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In Situ Photo-crosslinkable Hyaluronic Acid/Gelatin Hydrogel for Local Nitric Oxide Delivery

  • Daniele M. Catori
    Daniele M. Catori
    Institute of Chemistry, University of Campinas, UNICAMP, Campinas 13083-970, São Paulo, Brazil
  • Laura C. E. da Silva
    Laura C. E. da Silva
    Institute of Chemistry, University of Campinas, UNICAMP, Campinas 13083-970, São Paulo, Brazil
  • Matheus F. de Oliveira
    Matheus F. de Oliveira
    Institute of Chemistry, University of Campinas, UNICAMP, Campinas 13083-970, São Paulo, Brazil
  • Grace H. Nguyen
    Grace H. Nguyen
    School of Chemical, Materials and Biomedical Engineering, College of Engineering, University of Georgia, Athens 30602, Georgia, United States
  • Joseph C. Moses
    Joseph C. Moses
    School of Chemical, Materials and Biomedical Engineering, College of Engineering, University of Georgia, Athens 30602, Georgia, United States
  • Elizabeth J. Brisbois
    Elizabeth J. Brisbois
    School of Chemical, Materials and Biomedical Engineering, College of Engineering, University of Georgia, Athens 30602, Georgia, United States
  • Hitesh Handa*
    Hitesh Handa
    School of Chemical, Materials and Biomedical Engineering, College of Engineering, University of Georgia, Athens 30602, Georgia, United States
    Pharmaceutical and Biomedical Sciences Department, College of Pharmacy, University of Georgia, Athens 30602, Georgia, United States
    *Email: [email protected]. Phone: (706) 542-8109.
    More by Hitesh Handa
  • , and 
  • Marcelo G. de Oliveira*
    Marcelo G. de Oliveira
    Institute of Chemistry, University of Campinas, UNICAMP, Campinas 13083-970, São Paulo, Brazil
    *Email: [email protected]. Phone: +55 (19) 3521-3132.
Cite this: ACS Appl. Mater. Interfaces 2023, 15, 42, 48930–48944
Publication Date (Web):October 12, 2023
https://doi.org/10.1021/acsami.3c10030
Copyright © 2023 American Chemical Society

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    Abstract

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    An increasing number of studies have shown that the local release of nitric oxide (NO) from hydrogels stimulates tissue regeneration by modulating cell proliferation, angiogenesis, and inflammation. The potential biomedical uses of NO-releasing hydrogels can be expanded by enabling their application in a fluid state, followed by controlled gelation triggered by an external factor. In this study, we engineered a hydrogel composed of methacrylated hyaluronic acid (HAGMA) and thiolated gelatin (GELSH) with the capacity for in situ photo-cross-linking, coupled with localized NO release. To ensure a gradual and sustained NO release, we charged the hydrogels with poly(l-lactic-co-glycolic acid) (PLGA) nanoparticles functionalized with S-nitrosoglutathione (GSNO), safeguarding SNO group integrity during photo-cross-linking. The formation of thiol–ene bonds via the reaction between GELSH’s thiol groups and HAGMA’s vinyl groups substantially accelerated gelation (by a factor of 6) and increased the elastic modulus of hydrated hydrogels (by 1.9–2.4 times). HAGMA/GELSH hydrogels consistently released NO over a 14 day duration, with the release of NO depending on the hydrogels’ equilibrium swelling degree, determined by the GELSH-to-HAGMA ratio. Biocompatibility assessments confirmed the suitability of these hydrogels for biological applications as they display low cytotoxicity and stimulated fibroblast adhesion and proliferation. In conclusion, in situ photo-cross-linkable HAGMA/GELSH hydrogels, loaded with PLGA-GSNO nanoparticles, present a promising avenue for achieving localized and sustained NO delivery in tissue regeneration applications.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.3c10030.

    • 1H NMR spectrum of HAGMA; schemes of the reaction between HA and GMA, and GEL and HCT; FTIR-ATR spectra of HA, GMA, HAGMA, GEL, and GELSH; mean hydrodynamic diameters of NPPLGA-GSNO obtained by dynamic light scattering; surface charge measured by zeta potential of NPPLGA-GSNO as a function of pH; calibration curve of GSNO in DMSO in the concentration range of 0.1–0.7 mmol L–1 measured at 336 nm; UV–vis absorption spectrum of NPPLGA-GSNO dispersed in DMSO; schemes of the photo-cross-linking reactions between vinyl groups of HAGMA, leading to the formation of HHA, and the reaction between the vinyl group of HGGMA and the thiol group of GELSH, leading to the formation of thiol–ene bond in HAG; variation of the G′ and G″ moduli as a function of the irradiation time for HHA in the absence and in the presence of free GSNO at the concentration of 0.15 mmol L–1; bar graph of the elastic modulus of HHA, NPHHA, HAG0.5, NPHAG0.5, HAG1, and NPHAG1; SEM images of the HHA, NPHHA, HAG0.5, NPHAG0.5, HAG1, and NPHAG1 hydrogels; and optical microscopy images of fibroblast adhesion on the controls (2D control and collagen) and HHA, NPHHA, HAG0.5, NPHAG0.5, HAG1, NPHAG1 hydrogels after 0 h, 24 and 72 h of incubation (PDF)

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