An Equivocal Final Link – Quantitative Determination of the Thermodynamic Efficiency of ATP Hydrolysis – Sullies the Chain of Electric, Ionic, Mechanical and Metabolic Steps Underlying Cardiac Contraction

Barclay, Christopher John; Loiselle, Denis S.

doi:10.3389/fphys.2020.00183

Cited by 8 publications

(10 citation statements)

References 68 publications

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“…b,c variation in time-dependence of diameter d,e variation in timedependent mid-lymphangion pressure f,g variation in time-dependence of outflow h,i variation in time-dependence of outlet valve resistance, showing the opening and closing with calcium oscillations ◂ number of mitochondria (Ohhashi 1987), so even small losses per mitochondria can sum up to cause losses comparable to cross-bridge cycling. By comparison, metabolic efficiency has been estimated as 80% for cardiac muscle; 4 × the cross-bridge cycling efficiency (Barclay & Loiselle 2020;Barclay et al 2003). Calculating the efficiency of lymphatic pumping is useful for a complete understanding of the regulatory mechanisms, particularly the effects of shear.…”

Section: Discussionmentioning

confidence: 99%

“…The thermodynamic efficiency of human skeletal muscle was reported as 40% at (He et al 2000 ). Cardiac muscle from various species exhibited thermodynamic efficiencies of around 20% (Barclay & Loiselle 2020 ; Barclay et al 2003 ). The efficiency of vascular smooth muscle (rabbit rectococcygeus) has been reported as 18% (Walker et al 1994 ).…”

Section: Discussionmentioning

confidence: 99%

“…LMCs contain a large number of mitochondria (Ohhashi 1987 ), so even small losses per mitochondria can sum up to cause losses comparable to cross-bridge cycling. By comparison, metabolic efficiency has been estimated as 80% for cardiac muscle; 4 × the cross-bridge cycling efficiency (Barclay & Loiselle 2020 ; Barclay et al 2003 ). Calculating the efficiency of lymphatic pumping is useful for a complete understanding of the regulatory mechanisms, particularly the effects of shear.…”

Section: Discussionmentioning

confidence: 99%

“…At the sliding filament level, energy is lost because not all heads complete the entire powerstroke. Incomplete powerstrokes liberate the same amount of energy but cannot convert all of the energy liberated to work (Barclay & Loiselle 2020 ; Eisenberg et al 1980 ). This is combined with the fact that ATP hydrolysis is irreversible so the excess liberated energy is not re-captured and is lost to entropy as heat (Chapman & Loiselle 2016 ; Loiselle et al 2010 ).…”

Section: Methodsmentioning

confidence: 99%

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A multiscale sliding filament model of lymphatic muscle pumping

Morris

Zawieja

Moore

2021

Biomech Model Mechanobiol

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The lymphatics maintain fluid balance by returning interstitial fluid to veins via contraction/compression of vessel segments with check valves. Disruption of lymphatic pumping can result in a condition called lymphedema with interstitial fluid accumulation. Lymphedema treatments are often ineffective, which is partially attributable to insufficient understanding of specialized lymphatic muscle lining the vessels. This muscle exhibits cardiac-like phasic contractions and smooth muscle-like tonic contractions to generate and regulate flow. To understand the relationship between this sub-cellular contractile machinery and organ-level pumping, we have developed a multiscale computational model of phasic and tonic contractions in lymphatic muscle and coupled it to a lymphangion pumping model. Our model uses the sliding filament model (Huxley in Prog Biophys Biophys Chem 7:255–318, 1957) and its adaptation for smooth muscle (Mijailovich in Biophys J 79(5):2667–2681, 2000). Multiple structural arrangements of contractile components and viscoelastic elements were trialed but only one provided physiologic results. We then coupled this model with our previous lumped parameter model of the lymphangion to relate results to experiments. We show that the model produces similar pressure, diameter, and flow tracings to experiments on rat mesenteric lymphatics. This model provides the first estimates of lymphatic muscle contraction energetics and the ability to assess the potential effects of sub-cellular level phenomena such as calcium oscillations on lymphangion outflow. The maximum efficiency value predicted (40%) is at the upper end of estimates for other muscle types. Spontaneous calcium oscillations during diastole were found to increase outflow up to approximately 50% in the range of frequencies and amplitudes tested.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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A multiscale sliding filament model of lymphatic muscle pumping

Morris

Zawieja

Moore

2021

Biomech Model Mechanobiol

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“…To achieve their diverse functions, proteins rely on efficient utilization of energy quanta released by the hydrolysis of adenosine triphosphate (ATP) to adenosine diphosphate (ADP) and inorganic phosphate (Pi). The Gibbs free energy of ATP hydrolysis (measured in eV) depends on the chemical concentration of substrates and products [4][5][6] ∆G ATP = ∆G 0 ATP +…”

Section: Introductionmentioning

confidence: 99%

Thermal stability of solitons in protein $α$-helices

Georgiev,

Glazebrook

2022

Preprint

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Protein α-helices provide an ordered biological environment that is conducive to soliton-assisted energy transport. The nonlinear interaction between amide I excitons and phonon deformations induced in the hydrogen-bonded lattice of peptide groups leads to self-trapping of the amide I energy, thereby creating a localized quasiparticle (soliton) that persists at zero temperature. The presence of thermal noise, however, could destabilize the protein soliton and dissipate its energy within a finite lifetime. In this work, we have computationally solved the system of stochastic differential equations that govern the quantum dynamics of protein solitons at physiological temperature, T = 310 K, for either a single isolated α-helix spine of hydrogen bonded peptide groups or the full protein α-helix comprised of three parallel α-helix spines. The simulated stochastic dynamics revealed that although the thermal noise is detrimental for the single isolated α-helix spine, the cooperative action of three amide I exciton quanta in the full protein α-helix ensures soliton lifetime of over 30 ps, during which the amide I energy could be transported along the entire extent of an 18-nm-long α-helix. Thus, macromolecular protein complexes, which are built up of protein α-helices could harness soliton-assisted energy transport at physiological temperature. Because the hydrolysis of a single adenosine triphosphate molecule is able to initiate three amide I exciton quanta, it is feasible that multiquantal protein solitons subserve a variety of specialized physiological functions in living systems.

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Thermal stability of solitons in protein α-helices

Georgiev

Glazebrook

2022

Chaos, Solitons & Fractals

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An Equivocal Final Link – Quantitative Determination of the Thermodynamic Efficiency of ATP Hydrolysis – Sullies the Chain of Electric, Ionic, Mechanical and Metabolic Steps Underlying Cardiac Contraction

Cited by 8 publications

References 68 publications

A multiscale sliding filament model of lymphatic muscle pumping

A multiscale sliding filament model of lymphatic muscle pumping

Thermal stability of solitons in protein $α$-helices

Thermal stability of solitons in protein α-helices

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