Energy interconversion by the sarcoplasmic reticulum Ca2+-ATPase: ATP hydrolysis, Ca2+ transport, ATP synthesis and heat production

Meis, Leopoldo de

doi:10.1590/s0001-37652000000300010

Cited by 13 publications

(7 citation statements)

References 43 publications

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“…For the analysis below, we also consider the remaining possible event orderings comprising other putative alternating-access mechanisms for a 3:1 H + :ATP stoichiometry (Fig. 2B), building on the demonstrated capacity for ATP-hydrolyzing transporters to be driven in reverse to synthesize ATP (34,35). In SI Appendix, analysis of 4:1 stoichiometry is given, yielding similar results.…”

Section: Significancementioning

confidence: 99%

“…Beyond the rotarybased model, we considered a series of alternating-access analogs (Fig. 2), building on the demonstrated capacity for ATP-hydrolyzing transporters to be driven in reverse to synthesize ATP (34,35). The discrete-state models do not include structural details, but implicitly incorporate conformational transitions; the models embody the basic mechanisms that have been appreciated over decades of biochemical and structural studies (25)(26)(27)(28)(29)(30)36), as well as thermodynamic constraints (36).…”

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confidence: 99%

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Biophysical comparison of ATP synthesis mechanisms shows a kinetic advantage for the rotary process

Anandakrishnan

Zhang

Donovan-Maiye

et al. 2016

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

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The ATP synthase (F-ATPase) is a highly complex rotary machine that synthesizes ATP, powered by a proton electrochemical gradient. Why did evolution select such an elaborate mechanism over arguably simpler alternating-access processes that can be reversed to perform ATP synthesis? We studied a systematic enumeration of alternative mechanisms, using numerical and theoretical means. When the alternative models are optimized subject to fundamental thermodynamic constraints, they fail to match the kinetic ability of the rotary mechanism over a wide range of conditions, particularly under low-energy conditions. We used a physically interpretable, closed-form solution for the steady-state rate for an arbitrary chemical cycle, which clarifies kinetic effects of complex free-energy landscapes. Our analysis also yields insights into the debated "kinetic equivalence" of ATP synthesis driven by transmembrane pH and potential difference. Overall, our study suggests that the complexity of the F-ATPase may have resulted from positive selection for its kinetic advantage.ATP synthase | kinetic mechanism | free-energy landscape | nonequilibrium steady state | evolution T he F-ATPase performs molecular-level free-energy (FE) transduction to phosphorylate ADP and yield ATP, the primary energy carrier that drives a vast range of cellular processes. It spurred Mitchell's chemiosmotic hypothesis (1) and Boyer's now-validated proposal for the binding-change mechanism (2) in which a proton electrochemical gradient is transduced to rotationbased mechanical energy and then back to chemical FE as ADP is phosphorylated. The F-ATPase's two-domain uniaxial rotary structure is conserved across all three domains of life (3-6), and details of its function have been the subject of a multitude of studies (e.g., refs. 7-30).Here, we address a relatively narrow question with potentially significant evolutionary implications: Why is ATP synthesized by a rotary mechanism instead of a potentially much simpler alternating-access mechanism (Fig. 1)? Using thermodynamic and kinetic constraints, we address the question of whether evolution tends to arrive at optimal molecular processes (31), building on established concepts of optimality-derived evolutionary convergence (32, 33). Presumably, performance advantages in the central task of ATP synthesis would be under significant evolutionary pressure. Previous modeling studies of the F-ATPase have addressed structural and mechanistic questions about the rotary mechanism (e.g., refs. 11-20), but not the metaissue of the mechanism itself compared with alternatives.To assess whether the rotary mechanism possesses any intrinsic performance advantage, we constructed a series of kinetic models abstracted from known mechanisms (Fig. 1). Beyond the rotarybased model, we considered a series of alternating-access analogs (Fig. 2), building on the demonstrated capacity for ATP-hydrolyzing transporters to be driven in reverse to synthesize ATP (34, 35). The discrete-state models do not include structural details, bu...

