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Protein Networks and Complexes in Photoreceptor Cilia

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Subcellular Proteomics

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References

  • Achenbach, S., Liu, Q. and Pierce E.A. (2004) The RP1 gene and protein in photoreceptor biology. In: Photoreceptor cell biology and inherited retinal degenerations. D.S. Williams, ed. (Singapore: World Scientific Publishing Co. Pte. Ltd.), pp. 223–257.

    Google Scholar 

  • Adato, A., Michel, Y., Kikkawa, Y., Reiners, J., Alagramam, K.N., Weil, D., Yonekawa, H., Wolfrum, U., El Amraoui, A. and Petit, C. (2005) Interactions in the network of Usher syndrome type 1 proteins. Hum. Mol. Genet. 14, 347–356.

    Article  PubMed  CAS  Google Scholar 

  • Arshavsky, V.Y., Lamb, T.D. and Pugh, E.N. Jr. (2002) G proteins and phototransduction. Annu. Rev. Physiol. 64, 153–187.

    Article  PubMed  CAS  Google Scholar 

  • Baker, S.A., Freeman, K., Luby-Phelps, K., Pazour, G.J. and Besharse, J.C. (2003) IFT20 links kinesin II with a mammalian intraflagellar transport complex that is conserved in motile flagella and sensory cilia. J. Biol. Chem. 278, 34211–34218.

    Article  PubMed  CAS  Google Scholar 

  • Baker, S.A., Pazour, G.J., Witman, G.B. and Besharse, J.C. (2004) Photoreceptor and intraflagellar transport. In: Photoreceptor Cell Biology and Inherited Retinal Degenerations. D.S. Williams ed. (Singapore: World Scientific Publishing Co. Pte. Ltd), pp. 109–132.

    Google Scholar 

  • Beales, P.L. (2005) Lifting the lid on Pandora’s box: the Bardet-Biedl syndrome. Curr. Opin. Genet. Dev. 15, 315–323.

    Article  PubMed  CAS  Google Scholar 

  • Beales, P.L., Elcioglu, N., Woolf, A.S., Parker, D. and Flinter, F.A. (1999) New criteria for improved diagnosis of Bardet-Biedl syndrome: results of a population survey. J. Med. Genet. 36, 437–446.

    PubMed  CAS  Google Scholar 

  • Berson, E.L. (1993) Retinitis pigmentosa. The Friedenwald lecture. Invest. Ophthalmol. Vis. Sci 34, 1659–1676.

    PubMed  CAS  Google Scholar 

  • Besharse, J.C., Baker, S.A., Luby-Phelps, K. and Pazour, G.J. (2003a) Photoreceptor intersegmental transport and retinal degeneration: a conserved pathway common to motile and sensory cilia. Adv. Exp. Med. Biol. 533, 157–164.

    PubMed  CAS  Google Scholar 

  • Besharse, J.C., Fogerty, J., Baker, S., Link, B., Pazour, G.J. and Luby-Phelps, K. (2003b) Expression of IFT proteins in vertebrate rod photoreceptors. ARVO Abstract 2863/B702.

    Google Scholar 

  • Besharse, J.C. and Horst, C.J. (1990) The photoreceptor connecting cilium - a model for the transitiontone. In: Ciliary and Flagellar Membranes. R.A. Bloodgood, ed. (New York: Plenum), pp. 389–417.

    Google Scholar 

  • Blacque, O.E. and Leroux, M.R. (2006) Bardet-Biedl syndrome: an emerging pathomechanism of intracellular transport. Cell. Mol. Life Sci. 63, 2145–2161.

    Article  PubMed  CAS  Google Scholar 

  • Boeda, B., El-Amraoui, A., Bahloul, A., Goodyear, R., Daviet, L., Blanchard, S., Perfettini, I., Fath, K.R., Shorte, S., Reiners, J., Houdusse, A., Legrain, P., Wolfrum, U., Richardson, G. and Petit, C. (2002) Myosin VIIa, harmonin and cadherin 23, three Usher 1 gene products that cooperate to shape the sensory hair cell bundle. EMBO J. 21, 6689–6699.

    Article  PubMed  CAS  Google Scholar 

  • Boylan, J.P. and Wright, A.F. (2000) Identification of a novel protein interacting with RPGR. Hum. Mol. Genet. 9, 2085–2093.

    Article  PubMed  CAS  Google Scholar 

  • Chang, B., Khanna, H., Hawes, N., Jimeno, D., He, S., Lillo, C., Parapuram, S.K., Cheng, H., Scott, A., Hurd, R.E., Sayer, J.A., Otto, E.A., Attanasio, M., O’Toole, J.F., Jin, G., Shou, C., Hildebrandt, F., Williams, D.S., Heckenlively, J.R. and Swaroop, A. (2006) In-frame deletion in a novel centroso- mal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum. Mol. Genet. 15, 1847–1857.

    Article  PubMed  CAS  Google Scholar 

  • Chishti, A.H., Kim, A.C., Marfatia, S.M., Lutchman, M., Hanspal, M., Jindal, H., Liu, S.C., Low, P.S., Rouleau, G.A., Mohandas, N., Chasis, J.A., Conboy, J.G., Gascard, P., Takakuwa, Y., Huang, S.C., Benz, E.J., Bretscher, A., Fehon, R.G., Gusella, A.F., Ramesh, V., Solomon, F., Marchesi, V.T., Tsukita, S., Arpin, M.,. Louvard, D., Tonks, N.K., Anderson, J.M., Fanning, A.S., Bryant, P.J., Woods, D.F. and Hoover, K.B. (1998) The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem. Sci. 23, 281–282.

    Article  PubMed  CAS  Google Scholar 

  • Cole, D.G., Diener, D.R., Himelblau, A.L., Beech, P.L., Fuster, J.C. and Rosenbaum, J.L. (1998) Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141, 993–1008.

