Are rod outer segment ATP-ase and ATP-synthase activity expression of the same protein?

Cellular and Molecular Neurobiology

Volumn 33, Issue 5, 2013, Pages 637-649

  Calzia, Daniela ^a   Candiani, Simona ^a   Garbarino, Greta ^a   Caicci, Federico ^b   Ravera, Silvia ^a   Bruschi, Maurizio ^c   Manni, Lucia ^b   Morelli, Alessandro ^a   Traverso, Carlo Enrico ^a   Candiano, Giovanni ^c   Tacchetti, Carlo ^a   Panfoli, Isabella ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c G GASLINI INSTITUTE   (Italy)

Author keywords

ATPase; F1Fo ATP synthase; IF1; Rod outer segments

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; IF1 PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG; METHYLENE BLUE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COW; ENZYME ACTIVITY; ENZYME INHIBITION; HYDROLYSIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RETINA ROD OUTER SEGMENT; TISSUE SECTION; WESTERN BLOTTING; ANIMAL; BIOLOGICAL MODEL; BOVINAE; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; OXIDATION REDUCTION REACTION; ULTRASTRUCTURE;

BOVINAE; VERTEBRATA;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; CATTLE; FLUORESCENT ANTIBODY TECHNIQUE; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; METHYLENE BLUE; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; PROTON-TRANSLOCATING ATPASES; ROD CELL OUTER SEGMENT;

EID: 84878677250     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-013-9926-7     Document Type: Article

References (81)

