Abstract
During early development of rod and cone photoreceptors, the outer segment (OS) assembles on the apical cell surface by an elaborate process of membrane and protein transport followed by membrane reorganization to form the highly organized stack of membrane disks found in the OS of mature cells. The process of membrane and protein transport continues in mature photoreceptors as the molecular components of the OS turnover at a prodigious rate for the life of the cell (Young, 1967). Intersegmental transport between the inner segment (IS) and the OS is a major logistical problem as all OS macromolecules are synthesized in the IS and must be transported to the OS. Elucidating the molecular pathways involved in intersegmental transport will ultimately require a refined understanding of the photoreceptor connecting cilium as this structure is the only stable connecting link between the IS and the OS and is the likely transport corridor (reviewed in Besharse and Horst, 1990). In addition, understanding the details of these pathways is likely to provide an improved understanding of photoreceptor degeneration diseases that involve trafficking between the two segments.
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References
Beech, P.L., K. Pagh-Roehl, Y. Noda, N. Hirokawa, B. Burnside, and J.L. Rosenbaum, 1996, Localization of kinesin superfamily proteins to the connecting cilium of fish photoreceptors, JCell Sci. 109:889–97.
Besharse, J.C., and C.J. Horst. 1990. The Photoreceptor Connecting Cilium. A Model for the Transition Zone. In Ciliary and Flagellar Membranes. R.A. Bloodgood, editor. Plenum Press, New York. 389–417. Boesze-Battaglia, K., and A.F. Goldberg, 2002, Photoreceptor renewal: a role for peripherin/rds, Int Rev Cytol. 217:183–225.
Cole, D.G., D.R. Diener, A.L. Himelblau, P.L. Beech, J.C. Fuster, and J.L. Rosenbaum, 1998, Chlamydomonas kinesin-Il-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons, J Cell Biol. 141:993–1008.
Deane, J.A., D.G. Cole, E.S. Seeley, D.R. Diener, and J.L. Rosenbaum, 2001, Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles, Curr Biol. 11:1586–90.
Gibbons, B.H., D.J. Asai, W.J. Tang, T.S. Hays, and I.R. Gibbons, 1994, Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins, Mol Biol Cell. 5:57–70.
Grissom, P.M., E.A. Vaisberg, and J.R. McIntosh, 2002, Identification of a novel light intermediate chain (D2LIC) for mammalian cytoplasmic dynein 2, Mol Biol Cell. 13:817–29.
Hagstrom, S.A., M. Adamian, M. Scimeca, B.S. Pawlyk, G. Yue, and T. Li, 2001, A role for the Tubby-like protein 1 in rhodopsin transport, Invest Ophthalmol Vis Sci. 42:1955–62.
Hagstrom, S.A., M. Duyao, M.A. North, and T. Li, 1999, Retinal degeneration in tulpl-/- mice: vesicular accumulation in the interphotoreceptor matrix, Invest Ophthalmol Vis Sci. 40:2795–802.
Haycraft, C.J., P. Swoboda, P.D. Taulman, J.H. Thomas, and B.K. Yoder, 2001, The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms, Development. 128:1493–505.
Horst, C.J., L.V. Johnson, and J.C. Besharse, 1990, Transmembrane assemblage of the photoreceptor connecting cilium and motile cilium transition zone contain a common immunologic epitope, Cell Motil Cytoskeleton. 17:329–44.
Iomini, C., V. Babaev-Khaimov, M. Sassaroli, and G. Pipemo, 2001, Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases,.1 Cell Biol. 153:13–24.
Liu, X., I.P. Udovichenko, S.D. Brown, K.P. Steel, and D.S. Williams, 1999, Myosin VIIa participates in opsin transport through the photoreceptor cilium, JNeurosci. 19:6267–74.
Marshall, W.F., and J.L. Rosenbaum, 2001, Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control, J Cell Biol. 155:405–14.
Marszalek, J.R., and L.S. Goldstein, 2000, Understanding the functions of kinesin-II, Biochim Biophys Acta. 1496:142–150.
Marszalek, J.R., X. Liu, E.A. Roberts, D. Chui, J.D. Mardi, D.S. Williams, and L.S. Goldstein, 2000, Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors [In Process Citation], Cell. 102:175–87.
Mikami, A., S.H. Tynan, T. Hama, K. Luby-Phelps, T. Saito, J.E. Crandall, J.C. Besharse, and R.B. Vallee, 2002, Molecular structure of cytoplasmic dynein 2 and its distribution in neuronal and ciliated cells, J Cell Sci. 115:4801–4808.
Moyer, J.H., M.J. Lee-Tischler, H.Y. Kwon, J.J. Schrick, E.D. Avner, W.E. Sweeney, V.L. Godfrey, N.L. Cacheiro, J.E. Wilkinson, and R.P. Woychik, 1994, Candidate gene associated with a mutation causing recessive polycystic kidney disease in mice, Science. 264:1329–33.
Murcia, N.S., W.G. Richards, B.K. Yoder, M.L. Mucenski, J.R. Dunlap, and R.P. Woychik, 2000, The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination, Development. 127:2347–55.
Muresan, V., A. Lyass, and B.J. Schnapp, 1999, The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors, JNeurosci. 19:1027–37.
