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Scavenger Function of Resident Autofluorescent Perivascular Macrophages and Their Contribution to the Maintenance of the Blood–Retinal Barrier

From the ¹Interdisciplinary Center of Research in Animal Health (CIISA), Faculty of Veterinary Medicine, Universidade Técnica de Lisboa, Lisbon, Portugal; the ²Center of Animal Biotechnology and Gene Therapy, and Departments of ³Animal Health and Anatomy and ⁷Biochemistry and Molecular Biology, School of Veterinary Medicine, Universitat Autònoma de Barcelona, Bellaterra, Spain; ⁴CIBER de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Barcelona, Spain; the ⁵Faculty of Medical Sciences, Universidade Nova de Lisboa, Lisbon, Portugal; and the ⁶Faculty of Medicine, Universitat Autònoma de Barcelona, Bellaterra, Spain.

Corresponding author: Jesús Ruberte, Center of Animal Biotechnology and Gene Therapy (CBATEG), Edifici H, Campus UAB, Bellaterra 08193, Barcelona, Spain; jesus.ruberte{at}uab.es.

Purpose. The retina contains two distinct populations of monocyte-derived cells: perivascular macrophages, and microglia. The present study was undertaken to evaluate the presence and function in mouse and human retinas of a subtype of resident perivascular macrophages with scavenger function, different from microglia, in physiological conditions and during retinopathy.

Methods. Perivascular macrophages were characterized by means of confocal microscopy, electron microscopy, and flow cytometry analyses. Two murine models of blood–retinal barrier breakdown and photoreceptor degeneration were used to analyze the role of these macrophages during retinopathy.

Results. The macrophages analyzed constituted a small population of resident perivascular cells different from microglia, since they were Iba-1 negative. Although these cells expressed F4/80 and CD11b antigens in common with microglia, they also expressed BM8 and MOMA-2 epitopes, which are macrophagic markers not expressed by microglia. Perivascular macrophages emitted autofluorescence due to cytoplasmic inclusions containing protein-bound oxidized lipids. They constitutively expressed the scavenger receptor class A and moved along blood vessels, providing an additional coating to thinner areas of the basement membrane. Moreover, they accumulated blood-borne horseradish peroxidase and acetylated low-density lipoprotein in healthy retinas. In addition, during blood–retinal barrier breakdown and photoreceptor degeneration, these cells migrated to the lesion site.

Conclusions. All these morphologic and functional features are consistent with those described for brain Mato cells. Thus, this study showed the presence of autofluorescent perivascular macrophages, different from microglia, with a scavenger function that may contribute to the maintenance of the blood–retinal barrier in healthy conditions and that are also involved in retinopathy.