Polyethylene glycol-fusion repair of sciatic allografts in female rats achieves immunotolerance via attenuated innate and adaptive responses

J Neurosci Res. 2020 Dec;98(12):2468-2495. doi: 10.1002/jnr.24720. Epub 2020 Sep 15.

Abstract

Ablation/segmental loss peripheral nerve injuries (PNIs) exhibit poor functional recovery due to slow and inaccurate outgrowth of regenerating axons. Viable peripheral nerve allografts (PNAs) as growth-guide conduits are immunologically rejected and all anucleated donor/host axonal segments undergo Wallerian degeneration. In contrast, we report that ablation-type sciatic PNIs repaired by neurorrhaphy of viable sciatic PNAs and a polyethylene glycol (PEG)-fusion protocol using PEG immediately restored axonal continuity for many axons, reinnervated/maintained their neuromuscular junctions, and prevented much Wallerian degeneration. PEG-fused PNAs permanently restored many sciatic-mediated behaviors within 2-6 weeks. PEG-fused PNAs were not rejected even though host/donors were neither immunosuppressed nor tissue-matched in outbred female Sprague Dawley rats. Innate and adaptive immune responses to PEG-fused sciatic PNAs were analyzed using electron microscopy, immunohistochemistry, and quantitative reverse transcription polymerase chain reaction for morphological features, T cell and macrophage infiltration, major histocompatibility complex (MHC) expression, apoptosis, expression of cytokines, chemokines, and cytotoxic effectors. PEG-fused PNAs exhibited attenuated innate and adaptive immune responses by 14-21 days postoperatively, as evidenced by (a) many axons and cells remaining viable, (b) significantly reduced infiltration of cytotoxic and total T cells and macrophages, (c) significantly reduced expression of inflammatory cytokines, chemokines, and MHC proteins, (d) consistently low apoptotic response. Morphologically and/or biochemically, PEG-fused sciatic PNAs often resembled sciatic autografts or intact sciatic nerves. In brief, PEG-fused PNAs are an unstudied, perhaps unique, example of immune tolerance of viable allograft tissue in a nonimmune-privileged environment and could greatly improve the clinical outcomes for PNIs relative to current protocols.

Keywords: RRID:AB_10917271; RRID:AB_1141521; RRID:AB_1210523; RRID:AB_2315387; RRID:AB_2341188; RRID:AB_2556545; RRID:AB_2556548; RRID:AB_306429; RRID:AB_531793; RRID:AB_566872; RRID:AB_567369; RRID:AB_791151; RRID:RGD_737903; RRID:SCR_001620; RRID:SCR_002285; RRID:SCR_002760; RRID:SCR_002798; RRID:SCR_003070; RRID:SCR_016517; Schwann cell; T cell; Wallerian degeneration; allograft rejection; axotomy; chemokines; cytokines; immune response; macrophage; nerve repair; polyethylene glycol; transplantation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptive Immunity / drug effects
  • Adaptive Immunity / physiology*
  • Allografts / immunology
  • Allografts / transplantation
  • Animals
  • Female
  • Immunity, Innate / drug effects
  • Immunity, Innate / physiology*
  • Male
  • Polyethylene Glycols / administration & dosage*
  • Rats
  • Rats, Sprague-Dawley
  • Sciatic Nerve / immunology*
  • Sciatic Nerve / transplantation*
  • Sciatic Neuropathy / immunology
  • Sciatic Neuropathy / therapy*
  • Transplantation, Homologous / methods

Substances

  • Polyethylene Glycols