Commonalities and differences in the Oxidative Phosphorylation of Mitochondria and Neuronal Membranes

2020 ◽  
Author(s):  
Silvia Ravera ◽  
Martina Bartolucci ◽  
Daniela Calzia ◽  
Alessandro M. Morelli ◽  
Isabella Panfoli
Keyword(s):  
Oxygen Consumption ◽  
Oxidative Phosphorylation ◽  
Myelin Sheath ◽  
Atp Synthesis ◽  
Functional Expression ◽  
Positive Control ◽  
Aerobic Metabolism ◽  
Rod Outer Segments ◽  
Outer Segments ◽  
Neuronal Membranes

ABSTRACTMitochondria are considered the exclusive site of aerobic metabolism. However, in recent years, the functional expression of the oxidative phosphorylation (OxPhos) machinery has been reported in several other membranous structures, including the plasma membrane, endoplasmic reticulum, nucleus, myelin sheath and disks of rod outer segments. Thus, to underline commonalities and differences between extra-mitochondrial and mitochondrial aerobic metabolism, we characterized the aerobic ATP synthesis in isolated myelin sheath (IM) and rod outer segment (OS) disks, using mitochondria-enriched fractions, as a positive control. Oxygen consumption and ATP synthesis were evaluated in the presence of conventional (pyruvate + malate or succinate) and unconventional (NADH) substrates. ATP synthesis was also assayed in the presence of 10-100 µM ATP in the assay medium. Data show that IM and OS disks consumed oxygen and synthesized ATP both in the presence of conventional and unconventional respiratory substrates, while the mitochondria-enriched fraction did not utilize NADH. Only in mitochondria, ATP synthesis was progressively lost in the presence of increasing ATP concentrations. Conversely, only myelin sheath and rod OS disks produced ATP at a later time or after the removal of respiratory substrates, reflecting their ability to accumulate energy and this opens up exciting perspectives in the study of sleep. Thus, these data suggest that the extramitochondrial OxPhos in IM and rod OS displays a different behavior concerning the classic mitochondrial aerobic metabolism, representing a possible basic molecular process involved in the physiology of the nervous system.Significance StatementMitochondria are considered the cell powerhouse, being the site of the oxidative phosphorylation (OxPhos), which produces the major part of cellular chemical energy by oxygen consumption. However, proteomics, microscopy, and biochemical analyses have described the ectopic functional expression of the OxPhos machinery also in other membranous structures, such as isolated myelin (IM) and rod outer segments (OS). The results reported in this work shows that, although the proteins involved in IM and rod OS OxPhos appear the same expressed in mitochondria, the comparison of mitochondrial and extramitochondrial OxPhos display some differences, opening a new scenario about the energy metabolism modulation.Graphical Abstract

scholarly journals Evidence of Oxidative Phosphorylation in Zebrafish Photoreceptor Outer Segments at Different Larval Stages

2018 ◽  
Vol 66 (7) ◽  
pp. 497-509 ◽  
Author(s):  
Daniela Calzia ◽  
Greta Garbarino ◽  
Federico Caicci ◽  
Mario Pestarino ◽  
Lucia Manni ◽  
...  
Keyword(s):  
Oxidative Phosphorylation ◽  
Atp Synthase ◽  
Aerobic Metabolism ◽  
Respiratory Chain Complexes ◽  
Atp Production ◽  
Photoreceptor Outer Segments ◽  
Larval Stages ◽  
Outer Segments ◽  
Chain Complexes ◽  
Transmission Electron

Summary Previous studies on purified bovine rod outer segments (OS) disks pointed to Oxidative Phosphorylation (OXPHOS) as being the most likely mechanism involved in ATP production, as yet not fully understood, to support the first phototransduction steps. Bovine and murine rod OS disks, devoid of mitochondria, would house respiratory chain complexes I to IV and ATP synthase, similar to mitochondria. Zebrafish ( Danio rerio) is a well-suited animal model to study vertebrate embryogenesis as well as the retina, morphologically and functionally similar to its human counterpart. The present article reports fluorescence and Transmission Electron Microscopy colocalization analyses of respiratory complexes I and IV and ATP synthase with zpr3, the rod OS marker, in adult and larval zebrafish retinas. MitoTracker Deep Red 633 staining and assays of complexes I and III–IV activity suggest that those proteins are active in OS. Results show that an extramitochondrial aerobic metabolism is active in the zebrafish OS at 4 and 10 days of larval development, as well as in adults, suggesting that it is probably maintained during embryogenesis. Data support the hypothesis of an extramitochondrial aerobic metabolism in the OS of zebrafish.

scholarly journals Effect of polyphenolic phytochemicals on ectopic oxidative phosphorylation in rod outer segments of bovine retina

2015 ◽  
Vol 172 (15) ◽  
pp. 3890-3903 ◽  
Author(s):  
Daniela Calzia ◽  
Michele Oneto ◽  
Federico Caicci ◽  
Paolo Bianchini ◽  
Silvia Ravera ◽  
...  
Keyword(s):  
Oxidative Phosphorylation ◽  
Rod Outer Segments ◽  
Bovine Retina ◽  
Outer Segments

Extra-mitochondrial aerobic metabolism in retinal rod outer segments: New perspectives in retinopathies

2012 ◽  
Vol 78 (4) ◽  
pp. 423-427 ◽  
Author(s):  
I. Panfoli ◽  
D. Calzia ◽  
S. Ravera ◽  
A.M. Morelli ◽  
C.E. Traverso
Keyword(s):  
Aerobic Metabolism ◽  
Rod Outer Segments ◽  
Outer Segments ◽  
Retinal Rod ◽  
Retinal Rod Outer Segments

