31P-NMR saturation transfer studies of aerobic Escherichia coli cells

Mitsumori, Fumiyuki; Rees, D. J. G.; Brindle, Kevin M.; Radda, George K.; Campbell, Iain D.

doi:10.1016/0167-4889(88)90074-2

Cited by 22 publications

(20 citation statements)

References 20 publications

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“…9, 10, and 13. This surprising finding was further examined in the present study under the conditions in which we have performed rigorous CMRO 2 measurements, using high-field 17 O MRS, ultimately, to test whether F f,ATPase determined by 31 P MT changed as brain energy demand was altered.…”

Section: Discussionmentioning

confidence: 99%

“…Most processes, however, are not fast enough relative to the intrinsic spin lattice time (T 1 ) of Pi to have a NMR detectable contribution. Surprisingly, the reactions catalyzed by glycolytic enzymes have been shown to be a major contributor to the Pi 3 ATP rate measured by the in vivo 31 P MT approach in Escherichia coli (17), yeast (18), liver (19), and myocardium (20). In the glucose perfused rat heart, the exchange mediated by the two coupled glycolytic enzymes of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and phosphoglycerate kinase (PGK) dominates the unidirectional Pi 3 ATP rate ¶ measured by the in vivo 31 P MT approach (20).…”

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confidence: 99%

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Tightly coupled brain activity and cerebral ATP metabolic rate

Zhu

Zhang

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

186

220

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A majority of ATP in the brain is formed in the mitochondria through oxidative phosphorylation of ADP with the F1F0-ATP (ATPase) enzyme. This ATP production rate plays central roles in brain bioenergetics, function and neurodegeneration. In vivo 31 P magnetic resonance spectroscopy combined with magnetization transfer (MT) is the sole approach able to noninvasively determine this ATP metabolic rate via measuring the forward ATPase reaction flux (F f,ATPase). However, previous studies indicate lack of quantitative agreement between F f,ATPase and oxidative metabolic rate in heart and liver. In contrast, recent work has shown that F f,ATPase might reflect oxidative phosphorylation rate in resting human brains. We have conducted an animal study, using rats under varied brain activity levels from light anesthesia to isoelectric state, to examine whether the in vivo 31 P MT approach is suitable for measuring the oxidative phosphorylation rate and its change associated with varied brain activity. Our results conclude that the measured F f,ATPase reflects the oxidative phosphorylation rate in resting rat brains, that this flux is tightly correlated to the change of energy demand under varied brain activity levels, and that a significant amount of ATP energy is required for ''housekeeping'' under the isoelectric state. These findings reveal distinguishable characteristics of ATP metabolism between the brain and heart, and they highlight the importance of in vivo 31 P MT approach to potentially provide a unique and powerful neuroimaging modality for noninvasively studying the cerebral ATP metabolic network and its central role in bioenergetics associated with brain function, activation, and diseases.A denosine triphosphate (ATP), a high-energy phosphate (HEP) compound, is the universal energy currency in living cells for supporting the energy needs of various cellular activities and functions. In the brain, a majority of ATP is formed in the mitochondria through oxidative phosphorylation of adenosine diphosphate (ADP) catalyzed by the enzyme of ATP synthase (ATPase) (1). A large portion of ATP energy is used in cytosol to pump sodium and potassium across the cellular membrane for maintaining transmembrane ion gradients and to support neurotransmitters cycling and, thus, sustaining electrophysiological activity and cell signaling in the brain. The ATP metabolism regulating both ATP production and utilization plays a fundamental role in cerebral bioenergetics, brain function, and neurodegenerative diseases (2-6).The brain ATP metabolism is mainly controlled by ATPase and creatine kinase (CK) reactions that are coupled together and constitute a complex chemical exchange system involving ATP, phosphocreatine (PCr), and intracellular inorganic phosphate (Pi) (i.e., a PCr^ATP^Pi chemical exchange system) (7-10). One vital function of this ATP metabolic network is to maintain a stable cellular ATP concentration by adjusting the reaction rates to ensure a continuous energy supply for sustaining electrophysiological activity and ...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Tightly coupled brain activity and cerebral ATP metabolic rate

Zhu

Zhang

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

186

220

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“…In perfused hearts, it was demonstrated that when glucose is present as a carbon substrate, GAPDH and PGK enzyme couple mediates P i -ATP exchange with fast unidirectional rates that significantly exceeded the net rate § of ATP synthesis by the glycolysis pathway and hence these enzymes (9). It was also demonstrated that when glucose is present GAPDH͞PGK-mediated exchange dominates the P i 3 ATP rate measured by saturation transfer in the myocardium (9) and in E. coli, yeast, and liver (12,35,36). Under these circumstances, unequivocal detection of the P i 3 ATP conversion caused by oxidative phosphorylation alone was feasible in the myocardium only after complete suppression of the GAPDH͞PGK reactions in situ (9).…”

Section: Glycolytic Contributions To Pi 3 Atp Rate Measured By Saturamentioning

confidence: 96%

“…Most such reactions are not sufficiently fast relative to the intrinsic T 1 of P i to have a detectable contribution. However, the ATP synthesis reaction catalyzed by the coupled activities of glycolytic enzymes GAPDH and phosphoglycerate kinase (PGK) has been shown to be a major contributor to the P i 3 ATP rate measured by saturation transfer in E. coli (35), yeast (36), liver (12), and the myocardium (9). In perfused hearts, it was demonstrated that when glucose is present as a carbon substrate, GAPDH and PGK enzyme couple mediates P i -ATP exchange with fast unidirectional rates that significantly exceeded the net rate § of ATP synthesis by the glycolysis pathway and hence these enzymes (9).…”

Section: Glycolytic Contributions To Pi 3 Atp Rate Measured By Saturamentioning

confidence: 99%

Measurement of unidirectional P_ito ATP flux in human visual cortex at 7 T by usingin vivo³¹P magnetic resonance spectroscopy

Lei

Uğurbil

Chen

2003

Proc. Natl. Acad. Sci. U.S.A.

