Diffuse or hitch a ride: how photoreceptor lipidated proteins get from here to there

References

Alkanderi, S., Molinari, E., Shaheen, R., Elmaghloob, Y., Stephen, L.A., Sammut, V., Ramsbottom, S.A., Srivastava, S., Cairns, G., Edwards, N., et al. (2018). ARL3 mutations cause Joubert syndrome by disrupting ciliary protein composition. Am. J. Hum. Genet. 103, 612–620.10.1016/j.ajhg.2018.08.015Suche in Google Scholar

Allan, V.J. (2011). Cytoplasmic dynein. Biochem. Soc. Trans. 39, 1169–1178.10.1042/BST0391169Suche in Google Scholar

Anant, J.S., Ong, O.C., Xie, H., Clarke, S., OBrien, P.J., and Fung, B.K.-K. (1992). In vivo differential prenylation of retinal cyclic GMP phosphodiesterase catalytic subunits. J. Biol. Chem. 267, 687–690.10.1016/S0021-9258(18)48336-6Suche in Google Scholar

Arshavsky, V.Y., Lamb, T.D., and Pugh Jr, E.N. (2002). G proteins and phototransduction. Annu. Rev. Physiol. 64, 153–187.10.1146/annurev.physiol.64.082701.102229Suche in Google Scholar

Artemyev, N.O. (2008). Light-dependent compartmentalization of transducin in rod photoreceptors. Mol. Neurobiol. 37, 44–51.10.1007/s12035-008-8015-2Suche in Google Scholar

Avasthi, P., Watt, C.B., Williams, D.S., Le, Y.Z., Li, S., Chen, C.K., Marc, R.E., Frederick, J.M., and Baehr, W. (2009). Trafficking of membrane proteins to cone but not rod outer segments is dependent on heterotrimeric kinesin-II. J. Neurosci. 29, 14287–14298.10.1523/JNEUROSCI.3976-09.2009Suche in Google Scholar

Baehr, W. (2014). Membrane protein transport in photoreceptors: the function of PDEdelta: the Proctor lecture. Invest. Ophthalmol. Vis. Sci. 55, 8653–8666.10.1167/iovs.14-16066Suche in Google Scholar

Baehr, W., Morita, E.A., Swanson, R.J., and Applebury, M.L. (1982). Characterization of bovine rod outer segment G-protein. J. Biol. Chem. 257, 6452–6460.10.1016/S0021-9258(20)65163-8Suche in Google Scholar

Barlowe, C.K. and Miller, E.A. (2013). Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193, 383–410.10.1534/genetics.112.142810Suche in Google Scholar PubMed PubMed Central

Barrasso, A.P., Wang, S., Tong, X., Christiansen, A.E., Larina, I.V., and Poche, R.A. (2018). Live imaging of developing mouse retinal slices. Neural. Dev. 13, 23.10.1186/s13064-018-0120-ySuche in Google Scholar PubMed PubMed Central

Besharse, J.C., Hollyfield, J.G., and Rayborn, M.E. (1977). Photoreceptor outer segments: accelerated membrane renewal in rods after exposure to light. Science 196, 536–538.10.1126/science.300504Suche in Google Scholar PubMed

Bielas, S.L., Silhavy, J.L., Brancati, F., Kisseleva, M.V., Al-Gazali, L., Sztriha, L., Bayoumi, R.A., Zaki, M.S., Abdel-Aleem, A., Rosti, R.O., et al. (2009). Mutations in INPP5E, encoding inositol polyphosphate-5-phosphatase E, link phosphatidyl inositol signaling to the ciliopathies. Nat. Genet. 41, 1032–1036.10.1038/ng.423Suche in Google Scholar PubMed PubMed Central

Bok, D. (1985). Retinal photoreceptor-pigment epithelium interactions. Friedenwald lecture. Invest. Ophthalmol. Vis. Sci. 26, 1659–1694.Suche in Google Scholar

Boldt, K., van Reeuwijk, J., Lu, Q., Koutroumpas, K., Nguyen, T.M., Texier, Y., van Beersum, S.E., Horn, N., Willer, J.R., Mans, D.A., et al. (2016). An organelle-specific protein landscape identifies novel diseases and molecular mechanisms. Nat. Commun. 7, 11491.10.1038/ncomms11491Suche in Google Scholar PubMed PubMed Central

