Macrophage-driven biomaterial degradation depends on scaffold microarchitecture

Tamar B. Wissing, Valentina Bonito, Eline E. van Haaften, Marina van Doeselaar, Marieke M.C.P. Brugmans, Henk M. Janssen, Carlijn V.C. Bouten, Anthal I.P.M. Smits (Corresponding author)

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Abstract

In situ tissue engineering is a technology in which non-cellular biomaterial scaffolds are implanted in order to induce local regeneration of replaced or damaged tissues. Degradable synthetic electrospun scaffolds are a versatile and promising class of biomaterials for various in situ tissue engineering applications, such as cardiovascular replacements. Functional in situ tissue regeneration depends on the balance between endogenous neo-tissue formation and scaffold degradation. Both these processes are driven by macrophages. Upon invasion into a scaffold, macrophages secrete reactive oxygen species (ROS) and hydrolytic enzymes, contributing to oxidative and enzymatic biomaterial degradation, respectively. This study aims to elucidate the effect of scaffold microarchitecture, i.e., μm-range fiber diameter and fiber alignment, on early macrophage-driven scaffold degradation. Electrospun poly-ε-caprolactone-bisurea (PCL-BU) scaffolds with either 2 or 6 μm (Ø) isotropic or anisotropic fibers were seeded with THP-1 derived human macrophages and cultured in vitro for 4 or 8 days. Our results revealed that macroph age-induced oxidative degradation in particular was dependent on scaffold microarchitecture, with the highest level of ROS-induced lipid peroxidation, NADPH oxidase gene expression and degradation in the 6 μm Ø anisotropic group. Whereas, biochemically polarized macrophages demonstrated a phenotype-specific degradative potential, the observed differences in macrophage degradative potential instigated by the scaffold microarchitecture could not be attributed to either distinct M1 or M2 polarization. This suggests that the scaffold microarchitecture uniquely affects macrophage-driven degradation. These findings emphasize the importance of considering the scaffold microarchitecture in the design of scaffolds for in situ tissue engineering applications and the tailoring of degradation kinetics thereof.

Original languageEnglish
Article number87
Number of pages20
JournalFrontiers in Bioengineering and Biotechnology
Volume7
Issue numberAPR
DOIs
Publication statusPublished - 26 Apr 2019

Fingerprint

Macrophages
Biocompatible Materials
Scaffolds (biology)
Biomaterials
Scaffolds
Degradation
Tissue Engineering
Tissue engineering
Fibers
Regeneration
Reactive Oxygen Species
Tissue
Tissue Scaffolds
Tissue regeneration
Oxygen
NADPH Oxidase
Gene expression
Lipids
Lipid Peroxidation
Enzymes

Keywords

  • Electrospinning
  • Enzymatic degradation
  • Foreign body response (FBR)
  • Immunomodulation
  • In situ tissue engineering
  • Macrophage polarization.
  • Oxidative degradation
  • Reactive Oxygen Species
  • immunomodulation
  • in situ tissue engineering
  • oxidative degradation
  • macrophage polarization
  • enzymatic degradation
  • electrospinning
  • reactive oxygen species
  • foreign body response

Cite this

@article{a43ddde0646c4347826cdee3fce17194,
title = "Macrophage-driven biomaterial degradation depends on scaffold microarchitecture",
abstract = "In situ tissue engineering is a technology in which non-cellular biomaterial scaffolds are implanted in order to induce local regeneration of replaced or damaged tissues. Degradable synthetic electrospun scaffolds are a versatile and promising class of biomaterials for various in situ tissue engineering applications, such as cardiovascular replacements. Functional in situ tissue regeneration depends on the balance between endogenous neo-tissue formation and scaffold degradation. Both these processes are driven by macrophages. Upon invasion into a scaffold, macrophages secrete reactive oxygen species (ROS) and hydrolytic enzymes, contributing to oxidative and enzymatic biomaterial degradation, respectively. This study aims to elucidate the effect of scaffold microarchitecture, i.e., μm-range fiber diameter and fiber alignment, on early macrophage-driven scaffold degradation. Electrospun poly-ε-caprolactone-bisurea (PCL-BU) scaffolds with either 2 or 6 μm ({\O}) isotropic or anisotropic fibers were seeded with THP-1 derived human macrophages and cultured in vitro for 4 or 8 days. Our results revealed that macroph age-induced oxidative degradation in particular was dependent on scaffold microarchitecture, with the highest level of ROS-induced lipid peroxidation, NADPH oxidase gene expression and degradation in the 6 μm {\O} anisotropic group. Whereas, biochemically polarized macrophages demonstrated a phenotype-specific degradative potential, the observed differences in macrophage degradative potential instigated by the scaffold microarchitecture could not be attributed to either distinct M1 or M2 polarization. This suggests that the scaffold microarchitecture uniquely affects macrophage-driven degradation. These findings emphasize the importance of considering the scaffold microarchitecture in the design of scaffolds for in situ tissue engineering applications and the tailoring of degradation kinetics thereof.",
keywords = "Electrospinning, Enzymatic degradation, Foreign body response (FBR), Immunomodulation, In situ tissue engineering, Macrophage polarization., Oxidative degradation, Reactive Oxygen Species, immunomodulation, in situ tissue engineering, oxidative degradation, macrophage polarization, enzymatic degradation, electrospinning, reactive oxygen species, foreign body response",
author = "Wissing, {Tamar B.} and Valentina Bonito and {van Haaften}, {Eline E.} and {van Doeselaar}, Marina and Brugmans, {Marieke M.C.P.} and Janssen, {Henk M.} and Bouten, {Carlijn V.C.} and Smits, {Anthal I.P.M.}",
year = "2019",
month = "4",
day = "26",
doi = "10.3389/fbioe.2019.00087",
language = "English",
volume = "7",
journal = "Frontiers in Bioengineering and Biotechnology",
issn = "2296-4185",
publisher = "Frontiers Research Foundation",
number = "APR",

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TY - JOUR

T1 - Macrophage-driven biomaterial degradation depends on scaffold microarchitecture

AU - Wissing, Tamar B.

