Proteomic identification of unique photoreceptor disc components reveals the presence of PRCD, a protein linked to retinal degeneration

Journal of Proteome Research

Volumn 12, Issue 6, 2013, Pages 3010-3018

  Skiba, Nikolai P ^a   Spencer, William J ^a   Salinas, Raquel Y ^a   Lieu, Eric C ^a   Thompson, J Will ^b   Arshavsky, Vadim Y ^a  

^a DUKE UNIVERSITY EYE CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

photoreceptor disc proteome; PRCD; protein correlation profiling; quantitative proteomics

Indexed keywords

PHOSPHATIDYLSERINE; PHOSPHODIESTERASE VI; PROGRESSIVE ROD AND CONE DEGENERATION PROTEIN; PROMININ 1; PROTEIN; RAB PROTEIN; RHODOPSIN; SNARE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BLINDNESS; CELL ORGANELLE; CELLULAR DISTRIBUTION; LIMIT OF DETECTION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR DISC; PHOTORECEPTOR INNER SEGMENT; PHOTOTRANSDUCTION; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; PROTEOMICS; RETINA DEGENERATION; RETINA ROD OUTER SEGMENT;

VERTEBRATA;

EID: 84879331601     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4003678     Document Type: Article

References (50)

1. Rodieck, R. W. The first steps in seeing; Sinauer Associates: Sunderland, 1998; p 562.
2. Insinna, C.; Besharse, J. C. Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors Dev. Dyn. 2008, 237 (8) 1982-92
3. Sung, C. H.; Chuang, J. Z. The cell biology of vision J. Cell Biol. 2010, 190 (6) 953-63
4. Smith, H. G., Jr.; Stubbs, G. W.; Litman, B. J. The isolation and purification of osmotically intact discs from retinal rod outer segments Exp. Eye Res. 1975, 20 (3) 211-7
5. Papermaster, D. S. Preparation of retinal rod outer segments Methods Enzymol. 1982, 81, 48-52
6. Arshavsky, V. Y.; Lamb, T. D.; Pugh, E. N., Jr. G proteins and phototransduction Annu. Rev. Physiol. 2002, 64, 153-87
7. Liu, Q.; Tan, G.; Levenkova, N.; Li, T.; Pugh, E. N., Jr.; Rux, J. J.; Speicher, D. W.; Pierce, E. A. The proteome of the mouse photoreceptor sensory cilium complex Mol. Cell. Proteomics 2007, 6 (8) 1299-317
8. Panfoli, I.; Musante, L.; Bachi, A.; Ravera, S.; Calzia, D.; Cattaneo, A.; Bruschi, M.; Bianchini, P.; Diaspro, A.; Morelli, A.; Pepe, I. M.; Tacchetti, C.; Candiano, G. Proteomic analysis of the retinal rod outer segment disks J. Proteome Res. 2008, 7 (7) 2654-69
9. Kwok, M. C.; Holopainen, J. M.; Molday, L. L.; Foster, L. J.; Molday, R. S. Proteomics of photoreceptor outer segments identifies a subset of SNARE and Rab proteins implicated in membrane vesicle trafficking and fusion Mol. Cell. Proteomics 2008, 7 (6) 1053-66
10. Andersen, J. S.; Wilkinson, C. J.; Mayor, T.; Mortensen, P.; Nigg, E. A.; Mann, M. Proteomic characterization of the human centrosome by protein correlation profiling Nature 2003, 426 (6966) 570-4
11. Zangerl, B.; Goldstein, O.; Philp, A. R.; Lindauer, S. J.; Pearce-Kelling, S. E.; Mullins, R. F.; Graphodatsky, A. S.; Ripoll, D.; Felix, J. S.; Stone, E. M.; Acland, G. M.; Aguirre, G. D. Identical mutation in a novel retinal gene causes progressive rod-cone degeneration in dogs and retinitis pigmentosa in humans Genomics 2006, 88 (5) 551-63
12. Nevet, M. J.; Shalev, S. A.; Zlotogora, J.; Mazzawi, N.; Ben-Yosef, T. Identification of a prevalent founder mutation in an Israeli Muslim Arab village confirms the role of PRCD in the aetiology of retinitis pigmentosa in humans J. Med. Genet. 2010, 47 (8) 533-7
13. McDowell, J. H. Preparing rod outer segment membranes, regenerating rhodopsin, and determining rhodopsin concentration Methods Neurosci 1993, 15, 123-130
14. Bownds, D.; Gordon-Walker, A.; Gaide-Huguenin, A. C.; Robinson, W. Characterization and analysis of frog photoreceptor membranes J. Gen. Physiol. 1971, 58 (3) 225-37
