A model for transport of membrane-associated phototransduction polypeptides in rod and cone photoreceptor inner segments

Vision Research

Volumn 48, Issue 3, 2008, Pages 442-452

  Karan, Sukanya ^a   Zhang, Houbin ^b   Li, Sha ^b   Frederick, Jeanne M ^b   Baehr, Wolfgang ^a,b  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Guanylate cyclase knockout; Pde6d knockout; Phototransduction; Rod and cone photoreceptors; Vesicular transport

Indexed keywords

BINDING PROTEIN; G PROTEIN COUPLED RECEPTOR KINASE; GUANYLATE CYCLASE; MEMBRANE PROTEIN; PHOSPHODIESTERASE; PRENYL BINDING PROTEIN; PROTEIN SUBUNIT; RHODOPSIN; UNCLASSIFIED DRUG;

ARTICLE; DOWN REGULATION; ENDOPLASMIC RETICULUM; NONHUMAN; PHENOTYPE; PHOTORECEPTOR MEMBRANE; PHOTOTRANSDUCTION; PRENYLATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RETINA DEGENERATION;

ANIMALS; CONES (RETINA); CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; DOWN-REGULATION; ENDOPLASMIC RETICULUM; GENE DELETION; GUANYLATE CYCLASE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MODELS, ANIMAL; NEOPRENE; PHOTOTRANSDUCTION; PROTEIN TRANSPORT; RETINAL DEGENERATION; RODS (RETINA);

EID: 38749148422     PISSN: 00426989     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.visres.2007.08.020     Document Type: Article

References (62)