AU - Bonito, Valentina

AU - van Haaften, Eline E.

AU - van Doeselaar, Marina

AU - Brugmans, Marieke M.C.P.

AU - Janssen, Henk M.

AU - Bouten, Carlijn V.C.

AU - Smits, Anthal I.P.M.

PY - 2019/4/26

Y1 - 2019/4/26

N2 - In situ tissue engineering is a technology in which non-cellular biomaterial scaffolds are implanted in order to induce local regeneration of replaced or damaged tissues. Degradable synthetic electrospun scaffolds are a versatile and promising class of biomaterials for various in situ tissue engineering applications, such as cardiovascular replacements. Functional in situ tissue regeneration depends on the balance between endogenous neo-tissue formation and scaffold degradation. Both these processes are driven by macrophages. Upon invasion into a scaffold, macrophages secrete reactive oxygen species (ROS) and hydrolytic enzymes, contributing to oxidative and enzymatic biomaterial degradation, respectively. This study aims to elucidate the effect of scaffold microarchitecture, i.e., μm-range fiber diameter and fiber alignment, on early macrophage-driven scaffold degradation. Electrospun poly-ε-caprolactone-bisurea (PCL-BU) scaffolds with either 2 or 6 μm (Ø) isotropic or anisotropic fibers were seeded with THP-1 derived human macrophages and cultured in vitro for 4 or 8 days. Our results revealed that macroph age-induced oxidative degradation in particular was dependent on scaffold microarchitecture, with the highest level of ROS-induced lipid peroxidation, NADPH oxidase gene expression and degradation in the 6 μm Ø anisotropic group. Whereas, biochemically polarized macrophages demonstrated a phenotype-specific degradative potential, the observed differences in macrophage degradative potential instigated by the scaffold microarchitecture could not be attributed to either distinct M1 or M2 polarization. This suggests that the scaffold microarchitecture uniquely affects macrophage-driven degradation. These findings emphasize the importance of considering the scaffold microarchitecture in the design of scaffolds for in situ tissue engineering applications and the tailoring of degradation kinetics thereof.

AB - In situ tissue engineering is a technology in which non-cellular biomaterial scaffolds are implanted in order to induce local regeneration of replaced or damaged tissues. Degradable synthetic electrospun scaffolds are a versatile and promising class of biomaterials for various in situ tissue engineering applications, such as cardiovascular replacements. Functional in situ tissue regeneration depends on the balance between endogenous neo-tissue formation and scaffold degradation. Both these processes are driven by macrophages. Upon invasion into a scaffold, macrophages secrete reactive oxygen species (ROS) and hydrolytic enzymes, contributing to oxidative and enzymatic biomaterial degradation, respectively. This study aims to elucidate the effect of scaffold microarchitecture, i.e., μm-range fiber diameter and fiber alignment, on early macrophage-driven scaffold degradation. Electrospun poly-ε-caprolactone-bisurea (PCL-BU) scaffolds with either 2 or 6 μm (Ø) isotropic or anisotropic fibers were seeded with THP-1 derived human macrophages and cultured in vitro for 4 or 8 days. Our results revealed that macroph age-induced oxidative degradation in particular was dependent on scaffold microarchitecture, with the highest level of ROS-induced lipid peroxidation, NADPH oxidase gene expression and degradation in the 6 μm Ø anisotropic group. Whereas, biochemically polarized macrophages demonstrated a phenotype-specific degradative potential, the observed differences in macrophage degradative potential instigated by the scaffold microarchitecture could not be attributed to either distinct M1 or M2 polarization. This suggests that the scaffold microarchitecture uniquely affects macrophage-driven degradation. These findings emphasize the importance of considering the scaffold microarchitecture in the design of scaffolds for in situ tissue engineering applications and the tailoring of degradation kinetics thereof.

KW - Electrospinning

KW - Enzymatic degradation

KW - Foreign body response (FBR)

KW - Immunomodulation

KW - In situ tissue engineering

KW - Macrophage polarization.

KW - Oxidative degradation

KW - Reactive Oxygen Species

KW - immunomodulation

KW - in situ tissue engineering

KW - oxidative degradation

KW - macrophage polarization

KW - enzymatic degradation

KW - electrospinning

KW - reactive oxygen species

KW - foreign body response

UR - http://www.scopus.com/inward/record.url?scp=85064634020&partnerID=8YFLogxK

U2 - 10.3389/fbioe.2019.00087

DO - 10.3389/fbioe.2019.00087

M3 - Article

C2 - 31080796

VL - 7

JO - Frontiers in Bioengineering and Biotechnology

JF - Frontiers in Bioengineering and Biotechnology

SN - 2296-4185

IS - APR

M1 - 87

ER -