Brooks, C., Murphy, J., Belcastro, M., Heller, D., Kolandaivelu, S., Kisselev, O., and Sokolov, M. (2018). Farnesylation of the transducin G protein gamma subunit is a prerequisite for its ciliary targeting in rod photoreceptors. Front. Mol. Neurosci. 11, 16.10.3389/fnmol.2018.00016Suche in Google Scholar PubMed PubMed Central

Burgoyne, T., Meschede, I.P., Burden, J.J., Bailly, M., Seabra, M.C., and Futter, C.E. (2015). Rod disc renewal occurs by evagination of the ciliary plasma membrane that makes cadherin-based contacts with the inner segment. Proc. Natl. Acad. Sci. USA 112, 15922–15927.10.1073/pnas.1509285113Suche in Google Scholar PubMed PubMed Central

Calvert, P.D., Strissel, K.J., Schiesser, W.E., Pugh, E.N., Jr., and Arshavsky, V.Y. (2006). Light-driven translocation of signaling proteins in vertebrate photoreceptors. Trends Cell Biol. 16, 560–568.10.1016/B978-0-12-374203-2.00176-7Suche in Google Scholar

Chadha, A., Volland, S., Baliaouri, N.V., Tran, E.M., and Williams, D.S. (2019). The route of the visual receptor rhodopsin along the cilium. J. Cell Sci. 132, pii: jcs229526.10.1242/jcs.229526Suche in Google Scholar PubMed PubMed Central

Chapple, J.P., Hardcastle, A.J., Grayson, C., Willison, K.R., and Cheetham, M.E. (2002). Delineation of the plasma membrane targeting domain of the X-linked retinitis pigmentosa protein RP2. Invest. Ophthalmol. Vis. Sci. 43, 2015–2020.Suche in Google Scholar

Chavez, M., Ena, S., Van Sande, J., de Kerchove d’Exaerde, A., Schurmans, S., and Schiffmann, S.N. (2015). Modulation of ciliary phosphoinositide content regulates trafficking and sonic hedgehog signaling output. Dev. Cell 34, 338–350.10.1016/j.devcel.2015.06.016Suche in Google Scholar PubMed

Cheguru, P., Zhang, Z., and Artemyev, N.O. (2014). The GAFa domain of phosphodiesterase-6 contains a rod outer segment localization signal. J. Neurochem. 129, 256–263.10.1111/jnc.12501Suche in Google Scholar PubMed PubMed Central

Cheung, P.Y. and Pfeffer, S.R. (2016). Transport vesicle tethering at the trans Golgi network: coiled coil proteins in action. Front. Cell Dev. Biol. 4, 18.10.3389/fcell.2016.00018Suche in Google Scholar PubMed PubMed Central

Conduit, S.E., Dyson, J.M., and Mitchell, C.A. (2012). Inositol polyphosphate 5-phosphatases; new players in the regulation of cilia and ciliopathies. FEBS Lett. 586, 2846–2857.10.1016/j.febslet.2012.07.037Suche in Google Scholar

Constantine, R., Zhang, H., Gerstner, C.D., Frederick, J.M., and Baehr, W. (2012). Uncoordinated (UNC)119: coordinating the trafficking of myristoylated proteins. Vision Res. 75, 26–32.10.1016/j.visres.2012.08.012Suche in Google Scholar

Cowan, C.W., Wensel, T.G., and Arshavsky, V.Y. (2000). Enzymology of GTPase acceleration in phototransduction. Methods Enzymol. 315, 524–538.10.1016/S0076-6879(00)15865-3Suche in Google Scholar

Deretic, D. (1997). Rab proteins and post-Golgi trafficking of rhodopsin in photoreceptor cells. Electrophoresis 18, 2537–2541.10.1002/elps.1150181408Suche in Google Scholar PubMed

Deretic, D. and Papermaster, D.S. (1993). Rab6 is associated with a compartment that transports rhodopsin from the trans-Golgi to the site of rod outer segment disk formation in frog retinal photoreceptors. J. Cell Sci. 106, 803–813.10.1242/jcs.106.3.803Suche in Google Scholar PubMed

Deretic, D. and Wang, J. (2012). Molecular assemblies that control rhodopsin transport to the cilia. Vision Res. 75, 5–10.10.1016/j.visres.2012.07.015Suche in Google Scholar PubMed PubMed Central

Deretic, D., Schmerl, S., Hargrave, P.A., Arendt, A., and McDowell, J.H. (1998). Regulation of sorting and post-Golgi trafficking of rhodopsin by its C-terminal sequence QVS(A)PA. Proc. Natl. Acad. Sci. U.S.A. 95, 10620–10625.10.1073/pnas.95.18.10620Suche in Google Scholar PubMed PubMed Central

