Abstract
The light-detecting organelle of the photoreceptor cell is a modified primary cilium, called the outer segment. The outer segment houses hundreds of light-sensitive membrane, “discs,” that are continuously renewed by the constant formation of new discs at the outer segment base and the phagocytosis of old ones from outer segment tips by the retinal pigment epithelium. In this chapter, we describe how an actin cytoskeleton network, residing precisely at the site of disc formation, provides the driving force that pushes out the ciliary plasma membrane to form each disc evagination that subsequently can mature into a bona fide disc. We highlight the functions of actin-binding proteins, particularly PCARE and Arp2/3, that are known to participate in disc formation. Finally, we describe a working model of disc formation built upon the many studies focusing on the role of actin during disc morphogenesis.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Arikawa K, Williams DS. Organization of actin filaments and immunocolocalization of alpha-actinin in the connecting cilium of rat photoreceptors. J Comp Neurol. 1989;288:640–6.
Besharse JC, Hollyfield JG, Rayborn ME. Turnover of rod photoreceptor outer segments. II. Membrane addition and loss in relationship to light. J Cell Biol. 1977;75:507–27.
Blanchoin L, Boujemaa-Paterski R, Sykes C, et al. Actin dynamics, architecture, and mechanics in cell motility. Physiol Rev. 2014;94:235–63.
Chaitin MH, Bok D. Immunoferritin localization of actin in retinal photoreceptors. Invest Ophthalmol Vis Sci. 1986;27:1764–7.
Chaitin MH, Burnside B. Actin filament polarity at the site of rod outer segment disk morphogenesis. Invest Ophthalmol Vis Sci. 1989;30:2461–9.
Chaitin MH, Carlsen RB, Samara GJ. Immunogold localization of actin in develo** photoreceptor cilia of normal and rds mutant mice. Exp Eye Res. 1988;47:437–46.
Chaitin MH, Schneider BG, Hall MO, et al. Actin in the photoreceptor connecting cilium: immunocytochemical localization to the site of outer segment disk formation. J Cell Biol. 1984;99:239–47.
Chen Z, Borek D, Padrick SB, et al. Structure and control of the actin regulatory WAVE complex. Nature. 2010;468:533–8.
Corral-Serrano JC, Lamers IJC, van Reeuwijk J, et al. PCARE and WASF3 regulate ciliary F-actin assembly that is required for the initiation of photoreceptor outer segment disk formation. Proc Natl Acad Sci U S A. 2020;117:9922–31.
Hale IL, Fisher SK, Matsumoto B. The actin network in the ciliary stalk of photoreceptors functions in the generation of new outer segment discs. J Comp Neurol. 1996;376:128–42.
Haruta M, Bush RA, Kjellstrom S, et al. Depleting Rac1 in mouse rod photoreceptors protects them from photo-oxidative stress without affecting their structure or function. Proc Natl Acad Sci U S A. 2009;106:9397–402.
Kaplan MW. Disk membrane initiation and insertion are not required for axial disk displacement in Xenopus laevis rod outer segments. Curr Eye Res. 1998;17:73–8.
Kevany BM, Zhang N, Jastrzebska B, et al. Animals deficient in C2Orf71, an autosomal recessive retinitis pigmentosa-associated locus, develop severe early-onset retinal degeneration. Hum Mol Genet. 2015;24:2627–40.
Nemet I, Tian G, Imanishi Y. Submembrane assembly and renewal of rod photoreceptor cGMP-gated channel: insight into the actin-dependent process of outer segment morphogenesis. J Neurosci. 2014;34:8164–74.
Nishimura DY, Baye LM, Perveen R, et al. Discovery and functional analysis of a retinitis pigmentosa gene, C2ORF71. Am J Hum Genet. 2010;86:686–95.
Sandoz D, Gounon P, Karsenti E, et al. Immunocytochemical localization of tubulin, actin, and myosin in axonemes of ciliated cells from quail oviduct. Proc Natl Acad Sci U S A. 1982;79:3198–202.
Soderling SH. Grab your partner with both hands: cytoskeletal remodeling by Arp2/3 signaling. Sci Signal. 2009;2:pe5.
Spencer WJ, Lewis TR, Pearring JN, et al. Photoreceptor discs: built like Ectosomes. Trends Cell Biol. 2020;30:904–15.
Spencer WJ, Lewis TR, Phan S, et al. Photoreceptor disc membranes are formed through an Arp2/3-dependent lamellipodium-like mechanism. Proc Natl Acad Sci U S A. 2019;116:27043–52.
Vaughan DK, Fisher SK. The distribution of F-actin in cells isolated from vertebrate retinas. Exp Eye Res. 1987;44:393–406.
Vaughan DK, Fisher SK. Cytochalasin D disrupts outer segment disc morphogenesis in situ in rabbit retina. Invest Ophthalmol Vis Sci. 1989;30:339–42.
Williams DS, Linberg KA, Vaughan DK, et al. Disruption of microfilament organization and deregulation of disk membrane morphogenesis by cytochalasin D in rod and cone photoreceptors. J Comp Neurol. 1988;272:161–76.
Acknowledgments
This work was supported by NIH grants EY012859, EY030451, and EY005722; the Knights Templar Eye Foundation; and Unrestricted Grant from Research to Prevent Blindness.
Author information
Authors and Affiliations
Corresponding author
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
Spencer, W.J., Arshavsky, V.Y. (2023). A Ciliary Branched Actin Network Drives Photoreceptor Disc Morphogenesis. 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_74
Download citation
DOI: https://doi.org/10.1007/978-3-031-27681-1_74
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)