    Article  PubMed  CAS  Google Scholar 

  • Cremers, F.P., van den Hurk, J.A. and den Hollander, A.I. (2002) Molecular genetics of Leber congenital amaurosis. Hum. Mol. Genet. 11, 1169–1176.

    Article  PubMed  CAS  Google Scholar 

  • den Hollander, A.I., Koenekoop, R.K., Yzer, S., Lopez, I., Arends, M.L., Voesenek, K.E., Zonneveld, M.N., Strom, T.M., Meitinger, T., Brunner, H.G., Hoyng, C.B., van den Born, L.I., Rohrschneider, K. and Cremers, F.P.M. (2006) Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber Congenital Amaurosis. Am. J. Hum. Genet. 79, 556–561.

    Article  PubMed  CAS  Google Scholar 

  • Deretic, D. (2004) From the golgi to the rod outer segment: formation, movement, docking and fusion of rhodopsin transport carriers. In: Photoreceptor Cell Biology and Inherited Retinal Degeneration. D.S. Williams, ed. (Singapore: World Scientific Publishing Co. Pte. Ltd.), pp. 29–64.

    Google Scholar 

  • Deretic, D., Huber, L.A., Ransom, N., Mancini, M., Simons, K. and Papermaster, D.S. (1995) Rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. J. Cell Sci. 108, 215–224.

    PubMed  CAS  Google Scholar 

  • Ebermann, I., Scholl, H.P., Charbel Issa, P., Becirovic, E., Lamprecht, J., Jurklies, B., Millan, J.M., Aller, E., Mitter, D. and Bolz, H. (2007) A novel gene for Usher syndrome type 2: mutations in the long isoform of whirlin are associated with retinitis pigmentosa and sensorineural hearing loss. Hum. Genet. 121, 203–211.

    Article  PubMed  CAS  Google Scholar 

  • Ferreira, P.A. (2005) Insights into X-linked retinitis pigmentosa type 3, allied diseases and underlying pathomechanisms. Hum. Mol. Genet. 14, R259-R267.

    Article  PubMed  CAS  Google Scholar 

  • Fliegauf, M. and Omran, H. (2006) Novel tools to unravel molecular mechanisms in cilia-related disorders. Trends Genet. 22, 241–245.

    Article  PubMed  CAS  Google Scholar 

  • Fotiadis, D., Jastrzebska, B., Philippsen, A., Muller, D.J., Palczewski, K. and Engel, A. (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr. Opin. Struct. Biol. 16, 252–259.

    Article  PubMed  CAS  Google Scholar 

  • Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D.A., Engel, A. and Palczewski, K. (2003) Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 421, 127–128.

    Article  PubMed  CAS  Google Scholar 

  • Gerber, S., Bonneau, D., Gilbert, B., Munnich, A., Dufier, J.L., Rozet, J.M. and Kaplan, J. (2006) USH1A: Chronicle of a Slow Death. Am. J. Hum. Genet. 78, 357–359.

    Article  PubMed  CAS  Google Scholar 

  • Giessl, A., Pulvermüller, A., Trojan, P., Park, J.H., Choe, H.-W., Ernst, O.P., Hofmann, K.P. and Wolfrum, U. (2004a) Differential expression and interaction with the visual G-protein transducin of centrin isoforms in mammalian photoreceptor cells. J. Biol. Chem. 279, 51472–51481.

    Article  PubMed  CAS  Google Scholar 

  • Giessl, A., Trojan, P., Pulvermüller, A. and Wolfrum, U. (2004b) Centrins, potential regulators of transducin translocation in photoreceptor cells. In: Photoreceptor Cell Biology and Inherited Retinal Degenerations. D.S. Williams, ed. (Singapore: World Scientific Publishing Co. Pte. Ltd.), pp. 195–222.

    Google Scholar 

  • Giessl, A., Trojan, P., Rausch, S., Pulvermüller, A. and Wolfrum, U. (2006) Centrins, gatekeepers for the light-dependent translocation of transducin through the photoreceptor cell connecting cilium. Vision Res. 46, 4502–4509.

    Article  PubMed  CAS  Google Scholar 

  • Green, J.S., Parfrey, P.S., Harnett, J.D., Farid, N.R., Cramer, B.C., Johnson, G., Heath, O., McManamon, P.J., O’Leary, E. and Pryse-Phillips, W. (1989) The cardinal manifestations of Bardet-Biedl syndrome, a form of Laurence-Moon-Biedl syndrome. N. Engl. J. Med. 321, 1002–1009.

    Article  PubMed  CAS  Google Scholar 

  • Hallett, M.A., Delaat, J.L., Arikawa, K., Schlamp, C.L., Kong, F.S. and Williams, D.S. (1996) Distribution of guanylate cyclase within photoreceptor outer segments. J. Cell Sci. 109, 1803–1812.

    PubMed  CAS  Google Scholar 

  • Hildebrandt, F and Otto, E. (2005) Cilia and centrosomes: a unifying pathogenic concept for cystic kidney disease? Nat. Rev. Genet. 6, 928–940.

    Article  PubMed  CAS  Google Scholar 

  • Hofmann, K.P., Spahn, C.M., Heinrich, R. and Heinemann, U. (2006) Building functional modules from molecular interactions. Trends Biochem. Sci. 31, 497–508.

    Article  PubMed  CAS  Google Scholar 

  • Hollander, B.A., Liang, M.-Y. and Besharse, J.C. (1999) Linkage of a nucleolin-related protein and casein kinase II with the detergent-stable photoreceptor cytoskeleton. Cell Motil. Cytoskeleton 43, 114–127.

    Article  PubMed  CAS  Google Scholar 

  • Hong, D.H., Pawlyk, B., Sokolov, M., Strissel, K.J., Yang, J., Tulloch, B., Wright, A.F., Arshavsky, V.Y. and Li, T. (2003) RPGR isoforms in photoreceptor connecting cilia and the transitional zone of motile cilia. Invest. Ophthalmol. Vis. Sci. 44, 2413–2421.