Deretic, D., Williams, A.H., Ransom, N., Morel, V., HArgrave, P.A., and Arendt, A. (2005). Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proc. Natl. Acad. Sci. USA 102, 3301–3306.10.1073/pnas.0500095102Suche in Google Scholar PubMed PubMed Central

Dharmat, R., Eblimit, A., Robichaux, M.A., Zhang, Z., Nguyen, T.T., Jung, S.Y., He, F., Jain, A., Li, Y., Qin, J., et al. (2018). SPATA7 maintains a novel photoreceptor-specific zone in the distal connecting cilium. J. Cell Biol. 217, 2851–2865.10.1083/jcb.201712117Suche in Google Scholar PubMed PubMed Central

Ding, J.D., Salinas, R.Y., and Arshavsky, V.Y. (2015). Discs of mammalian rod photoreceptors form through the membrane evagination mechanism. J. Cell Biol. 211, 495–502.10.1083/jcb.201508093Suche in Google Scholar PubMed PubMed Central

Fan, J., Rohrer, B., Frederick, J.M., Baehr, W., and Crouch, R.K. (2008). Rpe65^−/− and Lrat^−/− mice: comparable models of leber congenital amaurosis. Invest. Ophthalmol. Vis. Sci. 49, 2384–2389.10.1167/iovs.08-1727Suche in Google Scholar

Fansa, E.K. and Wittinghofer, A. (2016). Sorting of lipidated cargo by the Arl2/Arl3 system. Small GTPases 7, 222–230.10.1080/21541248.2016.1224454Suche in Google Scholar

Fansa, E.K., Kosling, S.K., Zent, E., Wittinghofer, A., and Ismail, S. (2016). PDE6d-mediated sorting of INPP5E into the cilium is determined by cargo-carrier affinity. Nat. Commun. 7, 11366.10.1038/ncomms11366Suche in Google Scholar

Garcia-Gonzalo, F.R., Phua, S.C., Roberson, E.C., Garcia 3rd, G., Abedin, M., Schurmans, S., Inoue, T., and Reiter, J.F. (2015). Phosphoinositides regulate ciliary protein trafficking to modulate hedgehog signaling. Dev. Cell 34, 400–409.10.1016/j.devcel.2015.08.001Suche in Google Scholar

Gelb, M.H., Brunsveld, L., Hrycyna, C.A., Michaelis, S., Tamanoi, F., Van Voorhis, W.C., and Waldmann, H. (2006). Therapeutic intervention based on protein prenylation and associated modifications. Nat. Chem. Biol. 2, 518–528.10.1038/nchembio818Suche in Google Scholar

Gillespie, P.G., Prusti, R.K., Apel, E.D., and Beavo, J.A. (1989). A soluble form of bovine rod photoreceptor phosphodiesterase has a novel 15-kDa subunit. J. Biol. Chem. 264, 12187–12193.10.1016/S0021-9258(18)63839-6Suche in Google Scholar

Godi, A., Pertile, P., Meyers, R., Marra, P., Di Tullio, G., Iurisci, C., Luini, A., Corda, D., and De Matteis, M.A. (1999). ARF mediates recruitment of PtdIns-4-OH kinase-b and stimulates synthesis of PtdIns(4,5)P₂ on the Golgi complex. Nat. Cell. Biol. 1, 280–287.10.1038/12993Suche in Google Scholar PubMed

Gomez-Navarro, N. and Miller, E.A. (2016). COP-coated vesicles. Curr. Biol. 26, R54–R57.10.1016/j.cub.2015.12.017Suche in Google Scholar PubMed

Gotthardt, K., Lokaj, M., Koerner, C., Falk, N., Giessl, A., andWittinghofer, A. (2015). A G-protein activation cascade from Arl13B to Arl3 and implications for ciliary targeting of lipidated proteins. Elife 4, pii: e11859.10.7554/eLife.11859.015Suche in Google Scholar

Grayson, C., Bartolini, F., Chapple, J.P., Willison, K.R., Bhamidipati, A., Lewis, S.A., Luthert, P.J., Hardcastle, A.J., Cowan, N.J., and Cheetham, M.E. (2002). Localization in the human retina of the X-linked retinitis pigmentosa protein RP2, its homologue cofactor C and the RP2 interacting protein Arl3. Hum. Mol. Genet. 11, 3065–3074.10.1093/hmg/11.24.3065Suche in Google Scholar PubMed

