Activating Macrophage Continual Efferocytosis via Microenvironment Biomimetic Short Fibers for Reversing Inflammation in Bone Repair

Adv Mater. 2024 Jul;36(30):e2402968. doi: 10.1002/adma.202402968. Epub 2024 May 14.

Abstract

Efferocytosis-mediated inflammatory reversal plays a crucial role in bone repairing process. However, in refractory bone defects, the macrophage continual efferocytosis may be suppressed due to the disrupted microenvironment homeostasis, particularly the loss of apoptotic signals and overactivation of intracellular oxidative stress. In this study, a polydopamine-coated short fiber matrix containing biomimetic "apoptotic signals" to reconstruct the microenvironment and reactivate macrophage continual efferocytosis for inflammatory reversal and bone defect repair is presented. The "apoptotic signals" (AM/CeO2) are prepared using CeO2 nanoenzymes with apoptotic neutrophil membrane coating for macrophage recognition and oxidative stress regulation. Additionally, a short fiber "biomimetic matrix" is utilized for loading AM/CeO2 signals via abundant adhesion sites involving π-π stacking and hydrogen bonding interactions. Ultimately, the implantable apoptosis-mimetic nanoenzyme/short-fiber matrixes (PFS@AM/CeO2), integrating apoptotic signals and biomimetic matrixes, are constructed to facilitate inflammatory reversal and reestablish the pro-efferocytosis microenvironment. In vitro and in vivo data indicate that the microenvironment biomimetic short fibers can activate macrophage continual efferocytosis, leading to the suppression of overactivated inflammation. The enhanced repair of rat femoral defect further demonstrates the osteogenic potential of the pro-efferocytosis strategy. It is believed that the regulation of macrophage efferocytosis through microenvironment biomimetic materials can provide a new perspective for tissue repair.

Keywords: biomimetic nanoenzymes; bone repair; efferocytosis; inflammation; short fibers.

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Biomimetic Materials* / chemistry
  • Biomimetic Materials* / pharmacology
  • Biomimetics / methods
  • Bone Regeneration / drug effects
  • Cellular Microenvironment / drug effects
  • Cerium* / chemistry
  • Cerium* / pharmacology
  • Efferocytosis
  • Indoles / chemistry
  • Indoles / pharmacology
  • Inflammation* / drug therapy
  • Macrophage Activation / drug effects
  • Macrophages* / drug effects
  • Macrophages* / metabolism
  • Mice
  • Osteogenesis / drug effects
  • Oxidative Stress / drug effects
  • Phagocytosis / drug effects
  • Polymers* / chemistry
  • Polymers* / pharmacology
  • RAW 264.7 Cells
  • Rats

Substances

  • Cerium
  • polydopamine
  • Polymers
  • ceric oxide
  • Indoles