Immune privilege in the eye: an evolutionary adaptation

The purpose of this study was to determine whether immune privilege exists in the eye of goldfish and to explore from an evolutionary point of view the relationship between the immunological and neurobiological microenvironments in the eye. Neural retinal or scale allografts and autografts were implanted into the vitreous cavity or the anterior chamber of goldfish eyes. Histological examinations were conducted to determine the fate of these grafts. In order to detect donor-specific immune suppression induced by intraocular retinal allografts, scale allografts obtained from the same donors were subsequently implanted orthotopically and evaluated. Neural retinal allografts implanted intraocularly were rapidly rejected by postimplantation day 8. In contrast, neural retinal autografts survived well within the eye with no inflammation. Prior intraocular allografts, either scale or retinal grafts, did not prevent rejection of subsequent scale allografts nor did they induce down-regulation of systemic immunity. Thus, immune privilege does not exist in the goldfish eye, implying that immune privilege in the eye (or central nervous system) may be an evolutionary adaptation acquired by higher vertebrates. Considering that the capacity for neural regeneration in the central nervous system diminishes during evolution, the hypothesis that immune privilege and neural regeneration may be mutually exclusive properties is addressed.