Griffiths, G. and Simons, K. (1986). The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234, 438–443.10.1126/science.2945253Suche in Google Scholar PubMed

Hammond, G.R., Machner, M.P., and Balla, T. (2014). A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J. Cell Biol. 205, 113–126.10.1083/jcb.201312072Suche in Google Scholar PubMed PubMed Central

Hanke-Gogokhia, C., Wu, Z., Gerstner, C.D., Frederick, J.M., Zhang, H., and Baehr, W. (2016). Arf-like Protein 3 (ARL3) regulates protein trafficking and ciliogenesis in mouse photoreceptors. J. Biol. Chem. 291, 7142–7155.10.1074/jbc.M115.710954Suche in Google Scholar PubMed PubMed Central

Hanzal-Bayer, M., Renault, L., Roversi, P., Wittinghofer, A., and Hillig, R.C. (2002). The complex of Arl2-GTP and PDEd: from structure to function. EMBO J. 21, 2095–2106.10.1093/emboj/21.9.2095Suche in Google Scholar PubMed PubMed Central

Humphries, M.M., Rancourt, D., Farrar, G.J., Kenna, P., Hazel, M., Bush, R.A., Sieving, P.A., Sheils, D.M., McNally, N., Creighton, P., et al. (1997). Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat. Genet. 15, 216–219.10.1038/ng0297-216Suche in Google Scholar PubMed

Insinna, C., Baye, L.M., Amsterdam, A., Besharse, J.C., and Link, B.A. (2010). Analysis of a zebrafish dync1h1 mutant reveals multiple functions for cytoplasmic dynein 1 during retinal photoreceptor development. Neural. Dev. 5, 12.10.1186/1749-8104-5-12Suche in Google Scholar PubMed PubMed Central

Ismail, S.A., Chen, Y.X., Miertzschke, M., Vetter, I.R., Koerner, C., and Wittinghofer, A. (2012). Structural basis for Arl3-specific release of myristoylated ciliary cargo from UNC119. EMBO J. 31, 4085–4094.10.1038/emboj.2012.257Suche in Google Scholar PubMed PubMed Central

Jacoby, M., Cox, J.J., Gayral, S., Hampshire, D.J., Ayub, M., Blockmans, M., Pernot, E., Kisseleva, M.V., Compere, P., Schiffmann, S.N., et al. (2009). INPP5E mutations cause primary cilium signaling defects, ciliary instability and ciliopathies in human and mouse. Nat. Genet. 41, 1027–1031.10.1038/ng.427Suche in Google Scholar PubMed

Jiang, L., Wei, Y., Ronquillo, C.C., Marc, R.E., Yoder, B.K., Frederick, J.M., and Baehr, W. (2015). Heterotrimeric kinesin-2 (KIF3) mediates transition zone and axoneme formation of mouse photoreceptors. J. Biol. Chem. 290, 12765–12778.10.1074/jbc.M115.638437Suche in Google Scholar PubMed PubMed Central

Kameni Tcheudji, J.F., Lebeau, L., Virmaux, N., Maftei, C.G., Cote, R.H., Lugnier, C., and Schultz, P. (2001). Molecular organization of bovine rod cGMP-phosphodiesterase 6. J. Mol. Biol. 310, 781–791.10.1006/jmbi.2001.4813Suche in Google Scholar PubMed

Kandachar, V., Tam, B.M., Moritz, O.L., and Deretic, D. (2018). TI-VAMP/ VAMP7-SNARE-Rab-GTPase interaction network within a ciliary membrane targeting complex. J. Cell Sci 131, pii: jcs222034.10.1242/jcs.222034Suche in Google Scholar PubMed PubMed Central

Kerov, V., Rubin, W.W., Natochin, M., Melling, N.A., Burns, M.E., and Artemyev, N.O. (2007). N-terminal fatty acylation of transducin profoundly influences its localization and the kinetics of photoresponse in rods. J. Neurosci. 27, 10270–10277.10.1523/JNEUROSCI.2494-07.2007Suche in Google Scholar PubMed PubMed Central

Kevany, B.M. and Palczewski, K. (2010). Phagocytosis of retinal rod and cone photoreceptors. Physiology (Bethesda) 25, 8–15.10.1152/physiol.00038.2009Suche in Google Scholar PubMed PubMed Central