    Article  PubMed  Google Scholar 

  • Hong, D.H., Yue, G., Adamian, M. and Li, T. (2001) Retinitis pigmentosa GTPase regulator (RPGRr)- interacting protein is stably associated with the photoreceptor ciliary axoneme and anchors RPGR to the connecting cilium. J. Biol. Chem. 276, 12091–12099.

    Article  PubMed  CAS  Google Scholar 

  • Horst, C.J., Forestner, D.M. and Besharse, J.C. (1987) Cytoskeletal-membrane interactions: Between cell surface glycoconjugates and doublet microtubules of the photoreceptor connecting cilium. J. Cell Biol. 105, 2973–2987.

    Article  PubMed  CAS  Google Scholar 

  • Horst, C.J., Johnson, L.V. and Besharse, J.C. (1990) Transmembrane assemblage of the photoreceptor connecting cilium and motile cilium transition zone contain a common immunologic epitope. Cell Motil. Cytoskeleton 17, 329–344.

    Article  PubMed  CAS  Google Scholar 

  • Iannaccone, A., Breuer, D.K., Wang, X.F., Kuo, S.F., Normando, E.M., Filippova, E., Baldi, A., Hiriyanna, S., MacDonald, C.B., Baldi, F., Cosgrove, D., Morton, C.C., Swaroop, A. and Jablonski, M.M. (2003) Clinical and immunohistochemical evidence for an X linked retinitis pigmentosa syndrome with recurrent infections and hearing loss in association with an RPGR mutation. J. Med. Genet. 40, e118.

    Article  PubMed  CAS  Google Scholar 

  • Iannaccone, A., Wang, X., Jablonski, M.M., Kuo, S.F., Baldi, A., Cosgrove, D., Morton, C.C. and Swaroop, A. (2004) Increasing evidence for syndromic phenotypes associated with RPGR mutations. Am. J. Ophthalmol. 137, 785–786.

    PubMed  Google Scholar 

  • Joubert, M., Eisenring, J.J., Robb, J.P. and Andermann, F. (1969) Familial agenesis of the cerebellar vermis. A syndrome of episodic hyperpnea, abnormal eye movements, ataxia, and retardation. Neurology 19, 813–825.

    PubMed  CAS  Google Scholar 

  • Kajimura, N., Harada, Y. and Usukura, J. (2000) High-resolution freeze-etching replica images of the disk and the plasma membrane surfaces in purified bovine rod outer segments. J. Electron Microsc. 49, 691–697.

    CAS  Google Scholar 

  • Kang, K., Bauer, P.J., Kinjo, T.G., Szerencsei, R.T., Bonigk, W., Winkfein, R.J. and Schnetkamp, P.P. (2003) Assembly of retinal rod or cone Na(+)/Ca(2+)-K(+) exchanger oligomers with cGMP-gated channel subunits as probed with heterologously expressed cDNAs. Biochemistry 42, 4593–4600.

    Article  PubMed  CAS  Google Scholar 

  • Kaplan, M.W., Iwata, R.T. and Sears, R.C. (1987) Lengths of immunolabeled ciliary microtubules in frog photoreceptor outer segments. Exp. Eye Res. 44, 623–632.

    Article  PubMed  CAS  Google Scholar 

  • Kaupp, U.B. and Seifert, R. (2002) Cyclic nucleotide-gated ion channels. Physiol. Rev. 82, 769–824.

    PubMed  CAS  Google Scholar 

  • Khanna, H., Hurd, T.W., Lillo, C., Shu, X., Parapuram, S.K., He, S., Akimoto, M., Wright, A.F., Margolis, B., Williams, D.S. and Swaroop, A. (2005) RPGR-ORF15, which is mutated in retinitis pigmentosa, associates with SMC1, SMC3, and microtubule transport proteins. J. Biol. Chem. 280, 33580–33587.

    Article  PubMed  CAS  Google Scholar 

  • Körschen, H.G., Beyermann, M., Müller, F., Heck, M., Vantler, M., Koch, K.W., Kellner, R., Bode, C., Wolfrum, U., Hofmann, K.P. and Kaupp, U.B. (1999) Interaction of glutamic acid-rich proteins with components of the cGMP-signaling pathway in rod photoreceptors. Nature 400, 761–766.

    Article  PubMed  Google Scholar 

  • Kozminski, K.G., Beech, P.L. and Rosenbaum, J.L. (1995) The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J. Cell Biol. 131, 1517–1527.

    Article  PubMed  CAS  Google Scholar 

  • Kremer, H., van Wijk, E., Märker, T., Wolfrum, U. and Roepman, R. (2006) Usher syndrome: molecular links of pathogenesis, proteins and pathways. Hum. Mol. Genet. 15(Supp. 12), R262-R270.

    Article  PubMed  CAS  Google Scholar 

  • Küssel-Andermann, P., El-Amraoui, A., Safieddine, S., Nouaille, S., Perfettini, I., Lecuit, M., Cossart, P., Wolfrum, U. and Petit, C. (2000) Vezatin, a novel transmembrane protein, bridges myosin VIIA to the cadherin-catenins complex. EMBO J. 19, 6020–6029.

    Article  PubMed  Google Scholar 

  • Li, J.B., Gerdes, J.M., Haycraft, C.J., Fan, Y., Teslovich, T.M., May-Simera, H., Li, H., Blacque, O.E., Li, L., Leitch, C.C., Lewis, R.A., Green, J.S., Parfrey, P.S., Leroux, M.R., Davidson, W.S., Beales, P.L., Guay-Woodford, L.M., Yoder, B.K., Stormo, G.D., Katsanis, N. and Dutcher, S.K. (2004b) Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117, 541–552.