Nir, I., and D.S. Papermaster, 1986, Immunocytochemical localization of opsin in the inner segment and ciliary plasma membrane of photoreceptors in retinas of rds mutant mice, Invest Ophthalmol Vis Sci. 27:836–40.
Nir, I., G. Sagie, and D.S. Papermaster, 1987, Opsin accumulation in photoreceptor inner segment plasma membranes of dystrophic RCS rats, Invest Ophthalmol Vis Sci. 28:62–9.
Pazour, G.J., S.A. Baker, J.A. Deane, D.G. Cole, B.L. Dickert, J.L. Rosenbaum, G.B. Witman, and J.C. Besharse, 2002, The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance, J Cell Biol. 157:103–14.
Pazour, G.J., B.L. Dickert, Y. Vucica, E.S. Seeley, J.L. Rosenbaum, G.B. Witman, and D.G. Cole, 2000, Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella, JCell Biol. 151:709–18.
Pazour, G.J., B.L. Dickert, and G.B. Witman, 1999, The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly, J Cell Biol. 144:473–81.
Pazour, G.J., C.G. Wilkerson, and G.B. Witman, 1998, A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT), J Cell Biol. 141:979–92.
Philp, N.J., W. Chang, and K. Long, 1987, Light-stimulated protein movement in rod photoreceptor cells of the rat retina, FEBS Lett. 225:127–32.
Pipemo, G., and K. Mead, 1997, Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella, Proc Natl Acad Sci USA. 94:4457–62.
Piperno, G., K. Mead, and S. Henderson, 1996, Inner dynein arms but not outer dynein arms require the activity of kinesin homologue protein KHPI(FLA10) to reach the distal part of flagella in Chlamydomonas, J Cell Biol. 133:371–9.
Porter, M.E., R. Bower, J.A. Knott, P. Byrd, and W. Dentler, 1999, Cytoplasmic dynein heavy chain lb is required for flagellar assembly in Chlamydomonas, Mol Biol Cell. 10:693–712.
Qin, H., J.L. Rosenbaum, and M.M. Barr, 2001, An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons, Curr Biol. 11:457-61.
Rohlich, P., 1975, The sensory cilium of retinal rods is analogous to the transitional zone of motile cilia, Cell Tissue Res. 161:421–30.
Roof, D.J., and C.A. Heth, 1988, Expression of transducin in retinal rod photoreceptor outer segments, Science. 241:845–7.
Rosenbaum, J.L., D.G. Cole, and D.R. Diener, 1999, Intraflagellar transport: the eyes have it, JCell Biol. 144:385–8.
Rosenbaum, J.L., and G.B. Witman, 2002, Intraflagellar transport, Nat Rev Mol Cell Biol. 3:813–25.
Signor, D., K.P. Wedaman, J.T. Orozco, N.D. Dwyer, C.I. Bargmann, L.S. Rose, and J.M. Scholey, 1999a, Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans, J Cell Biol. 147:519–30.
Signor, D., K.P. Wedaman, L.S. Rose, and J.M. Scholey, 1999b, Two heteromeric kinesin complexes in chemosensory neurons and sensory cilia of Caenorhabditis elegans, Mol Biol Cell. 10:345–60.
Sokolov, M., A.L. Lyubarsky, K.J. Strissel, A.B. Savchenko, V.I. Govardovskii, E.N. Pugh, and V.Y. Arshaysky, 2002, Massive Light-Driven Translocation of Transducin between the Two Major Compartments of Rod Cells. A Novel Mechanism of Light Adaptation, Neuron. 34:95–106.
Tai, A.W., J.Z. Chuang, C. Bode, U. Wolfrum, and C.H. Sung, 1999, Rhodopsin’s carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1, Cell. 97:877–87.
Traboulsi, E.I., 1998, Ocular malformations and developmental genes, JAapos. 2:317–23.
Walther, Z., M. Vashishtha, and J.L. Hall, 1994, The Chlamydomonas FLA10 gene encodes a novel kinesinhomologous protein, J Cell Biol. 126:175–88.
Whelan, J.P., and J.F. McGinnis, 1988, Light-dependent subcellular movement of photoreceptor proteins, J Neurosci Res. 20:263–70.
Whitehead, J.L., S.Y. Wang, L. Bost-Usinger, E. Hoang, K.A. Frazer, and B. Bumside, 1999, Photoreceptor localization of the KIF3A and KIF3B subunits of the heterotrimeric microtubule motor kinesin II in vertebrate retina, Exp Eye Res. 69:491–503.
Young, R.W., 1967, The renewal of photoreceptor cell outer segments, J Cell Biol. 33:61–72.
Young, R.W., and D. Bok, 1969, Participation of the retinal pigment epithelium in the rod outer segment renewal process, J Cell Biol. 42:392–403.
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Besharse, J.C., Baker, S.A., Luby-Phelps, K., Pazour, G.J. (2003). Photoreceptor Intersegmental Transport and Retinal Degeneration . In: LaVail, M.M., Hollyfield, J.G., Anderson, R.E. (eds) Retinal Degenerations. Advances in Experimental Medicine and Biology, vol 533. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0067-4_20
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DOI: https://doi.org/10.1007/978-1-4615-0067-4_20
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