Kong, S., Du, X., Peng, C., Wu, Y., Li, H., Jin, X., Hou, L., Deng, K., Xu, T., and Tao, W. (2013). Dlic1 deficiency impairs ciliogenesis of photoreceptors by destabilizing dynein. Cell Res. 23, 835–850.10.1038/cr.2013.59Suche in Google Scholar PubMed PubMed Central

Koning, R.I., Koster, A.J., and Sharp, T.H. (2018). Advances in cryo-electron tomography for biology and medicine. Ann. Anat. 217, 82–96.10.1016/j.aanat.2018.02.004Suche in Google Scholar PubMed

Kosling, S.K., Fansa, E.K., Maffini, S., and Wittinghofer, A. (2018). Mechanism and dynamics of INPP5E transport into and inside the ciliary compartment. Biol. Chem. 399, 277–292.10.1515/hsz-2017-0226Suche in Google Scholar PubMed

Kuhn, H. (1980). Light- and GTP-regulated interaction of GTPase and other proteins with bovine photoreceptor membranes. Nature 283, 587–589.10.1038/283587a0Suche in Google Scholar PubMed

Lahne, M. and Hyde, D.R. (2017). Live-cell imaging: new avenues to investigate retinal regeneration. Neural. Regen. Res. 12, 1210–1219.10.4103/1673-5374.213533Suche in Google Scholar PubMed PubMed Central

Lai, R.K., Perez-Sala, D., Cañada, F.J., and Rando, R.R. (1990). The gamma subunit of transducin is farnesylated. Proc. Natl. Acad. Sci. USA 87, 7673–7677.10.1073/pnas.87.19.7673Suche in Google Scholar PubMed PubMed Central

Lem, J., Krasnoperova, N.V., Calvert, P.D., Kosaras, B., Cameron, D.A., Nicolo, M., Makino, C.L., and Sidman, R.L. (1999). Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc. Natl. Acad. Sci. U.S.A. 96, 736–741.10.1073/pnas.96.2.736Suche in Google Scholar PubMed PubMed Central

Liu, X., Udovichenko, I.P., Brown, S.D., Steel, K.P., and Williams, D.S. (1999). Myosin VIIa participates in opsin transport through the photoreceptor cilium. J. Neurosci. 19, 6267–6274.10.1523/JNEUROSCI.19-15-06267.1999Suche in Google Scholar

Lobanova, E.S., Finkelstein, S., Herrmann, R., Chen, Y.M., Kessler, C., Michaud, N.A., Trieu, L.H., Strissel, K.J., Burns, M.E., and Arshavsky, V.Y. (2008). Transducin gamma-subunit sets expression levels of a- and b-subunits and is crucial for rod viability. J. Neurosci. 28, 3510–3520.10.1523/JNEUROSCI.0338-08.2008Suche in Google Scholar

Lodowski, K.H., Lee, R., Ropelewski, P., Nemet, I., Tian, G., and Imanishi, Y. (2013). Signals governing the trafficking and mistrafficking of a ciliary GPCR, rhodopsin. J. Neurosci. 33, 13621–13638.10.1523/JNEUROSCI.1520-13.2013Suche in Google Scholar

Marszalek, J.R., Liu, X., Roberts, E.A., Chui, D., Marth, J.D., Williams, D.S., and Goldstein, L.S. (2000). Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102, 175–187.10.1016/S0092-8674(00)00023-4Suche in Google Scholar

Mavlyutov, T.A., Zhao, H., and Ferreira, P.A. (2002). Species-specific subcellular localization of RPGR and RPGRIP isoforms: implications for the phenotypic variability of congenital retinopathies among species. Hum. Mol. Genet. 11, 1899–1907.10.1093/hmg/11.16.1899Suche in Google Scholar PubMed

May-Simera, H., Nagel-Wolfrum, K., and Wolfrum, U. (2017). Cilia – the sensory antennae in the eye. Prog. Retin. Eye Res. 60, 144–180.10.1016/j.preteyeres.2017.05.001Suche in Google Scholar PubMed

Miertzschke, M., Koerner, C., Spoerner, M., and Wittinghofer, A. (2014). Structural insights into the small G-protein Arl13B and implications for Joubert syndrome. Biochem. J. 457, 301–311.10.1042/BJ20131097Suche in Google Scholar PubMed

Milligan, G. (2007). G protein-coupled receptor dimerisation: molecular basis and relevance to function. Biochim. Biophys. Acta 1768, 825–835.10.1016/j.bbamem.2006.09.021Suche in Google Scholar PubMed