1. Abrahams JP, Leslie AG, Lutter R, Walker JE (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370(6491):621-628
2. +-ATP synthase in the extracellular ATP synthesis and proliferation of human umbilical vein endothelial cells. Mol Cancer Res 1(13):931-939
3. Berman SB, Watkins SC, Hastings TG (2000) 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(2):415-425
4. Berson EL (1971) Light deprivation for early retinitis pigmentosa. A hypothesis. Arch Ophthalmol 85(5):521-529
5. Beutner G, Ruck A, Riede B, Welte W, Brdiczka D (1996) Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett 396(2-3):189-195
6. Bianchini P, Calzia D, Ravera S, Candiano G, Bachi A, Morelli A, Bruschi M, Pepe IM, Diaspro A, Panfoli I (2008) Live imaging of mammalian retina: rod outer segments are stained by conventional mitochondrial dyes. J Biomed Opt 13(5):054017
7. Biernbaum MS, Bownds MD (1985) 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(1):107-121
8. Bonting SL, Caravaggio LL, Canady MR (1964) Studies on sodium-potassium activated adenosine triphosphatase. X. occurrence in retinal rods and relation to rhodopsin. Exp Eye Res 3:47-56
9. Boyer PD (1997) The ATP synthase: a splendid molecular machine. Annu Rev Biochem 66:717-749
10. Burrell HE, Wlodarski B, Foster BJ, Buckley KA, Sharpe GR, Quayle JM, Simpson AW, Gallagher JA (2005) Human keratinocytes release ATP and utilize three mechanisms for nucleotide interconversion at the cell surface. J Biol Chem 280(33):29667-29676
11. Burstedt MS, Ristoff E, Larsson A, Wachtmeister L (2009) Rod-cone dystrophy with maculopathy in genetic glutathione synthetase deficiency: a morphologic and electrophysiologic study. Ophthalmology 116(2):324-331
12. Burwick NR, Wahl ML, Fang J, Zhong Z, Moser TL, Li B, Capaldi RA, Kenan DJ, Pizzo SV (2005) An inhibitor of the F1 subunit of ATP synthase (IF1) modulates the activity of angiostatin on the endothelial cell surface. J Biol Chem 280(3):1740-1745
13. Bygrave FL, Lehninger AL (1967) The affinity of mitochondrial oxidative phosphorylation mechanisms for phosphate and adenosine diphosphate. Proc Natl Acad Sci USA 57(5):1409-1415
14. Cabezon E, Butler PJ, Runswick MJ, Walker JE (2000) Modulation of the oligomerization state of the bovine F1-ATPase inhibitor protein, IF1, by pH. J Biol Chem 275(33):25460-25464
15. Cabezon E, Montgomery MG, Leslie AG, Walker JE (2003) The structure of bovine F1-ATPase in complex with its regulatory protein IF1. Nat Struct Biol 10(9):744-750
16. Chinopoulos C, Starkov AA, Fiskum G (2003) Cyclosporin A-insensitive permeability transition in brain mitochondria: inhibition by 2-aminoethoxydiphenyl borate. J Biol Chem 278(30):27382-27389
17. Contessi S, Comelli M, Cmet S, Lippe G, Mavelli I (2007) IF(1) distribution in HepG2 cells in relation to ecto-F(0)F (1)ATPsynthase and calmodulin. J Bioenerg Biomembr 39(4):291-300
18. Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnoczky G (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174(7):915-921
19. Fabre I, Gallarda T (2006) Vascular depression: important and limited issues of the concept. Encephale 32(Pt 4):S1141-S1144
20. Finnemann SC, Bonilha VL, Marmorstein AD, Rodriguez-Boulan E (1997) 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 USA 94(24):12932-12937
21. Frank RN, Goldsmith TH (1965) Adenosine triphosphatase activity in the rod outer segments of the pig retina. Arch Biochem Biophys 110(3):517-525
22. Giorgi C, Ito K, Lin HK, Santangelo C, Wieckowski MR, Lebiedzinska M, Bononi A, Bonora M, Duszynski J, Bernardi R, Rizzuto R, Tacchetti C, Pinton P, Pandolfi PP (2010) PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 330(6008):1247-1251. doi: 10.1126/science.1189157
23. Green DW, Grover GJ (2000) The IF(1) inhibitor protein of the mitochondrial F(1)F(0)-ATPase. Biochim Biophys Acta 1458(2-3):343-355
24. Hayashi T, Rizzuto R, Hajnoczky G, Su TP (2009) MAM: more than just a housekeeper. Trends Cell Biol 19(2):81-88
25. Hemminki K (1975) Localization of ATPase in bovine retinal outer segments. Exp Eye Res 20(1):79-88
26. Hsu SC, Molday RS (1991) Glycolytic enzymes and a GLUT-1 glucose transporter in the outer segments of rod and cone photoreceptor cells. J Biol Chem 266(32):21745-21752
27. Hsu SC, Molday RS (1994) Glucose metabolism in photoreceptor outer segments. Its role in phototransduction and in NADPH-requiring reactions. J Biol Chem 269(27):17954-17959
28. Ikemoto N (1974) The calcium binding sites involved in the regulation of the purified adenosine triphosphatase of the sarcoplasmic reticulum. J Biol Chem 249(2):649-651
