Sarcomere-length dependence of lattice volume and radial mass transfer of myosin cross-bridges in rat papillary muscle

Yagi, Naoto; Okuyama, Hiroshi; Toyota, Hiroko; Araki, Junichi; Shimizu, Juichiro; Iribe, Gentaro; Nakamura, Kazufumi; Mohri, Satoshi; Tsujioka, Katsuhiko; Suga, Hiroyuki; Kajiya, Fumihiko

doi:10.1007/s00424-004-1243-z

Cited by 28 publications

(38 citation statements)

References 32 publications

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“…Recent experiments by Martyn et al (21) may lend some credence to this concept. These investigators demonstrated that an increase in either sarcomere length or externally applied osmotic pressure induces an increase in both the I 1,1 /I 1,0 intensity ratio and passive fiber stiffness, thus implicating an increase in the number of thin filament-associated cross-bridges under those conditions consistent with the aforementioned results of Yagi et al (37). Martyn et al (21), however, concluded that the observed changes in I 1,1 /I 1,0 intensity ratio were caused by changes in interfilament spacing.…”

Section: "Lattice Spacing Hypothesis" Revisitedsupporting

confidence: 69%

“…Moreover, we observed here that a small amount of myofilament lattice compression by application of 1% dextran (equivalent to 0.38 kPa applied osmotic compression) induced a change in the I 1,1 /I 1,0 intensity ratio from ϳ0.3 to ϳ0.45 in relaxed, isolated skinned myocardium. Various measurements of this parameter have been made previously in intact, nonskinned myocardium by Matsubara and colleagues (I 1,1 /I 1,0 ϭ 0.375) (23) and (I 1,1 /I 1,0 ϭ 0.581) (24), as well as Yagi and colleagues (I 1,1 /I 1,0 ϭ 0.4) (38) and (I 1,1 /I 1,0 ϭ 0.444) (37). Of interest, these values are similar to those observed in this present study in skinned rat cardiac trabeculae in the high-myofilament calcium sensitivity state, that is, those muscles that were compressed by application of Ͼ1.0% dextran (0.38 kPa).…”

Section: Discussionmentioning

confidence: 78%

“…Yagi et al (37) presented results from intact, twitching papillary muscle that, although their data showed considerable scatter, demonstrated a small but significant increase in I 1,1 /I 1,0 under diastolic conditions with increasing sarcomere length from 1.7 to 2.3 m, supporting the notion that the underlying causes of changes in I 1,1 /I 1,0 may be related to the changes in calcium sensitivity with changing length. However, it should be noted that the function of the cardiac sarcomere within the cell is sufficiently complex to warrant caution in extrapolating data obtained in skinned myocardium to the intact beating heart.…”

Section: Limitations Of Studymentioning

confidence: 92%

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Impact of osmotic compression on sarcomere structure and myofilament calcium sensitivity of isolated rat myocardium

