The Frank–Starling mechanism in vertebrate cardiac myocytes

Shiels, Holly A.; White, Ed

doi:10.1242/jeb.003145

Cited by 157 publications

(120 citation statements)

References 85 publications

Supporting

Mentioning

111

Contrasting

Unclassified

Order By: Relevance

“…This elevated sensitivity of the fish hearts to the Starling response, well documented in both temperate eurytherm and cold-adapted teleosts (gilthead seabream, Icardo et al 2005;eel, Imbrogno et al 2001;icefish, Tota et al 1991), has been in part attributed to a greater myocardial extensibility of the highly trabeculate fish heart, coupled to a maintained increase in myofilament Ca 2þ sensitivity over a large range of sarcomere lengths (Di Maio & Block 2008;Shiels & White 2008).…”

Section: Introductionmentioning

confidence: 91%

Phospholamban S-nitrosylation modulates Starling response in fish heart

et al. 2009

View full text Add to dashboard Cite

The Frank -Starling mechanism is a fundamental property of the vertebrate heart, which allows the myocardium to respond to increased filling pressure with a more vigorous contraction of its lengthened fibres. In mammals, myocardial stretch increases cardiac nitric oxide (NO) release from both vascular endothelium and cardiomyocytes. This facilitates myocardial relaxation and ventricular diastolic distensibility, thus influencing the Frank -Starling mechanism.In the in vitro working heart of the eel Anguilla anguilla, we previously showed that an endogenous NO release affects the Frank -Starling response making the heart more sensitive to preload. Using the same bioassay, we now demonstrate that this effect is confirmed in the presence of the exogenous NO donor S-nitroso-N-acetyl penicillamine, is independent from endocardial endothelium and guanylate cyclase/ cGMP/protein kinase G and cAMP/protein kinase A pathways, involves a PI(3)kinase-mediated activation of endothelial NO synthase and a modulation of the SR-CA 2þ ATPase (SERCA2a) pumps. Furthermore, we show that NO influences cardiac response to preload through S-nitrosylation of phospholamban and consequent activation of SERCA2a. This suggests that in the fish heart NO modulates the Frank -Starling response through a beat-to-beat regulation of calcium reuptake and thus of myocardial relaxation.We propose that this mechanism represents an important evolutionary step for the stretch-induced intrinsic regulation of the vertebrate heart, providing, at the same time, a stimulus for mammalian-oriented studies.

show abstract

Section: Introductionmentioning

confidence: 91%

Phospholamban S-nitrosylation modulates Starling response in fish heart

et al. 2009

View full text Add to dashboard Cite

show abstract

“…Therefore, like muscles from mdm mice, cardiac myocytes are predicted to lack binding of N2A titin to the thin filaments. Cardiac myocytes of rats and mice exhibit no plateau in active force [46,47]. By contrast, cardiac myocytes from trout express the larger N2BA isoform, which includes both N2A and N2B isoforms, and is therefore predicted to exhibit Ca 2þ -dependent binding to thin filaments.…”

Section: Ca 21 -Dependent N2a -Actin Interactions Contribute To Lengtmentioning

confidence: 99%

Is titin a ‘winding filament’? A new twist on muscle contraction

et al. 2011

View full text Add to dashboard Cite

Recent studies have demonstrated a role for the elastic protein titin in active muscle, but the mechanisms by which titin plays this role remain to be elucidated. In active muscle, Ca 2þ -binding has been shown to increase titin stiffness, but the observed increase is too small to explain the increased stiffness of parallel elastic elements upon muscle activation. We propose a 'winding filament' mechanism for titin's role in active muscle. First, we hypothesize that Ca 2þ -dependent binding of titin's N2A region to thin filaments increases titin stiffness by preventing low-force straightening of proximal immunoglobulin domains that occurs during passive stretch. This mechanism explains the difference in length dependence of force between skeletal myofibrils and cardiac myocytes. Second, we hypothesize that cross-bridges serve not only as motors that pull thin filaments towards the M-line, but also as rotors that wind titin on the thin filaments, storing elastic potential energy in PEVK during force development and active stretch. Energy stored during force development can be recovered during active shortening. The winding filament hypothesis accounts for force enhancement during stretch and force depression during shortening, and provides testable predictions that will encourage new directions for research on mechanisms of muscle contraction.

show abstract

“…This differs from mammals, which, for the most part, modulate cardiac output via larger changes in heart rate than stroke volume. These comparisons suggest a shift in the role of volume (and so myocardial stretch) in the regulation of cardiac output during vertebrate evolution (Burggren et al, 1997;Shiels and White, 2008). Indeed, we have recently shown that the fish heart is specialized for large extensions during diastolic filling and for active tension development during systolic emptying from a wide range of lengths (Patrick et al, 2010b).…”

Section: Introductionmentioning

confidence: 96%

“…It is surprising that the SFR has been largely ignored in nonmammalian myocardium, as non-mammalian vertebrates in general, and fish in particular, are known to be exquisitely sensitive to cardiac stretch (Farrell, 1991;Shiels et al, 2006;Shiels and White, 2008). Rainbow trout (Oncorhynchus mykiss) modulate their cardiac output primarily via changes in stroke volume, and can increase stroke volume by up to 300% during strenuous activity with little change in heart rate (Farrell and Olson, 2000).…”

Section: Introductionmentioning

confidence: 99%

Rainbow trout myocardium does not exhibit a slow inotropic response to stretch

Patrick

White

Shiels

2011

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

SUMMARYMammalian myocardial studies reveal a biphasic increase in the force of contraction due to stretch. The first rapid response, known as the Frank-Starling response, occurs within one heartbeat of stretch. A second positive inotropic response occurs over the minutes following the initial stretch and is known as the slow force response (SFR). The SFR has been observed in mammalian isolated whole hearts, muscle preparations and individual myocytes. We present the first direct study into the SFR in the heart of a non-mammalian vertebrate, the rainbow trout (Oncorhynchus mykiss). We stretched ventricular trabecular muscle preparations from 88% to 98% of their optimal length and individual ventricular myocytes by 7% of their slack sarcomere length (SL). Stretch caused an immediate increase in force in both preparations, indicative of the Frank-Starling response. However, we found no significant effect of prolonged stretch on the force of contraction in either the ventricular trabecular preparations or the single myocytes. This indicates that rainbow trout ventricular myocardium does not exhibit a SFR and that, in contrast to mammals, the piscine Frank-Starling response may not be associated with the SFR. We speculate that this is due to the fish myocardium modulating cardiac output via changes in stroke volume to a larger extent than heart rate.

show abstract

The Frank–Starling mechanism in vertebrate cardiac myocytes

Cited by 157 publications

References 85 publications

Phospholamban S-nitrosylation modulates Starling response in fish heart

Phospholamban S-nitrosylation modulates Starling response in fish heart

Is titin a ‘winding filament’? A new twist on muscle contraction

Rainbow trout myocardium does not exhibit a slow inotropic response to stretch

Contact Info

Product

Resources

About