    Article  PubMed  CAS  Google Scholar 

  • Li, M., Sun, J., Baker, S., Freeman, K. and Besharse, J.C. (2004a) The intraflagellar transport protein, IFT88, directly interacts with the chaperone protein MRJ in photoreceptors. ARVO Abstract 3650/B111.

    Google Scholar 

  • Lillo, C., Siemens, J., Kazmierczak, P., Mueller, U. and Williams, D.S. (2005) Roles and interactions of three USH1 proteins in the retina and inner ear. ARVO Abstract 46/5176.

    Google Scholar 

  • Linari, M., Ueffing, M., Manson, F., Wright, A., Meitinger, T. and Becker, J. (1999) The retinitis pigmentosa GTPase regulator, RPGR, interacts with the delta subunit of rod cyclic GMP phosphodiesterase. Proc. Natl Acad. Sci. U.S.A. 96, 1315–1320.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Q., Tan, G., Lenenkova, N., Rux, J., Speicher, D.W. and Pierce, E. (2006) The proteome of mammalian sensory cilium, the mouse photoreceptor outer segment. ARVO Abstract 3725/B368.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Liu, X.R., Vansant, G., Udovichenko, I.P., Wolfrum, U. and Williams, D.S. (1997) Myosin VIIa, the product of the Usher 1B syndrome gene, is concentrated in the connecting cilia of photoreceptor cells. Cell Motil. Cytoskeleton 37, 240–252.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Q., Zhou, J., Daiger, S.P., Farber, D.B., Heckenlively, J.R., Smith, J.E., Sullivan, L.S., Zuo, J., Milam, A.H. and Pierce, E.A. (2002) Identification and subcellular localization of the RP1 protein in human and mouse photoreceptors. Invest. Ophthalmol. Vis. Sci. 43, 22–32.

    PubMed  Google Scholar 

  • Liu, X., Bulgakov, O.V., Darrow, K.N., Pawlyk, B., Adamian, M., Liberman, M.C. and Li, T. (2007) A novel gene for Usher syndrome type 2: mutations in the long isoform of whirlin are associated with retinitis pigmentosa and sensorineural hearing loss. Proc. Natl. Acad. Sci. U.S.A. 104, 4413–4418.

    Article  PubMed  CAS  Google Scholar 

  • Marszalek, J.R., Liu, X., Roberts, E.A., Chui, D., Marth, J.D., Williams, D.S., Goldstein and L.S,. (2000) Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102, 175–187.

    Article  PubMed  CAS  Google Scholar 

  • McGee, J., Goodyear, R.J., McMillan, D.R., Stauffer, E.A., Holt, J.R., Locke, K.G., Birch, D.G., Legan, P.K., White, P.C., Walsh, E.J. and Richardson, G.P. (2006) The very large G-protein-coupled receptor VLGR1: a component of the ankle link complex required for the normal development of auditory hair bundles. J. Neurosci. 26, 6543–6553.

    Article  PubMed  CAS  Google Scholar 

  • Meindl, A., Dry, K., Herrmann, K., Manson, F., Ciccodicola, A., Edgar, A., Carvalho, M.R., Achatz, H., Hellebrand, H., Lennon, A., Migliaccio, C., Porter, K., Zrenner, E., Bird, A., Jay, M., Lorenz, B., Wittwer, B., D’Urso, M., Meitinger, T. and Wright, A. (1996) A gene (RPGR) with homology to the RCC1 guanine nucleotide exchange factor is mutated in X-linked retinitis pigmentosa (RP3). Nat. Genet. 13, 35–42.

    Article  PubMed  CAS  Google Scholar 

  • Molday, R.S. (2004) Molecular organization of rod outer segments. In: Photoreceptor Cell Biology and Inherited Retinal Degenerations. D.S. Williams, ed. (Singapore: World Scientific Publishing Co. Pte. Ltd.), pp. 259–300.

    Google Scholar 

  • Molday, R.S. and Kaupp, U.B. (2000) Ion channels of vertebrate photoreceptors. In: Molecular Mechanism in Visual Transduction. D.G. Stavenga, W.J. Degrip and E.N. Pugh Jr., eds. (Amsterdam: Elsevier Science Publishers B.V.), pp. 143–182.

    Google Scholar 

  • Mollet, G., Salomon, R., Gribouval, O., Silbermann, F., Bacq, D., Landthaler, G., Milford, D., Nayir, A., Rizzoni, G., Antignac, C. and Saunier, S. (2002) The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin. Nat. Genet. 32, 300–305.

    Article  PubMed  CAS  Google Scholar 

  • Mollet, G., Silbermann, F., Delous, M., Salomon, R., Antignac, C. and Saunier, S. (2005) Characterization of the nephrocystin/nephrocystin-4 complex and subcellular localization of nephrocystin-4 to primary cilia and centrosomes. Hum. Mol. Genet. 14, 645–656.

    Article  PubMed  CAS  Google Scholar 

  • Montell, C. (1999) Visual transduction in Drosophila. Annu. Rev. Cell Dev. Biol. 15, 231–268.

    Article  PubMed  CAS  Google Scholar 

  • Moore, A., Escudier, E., Roger, G., Tamalet, A., Pelosse, B., Marlin, S., Clement, A., Geremek, M., Delaisi, B., Bridoux, A.M., Coste, A., Witt, M., Duriez, B. and Amselem, S. (2006) RPGR is mutated in patients with a complex X linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa. J. Med. Genet. 43, 326–333.

    Article  PubMed  CAS  Google Scholar 

  • Moore, S.J., Green, J.S., Fan, Y., Bhogal, A.K., Dicks, E., Fernandez, B.A., Stefanelli, M., Murphy, C., Cramer, B.C., Dean, J.C., Beales, P.L., Katsanis, N., Bassett, A.S., Davidson, W.S. and Parfrey, P.S. (2005) Clinical and genetic epidemiology of Bardet-Biedl syndrome in Newfoundland: a 22-year prospective, population-based, cohort study. Am. J. Med. Genet. A 132, 352–360

    PubMed  Google Scholar 

  • Muresan, V., Joshi, H.C. and Besharse, J.C. (1993) Gamma-tubulin in differented cell types: Localization in vicinity of basal bodies in retinal photoreceptors and ciliated epithelia. J. Cell. Sci. 104, 1229–1237.