15. Wisniewski, J. R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis Nat. Methods 2009, 6 (5) 359-62
16. Reidel, B.; Thompson, J. W.; Farsiu, S.; Moseley, M. A.; Skiba, N. P.; Arshavsky, V. Y., Proteomic profiling of a layered tissue reveals unique glycolytic specializations of photoreceptor cells. Mol. Cell. Proteomics 2011, 10 (3), 10.1074/mcp.M110.002469.
17. Lobanova, E. S.; Herrmann, R.; Finkelstein, S.; Reidel, B.; Skiba, N. P.; Deng, W. T.; Jo, R.; Weiss, E. R.; Hauswirth, W. W.; Arshavsky, V. Y. Mechanistic basis for the failure of cone transducin to translocate: why cones are never blinded by light J. Neurosci. 2010, 30 (20) 6815-24
18. Lobanova, E. S.; Finkelstein, S.; Herrmann, R.; Chen, Y. M.; Kessler, C.; Michaud, N. A.; Trieu, L. H.; Strissel, K. J.; Burns, M. E.; Arshavsky, V. Y. Transducin γ-subunit sets expression levels of α- and β-subunits and is crucial for rod viability J. Neurosci. 2008, 28 (13) 3510-3520
19. Foster, L. J.; de Hoog, C. L.; Zhang, Y.; Xie, X.; Mootha, V. K.; Mann, M. A mammalian organelle map by protein correlation profiling Cell 2006, 125 (1) 187-99
20. Wiese, S.; Gronemeyer, T.; Ofman, R.; Kunze, M.; Grou, C. P.; Almeida, J. A.; Eisenacher, M.; Stephan, C.; Hayen, H.; Schollenberger, L.; Korosec, T.; Waterham, H. R.; Schliebs, W.; Erdmann, R.; Berger, J.; Meyer, H. E.; Just, W.; Azevedo, J. E.; Wanders, R. J.; Warscheid, B. Proteomics characterization of mouse kidney peroxisomes by tandem mass spectrometry and protein correlation profiling Mol. Cell. Proteomics 2007, 6 (12) 2045-57
21. Borner, G. H.; Antrobus, R.; Hirst, J.; Bhumbra, G. S.; Kozik, P.; Jackson, L. P.; Sahlender, D. A.; Robinson, M. S. Multivariate proteomic profiling identifies novel accessory proteins of coated vesicles J. Cell Biol. 2012, 197 (1) 141-60
22. Wensel, T. G. Signal transducing membrane complexes of photoreceptor outer segments Vision Res. 2008, 48 (20) 2052-61
23. Palczewski, K. Chemistry and biology of vision J. Biol. Chem. 2012, 287 (3) 1612-9
24. Arshavsky, V. Y.; Burns, M. E. Photoreceptor signaling: Supporting vision across a wide range of light intensities J. Biol. Chem. 2012, 287 (3) 1620-6
25. Baehr, W.; Morita, E. A.; Swanson, R. J.; Applebury, M. L. Characterization of bovine rod outer segment G-protein J. Biol. Chem. 1982, 257 (11) 6452-60
26. Anant, J. S.; Ong, O. C.; Xie, H. Y.; Clarke, S.; O'Brien, P. J.; Fung, B. K. In vivo differential prenylation of retinal cyclic GMP phosphodiesterase catalytic subunits J. Biol. Chem. 1992, 267 (2) 687-90
27. Bigay, J.; Faurobert, E.; Franco, M.; Chabre, M. Roles of lipid modifications of transducin subunits in their GDP-dependent association and membrane binding Biochemistry 1994, 33 (47) 14081-90
28. Seitz, H. R.; Heck, M.; Hofmann, K. P.; Alt, T.; Pellaud, J.; Seelig, A. Molecular determinants of the reversible membrane anchorage of the G-protein transducin Biochemistry 1999, 38 (25) 7950-60
29. Fukada, Y.; Matsuda, T.; Kokame, K.; Takao, T.; Shimonishi, Y.; Akino, T.; Yoshizawa, T. Effects of carboxyl methylation of photoreceptor G protein gamma-subunit in visual transduction J. Biol. Chem. 1994, 269 (7) 5163-70
30. Kosloff, M.; Alexov, E.; Arshavsky, V. Y.; Honig, B. Electrostatic and lipid anchor contributions to the interaction of transducin with membranes: Mechanistic implications for activation and translocation J. Biol. Chem. 2008, 283 (45) 31197-207
31. Hu, G.; Wensel, T. G. R9AP, a membrane anchor for the photoreceptor GTPase accelerating protein, RGS9-1 Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (15) 9755-60
32. Farjo, R.; Naash, M. I. The role of Rds in outer segment morphogenesis and human retinal disease Ophthalmic Genet. 2006, 27 (4) 117-22
