Evidence for aerobic ATP synthesis in isolated myelin vesicles

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 7, 2009, Pages 1581-1591

  Ravera, Silvia ^a   Panfoli, Isabella ^a   Calzia, Daniela ^a   Aluigi, Maria Grazia ^a   Bianchini, Paolo ^b   Diaspro, Alberto ^b   Mancardi, Gianluigi ^a   Morelli, Alessandro ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b MicroScoBiO Research Center   (Italy)

Author keywords

ATP synthase; Myelin; Neuroenergetics; Oxygen absorption; Respiratory complexes

Indexed keywords

ADENOSINE TRIPHOSPHATE; MYELIN; MYELIN BASIC PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

AEROBIC METABOLISM; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BODY WEIGHT; BREATHING RATE; CONFOCAL LASER MICROSCOPY; IMMUNOHISTOCHEMISTRY; ISOLATION PROCEDURE; MYELIN SHEATH; NERVE FIBER MEMBRANE; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE; OXYGEN CONSUMPTION; PROTEIN LOCALIZATION; PROTEOMICS; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; AEROBIOSIS; ANIMALS; BLOTTING, WESTERN; CATTLE; CELL RESPIRATION; CYTOPLASMIC VESICLES; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MYELIN BASIC PROTEINS; MYELIN SHEATH; OPTIC NERVE; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PROSENCEPHALON; PROTEIN TRANSPORT; PROTON-TRANSLOCATING ATPASES; PROTONS; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 63049100743     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.01.009     Document Type: Article

References (61)

