Proteomic analysis of the retinal rod outer segment disks

Journal of Proteome Research

Volumn 7, Issue 7, 2008, Pages 2654-2669

  Panfoli, Isabella ^a   Musante, Luca ^b,c   Bachi, Angela ^d   Ravera, Silvia ^a   Calzia, Daniela ^a   Cattaneo, Angela ^d   Bruschi, Maurizio ^b,c   Bianchini, Paolo ^a   Diaspro, Alberto ^a,e   Morelli, Alessandro ^a   Pepe, Isidoro M ^a   Tacchetti, Carlo ^a   Candiano, Giovanni ^b  

^a UNIVERSITY OF GENOA   (Italy)

^b Laboratory on Pathophysiology of Uremia   (Italy)

^c Renal Child Foundation   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

Confocal laser scanning microscopy; Disks; F1F0 ATP synthase; MALDI TOF; nLC ESI MS MS; Redox chain complexes; Rod outer segment; Two dimensional polyacrylamide gel electrophoresis

Indexed keywords

PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ADENOSINE TRIPHOSPHATE; PROTEIN SUBUNIT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

AEROBIC METABOLISM; ANIMAL TISSUE; ARTICLE; COW; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC DISK; OXIDATIVE PHOSPHORYLATION; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEOMICS; RETINA ROD; UNINDEXED SEQUENCE; ANIMAL; BIOSYNTHESIS; CATTLE; ELECTROSPRAY MASS SPECTROMETRY; MASS SPECTROMETRY; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; RETINA ROD OUTER SEGMENT; TANDEM MASS SPECTROMETRY;

BOVINAE; VERTEBRATA;

ADENOSINE TRIPHOSPHATE; ANIMALS; CATTLE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; PROTEIN SUBUNITS; PROTEOME; PROTON-TRANSLOCATING ATPASES; ROD OUTER SEGMENTS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 51649118362     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr7006939     Document Type: Article

References (48)