Molday, R.S. and Moritz, O.L. (2015). Photoreceptors at a glance. J. Cell Sci. 128, 4039–4045.10.1242/jcs.175687Suche in Google Scholar PubMed PubMed Central

Moritz, O.L., Tam, B.M., Hurd, L.L., Peranen, J., Deretic, D., and Papermaster, D.S. (2001). Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol. Biol. Cell 12, 2341–2351.10.1091/mbc.12.8.2341Suche in Google Scholar PubMed PubMed Central

Nakatsu, F. (2015). A phosphoinositide code for primary cilia. Dev. Cell 34, 379–380.10.1016/j.devcel.2015.08.008Suche in Google Scholar PubMed

Nemet, I., Ropelewski, P., and Imanishi, Y. (2015). Rhodopsin trafficking and mistrafficking: signals, molecular components, and mechanisms. Prog. Mol. Biol. Transl. Sci. 132, 39–71.10.1016/bs.pmbts.2015.02.007Suche in Google Scholar PubMed

Nickell, S., Park, P.S., Baumeister, W., and Palczewski, K. (2007). Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J. Cell Biol. 177, 917–925.10.1083/jcb.200612010Suche in Google Scholar PubMed PubMed Central

Norton, A.W., Hosier, S., Terew, J.M., Li, N., Dhingra, A., Vardi, N., Baehr, W., and Cote, R.H. (2005). Evaluation of the 17-kDa prenyl-binding protein as a regulatory protein for phototransduction in retinal photoreceptors. J. Biol. Chem. 280, 1248–1256.10.1074/jbc.M410475200Suche in Google Scholar PubMed PubMed Central

Nozaki, S., Katoh, Y., Terada, M., Michisaka, S., Funabashi, T.,Takahashi, S., Kontani, K., and Nakayama, K. (2017). Regulation of ciliary retrograde protein trafficking by the Joubert syndrome proteins ARL13B and INPP5E. J. Cell Sci. 130, 563–576.10.1242/jcs.197004Suche in Google Scholar PubMed

Palczewski, K., Kumasaka, T., Hori, T., Behnke, C.A., Motoshima, H., Fox, B.A., Le Trong, I., Teller, D.C., Okada, T., Stenkamp, R.E., et al. (2000). Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739–745.10.1126/science.289.5480.739Suche in Google Scholar PubMed

Papermaster, D.S., Schneider, B.G., Defoe, D., and Besharse, J.C. (1986). Biosynthesis and vectorial transport of opsin on vesicles in retinal rod photoreceptors. J. Histochem. Cytochem. 34, 5–16.10.1177/34.1.2934469Suche in Google Scholar PubMed

Pearring, J.N., Salinas, R.Y., Baker, S.A., and Arshavsky, V.Y. (2013). Protein sorting, targeting and trafficking in photoreceptor cells. Prog. Retin. Eye Res. 36, 24–51.10.1016/j.preteyeres.2013.03.002Suche in Google Scholar PubMed PubMed Central

Pearring, J.N., San Agustin, J.T., Lobanova, E.S., Gabriel, C.J., Lieu, E.C., Monis, W.J., Stuck, M.W., Strittmatter, L., Jaber, S.M., Arshavsky, V.Y., et al. (2017). Loss of Arf4 causes severe degeneration of the exocrine pancreas but not cystic kidney disease or retinal degeneration. PLoS Genet. 13, e1006740.10.1371/journal.pgen.1006740Suche in Google Scholar PubMed PubMed Central

Qureshi, B.M., Schmidt, A., Behrmann, E., Burger, J., Mielke, T., Spahn, C.M.T., Heck, M., and Scheerer, P. (2018). Mechanistic insights into the role of prenyl-binding protein PrBP/delta in membrane dissociation of phosphodiesterase 6. Nat. Commun. 9, 90.10.1038/s41467-017-02569-ySuche in Google Scholar PubMed PubMed Central

Rao, K.N., Zhang, W., Li, L., Anand, M., and Khanna, H. (2016). Prenylated retinal ciliopathy protein RPGR interacts with PDE6d and regulates ciliary localization of Joubert syndrome-associated protein INPP5E. Hum. Mol. Genet. 25, 4533–4545.10.1093/hmg/ddw281Suche in Google Scholar

Rohlich, P. (1975). The sensory cilium of retinal rods is analogous to the transitional zone of motile cilia. Cell Tissue Res. 161, 421–430.10.1007/BF00220009Suche in Google Scholar

