Regulation of phagolysosomal digestion by caveolin-1 of the retinal pigment epithelium is essential for vision
Open accessAbstract
Caveolin-1 associates with the endo/lysosomal machinery of cells in culture, suggesting that it functions at these organelles independently of its contribution to cell surface caveolae. Here we explored mice lacking caveolin-1 specifically in the retinal pigment epithelium (RPE). The RPE supports neighboring photoreceptors via diurnal phagocytosis of spent photoreceptor outer segment fragments. Like mice lacking caveolin-1 globally, (RPE)CAV1(-/-) mice developed a normal RPE and neural retina but showed reduced rod photoreceptor light responses, indicating that lack of caveolin-1 affects photoreceptor function in a non-cell-autonomous manner. (RPE)CAV1(-/-) RPE in situ showed normal particle engulfment but delayed phagosome clearance and reversed diurnal profiles of levels and activities of lysosomal enzymes. Therefore, eliminating caveolin-1 specifically impairs phagolysosomal degradation by the RPE in vivo. Endogenous caveolin-1 was recruited to maturing phagolysosomes in RPE cells in culture. Consistent with these in vivo data, a moderate increase (to ∼ 2.5-fold) or decrease (by half) of caveolin-1 protein levels in RPE cells in culture was sufficient to accelerate or impair phagolysosomal digestion, respectively. A mutant form of caveolin-1 that fails to reach the cell surface augmented degradation like wild-type caveolin-1. Acidic lysosomal pH and increased protease activity are essential for digestion. We show that halving caveolin-1 protein levels significantly alkalinized lysosomal pH and decreased lysosomal enzyme activities. Taken together, our results reveal a novel role for intracellular caveolin-1 in modulating phagolysosomal function. Moreover, they show, for the first time, that organellar caveolin-1 significantly affects tissue functionality in vivo.
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Caveolin-1 is recruited to maturing phagolysosomes and appears to be important for regulating lysosomal acidification and cathepsin D enzyme activity; increasing or decreasing caveolin-1 protein levels in vitro accelerated or decelerated phagosome degradation, respectively.
“Additionally, the membrane organizer, caveolin-1, is recruited to maturing phagolysosomes and appears to be important for regulating lysosomal acidification and cathepsin D enzyme activity; increasing or decreasing caveolin-1 protein levels in vitro accelerated or decelerated phagosome degradation, respectively (Sethna et al., 2016), although the underlying mechanism remains unclear.”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Sethna et al., 2016
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Voisin, A., Gaillard, A., Balbous, A., & Leveziel, N. (2022) · Antioxidants · doi:10.3390/antiox11040713 · Cited by 11 · see citing works
Loo, J. H., Wang, Z., & Chong, R. S. (2023) · Frontiers in Medicine · doi:10.3389/fmed.2023.1087123 · Cited by 10 · see citing works
The Role of Caveolin-1 in Retinal Inflammation.
Gurley, J., & Elliott, M. H. (2019) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-27378-1_28 · Cited by 5 · see citing works
Gao, F., Tom, E., Lieffrig, S. A., Finnemann, S. C., & Skowronska‐Krawczyk, D. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1279457 · Cited by 5 · see citing works
Müller, C., & Finnemann, S. C. (2020) · Springer eBooks · doi:10.1007/978-3-030-28384-1_3 · Cited by 6 · see citing works
Ahmed, M. R., Sethna, S., Krueger, L. A., Yang, M. B., & Hufnagel, R. B. (2022) · Genes · doi:10.3390/genes13030411 · Cited by 5 · see citing works
Differences in Diurnal Rhythm of Rod Outer Segment Renewal between 129T2/SvEmsJ and C57BL/6J Mice
Vargas, J. A., & Finnemann, S. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169466 · Cited by 5 · see citing works
The Chx10-Traf3 Knockout Mouse as a Viable Model to Study Neuronal Immune Regulation
Gurley, J. M., Gmyrek, G. B., Hargis, E. A., Bishop, G. A., Carr, D. J. J., & Elliott, M. H. (2021) · Cells · doi:10.3390/cells10082068 · Cited by 3 · see citing works
Redox Regulation of Signaling Complex between Caveolin-1 and Neuronal Calcium Sensor Recoverin
Vladimirov, V. I., Shchannikova, M. P., Baldin, A. V., Kazakov, A. S., Shevelyova, M. P., Nazipova, A. A., Baksheeva, V. E., Леонидовна, Н. Е., Frolova, A. S., Tikhomirova, N. K., et al. (2022) · Biomolecules · doi:10.3390/biom12111698 · Cited by 2 · see citing works
Loss of CIB2 causes non-canonical autophagy deficits and visual impairmentPreprint
Sethna, S., Scott, P. A., Giese, A. P. J., Duncan, T. E., Redmond, T. M., Riazuddin, S., & Ahmed, Z. M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.18.302174 · Cited by 2 · see citing works
Is Caveolin-1 Required for Retinal Neuroprotection?