Functional expression of electron transport chain complexes in mouse rod outer segments

Biochimie ◽  
2014 ◽  
Vol 102 ◽  
pp. 78-82 ◽  
Author(s):  
Daniela Calzia ◽  
Greta Garbarino ◽  
Federico Caicci ◽  
Lucia Manni ◽  
Simona Candiani ◽  
...  
Keyword(s):  
Electron Transport ◽  
Electron Transport Chain ◽  
Functional Expression ◽  
Rod Outer Segments ◽  
Outer Segments ◽  
Chain Complexes ◽  
Transport Chain

Mitochondrial cytochrome c oxidase and control of energy metabolism: measurements in suspensions of isolated mitochondria

2014 ◽  
Vol 117 (12) ◽  
pp. 1424-1430 ◽  
Author(s):  
David F. Wilson ◽  
David K. Harrison ◽  
Andrei Vinogradov
Keyword(s):  
Oxygen Consumption ◽  
Energy Metabolism ◽  
Cytochrome C ◽  
Oxidative Phosphorylation ◽  
Respiratory Rate ◽  
Cytochrome C Oxidase ◽  
Energy State ◽  
Atp Synthesis ◽  
Oxygen Depletion ◽  
High Energy

Cytochrome c oxidase is the enzyme responsible for oxygen consumption by mitochondrial oxidative phosphorylation and coupling site 3 of oxidative phosphorylation. In this role it determines the cellular rate of ATP synthesis by oxidative phosphorylation and is the key to understanding how energy metabolism is regulated. Four electrons are required for the reduction of oxygen to water, and these are provided by the one-electron donor, cytochrome c. The rate of oxygen consumption (ATP synthesis) is dependent on the fraction of cytochrome c reduced (fred), oxygen pressure (pO2), energy state ([ATP]/[ADP][Pi]), and pH. In coupled mitochondria (high energy state) and pO2 >60 torr, the rate increases in an exponential-like fashion with increasing fred. When the dependence on fred is fitted to the equation rate = a(fred)b, a decreased from 100 to near 20, and b increased from 1.3 to 4 as the pH of the medium increased from 6.5 to 8.3. During oxygen depletion from the medium fred progressively increases and the rate of respiration decreases. The respiratory rate falls to ½ (P50) by about 1.5 torr, at which point fred is substantially increased. The metabolically relevant dependence on pO2 is obtained by correcting for the increase in fred, in which case the P50 is 12 torr. Adding an uncoupler of oxidative phosphorylation eliminates the dependence of the cytochrome c oxidase activity on pH and energy state. The respiratory rate becomes proportional to fred and the P50 decreases to less than 1 torr.

ATP synthesis in the disk membranes of rod outer segments of bovine retina

2002 ◽  
Vol 66 (2) ◽  
pp. 148-152 ◽  
Author(s):  
I.M Pepe ◽  
L Notari ◽  
C Cugnoli ◽  
I Panfoli ◽  
A Morelli
Keyword(s):  
Atp Synthesis ◽  
Rod Outer Segments ◽  
Bovine Retina ◽  
Outer Segments

Impairment of extramitochondrial oxidative phosphorylation in mouse rod outer segments by blue light irradiation

Biochimie ◽  
2016 ◽  
Vol 125 ◽  
pp. 171-178 ◽  
Author(s):  
Daniela Calzia ◽  
Isabella Panfoli ◽  
Nora Heinig ◽  
Ulrike Schumann ◽  
Marius Ader ◽  
...  
Keyword(s):  
Oxidative Phosphorylation ◽  
Blue Light ◽  
Light Irradiation ◽  
Rod Outer Segments ◽  
Outer Segments

scholarly journals Regulation of metabolism: the rest-to-work transition in skeletal muscle

2015 ◽  
Vol 309 (9) ◽  
pp. E793-E801 ◽  
Author(s):  
David F. Wilson
Keyword(s):  
Skeletal Muscle ◽  
Oxygen Consumption ◽  
Oxidative Phosphorylation ◽  
Atp Synthesis ◽  
Creatine Phosphate ◽  
Valuable Insight ◽  
Metabolic Homeostasis ◽  
Lag Period ◽  
Metabolic Behavior

Mitochondrial oxidative phosphorylation is programmed to set and maintain metabolic homeostasis, and understanding that program is essential for an integrated view of cellular and tissue metabolism. The behavior predicted by a mechanism-based model for oxidative phosphorylation is compared with that experimentally measured for skeletal muscle when work is initiated. For the model, initiation of work is simulated by imposing a rate of ATP utilization of either 0.6 (equivalent of 13.4 ml O2·100 g tissue−1·min−1 or 6 μmol O2·g tissue−1·min−1) or 0.3 mM ATP/s. Creatine phosphate ([CrP]) decrease, both experimentally measured and predicted by the model, can be fit to a single exponential. Increase in ATP synthesis begins immediately but can show a “lag period,” during which the rate accelerates. The length of the lag period is similar for both experiment and model; in the model, the lag depends on intramitochondrial [NAD+]/[NADH], mitochondrial content, and size of the creatine pool ([CrP] + [Cr]) as well as the resting [CrP]/[Cr]. For in vivo conditions, increase in oxygen consumption may be linearly correlated with a decrease in [CrP] and an increase in inorganic phosphate ([Pi]) and [Cr]. The decrease in [CrP], resting and working steady state [CrP], and the increase in oxygen consumption are dependent on the Po2 in the inspired gas (experimental) or tissue Po2 (model). The metabolic behavior predicted by the model is consistent with available experimental measurements in muscle upon initiation of work, with the model providing valuable insight into how metabolic homeostasis is set and maintained.

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