Skip to main content

Revisiting the Daily Timing of POS Phagocytosis

  • Conference paper
  • First Online:
Retinal Degenerative Diseases XIX

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 349.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 449.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Dowling JE, Gibbons IR. The fine structure of the pigment epithelium in the albino rat. J Cell Biol. 1962;14:459–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Young RW. The renewal of photoreceptor cell outer segments. J Cell Biol. 1967;33:61–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Young RW, Bok D. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J Cell Biol. 1969;42:392–403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Young RW. The renewal of rod and cone outer segments in the rhesus monkey. J Cell Biol. 1971;49:303–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Besharse JC, Hollyfield JG. Turnover of mouse photoreceptor outer segments in constant light and darkness. Invest Ophthalmol Vis Sci. 1979;18:1019–24.

    CAS  PubMed  Google Scholar 

  6. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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.

    Article  CAS  PubMed  Google Scholar 

  8. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Williams DS, Fisher SK. Prevention of rod disk shedding by detachment from the retinal pigment epithelium. Invest Ophthalmol Vis Sci. 1987;28:184–7.

    CAS  PubMed  Google Scholar 

  10. 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.

    Google Scholar 

  11. LaVail MM. Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science. 1976;194:1071–4.

    Article  CAS  PubMed  Google Scholar 

  12. Basinger S, Hoffman R, Matthes M. Photoreceptor shedding is initiated by light in the frog retina. Science. 1976;194:1074–6.

    Article  CAS  PubMed  Google Scholar 

  13. 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.

    Article  CAS  PubMed  Google Scholar 

  14. 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.

    Article  CAS  PubMed  Google Scholar 

  15. 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.

    CAS  PubMed  Google Scholar 

  16. Tabor GA, Fisher SK, Anderson DH. Rod and cone disc shedding in light-entrained tree squirrels. Exp Eye Res. 1980;30:545–57.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    CAS  PubMed  Google Scholar 

  18. Immel JH, Fisher SK. Cone photoreceptor shedding in the tree shrew (Tupaia belangerii). Cell Tissue Res. 1985;239:667–75.

    Article  CAS  PubMed  Google Scholar 

  19. 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.

    Article  CAS  PubMed  Google Scholar 

  20. 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.

    Article  PubMed  Google Scholar 

  21. Lewis TR, Kundinger SR, Link BA, Insinna C, Besharse JC. Kif17 phosphorylation regulates photoreceptor outer segment turnover. BMC Cell Biol. 2018;19:25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 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.

    CAS  PubMed  Google Scholar 

  23. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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.

    Article  PubMed  Google Scholar 

  27. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  30. 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.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors are supported by a BrightFocus Foundation postdoctoral fellowship (A.E.P., M2021004F) and NIH R01EY027442 grant.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Antonio E. Paniagua or David S. Williams .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this paper

Check for updates. Verify currency and authenticity via CrossMark

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

Publish with us

Policies and ethics