Severing corneal nerves in one eye induces sympathetic loss of immune privilege and promotes rejection of future corneal allografts placed in either eye

Am J Transplant. 2015 Jun;15(6):1490-501. doi: 10.1111/ajt.13240. Epub 2015 Apr 14.

Abstract

Less than 10% of corneal allografts undergo rejection even though HLA matching is not performed. However, second corneal transplants experience a threefold increase in rejection, which is not due to prior sensitization to histocompatibility antigens shared by the first and second transplants since corneal grafts are selected at random without histocompatibility matching. Using a mouse model of penetrating keratoplasty, we found that 50% of the initial corneal transplants survived, yet 100% of the subsequent corneal allografts (unrelated to the first graft) placed in the opposite eye underwent rejection. The severing of corneal nerves that occurs during surgery induced substance P (SP) secretion in both eyes, which disabled T regulatory cells that are required for allograft survival. Administration of an SP antagonist restored immune privilege and promoted graft survival. Thus, corneal surgery produces a sympathetic response that permanently abolishes immune privilege of subsequent corneal allografts, even those placed in the opposite eye and expressing a completely different array of foreign histocompatibility antigens from the first corneal graft.

Keywords: Basic (laboratory) research/science; corneal transplantation/ophthalmology; immune regulation; rejection; tolerance: experimental.

Publication types

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

MeSH terms

  • Allografts
  • Animals
  • Cornea / innervation*
  • Corneal Transplantation*
  • Denervation / methods*
  • Female
  • Graft Rejection / immunology*
  • Graft Rejection / physiopathology
  • Graft Survival / immunology
  • Graft Survival / physiology
  • Histocompatibility Antigens / immunology
  • Immune Tolerance / drug effects
  • Immune Tolerance / immunology*
  • Immune Tolerance / physiology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Models, Animal
  • Sensory Receptor Cells*
  • Substance P / antagonists & inhibitors
  • Substance P / pharmacology
  • Substance P / physiology
  • T-Lymphocytes, Regulatory / physiology

Substances

  • Histocompatibility Antigens
  • Substance P