    PubMed  CAS  Google Scholar 

  • Nakatani, K., Chen, C., Yau, K.W. and Koutalos, Y. (2002) Calcium and phototransduction. In: Photoreceptors and Calcium. W. Baehr and K. Palczewski, eds. (New York: Kluwer Academic/Plenum Publishers and Landes Biosciences/Eureka.com), pp. 1–20.

    Google Scholar 

  • Okada, T., Ernst, O.P., Palczewski, K. and Hofmann, K.P. (2001) Activation of rhodopsin: new insights from structural and biochemical studies. Trends Biochem. Sci. 26, 318–324.

    Article  PubMed  CAS  Google Scholar 

  • Olbrich, H., Fliegauf, M., Hoefele, J., Kispert, A., Otto, E., Volz, A., Wolf, M.T., Sasmaz, G., Trauer, U., Reinhardt, R., Sudbrak, R., Antignac, C., Gretz, N., Walz, G., Schermer, B., Benzing, T., Hildebrandt, F. and Omran, H. (2003) Mutations in a novel gene, NPHP3, cause adolescent nephronophthisis, tapetoretinal degeneration and hepatic fibrosis. Nat. Genet. 34, 455–459.

    Article  PubMed  CAS  Google Scholar 

  • Orozco, J.T., Wedaman, K.P., Signor, D., Brown, S., Rose, L. and Scholey, J.M, (1999) Movement of motor and cargo along cilia. Nature 398, 674.

    Article  PubMed  CAS  Google Scholar 

  • Otto, E., Hoefele, J., Ruf, R., Mueller, A.M., Hiller, K.S., Wolf, M.T., Schuermann, M.J., Becker, A., Birkenhager, R., Sudbrak, R., Hennies, H.C., Nurnberg, P. and Hildebrandt, F. (2002) A gene mutated in nephronophthisis and retinitis pigmentosa encodes a novel protein, nephroretinin, conserved in evolution. Am. J. Hum. Genet. 71, 1161–1167.

    Article  PubMed  CAS  Google Scholar 

  • Otto, E.A., Loeys, B., Khanna, H., Hellemans, J., Sudbrak, R., Fan, S., Muerb, U., O’Toole, J.F., Helou, J., Attanasio, M., Utsch, B., Sayer, J.A., Lillo, C., Jimeno, D., Coucke, P., de Paepe, A., Reinhardt, R., Klages, S., Tsuda, M., Kawakami, I., Kusakabe, T., Omran, H., Imm, A., Tippens, M., Raymond, P.A., Hill, J., Beales, P., He, S., Kispert, A., Margolis, B., Williams, D.S., Swaroop, A. and Hildebrandt, F. (2005) Nephrocystin-5, a ciliary IQ domain protein, is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nat. Genet. 37, 282–288.

    Article  PubMed  CAS  Google Scholar 

  • Otto, E.A., Schermer, B., Obara, T., O’Toole, J.F., Hiller, K.S., Mueller, A.M., Ruf, R.G., Hoefele, J., Beekmann, F., Landau, D., Foreman, J.W., Goodship, J.A., Strachan, T., Kispert, A., Wolf, M.T., Gagnadoux, M.F., Nivet, H., Antignac, C., Walz, G., Drummond, I.A., Benzing, T. and Hildebrandt, F. (2003) Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nat. Genet. 34, 413–420.

    Article  PubMed  CAS  Google Scholar 

  • Pagh-Roehl, K., Wang, E. and Burnside, B. (1992) Shortening of the calycal process actin cytoskeleton is correlated with myoid elongation in teleost rods. Exp. Eye Res. 55, 735–746.

    Article  PubMed  CAS  Google Scholar 

  • Pan, J. and Snell, W.J. (2003) Kinesin II and regulated intraflagellar transport of Chlamydomonas aurora protein kinase. J. Cell. Sci. 116, 2179–2186.

    Article  PubMed  CAS  Google Scholar 

  • Pan, J., Wang, Q. and Snell, W.J. (2005) Cilium-generated signaling and cilia-related disorders. Lab. Invest. 85, 452–463.

    Article  PubMed  CAS  Google Scholar 

  • Papermaster, D.S. (2002) The birth and death of photoreceptors: the Friedenwald lecture. Invest. Ophthalmol. Vis. Sci. 43, 1300–1309.

    PubMed  Google Scholar 

  • Papermaster, D.S., Schneider, B.G. and Besharse, J.C. (1985) Vesicular transport of newly synthesized opsin from the Golgi apparatus toward the rod outer segment. Invest. Ophthalmol. Vis. Sci. 26, 1386–1404.

    PubMed  CAS  Google Scholar 

  • Park, J.H., Pulvermüller, A., Scheerer, P., Rausch, S., Giessl, A., Höhne, W., Wolfrum, U., Hofmann, K.P., Ernst, O.P., Choe, H.-W. and Krauss, N. (2006) Insights into functional aspects of centrins from the structure of N-terminally extended mouse centrin 1. Vision Res. 46, 4568–4574.

    Article  PubMed  CAS  Google Scholar 

  • Pazour, G.J., Baker, S.A., Deane, J.A., Cole, D.G., Dickert, B.L., Rosenbaum, J.L., Witman, G.B. and Besharse, J.C. (2002) The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J. Cell Biol. 157, 103–113.

    Article  PubMed  CAS  Google Scholar 

  • Pazour, G.J., Dickert, B.L., Vucica, Y., Seeley, E.S., Rosenbaum, J.L., Witman, G.B.and Cole, D.G. (2000) Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease Tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151, 709–718.