154

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Taking advantage of the high NMR detection sensitivity and the large chemical shift dispersion offered by ultra-high field strength of 7 T, the effect of magnetization transfer on inorganic phosphate (Pi) resonance during saturation of ␥-ATP resonance, mediated by the ATP synthesis reaction, was observed noninvasively in the human primary visual cortex by using in vivo 31 P magnetic resonance spectroscopy. The unidirectional flux from Pi to ATP was measured by using progressive saturation transfer experiments. The cerebral ATP synthesis rate in the human primary visual cortex measured by 31 P magnetic resonance spectroscopy in this study was 12.1 ؎ 2.8 mol ATP͞g per min, which agreed well with the value that was calculated indirectly from the cerebral metabolic rate of glucose consumption reported previously. E nergy requirements in tissues are met predominantly through hydrolysis of the high-energy molecule ATP. In the brain, this molecule is synthesized almost exclusively by mitochondrial oxidative phosphorylation, with only a small contribution coming from nonoxidative glycolysis (1). Despite the critical role of ATP in cellular functions, the kinetics of ATP synthesis and hydrolysis is often difficult to measure directly in intact cells and even more so in intact animals and humans. Cerebral ATP synthesis rate has been calculated indirectly from experimentally measured cerebral metabolic rates of glucose (CMR glu ) and oxygen (CMRO 2 ) (1, 2), and it has been estimated to be Ϸ14 mol ATP͞g per min (2) in the resting human brain.The magnetization transfer (MT) technique based on magnetic resonance spectroscopy (MRS) has the capability of measuring the reaction kinetics of enzymes noninvasively in situ when the reaction rates involved are relatively fast (e.g., for review see refs. 3 and 4). Using this technique to study the kinetics of ATP synthesis in biological tissues with 31 P MRS was first introduced in the late 1970s in suspensions of Escherichia coli cells (5). Since then, it has been applied to yeast (6), intact perfused hearts (4, 7-11), liver (12), kidney (13), canine myocardium in vivo (14), skeletal muscle (15), and rat brain (16). It was demonstrated that, under appropriate conditions, the MT technique is capable of measuring the net rate of oxidative ATP synthesis catalyzed by mitochondrial ATPase (7-10); because, by definition, this rate is proportional to the oxygen consumption rate by the P͞O ratio, those experiments yielded for the first time the P͞O ratio in an intact organ under functional conditions.Because of the relatively low concentration of P i in normal intact tissues and the low intrinsic detection sensitivity of in vivo 31 P MRS, virtually all previous experiments using the MT methodology to study P i -ATP exchange were performed in excised perfused organ models or in small animals, where the radio frequency coil geometry relative to the organ of interest can be optimized to yield significant gains in signal-to-noise ratio compared with what is possible in humans. In addition, all ...

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“…All the units are mmol/gDCW h. The ATP needed for the growth of the strain was 94 mmol/gDCW (Licona-Cassani et al, 2012). Total ATP generation rate account for the generation of ATP, NADH and FADH2, assuming that 1 mol NADH forms 3 mol ATP and 1 mol FADH2 forms 2 mol ATP (Mitsumori et al, 1988). The maintenance energy was the result of total ATP minus the ATP needed for biomass formation.…”

Section: Impacts Of Proline On Central Metabolismmentioning

confidence: 99%

Impacts of proline on the central metabolism of an industrial erythromycin-producing strain Saccharopolyspora erythraea via 13 C labeling experiments

Hong

Huang

Chu

et al. 2016

Journal of Biotechnology

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31P-NMR saturation transfer studies of aerobic Escherichia coli cells

Cited by 22 publications

References 20 publications

Tightly coupled brain activity and cerebral ATP metabolic rate

Tightly coupled brain activity and cerebral ATP metabolic rate

Measurement of unidirectional P_ito ATP flux in human visual cortex at 7 T by usingin vivo³¹P magnetic resonance spectroscopy

Impacts of proline on the central metabolism of an industrial erythromycin-producing strain Saccharopolyspora erythraea via 13 C labeling experiments

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31P-NMR saturation transfer studies of aerobic Escherichia coli cells

Cited by 22 publications

References 20 publications

Tightly coupled brain activity and cerebral ATP metabolic rate

Tightly coupled brain activity and cerebral ATP metabolic rate

Measurement of unidirectional Pito ATP flux in human visual cortex at 7 T by usingin vivo31P magnetic resonance spectroscopy

Impacts of proline on the central metabolism of an industrial erythromycin-producing strain Saccharopolyspora erythraea via 13 C labeling experiments

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Measurement of unidirectional P_ito ATP flux in human visual cortex at 7 T by usingin vivo³¹P magnetic resonance spectroscopy