1. Anant J.S., Ong O.C., Xie H., Clarke S., O'Brien P.J., and Fung B.K.K. In vivo differential prenylation of retinal cyclic GMP phosphodiesterase catalytic subunits. Journal of Biological Chemistry 267 (1992) 687-690
2. Baehr W., Karan S., Maeda T., Luo D.G., Li S., Bronson J.D., et al. The function of Guanylate Cyclase 1 (GC1) and Guanylate Cyclase 2 (GC2) in rod and cone photoreceptors. Journal of Biological Chemistry 282 (2007) 8837-8847
3. Becker J., Linari M., Manson F., Wright A., Meindl A., and Meitinger T. The delta subunit of rod phosphodiesterase interacts with the RCC1 homologous domain of RPGR. Investigative Ophthalmology & Visual Science 39 (1998) S953
4. Besharse J.C., and Hollyfield J.G. Turnover of mouse photoreceptor outer segments in constant light and darkness. Investigative Ophthalmology & Visual Science 18 (1979) 1019-1024
5. Burns M.E., and Arshavsky V.Y. Beyond counting photons: Trials and trends in vertebrate visual transduction. Neuron 48 (2005) 387-401
6. Chang B., Hawes N.L., Hurd R.E., Davisson M.T., Nusinowitz S., and Heckenlively J.R. Retinal degeneration mutants in the mouse. Vision Research 42 (2002) 517-525
7. Coleman J.E., Zhang Y., Brown G.A., and Semple-Rowland S.L. Cone cell survival and downregulation of GCAP1 protein in the retinas of GC1 knockout mice. Investigative Ophthalmology & Visual Science 45 (2004) 3397-3403
8. Cook T.A., Ghomashchi F., Gelb M.H., Florio S.K., and Beavo J.A. Binding of the delta subunit to rod phosphodiesterase catalytic subunits requires methylated, prenylated C-termini of the catalytic subunits. Biochemistry 39 (2000) 13516-13523
9. Dalke C., and Graw J. Mouse mutants as models for congenital retinal disorders. Experimental Eye Research 81 (2005) 503-512
10. Deretic D. Post-Golgi trafficking of rhodopsin in retinal photoreceptors. Eye 12 Pt. 3b (1998) 526-530
11. Deretic D. A role for rhodopsin in a signal transduction cascade that regulates membrane trafficking and photoreceptor polarity. Vision Research 46 (2006) 4427-4433
12. Deretic D., Williams A.H., Ransom N., Morel V., HArgrave P.A., and Arendt A. Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proceedings of the National Academy of Sciences of the United States of America 102 (2005) 3301-3306
13. Fain G.L., and Lisman J.E. Light, Ca2+, and photoreceptor death: New evidence for the equivalent- light hypothesis from arrestin knockout mice [In Process Citation]. Investigative Ophthalmology & Visual Science 40 (1999) 2770-2772
14. Farber D.B., and Lolley R.N. Cyclic guanosine monophosphate: Elevation in degenerating photoreceptor cells of the C3H mouse retina. Science 186 (1974) 449-451
15. Fariss R.N., Molday R.S., Fisher S.K., and Matsumoto B. Evidence from normal and degenerating photoreceptors that two outer segment integral membrane proteins have separate transport pathways. The Journal of Comparative Neurology. 387 (1997) 148-156
16. Fu Y., and Yau K.W. Phototransduction in mouse rods and cones. Pflugers Arch. 454 (2007) 805-819
17. Gelb M.H., Brunsveld L., Hrycyna C.A., Michaelis S., Tamanoi F., Van Voorhis W.C., et al. Therapeutic intervention based on protein prenylation and associated modifications. Nature Chemical Biology 2 (2006) 518-528
18. Hafezi F., Grimm C., Simmen B.C., Wenzel A., and Reme C.E. Molecular ophthalmology: An update on animal models for retinal degenerations and dystrophies. The British Journal of Ophthalmology 84 (2000) 922-927
19. Hancock J.F., Cadwallader K., Paterson H., and Marshall C.J. A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. The EMBO Journal 10 (1991) 4033-4039
20. Hanzal-Bayer M., Renault L., Roversi P., Wittinghofer A., and Hillig R.C. The complex of Arl2-GTP and PDE delta: From structure to function. The EMBO Journal 21 (2002) 2095-2106
21. Humphries M.M., Rancourt D., Farrar G.J., Kenna P., Hazel M., Bush R.A., et al. Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nature Genetics 15 (1997) 216-219
22. Inglese J., Koch W.J., Caron M.G., and Lefkowitz R.J. Isoprenylation in regulation of signal transduction by G-protein- coupled receptor kinases. Nature 359 (1992) 147-150