Farman¹,

Walker²,

Tombe³

et al. 2006

American Journal of Physiology-Heart and Circulatory Physiology

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Farman, Gerrie P., John S. Walker, Pieter P. de Tombe, and Thomas C. Irving. Impact of osmotic compression on sarcomere structure and myofilament calcium sensitivity of isolated rat myocardium. Am J Physiol Heart Circ Physiol 291: H1847-H1855, 2006. First published June 2, 2006 doi:10.1152/ajpheart.01237.2005.-Changes in interfilament lattice spacing have been proposed as the mechanism underlying myofilament length-dependent activation. Much of the evidence to support this theory has come from experiments in which high-molecular-weight compounds, such as dextran, were used to osmotically shrink the myofilament lattice. However, whether interfilament spacing directly affects myofilament calcium sensitivity (EC50) has not been established. In this study, skinned isolated rat myocardium was osmotically compressed over a wide range (Dextran T500; 0 -6%), and EC50 was correlated to both interfilament spacing and I1,1/I1,0 intensity ratio. The latter two parameters were determined by X-ray diffraction in a separate group of skinned muscles. Osmotic compression induced a marked reduction in myofilament lattice spacing, concomitant with increases in both EC50 and I1,1/I1,0 intensity ratio. However, interfilament spacing was not well correlated with EC50 (r 2 ϭ 0.78). A much better and deterministic relationship was observed between EC50 and the I1,1/I1,0 intensity ratio (r 2 ϭ 0.99), albeit with a marked discontinuity at low levels of dextran compression; that is, a small amount of external osmotic compression (0.38 kPa, corresponding to 1% Dextran T500) produced a stepwise increase in the I1,1/I1,0 ratio concomitant with a stepwise decrease in EC50. These parameters then remained stable over a wide range of further applied osmotic compression (up to 6% dextran). These findings provide support for a "switch-like" activation mechanism within the cardiac sarcomere that is highly sensitive to changes in external osmotic pressure. skinned muscle; trabeculae; X-ray diffraction; dextran; osmotic pressure; myofilament length-dependent activation; regulation MYOFILAMENT LENGTH-DEPENDENT activation (LDA) is a phenomenon found in all striated muscle, but to varying extents, being a prominent feature of cardiac muscle (2,4,7,15,16) and the indirect flight muscle of insects (33) but is less prominent in skeletal muscle (17,26,32). LDA is defined as an increase in the amount of active force developed at longer sarcomere length for a given concentration of activating calcium ions. LDA is the underlying cellular mechanism that underlies the Frank-Starling law of the heart (16). This increase in myofilament calcium sensitivity is commonly measured by the EC 50 parameter, that is, the calcium concentration at which the active developed force is half that observed at a saturating calcium concentration. An understanding of the molecular mechanism(s) underlying LDA has remained elusive. A popular hypothetical mechanism for LDA is that changes in interfilament lattice spacing, usually estimated as changes in fiber width, are directly linke...

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Section: "Lattice Spacing Hypothesis" Revisitedsupporting

confidence: 69%

Section: Discussionmentioning

confidence: 78%

Section: Limitations Of Studymentioning

confidence: 92%

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Impact of osmotic compression on sarcomere structure and myofilament calcium sensitivity of isolated rat myocardium

Farman¹,

Walker²,

Tombe³

et al. 2006

American Journal of Physiology-Heart and Circulatory Physiology

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“…The presence of the sarcolemma in intact striated fibers enables the cell to maintain an approximately constant volume as length changes, producing an inverse relationship between sarcomere length and interfilament lattice spacing (11,15,(41)(42)(43). In demembranated fibers, however, the permeabilized sarcolemma cannot maintain a constant volume, and lattice spacing is determined by a combination of sarcomere length, solution composition, and physical constraints, as well as attractive and repulsive forces between the filaments (11).…”

Section: Discussionmentioning

confidence: 99%

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Fenwick

Leighton

Tanner

2016

Biophysical Journal

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Actin-myosin cross-bridges use chemical energy from MgATP hydrolysis to generate force and shortening in striated muscle. Previous studies show that increases in sarcomere length can reduce thick-to-thin filament spacing in skinned muscle fibers, thereby increasing force production at longer sarcomere lengths. However, it is unclear how changes in sarcomere length and lattice spacing affect cross-bridge kinetics at fundamental steps of the cross-bridge cycle, such as the MgADP release rate. We hypothesize that decreased lattice spacing, achieved through increased sarcomere length or osmotic compression of the fiber via dextran T-500, could slow MgADP release rate and increase cross-bridge attachment duration. To test this, we measured cross-bridge cycling and MgADP release rates in skinned soleus fibers using stochastic length-perturbation analysis at 2.5 and 2.0 mm sarcomere lengths as pCa and [MgATP] varied. In the absence of dextran, the force-pCa relationship showed greater Ca 2þ sensitivity for 2.5 vs. 2.0 mm sarcomere length fibers (pCa 50 ¼ 5.68 5 0.01 vs. 5.60 5 0.01). When fibers were compressed with 4% dextran, the length-dependent increase in Ca 2þ sensitivity of force was attenuated, though the Ca 2þ sensitivity of the force-pCa relationship at both sarcomere lengths was greater with osmotic compression via 4% dextran compared to no osmotic compression. Without dextran, the cross-bridge detachment rate slowed by~15% as sarcomere length increased, due to a slower MgADP release rate (11.2 5 0.5 vs. 13.5 5 0.7 s À1 ). In the presence of dextran, cross-bridge detachment was~20% slower at 2.5 vs. 2.0 mm sarcomere length due to a slower MgADP release rate (10.1 5 0.6 vs. 12.9 5 0.5 s À1 ). However, osmotic compression of fibers at either 2.5 or 2.0 mm sarcomere length produced only slight (and statistically insignificant) slowing in the rate of MgADP release. These data suggest that skeletal muscle exhibits sarcomere-length-dependent changes in cross-bridge kinetics and MgADP release that are separate from, or complementary to, changes in lattice spacing.