1. Ames III A. CNS energy metabolism as related to function. Brain Res Brain Res Rev 34 (2000) 42-68
2. Arakaki N., Nagao T., Niki R., Toyofuku A., Tanaka H., Kuramoto Y., et al. Possible role of cell surface H+-ATP synthase in the extracellular ATP synthesis and proliferation of human umbilical vein endothelial cells. Mol Cancer Res 1 (2003) 931-939
3. Attwell D., and Laughlin S.B. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21 (2001) 1133-1145
4. +)ATPase after in vitro hypoxia and reoxygenation are affected by methods of membrane preparation. J Neurosci Methods 79 (1998) 201-206
5. Balice-Gordon R.J., Bone L.J., and Scherer S.S. Functional gap junctions in the Schwann cell myelin sheath. J Cell Biol 142 (1998) 1095-1104
6. 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
7. Baumann N., and Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81 (2001) 871-927
8. Berger P., Niemann A., and Suter U. Schwann cells and the pathogenesis of inherited motor and sensory neuropathies (Charcot-Marie-Tooth disease). Glia 54 (2006) 243-257
9. 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 396 (1996) 189-195
10. 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
11. Boyer P.D. The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66 (1997) 717-749
12. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
13. Chi S.L., and Pizzo S.V. Cell surface F1Fo ATP synthase: a new paradigm?. Ann Med 38 (2006) 429-438
14. 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
15. Correale J., Mel F., and Ysrraeli C. Neuronal injury in multiple sclerosis. Medicina (B. Aires) 66 (2006) 472-485
16. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341 (1999) 233-249
17. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255 (1988) 357-360
18. Crotty W.J., and Ledbetter M.C. Membrane continuities involving chloroplasts and other organelles in plant cells. Science 182 (1973) 839-841
19. Diaz R.S., and Monreal J. Unusual low proton permeability of liposomes prepared from the endogenous myelin lipids. J Neurochem 62 (1994) 2022-2029
20. Duffy T.E., Kohle S.J., and Vannucci R.C. Carbohydrate and energy metabolism in perinatal rat brain: relation to survival in anoxia. J Neurochem 24 (1975) 271-276
21. Edgar J.M., McCulloch M.C., Thomson C.E., and Griffiths I.R. Distribution of mitochondria along small-diameter myelinated central nervous system axons. J Neurosci Res 86 (2008) 2250-2257
22. 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
23. Ferguson B., Matyszak M.K., Esiri M.M., and Perry V.H. Axonal damage in acute multiple sclerosis lesions. Brain 120 Pt 3 (1997) 393-399
24. Goldberg G.S., Moreno A.P., and Lampe P.D. Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and ATP. J Biol Chem 277 (2002) 36725-36730
25. Haines T.H., and Dencher N.A. Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Lett 528 (2002) 35-39
26. Hales K.G. The machinery of mitochondrial fusion, division, and distribution, and emerging connections to apoptosis. Mitochondrion 4 (2004) 285-308
27. Haley J.E., Samuels F.G., and Ledeen R.W. Study of myelin purity in relation to axonal contaminants. Cell Mol Neurobiol 1 (1981) 175-187
28. Hargittai P.T., and Lieberman E.M. Axon-glia interactions in the crayfish: glial cell oxygen consumption is tightly coupled to axon metabolism. Glia 4 (1991) 417-423
29. Heape A., Juguelin H., Fabre M., Boiron F., and Cassagne C. A quantitative developmental study of the peripheral nerve lipid composition during myelinogenesis in normal and trembler mice. Brain Res 390 (1986) 181-189
30. Hertz L., Peng L., and Dienel G.A. Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J Cereb Blood Flow Metab 27 (2007) 219-249
31. 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
32. 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
33. Kann O., and Kovacs R. Mitochondria and neuronal activity. Am J Physiol Cell Physiol 292 (2007) C641-C657
34. Korf J. Is brain lactate metabolized immediately after neuronal activity through the oxidative pathway?. J Cereb Blood Flow Metab 26 (2006) 1584-1586
35. Kursula P. The current status of structural studies on proteins of the myelin sheath. Int J Mol Med 8 (2001) 475-479 [Review]
36. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
37. 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
38. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191 (1961) 144-148
39. Morell P., and Norton W.T. Myelin. Sci Am 242 (1980) 88-90 92, 96 passim
40. Norton W.T., and Poduslo S.E. Myelination in rat brain: method of myelin isolation. J Neurochem 21 (1973) 749-757
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. Pellerin L., and Magistretti P.J. Neuroscience. Let there be (NADH) light. Science 305 (2004) 50-52
43. Poot M., Zhang Y.Z., Kramer J.A., 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. 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
45. Ravera S., Calzia D., Bianchini P., Diaspro A., and Panfoli I. Confocal laser scannino microscopy of retinal rod outer segment intact disks: new labeling technique. J Biomed Opt 12 (2007) 050501-050503
46. Schurr A. Lactate: the ultimate cerebral oxidative energy substrate?. J Cereb Blood Flow Metab 26 (2006) 142-152
47. Sgarbi G., Baracca A., Lenaz G., Valentino L.M., Carelli V., and Solaini G. Inefficient coupling between proton transport and ATP synthesis may be the pathogenic mechanism for NARP and Leigh syndrome resulting from the T8993G mutation in mtDNA. Biochem J 395 (2006) 493-500
48. 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
49. Shaw J.M., and Nunnari J. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol 12 (2002) 178-184
50. Silver I., and Erecinska M. Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv Exp Med Biol 454 (1998) 7-16
51. Sidell B.D. Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J Exp Biol 201 (1998) 1119-1128
52. Soltys B.J., and Gupta R.S. Mitochondrial-matrix proteins at unexpected locations: are they exported?. Trends Biochem Sci 24 (1999) 174-177
53. Soltys B.J., and Gupta R.S. Mitochondrial proteins at unexpected cellular locations: export of proteins from mitochondria from an evolutionary perspective. Int Rev Cytol 194 (2000) 133-196
54. Sottocasa G.L., Kuylenstierna B., Ernster L., and Bergstrand A. An electron-transport system associated with the outer membrane of liver mitochondria. J Cell Biol 32 (1967) 415-438
55. Taylor C.M., Marta C.B., Claycomb R.J., Han D.K., Rasband M.N., Coetzee T., et al. Proteomic mapping provides powerful insights into functional myelin biology. Proc Natl Acad Sci USA 101 (2004) 4643-4648
56. Tomasselli A.G., Schirmer R.H., and Noda L.H. Mitochondrial GTP-AMP phosphotransferase. 1. Purification and properties. Eur J Biochem 93 (1979) 257-262
57. Vanrobaeys F., Van Coster R., Dhondt G., Devreese B., and Van Beeumen J. Profiling of myelin proteins by 2D-gel electrophoresis and multidimensional liquid chromatography coupled to MALDI TOF-TOF mass spectrometry. J Proteome Res 4 (2005) 2283-2293
58. Veltri K., Espiritu M., and Singh G. Distinct genomic copy number in mitochondria of different mammalian organs. J Cell Physiol 143 (1990) 160-164
59. Wang H.Y., Jackson S.N., and Wood A.S. Direct MALDI-MS analysis of cardiolipin from rat organs sections. J Am Soc Mass Spectrom 18 (2007) 567-577
60. Werner H.B., Kuhlmann K., Shen S., Uecker M., Schardt A., Dimova K., et al. Proteolipid protein is required for transport of sirtuin 2 into CNS myelin. J Neurosci 27 (2007) 7717-7730
61. Zhang M., Mileykovskaya E., and Dowhan W. Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J Biol Chem 280 (2005) 29403-29408