    Article  PubMed  CAS  Google Scholar 

  • Pazour, G.J., Dickert, B.L. and Witman, G.B. (1999) The DHClb (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. 144, 473–481.

    Article  PubMed  CAS  Google Scholar 

  • Pedersen, L.B., Miller, M.S., Geimer, S., Leitch, J.M., Rosenbaum, J.L. and Cole, D.G. (2005) Chlamydomonas IFT172 is encoded by FLA11, interacts with CrEBl, and regulates IFT at the flagellar tip. Curr. Biol. 15, 262–266.

    Article  PubMed  CAS  Google Scholar 

  • Piperno, G. and Mead, K. (1997) Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella. Proc. Natl Acad. Sci. U.S.A. 94, 4457–4462.

    Article  PubMed  CAS  Google Scholar 

  • Poetsch, A., Molday, L.L. and Molday, R.S. (2001) The cGMP-gated channel and related glutamic acidrich proteins interact with peripherin-2 at the rim region of rod photoreceptor disc membranes. J. Biol. Chem. 276, 48009–48016.

    PubMed  CAS  Google Scholar 

  • Pugh, E.N. Jr. and Lamb, T. (2000) Photo transducin in vertebrate rods and cones: Molecular mechanism of amplification, recovery and light adaptation. In: Molecular Mechanism in Visual Transduction. D.G. Stavenga, W.J. Degrip and E.N. Pugh Jr., eds. (Amsterdam, The Netherlands: Elsevier Science Publishers B.V.), pp. 183–255.

    Google Scholar 

  • Pulvermüller, A., Giessl, A., Heck, M., Wottrich, R., Schmitt, A., Ernst, O.P., Choe, H.-W., Hofmann, K.P. and Wolfrum, U. (2002) Calcium dependent assembly of centrin/G-protein complex in photoreceptor cells. Mol. Cell. Biol. 22, 2194–2203.

    Article  PubMed  CAS  Google Scholar 

  • Qin, H., Diener, D.R., Geimer, S., Cole, D.G. and Rosenbaum, J.L. (2004) Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J. Cell Biol. 164, 255–266.

    Article  PubMed  CAS  Google Scholar 

  • Qin, H., Rosenbaum, J.L. and Barr, M.M. (2001) An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr. Biol. 11, 457–461.

    CAS  Google Scholar 

  • Rattner, A., Chen, J. and Nathans, J. (2004) Proteolytic shedding of the extracellular domain of photoreceptor cadherin. Implications for outer segment assembly. J. Biol. Chem. 279, 42202–42210.

    Article  PubMed  CAS  Google Scholar 

  • Rattner, A., Smallwood, P.M., Williams, J., Cooke, C., Savchenko, A., Lyubarsky, A., Pugh, E.N. and Nathans, J. (2001) A photoreceptor-specific cadherin is essential for the structural integrity of the outer segment and for photoreceptor survival. Neuron 32, 775–786.

    Article  PubMed  CAS  Google Scholar 

  • Reiners, J., Marker, T., Jurgens, K., Reidel, B. and Wolfrum, U. (2005a) Photoreceptor expression of the Usher syndrome type 1 protein protocadherin 15 (USH1F) and its interaction with the scaffold protein harmonin (USH1C). Mol. Vis. 11, 347–355.

    PubMed  CAS  Google Scholar 

  • Reiners, J., Nagel-Wolfrum, K., Jurgens, K., Märker, T. and Wolfrum, U. (2006) Molecular basis of human Usher syndrome: deciphering the meshes of the Usher protein network provides insights into the pathomechanisms of the Usher disease. Exp. Eye Res. 83, 97–119.

    Article  PubMed  CAS  Google Scholar 

  • Reiners, J., Reidel, B., El-Amraoui, A., Boeda, B., Huber, I., Petit, C. and Wolfrum, U. (2003) Differential distribution of harmonin isoforms and their possible role in Usher-1 protein complexes in mammalian photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 44, 5006–5015.

    Article  PubMed  Google Scholar 

  • Reiners, J., van Wijk, E., Marker, T., Zimmermann, U., Jurgens, K., te, B.H., Overlack, N., Roepman, R., Knipper, M., Kremer, H. and Wolfrum, U. (2005b) Scaffold protein harmonin (USH1C) provides molecular links between Usher syndrome type 1 and type 2. Hum. Mol. Genet. 14, 3933–3943.

    Article  PubMed  CAS  Google Scholar 

  • Roepman, R., Bauer, D., Rosenberg, T., van Duynhoven, G., van de Vosse, E., Platzer, M., Rosenthal, A., Ropers, H.-H., Cremers, F.P.M. and Berger, W. (1996a) Identification of a gene disrupted by a microdeletion in a patient with X-linked retinitis pigmentosa. Hum. Mol. Genet. 5, 827–833.

    Article  PubMed  CAS  Google Scholar 

  • Roepman, R., Bernoud-Hubac, N., Schick, D.E., Maugeri, A., Berger, W., Ropers, H.H., Cremers, F.P.M. and Ferreira, P.A. (2000a) The retinitis pigmentosa GTPase regulator (RPGR) interacts with novel transport-like proteins in the outer segments of rod photoreceptors. Hum. Mol. Genet. 9, 2095–2105.

    Article  PubMed  CAS  Google Scholar 

  • Roepman, R., Letteboer, S.J.F., Arts, H.H., van Beersum, S.E.C., Lu, X., Krieger, E., Ferreira, P.A. and Cremers, F.P.M. (2005) Interaction of nephrocystin-4 and RPGRIPl is disrupted by nephronophthisis or Leber congenital amaurosis-associated mutations. Proc. Natl Acad. Sci. U.S.A. 102, 18520–18525.

    Article  PubMed  CAS  Google Scholar 

  • Roepman, R., Schick, D. and Ferreira, P.A. (2000b) Isolation of retinal proteins that interact with retinitis pigmentosa GTPase regulator by interaction trap screen in yeast. Meth. Enzymol. 316, 688–704.

