differentiation of Encapsulated Stem Cells via Dual Crosslinking , 2017 .

[32]  K. Furukawa,et al.  Enhancing osteogenic differentiation of MC3T3-E1 cells by immobilizing inorganic polyphosphate onto hyaluronic acid hydrogel. , 2015, Biomacromolecules.

[33]  R. Swaminathan Magnesium metabolism and its disorders. , 2003, The Clinical biochemist. Reviews.

[34]  K. Chapman,et al.  The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights , 2011, Molecular and Cellular Endocrinology.

[35]  Christopher S. Chen,et al.  Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. , 2004, Developmental cell.

[36]  N. Lane,et al.  Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. , 2008, Arthritis and rheumatism.

[37]  Hongbo Wang,et al.  An Injectable Supramolecular Polymer Nanocomposite Hydrogel for Prevention of Breast Cancer Recurrence with Theranostic and Mammoplastic Functions , 2018 .

[38]  R. Weinstein,et al.  Apoptosis of osteocytes in glucocorticoid-induced osteonecrosis of the hip. , 2000, The Journal of clinical endocrinology and metabolism.

[39]  Zhen Gu,et al.  ATP-triggered anticancer drug delivery , 2014, Nature Communications.

[40]  Robert Langer,et al.  An inflammation-targeting hydrogel for local drug delivery in inflammatory bowel disease , 2015, Science Translational Medicine.

[41]  Liming Bian,et al.  Nanocomposite hydrogels stabilized by self-assembled multivalent bisphosphonate-magnesium nanoparticles mediate sustained release of magnesium ion and promote in-situ bone regeneration. , 2017, Acta biomaterialia.

[42]  L. Raisz,et al.  Glucocorticoid-induced osteoporosis: pathogenesis and management. , 1990, Annals of internal medicine.

[43]  Y. Yamagami,et al.  Effects of suppressed bone remodeling by minodronic acid and alendronate on bone mass, microdamage accumulation, collagen crosslinks and bone mechanical properties in the lumbar vertebra of ovariectomized cynomolgus monkeys. , 2017, Bone.

[44]  B. Boyan,et al.  Inhibition of angiogenesis impairs bone healing in an in vivo murine rapid resynostosis model. , 2017, Journal of biomedical materials research. Part A.

[45]  B. Evans,et al.  The effect of nitrogen containing bisphosphonates, zoledronate and alendronate, on the production of pro-angiogenic factors by osteoblastic cells. , 2015, Cytokine.

[46]  Hongling Li,et al.  miR-216a rescues dexamethasone suppression of osteogenesis, promotes osteoblast differentiation and enhances bone formation, by regulating c-Cbl-mediated PI3K/AKT pathway , 2015, Cell Death and Differentiation.