Evidence for aerobic metabolism in retinal rod outer segment disks

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 12, 2009, Pages 2555-2565

  Panfoli, Isabella ^a   Calzia, Daniela ^a   Bianchini, Paolo ^a   Ravera, Silvia ^a   Diaspro, Alberto ^b   Candiano, Giovanni ^c   Bachi, Angela ^d   Monticone, Massimiliano ^e   Aluigi, Maria Grazia ^a   Barabino, Stefano ^a   Calabria, Giovanni ^a   Rolando, Maurizio ^a   Tacchetti, Carlo ^a   Morelli, Alessandro ^a   Pepe, Isidoro M ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c G GASLINI INSTITUTE   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e Advanced Biotechnology Centre   (Italy)

Author keywords

Aerobic metabolism; Bioenergetics; F1F0 ATP synthase; Oxidative phosphorylation; Respiratory chain complexes

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIMYCIN A1; CITRATE SYNTHASE; FICOLL; MITOCHONDRIAL DNA; POTASSIUM CHANNEL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; RHODAMINE 123; ROTENONE; SUCCINIC ACID;

AEROBIC METABOLISM; ANIMAL TISSUE; ARTICLE; CELL ENERGY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SYNTHESIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OPTIC DISK; OPTICAL DENSITY; OXIDATIVE PHOSPHORYLATION; OXIMETRY; OXYGEN CONSUMPTION; PHOTOCHEMICAL QUENCHING; PHOTOTRANSDUCTION; PROTEIN LOCALIZATION; PROTON MOTIVE FORCE; QUANTITATIVE ANALYSIS; RESPIRATORY CHAIN; RETINA ROD OUTER SEGMENT; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATASES; AEROBIOSIS; ANIMALS; ANTIMYCIN A; CARRIER PROTEINS; CATTLE; CELL RESPIRATION; CELLS, CULTURED; ELECTRON TRANSPORT; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; NAD; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; POTASSIUM CYANIDE; RETINAL PHOTORECEPTOR CELL OUTER SEGMENT; RETINAL ROD PHOTORECEPTOR CELLS; ROTENONE; UNCOUPLING AGENTS;

VERTEBRATA;

EID: 70350523599     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.08.013     Document Type: Article

References (61)