23. Johnson R.S., Ohguro H., Palczewski K., Hurley J.B., Walsh K.A., and Neubert T.A. Heterogeneous N-acylation is a tissue- and species-specific posttranslational modification. Journal of Biological Chemistry 269 (1994) 21067-21071
24. Lai R.K., Perez-Sala D., Cañada F.J., and Rando R.R. The gamma subunit of transducin is farnesylated. Proceedings of the National Academy of Sciences of the United States of America 87 (1990) 7673-7677
25. Lamb T.D., and Pugh Jr. E.N. Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Investigative Ophthalmology & Visual Science 47 (2006) 5138-5152
26. LaVail M.M. Rod outer segment disk shedding in rat retina: Relationship to cyclic lighting. Science 194 (1976) 1071-1074
27. Lee E.S., Burnside B., and Flannery J.G. Characterization of peripherin/rds and rom-1 transport in rod photoreceptors of transgenic and knockout animals. Investigative Ophthalmology & Visual Science 47 (2006) 2150-2160
28. Lem J., Krasnoperova N.V., Calvert P.D., Kosaras B., Cameron D.A., Nicolo M., et al. Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proceedings of the National Academy of Sciences of the United States of America 96 (1999) 736-741
29. Li N., and Baehr W. Expression and characterization of human PDEd and its Caenorhabditis elegans ortholog CEd. FEBS Letters 440 (1998) 454-457
30. Li T., Volpp K., and Applebury M.L. Bovine cone photoreceptor cGMP phosphodiesterase structure deduced from a cDNA clone. Proceedings of the National Academy of Sciences of the United States of America 87 (1990) 293-297
31. Linari M., Hanzal-Bayer M., and Becker J. The delta subunit of rod specific cyclic GMP phosphodiesterase, PDE delta, interacts with the Arf-like protein Arl3 in a GTP specific manner. FEBS Letters 458 (1999) 55-59
32. Linari M., Ueffing M., Manson F., Wright A., Meitinger T., and Becker J. The retinitis pigmentosa GTPase regulator, RPGR, interacts with the delta subunit of rod cyclic GMP phosphodiesterase. Proceedings of the National Academy of Sciences of the United States of America 96 (1999) 1315-1320
33. Lippincott-Schwartz J., Roberts T.H., and Hirschberg K. Secretory protein trafficking and organelle dynamics in living cells. Annual Review of Cell and Developmental Biology 16 (2000) 557-589
34. Lobanova E.S., Finkelstein S., Song H., Tsang S.H., Chen C.K., Sokolov M., et al. Transducin translocation in rods is triggered by saturation of the GTPase-activating complex. Journal of Neuroscience 27 (2007) 1151-1160
35. Magee T., and Seabra M.C. Fatty acylation and prenylation of proteins: What's hot in fat. Current Opinion in Cell Biology 17 (2005) 190-196
36. Margulis A., Goraczniak R.M., Duda T., Sharma R.K., and Sitaramayya A. Structural and biochemical identity of retinal rod outer segment membrane guanylate cyclase. Biochemical and Biophysical Research Communications 194 (1993) 855-861
37. Marszalek J.R., Liu X., Roberts E.A., Chui D., Marth J.D., Williams D.S., et al. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102 (2000) 175-187
38. McTaggart S.J. Isoprenylated proteins. Cellular and molecular life sciences 63 (2006) 255-267
39. Michalakis S., Geiger H., Haverkamp S., Hofmann F., Gerstner A., and Biel M. Impaired opsin targeting and cone photoreceptor migration in the retina of mice lacking the cyclic nucleotide-gated channel CNGA3. Investigative Ophthalmology & Visual Science 46 (2005) 1516-1524
40. Nair K.S., Hanson S.M., Mendez A., Gurevich E.V., Kennedy M.J., Shestopalov V.I., et al. Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions. Neuron 46 (2005) 555-567
41. Neubert T.A., Johnson R.S., Hurley J.B., and Walsh K.A. The rod transducin a subunit amino terminus is heterogeneously fatty acylated. Journal of Biological Chemistry 267 (1992) 18274-18277
42. Norton A.W., Hosier S., Terew J.M., Li N., Dhingra A., Vardi N., et al. Evaluation of the 17-kDa prenyl-binding protein as a regulatory protein for phototransduction in retinal photoreceptors. Journal of Biological Chemistry 280 (2005) 1248-1256
43. Olshevskaya E.V., Calvert P.D., Woodruff M.L., Peshenko I.V., Savchenko A.B., Makino C.L., et al. The Y99C mutation in guanylyl cyclase-activating protein 1 increases intracellular Ca2+ and causes photoreceptor degeneration in transgenic mice. Journal of Neuroscience 24 (2004) 6078-6085
