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

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

Research output: Contribution to journal › Article

6 Citations (Scopus)

Abstract

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 F1F o-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 F1F o 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.

Original languageEnglish
Pages (from-to)637-649
Number of pages13
JournalCellular and Molecular Neurobiology
Volume33
Issue number5
DOIs
Publication statusPublished - Jul 2013

Fingerprint

Rod Cell Outer Segment
Adenosine Triphosphate
Proteins
Oxidative Phosphorylation
Retinal Photoreceptor Cell Outer Segment
Light Signal Transduction
Retinal Rod Photoreceptor Cells
Ca(2+) Mg(2+)-ATPase
Adenosine Triphosphatases
Vertebrates
Hydrolysis
Cell Membrane

Keywords

  • ATPase
  • FF-ATP synthase
  • IF1
  • Rod outer segments

ASJC Scopus subject areas

  • Cellular and Molecular Neuroscience
  • Cell Biology
  • Medicine(all)

Cite this

Calzia, D., Candiani, S., Garbarino, G., Caicci, F., Ravera, S., Bruschi, M., ... Panfoli, I. (2013). Are rod outer segment ATP-ase and ATP-synthase activity expression of the same protein? Cellular and Molecular Neurobiology, 33(5), 637-649. https://doi.org/10.1007/s10571-013-9926-7

Are rod outer segment ATP-ase and ATP-synthase activity expression of the same protein? / Calzia, Daniela; Candiani, Simona; Garbarino, Greta; Caicci, Federico; Ravera, Silvia; Bruschi, Maurizio; Manni, Lucia; Morelli, Alessandro; Traverso, Carlo Enrico; Candiano, Giovanni; Tacchetti, Carlo; Panfoli, Isabella.

In: Cellular and Molecular Neurobiology, Vol. 33, No. 5, 07.2013, p. 637-649.

Research output: Contribution to journal › Article

Calzia, D, Candiani, S, Garbarino, G, Caicci, F, Ravera, S, Bruschi, M, Manni, L, Morelli, A, Traverso, CE, Candiano, G, Tacchetti, C & Panfoli, I 2013, 'Are rod outer segment ATP-ase and ATP-synthase activity expression of the same protein?', Cellular and Molecular Neurobiology, vol. 33, no. 5, pp. 637-649. https://doi.org/10.1007/s10571-013-9926-7
Calzia D, Candiani S, Garbarino G, Caicci F, Ravera S, Bruschi M et al. Are rod outer segment ATP-ase and ATP-synthase activity expression of the same protein? Cellular and Molecular Neurobiology. 2013 Jul;33(5):637-649. https://doi.org/10.1007/s10571-013-9926-7
Calzia, Daniela ; Candiani, Simona ; Garbarino, Greta ; Caicci, Federico ; Ravera, Silvia ; Bruschi, Maurizio ; Manni, Lucia ; Morelli, Alessandro ; Traverso, Carlo Enrico ; Candiano, Giovanni ; Tacchetti, Carlo ; Panfoli, Isabella. / Are rod outer segment ATP-ase and ATP-synthase activity expression of the same protein?. In: Cellular and Molecular Neurobiology. 2013 ; Vol. 33, No. 5. pp. 637-649.
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abstract = "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 F1F o-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 F1F o 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.",
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