29. Kann O, Kovacs R (2007) Mitochondria and neuronal activity. Am J Physiol 292(2):C641-C657
30. Kaupp UB, Schnetkamp PP, Junge W (1981) 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(19):5500-5510
31. Klein G, Satre M, Dianoux AC, Vignais PV (1980) Radiolabeling of natural adenosine triphosphatase inhibitor with phenyl (14C)isothiocyanate and study of its interaction with mitochondrial adenosine triphosphatase. Localization of inhibitor binding sites and stoichiometry of binding. Biochemistry 19(13):2919-2925
32. Krishnadev N, Meleth AD, Chew EY (2010) Nutritional supplements for age-related macular degeneration. Curr Opin Ophthalmol 21(3):184-189
33. Krull KW, Schuster SM (1981) Kinetic studies of beef heart mitochondrial adenosine triphosphatase: interaction of the inhibitor protein and adenosine triphosphate analogues. Biochemistry 20(6):1592-1598
34. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680-685
35. Lamb TD, Pugh EN Jr (2006) Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest Ophthalmol Vis Sci 47(12):5137-5152
36. Lebowitz MS, Pedersen PL (1996) Protein inhibitor of mitochondrial ATP synthase: relationship of inhibitor structure to pH-dependent regulation. Arch Biochem Biophys 330(2):342-354
37. Lenaz G, Genova ML (2012) Supramolecular organisation of the mitochondrial respiratory chain: a new challenge for the mechanism and control of oxidative phosphorylation. Adv Exp Med Biol 748:107-144. doi: 10.1007/978-1-4614-3573-0-5
38. Linton JD, Holzhausen LC, Babai N, Song H, Miyagishima KJ, Stearns GW, Lindsay K, Wei J, Chertov AO, Peters TA, Caffe R, Pluk H, Seeliger MW, Tanimoto N, Fong K, Bolton L, Kuok DL, Sweet IR, Bartoletti TM, Radu RA, Travis GH, Zagotta WN, Townes-Anderson E, Parker E, Van der Zee CE, Sampath AP, Sokolov M, Thoreson WB, Hurley JB (2010) Flow of energy in the outer retina in darkness and in light. Proc Natl Acad Sci USA 107(19):8599-8604
39. Lippe G, Sorgato MC, Harris DA (1988a) The binding and release of the inhibitor protein are governed independently by ATP and membrane potential in ox-heart submitochondrial vesicles. Biochim Biophys Acta 933(1):12-21
40. Lippe G, Sorgato MC, Harris DA (1988b) Kinetics of the release of the mitochondrial inhibitor protein. Correlation with synthesis and hydrolysis of ATP. Biochim Biophys Acta 933(1):1-11
41. Mangiullo R, Gnoni A, Leone A, Gnoni GV, Papa S, Zanotti F (2008) Structural and functional characterization of F(o)F(1)-ATP synthase on the extracellular surface of rat hepatocytes. Biochim Biophys Acta 1777(10):1326-1335
42. Martinez LO, Jacquet S, Esteve JP, Rolland C, Cabezon E, Champagne E, Pineau T, Georgeaud V, Walker JE, Terce F, Collet X, Perret B, Barbaras R (2003) Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 421(6918):75-79
43. McConnell DG, Rafferty CN, Dilley RA (1968) The light-induced proton uptake in bovine retinal outer segment fragments. J Biol Chem 243(22):5820-5826
44. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144-148
45. Morelli A, Ravera S, Panfoli I (2011) Hypothesis of an energetic function for myelin. Cell Biochem Biophys 61(1):179-187
46. Moser TL, Kenan DJ, Ashley TA, Roy JA, Goodman MD, Misra UK, Cheek DJ, Pizzo SV (2001) Endothelial cell surface F1-F0 ATP synthase is active in ATP synthesis and is inhibited by angiostatin. Proc Natl Acad Sci USA 98(12):6656-6661
47. Okawa H, Sampath AP, Laughlin SB, Fain GL (2008) ATP consumption by mammalian rod photoreceptors in darkness and in light. Curr Biol 18(24):1917-1921. doi: 10.1016/j.cub.2008.10.029
48. Ostwald TJ, Heller J (1972) Properties of a magnesium- or calcium-dependent adenosine triphosphatase from frog rod photoreceptor outer segment disks and its inhibition by illumination. Biochemistry 11(25):4679-4686
49. Panchenko MV, Vinogradov AD (1985) Interaction between the mitochondrial ATP synthetase and ATPase inhibitor protein. Active/inactive slow pH-dependent transitions of the inhibitor protein. FEBS Lett 184(2):226-230
50. Panfoli I, Musante L, Bachi A, Ravera S, Calzia D, Cattaneo A, Bruschi M, Bianchini P, Diaspro A, Morelli A, Pepe IM, Tacchetti C, Candiano G (2008) Proteomic analysis of the retinal rod outer segment disks. J Proteome Res 7(7):2654-2669
51. Panfoli I, Calzia D, Bianchini P, Ravera S, Diaspro A, Candiano G, Bachi A, Monticone M, Aluigi MG, Barabino S, Calabria G, Rolando M, Tacchetti C, Morelli A, Pepe IM (2009) Evidence for aerobic metabolism in retinal rod outer segment disks. Int J Biochem Cell Biol 41(12):2555-2565
