Abstract
Retinal pigment epithelium (RPE) cells daily ingest the tips of the photoreceptor outer segments (POSs), with phagosome number varying throughout a 24-h cycle. A major focus in the literature has been on a peak in phagosome concentration shortly after lights-on. Moreover, this peak has frequently been inferred to represent a peak in POS tip ingestion. Here, we have reviewed old and new literature on the daily cycle of phagosome number in the RPE and conclude that there is more variation in the timing of phagosome concentration peaks than is currently acknowledged. We also discuss that phagosome quantity is affected by the rate of phagosome degradation as well as the rate of ingestion; given that phagosome half-life may not be constant throughout the daily cycle, maximal POS ingestion may not necessarily coincide with a peak in phagosome concentration.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Dowling JE, Gibbons IR. The fine structure of the pigment epithelium in the albino rat. J Cell Biol. 1962;14:459–74.
Young RW. The renewal of photoreceptor cell outer segments. J Cell Biol. 1967;33:61–72.
Young RW, Bok D. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J Cell Biol. 1969;42:392–403.
Young RW. The renewal of rod and cone outer segments in the rhesus monkey. J Cell Biol. 1971;49:303–18.
Besharse JC, Hollyfield JG. Turnover of mouse photoreceptor outer segments in constant light and darkness. Invest Ophthalmol Vis Sci. 1979;18:1019–24.
Volland S, Esteve-Rudd J, Hoo J, Yee C, Williams DS. A comparison of some organizational characteristics of the mouse central retina and the human macula. PLoS One. 2015;10:e0125631.
Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, et al. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet. 2000;26:270–1.
Esteve-Rudd J, Hazim RA, Diemer T, Paniagua AE, Volland S, Umapathy A, et al. Defective phagosome motility and degradation in cell nonautonomous RPE pathogenesis of a dominant macular degeneration. Proc Natl Acad Sci U S A. 2018;115:5468–73.
Williams DS, Fisher SK. Prevention of rod disk shedding by detachment from the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1987;28:184–7.
Lakkaraju A, Umapathy A, Tan LX, Daniele L, Philp NJ, Boesze-Battaglia K, et al. The cell biology of the retinal pigment epithelium. Prog Retin Eye Res. 2020:100846.
LaVail MM. Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science. 1976;194:1071–4.
Basinger S, Hoffman R, Matthes M. Photoreceptor shedding is initiated by light in the frog retina. Science. 1976;194:1074–6.
Young RW. The daily rhythm of shedding and degradation of cone outer segment membranes in the lizard retina. J Ultrastruct Res. 1977;61:172–85.
O'Day WT, Young RW. Rhythmic daily shedding of outer-segment membranes by visual cells in the goldfish. J Cell Biol. 1978;76:593–604.
Young RW. The daily rhythm of shedding and degradation of rod and cone outer segment membranes in the chick retina. Invest Ophthalmol Vis Sci. 1978;17:105–16.
Tabor GA, Fisher SK, Anderson DH. Rod and cone disc shedding in light-entrained tree squirrels. Exp Eye Res. 1980;30:545–57.
Fisher SK, Pfeffer BA, Anderson DH. Both rod and cone disc shedding are related to light onset in the cat. Invest Ophthalmol Vis Sci. 1983;24:844–56.
Immel JH, Fisher SK. Cone photoreceptor shedding in the tree shrew (Tupaia belangerii). Cell Tissue Res. 1985;239:667–75.
Anderson DH, Fisher SK, Erickson PA, Tabor GA. Rod and cone disc shedding in the rhesus monkey retina: a quantitative study. Exp Eye Res. 1980;30:559–74.
Bobu C, Hicks D. Regulation of retinal photoreceptor phagocytosis in a diurnal mammal by circadian clocks and ambient lighting. Invest Ophthalmol Vis Sci. 2009;50:3495–502.
Lewis TR, Kundinger SR, Link BA, Insinna C, Besharse JC. Kif17 phosphorylation regulates photoreceptor outer segment turnover. BMC Cell Biol. 2018;19:25.
Herman KG, Steinberg RH. Phagosome movement and the diurnal pattern of phagocytosis in the tapetal retinal pigment epithelium of the opossum. Invest Ophthalmol Vis Sci. 1982;23:277–90.
Gibbs D, Kitamoto J, Williams DS. Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc Natl Acad Sci U S A. 2003;100:6481–6.
Wavre-Shapton ST, Meschede IP, Seabra MC, Futter CE. Phagosome maturation during endosome interaction revealed by partial rhodopsin processing in retinal pigment epithelium. J Cell Sci. 2014;127:3852–61.
Jiang M, Esteve-Rudd J, Lopes VS, Diemer T, Lillo C, Rump A, et al. Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis. J Cell Biol. 2015;210:595–611.
Esteve-Rudd J, Lopes VS, Jiang M, Williams DS. In vivo and in vitro monitoring of phagosome maturation in retinal pigment epithelium cells. Adv Exp Med Biol. 2014;801:85–90.
Finnemann SC, Bonilha VL, Marmorstein AD, Rodriguez-Boulan E. Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc Natl Acad Sci U S A. 1997;94:12932–7.
Nandrot EF, Kim Y, Brodie SE, Huang X, Sheppard D, Finnemann SC. Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking alphavbeta5 integrin. J Exp Med. 2004;200:1539–45.
Kocaoglu OP, Liu Z, Zhang F, Kurokawa K, Jonnal RS, Miller DT. Photoreceptor disc shedding in the living human eye. Biomed Opt Express. 2016;7:4554–68.
Zhang P, Shibata B, Peinado G, Zawadzki RJ, FitzGerald P, Pugh EN Jr. Measurement of diurnal variation in rod outer segment length in vivo in mice with the OCT optoretinogram. Invest Ophthalmol Vis Sci. 2020;61:9.
Acknowledgments
The authors are supported by a BrightFocus Foundation postdoctoral fellowship (A.E.P., M2021004F) and NIH R01EY027442 grant.
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this paper
Cite this paper
Paniagua, A.E., Sabharwal, H.S., Kethu, K., Chang, A.W., Williams, D.S. (2023). Revisiting the Daily Timing of POS Phagocytosis. In: Ash, J.D., Pierce, E., Anderson, R.E., Bowes Rickman, C., Hollyfield, J.G., Grimm, C. (eds) Retinal Degenerative Diseases XIX. Advances in Experimental Medicine and Biology, vol 1415. Springer, Cham. https://doi.org/10.1007/978-3-031-27681-1_75
Download citation
DOI: https://doi.org/10.1007/978-3-031-27681-1_75
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-27680-4
Online ISBN: 978-3-031-27681-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)