Rohrer, B., Lohr, H.R., Humphries, P., Redmond, T.M., Seeliger, M.W., and Crouch, R.K. (2005). Cone opsin mislocalization in Rpe65^−/− mice: a defect that can be corrected by 11-cis retinal. Invest. Ophthalmol. Vis. Sci. 46, 3876–3882.10.1167/iovs.05-0533Suche in Google Scholar

Rosenbaum, J.L. and Witman, G.B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3, 813–825.10.1038/nrm952Suche in Google Scholar

Sahl, S.J., Hell, S.W., and Jakobs, S. (2017). Fluorescence nanoscopy in cell biology. Nat. Rev. Mol. Cell Biol. 18, 685–701.10.1038/nrm.2017.71Suche in Google Scholar

Satoh, A.K., O’Tousa, J.E., Ozaki, K., and Ready, D.F. (2005). Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132, 1487–1497.10.1242/dev.01704Suche in Google Scholar

Schmidt, K., Cavodeassi, F., Feng, Y., and Stephens, D.J. (2013). Early stages of retinal development depend on Sec13 function. Biol. Open 2, 256–266.10.1242/bio.20133251Suche in Google Scholar

Schwarz, N., Hardcastle, A.J., and Cheetham, M.E. (2012). Arl3 and RP2 mediated assembly and traffic of membrane associated cilia proteins. Vision Res. 75, 2–4.10.1016/j.visres.2012.07.016Suche in Google Scholar

Steinberg, R.H., Fisher, S.K., and Anderson, D.H. (1980). Disc morphogenesis in vertebrate photoreceptors. J. Comp. Neurol. 190, 501–508.10.1002/cne.901900307Suche in Google Scholar

Tai, A.W., Chuang, J.Z., Bode, C., Wolfrum, U., and Sung, C.H. (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, 877–887.10.1016/S0092-8674(00)80800-4Suche in Google Scholar

Tam, B.M., Moritz, O.L., Hurd, L.B., and Papermaster, D.S. (2000). Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis. J. Cell Biol. 151, 1369–1380.10.1083/jcb.151.7.1369Suche in Google Scholar PubMed PubMed Central

Thomas, S., Wright, K.J., Le Corre, S., Micalizzi, A., Romani, M., Abhyankar, A., Saada, J., Perrault, I., Amiel, J., Litzler, J., et al. (2014). A homozygous PDE6D mutation in Joubert syndrome impairs targeting of farnesylated INPP5E protein to the primary cilium. Hum. Mutat. 35, 137–146.10.1002/humu.22470Suche in Google Scholar

Tian, G., Ropelewski, P., Nemet, I., Lee, R., Lodowski, K.H., and Imanishi, Y. (2014). An unconventional secretory pathway mediates the cilia targeting of peripherin/rds. J. Neurosci. 34, 992–1006.10.1523/JNEUROSCI.3437-13.2014Suche in Google Scholar

Trivedi, D., Colin, E., Louie, C.M., and Williams, D.S. (2012). Live-cell imaging evidence for the ciliary transport of rod photoreceptor opsin by heterotrimeric kinesin-2. J. Neurosci. 32, 10587–10593.10.1523/JNEUROSCI.0015-12.2012Suche in Google Scholar

Tsang, S.H., Gouras, P., Yamashita, C.K., Kjeldbye, H., Fisher, J., Farber, D.B., and Goff, S.P. (1996). Retinal degeneration in mice lacking the gamma subunit of the rod cGMP phosphodiesterase. Science 272, 1026–1029.10.1126/science.272.5264.1026Suche in Google Scholar

Wang, M. and Casey, P.J. (2016). Protein prenylation: unique fats make their mark on biology. Nat. Rev. Mol. Cell Biol. 17, 110–122.10.1038/nrm.2015.11Suche in Google Scholar

Wang, Y.J., Wang, J., Sun, H.Q., Martinez, M., Sun, Y.X., Macia, E., Kirchhausen, T., Albanesi, J.P., Roth, M.G., and Yin, H.L. (2003). Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299–310.10.1016/S0092-8674(03)00603-2Suche in Google Scholar

Wang, Q., Zhang, X., Zhang, L., He, F., Zhang, G., Jamrich, M., and Wensel, T.G. (2008). Activation-dependent hindrance of photoreceptor G protein diffusion by lipid microdomains. J. Biol. Chem. 283, 30015–30024.10.1074/jbc.M803953200Suche in Google Scholar PubMed PubMed Central

