| |
Are Rod Outer Segment ATP-ase and ATP-Synthase Activity Expression of the Same Protein?
- 作者:Daniela Calzia (1)
Simona Candiani (2) Greta Garbarino (2) Federico Caicci (3) Silvia Ravera (1) Maurizio Bruschi (4) Lucia Manni (3) Alessandro Morelli (1) Carlo Enrico Traverso (5) Giovanni Candiano (4) Carlo Tacchetti (6) Isabella Panfoli (1)
- 关键词:ATPase ; F1Fo ; ATP synthase ; IF1 ; Rod outer segments
- 刊名:Cellular and Molecular Neurobiology
- 出版年:2013
- 出版时间:July 2013
- 年:2013
- 卷:33
- 期:5
- 页码:637-649
- 全文大小:775KB
- 参考文献: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鈥?28 CrossRef
2. Arakaki N, Nagao T, Niki R, Toyofuku A, Tanaka H, Kuramoto Y, Emoto Y, Shibata H, Magota K, Higuti T (2003) 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(13):931鈥?39 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鈥?25 CrossRef 4. Berson EL (1971) Light deprivation for early retinitis pigmentosa. A hypothesis. Arch Ophthalmol 85(5):521鈥?29 CrossRef 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鈥?):189鈥?95 CrossRef 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 CrossRef 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鈥?21 CrossRef 8. Bonting SL, Caravaggio LL, Canady MR (1964) Studies on sodium鈥損otassium activated adenosine triphosphatase. X. occurrence in retinal rods and relation to rhodopsin. Exp Eye Res 3:47鈥?6 CrossRef 9. Boyer PD (1997) The ATP synthase: a splendid molecular machine. Annu Rev Biochem 66:717鈥?49 CrossRef 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鈥?9676 CrossRef 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鈥?31 CrossRef 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鈥?745 CrossRef 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鈥?415 CrossRef 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鈥?5464 CrossRef 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鈥?50 CrossRef 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鈥?7389 CrossRef 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鈥?00 CrossRef 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鈥?21 CrossRef 19. Fabre I, Gallarda T (2006) Vascular depression: important and limited issues of the concept. Encephale 32(Pt 4):S1141鈥揝1144 CrossRef 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鈥?2937 CrossRef 21. Frank RN, Goldsmith TH (1965) Adenosine triphosphatase activity in the rod outer segments of the pig retina. Arch Biochem Biophys 110(3):517鈥?25 CrossRef 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鈥?251. doi:10.1126/science.1189157 CrossRef 23. Green DW, Grover GJ (2000) The IF(1) inhibitor protein of the mitochondrial F(1)F(0)-ATPase. Biochim Biophys Acta 1458(2鈥?):343鈥?55 24. Hayashi T, Rizzuto R, Hajnoczky G, Su TP (2009) MAM: more than just a housekeeper. Trends Cell Biol 19(2):81鈥?8 CrossRef 25. Hemminki K (1975) Localization of ATPase in bovine retinal outer segments. Exp Eye Res 20(1):79鈥?8 CrossRef 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鈥?1752 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鈥?7959 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鈥?51 29. Kann O, Kovacs R (2007) Mitochondria and neuronal activity. Am J Physiol 292(2):C641鈥揅657 CrossRef 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鈥?510 CrossRef 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鈥?925 CrossRef 32. Krishnadev N, Meleth AD, Chew EY (2010) Nutritional supplements for age-related macular degeneration. Curr Opin Ophthalmol 21(3):184鈥?89 CrossRef 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鈥?598 CrossRef 34. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680鈥?85 CrossRef 35. Lamb TD, Pugh EN Jr (2006) Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest Ophthalmol Vis Sci 47(12):5137鈥?152 CrossRef 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鈥?54 CrossRef 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鈥?44. doi:10.1007/978-1-4614-3573-0_5 CrossRef 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鈥?604 CrossRef 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鈥?1 CrossRef 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鈥?1 CrossRef 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鈥?335 CrossRef 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鈥?9 CrossRef 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鈥?826 44. Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144鈥?48 CrossRef 45. Morelli A, Ravera S, Panfoli I (2011) Hypothesis of an energetic function for myelin. Cell Biochem Biophys 61(1):179鈥?87 CrossRef 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鈥?661 CrossRef 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鈥?921. doi:10.1016/j.cub.2008.10.029 CrossRef 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鈥?686 CrossRef 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鈥?30 CrossRef 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鈥?669 CrossRef 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鈥?565 CrossRef 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鈥?39 CrossRef 54. Pepe IM (2001) Recent advances in our understanding of rhodopsin and phototransduction. Prog Retin Eye Res 20(6):733鈥?59 CrossRef 55. Pullman ME, Monroy GC (1963) A naturally occurring inhibitor of mitochondrial adenosine triphosphatase. J Biol Chem 238:3762鈥?769 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鈥?0737 CrossRef 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鈥?591 CrossRef 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鈥?0 CrossRef 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鈥?0 CrossRef 60. Ridge KD, Abdulaev NG, Sousa M, Palczewski K (2003) Phototransduction: crystal clear. Trends Biochem Sci 28(9):479鈥?87 CrossRef 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鈥?73 CrossRef 62. Sachs G, Chang HH, Rabon E, Schackman R, Lewin M, Saccomani G (1976) A nonelectrogenic H+ pump in plasma membranes of hog stomach. J Biol Chem 251(23):7690鈥?698 63. Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science 283(5407):1488鈥?493 CrossRef 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鈥?456 CrossRef 65. Schnetkamp PP, Daemen FJ (1982) Isolation and characterization of osmotically sealed bovine rod outer segments. Methods Enzymol 81:110鈥?16 CrossRef 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鈥?00 CrossRef 67. Shintani K, Shechtman DL, Gurwood AS (2009) Review and update: current treatment trends for patients with retinitis pigmentosa. Optometry 80(7):384鈥?01 CrossRef 68. Silver I, Erecinska M (1998) Oxygen and ion concentrations in normoxic and hypoxic brain cells. Adv Exp Med Biol 454:7鈥?6 CrossRef 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鈥?55 70. Stock D, Leslie AG, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286(5445):1700鈥?705 CrossRef 71. Stryer L (1996) Vision: from photon to perception. Proc Natl Acad Sci USA 93(2):557鈥?59 CrossRef 72. Thacher SM (1978) Light-stimulated, magnesium-dependent ATPase in toad retinal rod outer segments. Biochemistry 17(15):3005鈥?011 CrossRef 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鈥?64 CrossRef 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鈥?06 CrossRef 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鈥?48 CrossRef 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鈥?533 CrossRef 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鈥?9 CrossRef 78. Wallace DC (1999) Mitochondrial diseases in man and mouse. Science 283(5407):1482鈥?488 CrossRef 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鈥?07 CrossRef 80. Zanotti F, Gnoni A, Mangiullo R, Papa S (2009) Effect of the ATPase inhibitor protein IF1 on H+ translocation in the mitochondrial ATP synthase complex. Biochem Biophys Res Commun 384(1):43鈥?8 CrossRef 81. Zeviani M, Di Donato S (2004) Mitochondrial disorders. Brain 127(Pt 10):2153鈥?172 CrossRef
- 作者单位:Daniela Calzia (1)
Simona Candiani (2) Greta Garbarino (2) Federico Caicci (3) Silvia Ravera (1) Maurizio Bruschi (4) Lucia Manni (3) Alessandro Morelli (1) Carlo Enrico Traverso (5) Giovanni Candiano (4) Carlo Tacchetti (6) Isabella Panfoli (1)
1. DIFAR, Universit脿 di Genova, Genoa, Italy 2. DISTAV, Universit脿 di Genova, Genoa, Italy 3. Dipartimento di Biologia, Universit脿 di Padova, Padua, Italy 4. Laboratorio di Fisiopatologia dell鈥橴remia, Istituto G. Gaslini, Genoa, Italy 5. Clinica Oculistica-DINOGMI, Universit脿 di Genova, Genoa, Italy 6. IFOM Centro di Oncologia cellulare e Ultrastruttura, Dipartimento di Medicina Sperimentale, Universit脿 degli Studi di Genova, Genoa, Italy
- ISSN:1573-6830
文摘
Vertebrate retinal rod outer segments (OS) consist of a stack of disks surrounded by the plasma membrane, where phototransduction takes place. Energetic metabolism in rod OS remains obscure. Literature described a so-called Mg2+-dependent ATPase activity, while our previous results demonstrated the presence of oxidative phosphorylation (OXPHOS) in OS, sustained by an ATP synthetic activity. Here we propose that the OS ATPase and ATP synthase are the expression of the same protein, i.e., of F1Fo-ATP synthase. Imaging on bovine retinal sections showed that some OXPHOS proteins are expressed in the OS. Biochemical data on bovine purified rod OS, characterized for purity, show an ATP synthase activity, inhibited by classical F1Fo-ATP synthase inhibitors. Moreover, OS possess a pH-dependent ATP hydrolysis, inhibited by pH values below 7, suggestive of the functioning of the inhibitor of F1 (IF1) protein. WB confirmed the presence of IF1 in OS, substantiating the expression of F1Fo ATP synthase in OS. Data suggest that the OS F1Fo ATP synthase is able to hydrolyze or synthesize ATP, depending on in vitro or in vivo conditions and that the role of IF1 would be pivotal in the prevention of the reversal of ATP synthase in OS, for example during hypoxia, granting photoreceptor survival.
| |
NGLC 2004-2010.National Geological Library of China All Rights Reserved.
Add:29 Xueyuan Rd,Haidian District,Beijing,PRC. Mail Add: 8324 mailbox 100083
For exchange or info please contact us via email.
| |