1. Ridge, K. D.; Abdulaev, N. G.; Sousa, M.; Palczewski, K. Phototrans-duction: crystal clear. Trends Biochem. Sci. 2003, 28 (9), 479-87.
2. Pepe, I. M. Recent advances in our understanding of rhodopsin and phototransduction. Prog. Retinal Eye Res. 2001, 20 (6), 733-59.
3. Bok, D. Retinal photoreceptor-pigment epithelium interactions. Friedenwald lecture. Invest. Ophthalmol. Visual Sci. 1985, 26 (12), 1659-94.
4. Young, R. W. Shedding of discs from rod outer segments in the rhesus monkey. J. Ultrastruct. Res. 1971, 34 (1), 190-203.
5. Albert, A. D.; Boesze-Battaglia, K. The role of cholesterol in rod outer segment membranes. Prog. Lipid Res. 2005, 44 (2-3), 99-124.
6. Finnemann, S. C.; Bonilha, V. L.; Marmorstein, A. D.; Rodriguez-Boulan, E. Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (24), 12932-7.
7. Hamm, H. E.; Bownds, M. D. Protein complement of rod outer segments of frog retina. Biochemistry 1986, 25 (16), 4512-23.
8. Nishizawa, Y.; Komori, N.; Usukura, J.; Jackson, K. W.; Tobin, S. L.; Matsumoto, H. Initiating ocular proteomics for cataloging bovine retinal proteins: microanalytical techniques permit the identification of proteins derived from a novel photoreceptor preparation. Exp. Eye Res. 1999, 69 (2), 195-212.
9. Hauck, S. M.; Schoeffmann, S.; Deeg, C. A.; Gloeckner, C. J.; Swiatek-de Lange, M.; Ueffing, M. Proteomic analysis of the porcine interphotoreceptor matrix. Proteomics 2005, 5 (14), 3623-36.
10. Nordgaard, C. L.; Berg, K. M.; Kapphahn, R. J.; Reilly, C.; Feng, X.; Olsen, T. W.; Ferrington, D. A. Proteomics of the retinal pigment epithelium reveals altered protein expression at progressive stages of age-related macular degeneration. Invest. Ophthalmol. Visual Sci. 2006, 47 (3), 815-22.
11. Smith, H. G., Jr.; Litman, B. J. Preparation of osmotically intact rod outer segment disks by Ficoll flotation. Methods Enzymol. 1982, 81, 57-61.
12. Schnetkamp, P. P.; Daemen, F. J. Isolation and characterization of osmotically sealed bovine rod outer segments. Methods Enzymol. 1982, 81, 110-6.
13. Ravera, S.; Calzia, D.; Bianchini, P.; Diaspro, A.; Panfoli, I. Confocal laser scanning microscopy of retinal rod outer segment intact disks: new labeling technique. J. Biomed. Opt. 2007, 12 (5), 050501.
14. Wald, G.; Brown, P. K. The molar extinction of rhodopsin. J. Gen Physiol 1953, 37 (2), 189-200.
15. Zanotti, F.; Raho, G.; Gaballo, A.; Papa, S. Inhibitory and anchoring domains in the ATPase inhibitor protein IF1 of bovine heart mitochondrial ATP synthase. J. Bioenerg. Biomembr. 2004, 36 (5), 447-57.
16. Pawley, J. B., Handbook of Biological Confocal Microscopy, 3rd Ed; York, P. P.-S.-N., Ed., 2006.
17. Herbert, B.; Galvani, M.; Hamdan, M.; Olivieri, E.; MacCarthy, J.; Pedersen, S.; Righetti, P. G. Reduction and alkylation of proteins in preparation of two-dimensional map analysis: why, when, and how. Electrophoresis 2001, 22 (10), 2046-57.
18. Mastro, R.; Hall, M. Protein delipidation and precipitation by tri-n-butylphosphate, acetone, and methanol treatment for isoelectric focusing and two-dimensional gel electrophoresis. Anal. Biochem. 1999, 273 (2), 313-5.
19. Candiano, G.; Musante, L.; Bruschi, M.; Ghiggeri, G. M.; Herbert, B.; Antonucci, F.; Righetti, P. G. Two-dimensional maps in soft immobilized pH gradient gels: a new approach to the proteome of the Third Millennium. Electrophoresis 2002, 23 (2), 292-7.
20. Bruschi, M.; Musante, L.; Candiano, G.; Ghiggeri, G. M.; Herbert, B.; Antonucci, F.; Righetti, P. G. Soft immobilized pH gradient gels in proteome analysis: a follow-up. Proteomics 2003, 3 (6), 821-5.
21. Oakley, B. R.; Kirsch, D. R.; Morris, N. R. A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal. Biochem. 1980, 105 (2), 361-3.
22. Candiano, G.; Bruschi, M.; Musante, L.; Santucci, L.; Ghiggeri, G. M.; Carnemolla, B.; Orecchia, P.; Zardi, L.; Righetti, P. G. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004, 25 (9), 1327-33.
23. Anderson, N. L.; Anderson, N. G. Analytical techniques for cell fractions. XXII. Two-dimensional analysis of serum and tissue proteins: multiple gradient-slab gel electrophoresis. Anal. Biochem. 1978, 85 (2), 341-54.
24. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68 (5), 850-8.
25. Zhang, W.; Chait, B. T. ProFound: an expert system for protein identification using mass spectrometric peptide mapping information. Anal. Chem. 2000, 72 (11), 2482-9.
26. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227 (5259), 680-5.
27. Turina, P.; Melandri, B. A.; Graber, P. ATP synthesis in chromato-phores driven by artificially induced ion gradients. Eur. J. Biochem. 1991, 196 (1), 225-9.
28. Lamba, O. P.; Borchman, D.; O'Brien, P. J. Fourier transform infrared study of the rod outer segment disk and plasma membranes of vertebrate retina. Biochemistry 1994, 33 (7), 1704-12.
29. Molday, R. S.; Molday, L. L. Differences in the protein composition of bovine retinal rod outer segment disk and plasma membranes isolated by a ricin-gold-dextran density perturbation method. J. Cell Biol. 1987, 105 (6), 2589-601.
30. 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.
31. Bruschi, M.; Seppi, C.; Arena, S.; Musante, L.; Santucci, L.; Balduini, C.; Scaloni, A.; Lanciotti, M.; Righetti, P. G.; Candiano, G. Proteomic analysis of erythrocyte membranes by soft Immobiline gels combined with differential protein extraction. J. Proteome Res. 2005, 4 (4), 1304-9.
32. Strissel, K. J.; Lishko, P. V.; Trieu, L. H.; Kennedy, M. J.; Hurley, J. B.; Arshavsky, V. Y. Recoverin undergoes light-dependent intracellular translocation in rod photoreceptors. J. Biol. Chem. 2005, 280 (32), 29250-5.
33. Cook, N. J.; Molday, L. L.; Reid, D.; Kaupp, U. B.; Molday, R. S. The cGMP-gated channel of bovine rod photoreceptors is localized exclusively in the plasma membrane. J. Biol. Chem. 1989, 264 (12), 6996-9.
34. Hsu, S. C.; Molday, R. S. Glucose metabolism in photoreceptor outer segments. Its role in phototransduction and in NADPH-requiring reactions. J. Biol. Chem. 1994, 269 (27), 17954-9.
35. Dick, E. Enzymes of energy metabolism in the mudpuppy retina. J. Neurochem. 1984, 43 (4), 1124-31.
36. Hsu, S. C.; Molday, R. S. Glyceraldehyde-3-phosphate dehydrogenase is a major protein associated with the plasma membrane of retinal photoreceptor outer segments. J. Biol. Chem. 1990, 265 (22), 13308-13.
37. Boesze-Battaglia, K. Fusion of intracellular rod outer segment disk membranes with the surrounding plasma membrane. Invest. Ophthalmol. Visual Sci. 1997, 38 (2), 487-97.
38. Righetti, P. G.; Gelfi, C.; Bossi, M. L.; Boschetti, E. Isoelectric focusing and non-isoelectric precipitation of ferritin in immobilized pH gradients: An improved protocol overcoming protein-matrix interactions. Electrophoresis 1987, 8, 62-70.
39. Plantner, J. J.; Kean, E. L. Multiple isoelectric forms of detergent -solubilized bovine rhodopsin. I. Identity, composition and properties. Biochim. Biophys. Acta 1983, 744 (3), 312-9.
40. Fotiadis, D.; Liang, Y.; Filipek, S.; Saperstein, D. A.; Engel, A.; Palczewski, K. Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 2003, 421 (6919), 127-8.
41. Choudhary, J.; Grant, S. G. Proteomics in postgenomic neuro-science: the end of the beginning. Nat. Neurosci. 2004, 7 (5), 440-5.
42. Hubbell, W. L.; Altenbach, C.; Hubbell, C. M.; Khorana, H. G. Rhodopsin structure, dynamics, and activation: a perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking. Adv. Protein Chem. 2003, 63, 243-90.
43. Mootha, V. K.; Bunkenborg, J.; Olsen, J. V.; Hjerrild, M.; Wisniewski, J. R.; Stahl, E.; Bolouri, M. S.; Ray, H. N.; Sihag, S.; Kamal, M.; Patterson, N.; Lander, E. S.; Mann, M. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 2003, 115 (5), 629-40.
44. Uhl, R.; Zellmann-Kraska, R.; Desel, H. Optical probes of intradiskal processes in rod photoreceptors. I: Light-scattering study of ATP-dependent dark reactions. J. Photochem. Photobiol., B 1989, 3 (4), 529-48.
45. McConnell, D. G.; Rafferty, C. N.; Dilley, R. A. The light-induced proton uptake in bovine retinal outer segment fragments. J. Biol. Chem. 1968, 243 (22), 5820-6.
46. Kaupp, U. B.; Schnetkamp, P. P.; lunge, W. Rapid calcium release and proton uptake at the disk membrane of isolated cattle rod outer segments. 1. Stoichiometry of light-stimulated calcium release and proton uptake. Biochemistry 1981, 20 (19), 5500-10.
47. Biernbaum, M. S.; Bownds, M. D. Light-induced changes in GTP and ATP in frog rod photoreceptors. Comparison with recovery of dark current and light sensitivity during dark adaptation. J. Gen, Physiol, 1985, 85 (1), 107-21.
48. Olson, A.; Pugh, E. N., Jr. Diffusion coefficient of cyclic GMP in salamander rod outer segments estimated with two fluorescent probes. Biophys. J. 1993, 65 (3), 1335-52.