Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imaging
Abstract Artificial biomaterials can significantly increase the rate of tissue regeneration. However, implantation of scaffolds leads not only to accelerated tissue healing but also to an immune response of the organism, which results in the degradation of the biomaterial. The synergy of the immune...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2022-06-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-14138-5 |
| _version_ | 1811334590769397760 |
|---|---|
| author | B. P. Yakimov I. I. Vlasova Y. M. Efremov E. G. Maksimov E. A. Shirshin V. E. Kagan P. S. Timashev |
| author_facet | B. P. Yakimov I. I. Vlasova Y. M. Efremov E. G. Maksimov E. A. Shirshin V. E. Kagan P. S. Timashev |
| author_sort | B. P. Yakimov |
| collection | DOAJ |
| description | Abstract Artificial biomaterials can significantly increase the rate of tissue regeneration. However, implantation of scaffolds leads not only to accelerated tissue healing but also to an immune response of the organism, which results in the degradation of the biomaterial. The synergy of the immune response and scaffold degradation processes largely determines the efficiency of tissue regeneration. Still, methods suitable for fast, accurate and non-invasive characterization of the degradation degree of biomaterial are highly demandable. Here we show the possibility of monitoring the degradation of decellularized bovine pericardium scaffolds under conditions mimicking the immune response and oxidation processes using multiphoton tomography combined with fluorescence lifetime imaging (MPT-FLIM). We found that the fluorescence lifetimes of genipin-induced cross-links in collagen and oxidation products of collagen are prominent markers of oxidative degradation of scaffolds. This was verified in model experiments, where the oxidation was induced with hypochlorous acid or by exposure to activated neutrophils. The fluorescence decay parameters also correlated with the changes of micromechanical properties of the scaffolds as assessed using atomic force microscopy (AFM). Our results suggest that FLIM can be used for quantitative assessments of the properties and degradation of the scaffolds essential for the wound healing processes in vivo. |
| first_indexed | 2024-04-13T17:11:09Z |
| format | Article |
| id | doaj.art-da47c04e188c43d08f04a88b90605e19 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-13T17:11:09Z |
| publishDate | 2022-06-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-da47c04e188c43d08f04a88b90605e192022-12-22T02:38:17ZengNature PortfolioScientific Reports2045-23222022-06-0112111210.1038/s41598-022-14138-5Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imagingB. P. Yakimov0I. I. Vlasova1Y. M. Efremov2E. G. Maksimov3E. A. Shirshin4V. E. Kagan5P. S. Timashev6World-Class Research Center “Digital Biodesign and Personalized Healthcare”, Sechenov First Moscow State Medical UniversityWorld-Class Research Center “Digital Biodesign and Personalized Healthcare”, Sechenov First Moscow State Medical UniversityWorld-Class Research Center “Digital Biodesign and Personalized Healthcare”, Sechenov First Moscow State Medical UniversityFaculty of Biology, M.V. Lomonosov Moscow State UniversityWorld-Class Research Center “Digital Biodesign and Personalized Healthcare”, Sechenov First Moscow State Medical UniversityDepartment of Advanced Biomaterials, Institute for Regenerative Medicine, Sechenov First Moscow State Medical UniversityWorld-Class Research Center “Digital Biodesign and Personalized Healthcare”, Sechenov First Moscow State Medical UniversityAbstract Artificial biomaterials can significantly increase the rate of tissue regeneration. However, implantation of scaffolds leads not only to accelerated tissue healing but also to an immune response of the organism, which results in the degradation of the biomaterial. The synergy of the immune response and scaffold degradation processes largely determines the efficiency of tissue regeneration. Still, methods suitable for fast, accurate and non-invasive characterization of the degradation degree of biomaterial are highly demandable. Here we show the possibility of monitoring the degradation of decellularized bovine pericardium scaffolds under conditions mimicking the immune response and oxidation processes using multiphoton tomography combined with fluorescence lifetime imaging (MPT-FLIM). We found that the fluorescence lifetimes of genipin-induced cross-links in collagen and oxidation products of collagen are prominent markers of oxidative degradation of scaffolds. This was verified in model experiments, where the oxidation was induced with hypochlorous acid or by exposure to activated neutrophils. The fluorescence decay parameters also correlated with the changes of micromechanical properties of the scaffolds as assessed using atomic force microscopy (AFM). Our results suggest that FLIM can be used for quantitative assessments of the properties and degradation of the scaffolds essential for the wound healing processes in vivo.https://doi.org/10.1038/s41598-022-14138-5 |
| spellingShingle | B. P. Yakimov I. I. Vlasova Y. M. Efremov E. G. Maksimov E. A. Shirshin V. E. Kagan P. S. Timashev Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imaging Scientific Reports |
| title | Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imaging |
| title_full | Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imaging |
| title_fullStr | Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imaging |
| title_full_unstemmed | Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imaging |
| title_short | Detection of HOCl-driven degradation of the pericardium scaffolds by label-free multiphoton fluorescence lifetime imaging |
| title_sort | detection of hocl driven degradation of the pericardium scaffolds by label free multiphoton fluorescence lifetime imaging |
| url | https://doi.org/10.1038/s41598-022-14138-5 |
| work_keys_str_mv | AT bpyakimov detectionofhocldrivendegradationofthepericardiumscaffoldsbylabelfreemultiphotonfluorescencelifetimeimaging AT iivlasova detectionofhocldrivendegradationofthepericardiumscaffoldsbylabelfreemultiphotonfluorescencelifetimeimaging AT ymefremov detectionofhocldrivendegradationofthepericardiumscaffoldsbylabelfreemultiphotonfluorescencelifetimeimaging AT egmaksimov detectionofhocldrivendegradationofthepericardiumscaffoldsbylabelfreemultiphotonfluorescencelifetimeimaging AT eashirshin detectionofhocldrivendegradationofthepericardiumscaffoldsbylabelfreemultiphotonfluorescencelifetimeimaging AT vekagan detectionofhocldrivendegradationofthepericardiumscaffoldsbylabelfreemultiphotonfluorescencelifetimeimaging AT pstimashev detectionofhocldrivendegradationofthepericardiumscaffoldsbylabelfreemultiphotonfluorescencelifetimeimaging |