Thrombospondin Plays a Vital Role in the Immune Privilege of the Eye
Abstract
PURPOSE: The role of thrombospondin (TSP)-1 in TGF-beta activation and T-cell suppression was studied in the retinal pigment epithelial (RPE) cells, a monolayer of pigmented cells that line the subretinal space, an immune-privileged site in the eye. METHODS: Posterior eyecups were prepared by excising the anterior segment, lens, and retina from enucleated eyes of C57BL/6, thrombospondin-1 knockout (TSP-1KO), and TGF-beta2 receptor II double-negative (TGF-beta2 RII DN) mice, leaving behind a healthy monolayer of RPE resting on choroid and sclera. Serum-free medium was added to these RPE eyecups, and, after various time intervals, supernatants (SNs) were removed and tested. RESULTS: SNs of an ex vivo culture of RPE cells from C57BL/6 mice were shown to inhibit both antigen and anti-CD3 activation of T cells, partially due to constitutive production of TGF-beta and to the ability of RPE to activate the latent form of TGF-beta. Activation of TGF-beta was entirely dependent on TSP-1, also produced by RPE. SNs of RPE from TSP-1KO mice failed to inhibit T-cell activation. Ovalbumin (OVA)-specific delayed hypersensitivity (DH) was not impaired when OVA was injected either into the subretinal space or into the anterior chamber of TSP-1KO mice before OVA immunization. Moreover, experimental autoimmune uveoretinitis was significantly more intense in eyes of TSP-1KO mice and failed to undergo spontaneous resolution unlike wild-type mice. CONCLUSIONS: Production of both TSP-1 and active TGF-beta by RPE is essential to the creation and maintenance of immune privilege in the subretinal space and that the immune privilege limits the severity and duration of retinal inflammation due to autoimmunity.
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Active local or peripheral tolerance can be induced through conversion of T cells to regulatory T cells or apoptosis of infiltrated effector T cells by inhibitory molecules expressed on the retinal pigmented epithelium or resident stromal cells.
“An active local or peripheral tolerance to prevent runaway immune responses can be induced in some cases through the conversion of T cell to regulatory T cells (Treg) or the apoptosis of infiltrated effector T cells by inhibitory molecules expressed on the retinal pigmented epithelium (RPE) or resident stromal cells [9][10][11].”
From Risk mitigation of immunogenicity: a key to personalized retinal gene therapy (2021) · cites this paper as [9]
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Dwivedi, V. P., Tousif, S., Bhattacharya, D., Prasad, D. V. R., Kaer, L. V., Das, J., & Das, G. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.c111.327627 · Cited by 15 · see citing works
The retinal pigment epithelium (RPE) induces FasL and reduces iNOS and Cox2 in primary monocytes
Hettich, C., Wilker, S., Mentlein, R., Lucius, R., Roider, J. B., & Klettner, A. (2014) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-014-2742-z · Cited by 14 · see citing works
Thrombospondin-2 as a Potential Risk Factor in a General Population
Morikawa, N., Adachi, H., Enomoto, M., Fukami, A., Kumagai, E., Nakamura, S., Nohara, Y., Nakao, E., Kono, S., Tsuru, T., et al. (2019) · International Heart Journal · doi:10.1536/ihj.18-246 · Cited by 14 · see citing works
- Authors
- Zamiri, P., Masli, S., Kitaichi, N., Taylor, A. W., & Streilein, J. W.
- Affiliations
- Harvard University (US)
- Venue
- Investigative Opthalmology & Visual Science
- Published
- 2005-03-01
- Volume
- 46
- Issue
- 3
- Pages
- 908
- ISSN
- 0146-0404 (ISSN-L)
- 1552-5783
- OpenAlex
- W4240952760
- Cited by
- 143
- References
- 0
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 3 · 2023: 6 · 2022: 2 · 2021: 11 · 2020: 6 · 2019: 7 · 2018: 9 · 2017: 6 · 2016: 5 · 2015: 9 · 2014: 6 · 2013: 7 · 2012: 8
- FWCI
- 5.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Investigative Ophthalmology & Visual Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ey009595-13)
- National Eye Institute (EY-09595, EY10752, EY 05678)
- Topics
- Health Sciences › Medicine › Ophthalmology › Ocular Diseases and Behçet’s Syndrome
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- thrombospondin-1, immune privilege, retinal pigment epithelium, TGF-beta activation, T cell suppression, experimental autoimmune uveoretinitis, delayed-type hypersensitivity, ovalbumin, retinal autoimmunity, subretinal space, choroid
- MeSH terms
- Animals, Autoimmune Diseases, Enzyme-Linked Immunosorbent Assay, Immune System, Interferon-gamma, Lymphocyte Activation, Male, Mice, Inbred C57BL, Pigment Epithelium of Eye, Retinitis, T-Lymphocytes, Uveitis, Transforming Growth Factor beta, Mice, Knockout, Thrombospondin 1, Reverse Transcriptase Polymerase Chain Reaction, Mice, Transforming Growth Factor beta2
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