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“…The number of such heads increased when the systolic tension was larger at higher heart rates, providing early evidence for the basis of the force-frequency relation. 66 Since then, isolated intact papillary muscle of rat and ferret, [67][68][69] rat trabeculae, 70 and mouse myocytes 71,72 also have been studied. The advantage of the isolated preparations is that the sarcomere length can be monitored with laser diffraction or video microscopy.…”

Section: Current and Past Saxs Studies From Myocytes To The In Situ Hmentioning

confidence: 99%

Synchrotron Radiation Imaging for Advancing Our Understanding of Cardiovascular Function

Shirai

Schwenke

Tsuchimochi

et al. 2013

Circulation Research

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Synchrotron radiation (SR) is increasingly being used for micro-level and nano-level functionalimaging in in vivo animal experiments. This review focuses on the methodology that enables repeated and regional assessment of vessel internal diameter and flow in the resistance vessels of different organ systems. In particular, SR absorption microangiography approaches offer unique opportunities for real-time in vivo vascular imaging in small animals, even during dynamic motion of the heart and lungs. We also describe recent progress in the translation of multiple phase-contrast imaging techniques from ex vivo to in vivo smallanimal studies. Furthermore, we also review the utility of SR for multiple pinpoint (dimensions 0.2×0.2 mm) assessments of myocardial function at the cross-bridge level in different regions of the heart using small-angle X-ray scattering, resulting from increases in SR flux at modern facilities. Finally, we present cases for the use of complementary SR approaches to study cardiovascular function, particularly the pathological changes associated with disease using small-animal models. -times brighter than laboratory or medical X-ray sources). This brightness is attributable to the fine collimation of the X-ray beam (http:// www.spring8.or.jp/en/about_us/whats_sr/generation_sr/).At SPring-8 in Japan, which is one of the largest SR facilities in the world, one of the smallest beam sizes is ≈2 mm horizontally by 0.4 mm vertically at 40 m from the X-ray source. This divergence is much smaller than that of most laboratory lasers. The X-ray beam is further collimated with focusing optics, so that it is <0.2 mm in diameter at the sample, concentrating a large number of X-ray photons on the sample. There are tens of SR facilities around the world, most of which are available for public access (for details on SR facilities, SR characteristics, and other science applications, http://www.lightsources.org/cms/).The intense X-ray beam from the synchrotron beamlines only can be used in metal-shielded hutches. X-ray image formation and acquisition have to be performed under remote control, including operations to inject contrast medium into an animal or to stop artificial ventilation temporarily. Despite this restriction, when the animal is closely monitored, the experiment can be performed smoothly. At SR medical imaging beamlines important infrastructure for animal experiments such as an animal house, and biology and chemistry preparation laboratories are an essential capability for the experiments described in this review. SR Absorption MicroangiographyThe vascular smooth muscle tone of arterioles is meticulously modulated via multiple mechanistic pathways, including, but not limited to, the vessel endothelium, the vascular smooth muscle, and neurohumoral stimuli to regulate resistance to flow and, hence, to optimize regional blood flow. Impairment of any of these regulatory systems has the potential to adversely impact on the vascular control of blood flow and, thus, impair the homeostatic control...

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Sarcomere-length dependence of lattice volume and radial mass transfer of myosin cross-bridges in rat papillary muscle

Cited by 28 publications

References 32 publications

Impact of osmotic compression on sarcomere structure and myofilament calcium sensitivity of isolated rat myocardium

Impact of osmotic compression on sarcomere structure and myofilament calcium sensitivity of isolated rat myocardium

Myosin MgADP Release Rate Decreases as Sarcomere Length Increases in Skinned Rat Soleus Muscle Fibers

Synchrotron Radiation Imaging for Advancing Our Understanding of Cardiovascular Function

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