    PubMed  CAS  Google Scholar 

  • Roepman, R., van Duynhoven, G., Rosenberg, T., Pinckers, A.J.L.G., Bleeker-Wagemakers, E.M., Bergen, A.A.B., Post, J., Beck, A., Reinhardt, R., Ropers, H.-H., Cremers, F.P.M. and Berger, W. (1996b) Positional cloning of the gene for X-linked retinitis pigmentosa: homology with the guanine-nucleotide-exchange factor RCC1. Hum. Mol. Genet. 5, 1035–1041.

    Article  PubMed  CAS  Google Scholar 

  • Röhlich, P. (1975) The sensory cilium of retinal rods is analogous to the transitional zone of motile cilia. Cell Tissue Res. 161, 421–430.

    Article  PubMed  Google Scholar 

  • Rosenbaum, J.L. and Witman, G.B. (2002) Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3, 813–825.

    Article  PubMed  CAS  Google Scholar 

  • Salisbury, J.L. (1995) Centrin, centrosomes, and mitotic spindle poles. Curr. Opin. Cell Biol. 7, 39–45.

    Article  PubMed  CAS  Google Scholar 

  • Sayer, J.A., Otto, E.A., O’Toole, J.F., Nurnberg, G., Kennedy, M.A., Becker, C., Hennies, H.C., Helou, J., Attanasio, M., Fausett, B.V., Utsch, B., Khanna, H., Liu. Y., Drummond, I., Kawakami, I., Kusakabe, T., Tsuda, M., Ma, L., Lee, H., Larson, R.G., Allen, S.J., Wilkinson, C.J., Nigg, E.A., Shou, C., Lillo, C., Williams, D.S., Hoppe, B., Kemper, M.J., Neuhaus, T., Parisi, M.A., Glass, I.A., Petry, M., Kispert, A., Gloy, J., Ganner, A., Walz, G., Zhu, X., Goldman, D., Nurnberg, P., Swaroop, A., Leroux, M.R. and Hildebrandt, F. (2006) The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat. Genet. 38, 674–681.

    Article  PubMed  CAS  Google Scholar 

  • Schiebel, E. and Bornens, M. (1995) In search of a function for centrins. Trends Cell Biol. 5, 197–201.

    Article  PubMed  CAS  Google Scholar 

  • Schmitt, A. and Wolfrum, U. (2001) Identification of novel molecular components of the photoreceptor connecting cilium by immunoscreens. Exp. Eye Res. 73, 837–849.

    Article  PubMed  CAS  Google Scholar 

  • Scholey, J.M. and Anderson, K.V. (2006) Intraflagellar transport and cilium-based signaling. Cell 125, 439–442.

    Article  PubMed  CAS  Google Scholar 

  • Schrem, A., Lange, C., Beyermann, M. and Koch, K.W. (1999) Identification of a domain in guanylyl cyclase-activating protein 1 that interacts with a complex of guanylyl cyclase and tubulin in photoreceptors. J. Biol. Chem. 274, 6244–6249.

    Article  PubMed  CAS  Google Scholar 

  • Schwarzer, A., Schauf, H. and Bauer, P.J. (2000) Binding of the cGMP-gated channel to the Na/Ca-K exchanger in rod photoreceptors. J. Biol. Chem. 275, 13448–13454.

    Article  PubMed  CAS  Google Scholar 

  • Shu, X., Fry, A.M., Tulloch, B., Manson, F.D., Crabb, J.W., Khanna, H., Faragher, A.J., Lennon, A., He, S., Trojan, P., Giessl, A., Wolfrum, U., Vervoort, R., Swaroop, A. and Wright, A.F. (2005) RPGR ORF15 isoform co-localizes with RPGRIP1 at centrioles and basal bodies and interacts with nucleophosmin. Hum. Mol. Genet. 14, 1183–1197.

    Article  PubMed  CAS  Google Scholar 

  • Singla, V. and Reiter, J.F. (2006) The primary cilium as the cell’s antenna: signaling at a sensory organelle. Science 313, 629–633.

    Article  PubMed  CAS  Google Scholar 

  • Smith, C. and Graham, J. (1945) Congenital medullary cysts of the kidneys with severe refractory anemia. Am. J. Dis. Child. 69, 369–377.

    Google Scholar 

  • Sokolov, M., Lyubarsky, A.L., Strissel, K.J., Savchenko, A.B., Govardovskii, V.I., Pugh. E.N. Jr. and Arshavsky, V.Y. (2002) Massive light-driven translocation of transducin between the two major compartments of rod cells: a novel mechanism of light adaptation. Neuron 33, 95–106.

    Article  Google Scholar 

  • Spira, A.W. and Milman, G.E. (1979) The structure and distribution of the cross-striated fibril and associated membranes in guinea pig photoreceptors. Am. J. Anat. 155, 319–337.

    Article  PubMed  CAS  Google Scholar 

  • Steinberg, R.H., Fisher, S.K. and Anderson, D.H. (1980) Disc Morphogenesis in Vertebrate Photoreceptors. J. Comp. Neurol. 190, 501–518.

    Article  PubMed  CAS  Google Scholar 

  • Strissel, K.J., Sokolov, M., Trieu, L.H. and Arshavsky, V.Y. (2006) Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J. Neurosci. 26, 1146–1153.

    Article  PubMed  CAS  Google Scholar 

  • Sung, C.H. and Tai, A.W. (2000) Rhodopsin trafficking and its role in retinal dystrophies. Int. Rev. Cytol. 195, 215–267.

    Article  PubMed  CAS  Google Scholar 

  • Swiatek-de Lange, M., Beer, M. and Ueffing, M. (2006) Analysis of light-dependent dynamics of protein complexes in the retina. ARVO Abstract 3734/B377.