52. Panfoli I, Calzia D, Ravera S et al (2011a) Extramitochondrial tricarboxylic acid cycle in retinal rod outer segments. Biochimie. doi: 10.1016/j.biochi.2011.05.020
53. Panfoli I, Ravera S, Bruschi M, Candiano G, Morelli A (2011b) Proteomics unravels the exportability of mitochondrial respiratory chains. Expert Rev Proteomics 8(2):231-239
54. Pepe IM (2001) Recent advances in our understanding of rhodopsin and phototransduction. Prog Retin Eye Res 20(6):733-759
55. Pullman ME, Monroy GC (1963) A naturally occurring inhibitor of mitochondrial adenosine triphosphatase. J Biol Chem 238:3762-3769
56. Quillen EE, Haslam GC, Samra HS, Amani-Taleshi D, Knight JA, Wyatt DE, Bishop SC, Colvert KK, Richter ML, Kitos PA (2006) Ectoadenylate kinase and plasma membrane ATP synthase activities of human vascular endothelial cells. J Biol Chem 281(30):20728-20737
57. Ravera S, Panfoli I, Calzia D, Aluigi MG, Bianchini P, Diaspro A, Mancardi G, Morelli A (2009) Evidence for aerobic ATP synthesis in isolated myelin vesicles. Int J Biochem Cell Biol 41(7):1581-1591
58. Ravera S, Panfoli I, Aluigi MG, Calzia D, Morelli A (2010) Characterization of myelin sheath F(o)F (1)-ATP synthase and its regulation by IF (1). Cell Biochem Biophys 59(2):63-70
59. Ravera S, Panfoli I, Aluigi MG, Calzia D, Morelli A (2011) Characterization of myelin sheath F(o)F(1)-ATP synthase and its regulation by IF(1). Cell Biochem Biophys 59(2):63-70
60. Ridge KD, Abdulaev NG, Sousa M, Palczewski K (2003) Phototransduction: crystal clear. Trends Biochem Sci 28(9):479-487
61. Rouslin W (1986) Myocardial acidosis and the mitigation of tissue ATP depletion in ischemic cardiac muscle: the role of the mitochondrial ATPase. Adv Exp Med Biol 194:355-373
62. + pump in plasma membranes of hog stomach. J Biol Chem 251(23):7690-7698
63. Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science 283(5407):1488-1493
64. Schnetkamp PP (1981) Metabolism in the cytosol of intact isolated cattle rod outer segments as indicator for cytosolic calcium and magnesium ions. Biochemistry 20(9):2449-2456
65. Schnetkamp PP, Daemen FJ (1982) Isolation and characterization of osmotically sealed bovine rod outer segments. Methods Enzymol 81:110-116
66. Sgarbi G, Baracca A, Lenaz G, Valentino LM, Carelli V, Solaini G (2006) 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(3):493-500
67. Shintani K, Shechtman DL, Gurwood AS (2009) Review and update: current treatment trends for patients with retinitis pigmentosa. Optometry 80(7):384-401
68. Silver I, Erecinska M (1998) Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv Exp Med Biol 454:7-16
69. Soltys BJ, Kang D, Gupta RS (2000) Localization of P32 protein (gC1q-R) in mitochondria and at specific extramitochondrial locations in normal tissues. Histochem Cell Biol 114(3):245-255
70. Stock D, Leslie AG, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286(5445):1700-1705
71. Stryer L (1996) Vision: from photon to perception. Proc Natl Acad Sci USA 93(2):557-559
72. Thacher SM (1978) Light-stimulated, magnesium-dependent ATPase in toad retinal rod outer segments. Biochemistry 17(15):3005-3011
73. Uhl R, Desel H (1989) Optical probes of intradiskal processes in rod photoreceptors. II: light-scattering study of ATP-dependent light reactions. J Photochem Photobiol 3(4):549-564
74. Uhl R, Borys T, Abrahamson EW (1979) Evidence for a magnesium dependent ATPase in bovine rod outer segment disk membranes. Photochem Photobiol 29(4):703-706
75. Uhl R, Zellmann-Kraska R, Desel H (1989) Optical probes of intradiskal processes in rod photoreceptors I: Light-scattering study of ATP-dependent dark reactions. J Photochem Photobiol 3(4):529-548
76. Van Raaij MT, Oortgiesen M, Timmerman HH, Dobbe CJ, Van Loveren H (1996) Time-dependent differential changes of immune function in rats exposed to chronic intermittent noise. Physiol Behav 60(6):1527-1533
77. Vingolo EM, Pelaia P, Forte R, Rocco M, Giusti C, Rispoli E (1998) Does hyperbaric oxygen (HBO) delivery rescue retinal photoreceptors in retinitis pigmentosa? Doc Ophthalmol 97(1):33-39
78. Wallace DC (1999) Mitochondrial diseases in man and mouse. Science 283(5407):1482-1488
79. Wellard J, Lee D, Valter K, Stone J (2005) Photoreceptors in the rat retina are specifically vulnerable to both hypoxia and hyperoxia. Vis Neurosci 22(4):501-507
80. + translocation in the mitochondrial ATP synthase complex. Biochem Biophys Res Commun 384(1):43-48
81. Zeviani M, Di Donato S (2004) Mitochondrial disorders. Brain 127(Pt 10):2153-2172