Bankole, O. O., & Elliott, M. H. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-76550-6_47 · Cited by 1 · see citing works
The photoreceptor outer segment: Development and renewal
Hazim, R. A., Fisher, S. K., & Williams, D. S. (2025) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2025.07.002 · Cited by 1 · see citing works
CIB2 regulates autophagy via Rheb-mTORC1 signaling axisPreprint
Sethna, S., Bernstein, S. L., Jian, X., Riazuddin, S. A., Randazzo, P. A., Riazuddin, S., & Ahmed, Z. M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.18.302265 · Cited by 1 · see citing works
An Unexpected Role for GPR143 in Retinal HomeostasisPreprint
Tung, D., Congrove, N. R., Figueroa, A. G., Bliss, R. M., Zvavamwe, T., & McKay, B. S. (2023) · Preprints.org · doi:10.20944/preprints202301.0094.v1 · Cited by 1 · see citing works
Falcão, A. S., Lopes‐da‐Silva, M., Antas, P., Escrevente, C., Pedro, M., Coelho, R., Ferreira, I. S., Santos, I. P., Ciossek, T., Nicklin, P. L., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.17.613413 · Cited by 1 · see citing works
Sethna, S., Zein, W. M., Riaz, S., Giese, A. P. J., Schultz, J. M., Duncan, T. E., Hufnagel, R. B., Brewer, C. C., Griffith, A. J., Redmond, T. M., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.08.447565
A novel quantification method for RPE phagocytosis using a VLC-PUFA-based strategyPreprint
Gao, F., Tom, E., Lieffrig, S. A., Finnemann, S. C., & Skowronska‐Krawczyk, D. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.02.498584
Müller, C., & Finnemann, S. C. (2024) · Springer eBooks · doi:10.1007/978-3-031-35055-9_3
Photoreceptor Outer Segment Renewal
Hazim, R. A., Paniagua, A. E., & Williams, D. S. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-13820-1.00182-1
Falcão, A. S., Lopes‐da‐Silva, M., Antas, P., Escrevente, C., Pedro, M., Felgueiras, B., Caires, B., Coelho, R., Ferreira, I. S., Santos, I. P., et al. (2026) · Experimental Eye Research · doi:10.1016/j.exer.2026.111215 · Cited by 1 · see citing works
The functional anatomy of caveolae across cell types
Rusu, M. C., Zamfir, I. Ş., Varga, I., & Vintilă, B. (2026) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2026.107053
- Authors
- Sethna, S., Chamakkala, T., Gu, X., Thompson, T. C., Cao, G., Elliott, M. H., & Finnemann, S. C.
- Affiliations
- Fordham University (US)
- University of Oklahoma Health Sciences Center (US)
- The University of Texas MD Anderson Cancer Center (US)
- Corresponding author
- Elliott, Michael H.
- Finnemann, Silvia C.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 291
- Issue
- 12
- Pages
- 6494-6506
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC4813570
- OpenAlex
- W2291294034
- Cited by
- 53
- References
- 55
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 8 · 2022: 9 · 2021: 6 · 2020: 12 · 2019: 3 · 2018: 4 · 2017: 2 · 2016: 1
- FWCI
- 2.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Eye Institute (R01EY013295, R01EY019494, P30EY021725)
- Research to Prevent Blindness
- Fordham University (GSAS Alumni Dissertation Fellowship)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- caveolin-1, retinal pigment epithelium, photoreceptor outer segment phagocytosis, lysosomal pH, lysosomal enzyme activity, rod photoreceptor function, caveolin-1 knockout mice
- MeSH terms
- Animals, Cathepsin D, Cell Line, Circadian Rhythm, Lysosomes, Mice, Inbred C57BL, Phagocytosis, Phagosomes, Receptors, Transferrin, Vision, Ocular, Retinal Rod Photoreceptor Cells, Mice, Knockout, Protein Transport, Sus scrofa, Caveolin 1, Rats, Retinal Pigment Epithelium, Proteolysis
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