44. Palczewski K., Sokal I., and Baehr W. Guanylate cyclase-activating proteins: Structure, function, and diversity. Biochemical and Biophysical Research Communications 322 (2004) 1123-1130
45. Perrault I., Rozet J.-M., Calvas P., Gerber S., Camuzat A., Dollfus H., et al. Retinal-specific guanylate cyclase gene mutations in Leber's congenital amaurosis. Nature Genetics 14 (1996) 461-464
46. Qin N., Pittler S.J., and Baehr W. In vitro isoprenylation and membrane association of mouse rod photoreceptor cGMP phosphodiesterase a and b subunits expressed in bacteria. Journal of Biological Chemistry 267 (1992) 8458-8463
47. Ridge K.D., Abdulaev N.G., Sousa M., and Palczewski K. Phototransduction: Crystal clear. Trends in Biochemical Science 28 (2003) 479-487
48. Ritter L.M., Boesze-Battaglia K., Tam B.M., Moritz O.L., Khattree N., Chen S.C., et al. Uncoupling of photoreceptor peripherin/rds fusogenic activity from biosynthesis, subunit assembly, and targeting: A potential mechanism for pathogenic effects. Journal of Biological Chemistry 279 (2004) 39958-39967
49. Rohrer B., Lohr H.R., Humphries P., Redmond T.M., Seeliger M.W., and Crouch R.K. Cone opsin mislocalization in Rpe65-/- mice: A defect that can be corrected by 11-cis retinal. Investigative Ophthalmology & Visual Science 46 (2005) 3876-3882
50. Rosenzweig D.H., Nair K.S., Wei J., Wang Q., Garwin G., Saari J.C., et al. Subunit dissociation and diffusion determine the subcellular localization of rod and cone transducins. Journal of Neuroscience 27 (2007) 5484-5494
51. Semple-Rowland S.L., Lee N.R., Van-Hooser J.P., Palczewski K., and Baehr W. A null mutation in the photoreceptor guanylate cyclase gene causes the retinal degeneration chicken phenotype. Proceedings of the National Academy of Sciences of the United States of America 95 (1998) 1271-1276
52. Strissel K.J., Sokolov M., Trieu L.H., and Arshavsky V.Y. Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. Journal of Neuroscience 26 (2006) 1146-1153
53. Suber M.L., Pittler S.J., Qin N., Wright G.C., Holcombe V., Lee R.H., et al. Irish setter dogs affected with rod/cone dysplasia contain a nonsense mutation in the rod cGMP phosphodiesterase beta subunit gene. Proceedings of the National Academy of Sciences of the United States of America 90 (1993) 3968-3972
54. Tai A.W., Chuang J.Z., and Sung C.H. Cytoplasmic dynein regulation by subunit heterogeneity and its role in apical transport. Journal of Cell Biology 153 (2001) 1499-1509
55. Tam B.M., Moritz O.L., and Papermaster D.S. The C terminus of peripherin/rds participates in rod outer segment targeting and alignment of disk incisures. Molecular Biology of the Cell 15 (2004) 2027-2037
56. Vale R.D. The molecular motor toolbox for intracellular transport. Cell 112 (2003) 467-480
57. Yang R.B., Robinson S.W., Xiong W.H., Yau K.W., Birch D.G., and Garbers D.L. Disruption of a retinal guanylyl cyclase gene leads to cone-specific dystrophy and paradoxical rod behavior. Journal of Neuroscience 19 (1999) 5889-5897
58. Young R.W. Visual cells and the concept of renewal. Investigative Ophthalmology & Visual Science 15 (1976) 700-725
59. Zhang F.L., and Casey P.J. Protein prenylation: Molecular mechanisms and functional consequences. Annual Review of Biochemistry 65 (1996) 241-269
60. Zhang H., Hosier S., Terew J.M., Zhang K., Cote R.H., and Baehr W. Assay and functional properties of PrBP(PDEdelta), a prenyl-binding protein interacting with multiple partners. Methods in Enzymology 403 (2005) 42-56
61. Zhang H., Li S., Doan T., Rieke F., Detwiler P.B., Frederick J.M., et al. Deletion of PrBP/{delta} impedes transport of GRK1 and PDE6 catalytic subunits to photoreceptor outer segments. Proceedings of the National Academy of Sciences of the United States of America 104 (2007) 8857-8862
62. Zhang H., Liu X.H., Zhang K., Chen C.K., Frederick J.M., Prestwich G.D., et al. Photoreceptor cGMP phosphodiesterase delta subunit (PDEdelta) functions as a prenyl-binding protein. Journal of Biological Chemistry 279 (2004) 407-413