1. Aicardi G., and Solaini G. Effects of niridazole and 5-nitroimidazoles on heart mitochondrial respiration. Biochem Pharmacol 31 (1982) 3703-3705
2. Albert A.D., and Boesze-Battaglia K. The role of cholesterol in rod outer segment membranes. Prog Lipid Res 44 (2005) 99-124
3. Ames III A., Walseth T.F., Heyman R.A., Barad M., Graeff R.M., and Goldberg N.D. Light-induced increases in cGMP metabolic flux correspond with electrical responses of photoreceptors. J Biol Chem 261 (1986) 13034-13042
4. +-ATP synthase in the extracellular ATP synthesis and proliferation of human umbilical vein endothelial cells. Mol Cancer Res 1 (2003) 931-939
5. Baracca A., Sgarbi G., Solaini G., and Lenaz G. Rhodamine 123 as a probe of mitochondrial membrane potential: evaluation of proton flux through F(0) during ATP synthesis. Biochim Biophys Acta 1606 (2003) 137-146
6. Berman S.B., Watkins S.C., and Hastings T.G. Quantitative biochemical and ultrastructural comparison of mitochondrial permeability transition in isolated brain and liver mitochondria: evidence for reduced sensitivity of brain mitochondria. Exp Neurol 164 (2000) 415-425
7. Beutner G., Ruck A., Riede B., Welte W., and Brdiczka D. Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett 39 (1996) 189-195
8. Bianchini P., Calzia D., Ravera S., Candiano G., Bachi A., Morelli A., et al. Live imaging of mammalian retina: rod outer segments are stained by conventional mitochondrial dyes. J Biomed Opt 13 (2008) 054017
9. Biernbaum M.S., and 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 85 (1985) 107-121
10. Bok D. Retinal photoreceptor-pigment epithelium interactions. Friedenwald lecture. Invest Ophthalmol Vis Sci 26 (1985) 1659-1694
11. Boyer P.D. The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66 (1997) 717-749
12. Braun R.D., Linsenmeier R.A., and Goldstick T.K. Oxygen consumption in the inner and outer retina of the cat. Invest Ophthalmol Vis Sci 36 (1995) 542-554
13. Capaldi R.A., Aggeler R., Turina P., and Wilkens S. Coupling between catalytic sites and the proton channel in F1F0-type ATPases. Trends Biochem Sci 19 (1994) 284-289
14. Carretta A., and Cavaggioni A. On the metabolism of the rod outer segments. J Physiol 257 (1976) 687-697
15. Chi S.L., and Pizzo S.V. Cell surface F1Fo ATP synthase: a new paradigm?. Ann Med 38 (2006) 429-438
16. Chinopoulos C., Starkov A.A., and Fiskum G. Cyclosporin A-insensitive permeability transition in brain mitochondria: inhibition by 2-aminoethoxydiphenyl borate. J Biol Chem 278 (2003) 27382-27389
17. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255 (1988) 357-360
18. Emaus R.K., Grunwald R., and Lemasters J.J. Rhodamine 123 as a probe of transmembrane potential in isolated rat-liver mitochondria: spectral and metabolic properties. Biochim Biophys Acta 850 (1986) 436-448
19. Fabre A.C., Vantourout P., Champagne E., Terce F., Rolland C., Perret B., et al. Cell surface adenylate kinase activity regulates the F(1)-ATPase/P2Y (13)-mediated HDL endocytosis pathway on human hepatocytes. Cell Mol Life Sci 63 (2006) 2829-2837
20. Fain G.L., Matthews H.R., Cornwall M.C., and Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol Rev 81 (2001) 117-151
21. Finnemann S.C., Bonilha V.L., Marmorstein A.D., and Rodriguez-Boulan E. Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalisation. Proc Natl Acad Sci USA 94 (1997) 12932-12937
22. Genova M.L., Baracca A., Biondi A., Casalena G., Faccioli M., Falasca A.I., et al. Is supercomplex organization of the respiratory chain required for optimal electron transfer activity?. Biochim Biophys Acta 1777 (2008) 740-746
23. Hsu S.C., and Molday R.S. Glucose metabolism in photoreceptor outer segments. Its role in phototransduction and in NADPH-requiring reactions. J Biol Chem 269 (1994) 17954-17959
24. Janssen A.J., Trijbels F.J., Sengers R.C., Smeitink J.A., van den Heuvel L.P., Wintjes L.T., et al. Spectrophotometric assay for complex I of the respiratory chain in tissue samples and cultured fibroblasts. Clin Chem 53 (2007) 729-734
25. Jarskog L.F., and Gilmore J.H. Developmental expression of Bcl-2 protein in human cortex. Brain Res Dev Brain Res 119 (2000) 225-230
26. Kahlert S., Zundorf G., and Reiser G. Detection of de- and hyperpolarization of mitochondria of cultured astrocytes and neurons by the cationic fluorescent dye rhodamine 123. J Neurosci Methods 171 (2008) 87-92
27. Kaupp U.B., Schnetkamp P.P., and Junge 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 20 (1981) 5500-5510
28. Koch K.W., and Stryer L. Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334 (1988) 64-66
29. Kwok M.C., Holopainen J.M., Molday L.L., Foster L.J., and 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 7 (2008) 1053-1066
30. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
31. Lamb T.D., and Pugh Jr. E.N. Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest Ophthalmol Vis Sci 47 (2006) 5137-5152
