The contribution of melanoregulin to microtubule-associated protein 1 light chain 3 (LC3) associated phagocytosis in retinal pigment epithelium
Open accessAbstract
A main requisite in the phagocytosis of ingested material is a coordinated series of maturation steps which lead to the degradation of ingested cargo. Photoreceptor outer segment (POS) renewal involves phagocytosis of the distal disk membranes by the retinal pigment epithelium (RPE). Previously, we identified melanoregulin (MREG) as an intracellular cargo-sorting protein required for the degradation of POS disks. Here, we provide evidence that MREG-dependent processing links both autophagic and phagocytic processes in LC3-associated phagocytosis (LAP). Ingested POS phagosomes are associated with endogenous LC3 and MREG. The LC3 association with POSs exhibited properties of LAP; it was independent of rapamycin pretreatment, but dependent on Atg5. Loss of MREG resulted in a decrease in the extent of LC3-POS association. Studies using DQ-BSA suggest that loss of MREG does not compromise the association and fusion of LC3-positive phagosomes with lysosomes. Furthermore, the mechanism of MREG action is likely through a protein complex that includes LC3, as determined by colocalization and immunoprecipitation in both RPE cells and macrophages. We posit that MREG participates in coordinating the association of phagosomes with LC3 for content degradation with the loss of MREG leading to phagosome accumulation.
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Following ingestion of OS membrane by the RPE, LC3B-II, its conjugation factor ATG5, and the LC3 adaptor MREG are all found on a subpopulation of OS phagosomes within 15 min of ingestion.
“Following the ingestion of OS membrane by the RPE, LC3B-II, its conjugation factor, ATG5, as well as the LC3 adaptor melanoregulin (MREG), are all found on a subpopulation of OS phagosomes within 15 min of ingestion (Kim et al., 2013; Frost et al., 2015).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Frost et al., 2015
In vitro and in vivo studies suggest that approximately 30-45% of ingested phagosomes are LC3B-positive.
“While LC3B-II-opsin association is clearly observed (Fig. 10), the extent of LC3B-II association with opsin-positive phagosomes remains unclear; in vitro (Frost et al., 2015) and in vivo (Dhingra et al., 2018) studies suggest that ~30–45% of ingested phagosomes are LC3B-positive.”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Frost et al., 2015
A portion of OS phagosomes in the RPE recruit microtubule-associated protein 1 light chain 3 (LC3) in a process known as LC3-associated phagocytosis (LAP).
“In addition to the phagocytic machinery discussed in the preceding section, a portion of OS phagosomes in the RPE recruit microtubule-associated protein 1 light chain 3 (LC3) in a process known as LC3-associated phagocytosis (LAP) (Kim et al., 2013; Frost et al., 2015).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Frost et al., 2015
LAP is an autophagosome-independent process and does not require the upstream components needed for initiating or regulating classical autophagy.
“LAP is an autophagosome-independent process (Frost et al., 2015; Martinez et al., 2015; Klionsky et al., 2016), and does not require the upstream components needed for initiating or regulating classical autophagy.”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Frost et al., 2015
LC3B-II recruitment occurs on single-membraned phagosomes, unlike the double-membraned autophagosomes in classical autophagy.
“In addition, LC3B-II recruitment occurs on single-membraned phagosomes, unlike the double-membraned autophagosomes in classical autophagy (Frost et al., 2015; Martinez et al., 2015; Klionsky et al., 2016).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Frost et al., 2015
In 6-month-old C57BL/6J mice RPE, the phagocytic peak occurs 30 min after light onset with a subsequent peak in LC3B-II and ATG5-ATG12 expression 2 h after light onset.
“Based on current knowledge, it appears that there are two peaks of autophagy induction in response to OS membrane phagocytosis: in 6-month-old C57BL/6J mice RPE, the phagocytic peak occurs 30 min after light onset with a subsequent peak in LC3B-II and ATG5-ATG12 expression 2 h after light onset (Frost et al., 2015).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Frost et al., 2015
A portion of POS phagosomes becomes decorated by LC3 and converges on the autophagic pathway.
“Recent studies have shown that a portion of POS phagosomes becomes decorated by LC3 and converges on the autophagic pathway (Kim et al., 2013; Frost et al., 2014), suggesting the possibility of comparable regulation for some of the POS phagosomes.”
From Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis (2015) · cites this paper as Frost et al., 2014
The RPE relies on LC3 family proteins for phagocytic clearance of ingested OS.
“These cells rely on Microtubule-Associated Protein 1 Light Chain 3 (LC3) family of proteins for phagocytic clearance of the ingested OS.”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
The RPE relies on LC3 for LAP-mediated degradation of OS.
“and (2) a hybrid autophagy-phagocytosis degradative pathway termed LC3-associated phagocytosis (LAP) for degradation of OS (Kim et al., 2013; Frost et al., 2015; Martinez et al., 2015).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
The RPE has adapted LAP to eliminate stressors, including daily ingestion of lipids and proteins in OS tips.
“The RPE has adapted LAP to eliminate stressors, including the daily ingestion of lipids and proteins in the form of OS tips (Kim et al., 2013; Frost et al., 2015; Reyes-Reveles et al., 2017).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
LAP plays a critical role in visual pigment regeneration and phagosome degradation.
“LAP plays a critical role in visual pigment regeneration and phagosome degradation (Kim et al., 2013; Frost et al., 2015; Muniz-Feliciano et al., 2017)”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
The daily burst of OS phagocytosis is accompanied by an increase in LC3, levels of which fluctuate over the 12 h light/dark cycle.
“The daily burst of OS phagocytosis is accompanied by an increase in LC3, levels of which fluctuate over the 12 h light/dark cycle (Yao et al., 2014; Frost et al., 2015).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
Upon light onset, LAP-dependent pathways predominate, consistent with high MREG-LC3B levels at this time.
“we predict that upon light onset LAP-dependent pathways predominate, consistent with high MREG-LC3B levels at this time (Frost et al., 2015).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
LAP requires the LC3B adapter melanoregulin (MREG) to mediate LC3B association with newly ingested OS-phagosomes.
“This process requires the LC3B adapter, melanoregulin (MREG) to mediate LC3B association with newly ingested OS-phagosomes (Frost et al., 2015).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
There is a second LC3 peak 6 h after light onset.
“there is a second LC3 peak 6 h after light onset (Yao et al., 2014; Frost et al., 2015).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Frost et al., 2015
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Self-citation
- Authors
- Frost, L. S., Lopes, V. S., Bragin, A., Reyes-Reveles, J., Brancato, J., Cohen, A., Mitchell, C. H., Williams, D. S., & Boesze-Battaglia, K.
- Affiliations
- University of Pennsylvania (US)
- University of California, Los Angeles (US)
- Venue
- Molecular Neurobiology
- Published
- 2014-10-10
- Volume
- 52
- Issue
- 3
- Pages
- 1135-1151
- ISSN
- 0893-7648 (ISSN-L)
- 1559-1182
- PMC
- PMC5531606
- OpenAlex
- W2330533782
- Cited by
- 63
- References
- 60
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 5 · 2023: 9 · 2022: 3 · 2021: 7 · 2020: 14 · 2019: 3 · 2018: 6 · 2017: 3 · 2016: 5 · 2015: 2
- FWCI
- 2.52
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Molecular Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- ScholarlyCommons (University of Pennsylvania) (submittedVersion)
- Scholarly Commons (University of Pennsylvania) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Eye Institute (EY001583, R01EY013434, R01EY010420, P30-EY00331, R01 EY07042, R21EY018705, R01EY007042, P30EY001583, P30EY000331)
- National Institute of Dental and Craniofacial Research (R01DE022465)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- LC3-associated phagocytosis, retinal pigment epithelium, photoreceptor outer segment phagocytosis, autophagy, phagosome-lysosome fusion, ATG5, cargo sorting, macrophages
- MeSH terms
- Autophagy-Related Protein 5, Animals, Autophagy, Carrier Proteins, Cattle, Circadian Rhythm, Eye Proteins, Humans, Macrophages, Mice, Inbred C57BL, Mice, Mutant Strains, Microtubule-Associated Proteins, Phagocytosis, Phagosomes, Sirolimus, Protein Transport, Adaptor Proteins, Vesicular Transport, Multiprotein Complexes, Intracellular Signaling Peptides and Proteins, Mice, Retinal Pigment Epithelium, Retinal Photoreceptor Cell Outer Segment, Proteolysis
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