Watzlich, D., Vetter, I., Gotthardt, K., Miertzschke, M., Chen, Y.X., Wittinghofer, A., and Ismail, S. (2013). The interplay between RPGR, PDEdelta and Arl2/3 regulate the ciliary targeting of farnesylated cargo. EMBO Rep. 14, 465–472.10.1038/embor.2013.37Suche in Google Scholar PubMed PubMed Central

Winkler, B.S. (2008). An hypothesis to account for the renewal of outer segments in rod and cone photoreceptor cells: renewal as a surrogate antioxidant. Invest. Ophthalmol. Vis. Sci. 49, 3259–3261.10.1167/iovs.08-1785Suche in Google Scholar PubMed

Winter-Vann, A.M. and Casey, P.J. (2005). Post-prenylation-processing enzymes as new targets in oncogenesis. Nat. Rev. Cancer 5, 405–412.10.1038/nrc1612Suche in Google Scholar PubMed

Ying, G., Gerstner, C.D., Frederick, J.M., Boye, S.L., Hauswirth, W.W., and Baehr, W. (2016). Small GTPases Rab8a and Rab11a are dispensable for rhodopsin transport in mouse photoreceptors. PLoS One 11, e0161236.10.1371/journal.pone.0161236Suche in Google Scholar PubMed PubMed Central

Ying, G., Boldt, K., Ueffing, M., Gerstner, C.D., Frederick, J.M., and Baehr, W. (2018). The small GTPase RAB28 is required for phagocytosis of cone outer segments by the murine retinal pigmented epithelium. J. Biol. Chem. 293, 17546–17558.10.1074/jbc.RA118.005484Suche in Google Scholar PubMed PubMed Central

Young, R.W. (1967). The renewal of photoreceptor cell outer segments. J. Cell Biol. 33, 61–72.10.1083/jcb.33.1.61Suche in Google Scholar PubMed PubMed Central

Zhang, H., Liu, X.H., Zhang, K., Chen, C.K., Frederick, J.M.,Prestwich, G.D., and Baehr, W. (2004). Photoreceptor cGMP phosphodiesterase delta subunit (PDEd) functions as a prenyl-binding protein. J. Biol. Chem. 279, 407–413.10.1074/jbc.M306559200Suche in Google Scholar PubMed

Zhang, H., Li, S., Doan, T., Rieke, F., Detwiler, P.B., Frederick, J.M., and Baehr, W. (2007). Deletion of PrBP/d impedes transport of GRK1 and PDE6 catalytic subunits to photoreceptor outer segments. Proc. Natl. Acad. Sci. USA 104, 8857–8862.10.1073/pnas.0701681104Suche in Google Scholar PubMed PubMed Central

Zhang, H., Fan, J., Li, S., Karan, S., Rohrer, B., Palczewski, K., Frederick, J.M., Crouch, R.K., and Baehr, W. (2008). Trafficking of membrane-associated proteins to cone photoreceptor outer segments requires the chromophore 11-cis-retinal. J. Neurosci. 28, 4008–4014.10.1523/JNEUROSCI.0317-08.2008Suche in Google Scholar PubMed PubMed Central

Zhang, H., Constantine, R., Vorobiev, S., Chen, Y., Seetharaman, J., Huang, Y.J., Xiao, R., Montelione, G.T., Gerstner, C.D., Davis, M.W., et al. (2011). UNC119 is required for G protein trafficking in sensory neurons. Nat. Neurosci. 14, 874–880.10.1038/nn.2835Suche in Google Scholar PubMed PubMed Central

Zhang, H., Constantine, R., Frederick, J.M., and Baehr, W. (2012). The prenyl-binding protein PrBP/delta: a chaperone participating in intracellular trafficking. Vision Res. 75, 19–25.10.1016/j.visres.2012.08.013Suche in Google Scholar PubMed PubMed Central

Zhang, Z., He, F., Constantine, R., Baker, M.L., Baehr, W., Schmid, M.F., Wensel, T.G., and Agosto, M.A. (2015). Domain organization and conformational plasticity of the G protein effector, PDE6. J. Biol. Chem. 290, 17131–17132.10.1074/jbc.A115.647636Suche in Google Scholar PubMed PubMed Central

Zhao, X., Huang, J., Khani, S.C., and Palczewski, K. (1998). Molecular forms of human rhodopsin kinase (GRK1). J. Biol. Chem. 273, 5124–5131.10.1074/jbc.273.9.5124Suche in Google Scholar PubMed