32. Lamba O.P., Borchman D., and O'Brien P.J. Fourier transform infrared study of the rod outer segment disk and plasma membranes of vertebrate retina. Biochemistry 33 (1994) 704-712
33. Mangiullo R., Gnoni A., Leone A., Gnoni G.V., Papa S., and Zanotti F. Structural and functional characterization of F(o)F(1)-ATP synthase on the extracellular surface of rat hepatocytes. Biochim Biophys Acta 1777 (2008) 1326-1335
34. Maniatis T., Fritsch E.F., and Sambrook J. Molecular Cloning; a Laboratory Manual (1982), Cold Spring Harbor Laboratory Press, New York
35. Martinez L.O., Jacquet S., Esteve J.P., Rolland C., Cabezon E., Champagne E., et al. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 421 (2003) 75-79
36. McConnell D.G., Rafferty C.N., and Dilley R.A. The light-induced proton uptake in bovine retinal outer segment fragments. J Biol Chem 243 (1968) 5820-5826
37. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191 (1961) 144-148
38. Nickell S., Park P.S., Baumeister W., and Palczewski K. Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J Cell Biol 177 (2007) 917-925
39. Olson A., and Pugh Jr. E.N. Diffusion coefficient of cyclic GMP in salamander rod outer segments estimated with two fluorescent probes. Biophys J 65 (1993) 1335-1352
40. Orlov N.Y., Orlova T.G., Nomura K., Hanai N., and Kimura N. Transducin-mediated, isoform-specific interaction of recombinant rat nucleoside diphosphate kinases with bleached bovine retinal rod outer segment membranes. FEBS Lett 389 (1996) 186-190
41. Panfoli I., Musante L., Bachi A., Ravera S., Calzia D., Cattaneo A., et al. Proteomic analysis of the retinal rod outer segment disks. J Proteome Res 7 (2008) 2654-2669
42. Pepe I.M. Recent advances in our understanding of rhodopsin and phototransduction. Prog Retin Eye Res 20 (2001) 733-759
43. Poot M., Zhang Y.Z., Kramer J., Wells K.S., Jones L.J., Hanzel D.K., et al. Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J Histochem Cytochem 44 (1996) 1363-1372
44. Quillen E.E., Haslam G.C., Samra H.S., Amani-Taleshi D., Knight J.A., Wyatt D.E., et al. Ectoadenylate kinase and plasma membrane ATP synthase activities of human vascular endothelial cells. J Biol Chem 281 (2006) 20728-20737
45. Ravera S., Calzia D., Bianchini P., Diaspro A., and Panfoli I. Confocal laser scanning microscopy of retinal rod outer segment intact disks: new labeling technique. J Biomed Opt 12 (2007) 050501
46. Ravera S., Calzia D., Panfoli I., Pepe I.M., and Morelli A. Simultaneous detection of molecular weight and activity of adenylate kinases after electrophoretic separation. Electrophoresis 28 (2007) 291-300
47. Ravera S., Panfoli I., Calzia D., Aluigi M.G., Bianchini P., Diaspro A., et al. Evidence for aerobic ATP synthesis in isolated myelin vesicles. Int J Biochem Cell Biol 41 (2009) 1581-1591
48. Ridge K.D., Abdulaev N.G., Sousa M., and Palczewski K. Phototransduction: crystal clear. Trends Biochem Sci 28 (2003) 479-487
49. Rozen S., and Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132 (2000) 365-386
50. Schnetkamp P.P., and Daemen F.J. Isolation and characterization of osmotically sealed bovine rod outer segments. Methods Enzymol 81 (1982) 110-116
51. Sgobbo P., Pacelli C., Grattagliano I., Villani G., and Cocco T. Carvedilol inhibits mitochondrial complex I and induces resistance to H2O2 -mediated oxidative insult in H9C2 myocardial cells. Biochim Biophys Acta 1767 (2007) 222-232
52. Smith Jr. H.G., and Litman B.J. Preparation of osmotically intact rod outer segment disks by Ficoll flotation. Methods Enzymol 81 (1982) 57-61
53. Sottocasa G.L., Kuylenstierna B., Ernster L., and Bergstrand A. An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J Cell Biol 32 (1967) 415-438
54. Stryer L. Vision: from photon to perception. Proc Natl Acad Sci USA 93 (1996) 557-559
55. Turina P., Melandri B.A., and Graber P. ATP synthesis in chromatophores driven by artificially induced ion gradients. Eur J Biochem 196 (1991) 225-229
56. Uckermann O., Iandiev I., Francke M., Franze K., Grosche J., Wolf S., et al. Selective staining by vital dyes of Muller glial cells in retinal wholemounts. Glia 45 (2004) 59-66
57. Uhl R., Borys T., and Abrahamson E.W. Evidence for structural changes in the photoreceptor disk membrane, enabled by magnesium ATPase activity and triggered by light. FEBS Lett 107 (1979) 317-322
58. Uhl R., and Desel H. Optical probes of intradiskal processes in rod photoreceptors. II: light-scattering study of ATP-dependent light reactions. J Photochem Photobiol B 3 (1989) 549-564
59. Uhl R., Zellmann-Kraska R., and Desel H. Optical probes of intradiskal processes in rod photoreceptors. I: light-scattering study of ATP-dependent dark reactions. J Photochem Photobiol B 3 (1989) 529-548
60. Wallace D.C. Mitochondrial diseases in man and mouse. Science 283 (1999) 1482-1488
61. Zeviani M., and Di Donato S. Mitochondrial disorders. Brain 127 (2004) 2153-2172