    Google Scholar 

  • Thissen, M., Trojan, P., Giessl, A., Wolfrum, U., Krieglstein, J. and Klumpp, S. (2006) Protein phosphatase 2C dephosphorylates centrins. Int. Symposium on Neurodegeneration and Neuroprotection, Münster, Germany, Abstract.

    Google Scholar 

  • Thompson, J.R., Ryan, Z.C., Salisbury, J.L. and Kumar, R. (2006) The structure of the human centrin 2-xeroderma pigmentosum group C protein complex. J. Biol. Chem. 281, 18746–18752.

    Article  PubMed  CAS  Google Scholar 

  • Troutt, L.L., Wang, E., Pagh-Roehl, K. and Burnside, B. (1990) Microtubule nucleation and organization in teleost photoreceptors – microtubule recovery after elimination by cold. J. Neurocyt. 19, 213–223.

    Article  CAS  Google Scholar 

  • Usukura, J. and Obata, S. (1995) Morphogenesis of photoreceptor outer segments in retinal development. Prog. Retin. Eye Res. 15, 113–125.

    Article  Google Scholar 

  • Valente, E.M., Silhavy, J.L., Brancati, F., Barrano, G., Krishnaswami, S.R., Castori, M., Lancaster, M,A., Boltshauser, E., Boccone, L., Al Gazali, L., Fazzi, E., Signorini, S., Louie, C.M., Bellacchio, E., Bertini, E., Dallapiccola, B. and Gleeson, J.G. (2006) Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome. Nat. Genet. 38, 623–625.

    Article  PubMed  CAS  Google Scholar 

  • Van Dorp, D.B., Wright, A.F., Carothers, A.D. and Bleeker-Wagemakers, E.M. (1992) A family with RP3 type of X-linked retinitis pigmentosa: an association with ciliary abnormalities. Hum. Genet. 88, 331–334.

    Article  PubMed  CAS  Google Scholar 

  • van Wijk, E., van der, Z.B., Peters, T., Zimmermann, U., te, B.H., Kersten, F.F., Märker, T., Aller, E., Hoefsloot, L.H., Cremers, C.W., Cremers, F.P., Wolfrum, U., Knipper, M., Roepman, R. and Kremer, USH2A and VLGRl. Hum. Mol. Genet. 15, 751–765.

    Google Scholar 

  • Vervoort, R., Lennon, A., Bird, A.C., Tulloch, B., Axton, R., Miano, M.G., Meindl, A., Meitinger, T., Ciccodicola, A. and Wright, A.F. (2000) Mutational hot spot within a new RPGR exon in X-linked retinitis pigmentosa. Nat. Genet. 25, 462–466.

    Article  PubMed  CAS  Google Scholar 

  • Wang, Q., Pan, J. and Snell, W.J. (2006) Intraflagellar transport particles participate directly in ciliumgenerated signaling in Chlamydomonas. Cell 125, 549–562.

    Article  PubMed  CAS  Google Scholar 

  • Wolfrum, U., Giessl, A. and Pulvermüller, A. (2002) Centrins, a novel group of Ca2+ binding proteins in vertebrate photoreceptor cells. In: Photoreceptors and Calcium. W. Baehr and K. Palczewski, eds. (New York: Landes Bioscience and Kluwer Academic/Plenum Publishers), pp. 155–178.

    Google Scholar 

  • Wolfrum, U. and Salisbury, J.L. (1998) Expression of centrin isoforms in the mammalian retina. Exp. Cell Res. 242, 10–17.

    Article  PubMed  CAS  Google Scholar 

  • Wolfrum, U. and Schmitt, A. (2000) Rhodopsin transport in the membrane of the connecting cilium of mammalian photoreceptor cells. Cell Motil. Cytoskeleton 46, 95–107.

    Article  PubMed  CAS  Google Scholar 

  • Wolfrum, U., Trojan, P., Rausch, S., Wünschig, D., Giessl, A. and Pulvermüller, A. (2006) Light-dependent phosphorylation of centrins regulates binding to transducin in mammalian photoreceptors. ARVO Abstract 1091.

    Google Scholar 

  • Yang, J. and Li, T. (2006) Focus on molecules: rootletin. Exp. Eye Res. 83, 1–2.

    Article  PubMed  CAS  Google Scholar 

  • Yang, A., Miron, S., Duchambon, P., Assairi, L,. Blouquit, Y. and Craescu, C.T. (2006) The N-terminal domain of human centrin 2 has a closed structure, binds calcium with a very low affinity, and plays a role in the protein self-assembly. Biochemistry 45, 880–889.

    Article  PubMed  CAS  Google Scholar 

  • Young, R.W. (1967) The renewal of photoreceptor cell outer segments. J. Cell. Biol. 33, 61–72.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, Y., Hong, D.H., Pawlyk, B., Yue, G., Adamian, M., Grynberg, M., Godzik, A. and Li, T. (2003) The retinitis pigmentosa GTPase regulator (RPGR)- interacting protein: Subserving RPGR function and participating in disk morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 3965–3970.

    Article  PubMed  CAS  Google Scholar 

  • Zito, I., Downes, S.M., Patel, R.J., Cheetham, M.E., Ebenezer, N.D., Jenkins, S.A., Bhattacharya, S.S., Webster, A.R., Holder, G.E., Bird, A.C., Bamiou, D.E. and Hardcastle. A.J. (2003) RPGR mutation associated with retinitis pigmentosa, impaired hearing, and sinorespiratory infections. J. Med. Genet. 40, 609–615.

    Article  PubMed  CAS  Google Scholar 

  • Zuker, C.S. and Ranganathan. R. (1999) The path to specificity. Science 283, 650–651.

    Article  PubMed  CAS  Google Scholar 

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Roepman, R., Wolfrum, U. (2007). Protein Networks and Complexes in Photoreceptor Cilia. In: Bertrand, E., Faupel, M. (eds) Subcellular Proteomics. Subcellular Biochemistry, vol 43. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5943-8_10

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