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Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

Biophysical comparison of ATP synthesis mechanisms shows a kinetic advantage for the rotary process

Anandakrishnan

Zhang

Donovan-Maiye

et al. 2016

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

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“…In skeletal muscle, isoform SERCA 1 is expressed in fast-twitch muscle fibers. In contrast, slow-twitch muscle fibers express SERCA 1 and SERCA 2a [ 23 ], and only SERCA 1 can modulate the amount of heat produced during the ATP hydrolysis in the range of 7–32 Kcal/mol, depending on the established transmembrane Ca 2+ gradient across the SR membrane [ 24 ]. An important regulator of SERCA’s activity is sarcolipin (SLN) [ 25 ].…”

Section: Metabolic and Physiological Mechanisms Of Shivering And Nons...mentioning

confidence: 99%

Skeletal Muscle Uncoupling Proteins in Mice Models of Obesity

Bombek

Čater

2022

Metabolites

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Obesity and accompanying type 2 diabetes are among major and increasing worldwide problems that occur fundamentally due to excessive energy intake during its expenditure. Endotherms continuously consume a certain amount of energy to maintain core body temperature via thermogenic processes, mainly in brown adipose tissue and skeletal muscle. Skeletal muscle glucose utilization and heat production are significant and directly linked to body glucose homeostasis at rest, and especially during physical activity. However, this glucose balance is impaired in diabetic and obese states in humans and mice, and manifests as glucose resistance and altered muscle cell metabolism. Uncoupling proteins have a significant role in converting electrochemical energy into thermal energy without ATP generation. Different homologs of uncoupling proteins were identified, and their roles were linked to antioxidative activity and boosting glucose and lipid metabolism. From this perspective, uncoupling proteins were studied in correlation to the pathogenesis of diabetes and obesity and their possible treatments. Mice were extensively used as model organisms to study the physiology and pathophysiology of energy homeostasis. However, we should be aware of interstrain differences in mice models of obesity regarding thermogenesis and insulin resistance in skeletal muscles. Therefore, in this review, we gathered up-to-date knowledge on skeletal muscle uncoupling proteins and their effect on insulin sensitivity in mouse models of obesity and diabetes.

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“…During this process, part of Ca 2+ is coupled with the synthesis of ATP, and part of Ca 2+ leaks and deviates from ATP. It is synthesized and leads to heat loss (De Meis et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

“…During this process, part of Ca 2+ is coupled with the synthesis of ATP, and part of Ca 2+ leaks and deviates from ATP. It is synthesized and leads to heat loss (De Meis et al., 1997). During mild and severe cold adaptation, nonshivering thermogenesis of muscle and BAT are simultaneously activated.…”

Section: Introductionmentioning

confidence: 99%

Characterization of pig skeletal muscle transcriptomes in response to low temperature

Dong-jie

Wang

et al. 2022

Veterinary Medicine & Sci

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Objectives The response of mammals to cold environment is a complex physiological activity, and its underlying mechanism must be analyzed from multiple perspectives. Skeletal muscle is an important thermogenic tissue that maintains body temperature in mammals. We dissected the molecular mechanism of pig skeletal muscle response to a cold environment by performing comparative transcriptome analysis in the Enshi black pig. Methods Three pigs were subjected to acute cold stress (3 days), three pigs were subjected to cold acclimation (58 days), and three pigs were used as controls. RNA‐seq was used to screen the differentially expressed genes (DEGs) of skeletal muscle. Results Using RNA‐seq methods, we identified 1241 DEGs within the acute cold stress group and 1886 DEGs within the cold acclimation group. Prolonged cold exposure induced more gene expression changes. A total of 540 key cold‐responsive DEGs were found, and their trends were consistent within the acute cold stress group and cold acclimation group. Gene expression pattern analysis showed that there were significant differences between the low‐temperature treatment groups and the control group, and there were also differences between individuals after long‐term low‐temperature treatment. Analysis of DEGs revealed that 134 pathways were significantly enriched in the cold adaptation group, 98 pathways were significantly enriched in the acute cold stress group, and 71 pathways were shared between the two groups. The 71 shared pathways were mainly related to lipid, amino acid, and carbohydrate metabolism; signal transduction; endocrine, immune, and nervous system; cardiovascular disease; infectious diseases caused by bacteria or viruses; and neurodegenerative disease. Conclusions In conclusion, this study provides insights into the molecular mechanism of porcine skeletal muscle response under low‐temperature environment. The data may assist further research on the mechanism of pig response to cold exposure.

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Energy interconversion by the sarcoplasmic reticulum Ca2+-ATPase: ATP hydrolysis, Ca2+ transport, ATP synthesis and heat production

Cited by 13 publications

References 43 publications

Biophysical comparison of ATP synthesis mechanisms shows a kinetic advantage for the rotary process

Biophysical comparison of ATP synthesis mechanisms shows a kinetic advantage for the rotary process

Skeletal Muscle Uncoupling Proteins in Mice Models of Obesity

Characterization of pig skeletal muscle transcriptomes in response to low temperature

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