33. Goldberg, A. F. Role of peripherin/rds in vertebrate photoreceptor architecture and inherited retinal degenerations Int. Rev. Cytol. 2006, 253, 131-75
34. Molday, R. S.; Warren, R.; Loewen, C.; Molday, L. Cyclic GMP-gated channel and peripherin/rds-rom-1 complex of rod cells Novartis Found. Symp. 1999, 224, 249-61
35. Boesze-Battaglia, K.; Goldberg, A. F.; Dispoto, J.; Katragadda, M.; Cesarone, G.; Albert, A. D. A soluble peripherin/Rds C-terminal polypeptide promotes membrane fusion and changes conformation upon membrane association Exp. Eye Res. 2003, 77 (4) 505-14
36. Weng, J.; Mata, N. L.; Azarian, S. M.; Tzekov, R. T.; Birch, D. G.; Travis, G. H. Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice Cell 1999, 98 (1) 13-23
37. Sun, H.; Molday, R. S.; Nathans, J. Retinal stimulates ATP hydrolysis by purified and reconstituted ABCR, the photoreceptor-specific ATP-binding cassette transporter responsible for Stargardt disease J. Biol. Chem. 1999, 274 (12) 8269-81
38. Sparrow, J. R.; Hicks, D.; Hamel, C. P. The retinal pigment epithelium in health and disease Curr. Mol. Med. 2010, 10 (9) 802-23
39. Kevany, B. M.; Palczewski, K. Phagocytosis of retinal rod and cone photoreceptors Physiology 2010, 25 (1) 8-15
40. Coleman, J. A.; Kwok, M. C.; Molday, R. S. Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes J. Biol. Chem. 2009, 284 (47) 32670-9
41. Coleman, J. A.; Molday, R. S. Critical role of the beta-subunit CDC50A in the stable expression, assembly, subcellular localization, and lipid transport activity of the P4-ATPase ATP8A2 J. Biol. Chem. 2011, 286 (19) 17205-16
42. Yang, Z.; Chen, Y.; Lillo, C.; Chien, J.; Yu, Z.; Michaelides, M.; Klein, M.; Howes, K. A.; Li, Y.; Kaminoh, Y.; Chen, H.; Zhao, C.; Al-Sheikh, Y. T.; Karan, G.; Corbeil, D.; Escher, P.; Kamaya, S.; Li, C.; Johnson, S.; Frederick, J. M.; Zhao, Y.; Wang, C.; Cameron, D. J.; Huttner, W. B.; Schorderet, D. F.; Munier, F. L.; Moore, A. T.; Birch, D. G.; Baehr, W.; Hunt, D. M.; Williams, D. S.; Zhang, K. Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice J. Clin. Invest. 2008, 118 (8) 2908-16
43. Han, Z.; Anderson, D. W.; Papermaster, D. S. Prominin-1 localizes to the open rims of outer segment lamellae in Xenopus laevis rod and cone photoreceptors Invest. Ophthalmol. Vis. Sci. 2012, 53 (1) 361-73
44. Pentia, D. C.; Hosier, S.; Cote, R. H. The glutamic acid-rich protein-2 (GARP2) is a high affinity rod photoreceptor phosphodiesterase (PDE6)-binding protein that modulates its catalytic properties J. Biol. Chem. 2006, 281 (9) 5500-5
45. Martemyanov, K. A.; Krispel, C. M.; Lishko, P. V.; Burns, M. E.; Arshavsky, V. Y. Functional comparison of RGS9 splice isoforms in a living cell Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (52) 20988-93
46. Peshenko, I. V.; Olshevskaya, E. V.; Savchenko, A. B.; Karan, S.; Palczewski, K.; Baehr, W.; Dizhoor, A. M. Enzymatic properties and regulation of the native isozymes of retinal membrane guanylyl cyclase (RetGC) from mouse photoreceptors Biochemistry 2011, 50 (25) 5590-600
47. Lyubarsky, A. L.; Daniele, L. L.; Pugh, E. N., Jr. From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG Vision Res. 2004, 44 (28) 3235-51
48. Nickell, S.; Park, P. S.; Baumeister, W.; Palczewski, K. Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography J. Cell Biol. 2007, 177 (5) 917-25
49. Deretic, D.; Wang, J. Molecular assemblies that control rhodopsin transport to the cilia Vision Res. 2012, 75, 5-10
50. Oesterlin, L. K.; Goody, R. S.; Itzen, A. Posttranslational modifications of Rab proteins cause effective displacement of GDP dissociation inhibitor Proc. Natl. Acad. Sci. U.S.A. 2012, 109 (15) 5621-6